Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis

Bark and Wood Boring Insects in Living Trees in Europe,
a Synthesis
Bark and Wood Boring
Insects in Living Trees
in Europe,
a Synthesis
Edited by
François Lieutier
Laboratoire de Biologie des Ligneux et des Grandes Cultures,
Université d’Orléans, Ardon, Orléans, France
Keith R. Day
University of Ulster,
Coleraine, United Kingdom
Andrea Battisti
Università di Padova,
Legnaro, Italy
Jean-Claude Grégoire
Université Libre de Bruxelles,
Bruxelles, Belgium
and
Hugh F. Evans
Forestry Commission,
Wrecclesham, Farnham, United Kingdom
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 978-1-4020-2240-1 (HB)

ISBN 978-1-4020-2241-8 (e-book)
Published by Springer,
P.O. Box 17, 3300 AA Dordrecht, The Netherlands.
www.springer.com
Cover photos:
The forest of Lispach in the Massif of Vosges, Eastern France (photo taken by Michel Pitsch).
Ips sexdentatus (six-spined engraver beetle), a bark beetle attacking pines (photo taken by Janin – INRA).
Printed on acid-free paper
First Edition 2004, Reprinted 2007
All Rights Reserved

© 2004, 2007 Springer
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Table of Contents
Preface………………………………………………………………..……..ix
Acknowledgments……………………………………………..........………xi
The BAWBILT bases in Europe…………………................................…….1
Chapter 1 The BAWBILT context in Europe……………....................……3

F. LIEUTIER
Chapter 2 The directory of European experts…………......................……11

A. BATTISTI & M. FACCOLI
Chapter 3 The BAWBILT database……………………….........................15

M. GILBERT & D. SAUVARD
Chapter 4 Damage and control of BAWBILT organisms, an overview…..19

J-C. GRÉGOIRE & H.F. EVANS
Part 1, Bark Beetles.......................................................................................39
Chapter 5 Taxonomy and systematics off bark and ambrosia beetles……...41

M. KNÍŽEK & R. BEAVER
Chapter 6 Genetic tools in Scolytid research…………………...................55

C. STAUFFER
Chapter 7 General biology of bark beetles……………............…………...63

D. SAUVARD
Chapter 8 Chemical ecology of bark beetles in a complex olfactory

landscape…………………………………………………………...............89
J.A. BYERS
Chapter 9 Host resistance to bark beetles and its variations….....……….135

F. LIEUTIER
v
vi
Chapter 10 Fungal associates of European bark beetles with special

emphasis on the Ophiostomatoid fungi….....................................................181
T. KIRISITS
Chapter 11 Research on parasitoids and predators of Scolytidae,

a review .......................................................................................................237
M. KENIS, B. WERMELINGER & J-C. GRÉGOIRE
Chapter 12 Pathogens in bark beetles……………………………….........291

R. WEGENSTEINER
Part 2, Bark Weevils....................................................................................315
Chapter 13 Taxonomy and systematics of bark weevils…………......…..317

G. LEMPÉRIÈRE, A. MANTILLERI & C. CONORD
Chapter 14 General biology and life cycles of bark weevils……………..331

K.R. DAY, G. NORDLANDER, M. KENIS & G. HALLDORSON
Chapter 15 Semiochemicals in the life of bark feeding weevils………....351

F. SCHLYTER
Chapter 16 Hylobius abietis – Host utilisation and resistance………..….365

D. WAINHOUSE
Chapter 17 Fungi associated with Hylobius abietis and other weevils…..381

H. VIIRI
Chapter 18 Parasitoids, predators, nematodes and pathogens

associated with bark weevil pests................................................................395
M. KENIS, R. WEGENSTEINER & C.T. GRIFFIN
Chapter 19 Damage, control and management of weevil pests,

especially Hylobius abietis…………………………………......…………415
B. LÅNGSTRÖM & K.R. DAY
vii
Part 3, Buprestids and Longhorns................................................................445
Chapter 20 Biology, ecology and economic importance of Buprestidae

and Cerambycidae…...………………………………………........………447
H.F. EVANS, L.G. MORAAL & J.A. PAJARES
Chapter 21 Natural enemies of Cerambycidae and Buprestidae infesting

living trees………………………………………………………………...475
M. KENIS & J. HILSZCZANSKI
Part 4, “Non-Coleopteran” BAWBILT organisms......................................499
Chapter 22 Non-Coleopteran insects…………………………………..…501

B. LÅNGSTRÖM, K. HELIÖVAARA, L.G. MORAAL, M. TURýÁNI, M.
VIITASAARI & T. YLIOJA
Research needs and priorities for Europe....................................................539
Chapter 23 General conclusions and research priorities for BAWBILT

organisms in Europe………………………………………………………541
F. LIEUTIER, K.R. DAY, H.F. EVANS & B. LÅNGSTRÖM
Index of scientific names……………………………………….........……553

Preface
This book is the final product of a European joint research project that allowed
around 100 scientists from 24 European countries to work together actively from
November 1998 to December 2002. It presents a commented synthesis on the
research work done in Europe on bark beetles, bark weevils, longhorn beetles,
buprestid beetles, and other xylophagous insects that attack living trees. The project
was granted by the European Community, in the framework of the COST Actions,
under the title “Bark And Wood Boring Insects in Living Trees (BAWBILT)”. The
idea of such a synthesis was born in 1995 from a core interest in bark beetles,
matured while enlarging the scope to other groups in 1996 and the project was
approved by the Committee of Senior Officials of COST at the beginning of 1998.
COST (Cooperation in the field of Scientific and Technical research) is a
permanently open call by the European Commission for proposals that favour
actions such as networks, which aim att developing communications and exchanges
between European researchers and federating research groups at the European level.
It has several divisions including the section “Forest and Forestry Products”, to
which the BAWBILT Action belongs.
The objective of this book is to present a synthesis of BAWBILT organisms,
while providing a European focus. The ambition is thus more than a presentation of
the biology of the European BAWBILT species. The book reviews and comments
on all the European literature on these insects, while considering the biological
aspects (trees, insects, associated organisms, and their relationships), but it also
compares the available information and interpretations to those concerning similar
species in other continents. Indeed, for several BAWBILT organisms, especially
bark beetles, research is a global process, and studies, in parallel to the European
ones, have often been carried out mainly in North America. As a consequence,
although this synthesis is centred on the European species, numerous references
from North American studies are cited. This allows important generalizations in the
conclusions and the theoretical models. It also highlights specific differences in the
European species, as well as the strengths and shortcomings of the European
research. This comparative approach is more or less developed in each of the
different chapters, depending on the topic concerned. Some chapters, although
largely referring to the European species, present a synthesis of both European and
North American species. Others, while presenting such a synthesis, make a
comparison by directing attention to which results come from studies on the
European or the North American species. Others, due to the European focus of the
subject, deal with European results.
After a section presenting the structure and the information sources of the
BAWBILT group, and the characteristics of damage and control of the European
BAWBILT organisms in general, the book is structured in four parts: bark beetles;
weevils; buprestids and longhorns; non-coleopteran BAWBILT organisms. In each
of these parts, a commented review off all European literature is done, under
approximately the same organisational canvas: taxonomy and phylogeny; general
biology, life cycles and relations with abiotic factors; chemical ecology and host
ix
x
finding; host resistance; associated fungi; natural enemies. In each part, all factors
of population dynamics, each corresponding to a particular chapter, are thus
considered with their role, making unnecessary a special chapter on this subject.
The general characteristics of the population dynamics are however presented in the
chapter on general biology. The book ends with a concluding chapter presenting
research needs and priorities for Europe. An index of scientific names is given.
All chapters presented in this book have been peer reviewed by at least two
independent reviewers prior to acceptance. The book is the result of a collective
work gathering together all existing European competence, but it is not simply a
collection of different chapters written independently by specialists. It is rather the
fruit of a real collective synthesis in which all European specialists on BAWBILT
organisms have participated.
A CD accompanies the book. It contains a relational database gathering together
all BAWBILT research papers (including some “grey literature”) published in
Europe during the last 30 years as well as the most important ones that have been
published previously. The references from other continents used for the synthesis
are not contained in the CD but are included in the lists of references at the end of
the different chapters. The CD also contains a series of colour pictures illustrating
the different chapters.
The editors
Acknowledgments
The project was carried out with financial support from the Commission of the
European Communities, COST specific program, E16 COST Action “Bark and
wood boring insects in living trees”. This support greatly facilitated
communications between all European BAWBILT scientists, and the joint work,
thus allowing building the foundations of the present synthesis. However, the ideas
expressed in this book do not necessarily reflect the views of the Commission and in
no way anticipate the Commission’s future policy in the corresponding areas.
The numerous reviewers of the chapters are thanked for their constructive
remarks, as well as the English speaking authors of the book for revising the English
in most of the chapters written by their non English speaking colleagues. Thanks
also to D. Sauvard (INRA, France) who prepared the index of scientific names and
the CD containing the database and the colour pictures. The BAWBILT colleagues
who provided colour pictures are also acknowledged. P. Romary (INRA, France)
helped in preparing pictures and M. Pitsch (INRA, Nancy) provided the background
picture of the cover. Non-EU and EU scientists not involved in the Action, and who
presented lectures during a plenary meeting must also be thanked (list 1).
It must be especially emphasized that this synthesis would not have been
possible without the efficient participation in the Action of all the European
BAWBILT colleagues who, even if they were not authors of a chapter or if their
country is not a member of COST, worked very hard in the different working groups
and the plenary workshops, and in their respective countries, to gather all the
necessary information and build the databases of the synthesis, and in this way
contributed to the achievement of the project aims. All these colleagues are
gratefully acknowledged. The list of all European BAWBILT colleagues who were
involved actively in the Action is presented below in alphabetical order for each
participating country (list 2).
List 1. Experts invited to give a lecture during the final plenary meeting in Vienna (Austria).
Ayres, Matthews P., Department of Biological Sciences, Hanover, USA. “Tree

susceptibility to bark beetle attacks in relation to climatic changes”.
Govender, Prem, Forestry and Agricultural Biotechnology Institute, University of
Pretoria, Republic of South Africa. “Pest problems in relation to invasive forest
insect species and introduced tree species in South Africa”
Haack, Robert A., USDA Forest Service, Eastt Lansing, USA. “Invasive forest insect
species in North America”.
Jactel, Hervé, Institut National de la Recherche Agronomique, Pierroton, France.
“Tree species biodiversity and pest dynamics”
Raffa, Kenneth F., Department of Entomology, University of Wisconsin, Madison,
USA. “Role of insect-fungus relationships on population dynamics and host
selection behavior in forest insects”
Wagner, Michael R. School of Forestry, North Arizona University, Flagstaff, USA.
“Drought and bark beetle outbreaks”.
xi
xii
List 2. BAWBILT experts who participated actively in the Action.
Austria
Berger, Roland, BOKU-University of Natural Resources and Applied Life
Sciences, Vienna.
Führer, Erwin, BOKU-University of Natural Resources and Applied Life
Sciences, Vienna.
Holzschuh, Carolus, Austrian Federal Office and Research Centre for Forests,
Vienna.
Kirisits, Thomas, BOKU-University of Natural Resources and Applied Life
Sciences, Vienna.
Krehan, Hannes, Austrian Federal Office and Research Centre for Forests,
Vienna.
Schopf, Axel, BOKU-University of Natural Resources and Applied Life
Sciences, Vienna.
Stauffer, Christian, BOKU-University of Natural Resources and Applied Life
Sciences, Vienna.
Tomiczek, Christian, Austrian Federal Office and Research Centre for Forests,
Vienna.
Wegensteiner, Rudolph, BOKU-University of Natural Resources and Applied
Life Sciences, Vienna.
Belgium
De Proft, Michel, Centre de Recherches agronomiques de Gembloux
Franklin, Anne, Université Libre de Bruxelles
Gilbert, Marius, Université Libre de Bruxelles
Grégoire, Jean-Claude, Université Libre de Bruxelles
Czech Republic
Knizek, Milos, Forestry Research Institute, Zbraslav
Zahradnik, Petr, Forest and Game Management Research Institute, Zbraslav
Denmark
Harding, Susanne, The Royal Veterinary and Agricultural University,
Copenhagen
Ravn, Hans Peter, The Royal Veterinary and Agricultural University, Hoersholm
Estonia
Voolma, Kaljo, Estonian Agricultural University, Tartu
Finland
Annila, Erkki, Finnish Forest Research Institute
Heliovaara, Kari, University of Helsinki
Kyto, Maarit, Finnish Forest Research Institute
Mannerkoski, Ilpo, Finnish Environment Institute
Niemela, Pekka, University of Joensuu
Siitonen, Juha, Finnish Forest Research Institute
Viiri, Heli, Finnish Forest Research Institute
Viitassari, Matti, University of Helsinki
Ylioja, Tiina, Finnish Forest Research Institute
France
Bouhot-Delduc, Laurence, Département de la Santé des Forêts, Paris
xiii
Lempérière, Guy, Université Joseph Fourrier, Grenoble

Lieutier, François, Université d’Orléans and Institut National de la Recherche
Agronomique, Orléans
Malphettes, Claude Bernard, Cemagref, Orléans
Nageleisen, Louis-Michel, Département de la Santé des Forêts, Nancy
Piou, Dominique, Ecole National du Génie Rural et des Eaux et Forêts, Nogent-
sur-Vernisson
Saintonge, François-Xavier, Département de la Santé des Forêts, Orléans
Sauvard, Daniel, Institut National de la Recherche Agronomique, Orléans
Yart, Annie, Institut National de la Recherche Agronomique, Orléans
Germany
Bathon, Hornst, Institute for Biological Control, Darmstadt
Niemeyer, Hans, Forest Research Station of Lower Saxony, Göttingen
Wulf, Alfred, Federal Biological Research Centre for Agriculture and Forestry,
Braunschweig
Hungary
Lakatos, Ferenc, University of Forestry and Wood Sciences, Sopron
Iceland
Halldorsson, Gudmundur, Icelandic Forest Research, Mosfellsbaer
Sverrisson, Halldor, Icelandic Forest Research, Reykjavik
Ireland
Cahalane, Gerard, Forest Service, Dublin
Griffin, Christine, National University of Irelandaynooth, Maynooth
Ward, Declan, Irish Forestry Board, Coillte
Italy
Ambrosi, Paolo, Istituto Agrario San Michele all'Adige, San Michele all’Adige
Battisti, Andrea, Università di Padova, Legnaro
Faccoli, Massimo, Università di Padova, Legnaro
Francardi, Valeria, Istituto Sperimentale Zoologia agraria, Firenze
Minerbi, Stefano, Ispettorato Forestale Bolzano, Bolzano
Pennacchio, Fabrizio, Istituto Sperimentale Zoologia agraria, Firenze
Roversi, Pio Federico, Istituto Sperimentale Zoologia agrarian, Firenze
Stergulc, Fabio, Udine
Tagliaferri, Antonio, Regione Lombardia, Azienda Regionale Foreste, Milano
Lithuania
Zolubas, P., Lithuanian Forest Research Institute, Kaunas
Norway
Christiansen, Erik, Norwegian Forest Research Institute, As
Krokene, Paal, Norwegian Forest Research Institute, As
Poland
Grodski, Wojciech, Forest Research Institute, Cracow
Skrzecz, Iwona, Forest Research Institute, Warsaw
Portugal
Arnaldo, Paula, Universidade de Trás-Os.Montes e Alto Douro
Bonifácio, Luis, Estação Florestal Nacional, Oeiras
Branco, Manuela, Instituto Superior de Agronomia, Lisboa
De Sousa, Edmundo, Estação Florestal Nacional, Oeiras
xiv
Nunes, Luisa, Escola Superior Agrária de Castelo Branco

Paiva, Maria Rosa, Universidade Nova De Lisboa
Vasconcelos, Teresa Maria Amado, Escola Superior Agrária de Coimbra
Romania
Ciornei, C., Institut Cercetari Amenajari Silvice, Bacau
Danci Adela, Institut Cercetari Amenajari Silvice
Lupu, Daniel, Institut Cercetari Amenajari Silvice,
Mihalciuc, Vasile, Institut Cercetari Amenajari Silvice, Brasov
Miorcioiu, L., Institut Cercetari Amenajari Silvice, Brasov
Olenici, Nicolae, Institut Cercetari Amenajari Silvice,
Russia
Pashenova, Natalia, Sukachev Institute of Forest, Krasnoyarsk
Polyakova, Galina, Sukachev Institute of Forest, Krasnoyarsk
Vetrova, Valentina, Institute of Ecology, Petropavlovsk-Kamchatskij
Slovakia
Jakus, Rastislav, Slovak Academy of Sciences, Zvolen
Turcani, Marek, Forest Research Institute, Zvolen
Spain
Fernández Fernández, Mercedes, Universidad de Valladolid.
Gázquez Alcoba, Paz, Laboratorio Agroalimentario de Santafé, Granada
González Ruiz, Ramón, Universidad de Jaén
Pajares Alonso, Juan Alberto, Universidad de Valladolid
Sweden
Birgerson, Göran, Göteborg University, Göteborg
Byers John, The Swedish University of Agricultural Sciences; Alnarp (presently:
Western Cotton Research Lab., Agric. Res. Serv. USDA, Phoenix, USA)
Långström, Bo, The Swedish University of Agricultural Sciences
Månsson, P., The Swedish University of Agricultural Sciences; Alnarp
Nordlander Göran, The Swedish University of Agricultural Sciences; Uppsala
Schlyter, Fredrik, The Swedish University of Agricultural Sciences; Alnarp
Schroeder, Martin, The Swedish University of Agricultural Sciences, Uppsala
Weslien, Jan-Olov, The Swedish Forest Research Institute, Uppsala.
Zhang, Qing-He., The Swedish University of Agricultural Sciences; Alnarp
Switzerland:
Forster, Beat, Swiss Federal Institute WSL, Birmensdorf
Kenis, Marc, CABI Bioscience Centre,
Wermelinger, Beat, Swiss Federal Institute WSL, Birmensdorf
The Netherlands
Moraal, Leen G., Wageningen University and Research Centre, Wageningen
United Kingdom
Bell, Alan, Department of Agriculture & Rural Development, N. Ireland
Day, Keith, University of Ulster, Coleraine
Evans, Hugh, Forestry Commission Research Division, Wrecclesham
Johnston, Jack, Forest Research Agency,
Leather, Simon, Imperial College, University of London
Moore, Roger, Northern Research Station, Forestry Commission, Roslin
Wainhouse, David, Forestry Commission Research Division, Wrecclesham
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The BAWBILT bases in
Europe
Chapter 1
THE BAWBILT CONTEXT IN EUROPE
F. LIEUTIER
Université d’Orléans, rue de Chartres, B.P. 6759, F-45067 Orléans Cedex, France
WHAT ARE EUROPEAN BAWBILT?

Typically, BAWBILT organisms, the Bark And Wood Boring Insects in Living
Trees, correspond to the guilds of insects that develop, at least part of their life
cycle, inside living xylem or phloem tissues of trees. Strictly following that
definition, weevils such as Hylobius species, whose adults feed on trees externally
and the larvae develop inside dying stumps, should not belong to the BAWBILT
organisms. However, to circumscribe all xylophagous and phloeophagous insects of
living trees, the concept has been enlarged to include weevils. BAWBILT is thus
more than a guild but rather an assemblage of several guilds that have been studied
in parallel with some similarities in their relations with living host trees. As a
consequence of this distinction, all insects that attack only dead trees are excluded.
Galling insects are also excluded because they do not operate as true xylophagous or
phloeophagous species. The project focused on the European BAWBILT species.
However, not only the indigenous species have been considered, but also the
European introductions (e.g. the eucalyptus borer Phoracantha semipunctata
introduced several decades ago, the longhorn borers Anoplophora species
discovered only few years ago in central and southern Europe). The list of the
species that have been considered as European BAWBILT is presented in table 1.
Two North American bark beetle species Dendroctonus ponderosae and
Dendroctonus rufipennis are cited in this list, although not introduced to Europe,
because they have been intercepted in English ports and are the subjects of several
European studies. They will however not be considered as European species in the
synthetic chapters. Europe has been interpreted inclusively in its broadest
geographical manifestation, latitudinally from the Mediterranean Sea to Northern
Norway, and longitudinally from Iceland to the western part of Russia.
3
F. Lieutier et al. (Eds), Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis,
3–10.
© 2007 Springer.
4 F. LIEUTIER
Table 1. Recorded European BAWBILT species. Main synonyms are in brackets
Isoptera
Kalotermitidae
Kalotermes flavicollis
Heteroptera
Aradidae
Aradus cinnamomeus
Coleoptera
Buprestidae
Agrilus angustulus
Agrilus biguttatus ((A. pannonicus)
Agrilus populneus ((A. suvorovi)
Agrilus viridis
Coroebus florentinus (C. bifasciatus, C. fasciatus, Coraebus florentinus)
Coroebus undatus (Coraebus undatus)
Melanophila picta (Trachypteris picta)
Phaenops cyanea (Melanophila cyanea, M. tarda)
Cerambycidae
Anoplophora chinensis
Anoplophora glabripennis
Arhopalus rusticus (Criocephalus rusticus)
Cerambyx velutinus
Lamia textor
Monochamus galloprovincialis
Monochamus sartor
Monochamus sutor
Phoracantha semipunctata
Saperda carcharias ((Anaerea carcharias)
Saperda populnea (Compsidia populnea)
Tetropium castaneum ((Isarthron castaneum)
Tetropium fuscum
Tetropium gabrieli ((Isarthron gabrieli)
Curculionidae
Cryptorhynchus lapathi (Cryptorrhynchus lapathi)
Hylobius abietis ((Hylobitelus abietis)
Hylobius pinastri ((Hylobitelus pinastri)
Otiorrhynchus arcticus
Otiorrhynchus nodosus (O. dubius)
Otiorrhynchus singularis (O. picepes, Brachyrinus singularis)
Otiorrhynchus sulcatus (Brachyrinus sulcatus)
Pissodes castaneus (P. notatus)
Pissodes harcyniae (P. hercyniae)
Pissodes piceae
THE BAWBILT CONCEPT IN EUROPE 5
Pissodes pini
Pissodes piniphilus
Scolytidae
Cryphalus piceae (C. numidicus)
Dendroctonus micans
Dendroctonus ponderosae ((D. monticolae)
Dendroctonus rufipennis ((D. borealis, D. engelmanni, D. obesus)
Gnathotrichus materiarius
Hylastes angustatus
Hylastes ater
Hylastes attenuatus
Hylastes brunneus
Hylastes cunicularius ((Hylesinus cunicularius)
Hylastes opacus
Hylesinus crenatus
Hylurgus ligniperda
Ips acuminatus
Ips amitinus
Ips cembrae
Ips duplicatus
Ips sexdentatus
Ips typographus
Leperisinus varius ((L. fraxini, Hylesinus fraxini, H. varius)
Orthotomicus erosus
Phloeosinus armatus
Phloeosinus bicolor (P. aubei)
Phloeosinus thujae (P. prostratus, P. serrifer)
Phloeotribus scarabaeoides (P. oleae)
Pityogenes chalcographus
Pityogenes conjunctus (P. alpinus, P. baicalicus)
Pityogenes trepanatus
Pityokteines curvidens
Pityokteines spinidens
Pityokteines vorontzovi (P. vorontzoia)
Pityophthorus pityographus
Polygraphus poligraphus (P. pubescens)
Scolytus intricatus (Eccoptogaster intricatus)
Scolytus laevis (Eccoptogaster laevis)
Scolytus multistriatus (S. orientalis, S. ulmi, Eccoptogaster multistriatus)
Scolytus ratzeburgi (Eccoptogaster destructor, E. ratzeburgi)
Scolytus scolytus (S. geoffroyi, Eccoptogaster scolytus)
Scolytus sulcifrons
Scolytus triarmatus
Tomicus destruens (Blastophagus destruens, Myelophilus destruens)
Tomicus minor (Blastophagus minor, Myelophilus minor)
Tomicus piniperda (Blastophagus piniperda, Myelophilus piniperda)
6 F. LIEUTIER
Trypodendron domesticum ((Xyloterus domesticus)

Trypodendron lineatum ((Xyloterus bivittatum, X. lineatus)
Trypodendron signatum ((Apate signatus, Xyloterus signatus)
Xyleborus dispar ((X. pyri, Anisandrus dispar, A. pyri, Apate dispar)
Xylosandrus germanus ((Xyleborus germanus)
Platypodidae
Platypus cylindrus (P. cylindriformis)
Lepidoptera
Tortricidae
Rhyacionia buoliana (Evetria buoliana, Retinia buoliana)
Cossidae
Cossus cossus (C. ligniperda, Phalaena cossus)
Zeuzera pyrina (Z. aesculi, Cossus aesculi)
Sesiidae
Paranthrene tabaniformis ((Aegeria tabaniformis, Sesia tabaniformis)
Sesia apiformis ((Aegeria apiformis, Trochilium apiforme)
Synanthedon myopaeformis ((Aegeria myopaeformis, Sesia myopaeformis)
Pyralidae
Dioryctria splendidella ((D. sylvestrella)
Diptera
Agromyzidae
Phytobia betulae ((Agromyza betulae, Dendromyza betulae)
Hymenoptera
Siricidae
Sirex cyaneus (S. abbottii)
Sirex juvencus (Paururus juvencus)
Urocerus augur
Urocerus gigas
OBJECTIVES AND RESULTS OF THE BAWBILT ACTION

As in many other research fields, research on BAWBILT in Europe during the last
50 years has suffered from the fragmentation of the research community in about 35
countries and an almost equal number of languages. Until recently, this situation
was a handicap for the community of European scientists, with the consequence of
little exchange of information, duplication off research in some specialities, gaps in
others, and very limited possibilities for syntheses. International collaborations,
when they existed, were generally limited to a few bilateral exchanges. This
problem has progressively decreased during the last 15 years, partly due to the
development of modern and rapid communication systems, but mainly to financial
support from the EU for large cross-border projects involving several European
partners. Under these circumstances, national funding has often had secondary
importance for many research teams. This fragmented situation of European
research in the BAWBILT field was the first reason for building this Action.
Moreover, from a practical point of view regarding damage and control of forest
pets, almost each country has its own strategy.

t Survey and damage are often
evaluated using different techniques and units of measurement, depending on the
country, while decisions on control methods are not reached using the same
theoretical and practical frameworks. Evidently, a common strategy for survey,
damage evaluation and control methods throughout Europe, based on the existence
of ecological boundaries rather than political borders, would be more appropriate to
the biology of the pests and would thus be more efficient, especially in the case of
widespread pests, expansion of localized pests or accidental introductions. The need
to define European standards for such a common approach was another reason for
building the BAWBILT network.
A general aim was to consolidate the knowledge base for BAWBILT that would
support improvement in forest conservation and protection in future. The practical
objectives of the BAWBILT COST Action were thus: 1- to increase communication
between European scientists; 2- to build a balance-sheet on damage caused by
BAWBILT organisms in Europe; 3- to make proposals for more concerted and
efficient control strategies at the international level; 4- to build a catalogue and a
synthesis of research papers and research activities on BAWBILT in Europe; 5- to
make proposals for a European research policy in that field; 6- to publish the results
of the network activities.
A priority result of this Action is thus the strengthening of collaborations
between European scientists. New collaborations and wide exchange of information
have been established, and exchanges of young scientists realized. No team is any
longer isolated and all BAWBILT teams are now known throughout Europe.
Another positive result is the assembly off a database that includes all recent
European references to BAWBILT and some of the older ones. The third important
result of the Action is the present synthetic book which would have not been
possible until recently. For the first time, and thanks to an open communication
forum between scientists from most European countries working together in the
framework of the same European Project, a synthesis at the scale of the European
continent has been built taking into accountt all research fields related to all
BAWBILT organisms.
PARTICIPANTS AND ORGANIZATION OF THE RESEARCH WORK

A total of 101 experts belonging to 59 Institutions and 24 countries participated
actively in the Action. All natural areas of Europe were represented (Fig. 1).
However, gaps existed in the geographic coverage of Europe since countries from
Eastern Mediterranean sea and the Balkans and from Central Eastern Europe were
not able to participate. The list of the participating countries with their
representatives is given in the acknowledgment chapter (list 2).
The research work was structured into six tasks corresponding to the practical
objectives presented above.
Task 1 was devoted to facilitating communication between scientists. A
directory of European experts in the field of BAWBILT was built (task 1a, Battisti
and Faccoli, chapter 2). All European experts with experience of BAWBILT
8 F. LIEUTIER
organisms were approached through a questionnaire, including those not directly

involved in the network. Their research fields, objectives, methods and particular
experience were included in the directory, with indexes by key-words and country.
Figure 1. European countries having participated in the BAWBILT network (in dark grey).
Pale grey: other European countries. Austria (AT), Belgium (BE),Czech Republic (CZ),
Denmark (DK), Estonia (EE), Finland (FI), France (FR), Germany (DE), Hungary (HU),
Iceland (IL), Ireland (IR), Italy (IT), Lithuania (LT), Norway (NO), Poland (PL), Portugal
(PT), Romania (RO), Russia (RU), Slovakia (SK), Spain (ES), Sweden (SE), Switzerland
(CH), The Netherland (NL), United Kingdom (UK)
This directory facilitated exchange of information and can continue to be used as a

basis for building cooperative links. It can also been used to define fields or
specialities where the BAWBILT research group could be particularly effective. A
second aspect (task 1b) was the building of a BAWBILT WEB site where the
project is presented, together with the fields of interest of the participants. The WEB
site is accessible at http://www.bio.ic.ac.uk./staff/srl/bawbilt/bawbilt.htm. Periodic
working plenary meetings accompanied by poster sessions and working group
meetings also facilitated contact between participants (see below).
Task 2 dealt with damage. The aim was to collect data which would form a basis
for later definition of research priorities. A geographic and quantitative balance-
sheet of damage has been established (Grégoire and Evans, chapter 4; Långström
and Day, chapter 19; Evans et al. chapter 20; Långström et al. chapter 22).
Quantitative assessments of damage have been made by taking into consideration
the periods, the areas, the volumes, the number of trees, and the financial losses,
depending on the available data. Types off damage and the most frequently cited
species have been identified. The results have also been analyzed by country.
Task 3 was the review of control strategies (Grégoire and Evans, chapter 4;
Långström and Day, chapter 19; Evans et al. chapter 20; Långström et al. chapter
22). Current strategies in all BAWBILT species were assessed. The aim was to
suggest improvements and standardisations for more concerted and efficient actions
at the European level. Strategies have been classified in different control practices
and monitoring options.
Task 4 was the assembly of a catalogue and the synthesis of research papers and
activities. A period covering the last 30 years has been chosen because it
corresponds to a considerable diversification of the topics and increase in the
numbers of researchers active in the BAWBILT field. A full bibliography was first
compiled and organized in a catalogue. Classification was based on different topics
defined by key-words included in a thesaurus and a database was built, which also
includes data on damage and control (Gilbert and Sauvard, chapter 3). Indexes by
author, pest, tree species and country complete the catalogue. The syntheses by
research fields, which form the different chapters of this book, were then built by
using the database, in parallel with data from non European regions to allow
comparisons. As with task 1, these syntheses have helped in recognizing areas
where the BAWBILT group could be particularly effective. As with tasks 2 and 3,
they have been used to define research priorities. In addition, together with the
results from tasks 2 and 3, the achievement of task 4 provides a state of the art
reference book useful for future research.
Task 5 focused on defining research priorities for Europe in the BAWBILT field.
It was carried out after completion of tasks 2, 3 and 4, and in agreement with the
objectives of the EU research program (Lieutier et al., chapter 23).
Task 6 has been completed through the publication of the present book with the
joint CD.
MANAGEMENT OF THE BAWBILT ACTION

The organization of the BAWBILT network was based on the existence of a
National Responsible Scientist (NRS) in each participating country, having a role of
promoter and coordinator for all other scientists in his/her country. The NRS was in
charge of organizing tasks 1a, 2, 3 and 4 in his/her country in concert with other
scientists and with a National Task Scientist (NTS) for each task. Thus, in each
country, there were 1 NRS and 4 NTS, except for countries with less than 4
participants where the same person was in charge of several tasks. Each NTS
contributed to the European syntheses with the NTS from other countries, for the
task for which he/she had responsibilities. The European syntheses were carried out
in working groups under the supervision of Task Coordinators (TC). There was one
working group for each of the tasks 1a, 2, 3 and 4, plus one special working group
charged with making coherent and gathering together the databases from each other
group. Each group (except the database group) was composed of at least one
10 F. LIEUTIER
representative (the corresponding NTS) of each participating countryt and chaired by

the corresponding TC. These groups met periodically, especially on the occasion of
plenary meetings gathering all participants in the Action. Most often, groups 2 and
3 met together. The list of the BAWBILT species (Table 1) was prepared in each
country and then discussed and definitely adopted in plenary session. The
modalities of the general synthesis and its publication (tasks 5 and 6) were discussed
between all participants during plenary meetings. Task 5 and the coordination of
task 6 were assumed by the Chairman of the Action assisted by the Vice-chairman
and the scientists in charge of coordinating the different parts of the book, in
collaboration with the TCs.
The network was managed by a management committee composed of two
representatives of each COST country, and chaired by the chairman of the Action.
Participants in the Action, who were not members of this committee but
participating in the working groups, were invited to each management committee
meeting, thus giving opportunities
t to hold plenary sessions. Seven management
committee meetings and plenary sessions were held: Brussels (Belgium, 28-29
January 1999), Florence (Italy, 1-2 July 1999), Cracow (Poland, 13-14 April 2000),
Granada (Spain, 26-28 October 2000), Helsinki (Finland, 20-22 July 2001), Orléans
(France, 24-25 May 2002), Vienna (Austria, 6-7 December 2002). In addition to
managing the network and having working plenary and group meetings, these
sessions were the opportunity for the BAWBILT members to present the scientific
results of their work as posters. A special day was arranged during the final plenary
meeting, when five non-EU and one EU experts were invited to give presentations
on topics enlarging the strict field of BAWBILT. The list of these experts with the
presented topics is given in the acknowledgment chapter (list 1).
Chapter 2
THE DIRECTORY OF EUROPEAN EXPERTS
A. BATTISTI & M. FACCOLI
University of Padova, Agripolis, 35020 Legnaro PD, Italy
1. INTRODUCTION
The aim of sub-task 1a was to build a directory of European scientists working with
BAWBILT organisms. Experts were approached via a national responsible who
collected information concerning personal details, research activities, host plant and
insect group/species. Results were indexed by keywords and by countries. The
directory is accessible at the web site http://lubies.ulb.ac.be/bawbilt/ and is regularly
updated by each expert. Any change or new entry is formally checked by task 1a
responsible before it becomes accessible to the public.
2. RESULTS AND DISCUSSION

A total of 201 experts from 23 countries (no expert from Russia has registered) were
included in the directory. The number of experts in each country is presented in Fig.
1.
The number of experts was not closely related to the area covered by forest in
each country. This could be due to several factors, such as the local importance of
BAWBILT organisms, or the presence of specialised research teams working with
BAWBILT organisms or with specialised forest plantations, e.g. Eucalyptus in
Portugal. Experts belonged mainly to public research institutes (49.1 %) and
universities (46.4 %), whereas a small number was employed in private enterprises
(4.5 %).
The fields of interest within BAWBILT organisms cited by experts are presented
in Tab. 1. Control and monitoring methods were the topics sharing the highest
interest, followed by basic biology and ecology, with special attention to chemical
communication and insect-tree relationships. Natural enemies and systematics were
also covered by a considerable number of experts, and so were the relatively new
fields such as insect genetics and conservation biology.
11
F. Lieutier et al. (eds.), Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis,
11–14.
© 2007 Springer.
12 A. BATTISTI & M. FACCOLI
30 30
25 expert 25
forest
Forest area (10^6 ha)

20 20
No. of experts
15 15
10 10
5 5
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ry
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ia
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Figure 1. Distribution of experts involved in BAWBILT among 23 countries which showed an

interest in the project. Forest land is taken from FAO ‘Forest Resources
e Assessment 2001’.
All experts expressed their interest in one or several BAWBILT organisms host-
plants (415 records), mostly recorded as tree genus or species (Fig. 2). Conifers were
largely preferred over broadleaved trees, even if the area occupied by the two groups
of trees is similar (FAO, 2001). This is probably related to the more extensive use of
conifer trees in plantations. The ongoing restoration of these secondary stands with
broadleaved trees in many countries will likely move the future attention to
broadleaved trees (Battisti, 2000). Most experts expressed their interested in
northern conifer trees, whereas southern species of trees, and especially broadleaves,
appeared to be largely under-represented.
A total of 159 experts expressed their interest in one or several BAWBILT
organisms (246 records; Fig. 3). Beetles, and dominantly conifer bark beetles and
Hylobius spp., were by far the favourite group of most experts. This pattern reflects
the distribution of the preferences expressed for the host trees. The presence of
species new to Europe (e.g. the longhorn beetles Anoplophora spp.) or potential
vectors of the recently introduced pine wood nematode (Monochamus spp.) is
indicative of the readiness to undertake new research on these organisms, which
represent serious threats to the European forests.
The directory can provide a good starting point to strengthen the collaboration
among European experts, with the development of common projects and the
exchange of information. It may also show gaps in the research on BAWBILT in
Europe, which need to be filled by future work. More attention should be paid to
alien species, especially in relation to their potential as vectors of plant pathogens,
and to the role of BAWBILT organisms in deciduous stands. Biodiversity and
THE DIRECTORY OF EUROPEAN EXPERTS 13
conservation issues deserve more attention too, as they may play an important role
in the future management of European forests.
140
120
Experts No.
100
80
60
40
20
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us
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us
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Conifer and broadleaved tree genera
Fig. 2. Preferences expressed by experts for a tree genus. There was no upper limit to the
number of preferences for each expert. Preferences are listed in order of decreasing
abundance within conifer and broadleaved trees, respectively. Tree genera with only one
record (No. 11) were excluded.
60
50
Experts No.
40
30
20
10
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ia
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Conifer and broadleaved insect genera
Fig. 3. Preferences expressed by experts for insect genera. There was no upper limit to the
number of preferences for each expert. Preferences are listed in order of decreasing
abundance within conifer and broadleaved trees, respectively. Insect genera with only one
record (No. 21) were excluded.
14 A. BATTISTI & M. FACCOLI
Table 1. List of fields of interest in BAWBILT

W organisms expressed by 198 experts. There was
no upper limit to the number off preferences off each expert.
Field of interest Experts No.

Forest management – Control methods 89
Forest management – Monitoring 59
Insect – Basic biology 53
Insect – Population study 40
Insect – Chemical communication 32
Insect – Natural enemies 32
Insect-Tree relationship – Tree susceptibility 26
Insect – Systematic 25
Insect-Tree relationship – Host defences 23
Forest management – Management 17
Forest management – Damage 16
Insect – Geographic distribution 15
Insect – Genetics 13
Forest management – Risk assessment 13
Insect – Conservation biology 11
Insect – Dispersal 8
Insect-Tree relationship – Attack strategies 8
Insect – Insect performance 4
Insect-Tree relationship – Entomological techniques 2
Forest management – Legislation 2
Other – Urban and amenity trees 2
Insect – Anatomy and physiology 1
Other – Fire ecology 1
Other – Data management 1
Total of preferences expressed by 201 experts 492
3. REFERENCES
Battisti A., 2000. The role of phytophagous insects in the restoration process off secondary coniferous
stands. In. Forest Ecosystem Restoration. H. Hasenauer (ed.), Proceedings International Conference
Vienna 10-12 April 2000. Institut Forest Growth, BOKU, Vienna.
FAO, 2001. Forest Resources Assessment. http tp://www.fa
f o.org
g/fo
f restry
y/fo
f /country
y/index.
Chapter 3
THE BAWBILT DATABASE

Gathering and sharing information related to BAWBILT
organisms
M. GILBERT 1 & D. SAUVARD 2
1
Université Libre de Bruxelles, 50 avenue F.D. Roosevelt, B-1050 Bruxelles,
Belgium
2
Institut National de la Recherche Agronomique, avenue de la Pomme de Pin,
B.P. 20619, Ardon, F-45166 Olivet Cedex, France
1. INTRODUCTION
Several tasks of the BAWBILT Cost Action (Task 1a: Directory of European
scientists; Task 2: Synthesis of damage; Task 3: Control method; Task 4: Catalogue
and synthesis of research papers and research activities) required the collection,
treatment and display of data from participating countries. Although it was not
identified as a separate task in the initial action outline, it became quickly obvious
that the development of a common on-line database would greatly facilitate data
exchange from and to participating countries. A separate working group was thus
set-up in Florence meeting (July 1999) that worked in parallel as the other working
groups throughout the duration of the BAWBILT action.
No specific resource had been planned for the development of the database. The
main challenge was thus to find a good balance between simplicity such as to allow
the developments to be carried out by our own limited resource, flexibility to do not
restrict further potential uses of the database, and functions required by the separate
tasks.
2. OBJECTIVES AND DESIGN

The general aims of the BAWBILT database were i) to allow country
representatives or experts to enter and modify information regarding their countries,
ii) to facilitate the synthesis of these data by task coordinators, and iii) to allow data
15
15–18.
© 2007 Springer.
16 M. GILBERT & D. SAUVARD
retrieval by the BAWBILT community and by the public. Three modules

corresponding to separate tasks were developed (Table 1). Task 2 & 3 were grouped
in a single module because damage and control are closely related and shared many
common fields.
Table 1. Characteristics of the three database modules. Tasks : 1a: Directory of experts,
2 & 3: Damage and control methods, 4: Literature. CR: Country representative. TC: Task
Coordinator. Access to 2 & 3 module was internal up to the end of these tasks.
Task Data entry Data validation Access

1a Anyone CR / TC Public
2&3 CR — Internal then public
4 Registered scientists CR / TC Registered scientists
The database was designed in MS Access 2000. On-line data entry, validation
and retrieval procedure were written in MS Active Server Page (ASP) using the MS
Internet Information Server 4 (IIS4) as web server. Several tables were shared by all
modules: the list of species (See chapter 1) established in Krakow’s meeting (April
2000), the list of host-plant species (appendix A), the list of participating countries
(See chapter 1), and a subject thesaurus (appendix B).
2.1. Input data

The procedure for entering and modifying data is common to all modules. The user
search firstly for records already present in the database. The user has then the
possibility to add a new recordd to the list, or to update an existing record. The
directory of experts (task 1a) records data per individual expert such as personal
details (title, affiliation, address, phone, fax, e-mail, URL), area of interest
(according to the subject thesaurus), BAWBILT species and host-plant species. The
table on damage and control methods (tasks 2 & 3) records information grouped by
country and by BAWBILT species: species relationship to the host; type of impact;
type and extent of damage; damage estimates; type and extent of control strategies;
and type of monitoring, risk rating or decision-support systems. The literature
database records data per individual reference including classical bibliographic
fields (authors, year, title source, etc.) in addition to several indexing fields (text
language, summary language, geographic region, ecological region, BAWBILT
species, host-tree, subject), additional description fields (BAWBILT abstract1,
BAWBILT abstract author, availability within the BAWBILT community,
commentaries) and administrative fields (reference country and validation status).
2.2. Outputs
The procedure for retrieving data is also common to all modules. The user searches
through the database according to criteria entered in search forms, receives a list of
output records with limited amount of displayed details and has the possibility to
THE BAWBILT DATABASE 17
access the complete records by selecting any of the records displayed in the list.
Queries on experts can be done by last name, country, BAWBILT species, host-tree,
subject or by any combination of these fields. Queries on damage and control
methods can be done by country, pest species, host-tree or by any combination of
these fields. Queries of the literature database can be done at two levels: basic
search with a limited number of search fields such as classical bibliographic fields,
or advanced search offering the possibility to search though all fields used in the
literature database.
3. DISCUSSION AND POTENTIAL IMPROVEMENTS

The database has efficiently played its role in facilitating information gathering
regarding experts, damage & control methods, and literature for the present
synthesis. However, at the present stage of development, it is not as such a
satisfying information source in a longer termm perspective. Several steps should be
achieved in order to make it a valuable knowledge resource regarding BAWBILT
organisms.
Firstly, a solution should be found to ensure that the database remains up to date.
This would require a network of researcher willing to regularly check the data,
contact country representatives to requestt updated information, and add, edit or
delete relevant records.
Secondly, we received a lot of feedback from users who used the database during
the BAWBILT action. Several forms and procedures for data entry and searches
need to be modified according to these feedback.
Finally, the current type of outputs do not take yet fully advantage of the
database structure and data. For example, searches are currently made separately
within each module and cross-searches that would allow to display in a single page
all experts, damage and control method records, and references related to a given
species would be a valuable output. Another valuable output of the database would
be to allow on-the-fly comparison of damage and control methods regarding one
species between countries across Europe.
It is believed that the database will probably not survive the BAWBILT COST
action if none of these steps is achieved. Conversely, given the critical mass of data
brought together to date, and if a limited amount of resource is put together to
achieve these steps, the BAWBILT database could become a highly valuable
knowledge base regarding BAWBILT organisms and contribute in a long term
perspective to better address threats caused by these pests to European forests.
The database can be accessed at: http://lubies.ulb.ac.be/bawbilt
4. NOTES
1 This field is designed to allow country representative to enter abstracts of reference from gray
literature having no text nor abstract written in English.
18 M. GILBERT & D. SAUVARD
5. ACKNOWLEDGEMENTS
The authors wish to thanks all those who attended the database working group
meetings, peoples providing feedback on the use of the database and those who
participated actively to its development, in particular: Andrea Battisti, John Byers,
Jacopo de Silva, Hugh Evans, Helmut Feichter, Valeria Francardi, Jean-Claude
Grégoire and Anne Franklin.
APPENDIX A: HOST-PLANT SPECIES

Abies sp., Abies alba, Abies cephalonica, Abies grandis, Abies lasiocarpa, Abies nobilis,
Abies nordmanniana, Abies procera, Abies sibirica, Acer sp., Acer campestre, Acer
platanoides, Acer pseudoplatanus, Acer tataricum, Aesculus hippocastanum, Alnus sp., Alnus
cordata, Alnus glutinosa, Alnus incana, Betula sp., Betula pendula, Betula pubescens,
Carpinus betulus, Carya ovata, Castanea sativa, Celtis australis, Celtis tournefortii,
Ceratonia siliqua, Cercis siliquastrum, Chamaecyparis lawsoniana, Chamaerops humilis,
Corylus sp., Corylus avellana, Corylus colurna, Cupressus sempervirens, Cydonia oblonga,
Erica azorica, Eucalyptus sp., Fagus sp., Fagus orientalis, Fagus sylvatica, Frangula sp.,
Fraxinus sp., Fraxinus angustifolia, Fraxinus excelsior, Fraxinus ornus, Ilex perado, Juglans
sp., Juglans cinerea, Juglans nigra, Juglans regia, Juniperus sp., Juniperus brevifolia,
Juniperus excelsa, Juniperus oxycedrus, Larix sp., Larix decidua, Larix gmelinii, Larix
kaempferi, Larix leptolepis, Larix × eurolepis, Laurus azorica, Myrica faia, Olea sp, Ostrya
sp, Picea sp., Picea abies, Picea omorika, Picea sitchensis, Pinus sp., Pinus halepensis, Pinus
cembra, Pinus contorta, Pinus nigra var austriaca, Pinus nigra var corsicana, Pinus pinaster,
Pinus pinea, Pinus strobus, Pinus sylvestris, Platanus × acerifolia, Populus sp., Populus alba,
Populus alba × canescens, Populus deltoïdes, Populus euramericana, Populus nigra, Populus
tremula, Populus trichocarpa, Prunus sp., Prunus avium, Prunus serotina, Pseudotsuga
menziesii, Quercus sp., Quercus frainetto, Quercus ilex, Quercus petraea, Quercus
pubescens, Quercus robur, Quercus rubra, Quercus suber, Robinia pseudoacacia, Salix sp.,
Salix alba, Salix caprea, Salix fragilis, Sequoia sempervirens, Sorbus sp., Sorbus aria, Sorbus
aucuparia, Sorbus austriaca, Sorbus domestica, Sorbus hybrida, Sorbus intermedia, Sorbus
latifolia, Sorbus torminalis, Tamarix africana, Thuja plicata, Tilia sp., Tilia cordata, Tilia
platyphyllos, Tilia tomentosa, Tilia tomentosa, Tsuga heterophylla, Ulmus sp., Ulmus
campestris, Ulmus glabra, Ulmus montana, Ulmus procera, Vaccinium cylindraceum.
APPENDIX B: SUBJECT THESAURUS

Insect related keywords: Systematic, Basic biology, Geographic distribution, Anatomy and
physiology, Communications, Dispersal, Pathology, Population study, Insect performance,
Entomological technique. Insect-tree relationship related keywords: Tree finding, Tree
susceptibility. Forest management related keywords: Forest management, Insect damage,
Risk assessment, Pest management, Legislation. Other keywords: Abiotic factor, Insect -
fungus relationship, Natural enemy, Non target organism.
Chapter 4
DAMAGE AND CONTROL OF BAWBILT ORGANISMS

AN OVERVIEW
J.-C. GRÉGOIRE 1 & H.F. EVANS 2
1
Université Libre de Bruxelles, 50 avenue F.D. Roosevelt, 1050 Bruxelles,
Belgium;
2
Forest Research, Alice Holt Lodge, Wrecclesham Farnham, Surrey GU10 4LH,
United Kingdom
1. INTRODUCTION
The BAWBILT database on damage and control (Gilbert and Sauvard, chapter 3)
was queried in January 2003. It then contained 478 entries, on 95 species of the
BAWBILT list, with entries from 19 countries. In each entry, a series of fields
concerned the total areas potentially affected, the types of damage (death of trees,
caused by the insects themselves or by pathogenic fungi, timber degrade, impact on
growth, on erosion, on avalanches,…), quantitative assessments of damage (periods,
areas, volumes of timber, numbers of trees, financial losses), and scoring (+ to +++)
for aggressivity and for territorial coverage. A series of fields regarding control
practices (e.g. do nothing, sanitary thinning, clearfelling, traptrees, pheromone
trapping, insecticide treatments) and monitoring options (e.g. visual assessments,
pheromone trapping, questionnaires) was also available.
To avoid unnecessary duplication, damage and control are covered together in
this section.
In this short overview, we shall first identify the most frequently cited species
and then provide statistics per country. Finally, we shall analyse more closely the
data available on the "top ten" species, i.e. those species that were scored +++ for
aggressivity at least three times. This more detailed analysis will consider the types
of damage, quantitative information when available (numbers of trees/volume killed,
acreages, etc) and control methods.
19
F. Lieutier et al. (eds), Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis,
19—37.
© 2007 Springer.
20 J.C. GRÉGOIRE & H.F. EVANS
2. THE MOST DAMAGING PESTS

Table 1 lists important pest species which were scored +++, and Table 2 lists those
which were either scored +++ or ++. Ten species, among which were seven
Scolytids, received a +++ score at least three times: Hylobius abietis (Coleoptera:
Curculionidae), Ips typographus; Ips acuminatus; Pityogenes chalcographus;
Scolytus multistriatus; Scolytus scolytus; Scolytus laevis; Tomicus piniperda
(Coleoptera: Scolytidae), Phaenops cyanea (Coleoptera: Cerambycidae) and
Rhyacionia buoliana (Lepidoptera: Tortricidae). Two species received the most
attention for both damage and, not surprisingly, control: Ips typographus (15
citations) and Hylobius abietis (12 citations).
Table 1. BAWBILT organisms scored +++ in the BAWBILT database

Number of
Species
occurences
Ips typographus 15
Hylobius abietis 12
Pityogenes chalcographus ; Scolytus multistriatus ; Scolytus scolytus 6
Ips acuminatus 5
Tomicus piniperda 4
Phaenops cyanea ; Rhyacionia buoliana ; Scolytus laevis 3
Cryptorhynchus lapathi; Dendroctonus micans ; Ips duplicatus; Ips sexdentatus;
Paranthrene tabaniformis; Pissodes castaneus; Tomicus minor; Trypodendron lineatum;
Zeuzera pyrina 2
Agrilus biguttatus; Gnathotrichus materiarius; Hylastes ater; Hylastes cunicularius;
Hylobius pinastri; Ips amitinus; Ips cembrae; Leperesinus varius; Monochamus sartor;
Pissodes piniphilus; Pityokteines curvidens; Polygraphus poligraphus; Saperda
carcharias; Saperda populnea; Scolytus
l intricatus; Scolytus triarmatus; Sirex juvencus;
Tetropium gabrieli; Trypodendron domesticum; Urocerus gigas 1
3. SPECIES PER COUNTRY

The numbers of species considered to be significant pests varied greatly between
countries (21 +++ pests in Romania, 16 in Germany, 1 in Belgium, France or The
Netherlands): Fig. 1 and Table 3. It is unclear how much these differences can be
explained by local variations in forest coverage, forest uses, tree species,
silvicultural practices, climate, topography, etc. Part of these differences may also
stem from divergences in damage assessment methods and criteria. For example,
numbers of trees killed, cubic metres of timber lost, financial value of timber
degrade or areas "hit" by a pest give quite different damage assessments. An
important outcome of the BAWBILT programme could be to discuss more carefully
the status of the species identified as aggressive and to determine the key factors
leading to their highly damaging status.
DAMAGE AND CONTROL OF BAWBILT ORGANISMS 21
Table 2. BAWBILT organisms scored either +++ or ++ in the BAWBILT database
Number of
Species countries
Ips typographus 16
Hylobius abietis 15
Scolytus scolytus; Tomicus piniperda 9
Ips acuminatus; Pityogenes chalcographus; Scolytus multistriatus; Tomicus minor 8
Ips amitinus 7
Hylastes cunicularius; Ips sexdentatus 6
Ips cembrae; Phaenops cyanea; Pityokteines curvidens; Polygraphus poligraphus;
Rhyacionia buoliana; Scolytus intricatus 5
Agrilus biguttatus; Cryptorhynchus lapathi; Dendroctonus micans; Hylastes ater;
Ips duplicatus; Pissodes castaneus; Pissodes piniphilus; Saperda carcharias;
Tetropium gabrieli 4
Cryphalus piceae; Paranthrene tabaniformis; Pityokteines vorontzovi; Saperda populnea;
Scolytus laevis; Trypodendron domesticum; Trypodendron lineatum; Zeuzera pyrina 3
Cossus cossus; Leperesinus varius; Pissodes piceae; Pityokteines spinidens;
Pityophthorus pityographus; Sesia apiformis; Tetropium castaneum; Urocerus gigas;
Xyleborus dispar 2
Agrilus populneus; Aradus cinnamomeus; Gnathotrichus materiarius; Hylesinus crenatus;
Hylobius pinastri; Hylurgus ligniperda; Monochamus sartor; Orthotomicus erosus;
Phloeotribus scarabaeoides; Phoracantha semipunctata; Pissodes pini; Pityogenes
conjunctus; Scolytus ratzeburgi; Scolytus triarmatus; Sirex juvencus; Trypodendron
signatum 1
Belgium 1
France 1
The 1
Lithuania 2
United 2
Estonia 3
Ireland 3
Countries
Italy 3
Austria 4
Switzerland 4
Spain 5
Sweden 5
Hungary 6
Poland 7
Czech 8
Slovakia 9
Germany 16
Romania 21
0 5 10 15 20 25
Number of species cited as +++
Figure 1. Numbers of +++ species in the different BAWBILT countries

Table 3. Pests scored +++ in the different BAWBILT countries
Species Countries
Ips typographus Austria; Belgium; Czech Republic; Estonia; France; Germany; Hungary;
Ireland; Lithuania; Poland; Romania; Slovakia; Sweden; Switzerland;
United Kingdom
Hylobius abietis Austria; Czech Republic; Estonia; Germany; Hungary; Ireland; Lithuania;
Poland; Romania; Slovakia; Sweden; United Kingdom
Pityogenes chalcographus Austria; Czech Republic; Germany; Hungary; Romania; Slovakia
Scolytus multistriatus Czech Republic; Germany; Slovakia; Spain; Sweden; Switzerland
Scolytus scolytus Czech Republic; Germany; Slovakia; Spain; Switzerland; The Netherlands
Ips acuminatus Germany; Romania; Slovakia; Spain; Switzerland
Tomicus piniperda Czech Republic; Poland; Slovakia; Spain
Phaenops cyanea Czech Republic; Germany; Poland
Rhyacionia buoliana Hungary; Ireland; Romania)
Scolytus laevis Germany; Slovakia; Sweden
Cossus cossus Italy; Romania
Cryptorhynchus lapathi Hungary; Romania
Dendroctonus micans Germany; Romania
Ips duplicatus Poland; Slovakia
Ips sexdentatus Germany; Spain
Paranthrene tabaniformis Italy; Romania
Pissodes castaneus Hungary; Poland
Tomicus minor Czech Republic; Romania
Trypodendron lineatum Germany; Romania
Zeuzera pyrina Italy; Romania
Agrilus biguttatus Germany
Aradus cinnamomeus Finland
Gnathotrichus materiarius Germany
Hylastes ater Romania
Hylastes cunicularius Romania
Hylobius pinastri Estonia
Ips amitinus Romania
Ips cembrae Germany
Leperesinus varius Italy
Monochamus sartor Romania
Pissodes piniphilus Austria
Pityokteines curvidens Romania
Polygraphus poligraphus Romania
Saperda carcharias Romania
Saperda populnea Romania
Scolytus intricatus Poland
Scolytus triarmatus Sweden
Sirex juvencus Romania
Tetropium gabrieli Germany
Trypodendron domesticum Germany
Urocerus gigas Romania
4. DAMAGE OF THE "TOP TEN" SPECIES
4.1. Ips typographus

Table 4 provides scoring and quantitative data for Ips typographus. Although
incomplete, available information from ten countries indicates that over a potentially
threatened area of 7,640,000 ha, at least 2,819,000 ha were attacked between 1990 and
2001, resulting in the death of 31,643,000 m³ of spruce. Most of the data are connected
to the 1990 storms. Austria (11,000,000 m³), Poland (6,270,000 m³), Germany
(5,900,000 m³) and Slovakia (4,490,000 m³) reported the highest losses.
Table 4. Damage caused by Ips typographus

Timberr 1 degrade
Threatened Area
Physical danger
Volume (m³)
Avalanche 1
Tree death1
for people 1
Cosmetic 1
Area (ha)
Country
Erosion 1
Host age
Period
(ha)
Austria Pole 2,000,000 2 2 2 1992-2000 11,000,000 no data

Belgium Older no data 2 2 2 1992 250,000 no data
France Older no data 3 1990-01 1,500,000 no data
Germany Older 3,233,001 2 1990-98 5,901,254 192,760
Hungary Pole 24,000 2 2 1990-97 420,000 no data
Lithuania Older 221,155 3 1 1998-2001 no data 27,462
Poland Older 230,000 3 3 3 1990-99 6,270,000 no data
Romania Older 600,000 3 3 3 3 3 1991-2000 811,195 2,598,833
Slovakia Pole 600,000 3 2 2 3 1990-99 4,490,086 no data
Switzerland Older 492,000 2 2 2 2 1993-95 1,000,000 no data
Total (of available
7,640,156 35 12 9 12 8 3 1990-2001 31,642,535 2,819,055
figures)
1
Scoring from 1 to 3
4.2. Hylobius abietis

Death of coniferous transplants is, expectedly, the major impact of this species. A total
of 3,418,000 ha is regarded as threatened, of which 88,000 ha were seriously damaged
between 1980 and 2000 in Germany, Hungary, Lithuania, Romania, and Slovakia
(Table 5).
4.3. Pityogenes chalcographus

Available information from eight countries indicates that over a potentially threatened
area of 8,784,000 ha, at least 595,400 ha were attacked between 1990 and 2000,
resulting in the death of 7,828,000 m³ of conifers (Table 6). Although Poland reported
the highest losses (6,270,000 m³), this volume concerns the damage caused by the
complex of species occurring on Norway spruce, in which I. typographus is
dominating .
Table 5. Damage caused by Hylobius abietis
Tree death1
Threatened
Area (ha)
Area (ha)
Period
Country
Austria 3,000,000 2
Germany 6,466,455 2 1990-98 14,643
Hungary 246,000 2 1980-98 2,400
Ireland 8,000 3
Lithuania 7,264 2 1997-2001 9,142
Poland 27,000 2
Portugal 1 080 800 2
Romania 180,000 3 1991-2000 60,719
Slovakia 15,000 3 1990-99 1,354
Spain 100,000 2
United Kingdom 15,000 3
Total 3,418,264 39 1980-2000 88,258
1
Scoring from 1 to 3
Table 6. Damage caused by Pityogenes chalcographus

Threatened
Number of
Area (ha)
Area (ha)
Volume
Country
Period
trees
(m³)
Austria 2,500,000 1992-01 600,000

Germany 3,233,001
Hungary 246,000
Poland 513,000 1999 6,270,000
Portugal 1 080 800
Romania 1,200,000 1999-2000 730,049 730,049 595,400
Slovakia 600,000 1900-99 227,457
Switzerland 492,000
Total 8,784,001 1900-2000 730,049 7,827,506 595,400
4.4. Scolytus multistriatus and S. scolytus

Damage by these two species was usually reported together, as the vectors for Dutch
Elm Disease have not always been identified f with complete accuuracy. Much greater
damage obviously occurred throughout Europe from the late 1970s, but was not
reported in the BAWBILT database. The reason for this is probably the generally
doubtful status of Ulmus species as forest trees (Table 7).
Table 7. Damage caused by Scolytus multistriatus and S. scolytus
Volume (m³)
Threatened
Number of
Area (ha)
Area (ha)
Country
Period
trees
Spain 1984-99 3,000,000
Slovakia 1,500 1990-99 10,711
Romania 1,000 1991-2000 524
Portugal 221,600
Total 224,100 1991-2000 3,000,000 10,711 524
4.5. Ips acuminatus

Although nine countries provided quantitative data on this species, only Poland
reported high losses on pines (a total of 12,838,000 m³ killed by BAWBILT organisms
between 1990 and 1999: Table 8). The same 12,838,000 m³ are also cited in
connection with Tomicus piniperda a and Phaenops cyanea a in Poland (Tables 9 and 10).
The specific status of these three species found on the same dead pines in Poland is
unclear in the database; it results from the method used for data collection in this
country, namely the evidence of the volume of killed trees regardless the insect
specied causing the mortality (the volume of tree killed by I. acuminatus is much
lower).
4.6. Tomicus piniperda

Eight countries provided quantitative data for this species. Its status in Poland is
unclear (see above), however this species is one of the most aggressive and important
pine pests in this country. Significant losses were reported in Slovakia (93,000 m³) and
large acreages were reported in Spain (200,000 ha: Table 9).
Table 8. Damage caused byy Ips acuminatus
Threatened Area (ha)
Number of trees
Volume (m³)
Country
Area (ha)
Period
Austria 200,000 1993-2002 (?) 3,000
Germany 2,800,433
Poland 6,780,000 1990-99 12,838,000
Romania 90,000 1991-2000 8,109 2,028 2,235
Slovakia 120,000 1990-99 7,400
Spain 1,100,000 1990-99 10,000
Switzerland 45,000 1992-2000 30
Total 11,135,433 1990-2000 18,109 12,850,428 2,265
Table 9. Damage caused by Tomicus piniperda

Number of trees
Volume (m³)
Country
Area (ha)
Period
Switzerland 45,000
Spain 4,500,000 1990-99 200,000
Slovakia 120,000 1990-99 93,177
Romania 45,000 1991-2000 8109 2,028 2,235
Portugal 1 080 800
Poland 6,780,000 1990-99 12,838,000
Hungary 217,000
Germany 2,800,433
Total 14,507,433 1990-2000 8,109 12,933,205 202,235
4.7. Phaenops cyanea

Five countries provided quantitative data for this species (Table 9). The larger figures
concern Poland; the status of P. cyanea a in this country is similar as for T.piniperda,
which is not resulting clearly from the data in BAWBILT database (see comments in
previous section) .
Table 10. Damage caused by Phaenops cyanea
Volume (m³)
Country
Period
Slovakia 110,000 1990-99 1,159
Romania 50,000
Poland 4,400,000 1990-99 12,838,000
Hungary 217,000
Germany 3,233,001
Total 8,010,001 1990-99 12,839,159
4.8. Rhyacionia buoliana

Four countries provided quantitative information on this species. Significant damage
was reported on young pines in Hungary (17,300 ha) and in Romania (2,500 ha: Table
11).
Table 11. Damage caused by Rhyacionia buoliana

Country
Area (ha)
Period
Slovakia 100000 1990-99 343

Romania 10,000 1991-2000 2,495
Ireland 100,000
Hungary 217,000 1980-98 17,300
Total 327,000 1980-2000 20,138
4.9. Scolytus laevis

A total of 1,500 ha was reported to be potentially threatened by this species in
Slovakia, but no quantitative information on damage is available.
4.10. Synthesis of quantitative data on damage

Table 12 provides a synthetic account of the information above.
Table 12. A synthesis of quantitative data on damage caused by the "top ten" species
countries where
data available
Threatened
Number of
Number of
Area (ha)
Area (ha)
Species
Volume
Period
trees
Ips typographus 10 7,640,156 1990-2001 31,642,535 2,819,055
Hylobius abietis 11 3,418,264 1980-2000 88,258
Pityogenes chalcographus 8 8,784,001 1900-2000 730,049 7,827,506 595,400
Scolytus multistriatus and
4 224,100 1991-2000 3,000,000 10,711 524
Scolytus scolytus
Ips acuminatus 7 11,135,433 1990-2000 18,109 12,850,428 2,265
Tomicus piniperda 8 14,507,433 1990-2000 8,109 12,933,205 202,235
Phaenops cyanea 5 8,010,001 1990-99 12,839,159
Rhyacionia buoliana 4 327,000 1980-2000 20,138
5. CONTROL
During the early stages of BAWBILT there was considerable discussion on the types
of control measures that should be included in the database. General agreement was
reached on a number of categories of control which are shown in Appendix 1. On-line
data entry was carried out by 19 countries and most of the control options were
accessed, although not for all organisms in the list. However, it was interesting to note
that the number of control measures adopted was related to the degree of aggressivity
indicated in the Damage part of the database. Consequently, we have analysed the
control data using the list of organisms, in the same order of agressivity summarised in
Table 3. This is presented as a series off Tables for each of the principal control
categories in Appendix 1, namely Quarantine, Silvicultural Management, Chemical
Insecticide Application, Trapping Out, Biological Control, Other Control Strategies,
Monitoring, Risk Rating and Decision Support Systems. The degree of employment of
each strategy varied with the type of pest and, particularly with the damage rating of
that pest.
5.1. Quarantine
This category is concerned principally with prevention of movement of pests between
countries and, in some cases, within countries. The results are shown in Table 13. In
many respects, it is surprising that there were so many entries in this category. It can
only be assumed that the measures are related to the international movement of wood
and wood products from the countries concerned to other countries with restrictions on
importation of the named pests.
5.2. Silvicultural Management

This category contains the most commonly employed management options for
BAWBILT organisms. This reflects the possibility of enhancing tree health and,
thereby, increasing the ability of living trees to defend themselves against attack by a
range of pests, especially those entering through the bark. The results are shown in
Table 14.
Removal of breeding material through forest sanitation or, as an extreme measure,
clearfelling is practised for most of the pests in Table 14. These are traditional
measures and, although expensive to implement if they have to be carried out early in
the economic life of a crop, can provide some financial return from sales of extracted
timber.
5.3. Chemical Insecticide Application

Results for this analysis are shown in Table 15. Not all the organisms in the table have
been managed using insecticides and relatively few were treated as standing trees; in
this category the target is universally the adult stage. The most common usage was for
treatment of felled trees either to prevent attack or to prevent emergence of the
organisms that were breeding in the felled material.
5.4. Trapping Out

This is an alternative approach to silvicultural management and involves the deliberate
use of material to attract the adult stages of the BAWBILT pests and then to remove
the material before a full breeding cycle aand subsequent emergence can take place or,
in the case of pheromone traps, to prevent adult pests from reaching susceptible host
trees. The results are shown in Table 16. The measures have been most commonly
employed against Scolytidae, aided by the known attraction of the adult stages to
freshly cut or damaged trees. There are also commercially available pheromone lures
for the majority of the most damaging Scolytidae.
Table 13. Quarantine control measures employed against the most aggressive BAWBILT
organisms as listed in Table 3. The figures represent the numbers of countries which
implemented different types of quarantine measures against each species
Physical Treatment
restrictions
restrictions
Movement
Composting
Wet storage
Storage
Processing
Debarking
Covering
Species
Burning
HT/KD
Ips typographus 3 3 9 4 3 1 2 5 2
Hylobius abietis 1 1 1 1
Pityogenes chalcographus 4 3 2 1 1 4
Scolytus multistriatus 1 1 3 1 4
Scolytus scolytus 2 1 3 1 3
Ips acuminatus 1 4 2 3 3
Tomicus piniperda 1 5 1 1 2 3
Phaenops cyanea 2 1 1 2
Rhyacionia buoliana 1
Scolytus laevis 1 1 1 1
Cossus cossus 1
Cryptorhynchus lapathi 1 2
Dendroctonus micans 4 6 3 1 1 2 2
Ips duplicatus 2 4 1 1 1 2 1
Ips sexdentatus 1 1 4 2 1 1
Paranthrene tabaniformis 1
Pissodes castaneus 2 2
Tomicus minor 1 4 1 2 2 3
Trypodendron lineatum 1 3 2 1 1 1 3 1
Zeuzera pyrina 1 2
Agrilus biguttatus
Gnathotrichus materiarius 1 1 1 1 1
Hylastes ater 1
Hylastes cunicularius 1 1
Hylobius pinastri
Ips amitinus 1 8 3 3 1 2 4
Ips cembrae 1 4 3 1 1
Leperesinus varius 2 1 2
Monochamus sartor 1
Pissodes piniphilus 2 1
Pityokteines curvidens 4 2 1 3
Polygraphus poligraphus 2 1 1 1
Saperda carcharias 1 1
Saperda populnea 1
Scolytus intricatus 2 1
Scolytus triarmatus
Sirex juvencus 1 1 1
Tetropium gabrieli 2 2 1 1
Trypodendron domesticum 1 1 1
Urocerus gigas 1 1 1
Table 14. Silvicultural management measures employed against the most aggressive
BAWBILT organisms as listed in Table 3. The figures represent the numbers of countries
which implemented silvicultural management methods of each category for each species
Sanitary felling
Silvicultura
preparation
protection
sanitation
Selective
Physical
thinning
Pruning
l choice
felling
Forest
Clear
Species
Site
Ips typographus 9 9 3 12
Hylobius abietis 10 7 8 4
Pityogenes chalcographus 3 5 1 2 5
Tomicus piniperda 4 8 1 12
Phaenops cyanea 1 3 1 2 2
Rhyacionia buoliana 1 1 1 1
Scolytus laevis 5 2 2
Cossus cossus 1 4 4 2 1 3
Cryptorhynchus lapathi 2 3 1 1 1 3
Dendroctonus micans 2 7 1 2 5
Ips duplicatus 1 3 1 4
Ips sexdentatus 3 7 5
Paranthrene tabaniformis 1 3 3 1 1 3
Pissodes castaneus 1 4 2 9
Tomicus minor 2 4 1 2 8
Trypodendron lineatum 1 1
Zeuzera pyrina 3 1 5 1 2
Agrilus biguttatus 2 4 1 1 2
Gnathotrichus materiarius 1 1
Hylastes ater 1 2 1 1 4
Hylastes cunicularius 1 1 2 3
Hylobius pinastri 1 1
Ips amitinus 3 5 1 5
Ips cembrae 1 6 1 4
Leperesinus varius 2 1 1 2
Monochamus sartor 1
Pissodes piniphilus 2 3 1
Pityokteines curvidens 2 4 1 2 2
Polygraphus poligraphus 1 3 1
Saperda carcharias 1 4 1 3
Saperda populnea 4 1 1 2
Scolytus intricatus 4 1 4
Scolytus triarmatus 1 1
Sirex juvencus 1 5
Tetropium gabrieli 1 2
Trypodendron domesticum 1 1 1 1 2
Urocerus gigas 1 6
Table 15. Chemical insecticide measures employed against the most aggressive
BAWBILT organisms as listed in Table 3. The figures represent the numbers of
countries which use chemical insecticide treatments on each category of trees for
each pest species.
Systemic
Standing Felled Mature
Transplants Transplants
trees trees trees
Ips typographus 10
Hylobius abietis 2 14 6
Pityogenes chalcographus 5
Scolytus multistriatus 3 2 2
Scolytus scolytus 2 2 1
Ips acuminatus 6
Tomicus piniperda 1 6
Phaenops cyanea 2
Rhyacionia buoliana 2 1
Scolytus laevis 1
Cossus cossus 4
Cryptorhynchus lapathi 2 2 1 1
Dendroctonus micans 3 1
Ips duplicatus 1
Ips sexdentatus 4
Paranthrene tabaniformis 4 2 2
Pissodes castaneus 1 1 1 1
Tomicus minor 5
Trypodendron lineatum 4
Zeuzera pyrina 5
Agrilus biguttatus 1
Gnathotrichus materiarius 1
Hylastes ater 5 3
Hylobius pinastri 1
Ips amitinus 4 1
Ips cembrae 3
Leperesinus varius 1
Monochamus sartor 1
Pissodes piniphilus 2
Pityokteines curvidens 4
Polygraphus poligraphus 3
Saperda carcharias 3
Saperda populnea 1 2 1
Scolytus intricatus 2
Scolytus triarmatus
Sirex juvencus 1
Tetropium gabrieli 1
Trypodendron domesticum 1 3
Urocerus gigas 2
Table 16. Trapping out measures employed against the most aggressive BAWBILT organisms
as listed in Table 3. The figures represent the numbers of countries
t which use different types
of trapping out measures against each species.
Pheromone Baited
Trap trees Trap logs traps trees Baited slash
Ips typographus 7 9 12 7 1
Scolytus multistriatus 3 2 4 1
Scolytus scolytus 3 2 4 1
Ips acuminatus 5 4 1 1
Tomicus piniperda 7 8 1
Phaenops cyanea 3 1
Scolytus laevis 1 1 1
Cossus cossus 1 1 1
Cryptorhynchus lapathi
Dendroctonus micans 1
Ips duplicatus 2 2
Ips sexdentatus 4 5 2 1
Paranthrene tabaniformis 1 1
Pissodes castaneus 5
Tomicus minor 6 7 1
Trypodendron lineatum 1 1 2 1
Zeuzera pyrina 1 1
Agrilus biguttatus 1 1
Hylastes ater 1 2
Hylobius pinastri
Ips amitinus 6 3
Ips cembrae 1 1 2 1
Leperesinus varius 1 1
Monochamus sartor 1 1
Pityokteines curvidens 3 1 1
Saperda carcharias
Saperda populnea
Scolytus intricatus 2 1
Scolytus triarmatus
Sirex juvencus 1 1
Tetropium gabrieli
Trypodendron domesticum 2 1 1
Urocerus gigas 1 1
5.5. Biological Control

Although this category was included in the list of control measures, there were very
few records of use of biological control agents and, therefore, a full analysis has not
been carried out. However, this is covered in more detail elsewhere in this book (Kenis
et al., chapters 11 and 18; Kenis and Hilszczanski, chapter 21).
5.6. Monitoring
Part of effective management of pests is knowledge of their distribution and
abundance, especially in relation to availability
a of breeding material. Monitoring is,
therefore, an important element in making decisions about whether to apply active
control measures. Most countries implemented some form of monitoring system and
these are listed for the major pests in Table 17. The most commonly employed
measures use a combination of visual surveys, supplemented by use of various trap
systems using pheromones/attractants or trap trees/logs. Remote sensing has rarely
been employed and may offer opportunities for further development in the future.
5.7. Risk Rating and Decision Support Systems

This category received relatively few responses, but would appear to offer promise for
future integrated management of the most serious pests. Results of the analysis are
shown in Table 18. As with other control measures, the development of risk models
and decision support systems has made most progress with the most serious pests,
especially for I. typographus. It is likely that this approach will expand in the future,
especially with the increasing use and sophistication of GIS systems that are now
available.
6. CONCLUSIONS
Overall the information in the BAWBILT database has provided useful summaries of
the range of control measures employed by the member countries. The range of
measures has, predictably, been linked to the degree of severity of the damage caused
by the listed pests. It was not, however, possible to carry out cost-benefit analyses of
the various control measures carried out or even to assess the relative efficacy of those
measures. This indicates that improved quantification of the cost and effectiveness of
pest management for BAWBILT organisms could be a priority for the future. In
addition, work should aim to integrate experiences from the countries involved in this
COST action to develop procedures of wide applicability for management of
BAWBILT pests.
Table 17. Monitoring systems employed against the most aggressive BAWBILT organisms as
listed in Table 3. The figures represent the numbers of countries which use different types of
monitoring systems against each species
Pheromones/
Questionnaire
attractants
trees/logs
sampling
Remote
sensing
survey/
Visual
Trap
Species
Hylobius abietis 3 5 11 0 3
Tomicus piniperda 1 5 8 0 2
Phaenops cyanea 0 2 4 0 2
Rhyacionia buoliana 2 1 5 1 2
Scolytus laevis 0 2 2 0 1
Cossus cossus 1 0 5 1 2
Cryptorhynchus lapathi 0 0 5 0 2
Dendroctonus micans 0 3 9 2 1
Ips duplicatus 4 4 3 0 2
Ips sexdentatus 3 3 7 0 1
Paranthrene tabaniformis 1 0 2 0 2
Pissodes castaneus 1 3 5 0 0
Tomicus minor 1 5 7 0 1
Trypodendron lineatum 3 1 3 0 1
Zeuzera pyrina 3 0 6 1 0
Agrilus biguttatus 0 2 3 0 2
Gnathotrichus materiarius 0 0 2 0 0
Hylastes ater 0 0 3 0 1
Hylastes cunicularius 0 0 5 0 1
Hylobius pinastri 0 0 1 0 0
Ips amitinus 3 7 7 0 2
Ips cembrae 3 3 4 0 2
Leperesinus varius 0 0 4 0 1
Monochamus sartor 0 0 0 0 0
Pissodes piniphilus 0 0 4 0 0
Pityokteines curvidens 0 1 4 0 2
Polygraphus poligraphus 1 1 4 0 1
Saperda carcharias 0 0 5 0 1
Saperda populnea 0 0 3 0 1
Scolytus intricatus 0 1 3 0 3
Scolytus triarmatus 0 0 1 0 0
Sirex juvencus 0 0 1 0 0
Tetropium gabrieli 0 0 1 0 1
Trypodendron domesticum 1 0 3 0 2
Urocerus gigas 0 0 1 0 0
Table 18. Risk rating and decision support systems

y employed against the most aggressive
BAWBILT organisms as listed in Table 3. The figures represent the numbers of countries
which use different risk rating and decision
i support systems for each species.
Risk models Decision

Species Local Regional National GIS support
scale scale scale systems
Pityogenes chalcographus 3 2 1
Scolytus multistriatus 1
Scolytus scolytus 1 1
Ips acuminatus 3 2
Tomicus piniperda 2 2 1
Phaenops cyanea 1
Scolytus laevis 1
Cossus cossus 1
Cryptorhynchus lapathi 1
Dendroctonus micans 1 1
Ips duplicatus 1
Ips sexdentatus 1 1 1
Paranthrene tabaniformis 1 1
Pissodes castaneus
Tomicus minor 2
Trypodendron lineatum 1 1
Zeuzera pyrina 1
Agrilus biguttatus 1
Hylastes ater 1
Hylastes cunicularius 1
Hylobius pinastri
Ips amitinus 3 1
Ips cembrae 1 1
Lesperesinus varius
Monochamus sartor 1
Pityokteines curvidens 1 1
Saperda carcharias 1
Saperda populnea 1
Scolytus intricatus 1
Scolytus triarmatus
Sirex juvencus 1
Tetropium gabrieli
Trypodendron domesticum 1
Urocerus gigas
Appendix 1: Categories of control measures in the BAWBILT Database
Quarantine Movement restrictions

Storage restrictions
Physical treatment Debarking
Covering
Processing
Composting
Heat treatment/KD
Wet storage
Burning
Silvicultural management Sanitary felling Clear felling
Selective thinning
Site preparation
Pruning
Physical protection
Silvicultural choice
Forest sanitation
Other
Chemical insecticide application Standing trees
Transplants
Felled trees
Systemic Transplants
Mature trees
Trapping out Trap trees
Trap logs
Pheromone traps
Baited trees
Baited slash
Other
Biological control Predators
Parasitoids
Microbial control Bacteria
Fungi
Nematodes
Protozoa
Viruses
Other
Other control strategies Interruption of attack: thinning
Prevention of attack
Fallow period
Ectomycorrhizae
Monitoring Pheromone traps
Trap trees/logs
Visual surveys
Remote sensing
Other
Risk rating and Decision Support Risk models Local scale
Systems Regional scale
National scale
GIS
Decision support systems
Part 1
Bark Beetles
Chapter 5
TAXONOMY AND SYSTEMATICS OF BARK AND

AMBROSIA BEETLES
K 1 & R. BEAVER
M. KNÍŽEK R2
1
tČ – Strnady, CZ 150 00,
Forestry and Game Management Research Institute, JílovištČ
Praha 5 – Zbraslav, Czech Republic
2
161/2 Mu 5, Soi Wat Pranon, Tambon Donkaew,Ampur Maerim, 50180 Chiangmai,
Thailand
1. INTRODUCTION
Bark beetles in a wide sense include the true bark beetles (many Scolytidae), which
breed in and feed on the phloem (phloeophagous species), and the ambrosia beetles
(many Scolytidae, and all Platypodidae), which bore into the wood and feed
primarily on symbiotic ambrosia fungi living in the tunnels (xylomycetophagous
species). Some Scolytidae also develop in hard seeds and fruits (spermophagous
species), in the central pith of twigs and other small stems, or in the petioles of fallen
leaves (myelophagous species). We use the term 'bark beetles' to cover all these
categories, unless otherwise specified. Bark beetles usually live in scattered habitat
units, which are suitable for breeding for only a single generation of beetles. This
means that the new generation of adults must disperse to find new breeding sites.
These two features mean that bark and ambrosia beetle populations are very variable
both in space and time, depending on the spatial and temporal availability of suitable
breeding material. The study of their temporal and spatial dynamics is very
important both because of their economic importance
m in forests, and the ease with
which these small beetles can be transported to, and become established in, new
areas. The majority of species breed in dead or dying tissues, and are not normally
of economic importance. However, such species can become economically
important if their galleries create holes in timber used for furniture or veneer, or if
they transport pathogenic fungi to living trees during a period of feeding by young
adults to mature the gonads. The relatively small number of species that attack living
trees, saplings or seedlings, or the seeds off commercial crops (e.g. coffee, palms) are
sometimes of major economic importance, causing damage estimated in millions of
41
41—54.
© 2007 Springer.
42 M. KNÍŽEK & R. BEAVER
dollars. Such losses occur in both temperate and tropical zones, especially where
there are monocultures and plantations, which can provide suitable conditions for
rapid population increase, for example following extensive windfalls. As a result,
the beetles have been of particular interest to foresters for hundreds of years, and
much of the work on them has been done by forest entomologists.
2. HISTORICAL STATUS OF THE FAMILY SCOLYTIDAE AND

PLATYPODIDAE
2.1. Historical overview

The first five species of Scolytidae to be described were named by Linnaeus (1758),
and placed in his genus Dermestes. All are European species, but now placed, of
course, in other genera. Geoffroy (1762) described the genus Scolytus for the species
S. scolytus, and transferred Linnaeus' species to the genus Bostrichus. Fabricius
(1801) included 52 species of scolytid in his monograph, and added the genus
Hylesinus. He also described the first platypodid species, Platypus cylindrus,
although in the genus Bostrichus. Latreille (1807) was the first to consider the
scolytids at the family level, and Shuckard (1840) the platypodids. Later, in the 19th
century, several authors increased the number of species and genera in both families.
Here we should mention especially the monographs of Chapuis (1865) on
Platypodidae and Chapuis (1869) on Scolytidae, and the monograph of Eichhoff
(1879) on Scolytidae, which laid the foundation for later studies. The first catalogue
of Scolytidae (including Platypodidae) was included in the systematic catalogue of
Gemminger and Harold (1872), who listed 534 valid species in 60 genera.
In the first half of the 20th century, there were great advances in bark beetle
systematics. Blandford monographed the species of Central America in the series of
contributions between 1895-1905. In the set Coleopterorum Catalogus, Hagedorn
(1910a) catalogued the genera and species of Scolytidae (1234 species in 115
genera), and Strohmeyer (1912) those of Platypodidae (323 species in 13 genera).
These authors also contributed fascicles on their respective families to the series
Genera Insectorum (Hagedorn 1910b; Strohmeyer 1914a,b). Reitter (1913) provided
a workable key to the species of Europe and neighbouring countries. In North
America, the studies of A.D. Hopkins and M.W. Blackman greatly advanced the
work of J.L. LeConte in the previous century. Much more work was also done on
tropical species, particularly by the German Hans Eggers, the Austrian Karl Schedl,
and the Pole Marian Nunberg. In the second half of the 20th century, major
contributions have been made in the palearctic region by A. Balachowsky (France),
A. Pfeffer (Czech Republic), V.N. Stark (the t former Soviet Union), J. Murayama
and A. Nobuchi (Japan). In the Americas, we have the important works of S.L.
Wood and D.E. Bright, and in the old world tropics, those of F.G. Browne, and H.
Roberts (United Kingdom). In particular, our knowledge of bark beetle classification
has benefited from the generic level studies of Wood (1986) on Scolytidae and
Wood (1993) on Platypodidae. Many others have also contributed, and
accompanying this systematic knowledge, there has been considerable advance in
SYSTEMATICS OF BARK AND AMBROSIA BEETLES 43
our knowledge of the biology and ecology of the beetles. Recently some new
specialists have begun publishing to continue taxonomic studies. In addition,
molecular studies have begun both to add to our knowledge, and to cast doubt on
currently accepted classifications.
After the catalogues of Hagedorn and Strohmeyer, no further attempt was made
to catalogue the families worldwide until the work of Wood and Bright (1992).
These authors provided a detailed catalogue giving not only a list of all genera and
species with synonyms, but information on types, host plants and distribution, and a
list of references to each species. The catalogue deals with 5 812 species in 225
genera in 25 tribes, illustrating the enormous
r increase in knowledge of bark and
ambrosia beetles since the early years of the century. Two supplements to this
catalogue have appeared (Bright and Skidmore 1997, 2002) bringing the work up to
the year 1999. Together, these works form what must be one of the finest references
available to workers on any family of beetles.
2.2. Bibliographies
Because of the importance of bark beetles in forest protection and forest industry,
many works and notices about their biology, faunistics and forest protection
methods have been published in forestry-oriented papers. This caused problems in
collating information, and the need for bibliographical work developed. The first
bibliography was published by Trédl and Kleine (1911) in the journal
Entomologische Blätter, including 1 800 citations. In 1939, a new Kleine
bibliography was published in the Stettiner Entomologische Zeitung including
nearly 4 000 citations. In 1946 – 1949, Schedl published a continuation of these
bibliographies in Zentralblatt für das Gesamtgebiet der Entomologie, and later he
collected all these works together in Bibliografia Mundial Sobre Scolytidae e
Platypodidae (Schedl 1974), which lists nearly 5 000 citations of particular articles
or monographs as well as giving a list of sources for the bibliography (journals etc.).
As indicated above, numerous, more or less locally oriented faunas, check-lists,
catalogues and smaller monographs, as well as the descriptions of the new species,
were published by numerous authors within the 20th century. The most recent
comprehensive bibliography of Scolytidae and Platypodidae was published by
Wood and Bright in 1987 (including 21 488 references). Supplements to this are by
Wood and Bright (1987) (2 664 references), Bright and Skidmore (1997) (1 420
references) and Bright and Skidmore (2002) (1 341 references). This is an
outstanding series of publications giving us a total overview of both families,
Scolytidae and Platypodidae, from a bibliographical as well as a systematic view.
We may mention here the difficulty of continuing such a huge work. The number of
citations is increasing rapidly and it is doubtful if one or even a small group of
specialists will be able to gather and collate all this information and prepare further
Supplements or a more comprehensive work. The development of a computerized
version would help.
2.3. Recent status of the families Scolytidae and Platypodidae

Traditionally both taxonomic groups, Scolytidae and Platypodidae, have been

considered as separate families within the superfamily Curculionoidea, although
K.E. Schedl, in particular considered them to form a separate superfamily
Scolytoidea. Crowson (1967) included both these families in the Curculionidae,
primarily on the basis of the absence of convenient larval characters that could
separate them from that family. However, the family status for all these groups was
still generally accepted, although rather strong
t comments were made on this topic
(Wood 1973, pers. comm.). The leading authority on the families, Stephen Wood
(1973, 1986) has continued to maintain them as distinct families. His arguments are
based primarily on the presence of a distinct 'pregular' sclerite (=submentum) and
'pregular' sutures (but see Lyal 1995), and on the presence of denticles on the tibiae
or stout socketed setae (occasionally secondarily lost). Wood (1986) notes that,
although platypodid larvae are distinguishable from those of other curculionoids,
those of some scolytids are not. However, he suggests that this may be related to
simplification and reduction resulting from small size. More recently, and
particularly since the publication of Lawrence and Newton (1995), there has been a
tendency to reconsider the two families, or at least the Scolytidae, as subfamilies of
Curculionidae. This opinion is based partly on morphological (Thompson 1992;
Kuschel 1995) and partly on molecular data (Marvaldi et al. 2002). It is also
possible that the platypodids should be included as a tribe within the subfamily
Scolytinae (Kuschel et al. 2000; Farrell et al. 2001), although Marvaldi et al. (2002)
argue that the evidence for this is weak. Arguments are likely to continue for some
time before a consensus is reached. Forest entomologists, unconcerned with the
niceties of systematic position, will no doubt continue to consider the Scolytidae and
Platypodidae as distinct families for some time to come – as we have done here. In
the meantime, the change has brought some inconvenience to those working on the
two groups, for the Zoological Record has lumped them within the Curculionidae, so
that workers have to search through the whole of this large section to try to locate
new information.
The situation in systematics of the whole superfamily of Curculionoidea was
nicely characterized by Alonso-Zarazaga and Lyal (1999), from which we would
like to cite a few sentences:
“The superfamily Curculionoidea ('weevils') contains a significant proportion of
all known species of Coleoptera and includes, as presently understood, the largest
family of animals, the Curculionidae. Although the group is large, conspicuous and
important (and perhaps for all these reasons), the systematics at almost all levels is
chaotic, and access to current nomenclature very difficult.
In modern treatments of the Curculionoidea (notably Thompson 1992; Kuschel
1995; Zimmerman 1994 and the beetle catalogue of Lawrence & Newton 1995)
widely differing family concepts are used. The range of accepted families in recent
works is between 22 and 6, and the number of subfamilies between 100 and 10!
(Kuschel 1994). This would not be very important if the various concepts were
consistent and differences were simply in rank. Unfortunately this is not so, and
many subfamilies, tribes and genera 'float' between higher taxa without any clear
idea being given in the papers making the changes of what characters indicated these
placements and how these characters were interpreted. Thus present classifications
(of Curculionoidea) are a mixture of monophyletic, paraphyletic and polyphyletic
taxa.”
3. TAXONOMY
3.1. Identification
For any economically important insect group, a sound taxonomic and biological
knowledge is an essential basis for any attempt at management or control. The
accurate determination of the species involved is the basis for decision-making.
Without this knowledge, actions taken could well be ineffective or erroneous. This is
true for the bark beetles, which, as indicated earlier, have a variety of habits.
Management and control strategies must be related to the habits of the particular
species involved.
In Europe, the bark beetle fauna is well known, and there are both regional and
more local keys available which will allow an accurate identification of nearly all
species if used with care. In the authors' opinion, the most useful and up-to-date key
to the bark beetles of the European region and neighbouring areas, extending from
North Africa to Central Asia, is the publication by Pfeffer (1995). Other keys for
more local areas include Balachowsky (1949) (France); Hansen (1956) (Denmark);
Pfeffer (1955, 1989) (Czech Republic and Slovakia); Nunberg (1954) (Poland);
Karaman (1971) (Macedonia); Stark (1952) (Russia).
R The older publications should
be used with some care, because there have been considerable taxonomic changes at
generic and specific levels, new and changed synonymy, and most importantly,
newly introduced species, which do not appear in some of the keys. Fortunately,
Wood's generic revisions of Scolytidae (Wood 1986) and Platypodidae (Wood 1993)
provide a means to determine at least the genus of introduced species. In addition,
two publications, which include distribution maps, should be mentioned – Lekander
et al. (1977) covering the Nordic countries, and Bovey (1987) covering Switzerland.
Again, it needs to be remembered that the distribution of a number of species of bark
beetle is changing, in response to changes in host distribution, climate, etc. (see
below).
3.2. Basis of Classification
3.2.1. External Morphology

The most recent classification of Scolytidae and Platypodidae at the tribal and
generic levels is that of Wood (1986, 1993). This has been fairly generally accepted,
although there are problems with the delimitation of some tribes and genera, and the
inclusion of certain genera within the Platypodidae. Some changes may be expected
in the future. Wood (1986) divides the Scolytidae into two subfamilies and 25 tribes.
Both subfamilies and the following fifteen tribes are represented in the European
area: Hylesininae: Hylastini, Hylesinini, Tomicini, Phloeotribini, Phloeosinini,
Hypoborini, Polygraphini; Scolytinae: Scolytini, Ipini, Dryocoetini, Crypturgini,
Xyloterini, Xyleborini, Cryphalini, Corthylini. The Platypodidae is a largely tropical

family, and only two species are present in Europe, both in the tribe Platypodini.
The classification of Wood is based almost entirely on external morphology.
Wood (1978, 1993) has discussed in detail the characters which are of value in
classifying the families at tribal and generic levels, and only a brief resume will be
given here, omitting the Platypodidae,
t for which reference can be made to Wood
(1993). In the Scolytidae, many characters of the head are used in classification. The
frons presents characters (shape, sculpture and ornamentation) useful at almost all
levels from tribe to sexual differences. The eyes are usually elongate-oval, but may
be entire, emarginate, or divided into two parts, as in Trypodendron and most
species of Polygraphus. The antenna is of considerable importance in classification.
The primitive number of funicular segments (7) is often reduced. The number is
characteristic of certain tribes (e.g. Hylastini (7), Xyloterini (4)), and can be useful
in separating genera. The club is extremely variable, and can be conical, compressed
or obliquely truncate, symmetrical or asymmetrical, with sutures visible on both
sides or only one, with three or one segments, and occasionally with five or more
pseudosutures. In the genus Phloeotribus, the segments of the antennal club are
lamellate and independently movable.
In the thorax, the shape of the pronotum is important. In the Hylesininae, it is not
strongly declivous anteriorly, and the head is visible from above; in the Scolytinae,
changes in the axis of the anterior foramen from vertical to oblique, have led to the
restructuring of the segment, so that the sternal area is shortened, and the dorsal part
of the pronotum has become declivous, and the head is largely orr entirely concealed
beneath it. The detailed form of the pronotum is often characteristic of genera. The
shape and visibility of the scutellum is a very useful character, primarily at generic
level, but also at subfamily level. In the Hylesininae, the scutellum, if visible, is
usually small, convex, and slightly depressed below the level of the elytra in a
sutural notch. In the Scolytinae, it is usually large and flat, and lies flush with the
elytral surface. However, there are many exceptions to this in the Xyleborini.
The elytra are extremely variable in structure and sculpture. In the Hylesininae,
the basal margins of the elytra are procurved and slightly raised and bear a row of
crenulations; in the Scolytinae, the basal margin is unarmed and usually forms a
straight, transverse line across the body. Again there are exceptions to this in the
Xyleborini, related to the presence of mycangia in or near the elytral bases. The
variation in elytral form and sculpture is particularly important at the specific level,
but particular elytral forms can be characteristic of certain genera. The
metepisternum is usually visible throughout its length in scolytids, but in the tribes
Cryphalini and Corthylini, it is largely covered by the elytra and only the anterior
part is visible. Further metathoracic characters are discussed by Wood (1978).
Whilst of clear classificatory importance, they have the disadvantage of being
hidden from view unless one elytron is removed, or the elytra are spread, and are
difficult to use in keys. The legs are also important in classification, especially the
tibiae. The tibiae bear spines on the outer margin that may be unsocketed or
socketed, the latter presumed to have a setal origin. In the Scolytini (and some other
extra-limital groups) they have been secondarily lost, and the tibiae bear simply an
apical curved spine. The shape of the tibia is also important in separating certain
tribes and genera. The presence or absence of a groove for reception of the tarsus is
also used in classification (e.g. Cryphalini). The size of separation of the coxae is
used to separate some genera (e.g. Xyleborus and Xylosandrus).
The abdomen has not been much used in scolytid classification, although its
sculpture is important in separating species of Scolytus. In the Scolytini and
Xyloctonini, the elytra are flat, and the abdomen ascends to meet them. In the
majority of scolytids the elytra are declivous, and the abdomen correspondingly
more or less flat.
The majority of the ambrosia beetles have mycangia. These are cuticular tubes,
pouches or pits of various sizes, associated with glandular cells and opening to the
surface of the body. They are used to carry the spores of the symbiotic ambrosia
fungi. They may be found in many parts of the body (head, thorax, and elytra), but
are usually constant in position in particularr genera (Beaver 1989). As yet, they have
not been used in classification.
3.2.2. Sexual dimorphism

Nearly all Scolytidae and Platypodidae are sexually dimorphic to some degree.
Structures involved include the frons (e.g. Hylesinus, Trypodendron), the elytral
declivity (some Crypturgus species), or both ((Ips, Pityokteines, Phloeosinus), the
abdominal ventrites (Scolytus), and the presence of mycangia (Scolytoplatypus).
Various combinations of these and other characters may also be involved. Many
scolytids and platypodids can stridulate producing sounds which are used in inter-
individual interactions. Three types of stridulatory systems of the file-plectrum type
are found in the Scolytidae, and one in the Platypodidae, nearly always less well
developed (or absent) in the female than in the male (Lyal and King 1996). The
differences between the sexes are greatest in the inbreeding groups (e.g. Xyleborini,
some Dryocoetini and Cryphalini) in which the male is dwarfed, wingless, and with
reduced eyes, and usually with reduced sclerotisation. It may have a similar form to
the female, or the pronotum may be modified in various ways. The extreme case is
the genus Ozopemon (Dryocoetini), in which the male is neotenous and larviform,
but has a well-developed aedeagus. In the Platypodidae, the sculpture of the elytra is
always better developed in the male. There may also be differences between the
sexes in the structure and ornamentation of the frons, and in the presence, number
and size of the mycangia, and in other characters.
3.2.3. Internal Morphology

Internal morphology has not been generally used in the classification of bark beetles.
Hagedorn (1910c) attempted to use the mouthparts as the basis of his classification
of Scolytidae, but his scheme is unworkable. Mouthparts have some value in
separating the major divisions of the Platypodidae (Wood 1993). Characters of the
mouthparts have occasionally been used to distinguish species (Erichson 1836), as
have the internal sclerotized processes in the proventriculus (e.g. Nobuchi 1969).
Other characters of the alimentary canal could also be of some taxonomic value
(Thomas 1967; May 1995). Sometimes entomologists have tried to use the
characters of the copulatory organs, mainly in males (e.g. Israelson 1972), but also
females (e.g. Fuchs 1911). The characters of the male aedeagus do have value
taxonomically, but most workers on the bark beetles have based their classifications
primarily on more easily visible external characters.
3.2.4. Immature Stages

Knowledge of the immature stages of Scolytidae and Platypodidae remains limited,
and there have been rather few papers published. Thomas (1957) provided a useful
discussion of the use of larval anatomy in bark beetle studies, and Lekander (1968)
published the most comprehensive survey of scolytid larvae so far. Browne (1972)
reviewed the characters of many platypodid genera. These papers, together with the
work of May (1993), suggest that a classification based on larval morphology would
be reasonably concordant with one based on adult characters. However, most papers
have dealt with the description of the larvae (rarely pupae) of particular species, and
have not attempted to integrate their work into a more general scheme. This is an
area of research in which much more work needs to be done.
Another feature which has been used in the preliminary identification of the true
bark beetles is the form of the gallery system below the bark. This often has a form,
which is characteristic of a species (see for example the figures in Balachowsky
(1949) or Pfeffer (1995)). The form of the gallery system is less informative in the
non-phloeophagous bark beetles.
4. GEOGRAPHICAL DISTRIBUTION
4.1. General distribution

More than 6000 species of Scolytids and approximately 1500 species of platypodids
have now been described worldwide. More than 600 scolytid species occur in North
America and nearly 900 species occur in the Palaearctic region. We can easily
conclude from these numbers, that the main centre of geographical distribution and
species diversity of bark and ambrosia beetles is in the subtropical and tropical
regions. It is also in this region that much speciation seems to have occurred,
particularly in the tribes Dryocoetini, Xyleborini, and Cryphalini. This
diversification seems to have been related to the evolution of an inbreeding strategy,
characterised by sib-mating before the new generation of females emerges from the
gallery system, haplodiploidy (in Dryocoetini and Xyleborini), or its genetical
equivalent, pseudoarrhenotoky (in Cryphalini), and sex ratios strongly biased
towards females. This strategy seems to have evolved once in the evolutionary line
including the Dryocoetini and Xyleborini (Jordal et al. 2000), and separately in the
Cryphalini. The advantages of the strategy are that it increases the biotic potential of
the species because nearly all individuals are female, and can reproduce; secondly
that the colonization of isolated habitats is made easier if both male and female do
not need to find the habitat at the same time (Beaver 1977). By these facts the
particular species can easily distribute into the new territories. The reasons for the
relative lack of species adopting the strategy in the temperate zone remain unclear.
The total number of species of bark beetle in Europe depends on where the
geographical boundaries are set, particularly in the East (whether the Caucasian
countries are included or not), and whether African island groups, such as the
Canary Islands, are included. Quite large areas are sometimes omitted from
databases and recent publications, giving totals thatt vary from about 250 – 300
species. (By contrast, the island of Borneo in the Southeast Asian tropics, with an
area less than 10% of Europe has a fauna of about 600 described species, with many
more undescribed.) The regional distribution of bark beetles depends on many
factors, but is determined mainly by climate and the distribution of the host plants.
In considering the host plants, it is important to consider historical changes in host
plant distribution, the frequency of occurrence of species in the region, and forest
management practices. In recent decades, commercial trade has also had a large and
important influence on bark beetle distribution (see below).
The local distribution of bark beetles is related primarily to the presence of
suitable habitat for breeding and for use as a food source. Sudden increases in the
abundance of suitable habitat, e.g. following a windfall, may result in the course of
2-3 years in a population reaching outbreak proportions. This can be important if the
presence of very large numbers of beetles allows them to overcome host resistance,
and successfully attack and kill living trees. However, most species remain at low
population densities on a regional scale, although they may be abundant locally.
4.2. Introduction of exotic species and changes in distribution

One of the consequences of increased international trade has been the introduction
of 'exotic' species into countries outside their normal distributional range. According
to some estimates, approximately 20% of the species of bark beetle found in Europe
have actual or potential importance as forest pests, having economically important
consequences for the forest and timber industries. For this reason, we have to care
about both the introduction of new species and possible pests into Europe, and also
the export of pest species to other countries. Some of the more important bark beetle
pests in North America have been imported from Europe (e.g. Scolytus multistriatus
(Marsham), Tomicus piniperda (L.)). It is not only the introduction of these exotics
that is important, but the fact that they may carry with them pathogenic
microorganisms and fungi (Wegensteiner et al. 1996). Probably all bark beetles, not
just the ambrosia beetles, are associated in some way with fungi. The primary role of
the mycangia of ambrosia beetles is to carry symbiotic fungi, but they, and the body
surface, may sometimes transport spores off fungi, which are pathogenic to the host
trees, as with the well-known example of the Dutch elm disease fungus (Webber
2000).
The most important sources of potential pest species for Europe are areas which
are similar climatically, e.g. temperate and subtropical areas of Asia and North
America. The most frequent introductions into Europe have been from the Far East
(Siberia), Japan and the U.S.A. (e.g. Gnathotrichus materiarius (Fitch), and
Xylosandrus germanus (Blandford), both of which are ambrosia beetles). Other
species have increased their natural distribution as a result of changes in their
environment. An example is the important forest pest, Ips typographus (L.), which
was originally restricted in its distribution to the native territory of its host plant,
spruce (Picea). Because of the development of extensive plantations of spruce,
mostly in monoculture, throughout much of Europe, its range has increased very
rapidly, and it can now be found everywhere that spruce is planted. In other cases,
species have moved into warmer climates from northern areas, or from higher to
lower elevations on mountains. If, as a result, they become multivoltine in the
warmer climate, they may more likely become pests. Some species which have
increased their distribution in Europe in the last hundred years are Ips amitinus
(Eichhoff), I.duplicatus (Sahlberg), Orthotomicus robustus (Knotek), Pityophthorus
micrographus (L.) and several species in the tribe Xyleborini (Pfeffer and Knížek
1989). Internal trade can also result in changes in distribution within Europe (e.g.
Dendroctonus micans (Kugelann)).
The primary points of entry of exotic species are likely to be the ports of coastal
states, which import goods from all over the world. Direct trade in lumber or wood
products can introduce bark beetles, but they are often present in the pallets and
dunnage of other commodities, and can easily escape the attention of inspectors. As
restrictions on the import of untreated or unbarked timber have been introduced,
such packing has become a frequent source of introductions. It is very important to
be prepared for such introductions, and to be able to correctly determine the species
involved. Once this has been done, knowledge of the bionomics of the species in its
native habitat is essential in order to determine the possible consequences of its
establishment. The majority of imported species do not establish themselves, but the
economic consequences of even one doing so can be very great.
We can divide introduced species into three categories:
1. Individuals of the exotic species are introduced into a new territory, but do not
find conditions suitable for their breeding and development, and die. Such
species are unimportant from an economic point of view.
2. Introduced individuals find suitable conditions and survive initially because they
can establish a new brood in a suitable host plant. However, because of the
unsuitable climate, the whole population dies, usually within one year.
3. Introduced individuals find the suitable conditions for their development,
establish and become new permanent members of the local fauna. Here we can
recognize three grades:
a. Established species persist but do not cause any economic or other damage,
and are not aggressive against the native fauna.
b. Established species, which fully occupy a free or previously, by other
species, occupied niche. They may eliminate native species, but do not
cause any economic or other damage.
c. Established species, which fully occupy a free or previously, by other
species, occupied niche, and may eliminate some native species, but the
new conditions facilitate their multiplication to outbreak status, resulting
in economic and other damage.
In all these cases, not only climatic conditions and the presence of suitable
breeding material can influence the result, but also the presence or absence of
natural enemies. However, natural enemies react only after a time delay to the
presence of a new host or prey population, and their influence may be too small or
too late. It is also important to note that species, which mate before dispersal, such
as the Xyleborini, have a greater chance of establishing new populations, because
only the female, and not both sexes, need to be introduced into the new country at
the same time.
The European and Mediterranean Plant Protection Organization lists the
following non-European species on its quarantine list (http://www.eppo.org/):
Dendroctonus adjunctus Blandford, d Dendroctonus brevicomis LeConte,
Dendroctonus frontalis Zimmermann, n Dendroctonus ponderosae Hopkins,
Dendroctonus pseudotsugae Hopkins, Dendroctonus rufipennis Kirby, y Dryocoetes
confusus Swaine, Gnathotrichus sulcatus (LeConte), Ips calligraphus (Germar), Ips
confusus (LeConte), Ips grandicollis (Eichhoff), Ips lecontei Swaine, Ips
paraconfusus Lanier, r Ips pini (Say), Ips plastographus (LeConte).
All of these species are native to North America, where some of them are very
important pests, partly because they are able, through mass attacks, to overcome the
resistance of living trees, and cause extensive tree mortality. It may be noted that
species from the eastern half of the Palaearctic region and tropical regions are not
included in the list, except Scolytus morawitzi Semenov is mentioned in additional
list. As the candidates for including are Ips hauseri Reiter andd I. subelongatus
(Motschulsky). EU ranges between quarantine pests two species namely,
Pseudopityophthorus pruinosus (Eichhoff) and P. minutissimus (Zimmermann), and
other bark beetles specifies as Scolytidae spp. – all non-European species related to
plants of conifers over 3 m in height, othert than fruit and seeds, wood of conifers
(Coniferales) with bark, and isolated bark of conifers (Coniferales), originating in
non-European countries.
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Platypodidae). Basel: Pro Entomologia.
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Publishing.
Chapter 6
GENETIC TOOLS IN SCOLYTID RESEARCH
C. STAUFFER
BOKU – University of Natural Resources & Applied Life Sciences, Vienna,

Institute of Forest Entomology, Forest Pathology & Forest Protection,
Hasenauerstraße 38, A-1190 Wien, Austria
1. INTRODUCTION
At the beginning of the 1960’s, allozyme electrophoresis revolutionised many
research fields, including those of systematic and population genetics. In the mid
1990’s, the polymerase chain reaction (PCR) improved DNA sequencing and lead to
the flourish of molecular markers for systematic and population genetic studies.
Many of these techniques have been applied to scolytid research and have helped
answering phylogenetic and phylogeographic questions. This review deals with
species within the databank of the EU funded Bark and Wood Boring Insects in
Living Trees (BAWBILT). Papers that deal with topics like the bark beetle sexual
evolution or host-beetle co evolution are nott described in this review (e.g. Normark
et al. 1999, Farrell et al. 2001, Jordal 2002).
2. PHYLOGENETICS
American scolytid specialists Steven Wood and Donald Bright called to attention the
lack of students of scolytid systematics (Wood & Bright 1998 - personal
communication at the European Entomological Congress). It will be important to
define scolytid species by sequencing specific regions of the DNA and these
diagnostic markers need to be associated with morphological characters that define the
species as it is also proposed by Tautz et al. (2003). The data entries in the Genbank,
allow scientists worldwide to use the existing ones for their analysis.
2.1. Genus Ips

In Central Europe Ips species are characterized by differences in morphology,
structure of galleries, host specificity and aggressiveness. An analysis with a partial
region of the mitochondrial DNA revealed high inter-specific and low intra-specific
55
55–61.
© 2007 Springer.
56 C. STAUFFER
sequence divergence. A phylogenetic analysis both with maximum parsimony and

distance method clustered I. typographus, Ips cembrae, I. amitinus, I. duplicatus and
I. acuminatus, and put I. mannsfeldi and I. sexdentatus like the two outgroup
species. I. mannsfeldi and the outgroup O. erosus emerged as sister pairs. These
findings agree with Cognato & Sperling (2000), except that Ips acuminatus does not
have the close relationships to the eight spined bark beetles. I. mannsfeldi was
further removed from Ips to Orthotomicus (Cognato & Vogler 2001) as already
proposed by Wood (1982) and Escherich (1923). It is further likely that the genus
Orthotomicus comprises two genera (Cognato personal communication).
The eight spined larch bark beetles that infest various Larix species in Europe
and Asia were analysed (Stauffer et al. 2001). Ips subelongatus, Ips fallax, Ips
shinanonensis and Ips cembrae var. engadinensis were often treated as synonyms of
I. cembrae. These four taxa are distinguished by host tree and geographic
distribution, as morphological diagnostic characters are deficient. The European
populations differed by 4.3% from the Asian populations. The phylogenetic analysis
placed the European and Asian haplotypes in significantly distinct clusters. The
results suggest that the I. cembrae complex contains at least two taxa: I. cembrae in
Europe and I. subelongatus in Asia.
In 1913, Fuchs described Ips amitinus var. montana as a race of Ips amitinus.
The differences were based on the different host trees and on body size. The main
host of I. amitinus is Picea abies and of I. amitinus var. montana are Pinus cembra
and Pinus montana. Four populations of I. amitinus and two populations of I.
amitinus var. montana were studied in order to evaluate evolutionary and ecological
implications of this race differentiation. Behavioural, ecological and DNA analysis
revealed no evidence to suggest distinct races (Stauffer & Zuber 1998).
Ips japonicus was first described by Niijima (1909) on Yezo spruce, Picea
jezoensis and Sachalin spruce, Picea glehnii in Japan. In literature Ips japonicus is
often mentioned as a form of I. typographus. Pfeffer (1994) and Wood (1982)
described Ips japonicus as synonym of I. typographus. Phylogenetic relationship of
I. typographus f. japonicus and I. typographus populations helped to define their
taxonomy. The European haplotypes and the Asian haplotypes formed monophyletic
clusters, indicating that these two forms are geographically isolated (Stauffer et al.,
unpubl. data).
2.2. Genus Tomicus

The genus Tomicus contains six species within Europe and Asia which infest pine
species. T. piniperda and T. minorr are Eurasian species, T. destruens occurs in the
Mediterranean area, and T. brevipilosus, T. puellus and T. pilifer are found in Asia.
The pine shoot beetle T. piniperda and its sibling species T. destruens were often
synonymised in the past (e.g. Schedl 1932). Recent phylogenetic analyses based on
the mitochondrial and nuclear genes, revealed two distinct species supported by
many characters (Gallego & Galián 2001, Kerdelhué et al. 2002, Kohlmayr et al.
2002) These results confirm the classification of Pfeffer (1994) and Wood & Bright
(1992). On the other hand, both mitochondrial and nuclear markers showed that a
GENETIC TOOLS IN SCOLYTID RESEARCH 57
new species of Tomicus, morphologically undistinguishable from T. piniperda,

occurs in Yunnan Province, China, causing heavy tree damages on Pinus
yunnanensis (Duan et al. unpublished data)
3 ECOLOGICAL GENETICS OF SCOLYTIDS

Adaptations and differentiation of wild populations in relation to their environment
as explained by the genetics is the subject of Ecological Genetics. This research
field often includes experimental ecology of natural populations through a
combination of field and laboratory work. Behavioural and eco-physiological
characteristics such as aggression, dormancy reaction, pheromone response, vary
geographically and are often associated with the genetic structure of a population or
individual. The understanding of such characters is important for long-term
biological pest control programs.
3.1. Pityogenes chalcographus

Intra-specific investigations show that P. chalcographus form races within Europe.
Antennal size and spine morphology of the elytral declivity revealed significant
differences between Northeast and Central t European populations (Führer 1978).
Allopatric females were partly rejected by males, in mating experiments which
simultaneously presented sympatric and allopatric females (Sturies & Führer 1979).
Post-zygotic incompatibilities were observed for the few instants of fertilisation
(Führer 1976, 1977). Mating among Scandinavian, Polish and Alpine races resulted
in different degrees of inter-population heterosis (Führer & Klipstein 1980).
Analysing the sperm polyploidy inter-popular hybrids showed increased polyploid
sperm (Führer 1980). Allozyme electrophoreses revealed significant differences
among populations reared at the institute (Ritzengruber 1990), however, no
significant conclusion could be given regarding the race formation.
3.2. Ips typographus

The European spruce bark beetle (Ips typographus) populations are reported to show
variation in their reaction towards synthetic pheromone traps and vary in their
epidemiological behaviour. In order to quantify the degree of population
differentiation and to estimate the levels of gene flow, European populations were
analysed by sequence analysis (Stauffer et al. 1999). The data of a partial sequence
of the mitochondrial DNA and an enzyme analysis suggested that the population
structure of the European I. typographus has been influenced by events which took
place during and after the last ice age. Populations were forced into refugial areas in
the south and in the area north of Moscow along with the host tree. After
amelioration of temperature, beetles spread perpendicular to the distribution of P.
abies. I. typographus migrated from the south to the north and not from the east
(Moscow) to the west as did the host tree. Whilst there is evidence for high gene
flow among populations, founder effects can still be detected in the North. The
58 C. STAUFFER
distribution of the genotypes in the European populations might explain the

behavioural and epidemiological differences.
Allozymes were used to study the genetic variation of local populations of Ips
typographus during the last two decades (Stauffer et al. 1992, Pavlicek et al. 1997,
Gruppe 1997, Viktorinová 1999). These studies showed that I. typographus
populations had a lack of heterozygotes. Several groups addressed the association of
genetic variation with obligate and facultative diapausing beetles (Perny 1992,
Gasser 2001), pioneer beetles (Stauffer 1994) and pheromone reacting beetles
(Leitinger & Schreiber 1990, Hösle 1999). However, significant results could not be
demonstrated either.
3.3. Ips acuminatus

Ips acuminatus was described to have bisexual and clonal (parthenogenetic) females
(Kirkendaal 1983). Although both forms are morphologically indistinguishable, they
were separated by differences in the mitochondrial DNA. A restriction enzyme
facilitates the distinction (Kirkendaal personal communication).
3.4. Tomcus piniperda

Besides P. sylvestris, 16 other pine species and Picea spp. (Wood & Bright 1992,
Pfeffer 1994) are recorded as host trees of T. piniperda. Host association can be an
important factor in speciation. There was little indication that host choice affects the
genetic structure of T. piniperda (Kerdelhué et al. 2002). The phylogeographic
analysis of European, Chinese and American populations revealed 25 haplotypes
that are being analysed using a nested clade analysis (Ritzerow et al., 2003). The
Central & Northern European, American populations had most of the haplotypes in
common whereas the Iberian populations had haplotypes not found in Central
Europe. The postglacial history of Pinus sylvestris suggests that the Pyrenees were
likely a major barrier for gene flow and thus also for the insect. The Northern
Chinese populations had also haplotypes which were not found in Europe - the
sequence divergence was quite low with 1,5%. A high mitochondrial sequence
divergence (4,2%) between European and Asian T. minorr was detected, but
interestingly they apparently revealed almost no divergence on nuclear sequences
(Duan et al. unpublished data).
4. PERSPECTIVES
In phylogeographic questions it will be important to develop faster evolving markers
in order to be able to analyse questions from the most recent past and regarding
quarantine control. A method that has been applied in many plant and animal species
during the last decade is the use of microsatellites. Much effort has been dedicated
to isolate microsatellite primers for coleopteran species, however, only few
polymorphic loci have been characterised, yet, compared to other insect orders.
Microsatellite loci have been reported from chrysomelids (Batley et al. 1998),
carabids (Keller & Largadièr 2001), and also recently for scolytids (Kerdelhué et al.
2003, Berg et al. 2003, Sallé et al. 2003). In latter isolations, the five loci from T.
piniperda showed cross-species amplification to three other Tomicus species
(Kerdelhué et al. 2003), five loci were isolated from Ips typographus (Sallé et al.
2003) and 14 loci from Coccotrypes carpophagus (Berg et al. 2003) were scored. In
Ips typographus further reports on four microsatellite loci from Pavlová (2000) and
three loci isolated by Stauffer (1998) were described.
It will be important to isolate also other
t nuclear markers like in the non-coding
regions that so far seem to have more variable
a sites. Viktorinová (2001) partially
isolated the α-amylase gene. The intron-exon structure was used for exon-primed
intron-crossing (EPIC) PCR. This method was subsequently used for population
structure analysis.
5. REFERENCES
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Chapter 7
GENERAL BIOLOGY OF BARK BEETLES
D. SAUVARD
Institut National de la Recherche Agronomique, avenue de la Pomme de Pin,

B.P. 20619, Ardon, F-45166 Olivet Cedex, France
1. INTRODUCTION
Bark and ambrosia beetles are a small group of insects from the huge Coleoptera
family Curculionidae (they were formerly separated in the families Scolytidae and
Platypodidae). They are small endophytic beetles, living inside plant tissues during
their whole life except short periods of their imaginal stage. The bark beetles
generally live inside and consume phloem, a thin but nutritious tissue between outer
bark and wood, while ambrosia beetles live inside wood and feed on symbiotic
fungi. This group includes some of the most injurious insects for trees, especially
the tree-killing bark beetles, so-called because the death off their host tree is normally
necessary to the success of their reproduction (Grégoire and Evans, chapter 4). Bark
and ambrosia beetles are particularly damaging for conifers. It is the most important
group of the European BAWBILT, including alone half of the recorded species.
Most of them are bark beetles, so this term will be used in the following to refer to
all bark and ambrosia beetles.
Considering their economic importance, bark beetles have been the subject of
many studies since the beginning of forest entomology (Ratzeburg 1839; Escherich
1923; Schwenke 1974), and a large part of them is concerned with their general
biology. These studies mainly deal with species considered as the most injurious.
Forty-seven BAWBILT bark beetle species are recorded in Europe, but one fifth of
the related studies deals with Ips typographus, half of them deals with only six
species (I(I. typographus, Dendroctonus micans, the species complex Tomicus
piniperda / T.T destruens, Pityogenes chalcographus and Trypodendron lineatum)
and three quarters deals with only twelve species (the previous ones plus Scolytus
scolytus, Ips sexdentatus, S. multistriatus, I. I amitinus, Tomicus minorr and I. I
acuminatus). On the other hand, very few studies deal with the biology of half of
the European BAWBILT bark beetles. Consequently, knowledge about bark beetle
biology varies greatly according to species. The main traits are generally known for
63
63–88.
© 2007 Springer.
64 D. SAUVARD
all of them, but details only for a few. So it is often necessary to extrapolate from
the well-known European species or from closely related species living in other part
of the world, mainly in North America where similar species exist.
The majority of European bark beetle species does not belong to BAWBILT.
They generally lives on dead trees or branches. Their biology, often poorly known,
appears similar to BAWBILT species, but their particular features will not be taken
into account in this paper. Research about bark beetles is a world process, and
similar studies have often been performed in different parts of the world. However,
this review is centred on European studies, so non-European results will be cited
only if they differ from European ones or if there is no European equivalent.
2. LIFE CYCLE
2.1. Standard bark beetle life cycle and particularities

Life cycle description has been the main subject of a large part of the publications
about bark beetles since the beginning of forest entomology. Their main features are
well known and consistent, at least for the most important species (Chararas 1962),
allowing a synthetic description of the life cycles.
A bark beetle life cycle is organised att each generation around a basic cycle with
three phases: reproduction, development, maturation and dispersal (Fig. 1). Each of
these phases could present different characteristics, leading to a rather large
variability of life cycles among these species. Furthermore, the basic cycle could be
repeated one or several times a year and interrupted by overwintering.
Maturation & Dispersal
Development Reproduction
Figure 1. Basic bark beetle life cycle. Hatching density indicates the proportion of each phase
which is endophytic.
2.1.1. Reproduction phase

The reproduction phase begins when mature insects arrive on their host tree. The
choice of this tree is discussed elsewhere in this book (Byers, chapter 8; Lieutier,
chapter 9). Most species are aggregative, a large number of adults arriving on the
host tree in few hours or days. This behaviour helps meetings between males and
females. It is generally controlled by y pheromones and more rarely by primary
attractants. In some species, such as Dendroctonus micans, each insect attacks the
host tree alone. The tree choice mechanism is poorly known in this case.
GENERAL BIOLOGY OF BARK BEETLES 65
Mating generally occurs on the host tree. In polygamous species ((Ips,

Pityogenes), the male arrives first and bores an entrance hole and a mating chamber
in the phloem where it waits for females. The sex ratio during reproduction varies
from 1 to 4 or more females per male depending on species and local conditions
(Kirkendall 1983). On the other hand in monogamous species (Scolytus,
Trypodendron, Tomicus) the female arrives first and bores the entrance hole and the
beginning of a gallery where the male joins it. Platypus, whose males initiate
galleries, is a notable exception (Kirkendall 1983). The sex ratio during
reproduction is equilibrated in these species.
The mating behaviour have been described in several species (Chararas 1962;
Paynter et al. 1990). Males and females recognise themselves using a combination
of semiochemical and sonic stimuli, but this sequence have been mainly described in
north American species (Rudinsky and Ryker 1977). Mating takes place on the bark
or in the mating chamber, if it exists.
In some species like Xyleborus disparr or Dendroctonus micans males are not
found during the reproduction phase. Mating takes place during maturation and
dispersal phase (see below) and females alone bore the gallery.
After mating, if it occurs, the female (each of them in polygamous species) bores
a breeding gallery. The male could help to clear away frass, but it does not take part
in gallery boring. The pattern of this gallery is species specific. In phleophagous
species it could be longitudinal (Tomicus piniperda, Scolytus scolytus), transverse
(Tomicus minor, Leperesinus varius), radiating from the mating chamber ((Ips
typographus, Pityophthorus pityographus), circular (Cryphalus piceae), or irregular
(
(Dendroctonus micans) (Fig. 2). Eggs are generally laid in the sides of the gallery,
each in a small hole, but D. micans just lays an egg heap in the gallery. In
xylomycetophagous species (Trypodendron, Xyleborus) the gallery drives straight in
the wood where it is more or less branched. Egg heaps are laid in the branches.
Figure 2. Examples of bark beetle gallery systems. Maternal galleries are in grey. A: Scolytus
scolytus. B: Leperesinus varius. C: Ips typographus. D: Pityophthorus pityographus. E:
Cryphalus piceae. From Balachowsky 1949, modified.
2.1.2. Development phase

66 D. SAUVARD
The development phase is entirely endophytic. Larvae and pupae are unable to
survive outside of the host tree. Post-embryonic development is similar in all
species, with 3 to 5 larval stages and pupa, but larval behaviour varies, mainly
between phloeophagous and xylomycetophagous species.
Larvae of phloeophagous species feed on phloem, generally boring individual
galleries more or less perpendicular to the maternal gallery, together constituting a
gallery system. The pattern of larval galleries is species specific but less variable
than maternal ones (Fig. 2). The larvae moult in their gallery. Pupation takes place
(I. sexdentatus) or
in little individual chambers bored by the old larvae in the phloem (I
in outer bark (T.T piniperda). Some species have particular characteristics, such as T.
T
minorr whose old larvae feed on fungi which have invaded phloem (Långström
1983b). D. micans larvae have a very specific behaviour. They are gregarious,
boring collectively from the egg chamber bored by the female. The cohesion of the
group of larvae is assured by a specific pheromone (Grégoire et al. 1982; Storer et
al. 1997).
Larvae of xylomycetophagous species remain inside the maternal gallery and
generally do not bore wood. They feed on symbiotic fungi called Ambrosia. The
fungus is inoculated by the female during gallery boring. It invades wood from
where it extracts its nutrients. Larvae eat the mycelium and the fructifications which
develop in the gallery. Pupation takes place in the gallery and young adults are
contaminated by fungus when they move within it.
2.1.3. Maturation and dispersal phase

After the imaginal moult, bark beetles need a period of maturation before being able
to reproduce. It allows the achievement of sclerotisation, the constitution of fully
functional wing muscles and genitals, and the storage of energy reserves. The
imagoes need to undertake a maturation feeding to achieve this maturation (Gries
1986).
In most species like I.
I typographus maturation takes place where development
has taken place. Maturing beetles eatt remaining phloem around the galleries
(phloeophagous species) or symbiotic fungus (xylomycetophagous species). When
mature, adults emerge from the brood material using the maternal entrance hole, any
other hole in the bark, or if necessary by perforating it. They immediately search a
suitable host for reproduction. In these species maturation and dispersal are clearly
separated, and only one flight, named the swarming flight, occurs during the basic
life cycle.
In some species however, maturation does not take place in the brood material
but in the crown of healthy trees. Tomicus species bore axial maturation galleries in
the pine shoots (Långström 1983a; Fig. 3), while S. multistriatus and S. scolytus feed
on elm crown and particularly buds. Furthermore, beetles can change shoot or tree
several times during maturation, especially when the attacked shoot dries out. In
these species maturation and dispersal are then mixed. Their basic cycle presents
two main flights, an emergence flight after emergence and a swarming flight before
reproduction, and some minor flights could occur between them. Maturation
feeding in the crown of healthy trees could weaken them due to shoot destruction or
pathogen inoculation, and could thus predispose these trees to subsequent

reproductive attacks as observed with the Dutch elm disease (Kirisits, chapter 10).
Figure 3. Shoot damage on Scots pine due to maturation feeding of Tomicus piniperda (Photo
F. Lieutier).
Mating could occur during the maturation and dispersal phase. In species
normally mating during their reproduction phase, it has sometimes been observed
that a fraction of adults have mated before the beginning of this phase (Janin and
Lieutier 1988, for T.
T piniperda). But in some species mating normally occurs during
the maturation phase. D. micans and X. X disparr siblings mate in their breeding
material before their emergence. The females then emerge and search for a host tree
for reproduction. The males’ future is poorly known. They seem to die rapidly but
they might also search for other females at least in other broods on the same tree.
2.1.4. Succession of generation and overwintering

Most species go through several successive basic life cycles while climatic
conditions are favourable. They generally have one generation a year in northern
Europe and two in central Europe, sometimes more in southern Europe or during the
warmest years. The Tomicus species differ from the others because they are strictly
monovoltine. T. T destruens is also the only species to reproduce during autumn
instead of spring and summer. D. micans is another exception. It presents about one
generation each 18 months, and individuals are poorly synchronised, so all stages
could be encountered in all seasons, depending on the year (Vouland and Schvester
1994).
68 D. SAUVARD
The succession of basic life cycles is complicated by the existence of one or

several sister broods. During the reproduction phase females which have bored a
maternal gallery could re-emerge and establish
a a new maternal gallery where they
lay new eggs. This new gallery could be bored in the same tree, or in a new one.
Males are not necessary (Sauvard 1993). Females feed in the gallery before re-
emergence to regenerate wing muscles. Females from species maturing in the
crown could also undertake new maturation feeding in this place (Salonen 1973).
The sister broods have often been confused with real generations established by
female offspring, leading to mistakes in determining the number of generations a
year.
Bark beetles overwinter as imagoes during the maturation and dispersal phase.
Larvae seem generally not able to survive during the cold season, except for D.
micans which could overwinter at all stages. Most species overwinter in their
breeding material, waiting for spring to emerge. A part of the beetle population
could also overwinter in specific irregular feeding galleries bored during autumn.
On the other hand, some species have particular overwintering places. I. I
typographus (Biermann 1977; Botterweg 1982; Austarå et al. 1993) and T. T minor
(Bakke 1968) thus partly overwinter in the forest litter around the tree where they
have developed. T.T piniperda beetles have the most complex behaviour. In northern
and central Europe they mainly overwinter in small galleries bored in the bark of a
healthy tree collar (Salonen 1973). In southern Europe they mainly overwinter, as
do T.
T destruens, in the pine shoots where they mature, these shoots being on trees or
fallen on the litter (Salonen 1973). T.T minorr seems to have similar geographic
variation (Fernandez Fernandez and Pajares Alonso 1999).
The longevity of bark beetle imagoes is some months, nearly one year for the
overwintering generations. When they have bred, parent bark beetles usually seem
not able to survive to winter (Austarå and Midtgaard 1986), but some authors have
observed this possibility in experimental conditions (Schroeder and Risberg 1989).
2.2. Life cycle variability and regulation

Bark beetle life cycles could vary according external conditions. Most studies are
related to temperature effects. As poikilotherms, bark beetles are sensitive to
temperature. Its effect on reproduction and development has been extensively
studied (Bakke 1968; Annila 1969; Saaremaa 1985). The development is generally
stopped under 5 to 10°C and its rate increases rapidly up to 25 to 30°C, and then
decreases until lethal temperatures at around 35 to 40°C (Fig. 4). These
temperatures vary according to species, often in accordance with their latitudinal
distribution. Gallery construction and oviposition rate on one hand and pre-
emergence maturation rate on the other hand vary similarly with temperature.
Flight period is also sensitive to temperature. Each species has a temperature
threshold under which flight initiation is inhibited, for example 12°C for T. T
piniperda and 18°C for I. I typographus, and above it flight activity increases with
temperature. Contrary to endophytic process, flight is also clearly dependent on
other external conditions. Bark beetles fly only during the day (Salonen 1973;
Lanne et al. 1987; Byers and Löfqvist 1989). Their flight activity is favoured by
high luminosity (Franklin and Grégoire 1999) and inhibited by rain and strong wind.
Combined with the temperature effect, this explains why bark beetles primarily fly
during sunny days without wind, and in early afternoon (Bakke 1968; Annila 1969;
Salonen 1973).
0.03
(1/median emergence day)
Rate off development
0.00 0.01 0.02
0 5 10 15 20 25 30 35
Temperature (°C)
Figure 4. Influence of temperature on the development rate of Tomicus piniperda. From

Saarenmaa 1985, modified.
Species precocity is mainly determined by the flight temperature threshold, low
values of which allow beetles to fly earlier in the spring. However, maturity of the
overwintering beetles also influences precocity. In some species such as T. T
piniperda the overwintering adults have finished their maturation, so they can
swarm as soon as temperature increases beyond the flight temperature threshold.
This reinforces the effect of the low flight temperature threshold forr T. piniperda, so
that this species is the most precocious European bark beetle. On the other hand,
most species have not finished their maturation at the end of the winter. They must
achieve it before swarming, so this does generally not occur the first time the flight
temperature threshold is reached.
In autumn, bark beetles cease reproduction activity in order to overwinter.
Factors inducing this behaviour have not been frequently studied. When
overwintering occurs in a particular location, the movement from brood material to
this location seems to be induced by the first occurrence of low temperature (Annila
1969 for I.
I typographus; Salonen 1973, Långström 1983a for T. T piniperda). In other
species, inhibition of emergence could similarly be due to low temperature, but
photoperiod seems also to be involved, as for P. chalcographus. In this species
short photoperiods inhibit emergence, but high temperatures suppress this effect
(Führer and Chen 1979).
Temperature effects largely control bark beetle life cycles, especially the number
of generations a year. High temperature allows fast oviposition, development and
70 D. SAUVARD
maturation, thus a short generation time, as well as earlier swarming in the spring.
A larger number of generations could thus be completed during a favourable season.
This explains why most bark beetle species complete one generation a year in the
northern part of their distribution area and two or more in its southern part. This
could also partly determine the geographic distribution of some bark beetles. The
low frequency of I.
I sexdentatus and I.I acuminatus in southern Scandinavia could be
explained by temperature conditions that allow the beginning of a second generation
which cannot be achieved before the winter, leading to dramatic mortality (Bakke
1968).
The Tomicus species are exceptions. T. T piniperda and T. T minorr are always
monovoltine, while, if they can achieve one generation a year near to the polar
circle, temperature conditions in southern Europe are certainly sufficient for at least
a second generation. There is then certainly a factor inhibiting reproduction of
young imagoes in the summer. Photoperiod orr the necessity of low temperature to
achieve maturation could be involved in this regulation but this aspect has not been
studied. Similarly, the factor inducing T. T destruens reproduction in the autumn
remains unknown.
Synchronisation of bark beetle individuals is important for their reproduction,
especially for aggregative species for which only simultaneous attack of a large
number of insects could be successful. The temperature effect on reproduction and
development could not allow this synchronisation because temperature greatly
varies between beetle location (exposure, shade, position on the tree). Cold winter
temperatures are certainly an important factor. They destroy the developing broods,
thus eliminating the most divergent individuals. This effect is, however, less
effective in southern Europe or on species such as D. micans which could
overwinter as larvae. Moreover, its cost for species is high, so most species have
probably developed other regulation systems to avoid the possibility that some hot
days in autumn will lead to dramatic mortality. Cold winter temperatures are
probably also the main synchronising factor in northern and central Europe for
species such as T. T piniperda for which all individuals are mature during
overwintering and wait in quiescence for the first fair days to swarm. However, they
could hardly explain synchronisation of individuals in southern Europe or in species
which achieve maturation during spring. These different factors could thus partly
explain individual synchronisation, each factor being more or less important
depending on species, but they cannot explain all observations. There is probably
another mechanism to synchronise swarming, but this aspect has not really been
studied.
2.3. Concluding remark

Many studies have been done on European bark beetle life cycles, but the choice of
their focus is unbalanced. A lot of them are descriptions of the cycle in a particular
region, especially swarming dates. If these results are useful for pest management,
as in further research, they give few insights into cycle regulation and are hardly
transferable to other regions. Progress in the comprehension of life cycles of the
most common species needs detailed studies on the effects of the different factors,
including temperature but also other factors such as photoperiod, and their
interactions. This could lead to models applicable in large areas of Europe.
3. DISTRIBUTION AND HOST RANGE
3.1. Distribution
The distribution of bark beetles could be described at three levels: within a tree,
within a forest or forest region, and within a continent. The biogeography of bark
beetles is discussed elsewhere in this book (Knížek and Beaver, chapter 5; Stauffer,
chapter 6). Within-tree and within-forest distributions present completely different
patterns.
Tomicus pin
T i iper
i rd a I sexdentatus
Ips
Tomicus minor Ips acuminatus
Density of galleries
ness (mm)
Bark thick-
20 10
distribution of bark beetle galleries on pine

stems, in relation to bark thickness. From Bakke 1968, modified.
The main features of within-tree distribution have been known for a long time,
but in contrast to the north American situation, this has only been extensively
studied in a few species, especially T.
T piniperda. Most species attack the bole or
main branches. Attack distribution is organised around the gradient from the base to
the top of the bole (Fig. 5). Attack density is maximal near the bole base, regularly
decreasing towards its top, and becoming negligible above a certain height (Bakke
1968; Nilssen 1978; Saarenmaa 1983; Bouhot et al. 1988). This distribution is
correlated with the bark thickness (Saarenmaa 1983), but other possible factors have
been poorly studied. When boles are laid on the ground, beetle distribution also
varies between the upper and lower side, probably according to beetle thermal
preference (Bouhot et al. 1988). Inside a tree section, attack distribution is regular
(Nilssen 1978; Schlyter and Löfqvist 1990), which is interpreted as resulting from
beetle optimal spacing behaviour (De Jong and Sabelis 1988). This distribution
could however vary among trees. It could particularly be disturbed by bole crossing,
72 D. SAUVARD
inter-specific competition or irregular sunlight (Bouhot et al. 1988; Jakuš 1998). It

also become irregular, with attacked patches, when attack density is low. Attack
distribution could be constant (T.T piniperda) or change ((II. sexdentatus) during the
attack sequence (Bouhot et al. 1988). The latter seems to be related to the existence
of aggregation and anti-aggregation pheromones. Aggregation pheromone first
concentrates attacks on one part of the tree and then, when critical density is
reached, anti-aggregation pheromone shifts them to other parts of the tree.
Some species such as I. I acuminatus or P. chalcographus attack the upper part of
the bole and the branches (Fig. 5). Some data is available on their distribution in the
bole (Bakke 1968), but their distribution in the branches seems have not to have
been studied, perhaps because this part off the tree is more irregular than bole.
Within-tree distribution has also been studied during the maturation phase, when
it occurs in the tree crown. The beetles use the whole crown but generally prefer its
upper part (Riedl 1973, for S. multistriatus; Lånsgtröm 1980, 1983a for T. T
piniperda).
In contrast to within-tree distribution, within-forest distribution of bark beetles is
highly aggregative. All beetles are concentrated in a small number of trees, isolated
or in small patches, or in another scattered sites such as logs or logging residues, all
of them changing at each beetle generation. Such a distribution is difficult and
expensive to describe, and has rarely been studied. Some data however exist on the
distribution of I.
I typographus during outbreaks in central Europe (Jakuš et al. 2003).
Gilbert (2001) also demonstrated that trees attacked by the solitary species D.
micans are randomly distributed in a forest plot, and beetles frequently attack the
same trees during several years.
The distribution of beetles which mature in the crown is a very special case. It is
rather continuous and thus much easier to study. It has been demonstrated that T. T
piniperda is distributed with decreasing density in a circle about 1 kilometre around
its main reproduction sites (Sauvard et al. 1987; Långström and Hellqvist 1990).
To get round the difficulty of within-forest bark beetle distribution, some studies
have analysed this distribution at a larger scale. These recent studies, based on
spatial analyses, allowed the determination of different site characteristics, such as
tree age and density, altitude and slope, and forest structure, which are correlated to
bark beetle density (Gilbert 2001; Jakuš et al. 2003; Netherer 2003).
3.2. Host range

European bark beetle host range has been known for a long time (Balachowsky
1949; Chararas 1962). Most phloeophagous species are normally specific to one
tree genus ((II. typographus, D. micans and P. chalcographus on Picea, I.I acuminatus
and Tomicus species on Pinus, S. multistriatus and S. scolytus on Ulmus…). Only
some species attack trees from closely related genus, such as Phloeosinus bicolorr on
different Cupressaceae (Cupressus, Juniperus). Besides their usual hosts, they have
adaptation capabilities. Mostt of them have been accidentally observed and can
develop experimentally (Chararas 1973; Wainhouse and Beech-Garwood 1994) on a
rather wide variety of hosts. Their specificity is thus probably more related to beetle
choice behaviour, determined by the semiochemical content of the host (Byers,

chapter 8), than to developmental constraints. Adaptation capabilities of these bark
beetles allow them to attack different exotic trees, especially congeners of their
usual host (Sitka spruce, exotic pines, exotic Cupressaceae such as Thuja for P.
bicolor). They could allow southern species to attack new hosts in the north of their
current geographic distribution following global climatic change.
Phloeomycetophagous species are more polyphagous, generally attacking
different broadleaves (Trypodendron domesticum) or different conifers (T. T
lineatum). Xyleborus disparr is extremely polyphagous, attacking a wide range of
broadleaves, including forest trees and fruit trees. This polyphagy could be due to
their mycetophagy which reduces direct interactions between the insects and their
hosts.
Bark beetle preference between different hosts has been poorly studied in Europe
(Walker and Ross, 1975; Chararas et al. 1982; Lieutier et al. 1997). A possible
reason is the low species richness of this continent where, in many regions, each of
the main bark beetle species has only one natural usual host (such as Norway spruce
for I.
I typographus and Scots pine for I.I sexdentatus and T.
T piniperda in central and
northern Europe). Knowledge about this preference would be useful in forest
management, especially in multispecies pine forests in southern Europe. This need
will probably increase with increasing area of non indigenous tree species in many
European regions, and future change of insect and tree distribution following global
climatic changes. Very few data is available on intraspecific variations of bark
beetle preference.
4. DISPERSAL
Dispersal is an essential element of bark beetle biology. Except during outbreaks,
bark beetles are generally unable to reproduce on healthy trees (Lieutier, chapter 9),
and their reproduction usually entirely destroys the host tree, which is thus not
available for their offspring. At each generation, they must then find rare suitable
trees existing in the forest. As these trees are likely to be randomly distributed and
their distribution widely changes from year to year, their location is generally
unpredictable for the insects. Bark beetles have thus developed elaborate
mechanisms to find their hosts, mainly based on use of semiochemicals and in most
species on aggregation behaviour (D.L. Wood 1982). These mechanisms are
discussed elsewhere in this book (Byers, chapter 8). The importance of bark beetle
dispersal in their biology and in outbreak development has lead to several studies to
estimate dispersal capacity in the laboratory
r and effective dispersal in the field.
Flight capacities have been studied in the laboratory for some species, using
flight mills (Forsse 1989 and included review; Jactel 1993). The beetles are tethered
on an arm which can freely turn round an axis. This method is well adapted to bark
beetles (Forsse 1989). It places them in very artificial conditions, but allows the
determination of maximum flight capabilities and their distribution in beetle
populations.
74 D. SAUVARD
These studies show that bark beetles have high flight capabilities with wide
individual variations. Some individuals, 10 to 30%, seem unable to fly. This result
could however partly be an artefact because beetles are generally tested only once,
and beetles tested several times could fly on one day but not on an other (Forsse and
Solbreck 1985). On the other hand, numerous beetles are able to fly for one or
several hours: a quarter of I.
I sexdentatus or I.
I typographus individuals fly for more
than an hour, and up to four to six hours (Forsse and Solbreck 1985; Jactel 1993),
and repeat this flight over several successive days (Forsse 1989). Excluding short
flight (less then one minute), the distribution of flight capabilities among individuals
is log-normal (Fig. 6). Flight speed is between 1 and 2 ms-1, so a notable proportion
of bark beetles populations can actively fly tens of kilometres.
20
Percent off population
10
0
0 10 100 1000 10000
Flight time (s)
Figure 6. Distribution of flight duration of Ips typographus individuals (N=76). From Forsse
and Solbreck 1985, modified.
Bark beetle effective dispersal in the forest is difficult to determine. It is
impossible to follow them during their flight due to their small size and high speed,
so this aspect has been studied using indirect methods. Most data are provided by
mark-recapture experiments and capture of beetles outside their normal location.
These methods give information on effective dispersal distance of the captured
beetles, but no information about their flight behaviour. Mark-recapture
experiments also give information about the distribution of effective dispersal inside
the released population, but this must be carefully interpreted because only a small
fraction of beetles is recaptured.
Mark recapture studies show that bark beetles can fly from a few meters to at
least 1 to 4 kilometres (Botterweg 1982; Jactel 1991; Zumr 1992; Zolubas and Byers
1995; Duelli et al. 1997). The duration of flight is generally short: more than 80%
of released I.I sexdentatus are recaptured the same day (Jactel 1991). Longer
dispersal is indicated by captures of bark beetles outside their normal location.
Nilssen (1984) thus observed I. I typographus more than 40 kilometres from the
nearest forest, and some smaller bark beetles up to 150 kilometres from it. In that
case the beetles have probably been partly carried by wind. Other data on effective
dispersal is given by the invasion of Finland by I. I amitinus (Koponen 1980). The
expansion of this species has been estimated to cover about 20 km a year, indicating
that a large part of its population disperses to a distance of the same order.
In species with two flights such as T. T piniperda, the emergence flight also
contributes to dispersal. In this species, beetles seem to disperse about 1 kilometre
around their brood trees during this flight (Sauvard et al. 1987).
Effective dispersal depends on availability of suitable host trees, but also on
receptivity of the beetles to external stimuli. Most beetles are not receptive to tree or
congener attractiveness at the beginning of their flight, and this receptivity increases
during the flight. Such an increase is also observed with starvation, indicating it is
probably due to decreasing energy reserves (Sanders 1983; Gries 1985; Jactel 1991).
Interactions between flight and semiochemicals are discussed elsewhere in this book
(Byers, chapter 8). High receptivity of re-emergent beetles to host stimuli seems to
explain their low-range field dispersal (Anderbrandt 1985; Zolubas and Byers 1995)
Both laboratory and field experiments agree with high dispersal capabilities of
all bark beetle species, over at least several kilometres. Flight duration is similar
among populations from different locations and with different outbreak status
(Forsse 1991), and the variability is mainly observed inside populations. Factors
determining individual flight capabilities are unclear. Sex and size are not
correlated with them (Botterweg 1982; Forsse and Solbreck 1985; Jactel 1993). The
relation between fat content and flight duration is doubtful. Long flyers have higher
fat content (Jactel 1993) and fat content decreases during dispersal (Botterweg 1982,
Gries 1985), indicating that lipids are consumed as a result. However, the relation
between individual fat content and flight duration is not significant (Botterweg
1982; Forsse and Solbreck 1985; Jactel 1993). Nematode parasitism also seems to
have little influence on flight duration (Forsse 1987). It is possible that flight
capabilities are mainly genetically determined.
Bark beetle behaviour during dispersal is poorly known. Some experiments
indicate that they generally fly at low altitude, between 2 and 10 metres (Forsse and
Solbreck 1985; Duelli et al. 1986). However, 5 to 15% of beetles fly above 20m,
i.e. above the canopy, and could then been carried at long distance by wind. In the
absence of host stimuli, flight direction seems mainly influenced by wind, most
beetles flying with the wind (Helland et al. 1984; Jactel 1991). In contrast, they fly
against the wind to locate a pheromone source. Flight direction is also influenced by
light, the beetles preferring areas with high luminosity (Lobinger and Skatulla
1996).
5. REPRODUCTION
5.1. Reproduction mode

Bark beetle reproduction is usually classical sexual reproduction. Birth sex ratio is
generally equilibrated in most phloeophagous species, even in polygamous ones
such as I.
I typographus (Annila 1971). Sex ratio of these polygamous species shifts
76 D. SAUVARD
in favour of females after emergence, perhaps due to higher male mortality but this
point remains unclear. On the other hand, birth sex ratio is highly biased in some
species such as D. micans and most of the xylomycetophagous species ((Xyleborus,
Xylosandrus, but not Trypodendron), with 1 male for 5 females or more. This
unbalanced sex ratio is often associated with high sexual dimorphism with small and
generally flightless males. Female excess is balanced by high rates of polygyny.
The sex ratio control mechanism is unknown.
Parthenogenesis has been observed in some species, especially I. acuminatus
(Kirkendall 1990). Its populations contain a highly variable proportion of
pseudogamous females (from about 0 to more than 90%), resulting in a biased sex-
ratio. These females are triploid. Their reproduction is clonal but needs mating.
Reproductive incompatibility between allopatric populations has been observed
in P. chalcographus (Führer 1977). This phenomenon seems related to the existence
of sperm polyploidy (Klipstein 1986).
5.2. Reproductive success

Due to its importance in population dynamics, bark beetle reproductive success has
been studied intensively. It can be described by two parameters, beetle productivity
and offspring quality. Beetle productivity is the number of emerging beetles per
parent female. It results from female fecundity and brood survival. Bark beetle
fecundity is generally high, about several tens of eggs per female gallery. Brood
survival depends on natural enemies and host resistance (These aspects are
discussed by Kenis et al., chapter 11, Wegensteiner, chapter 12, and Lieutier,
chapter 9), but generally it is mainly dependent on intraspecific competition, except
in solitary species. Offspring quality is a synthetic parameter indicating the ability
of the new generation of beetles to survive and reproduce (Wellington 1977; Sahota
and Thomson 1979). It also depends on intraspecific competition.
The importance of intraspecific competition in bark beetle reproductive success
results from their biology. Most of them are aggregative, a large number of attacks
being necessary to their success on a living tree (Lieutier, chapter 9). The negative
consequence of this strategy is the increase of intraspecific competition. In
polygamous species, it also increases due to within-harem competition (Kirkendall
1989). Bark beetles have developed different adaptations to limit this competition.
In most species an anti-aggregation process stops aggregation as soon as a sufficient
attack density is reached (Byers, chapter 8). The effect of density is also reduced by
the optimisation of spacing between gallery systems (see 3.1). Finally, increasing
attack density induces an earlier re-emergence of the females and thus reduces their
fecundity (Thalenhorst 1958; Ogibin 1973; Anderbrandt et al. 1985; Sauvard 1989)
(Fig. 7). These adaptations are, however, unable to avoid an increase of larval
density when attack density increases (Anderbrandt et al. 1985; Jactel and Lieutier
1987; Sauvard 1989), resulting in increasing larval mortality by starvation and
perhaps cannibalism, even if larvae seem m able to avoid each other (De Jong and
Saarenmaa 1985; De Jong and Grijpma 1986). Globally, when attack density
increases, the beetle productivity continuously decreases. The offspring number per
bark unit area first rapidly increases with egg number, then stabilises at an optimum
and finally decreases due to dramatic larval mortality (Saarenmaa 1983; Sauvard
1989). Observed attack densities in the field often correspond to the optimum. At
high density the population multiplication rate could decrease below the threshold of
population replacement (Thalenhorst 1958; Anderbrandt et al. 1985).
Fecundity (/female
f ) Emerging beetles (/m²)
Total fecundity (/m²) Multiplication rate
100
Percentage off the maximum
50
0
12.5 25 50 100 200 400 800 1600
Attack density (females/m²)
Figure 7. Influence of intraspecific competition on reproductive success of Tomicus

piniperda. From data from Sauvard 1989.
Intraspecific competition also has a negative effect on offspring quality
(Anderbrandt and Schlyter 1989). Increasing attack density results in decreasing
beetle size, weight and fat content (Thalenhorst 1958; Botterweg 1983; Saarenmaa
1983; Anderbrandt et al. 1985). Moreover, small size and low fat content are
correlated with low pheromone production (Birgersson et al. 1988) and low survival
(Anderbrandt 1988), while, as indicated above, their effect on dispersal potential
remains unclear. Finally, high attack density reduces the offspring reproductive
success of I.
I typographus (Anderbrandt et al. 1985), but species with maturation
outside of breeding sites, such as T.
T piniperda, could escape this effect (Sauvard
1989).
Determination of bark beetle reproductive success must take into account the
existence of sister broods, but this aspect has been rarely studied. Sister brood
fecundity and reproductive success are similar to those of first broods, and are not
related to first brood conditions (Anderbrandt and Löfqvist 1988; Sauvard 1993).
As high attack density induces early re-emergence, it allows females to devote less
time to their first brood when this takes place under high competition, and thus to
78 D. SAUVARD
optimise distribution of their eggs among different sites (Anderbrandt 1988b). Early
re-emergence could also allow females to produce more successive broods. From
this point of view, sister broods could also be considered as a mechanism for
reducing negative effects of intraspecific competition.
Many abiotic factors have been recorded as influencing bark beetle reproductive
success, especially larval mortality: drought (Salonen 1973; Lieutier 1975),
development temperature and high temperature reached under sunny bark (Annila
1969), rain and phloem decay (Sauvard 1989). However, their effects are poorly
documented.
6. OVERWINTERING
Overwintering is a critical phase for insects in a temperate climate such as in
Europe. Winter cold temperatures decrease or eliminate bark beetle feeding and
dispersal capabilities, but the main risk is freezing. Bark beetles are not tolerant to
freezing which kills them. They have thus developed behavioural and physiological
adaptations to survive during winter.
Behavioural adaptations aim at avoiding the coldest temperatures. Most species
overwinter in their breeding site where bark allows limited protection. Species with
specific overwintering sites are much more protected. They overwinter in the litter
or in the tree collar where temperature is much higher than in the air above,
especially when snow, a good insulator, covers the ground (Bakke 1968). Snow
could also protect beetles in logs or felled trees (Wermelinger 2000). Migration to
the overwintering sites seems to be induced by the first occurrence of low
temperature in the autumn (see 2.2). This allows these species to adapt their
overwintering site to local temperature: breeding or maturation sites in southern
Europe, litter and tree collar in northern Europe.
As a physiological adaptation, bark beetles have developed supercooling
capabilities, being able to tolerate negative temperature up to –15 to –30°C without
freezing (Bakke 1968; Annila 1969). The cold-hardiness varies according to stage
and season. It is generally low for larvae, medium for newly emerged imagoes and
maximal in hibernating imagoes. It results from a physiological process during
autumn. The beetles stop feeding, eliminate gut content, reduce their water content
and accumulate in their haemolymph various supercooling substances such as
trehalose, glycerol, ethylene glycol or antifreeze proteins (Barson 1974; Gehrken
1984, 1989, 1992, 1995; Hansen and Sømme 1994; Netherer 2003). Supercooling is
dramatically reduced in the presence off water (Gehrken 1992), so optimal cold-
hardiness needs a proper overwintering site.
Overwintering survival of bark beetles results of the combination of both
behavioural and physiological adaptations, which varyy according to species. In
northern countries, some species such as T. T piniperda survive with a rather high
supercooling point (–18°C) owing to well-insulated overwintering sites (tree collar),
while other species such as I.I acuminatus overwinter in branches directly exposed to
low temperature but have a low supercooling point (–33°C) (Bakke 1968).
7. ANATOMY AND PHYSIOLOGY

Bark beetle anatomy has been described for a long time (Balachowsky 1949;
Chararas 1962), and rarely studied recently. It is similar to other coleopteran
insects. Bark beetle physiology has also rarely been studied. Their small size, the
difficulty of rearing them outside logs where they are poorly accessible, and the poor
expected utility for forest managementt prevent such study. Among the more
important physiological functions, only nutrition and reproduction seem to have
been studied.
Bark beetles are able to digest a large variety of carbohydrates, including soluble
ones, starch and some hemicelluloses, but not cellulose (Chararas 1983). Their
digestion is helped by some micro-organisms such as yeasts which complement the
insect enzymatic set and provide it with vitamins (Pignal et al. 1988). Precise
nutrition requirements are unknown.
Reproductive physiology is characterised by maturation cycles, especially in
females (Zumr and Soldán 1981; Långström m 1983). Gonadial maturation begins
during the maturation and dispersal phase butt it is not completed before arrival in
the breeding site. There, flight muscles and fat body regress while ovarioles develop
(Lieutier 1982). The opposite process occurs at the end of oviposition, before
female re-emergence. This cycle corresponds to nutrient transfer between flight
muscles, fat body and ovarioles (Lieutier 1983). It is repeated for each sister brood.
Besides maturation cycles, bark beetles present seasonal variations of the
concentration of different compounds, mainly energetic compounds such as fat or
glycogen which are stored during autumn as supercooling compounds and used
during winter (Botterweg 1982; Zumr et al. 1985; Krauße-Opatz et al. 1995). Some
bark beetles also exhibit low oxygen consumption during autumn and the beginning
of winter indicating a diapause (Gehrken 1985, with I. I acuminatus; Netherer 2003,
with I.
I typographus). The physiological control of these cycles is poorly known.
Sensorial organs and physiology, especially olfaction, and pheromone
biosynthesis have been well studied in relation to host localisation process. Results
are discussed elsewhere in this book (Byers, chapter 8).
8. POPULATION DYNAMICS AND OUTBREAK DETERMINATION

Population dynamics aims to describe and explain changes in population levels of a
species. To succeed, it has to synthesise all traits of the species biology and to
determine what are the key factors which explain these changes.
Most bark beetle species share many characters of their biology and population
dynamics. They are aggregative beetles which irregularly present important
outbreaks, classified as pulse eruptive (Thalenhorst 1958; Berryman 1987).
Outbreaks generally extend from 5 to 7 years during which time many trees are
killed (Bombosh 1954; Schroeder and Lindelöw 2002; Jakuš et al. 2003; Fig. 8).
When beetles are installed on a tree, their reproductive success is mainly regulated
by intraspecific competition, so offspring population level is determined by tree bark
surface, and at a population level by the abundance
a of trees which are susceptible to
be successfully attacked. This abundance is itself determined by the equilibrium
80 D. SAUVARD
between population level and tree resistance, which is the key factor in bark beetle
population dynamics. Each tree is able to contain beetle attacks up to an attack
density threshold above which the tree dies, allowing beetle reproduction (Lieutier,
chapter 9). This threshold depends on genetic and physiological factors.
10
Tree mortality (m /ha)
3
0
1991 1992 1993 1994 1995 1996 1997 1998 1999 2000
Year
Figure 8. Intensity of Ips typographus outbreaks in the Slovak Tatra Mountains in 1991-2000.
From Jakuš et al. 2003, modified.
In endemic conditions, bark beetles are not numerous enough to kill healthy
trees, so they reproduce on felled or dying ones and logging residues. These sites
are too rare to allow population increase. An outbreak happens when a perturbation
raises beetle population level and/or lowers tree resistance (Berryman 1982). This
allows beetles to attack living trees and thus provides them a large amount of
susceptible trees, inducing a positive feedback where population increase allows
increase of available hosts, and then new population increase. This feedback
induces a rapid increase of population level and a spread of the outbreak to
neighbouring areas.
The event inducing an outbreak is generally a climatic accident, mostly storm but
also fire, snow-break or severe drought, which provide breeding material to initiate
beetle population increase. However, an outbreak generally develops only if there
are helping factors reducing tree resistance, such as presence of old trees, storm-
induced root damage, drought, defoliation or any other stress. An outbreak is also
favoured by climatic conditions favourable to insect development such as high
temperature.
Outbreak spreading has been mainly studied in central Europe, on I. typographus
(Jakuš et al. 2003). During the progradation phase the outbreak mainly spreads by
initiation of new attacked tree spots. These spots generally appear within some
hundreds meters of an old one. On the contrary, during the culmination and
retrogradation phases, the outbreak mainly spreads by further expansion from the
old spots. This behavioural change may be related to the gradual exhaustion of
susceptible trees, which decreases the interest to search for them.
Outbreak decline generally happens when there are no more weakened trees due
to their death or strengthening. Beetles must attack the remaining trees with a
higher population density, which reduces their multiplication rate up to a point when
they are unable to maintain the population level. This induces a negative feedback
leading to its fast decrease. Bark beetle natural enemies or unfavourable climatic
conditions could also be involved in outbreak decline, with varying degrees of
importance (Kenis et al., chapter 11; Wegensteiner, chapter 12).
Some species, especially the solitary species D. micans, do not correspond to this
model of population dynamics (Grégoire 1988). Contrary to other species, D.
micans is able to successfully attack trees without aggregation. Its population
dynamics seem mainly to depend on its interactions with the specific predator
Rhizophagus grandis (Kenis et al., chapter 11). When the predator is present, it is
able to maintain bark beetle population at a low level. Outbreaks occur when the
bark beetle invades forests where the predator is missing, and they decline some
years after when the prey is rejoined by its predator. So, as D. micans has gradually
invaded Europe over the course of a century, outbreaks have been regularly
observed on their invasive front. Population dynamics of xylomycetophagous
species is poorly studied. It seems mainly to depend on the availability of suitable
wood, but factors allowing attacks on living trees are unclear.
Bark beetle population dynamics are mainly viewed as interactions between
beetle and its host, but these insects are also interacting with other organisms.
Relationships with fungi and natural enemies are discussed elsewhere in this book
(Kirisits, chapter 10; Kenis et al., chapter 11; Wegensteiner, chapter 12), but bark
beetles also interact with other xylophagous insects. Interactions between bark
beetles have been rarely studied in Europe. There are few species and they are
generally rather well ecologically separated by host, within-tree distribution (bole
vs. crown) or flight precocityy (early-flyer species such as T.
T piniperda vs. late-flyer
such as I.
I sexdentatus) (Grünwald 1986; Amezaga and Rodriguez 1998). Thus, if
interspecific competition could occasionally y occur and disturb their distribution
(Bakke 1968; Schlyter and Anderbrandt 1993), it seems to be of low importance in
their dynamics. Similarly, as bark beetles are generally the first xylophagous insects
attacking a tree and they develop rapidly, they are rarely disturbed by other
xylophagous insects. By comparison, their activity is an essential element of the
constitution of the biotope of the xylophagous species which succeed them.
The theoretical model of aggregative bark beetle population dynamics has been
mainly inferred from data obtained at a tree level, but it has not been really tested in
the field, and it is difficult to use in forest management due to several difficulties.
The first one is the lack of a good estimator of bark beetle populations. Due to their
aggregative distribution, they are difficult and expensive to sample, and trapping is
only moderately reliable due to its sensitivity to local conditions (Bakke and Strand
1981). The poorly defined but large area occupied by a bark beetle population,
which is related to high dispersal capabilities of the beetles, increases this difficulty.
Extensive sampling studies have been conducted in North America at tree, forest
and regional level (Coulson, 1979), but they are adapted to epidemic populations
82 D. SAUVARD
which are not encountered in the intensively-managed European forests. Most

authors thus use damage level as population estimator, but it is not very precise due
to the variability of attack density. The second difficulty is the complexity of the
model itself, which depends on characteristics and reactions of three organisms,
beetle, tree and generally associated fungi, some of which such as tree resistance are
difficult to estimate. Finally, several parameters of population dynamics are poorly
known, especially mortality during dispersal phases and the importance of sister
broods in the field. The incidence of insect quality in population dynamics is also
poorly understood.
The field test of this theoretical model and its application to forest management
need to have verifiable predictions. Such predictions might be obtained by building
a mathematical model of bark beetle population based on this theoretical model. As
outbreaks are often induced by climatic accident, the model will not predict them.
However it could be useful for hazard rating and for outbreak k management by
predicting future population level changes and consequences of different pest
control options. Such a model will be complex, so it could only be built at a
European level. It also must be modular to progressively integrate the different
factors. Some characteristics of bark beetle populations have already been modelled
(Saarenmaa 1983, 1985; Anderbrandt 1986), butt they remain isolated. Modelling
capabilities of bark beetle life cycles and dynamics are thus much lower in Europe
than in North America (Coulson 1979; Fettig et al. 2001).
Another approach to bark beetle population dynamics has been recently
developed, particularly resulting from the availability of new tools to manage space-
time data (Geographic Information Systems, spatial analysis). These tools allow
analysis of bark beetle epidemiology and are often associated with remote sensing
(aerial and space imagery) as tool for mapping (Gilbert 2001; Otto and Schreiber
2001; Wichmann and Ravn 2001; Jakuš et al. 2003). They are also used to define
outbreak hazard rating of different sites according to the characteristics of the
station, the trees or the beetle population (Gilbert 2001; Netherer 2003). They could
finally identify the most suitable sites for different bark beetle species (Jakuš 1995).
Besides their direct interest for hazard rating,
a such results could reveal important
factors in bark beetle population dynamics which have to be precisely studied. Such
an approach would thus be complementary to bark beetle population modelling.
9. CONCLUSION
European bark beetles have been intensively studied for about two centuries. Even
if their results are partially biased by their focus on a small number of highly
damaging species, these studies have allowed a good comprehension of the life
cycle and to lesser extent an understanding of the population dynamics of these
insects. For a forest manager, their main features are 1) their cryptic behaviour, so
their damage is often only visible after they have left trees, 2) their high dispersal
capabilities, allowing extensive redistribution of their population at each generation,
3) their high reproduction capabilities, and consequently 4) their ability to develop
sudden outbreaks, mainly in relation to climatic hazard. However, that does not
minimise their ecological role as a first step in forest regeneration, and the forest
health problems that their attacks often highlight.
European research on bark beetles has suffered from the division of the research
community on the basis of countries or languages, even though this problem is
declining, notably as a result of European Union projects. This division has
favoured duplication in different countries and redundant studies which are often
difficult to synthesise. It could be an obstacle to future research. As the main
features of the life cycles and dynamics of bark beetles are rather well known, future
investigations would probably be progressively focussed on the interactions between
different factors. Such complex research needs effective cooperation of several
researchers with different specialities. Modelling might be a useful enabling
approach for such studies.
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Chapter 8
CHEMICAL ECOLOGY OF BARK BEETLES IN A

COMPLEX OLFACTORY LANDSCAPE
J.A. BYERS
Department of Crop Science, Swedish University of Agricultural Sciences, 230 53

Alnarp, Sweden
Present address: Western Cotton Research Laboratory, Agricultural Research
Service, USDA, 4135 E. Broadway Rd., Phoenix, AZ 85040, USA
1. INTRODUCTION
The Scolytidae (bark and ambrosia beetles) comprise a taxonomic group of at least
6000 species that, although appearing similar, may differ widely in their ecology and
biochemical adaptations to host trees. Bark k beetle species that feed on phloem (a
relatively thin layer just under the corky bark) are usually restricted to one or a few
host species, whereas ambrosia beetle species that are xylomycetophagous (wood-
feeding) and introduce symbiotic fungi for "cultivation" in their galleries generally
colonize a larger range of hosts (S.L. Wood 1982). Most biological knowledge on bark
and ambrosia beetles derives from studies on relatively few pest species in the genera
Dendroctonus, Ips, Scolytus, Xyleborus, Trypodendron, Tomicus=Blastophagus
= (Fig.
1), Pityogenes, Hypothenemus, Pityophthorus, Hylastes, and Gnathotrichus.
Many of these species are obligate and facultative tree-killing bark beetles that
comprise only about 10% of scolytid species in the United States and Canada (Raffa et
al. 1993). However, these pests that kill trees are the most likely to significantly
influence the evolution of the host tree and its chemistry.
The diversity of bark beetle biology, in which each species is adapted to only one
or a few host tree species, probably has resulted due to natural selection from the great
variety of plant biochemicals. It is also theorized that each species of tree has
coevolved various chemicals to defend against the herbivorous selection pressures of
the tree-killing bark beetles (Erlich and Raven 1965; Feeny 1975; Cates 1981;
Berryman et al. 1985; Byers 1995). Semiochemicals (behavior modifying chemicals)
from both the tree and the beetle have many functions during the life cycle of a bark
beetle (for reviews see D.L. Wood 1982; Borden 1982, 1997; Lanier 1983; Birch
1984; Borden et al. 1986; Byers 1989a, b, 1995; Raffa et al. 1993; Schlyter and
89
F. Lieutier et al. (eds.), Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis
89–134.
© 2007 Springer.
90 J.A. BYERS
Birgersson 1999). Host and non-host plant chemicals can be attractive, repellent, toxic,
or nutritious to bark beetles. These chemicals may have affects on: (1) finding and
accepting the host tree (host selection and suitability), (2) feeding stimulation and
deterrence, (3) plant resistance, (4) pheromone/allomone biosynthesis and
communication, and (5) attraction of predators, parasites and competitors of bark
beetles.
Figure 1. Electron micrograph of male (top) and female Tomicus piniperda from Sweden.
Knowledge of bark beetle chemical ecology and insect-tree relationships is

important to devising better ways of managing
a bark beetle populations and their
damage to trees. The strategies that bark beetles use to avoid competition within and
between species, to avoid unsuitable host and nonhost trees, to find their host trees and
mates, and to maximize their reproductive success can be investigated with the
purpose of eventually manipulating these processes to the detriment of the beetles.
Most of the following presentation involves species in the genera Dendroctonus,
Tomicus, Ips, and Pityogenes. Before presenting theories on possible strategies bark
beetles use for locating suitable hosts and avoiding competition, it is useful to consider
an overview of the life cycle and behavior of bark beetles in relation to
semiochemicals.
2. BEHAVIORAL ECOLOGY AND PHYSIOLOGY IN THE LIFE CYCLE OF

BARK BEETLES
In general, adults of bark beetles in the above genera overwinter in either forest litter
(e.g., Ips, Pityogenes) or the brood tree (e.g., Dendroctonus, Ips, Pityogenes). In
species that have several generations during the summer, emergence is from the brood
CHEMICAL ECOLOGY OF BARK BEETLES 91
Figure 2. Storm-damaged Scots pine, Pinus sylvestris, releases monoterpenes attractive to both
sexes of Tomicus piniperda in the early spring.
tree. Tomicus piniperda has a more complex life cycle in which adults over-
winter in living, nonbrood trees (Salonen 1973; Långström 1983). After emergence,
the adults of all species attempt to locate a host tree (termed the dispersal flight), either
by orienting to pheromone or plant volatiles. Host suitability may be determined in
flight or after landing on the tree. In the monogamous genera Tomicus and
Dendroctonus (subfamily: Hylesininae), the females select the host tree and an
entrance hole (attack) to begin construction of oviposition galleries in the phloem. In
contrast, males of the polygynous genera Ips and Pityogenes (subfamily: Scolytinae)
begin the entrance hole and later accept several females. In most cases, individuals of
only one sex begin the attack, releasing a species-specific blend of chemicals
comprising an aggregation pheromone (Byers 1989a). However, in D. brevicomis, the
female and the joining male each produce a unique synergistic pheromone component
that when combined elicit maximal attraction response (Silverstein et al. 1968; Kinzer
et al. 1969). In T. piniperda, there is no evidence of an aggregation pheromone (Byers
et al. 1985; Löyttyniemi et al. 1988); instead, host-tree chemicals induce aggregation
(Fig. 2).
Species of bark beetles feed only on one or a few host tree species, which are
perceived and located by means of the beetle’s various sensory receptors that are
located on their antennae and mouthparts. Except for morphological studies on D.
ponderosae and I. typographus, little is known about the sensilla on the maxillary and
labial palpi mouthparts of bark beetles (Whitehead 1981; Hallberg 1982). In these
species there is clearly a large number of chemosensilla (Fig. 3), which appear to be
important for host selection and food discrimination.
In other insects, the tarsi and ovipositor have chemosensilla that are involved in
host acceptance (Städler 1984), but these structurest have not been studied in bark
92 J.A. BYERS
Figure 3. Electron micrograph of mouthparts of Tomicus piniperda.
Figure 4. Electron micrograph of antenna and eye of Tomicus piniperda.
beetles. Most work with bark beetles has focused on the antennae (Fig. 4), which are
known to have sensilla responsive to volatile pheromone and host components, as well
as other air-borne chemostimulants (Borden and Wood 1966; Payne et al. 1973; Payne
1979; Mustaparta 1984; Faucheux 1989).
The electrophysiological response of an insect to semiochemicals can be studied
with an electroantennogram (EAG) of the whole antenna or by the single-cell
technique that measures responses of specific receptor cells (Payne 1979). Each
antennal receptor cell contains multiple acceptor sites that interact with the chemicals.
Bark beetle olfactory cells on the antennae have been shown to be of several
functional types, which probably are found in all species. These types include: (1) a
highly specific cell such as the ipsdienol-sensitive ones in I. paraconfusus and I. pini
that are responsive only to one of two possible enantiomers (identical atomic structures
but not superimposable, e.g., α-pinene in Fig. 5), (2) a pheromone-sensitive one that is
also responsive to other synergists or inhibitors such as the frontalin cells of D.
frontalis, which have at least two acceptor types each specific for one enantiomer of
frontalin, and (3) a "generalist" type thatt responds to host monoterpenes as well as
pheromones (Mustaparta et al. 1980; Payne et al. 1982; Dickens et al. 1985; Dickens
1986).
Vision plays a vital role during orientation flights of bark beetles, and in
conjunction with antennae enable bark beetles to locate semiochemical sources. The
eyes of many bark beetles (e.g., Ips, Scolytus, and Pityogenes) consistently have only
about 100-240 ommatidia (Fig. 4), which is less than many insects (Chapman 1972;
Byers et al. 1989a). Based on electrophysiological recordings, two color receptor types
have been identified in the eyes with a maximum absorbance at 450 nm (blue) and 520
nm (green) (Groberman and Borden 1982).
Observations of I. paraconfusus, I. typographus, D. brevicomis, P. chalcographus,
and T. piniperda a in flight chambers under dim red light or in complete darkness using
an electronic vibration detector indicate they will not fly after dark (Lanne et al. 1987;
Byers and Löfqvist 1989; Byers unpublished). Bark beetles are attracted in greater
numbers to traps baited with host odor or pheromone that are placed next to "tree trunk
silhouettes" than to traps without such visual stimuli, indicating that beetles orient to
the tree trunk during landing (Moser and Browne 1978; Borden et al. 1982; Tilden et
al. 1983; Lindgren et al. 1983; Bombosch et al. 1985; Ramisch 1986; Chénier and
Philogène 1989). Beetles of some species prefer to land on horizontal silhouettes
rather than on vertical ones of the same size (Pitman and Vité 1969). Another
indication that bark beetles have relatively poor visual acuity is that T. piniperda
a males
must walk within 1 cm of a female beginning her entrance hole before they appear to
detect her and initiate guarding behavior (Byers 1991). Both T. piniperda a and D.
brevicomis individuals can be induced to drop off a tree by movements of the human
body about 2 m away (about the same angle of resolution and relative size, my
observations).
Primary attraction to host tree volatiles can be considered to occur over a "long-" or
"short-range." The concept of range differs between authors and depends on the insect
considered. Here I consider long-range aattraction for bark beetles to be flight
orientation over a meter or more to a semiochemical source. In reality the division is
arbitrary, since bark beetles may orient over practically any distance depending on the
release rate of the semiochemical. At very high release rates the insect may not closely
approach the source due to adaptation (Baker et al. 1988). However, the concept of
range is valid at natural release rates. Attraction to pheromone is certainly long-range.
For example, three parallel lines spaced 4.6 m apart and hung with sticky screens
spaced every 1.5 m intercepted I. paraconfusus in a "V"-shaped pattern narrowing to a
pheromone source of 50 males boring in a pine log (Byers 1983a). In this experiment,
beetles appeared to orient over a distance of at least 17 m. S. quadrispinosus beetles
94 J.A. BYERS
Figure 5. Major monoterpenes of conifers. Note that the enantiomers of α-pinene are identical
except that they are non-superimposable (mirror images). Camphene, ß-pinene, 3-carene, ß-
phellandrene, and limonene also have two enantiomers, although only (-)-ß-pinene and (+)-3-
carene are found in trees (Mirov 1961). Myrcene and terpinolene are achiral.
were intercepted by passive traps 12 m from a girdled hickory tree that was attracting
these beetles (Goeden and Norris 1964). The distance over which beetles respond
anemotactically depends primarily on the release rate of the volatile (under mild wind
conditions). In Denmark, I once observed I. typographus flying slowly upwind (0 to
0.5 m/s ground speed) in 3 m/s gusty winds to a large fallen spruce tree under massive
attack. During their orientation to this pheromone source, beetles were flying at 3-6 m
in height from at least as far away as 50 m downwind. Jactel (1991) estimated that the
maximum attraction distance of I. sexdentatus to pheromone-baited traps was 80 m.
An index of attraction strength for a particular semiochemical release rate is known
as the "effective attraction radius" (EAR
( ), which is proportional, but considerably
smaller, than the maximum attraction distance (Byers et al. 1989a). The EAR is the
radius that a trap would need to be enlarged, as a spherical "passive" trap, in order to
intercept as many dispersing insects as were actually caught on the trap when baited.
For example, the EAR of T. piniperda a to a blend of three host monoterpenes, released
at rates equivalent to a cut log of Scots pine from each of 10 traps along a 12-m high
pole, was largest at the lowest trap (EAR
( = 1.3 m). The same design found an EAR of
3.2 m for I. typographus response to a blend of its pheromone components (Fig. 5).
These comparisons indicate that the EAR can be larger for a pheromone than for host
volatiles. However, both these values would be greater at higher chemical release
rates. Schlyter (1992) discusses several additional concepts of attraction distance,
including the attraction range (the maximum distance over which insects can be shown
to be attracted) and the sampling range (the distance over which insects reach a source
in a given time period).
The optomotor anemotaxis mechanism for orientating to pheromone sources
proposed for insects, especially moths (David et al. 1982; Baker 1989), also appears to
function in bark beetles (Choudhury and Kennedy y 1980). In this theory, a bark beetle
attempts to fly directly upwind when in contact with a packet of pheromone-laden air
of the plume, but casts (flies from side to side with respect to the source) when contact
is lost. The beetle senses the wind direction while flying by observing the ground
below: in no wind, or head-on wind, the ground moves directly underneath during
flight. However, if the visual ground field also moves from right to left somewhat, for
example, then wind is coming from the left, and the beetle turns to the left to minimize
the transverse ground shift and keep the ground moving directly underneath, in this
manner the insect heads upwind and toward the pheromone source.
Short-range attraction could be considered to occur within one meter of the source
such as when flying along the trunk as I have observed for T. piniperda; however, after
landing the beetle must use a mechanism other than optomotor anemotaxis. While
walking, the ground does not move under the beetle due to wind, but the beetle
probably can still sense wind direction by mechanoreceptors, and use "casting" or
circling movements to locate the odor source. Beetles walking in an arena with
laminar airflow respond to a point source of synthetic pheromone (or air from an
attacked log) by walking directly upwind within the odor plume. If they walk outside
the plume, they would experience a concentration
a gradient decline as they walked. By
turning slightly with respect to the upwind angle (as detected by tactile hairs) they
would either soon re-contact the odor or the concentration would further decline. In the
later case they could reverse the angle or continue turning in a circle that would bring
them into contact with the odor, whereupon they could walk directly upwind again.
This mechanism is consistent with tracings of tracks of I. paraconfusus (Borden and
Wood 1966) responding to pheromone in the laboratory olfactometer (see Birch 1984)
as well as observations of other species in the genera Ips, Dendroctonus, Tomicus, and
Pityogenes responding to pheromone or host odors in similar olfactometers (Byers et
al. 1979; Byers and Wood 1981a; Lanne et al. 1987; Byers 1983a; Byers et al. 1990a,
b).
After the beetle orients and lands on a host tree and begin to release an aggregation
pheromone, the likelihood of successful colonization depends on (1) the population
level of beetles available for recruitment to the attack and (2) the resistance and health
of the tree and its ability to produce defensive resin (Fig. 6). Resistance of conifers,
especially pines, to bark beetle attacks has long been attributed to the amount of resin
exuded and pitch tubes formed (Webb 1906; Hodges et al. 1985). Dead beetles can
often be seen in crystallized resin of pitch tubes. However, species of Dendroctonus
and other aggressive bark beetles have a great ability to survive the "toxic"
monoterpenes and suffocating mucilage and may struggle for hours in copious resin
flows ((D. frontalis, Hodges et al. 1979; D. brevicomis, Byers 1995). Drought and poor
96 J.A. BYERS
water balance lower the resistance of conifers (Hodges and Lorio 1975; Hodges et al.
1979) probably by lowering the turgidity of resin duct cells, which lowers the
oleoresin exudation pressure (OEP). A correlation between higher OEP and greater
resistance of ponderosa pine to attack by D. brevicomis and I. paraconfusus has been
reported (Vité 1961; Wood and Vité 1961; Wood 1962; Brown et al. 1987). Oleoresin
and the monoterpenes indicate host resistance and therein are repellent to bark beetles
in concentrated amounts (Struble 1957; Pitman et al. 1966; Berryman and Ashraf
1970; Bordasch and Berryman 1977; Byers et al. 2000; El-Sayed and Byers, 2000).
Beetles of many species have specialized areas of the integument or pouches called
mycangia where symbiotic fungi are carried, and in some species nourished, until they
are introduced inside the entrance tunnel where they grow into the tree (Happ et al.
1976; Whitney 1982; Bridges et al. 1985; Paine and Stephen 1987; Levieux et al.
1991). Some of the fungal species (genera Ceratocystis=Ophiostoma, Trichosporium)
may attack the living tissues of the tree and paralyze the tree's ability to produce and
exude resin for defense against the beetle (Mathre 1964; Horntvedt et al. 1983; Paine
1984; Raffa and Berryman 1987; Paine and Stephen 1987; Paine et al. 1988). Other
fungal species of the beetle's mycangium grow in the galleries after the tree has been
killed and appear important to the nutrition and growth of the larvae (Bridges and
Perry 1985; Paine et al. 1988; Goldhammer et al. 1991). In ambrosia beetles, that
generally attack unhealthy or dead trees, the adults and larvae feed on fungi lining the
galleries instead of on the tree's tissues (Funk 1970; Furniss et al. 1987; Kajimura and
Hijii 1992).
Successful colonization and reproduction by a bark beetle in a living tree requires
release of enough aggregation pheromone to ensure the attraction of sufficient
conspecifics to overwhelm the host tree defenses (Fig. 6); however, after killing the
tree and securing mates, pheromone should stop in order to avoid further competition
for bark areas (Byers et al. 1984; Berryman et al. 1985). Semiochemicals play a role in
"cooperation" among beetles when killing the tree and in their avoidance of
competition (discussed later). "Pioneer" beetles that attack the tree first may suffer
most from the tree's defensive resin, but these beetles may have no choice but to attack
due to low fat reserves. The later that a beetle arrives in the colonization sequence of
the host, the poorer is the quality of the bark substrate due to (1) space utilization by
established conspecifics (intraspecific competition) and (2) degradation by
microorganisms (discussed subsequently).
Under the bark, females lay eggs that hatch to larvae and feed on the phloem for
several weeks. Chemicals from both the plant and microorganisms could affect beetle
survival at this time, but little is known about
a these interactions. However, once the
tree is dead, there can be no natural selection on the insects to evolve different tree
genotypes that produce chemicals harmful to beetles. The larvae pupate in the bark and
become yellow, callow adults where they feed and mature until emerging. The beetles
may begin a dispersal flight during the same season, or after overwintering in either
the tree ((Dendroctonus, Pityogenes and many Ips) or in the forest litter ((I. typographus
in colder climates). Tomicus minorr and T. piniperda a emerge from the bark and fly
relatively short distances to the tops of pine trees where they bore into a shoot during
the summer (Salonen 1973; Långström and Hellqvist 1991). In the autumn, beetles of
T. piniperdaa crawl down the trunk and bore into its base to overwinter, whereas T.
minorr overwinters in the litter (Salonen 1973; Långström 1983). The next sections will
present the details of some olfactory strategies employed during dispersal to find mates
and suitable host trees in which to reproduce.
Figure 6. Dendroctonus brevicomis in resin of ponderosa pine.
3. DISPERSAL FROM THE BROOD TREE OR OVERWINTERING SITE

Insects disperse when their habitat becomes unsuitable. This can be from a lack of
food resources, mating possibilities, territories and suitable domiciles, or from the need
to escape the local buildup of parasites and predators (c.f. Ricklefs 1990). Apparently
for the same reasons, bark beetles emerge from the dead brood tree, or litter near the
brood tree, and begin a dispersal flight seeking suitable host trees from among many
non-host and unsuitable host trees (Fig. 7).
During dispersal, bark beetles and associated predators and parasites feeding or
living in brood trees must locate a new host tree from among the relatively few widely
scattered suitable hosts in the forest. The host tree is restricted usually to one or a few
species and in most cases the bark beetles seek weakened, less resistant trees, or trees
that are in the initial stages of death and decay. Also, beetles try to avoid feeding and
reproduction in areas heavily colonized by conspecifics and competing species (Byers
1984, 1995; Fig. 8). Thus, it is expected that species have evolved behavioral
responses to volatile host-plant chemicals that indicate the presence of a suitable host
in which reproduction can occur.
The dispersal flight of a bark beetle may vary from only a few meters (as
observed during epidemics) to possibly several kilometers. Several factors interact
to cause the dispersal flight distance to vary between individuals. The most obvious
98 J.A. BYERS
is that a beetle encounters a susceptible tree early in the dispersal flight. However,
whether this tree is attacked may depend on the level of fat reserves that can be
mobilized for flight (Atkins 1966, 1969; Byers 1999). A beetle should have higher
reproductive fitness if it flies far from the brood tree since it can both avoid inbreeding
Figure 7. Many species of bark beetles disperse through a stand of Norway spruce in the
spring (Torsby, Sweden).
with siblings and, probably more importantly, escape predators and parasites that are
locally denser near the brood tree. Thus, the dispersal distance has been optimized
over evolutionary time to balance the probably logarithmically increasing benefits of
flying farther against the probably exponentially increasing likelihood of exhaustion
and failing to find a host. The fat level required for lengthy dispersal will depend on
the conditions in the brood tree during larval development; for example, disease,
insect, and climatic factors will affect the nutritional quality of the host (Fig. 9).
Severe competition among the larvae will reduce the size of adults as well as their
fat content (Atkins 1975; Anderbrant et al. 1985). Parasites would reduce the size
and fat content of some adults while predators would lessen competition for those
remaining locally, thereby increasing the variability of dispersal range in the
population. The population density of bark beetles should be stabilized by a
frequency-dependant competition for the susceptible trees. This would produce
increasingly stronger, longer-flying individuals with decreasing attack and larval
density while producing weaker, shorter-flying individuals with increasing
competition.
Knowledge of how far and where bark beetle populations disperse comes mainly
from (1) mark-release-recapture studies using pheromone traps and from (2) the
geographical occurrence of new infestations relative to previous ones. Both lines of
investigation are inconclusive since (1) only a few pheromone traps were used, usually
some tens to hundreds of meters from the release site, so that a large proportion of
Figure 8. Spacing of attacks of Ips typographus (larger

r circles) and Pityogenes chalcographus
(smaller circles) to avoid competition in the bark of Norway spruce (bark surface scraped
smooth on left to reveal attacks that were circled with ink pen).
released beetles escaped, or (2) the origins of attacking beetles were uncertain. Several
studies have placed various sized rings of pheromone traps around a source of marked
beetles. For example, the spruce bark beetle of Europe, I. typographus, was recaptured
at various outer distances from 120 to 1000 m (Botterweg 1982; Zumr 1992; Zolubas
and Byers 1995; Duelli et al. 1997). In California, I. paraconfusus was recaptured in
outer traps at 2 km (Gara 1963). The ambrosia beetle, Trypodendron lineatum, was
recaptured at 500 m (Salom and McLean 1989). As expected, the widely spaced outer
traps captured a small proportion of the released beetles, and the large gaps between
traps probably allowed many to slip through as they drifted with the wind (e.g., gaps of
785, 1257, and 393 m in Zumr 1992; Garaa 1963; and Salom and McLean 1989;
respectively). An adverse effect of marking, although discounted, might also influence
the dispersal.
The view that bark beetles can fly some tens of km is based less on mark-recapture
studies and more on collections of beetles far from forests. Nilssen (1978) found two I.
typographus in the stomach of a salmon 35 km from any spruce forest. Miller and
Keen (1960) report results of studies by the US Forest Service in California where the
western pine beetle, D. brevicomis, infested ìslands' of ponderosa pine, initially free
of beetles, that were separated from the main forest by open sagebrush areas. They
concluded that significant numbers of bark beetles must have flown a minimum of 3.2
km in one study, and 9.6 or 20 km in another
t study, to reach the infested trees.
100 J.A. BYERS
Increasing competition among larvae due to increasing densities of parents laying

broods was shown to reduce size and fat content of bark beetles (Atkins 1975;
Anderbrant et al. 1985) and thus should decrease dispersal ranges. However, this
seems in conflict with the statement of Forsse (1991) that flying time of I. typographus
on flight mills was "similar among populations and appeared unaffected by outbreak
Figure 9. Ips typographus preparing to begin the dispersal

i flight after emerging from the duff in
late May in Sweden.
conditions". Earlier, Forsse and Solbreck (1985) could not find any affect of sex or
body size on the duration of flight on mills. Botterweg (1982) also concluded that
there was little, if any, affect of beetle size or fat content on dispersal distance as
monitored in field traps. However, he did find that fat content of beetles declined over
the flight period. This was probably due to consumption of fat during host-seeking
rather than later emergence off lower-fat beetles since beetle's sizes (elytral weights)
did not decrease over the spring season. Birgersson et al. (1988) reported that newly
emerged I. typographus averaged about 10% fat, while after 24 hours of flight exercise
in a plastic box, they declined to only 5% since fat is used for energy. In trees, males
with nuptial chambers had about 8% fat (possibly replenishing some after feeding), but
after several more days of feeding after females had joined them, the males had 10%
fat again.
Bark beetles appear capable of flying quite far in the forest since newly emerged
D. pseudotsugae flew an average of 2 h on flight mills before resting (3 h total), while
some individuals flew up to 8 h uninterrupted (Atkins 1961). Jactel and Gaillard
(1991) flew I. sexdentatus on rotary flight mills and found that 50% of the beetles
could fly more than 20 km, and 10% more than 45 km, based on about 50 interrupted
flights. About 25% of I. typographus taken from litter in an outbreak area flew for
over 1 h, and 10% for more than 2.5 h on flight mills, with a maximum flight of 6 h
and 20 min recorded (Forsse and Solbreck 1985). At free-flying speeds of 1.9 to 2 m/s
(Gries et al. 1989; Byers 1996a), a maximum range would be 41 to 45.6 km without
wind transport. However, wing beat frequency declines with flight duration, which
may affect flight range. In the only case studied, the wing beat frequency of D.
pseudotsugae of about 95 Hz declines 18 % with flight time over 4 h to about 75 Hz
(Atkins 1960). Speed on flight mills also declined from 1.11 m/s to 0.99 m/s (Atkins
1961).
4. DECIDING WHETHER TO ACCEPT A HOST OR CONTINUE TO DISPERSE

Tradeoffs regarding host plant acceptance by insects have been reviewed by Miller
and Strickler (1984). They present a model (their Fig. 6.1) by Dethier (1982) where the
decision by the insect whether to accept the plant is dependent on external (olfaction,
vision, mechanoreception, and gustation) stimulatory
m and inhibitory inputs balanced
against internal excitatory and inhibitory inputs. A graphical, and simplified, model of
host acceptance is shown in Fig. 10 that is directly applicable to pioneer bark beetles.
In this model, as the bark beetle flies around searching for suitable host trees (usually
trees already under attack by conspecifics) they use up energy reserves of lipids
(Atkins 1969; Thompson and Bennett 1971) aand probably become increasingly willing
to accept substandard hosts.
The beetle may, by chance, encounter several hosts during the dispersal flight that
are more or less suitable for reproduction. The beetle will accept a host if the
combination of the host suitability and fatigue level of the beetle is above the curve
(Fig. 10); otherwise the beetle will continue searching for more suitable hosts. The
curve is asymptotic to the Y-axis for those beetles that require flight before responding
to semiochemicals, whereas the curve would intersect the Y-axis for species that are
immediately responsive after emergence. The suitability of the host is determined by
the nutritional quality, as well as by the density of established attacks by the same or
other species of bark beetle that indicate the potential for damaging competition.
At the beginning of a dispersal flight, bark beetles are considered rather unresponsive
to pheromone or host volatiles. The theory is that fat reserves are higher in freshly
emerged beetles so that they have the ability for extended flight and can gain adaptive
benefits from dispersal before responding to hosts (Borden et al. 1986; Anderbrant et
al. 1985; Gries et al. 1990). Graham (1959) showed that continued flight exercise by
T. lineatum caused an increase in responsiveness to visual and olfactory stimuli of the
host. Freshly emerged T. lineatum and D. pseudotsugae required 30 or 90 min of
flight, respectively, before responding to pheromone from female frass (Bennett and
Borden 1971). Atkins (1966) found that female D. pseudotsugae with more than 20 %
102 J.A. BYERS
fat (dry weight) were usually not responsive to the host, while those under 20 % fat
were responsive and still could fly. Beetles with less than 10% fat had trouble flying
since fat was required as an energy source (Atkins 1969). The fat metabolized by D.
pseudotsugae consists mainly of C16 and C18 fatty acids (Thompson and Bennett
1971). Other studies have found that scolytid beetles in the genera Trypodendron,
Dendroctonus, Scolytus, and Ips increased their responsiveness or upwind orientation
to host and pheromone after continued flight exercise (Choudhury and Kennedy 1980;
and cf. Borden et al. 1986).
Figure 10. Theoretical curve for the acceptance of host trees by bark beetles depending on
prerequisite flight exercise (asymptotic y-axis) and level of fatigue (amount of flight) and
suitability of the host for reproduction (which depends on nutritional quality and density of
colonization by competing bark beetles).
However, some bark beetles appear responsive to pheromone upon emergence.

Lindelöw and Weslien (1986) found that overwintered I. typographus, collected and
marked as they emerged from tents over forest litter, were caught in synthetic
pheromone traps within minutes of release. Schlyter and Löfqvist (1986) suggested
that preliminary experiments indicated I. typographus became more responsive to
pheromone with flight exercise, but further details were not reported. The majority of
I. paraconfusus in California responded to aggregation pheromone soon after
emergence (Wood and Bushing 1963; Gara 1963; Hagen and Atkins 1975). Botterweg
(1982) also found that I. typographus can immediately respond to pheromone when
beginning dispersal, and this is in accordance with his finding that beetles lost 40-50%
of their fat over the winter. Possibly, second generation beetles in southern Europe
would have higher fat content and consequently disperse further.
5. THEORIES OF HOW BARK BEETLES FIND SUITABLE HOST TREES

There are two general theories on how bark beetles find suitable host trees that have
not been previously colonized by conspecifics releasing pheromone (McMullen and
Atkins 1962). The first is that beetles locate such trees by orienting over several meters
to volatile chemicals usually released by damaged or diseased trees (called "primary
attraction"). It seems that Tomicus piniperda a finds hosts by primary attraction as the
species is attracted to monoterpenes in the resin (Fig. 11).
The second theory is that beetles fly about and encounter suitable host trees at
random, whereupon they land and test them by short-range olfaction or by taste. The
two theories are not mutually exclusive, and one or the other may primarily operate in
a particular species. In California, host finding by the important pests D. brevicomis
and I. paraconfusus is thought to be a random process. Ponderosa pines that were
killed by freezing with dry ice and then screened to prohibit bark beetle attack, did not
have higher landing rates for the prevalent D. brevicomis and I. paraconfusus bark
beetles (among other species) than did living trees. Landing rates on diseased and
healthy trees also were similar. It was estimated that about one D. brevicomis beetle
visited each tree in the forest each day (Moeck et al. 1981; D.L. Wood 1982). Logs of
freshly cut ponderosa pine placed in sticky screen traps did not catch beetles of these
species, while at the same time high numbers were attracted to synthetic pheromone or
infested logs (Moeck et al. 1981).
In addition to I. paraconfusus and D. brevicomis, many species probably visit trees
at random, whereupon the tree’s resistance is tested during an attack. For example,
Scolytus quadrispinosus was caught equally on traps placedd in host shagbark hickory,
Carya ovata, and nonhost white oak, Quercus albaa (Goeden and Norris 1965).
Berryman and Ashraf (1970) found attacks by Scolytus ventralis in the basal section of
74% of grand fir examined, while only 3.5% of these trees were colonized. Most
unsuccessful attacks were abandoned before beginning the gallery. The attacks on
grand fir appeared random during the early part of the flight period before
aggregations resulted. Hynum and Berryman (1980) caught D. ponderosae in traps on
96% of the lodgepole pines ((P. contorta) sampled, but only 66% of these pines were
killed. Also, they found no differences in landing rates between killed and surviving
lodgepole pines or between host and nonhost trees. A direct relationship between the
numbers of D. ponderosae caught on unattacked trees and the numbers of trees upon
which beetles landed was found in a study of lodgepole pines (Raffa and Berryman
1979). I. grandicollis landed equally on sticky traps on trees judged resistant or
susceptible based on crown area (Witanachchi and Morgan 1981). However,
Schroeder (1987) found an average of 35 T. piniperda a landing on lower vigor Scots
pine, P. sylvestris (as judged by less crown area), than on higher vigor trees (mean of
22 landing per tree). These differences could be due to secondary release of
monoterpenes by beetles boring in the low vigor trees that were less able to resist
attack.
There is some evidence that I. typographus is weakly attracted to host volatiles
(Austarå et al. 1986; Lindelöw et al. 1992) or monoterpenes such as α-pinene
(Rudinsky et al. 1971), but other studies have nott observed any attraction to host
volatiles or synergism of pheromone and host volatiles (Schlyter et al. 1987a). A
computer model by Gries et al. (1989), in which "beetles" must take a series of flights
between trees in a grid (each flight to one of eight neighboring trees) and test each tree
for suitability, showed that few beetles would find the widely scattered hosts
designated as susceptible. Thus, they concluded that a mechanism of long-range
104 J.A. BYERS
primary attraction would be required for maintenance of the population. However, a

more recent computer model, in which beetles "fly" more naturally among randomly
Figure 11. Attraction of Tomicus piniperda to monoterpenes released from oleoresin exuding
from cut end of a Scots pine log.
dispersed susceptible trees indicated that a significant proportion of the population

could find the susceptible trees by chance interception of the trunk diameter (Byers
1993a, 1996a). If beetles then test the defenses of the potential host (although this
rarely has been observed) then weaker, more susceptible, trees will not exude adequate
resin and allow the beetle to produce aggregation pheromone. According to the later
model, this will in effect greatly increase the effective "radius" of the tree (or EAR) so
that many more in the population can quickly find and colonize these trees (Byers
1993a, 1996a).
In addition to the “random landing” and “primary attraction” to host volatile
theories, some bark beetles may find weakened and susceptible host trees by orienting
to volatiles produced by competing species during colonization. The volatiles can be
host compounds that virtually any bark beetle would release upon attack (e.g.,
monoterpenes) or pheromone components of these other species. For example, D.
brevicomis responds to pheromone components of I. paraconfusus in the laboratory
(Byers and Wood 1981a); I. typographus responds to exo-brevicomin (from D. micans
and Dryocoetes spp., Borden et al. 1987) when combined with its pheromone
components (Tommerås et al. 1984); and several sympatric species of Ips in the
southeastern United States are cross-attracted to infested pine logs in the field (Birch et
al. 1980b).
Finally, bark beetles may be aided in locating suitable host trees by avoiding
volatiles from (1) hosts fully colonized by conspecifics or competing species and (2)
nonhost trees and plants. Avoidance of these types of substrates will be covered in
more detail in later sections on discriminating suitability of hosts, avoidance of

competition and decaying colonized hosts, and avoidance of nonhosts.
6. STRATEGIES OF “PIONEER” BARK BEETLES
Figure 12. Conceptual model of dispersal and host-seeking ecology of "aggressive" bark
beetles that use aggregation pheromones. Factors such as the beetle's fat reserves, chances of
encountering pheromone, and level of competition and host suitability determine whether a
beetle joins resident beetles in colonizing a tree or is the firstt "pioneer" to attack.
A beetle that lands on a tree and attempts to find a place on the bark to bore is termed a
"pioneer" if there are few others present. Pioneers are presumed to encounter
significant host resistance and resin when attacking compared to later arrivals
("joiners") when the tree is weakened or has succumbed (Berryman 1974; Raffa and
Berryman 1979; Wood 1982; Byers 1995). Only males, in the case of Ips and
Pityogenes, or females, in the case of Dendroctonus, initiate the entrance tunnel and
can be pioneers, but the joining sex in the early stages of colonization must incur some
increased risks of resinosis as well. One hypothesis
y is that since a few pioneers must
attack the tree and survive to produce pheromone before numerous others of the
population can exploit the resource, pioneers must be the largest and most vigorous
beetles of the population. In Fig. 12, an alternative theory is presented for the dispersal
and host-seeking flight under various conditions and circumstances. An individual
should prefer to orient to pheromone and a tree under colonization, but if fat reserves
become relatively low during dispersal, then a pioneer strategy becomes advantageous
106 J.A. BYERS
compared to exhaustion in flight (as in Fig. 10). As fat reserves become dangerously
low, the beetle might attempt to bore into any host tree in the expectation of
encountering one of low resistance (Fig. 2). Thus, smaller beetles, such as those that
suffered severe larval competition and have low fat (Anderbrant et al. 1985;
Anderbrant and Schlyter 1989), or those thatt have used up their fat reserves during a
host-seeking flight, regardless of size, are hypothesized to be the pioneers (Byers
1999).
If the pioneer beetle lands on a tree of low resistance that cannot produce
sufficient resin to repel the beetle, then it has time to feed and excrete pheromone
components with the fecal pellets. This then functions as a beacon to individuals of
the population in the surrounding area that a weakened host can be exploited as a
food and mate resource (Byers 1996a). Aggregation pheromone is an evolutionarily
adaptive signal since only trees too weak to vigorously repel beetles with resin will
allow beetles to produce pheromone and joining beetles will likely suffer less
mortality than as a pioneer. Some species, usually termed less aggressive ones, such
as the European pine shoot beetle, Tomicus piniperda, are attracted to monoterpene
volatiles produced after injury to the host tree by biotic or abiotic factors that
indicate susceptibility (Byers et al. 1985; Byers 1995, 1996a).
7. HOST SEMIOCHEMICALS ATTRACTIVE TO BARK BEETLES

Species of bark beetle that regularly attack and kill living trees (termed "aggressive")
have been shown nearly always to possess an aggregation pheromone, usually of two
or more components, but are weakly, if at all, attracted by host volatiles alone (Vité
and Pitman 1969; Byers 1989a, 1995). However, so-called "secondary" bark beetle
species (those that arrive later after the tree has already been killed by the aggressive
bark beetles or that feed as saprophytes in decaying trees) may not use an aggregation
pheromone, but generally are strongly attractedd to either host monoterpenes, ethanol or
a combination (Kohnle 1985; Klimetzek et al. 1986; Schroeder 1988; Schroeder and
Lindelöw 1989). Host volatiles are attractive to a number of forestt scolytids including
species in the genera Scolytus, Dendroctonus, Hylurgops, Trypodendron and Tomicus
(Goeden and Norris 1964; Rudinsky 1966; Meyer and Norris 1967a; Moeck 1970;
Byers et al. 1985; Lanne et al. 1987; Volz 1988; Lindelöw et al. 1992; Hobson et al.
1993; Macias-Samano et al. 1998).
Ethanol, probably released by microorganisms in decaying woody tissue (Graham
1968; Moeck 1970; Cade et al. 1970) and by alcoholic fermentation processes in
stressed plants (Kimmerer and Kozlowski 1982; Kelsey 1994, 1996; Kelsey and
Joseph 1997, 1999), is attractive to a wide variety of species of bark beetles (Moeck
1970, 1981; Magema et al. 1982; Montgomery and Wargo 1983; Kohnle 1985;
Klimetzek et al. 1986; Schroeder 1987, 1988; Schroeder and Eidmann 1987; Phillips
et al. 1988; Volz 1988; Chénier and Philogène 1989; Schroeder and Lindelöw 1989;
Byers 1992a). Primary alcohols other than ethanol have not been reported as being
attractive to scolytids. However, only a few studies have tested methanol (Moeck
1970; Montgomery and Wargo 1983; Byers 1992a); longer chain alcohols up to
hexanol did not attract Scolytids in Sweden when they were known to be flying (Byers
1992a). Electroantennogram (EAG) responses of T. piniperda a to a series of straight-

chain alcohols indicated that the antennae respond increasingly to longer chain length
up to a maximum between pentanol, and heptanol, and then decrease in responsiveness
(Lanne et al. 1987). The response spectrum could be due in part to differences in
volatility. Thus, although ethanol a plays a role in host selection (discussed
subsequently), the EAG response for ethanol is lower than for longer-chain alcohols,
which are not attractive but rather repellent. 1-Hexanol (from deciduous trees) inhibits
response of T. piniperda a to attractive monoterpenes (Schlyter et al. 2000). Ethanol and
CO2 are the usual end products of sugar fermentation by microorganisms whereas
methanol is not, which probably explains the evolution of the use of ethanol by forest
insects. Moeck (1970) found methanol to be a minor constituent and ethanol a major
constituent of extracts from Douglas-fir sapwood attractive to T. lineatum.
Various tree monoterpenes (e.g. α-pinene, myrcene, terpinolene, ß-pinene, Fig. 5)
and turpentine are also attractive to a large number of bark beetle species (Byers et al.
1985, 1992a; Phillips et al. 1988; Schroeder 1988; Chénier and Philogène 1989;
Schroeder and Lindelöw 1989; Miller and Borden 1990; Phillips 1990; Hobson et al.
1993). Synergism between ethanol and various monoterpenes (or turpentine) is also of
widespread occurrence (Nijholt and Schönherr 1976; Kohnle 1985; Vité et al. 1986;
Phillips et al. 1988; Volz 1988; Schroeder 1988; Chénier and Philogène 1989;
Schroeder and Lindelöw 1989; Phillips 1990). These compounds are not only
important for primary attraction to plants, but also may play a role in enhancing the
bark beetles' response to aggregation pheromone (Bedard et al. 1969, 1970; Pitman et
al. 1975; McLean and Borden 1977; Borden et al. 1980, 1981; Paiva and Kiesel 1985;
Byers et al. 1988; Miller and Borden 1990). Host-tree compounds, ethanol and
monoterpenes, elicited increased entering rates of bark beetles T. lineatum and P.
chalcographus, respectively, into pipe traps baited with aggregation pheromone (Vité
and Bakke 1979; Bakke 1983; Byers et al. 1988). ß-Phellandrene (Fig. 5) is slightly
attractive alone to I. pinii and enhances response to pheromone (Miller and Borden
1990), and so the monoterpene might induce entering of holes.
In most of the previously discussed studies, the discovery of host compounds
attractive to bark beetles has been by the comparative approachh (similar species are
known to be attracted) or by surmising that identified chemicals in the host would be
attractive. Thus, most studies are incomplete because of the possibility that there are
still undiscovered chemicals important for attraction to the host. Byers et al. (1985)
used the subtractive-combination bioassay a and fractionation method (Byers 1992b) to
rigorously identify the host volatiles responsible for aggregation of T. piniperda. A
S α-pinene, (+)-(R
combination of (-)-(S)- ( )-α-pinene, (+)-3-carene, and terpinolene, or
each alone, was effective in attracting both sexes (Fig. 5 and 11). During the isolation
study, designed for detection of synergistic pheromone components, no evidence was
found for beetle-produced compounds being attractive, in contrast to most bark beetles
that aggregate en masse on hosts (Byers 1989a). Byers et al. (1985) quantified the
release rates of α-pinene, terpinolene, and 3-carene from a freshly cut log of Scots pine
(28 cm x 13 cm diam.) and found them eachh to be about 15 mg/day. Release of
comparable amounts in the field competed favorably with a host log in attracting T.
piniperda. They theorized that the beetle’s attraction to monoterpenes functioned in
108 J.A. BYERS
the selection of host species because other common tree species have less
monoterpenes. In addition, this attraction to monoterpenes served in the beetle’s
recognition of its host's susceptibility since storm-damaged or felled trees have
resinous wounds releasing monoterpenes and are less able to resist attack due to the
injuries.
In the isolation of host volatiles attractive to T. piniperda, a gas-chromatographic
adsorbent (Porapak Q), widely used for trapping insect pheromones, was used to
collect headspace air from the infested pine logs. Unfortunately,
t Porapak Q will not
retain ethanol molecules due to their small size. Thus ethanol could be a constituent of
the attractive host odor. Vité et al. (1986) presented evidence that ethanol enhanced the
attraction of T. piniperda a to α-pinene and terpinolene (identified above) by about
eight-fold, but these results are difficult to confirm since the chemical release rates
were not given. They proposed that ethanol would be released from diseased trees and
thus indicate their suitability to T. piniperda. Ethanol is attractive when released on
healthy trees since T. piniperdaa were caught in ethanol-baited traps on trees; and these
beetles also attacked trees baited with ethanol (Schroeder and Eidmann 1987; Byers
1992a). However, the attraction to ethanol in traps away from trees is weak or
negligible, while monoterpenes in these traps are attractive (Schroeder 1988;
Schroeder and Lindelöw 1989; Byers 1992a).
Ethylene is another chemical that may be released by diseased or dying trees that
could be attractive to bark beetles. Campos et al. (1994) found that the olive bark
beetle, Phloeotribus scarabaeoides, was attracted to logs of olive that released
higher amounts of ethylene. Also, a chemical reaction of 2-chloroethylphosphonic
acid caused ethylene to be released, which attracted the beetles in the laboratory
(Campos and Pena 1995). Trees treated with the chemical released more ethylene
and caught more beetles on traps than traps on control trees (Gonzalez and Campos
1995). Treated wood also released more ethylene that resulted in higher densities of
attacks by olive bark beetles (Gonzales and Campos 1996). Inoculation of bark
beetle-vectored fungi, Ophiostoma minus and O. nigrocarpa, into slash and loblolly
pines induced ethylene release (Popp et al. 1995). Ethylene was also released from
needles of Monterey pine inoculated with the pitch canker fungal pathogen,
Fusarium circinatum. However, the twig-infesting Pityophthorus spp. was not
attracted to ethylene, cut branches, orr to branches plus ethylene (Bonello et al.
2001), although fungal infected branches were not tested. The authors concluded
that host discrimination occurs after landing. More research is needed to determine
if ethylene plays a role in primary attraction of other bark beetles to weakened hosts.
8. DISCRIMINATING THE SUITABILITY OF HOSTS

Plant suitability in insects was reviewed by Scriber (1984). A plant's suitability to bark
beetles varies with its nutritional quality and composition of deterrents and toxins.
Nonhost trees are probably less nutritional to a particular beetle than its hosts. The
beetle in most cases would not be expected to be able to detoxify some of the toxins in
nonhosts (which are avoided or not usually encountered) that may have evolved for
use against herbivorous insects. A beetle would save much time and energy if it could
discriminate between the host and the nonhost and determine the suitability of the host
by olfactory means from a distance without the need to land. Sometimes host and
nonhost trees are adjacent and the beetle could land by mistake on the nonhost;
however, short-range olfactory cues might indicate the inappropriateness of the
nonhost bark substrate (Byers et al. 1998, 2000). If the beetle still could not decide,
boring a short distance into the nonhost might reveal the lack of feeding stimulants or
the presence of deterrents causing the beetle to leave (Elkinton and Wood 1980; Byers
et al. 2000).
9. AVOIDANCE OF COMPETITION AND UNSUITABLE AREAS OF HOSTS
Verbenone is found in relatively large amounts (µg) in male hindguts of several bark
beetles of North America, D. frontalis, D. brevicomis, D. ponderosae, and D.
pseudotsugae (Renwick and Vité 1968; Rudinsky et al. 1974; Byers et al. 1984; Pierce
et al. 1987) but in low amounts (ng) in T. piniperdaa (Lanne et al. 1987), or essentially
absent in I. paraconfusus, I. typographus, and P. chalcographus (Byers 1983b;
Birgersson et al. 1984, 1990). Verbenone (Fig. 13) inhibits the attraction of these
beetles to their respective aggregation pheromones (Renwick and Vité 1969, 1970;
Byers and Wood 1980; Bakke 1981; Byers et al. 1989c; Byers 1993b).
Exposure of male and female D. brevicomis to (+)- and (-)- enantiomers of α-pinene
for several hours caused them to produce large amounts of (+)- and (-)-trans-verbenol
in their hindguts (Fig. 13, Byers 1983c). However, the biosynthesis of verbenone in
these beetles was not affected by exposure to α-pinene enantiomers, even though
verbenone is structurally similar to α-pinene (Fig. 5) and is found in males landing on
trees (Renwick and Vité 1968, 1970; Byers et al. 1984). The (-)-enantiomer of trans-
verbenol (Fig. 13) inhibits female D. brevicomis from entering holes and may serve as
a signal to arriving females that they should avoid areas colonized by conspecifics
(Byers 1983c).
Both verbenone and trans-verbenol are produced by D. brevicomis beetles in the
greatest amounts early in colonization so it was suggested that they play a role in
reducing intraspecific competition (Byers et al. 1984), as well as interspecific
competition with I. paraconfusus (Byers and Wood 1980). However, verbenone (and
possibly trans-verbenol) are also produced increasingly in ageing logs infested by bark
beetles (Birgersson and Bergström 1989; Byers et al. 1989c). A common bacterium,
Bacillus cereus, also isolated from I. paraconfusus, can make cis- and trans-verbenol
from α-pinene (Brand et al. 1975). Several yeasts from I. typographus can interconvert
the verbenols, and when grown in a phloem medium they produced the oxygenated
monoterpenes α-terpineol, borneol, myrtenol, terpenene-4-ol and trans-pinocarveol,
compounds also shown to be released increasingly from bark beetle holes with age of
attack (Leufvén et al. 1984, 1988; Birgersson and Bergström 1989). A mycangial
fungus grown in culture media converted alcohol products of α-pinene to verbenone,
the end product (Brand et al. 1976). These microorganisms are introduced by bark
beetles during colonization and after buildup may release verbenone, thus signaling to
flying beetles that remaining in these bark substrates would entail competition with
established bark beetle colonies. Recently, verbenone was found in twigs of eastern
110 J.A. BYERS
Figure 13. Pheromone components of bark beetles. Key: aggregation component (a), inhibitor
of aggregation (i). Row 1: 2-methyl-3-buten-2-ol (a, I. typographus); 3-methyl-3-buten-1-ol (a, I.
cembrae), 4-methyl-3-heptanol (a, S. multistriatus). Row 2: sulcatol (a, G. sulcatus, G. retusus);
seudenol (D. pseudotsugae, D. rufipennis, D. simplex); MCH (i, D. pseudotsugae); lanierone (a,
I. pini). Row 3: cis-verbenol (a, I. paraconfusus, I. typographus, I. calligraphus);
g trans-verbenol
(a, D. ponderosae, T. minor; i, D. brevicomis);
i verbenone (i, Dendroctonus); chalcogran (a,
Pityogenes). Row 4: ipsenol (a, Pityokteines curvidens, and many Ips: e.g. I. paraconfusus, I.
grandicollis), ipsdienol (a, many Ips, e.g. I. paraconfusus, I. duplicatus, I. pini, I. calligraphus, I.
avulsus); amitinol (a, I. amitinus); E-myrcenol (a, a I. duplicatus). Row 5: (+)-exo-brevicomin (a,
D. brevicomis, Dryocoetes); (-)-exo-brevicomin (a, Dryocoetes); methyl decadienoate (P.
chalcographus). Row 6: frontalin (a, many Dendroctonus);
r endo-brevicomin (i, D. frontalis);
multistriatin (a, S. multistriatus); lineatin (a, T. lineatum). References to above pheromones are
in reviews by Borden (1982) and Byers (1989a), and the following (Bakke 1975; Baker et al.
1977; Lanne et al. 1987; Borden et al. 1987; Byers et al. 1989b, 1990a, b; Teale et al. 1991;
Camacho et al. 1993).
cottonwood, Populus deltoids (personal comm. from Carlos Flechtmann, in Huber et

al. 1999).
Myrcene and α-pinene from host trees can be used as precursors of pheromones
and allomones in some species of conifer-feeding bark beetles. However, recent
research has shown that the majority of ipsdienol and ipsenol in Ips bark beetles results
from de novo biosynthesis from simple acetate and mevalonate precursors (Seybold
and Tittiger 2003). The later steps in the isoprenoid pathway lead to geranyl
diphosphate and myrcene before being stereoslectively, and species-specifically,
converted to various enantiomers of myrcene-like alcohols (e.g., ipsdienol, ipsenol, E-
myrcenol, amitinol) that are pheromone components (Seybold et al. 2000; Seybold
and Tittiger 2003). D. brevicomis, I. paraconfusus and I. pinii occur sympatrically in
California and Oregon and compete for ponderosa pine bark. Myrcene vapors can be
converted only by male D. brevicomis to (+)-ipsdienol (Fig. 13), also a pheromone
component of its competitor I. paraconfusus (Hughes 1973; Byers 1982). (+)-
Ipsdienol inhibits response of both D. brevicomis and I. pinii to their synthetic
aggregation pheromones (Birch et al. 1980a; Lanier et al. 1980; Byers 1982). In
Europe, ipsdienol, a pheromone component of I. duplicatus could act as an allomone
to inhibit response of I. typographus (Byers et al. 1990b; Schlyter et al. 1992). Mated
males of I. typographus produce small amounts of ipsdienol and ipsenol during
colonization that might function in avoiding competition (Birgersson et al. 1984;
Birgersson and Leufvén 1988; Birgersson et al. 1988). Although, ipsdienol was
previously thought to be an aggregation pheromone component of I. typographus
(Bakke et al. 1977), other studies have shown the compound to be either inactive or
inhibit attraction of these beetles to cis-verbenol and methyl butenol, the most potent
components (Schlyter et al. 1987b, c). Also, ipsdienol was not found in single males in
a nuptial chamber, while it was detected in small amounts in later phases of attack
when males had been joined by one or more females (Birgersson et al. 1988).
P. chalcographus of Europe (Fig. 14) produces a two- component aggregation
pheromone consisting of chalcogran and methyl decadienoate (Francke et al. 1977;
Byers et al. 1988, 1990a). Both chalcogran and methyl decadienoate (Fig. 13) cause I.
typographus to avoid landing on traps releasing their aggregation pheromone
components (cis-verbenol and methyl butenol) (Byers 1993b). However, P.
chalcographus attraction to its pheromone was not inhibited by pheromone
components of I. typographus even though the latter, and larger, beetle wins in
competitive situations when both species aattack simultaneously (Byers, unpublished).
112 J.A. BYERS
Figure 14. P. chalcographus searching for a boring site on the bark of Norway spruce
However, if P. chalcographus precedes I. typographus on the host by just a few

days then the former species will win inn competitive situations (Byers, unpublished).
Verbenone is increasingly released as colonized areas of I. typographus age
(Birgersson and Bergström 1989) and the compound is inhibitory to P. chalcographus
(Byers 1993b), as well as to I. typographus (Bakke 1981; Schlyter et al. 1989).
10. AVOIDANCE OF DECAYING OR FULLY COLONIZED HOSTS

As mentioned above, some microorganisms isolated from bark beetles or their gallery
walls, may convert α-pinene to cis- and trans-verbenol, or trans-verbenol to
verbenone. It was proposed that this process may account for termination of attack
(Brand et al. 1976). Verbenone is increasingly released from ageing logs of spruce and
pine colonized by bark beetles ((I. typographus, Birgersson and Bergström 1989; T.
piniperda, Byers et al. 1989c), possibly due to the activity of microorganisms. Byers
(1989a, b) speculated that if verbenone is a consistent signal of microbial activity in
decaying hosts, then bark beetle species may have evolved an avoidance to this
compound (a kairomone) in order to avoid unsuitable hosts. The bark beetle then could
have evolved to produce verbenone as a pheromone that reduced intraspecific
competition, since the avoidance response was already existent. Other bark beetle
species might then evolve to avoid species that produced verbenone (as an allomone),
and so avoid interspecific competition. Sympatric species on the same host might
coevolve responses to, and/or production of, verbenone since the chemical could serve
as a signal for several types of beneficial information (kairomone, pheromone, and
allomone).
Verbenone was reported to inhibit pheromone responses of over 10 species of bark
beetle (Borden 1997). However, verbenone does not always inhibit bark beetles. For
example, H. palliatus feeds in unhealthy or dying Scots pines that release verbenone
(Byers et al. 1989c), and the beetle's attraction to ethanol was not inhibited by
verbenone (Byers 1992a). Angiosperm trees in a state of decay may not release
verbenone since they probably do not have α-pinene, thus T. domesticum could evolve
to avoid degrading nonhost pines by avoiding verbenone (Byers 1992a). Another bark
beetle, P. bidentatus, attacks diseased limbs of Scots pine
i and is not affected by release
rates of verbenone, which inhibit more aggressive bark beetles. This is probably
because verbenone is expected to be present from the diseased host limbs (Byers et al.
2000). In the case of conifer bark beetles, Verbenone is increasingly implicated as a
general sign of host unsuitability in conifer-killing bark beetles (due to microbial
decay or competition with bark beetles). Therefore, it is paradoxical
a that conifers have
not evolved the capacity to convert α-pinene, which they have in abundance, to
verbenone in order to repel aggressive bark beetles.
Ethanol, also, sometimes reduces response to attractive baits. Klimetzek et al.
(1986) tested different release rates of ethanol (24 to 125 mg/day) with an unreported
release rate of α-pinene and terpinolene and found that the higher releases of ethanol
inhibited attraction of T. piniperda. However, a control with either ethanol alone or
terpenes alone was not reported. Schroeder (1988) increased the release of ethanol in
five dosages over an even wider range from 0 to 50 g/day in combination with a 240-
mg/day α-pinene release. In this case, the attraction of T. piniperda a declined linearly
with the logarithm of ethanol release, which is in conflict with the theory of Vité et al.
(1986) that ethanol was synergistic with monoterpenes.
Schroeder and Lindelöw (1989) provided the first evidence that could integrate the
disparate results. They found that high release rates of α-pinene were most attractive
to beetles and that ethanol releases alone from 0 to 3 g/day were barely attractive. At a
low release rate of α-pinene (2.4 or 22 mg/day), and thus low attraction, lower release
rates of ethanol from 0 to 3 g/day had a synergistic effect when combined with α-
pinene in attracting beetles (Schroeder and Lindelöw 1989). Their results are
supported by Byers (1992a); i.e., a weak enhancement of attraction by ethanol at low
release rates when blended with three host monoterpenes, but no observable effect of
ethanol on the greater attraction to higher release rates of monoterpenes.
Ethanol released at even higher rates, 120 mg/day (Klimetzek et al. 1986) or 50
g/day (Schroeder 1988), inhibited the response of T. piniperda a to monoterpenes.
Therefore, the beetle could find diseased, but physically uninjured, trees by a weak
response to a synergism between low monoterpene r release rates and moderate ethanol
rates - the hypothesis of Vité et al. (1986). Beetles would occasionally penetrate these
trees, and if low in resistance would permit continued feeding. Resinosis and
monoterpene release from the entrance holes would elicit increased numbers of beetles
joining in a mass attack. Injured trees with wound oleoresin, and trees under attack
with "pitch tubes", would have a higher monoterpene release and attract the greatest
numbers of beetles, according to Byers et al. (1985). Trees with high ethanol release
rates would indicate a tree in advanced decayy and unsuitable for reproduction, and thus
to be avoided, as theorized by Klimetzek et al. (1986). High monoterpene releases
from trees (freshly wounded and not dead) would not naturally coincide with high
ethanol release rates (presumably during decay after death). In addition, other
compounds such as verbenone from decaying hosts would inhibit response to
114 J.A. BYERS
monoterpenes from unsuitable hosts (discussed in the next part). These studies
emphasize the need for releasing semiochemicals at known rates during tests in the
field. In addition, measurements of the natural release rates of ethanol and
monoterpenes from various host and nonhost substrates are necessary for further
understanding of bark beetle chemical ecology.
11. AVOIDANCE OF NONHOSTS

According to studies discussed previously, bark beetles find their host tree by
attraction to host volatiles (or after random
a landing and probing), as well as by
avoiding chemicals from colonized hosts or decaying hosts. However, it is becoming
increasingly apparent that many beetles avoid nonhost trees due to specific odors. It is
inherently more difficult to isolate repellents and inhibitors used in avoidance behavior
than to isolate attractants since tests of avoidance require one to first isolate the
attractive host odors and then present these with and without the possibly inhibitory
nonhost odors. Several studies indicate that at least some species of bark beetle avoid
nonhost volatiles during their search for host trees. The attraction of both T. piniperda
and H. palliatus to ethanol (1-6 g/day) was reduced by odors from cut logs of nonhost
trees, birch, Betula pendula, and aspen, Populus tremula a (Schroeder 1992). In future
experiments, host logs (or monoterpenes aand ethanol) should be tested instead of
ethanol alone to simulate the host tree. Dickens et al. (1992) reduced the attraction
response of D. frontalis, I. grandicollis and I. avulsus to aggregation pheromone by
releasing the green-leaf volatiles, 1-hexanol and hexanal. T. domesticum colonizes
wood of deciduous trees (e.g. Fagus sylvatica, Quercus spp. Betulaa spp.) and is known
to be attracted to ethanol (Magema et al. 1982; Paiva and Kiesel 1985). Monoterpenes
of Scots pine and verbenone (from decaying conifers) reduced d response of this species
to ethanol (Byers 1992a) and would provide a mechanism for avoiding nonhosts and
unsuitable colonization areas. This also is valid for the hardwood-breeding species
Anisandrus disparr (Schroeder and Lindelöw 1989).
Recently, the spruce bark beetles Ips typographus and Pityogenes chalcographus
were shown to avoid volatiles of nonhost birch trees (both from bark and leaves, Fig.
15), which suggests the possibility that beetles may not enter areas of primarily birch
(Byers et al. 1998). However, it is more certain that the beetle would leave a birch tree
after landing due to a relatively high concentration of repellent nonhost volatiles at the
surface of the bark.
There is increasing evidence that aggregation responses to semiochemicals by
conifer-infesting bark beetles in several genera are reduced by volatiles from nonhost
angiosperm trees (e.g. Betula, Populus, Acer) r (Dickens et al. 1992; Schroeder 1992;
Schlyter et al. 1995; Wilson et al. 1996; Guerrero et al. 1997; Borden et al. 1997,
1998; Deglow and Borden 1998; Byers et al. 1998, 2000; Poland et al. 1998; Zhang et
al. 1999a, b, 2000, 2001; Huber et al. 1999, 2000, 2001; Huber and Borden 2001a, b;
Poland and Haack 2000; Schlyter et al. 2000; Zhang 2003; Zhang and Schlyter 2003).
These studies have found that some of the most important nonhost angiosperm
Z
compounds are (Z)-3-hexen-1-ol, (E)-2-hexen-1-ol, and 1-hexanol mostly from leaves,
as well as trans-conophthorin from bark.
Figure 15. Pityogenes chalcographus were induced to land on birch trees by baits of
aggregation pheromone but the individuals did not stay more than about 2 minutes due to
odors from the bark (probably 1-hexanol,
l trans-conophthorin, and other unidentified
compounds, Byers et al. 1998).
Volatiles from leaves or bark of nonhosts birch ((Betula pendula) and Norway
spruce (Picea
( abies) also dramatically reduced the attraction of the bark beetle,
Pityogenes bidentatus, to their aggregation pheromone components (cis-verbenol and
grandisol) in the field. Surprisingly, odors from either the needles or bark of the host
Scots pine, Pinus sylvestris, similarly inhibited attraction. Monoterpenes of pine and
spruce (α-pinene, ß-pinene, terpinolene, and 3-carene), as well as ethanol, chalcogran
Z
and some nonhost green leaf alcohols [(Z)-3-hexen-1-ol, (E)-2-hexen-1-ol, and 1-
hexanol], also reduced catches. Collections of volatiles from the field-tested plant
tissues indicated they released monoterpenes in amounts similar to the synthetics that
inhibited responses. The varied plant and insect sources of these inhibitory compounds
indicate that P. bidentatus bark beetles have evolved several strategies to increase their
fitness by avoiding nonhost and unsuitable host trees in a complex olfactory landscape.
12. FEEDING STIMULANTS AND DETERRENTS

Presumably, a beetle must not only determine that the bark underneath is the proper
host and is suitable for reproduction, but it must also judge potential competition by
whether nearby areas have bark beetles beginning their attacks. Many species of bark
beetle bore their entrance holes in a spaced or uniform pattern, indicating the beetles
try to avoid competition (Byers 1984, 1992c, 1996c). In some cases, the beetle will
bore through the outer bark, regardless of the host, until it encounters the phloem. For
example, I. paraconfusus will bore through the outer bark of the nonhost white fir,
Abies concolor, as readily as through bark of the host ponderosa pine. However, the
116 J.A. BYERS
beetle only bores about 1 mm in white fir phloem and then leaves (Elkinton and Wood
1980). In the initial boring phase, gustatory y (and possibly olfactory) stimulants,
deterrents, and physiological factors are considered in a decision whether to continue
feeding and excavating the gallery. The beetle probably can determine whether the
host tissue is of good quality in terms of nutritional
t and moisture factors (Webb and
Franklin 1978). The phloem of ponderosa pine, sugar pine ((P. lambertiana), Douglas-
fir ((Pseudotsuga menziesii), red fir ((Abies magnifica), and several other conifers
contain about equal amounts of glucose, fructose and sucrose (Smith and Zavarin
1960). Bark beetles have been induced to feed or lay eggs on several diets, but the
most successful diets contained some percentage of host (usually phloem) tissue
(Jones and Brindley 1970; Richeson et al. 1970; Whitney and Spanier 1982; Conn et
al. 1984; Byers and Wood 1981b), indicating the presence off feeding or ovipositional
stimulants. In experiments to introduce antibiotics, sucrose was found to increase
feeding by I. paraconfusus in powdered cellulose diets (Byers and Wood 1981b).
Few studies have attempted to isolate feeding stimulants in conifer-feeding bark
beetles, and none have isolated specific compounds. Elkinton et al. (1981) extracted
ponderosa pine phloem successively with diethyl ether (partitioned
r with water), water
and then methanol, and added these extracts to powdered cellulose diets. I.
paraconfusus beetles were then given a choice between a control diet and a diet with
extract. The diet with the ether extract did not cause beetles to remain longer and there
was no preferential boring, but the extract did cause more feeding compared to the
control. The water partition of the ether extract only caused beetles to remain longer.
The water extract elicited more boring and feeding, while the methanol extract was
inactive since feeding stimulants had already d been extracted by the ether and water
treatments. These results indicate that several compounds function in gustatory
preferences. Solvent (methanol-water-benzene) extracts of lodgepole pine ((Pinus
contorta) bark were absorbed by tissue paper and shown to induce feeding by D.
ponderosae (Raffa and Berryman 1982). The benzene fraction induced biting but not
feeding while the polar fraction (water-methanol) caused continued feeding.
Differences in feeding preferences for bark k extracts varied widely between trees, but
these differences could not be attributed to amounts of 13 monoterpenes as determined
by gas chromatography (GC). Also, extracts of trees judged resistant, because beetles
that had been forced to attack in cages either refused orr discontinued attack, were as
stimulatory to feeding beetles as those from susceptible trees. In contrast, Hynum and
Berryman (1980) found greater feeding preferences for bark extracts of susceptible
lodgepole pines than for comparable extracts of resistant lodgepole pine. However, the
susceptible trees had been killed by the beetles before solvent extraction, which might
have allowed microorganisms to produce additional feeding stimulants. White (1981)
also found differences in gustatory deterrent and stimulatory properties of bark extracts
from different trees of loblolly pine, P. taeda.
Most work on feeding stimulants and deterrents in beetles of deciduous trees
involves the elm bark beetle, Scolytus multistriatus. Vanillin and syringaldehyde are
short-range attractants inducing feeding in S. multistriatus (Meyer and Norris 1967b).
Feeding stimulants were isolated from the bark of American elm, Ulmus americana, of
which one was partially identified as a pentacyclic triterpene (Baker and Norris 1967).
Later some lignin intermediates and phenolics were suggested (Meyer and Norris
1974). Doskotch et al. (1973) succeeded in identifying another feeding stimulant in
elm bark as a catechin xyloside. A tritiated catechol-feeding stimulant was shown to
penetrate the gustatory receptor of S. multistriatus (Borg and Norris 1971). Scolytus
rugulosus is stimulated to feed in fruit trees by several phenolic compounds (Chararas
et al. 1982).
Scolytus multistriatus was induced to feed on sucrose pith disks when volatiles
from benzene extracts of bark of nonhost trees (Eastern cottonwood, Populus
deltoides, and yellow buckeye, Aesculus octandra) were placed 7 mm away (Baker
and Norris 1968). However, these nonhost trees were not fed upon since they
contained nonvolatile feeding deterrents, as shown by lowered feeding on a mixture of
host and nonhost extracts compared to host extracts. S. multistriatus beetles do not
attack the nonhost hickory, C. ovata, due to the presence of juglone
(5-hydroxy-1,4-napthoquinone), a feeding deterrent (Gilbert et al. 1967). Elm tree
tissue infected by the fungus Phomopsis oblonga a is avoided by S. multistriatus due to
several complex feeding deterrents. These include oblongolide (isomer of
dimethylnapthofuranone), a norsesquiterpene lactone, two tiglic esters of
5,6-dihydro-5-hydroxy-2-pyrones, nectriapyrone, 4-hydroxyphenylethanol,
5-methylmellein as well as acids of 2-furoic, orsellinic, 3-nitropropanoic, and
mellein-5-carboxylic (Begley and Grove 1985; Claydon et al. 1985).
Diterpene acids (e.g., abietic, levopimaric, neoabietic and palustric acids) have
been isolated from ponderosa pine oleoresin (Anderson et al. 1969; Himejima et al.
1992) and these are known to be antifeedants against aphids and sawflies (Wagner et
al. 1983; Schuh and Benjamin 1984; Rose et al. 1981). However, these compounds
have not been tested on bark beetles. Tannins, phenolics and terpenoids that can inhibit
feeding or digestion in other insects (Berenbaum and Isman 1989) could also affect
bark beetles. Ponderosa pine bark extracted first with ether yields behenic and
lignoceric acids, fatty alcohols, resin acids, and flavonols (quercetin and myricetin,
pinoquercetin, pinomyricetin and dihydroquercetin). A subsequent acetone extract
contains tannins and phlobaphenes, while a third hot-water extract has tannin (6-11 %
dry weight of bark) and carbohydrates (Anderson 1962; Anderson et al. 1969). Many
of these compounds are found only in the outer bark and although they may be
important in deterring nonhost bark beetles, at least the host-adapted I. paraconfusus
does not eat the outer bark (Elkinton and Wood 1980). However, host compounds of
lower volatility at close range may be important in deterring attacks after landing. For
example, Byers et al. (1998, 2000) found that P. chalcographus and P. bidentatus
would not attack non-host birch or spruce, respectively, after briefly landing in
response to pheromone baits (Fig. 13).
13. MANAGEMENT OF BARK BEETLES USING SEMIOCHEMICALS

Pheromones have been used in the field to disrupt mate finding in moths (Hodges et
al. 1984; Zvirgzdins et al. 1984; Flint and Merkle 1984; Campion et al. 1989), beetles
(Villavaso and McGovern 1981; Villavaso 1982), and flies (Jones et al. 1982). In most
cases, relatively large quantities of pheromone (consisting of several pheromone
118 J.A. BYERS
components) are more or less evenly distributed throughout the field to adapt
(overload) sensory receptors or habituate behavioral response (`confusion') or to
exhaust the individuals in orientation attempts (i.e. “wild-goose chases”). The best
successes so far have involved straight-chain olefinic acetates, alcohols, and aldehydes
of moths (Baker 1989; Byers 2002).
Bark beetles that colonize forest trees may present problems for disruption
techniques for several reasons, one is that their pheromone components, usually
oxygenated monoterpenes, are more volatile than moth straight-chain hydrocarbons
(Byers 1989a). More important perhaps is that compared to moths even larger
quantities are expected to be required for disruption of bark beetles since the latter
individuals generally release higher rates (ng to µg/h) of pheromone components than
moths (pg to ng/h) (Browne et al. 1979; Schlyter et al. 1987a; Birgersson and
Bergström 1989; Byers et al. 1990a, b; Ramaswamy and Cardé 1984; Du et al. 1987).
Furthermore, even higher quantities of synthetic pheromone are required to compete
with pest bark beetles that typically release semiochemicals in large aggregations on
their host tree as compared to individual female moths. Possibly because of these
reasons, as well as the fact that both sexes are attracted by pheromone, several
attempts to control bark beetles have used the mass-trapping method. This method
employs traps, either sticky-screen (Browne 1978) or cylinder with holes/barrier type
(Bakke 1989), baited with synthetic pheromone components. Traps releasing
pheromone components have been used in control programs to lure other pest insects
such as moths to their death (Haniotakis et al. 1991; Sternlicht et al. 1990).
Previous theoretical attempts at determining the effectiveness of pheromone mass
trapping have used population dynamic models (Knipling and McGuire 1966; Roelofs
et al. 1970; Beroza and Knipling 1972; Nakasuji u and Fujita 1980; Nakamura 1982;
Barclay 1984; Fisher et al. 1985; Barclay 1988; Barclay and Li 1991). These models
are mathematically complex and make several assumptions about beetle survival and
mating rates, as well as attraction rates to pheromone traps, which limits their
application. There have been no models where ìnsects' are moved in `real' time and
space in relation to traps of specific dimensions and positions, although two-
dimensional models of ‘correlated random walks’ are probably close to reality (Byers
1993a, 1996a, b, 1999, 2000, 2001).
The first major attempt to control bark beetle populations using pheromone-baited
traps was done in 1970 in California (Bedard et al. 1979; Wood 1980; DeMars et al.
1980). Large (1 x 2 m) sticky screens baited with exo-brevicomin and frontalin,
pheromone components of the western pine beetle, Dendroctonus brevicomis
(Silverstein et al. 1968; Kinzer et al. 1969), plus the host monoterpene, myrcene
(Bedard et al. 1969), were placed in ponderosa pine forests at Bass Lake, California. In
m2 each, 66 pheromone traps were deployed in a grid of about 161 m
four plots of 1.3 km
spacing. Over a million beetles were caught and the test appeared to be successful
since the number of trees killed by the beetle declined to 10% the pre-treatment level
for several years (Bedard et al. 1979; Wood 1980; DeMars et al. 1980).
Norway and Sweden have extensive conifer forests, and in the 1970's a major
outbreak of the European spruce engraver, I. typographus, devastated many areas
(Austarå et al. 1984). Since the pheromone of this beetle had recentlyy been identified
as a mixture of 2-methyl-3-buten-2-ol and (1S,4S,5S)- S cis-verbenol (Bakke et al. 1977),

an extensive mass-trapping control program was initiated in 1979 and may have led to
the decline of outbreaks after 1980 (Bakke 1985, 1989; Vité 1989). Several other
European studies have reported successful control of bark beetles with the intensive
use of pheromone-baited traps (Vrkoc 1989; Richter 1991; Jakus 1998).
These pioneering studies of mass trapping using pheromones did have some
deficiencies. Many of these studies lacked appropriate
a controls or check plots so it is
not possible to determine the success of the control programs. Also, a combination of
experience and intuition led to subjective estimates as to the level of trapping and the
pheromone release rate ultimately employed for control of the population. Certainly,
these questions are complex and it is not surprising that they were not solved entirely.
Models that employ various parameters can help to understand mass trapping. The
parameters include types of pheromone traps and spacings, bait strengths, and
treatment durations in conjunction with different population densities and host stand
conditions. This is a task with nearly unlimited possibilities. However, the models will
not be a substitute for experimentation with some of the parameters in the field.
Weber (1987) was critical of pheromone trapping of bark beetles for control since
he calculated that enough beetles would remain untrapped to then colonize susceptible
hosts and replenish the population
a density due to an absence of competition. This
assessment is conjectural since trapping experiments with different traps and
pheromone dosages were not done. Also, the complementary effects of other forest
management practices, such as removal of slash and infested trees to reduce
populations, were not considered. The consequences of population reduction to
densities below the threshold required to overcome tree resistance by means of a mass
attack were also not considered (Berryman and Stenseth 1989; Berryman et al. 1989).
In contrast, some models (Byers 1993a, 1996a) indicate that insect populations can
potentially be drastically reduced with a small number of traps with an effective radius
that seems smaller than what one might intuitively expect for pheromone baits.
However, whether this population reduction is sufficient to affect natural matings and
population levels over several generations is still an open question.
In many past control programs that used pheromone trapping, there has been the
problem of finding control areas to determine whether the treatment has been
effective. However, several monitor traps placed inside the control t area (or even the
control traps themselves) will indicate the population densityy and the progress of the
control program. If no more insects are being caught, then obviously the control is a
success, unless the flight period is over. This can be determined by monitoring traps
placed in untreated areas, some distance away, but still within the same general
biotope and climatic regime. Usually only one beetle or pair of bark beetles begin
attack of a tree and at this time pheromone release is relatively low compared to a few
days later when thousands of beetles participate in the mass attack. Thus, it seems
advantageous to initiate mass trapping before beetles swarm in the spring and have
time to build aggregations that can compete with traps for attraction of dispersing
beetles. The population levels need only be reduced below the thresholds required to
kill trees. In moths, reproduction can occur despite high trapping efficiency suggested
120 J.A. BYERS
by the model because male moths may mate with females before being trapped
(Roelofs et al. 1970).
There are several variables that can influence the trapping of the population so it
does not follow the predictions based on simulation models or iterative equations. For
example, the `flight' speed usedd in models (2 m/s, Byers et al. 1989a) may be more
than the speed observed for flying or wind-blown insects since they often stop to rest
or feed (Byers 1996a). Also, in the case of bark
a beetles, there can be host volatiles that
attract the beetles during their swarming flight, or trees under colonization where
aggregation pheromones are released (Byers 1989a). Several studies have indicated
that as the density of calling female moths increase, the catches on pheromone-baited
traps increase relatively less or may decline, probably due to competition between the
natural and synthetic sources (Raulston et al. 1979; Nakamura 1982; Witz et al. 1992).
Traps can also be overloaded with caught insects, and synthetic pheromone release
rates can diminish over time, which will cause catches in nature to differ from model
predictions. Pheromone release rates can decrease (and the effective pheromone trap
radius) due to compound degradation and inn other cases due to exponential decline
from substrates (e.g. rubber septa). Methyl decadienoate, a pheromone component of
the bark beetle Pityogenes chalcographus, is especially sensitive to sunlight, and
attraction rates can be halved in a few hours unless the compound is shaded. In
models, the shape of pheromone plumes emanating from traps has been transformed to
the EAR, which also reduces the correspondence between reality (some type of
Gaussian time-averaged plume depending on the wind) and the models (a circle).
Much research in the practical area is needed, unfortunately this is expensive and time
and labor consuming.
14. ECOLOGICAL ASPECTS AND CONCLUDING REMARKS

Bark beetles are a keystone species, meaning that they are evolutionarily and
historically a dominant component of the natural forest ecosystem. Without bark
beetles, many thousands of microbial, nematode, mite, and insect species would
become extinct since they rely on bark beetles to create a habitat for them (Dahlsten
and Stephen 1974). The aggressive interactions between bark beetles and trees also
must affect population genetics and evolution. Trees and parts of trees (shoots, cones,
limbs) are killed when eaten by bark beetles or by fungi introduced during feeding so
there is certainly a severe selection pressure on trees to evolve resistance mechanisms,
which they have, but bark beetles have also evolved counter-resistance mechanisms
(Byers 1995). This so-called evolutionary arms r race continues, especially with man's
activities introducing new species of tree and a bark beetle. In spite of a general
resistance having evolved in conifers, older, weak and unhealthy trees are removed by
bark beetles, and microbial diseases, which greatly influences the age and species
structure of the forest.
The main reason bark beetles have been studiedt so extensively is that they are
perceived as pests that damage forests. Certainly at outbreak levels, bark beetles kill
vast areas of conifer forests, which drastically affect the ecology and species
composition for a considerable time. In forest plantations used only for the production
of fiber, bark beetles are indeed pests. In forests with residential tracts, bark beetles are
a threat to the desired stability of old-growth stands. In wilderness areas and
recreational forests, bark beetles may be tolerated as part of the natural ecosystem. In
fact, bark beetles are a keystone species that naturally fluctuates in abundance as the
forest ages and succession processes occur. Many forests are designated as multi-use,
meaning that they are for recreation and for timber production. Obviously some uses
preclude other uses, or are at least in conflict. There often must be a compromise
between producing the most fiber per unit area (short term interest) and the
maintenance of natural forest biodiversity (long term interest). Over the long term
(longer than a human’s lifetime), most forest ecosystems require disturbances that
remove old trees and open the land to a succession of plant and animal species guilds.
Either bark beetles or fire, or both, are well known to carry out this natural long-term
cycling function. Man, however, usually does not appreciate these perturbative cycles
that progress over many decades. The discussion about the role of bark beetles, fire,
and overuse of forests by mankind will continue for many years to come, but research
in all these areas will help to understand
a how to better utilize and enjoy nature.
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Chapter 9
HOST RESISTANCE TO BARK BEETLES AND ITS

VARIATIONS
F. LIEUTIER
Université d’Orléans, rue de Chartres, B.P. 6759, F-45067 Orléans Cedex, France
1. INTRODUCTION AND DEFINITIONS

As with all other living organisms, trees are able to defend themselves against
attacks and, during their colonization process, bark beetles face and must overcome
a diversity of resistance mechanisms. Freshly felled trees, which pose very little
resistance to bark beetles, represent an easily accessible source of food, while the
very high resistance level of healthy trees makes them relatively inaccessible. By
conditioning the quantity of available food, tree resistance is thus the real key-factor
in the population dynamics of bark beetles that attack living trees. Consequently,
two aspects will be first considered in this chapter: the tree side encompassing
resistance mechanisms and their effects on bark
a beetles; the beetle side including the
strategies used by the insect to overcome tree resistance and to succeed in
establishing and breeding successfully.
The concepts of defence and resistance must be defined first. Following Karban
and Baldwin (1997), one can consider that they correspond to two complementary
“points of view” of the same phenomenon. Defence is considered from a tree’s
perspective and refers to the necessity to stop beetle attacks to ensure survival. It
also often supposes active mechanisms induced in response to attacks. Resistance
refers to mechanisms hampering beetle establishment in its host and can involve
both active induced and passive non-induced phenomena.
In a broad sense, resistance to bark beetles involves both mechanisms that act at
a distance through chemical communication, before the aggressor reaches the tree,
and mechanisms that act after physical contact between the host and its aggressor
has been established. Since chemical communication between trees and bark beetles
is largely developed elsewhere in this volume (Byers, chapter 8), this chapter
concentrates on a strict definition of tree resistance and is limited to what happens
after beetles have reached their host trees. In addition, because most bark beetle
damage on living trees largely concerns conifers, very few data are available
135
135–180.
© 2007 Springer.
136 F. LIEUTIER
regarding resistance of hardwood trees to these insects. Thus this chapter is

organized by referring to European conifers, mainly Norway spruce Picea abies and
Scots pine Pinus sylvestris, but will make comparisons with studies carried out on
species living outside Europe. First the different levels of tree resistance and the
general mechanisms of induced defences are presented, followed by a discussion on
the role and efficiency of these systems. Next, the beetle side will be considered by
presenting beetle behavior when encountering tree resistance. A discussion on the
effect of host resistance on bark beetle population dynamics will follow. Then, the
variations in tree resistance depending on genetic and environmental factors will be
considered in some detail. The possibilities of using tree resistance for bark beetle
management will be only mentioned because it is largely developed previously, and
the conclusion will focus on strengths and gaps in our knowledge of the
relationships between tree resistance and the European bark beetle species.
2. NATURE AND CHARACTERISTICS OF THE TREE RESISTANCE

SYSTEMS
Tree resistance systems have been presented in detail recently (Lieutier, 2002) and
only a summary is provided here, focusing on the European specificities and results.
2.1. Levels / systems of tree resistance

Classically, the systems of tree resistance to attacks are separated into two groups
according to the period of investment of the energy resources in defence. In
preformed resistance, resources are invested in defence before beetle attacks,
whereas they are mobilized only in response to aggression in the case of the induced
resistance. In this latter situation, there is gene activation by the aggressors,
followed by an increase in the syntheses of secondary metabolites involved in
defence, often accompanied by neosyntheses and building of new structures.
Secondary metabolites and histological structures also often occur in preformed
resistance but they are produced before beetle attack.
2.1.1. Systems of preformed resistance

These systems represent the first line of resistance met by the aggressors (beetle or
their associated fungi). Depending on the need for activation, two kinds of
preformed defences can be distinguished (Karban and Balwin, 1997). The
“constitutive defences” are active in the same state as they were before aggression.
As an example, bark thickness can often be responsible for the failure of attacks by
beetle species that localize attacks preferably in the upper part of the tree. Stone cell
masses are lignin patches that can be ffound in large quantities in the phloem of
Norway and Sitka spruce Picea sitchensis, and have been demonstrated to play a
role in arresting attacks by Dendroctonus micans (Wainhouse et al., 1990, 1997,
1998a). Low phloem moisture content can counteract oviposition and development
of this species in Norway spruce (Storer and Speight, 1996). Calcium oxalate
crystals, in combination with fiber rows, have also been suggested to contribute in
HOST RESISTANCE TO BARK BEETLES 137
limiting bark beetle attacks in the phloem of Pinaceae (Hudgins et al., 2003b). The
“preformed induced defences” are represented by two main anatomical systems
containing secondary metabolites. Blisters and resin canals store terpene
compounds (Johnson and Croteau, 1987), while specialized phloem parenchyma
cells store phenolic compounds (Franceschi et al., 1998). Wounding these systems
is necessary for their content to be released and to affect the attacking beetles.
Resin canal systems are largely developed in the genera without blisters, such as
in Europe, Pinus and, to a lesser extent, Larix and Picea, while blisters are found
mainly in Abies and Cedrus, which do not have resin canals. Typically, the resin
duct system is a network of interconnected vertical (in the sapwood) and radial (in
both the sapwood and the phloem) canals around which the cells responsible for
resin synthesis are located. In case of wounding, resin is immediately released from
this system and can cause failure of attacks when its flow is abundant. This flow,
however, dries up very rapidly (1 to 3 days). Because vertical canals are much more
numerous than radial ones, the resin flow released by a wound is generally
correlated with the density of vertical canals. For the same reason, the direction of
gallery boring is important for this defence system to play a significant role in tree
resistance to bark beetles (Berryman, 1972, Lieutier, 1992). It has been
demonstrated that resin flow can contribute significantly to the failure of D. micans
attacks on Norway spruce, and this has been attributed to the horizontal direction of
the maternal gallery that cuts both radial ducts and a high number of vertical ducts
during the whole tunneling activity of the beetle (Lieutier et al., 1992). It is much
less efficient against species that bore vertical galleries because vertical ducts are
cut, in that case, only at the very beginning of attack. Its role in such situations has
been demonstrated to be very limited, as in Europe for Ips typographus on Norway
spruce (Christiansen and Horntvedt, 1983), and Ips sexdentatus and Tomicus
piniperda in Scots pine where resin flow can play a role in arresting the attacking
beetles only at the time of initiating egg galleries (Lieutier et al., 1988b, 1995;
Schroeder, 1990). Similar conclusions have been drawn for North American species
(Raffa and Berryman, 1983a; Nebeker et al., 1988). Blisters are resin pockets
located inside the outer bark. Their role in resistance has not been studied in
Europe, but studies carried out in North America have demonstrated that, although
important resin quantities can be released by wounding, beetles seem able to avoid
them (Ferrell, 1983).
The polyphenolic parenchyma cell (PP cell) system has been described in detail
in Norway spruce (Franceschi et al., 1998; Krekling et al., 2000). PP cells are
organized in parallel concentric rows inside the phloem, inevitably resulting in their
destruction and certainly in the release of large quantities of phenolic compounds
when a beetle or its associated fungus invades the phloem. However, although the
abundance of PP cells and the phloem content of certain soluble phenols before
attacks are correlated with tree resistance (Storer and Speight, 1996; Franceschi et
al., 1998; Brignolas et al., 1998), no direct demonstration of their role in preformed
resistance has been provided yet.
2.1.2. Systems of induced resistance

138 F. LIEUTIER
Three main steps representing different degrees of complexity can be recognized

The “induced resin flow” is the simplest mechanism. It has been described as a
stimulation of resin synthesis by the cells surrounding the resin canals and which are
responsible for the synthesis of the preformed resin (Ruel et al., 1998). However,
because the chemical content of the new resin has not been investigated, it is not
known if this stimulation is accompanied byy modifications to the metabolism of the
secretory cells. It is typically a wound reaction which appears after repeated
wounding to the tree, and which produces larger quantities of resin than in the case
of preformed resistance. Certainly, this reaction can extend the effect of the
preformed resin flow in time. It has been described only in Pinus taeda in Southern
USA but it certainly also exists in European pines, especially in regions, such as the
Mediterranean basin, where trees are submitted to attacks all the year round.
The “hypersensitive reaction” of conifers to attacks by bark beetles and their
associated fungi has been studied in various regions of the world, after Reid et al
(1967) described it for the first time in a conifer (Pinus contorta) and suggested it
could play an essential role in resistance to bark beetles. In Europe, it has been
studied mainly in Norway spruce and Scots pine (Christiansen and Horntvedt, 1983;
Christiansen, 1985a; Christiansen et al., 1987; Lieutier et al., 1989b, 1995; Delorme
and Lieutier, 1990; Solheim and Langström, 1991; Langström et al., 1992; Lieutier,
1993; Brignolas et al., 1995a; Bois and Lieutier, 1997; among others) and has been
demonstrated to play a fundamental role in resistance in most situations. The
reaction is visible as a resin impregnated zone associated with extended cell
necrosis, which develops usually longitudinally around each point of attack, in both
the phloem and the sapwood, at a distance ahead of the area infested by the beetles
and their associated fungi. This zone is considerably impoverished in sugars and
enriched with terpenes and phenolic compounds, resulting from both stimulation of
syntheses and neosyntheses, the products off which invade intercellular spaces, sieve
cells and tracheids, leading to the death off the affected tissues (Christiansen and
Ericsson, 1986; Lieutier and Berryman, 1988; Delorme and Lieutier, 1990;
Langström et al., 1992; Brignolas et al., 1995a). Considerable changes occur in cell
metabolism and activities. The cells involved in induced syntheses of terpenes are
specialized phloem parenchyma cells, without relation to those involved in the
synthesis of the preformed resin (Cheniclet et al., 1988; Lieutier and Berryman,
1988). The PP cells already involved in phenolic preformed resistance seem also to
be responsible for the neosyntheses of the phenolics involved in the hypersensitive
reaction (Franceschi et al., 1988), but heavy changes occur in their metabolism
(Brignolas et al., 1995b; Chiron et al., 2000). However, in spite of the
delocalization of certain syntheses and considerable changes in cell metabolism, no
cell division and cell differentiation seems to occur. The reaction ends with the
formation of a wound periderm which develops after the aggressors have been
stopped or at least considerably slowed down (Müllick, 1977; Lieutier et al., 1990;
Lieutier, 1993), and isolates the reaction zone and the included aggressors from the
rest of the tree.
The extent of the resin impregnated zone (reaction zone) in the phloem has often
been used to compare the defensive abilities of trees. However, its development
results from both the host response and fungal growth, which has led to
contradicting interpretations after isolated inoculations (Raffa, 1991; Wallin and

Raffa, 2001). Krokene and Solheim (1999) showed that low density inoculations do
not always give a reliable estimate of tree resistance or of fungal virulence (see also
Långström et al. 2001). Nevertheless, Wallin and Raffa (2001) consider that the
delay in time after which this zone is measured is certainly of importance, if we
admit that trees producing the most rapid and intensive response exhibit longer
reaction zones with short delay, while the most susceptible trees need time to stop
the fungus, thus allowing the reaction to grow over longer period leading to a longer
reaction zone overall. They suggested that tree resistance levels should be compared
by using a fungal confinement rate corresponding to the ratio of reaction zone length
at day 6 to that at day 9. On the other hand, reaction zone length after punctual
inoculations has been demonstrated to be an indicator of virulence useful for
comparison of different fungi in the same tree (Lieutier et al., 1989b, 1990;
Långström et al., 1993b) and different isolates within the same fungus species
(Lieutier et al., 2004).
The “delayed resistance” corresponds to the most complex changes occurring in
response to bark beetle attack. The formation of the wound periderm mentioned
above refers to that kind of tree reaction but it interferes mainly in wound healing
processes and it is not discussed here. The phenomenon of “induced protection”, on
the contrary, directly interferes in tree resistance. It has been described recently in
Europe, in both Norway spruce and Scots pine (Christiansen et al., 1999a; Krokene
et al., 1999, 2000, 2001), although it certainly also exists in other conifers. It
corresponds to the induction of resistance to lethal densities of mass inoculations, in
trees pretreated at levels below the lethal density, with a phytopathogenic fungus. A
delay of at least one week after pretreatment is needed for the induction of
resistance, and trees are protected for at least one year after pretreatment (Krokene et
al., 2003). The detailed mechanisms of the induced protection are still largely
unknown but it has been hypothesized that traumatic resin ducts which usually form
after wounding in the sapwood, after the same delay as induced protection, are
involved (Krokene et al., 1999, 2003; Christiansen et al., 1999b; Nagy et al., 2000).
However, the induced protection stays local, whereas traumatic resin ducts can be
observed up to a distance of several meters from the inoculation site after one year
(Christiansen et al., 1999b). If this hypothesis is true and because these resin canals
are built de novo from cambial cells, induced protection would correspond to very
complex changes involving cell division and differentiation. Modifications in the
PP cells have been reported to be associated with this kind of resistance (Krokene et
al., 2003) supposedly in relation to methyl jasmonate release (Franceschi et al.,
2002; Martin et al., 2002; Fäldt et al., 2003; Hudgins et al., 2003a). In the same tree
species, a spatio-temporal study of host selection by D. micans in central France
concluded there was induced susceptibility following successful attacks by previous
beetle generations (Gilbert et al., 2001). This does not exclude, however, the
possibility that failed attacks increase tree resistance, in accordance with the delayed
resistance phenomenon.
2.2. General mechanisms of induced defences

140 F. LIEUTIER
2.2.1. Complementarity and interdependence

The three main levels of complexity of induced defences, ranking from simple
stimulation of cells already specialized in the same function to complex changes
accompanied by building of new cells, are equivalent to a ranking from short term to
long term responses. The induced resin flow appears only two to three days after the
beginning of wounding (Ruel et al., 1998). The hypersensitive reaction begins to be
clearly visible in the phloem as soon as three days after attack, but is fully developed
both histologically and chemically in 10 to 15 days, in Scots pine and Norway
spruce as well (Lieutier et al., 1990; Brignolas et al., 1995a,b; Franceschi et al.,
1998). The formation of traumatic resin ducts, involving more complex changes, is
slower. They need more than two weeks to be built locally, and one year at a
distance of some meters (Christiansen et al., 1999b; Nagy et al., 2000). In terms of
tree resistance to attacks, the induced defence systems thus seem to complement
each others very well in time, after the rapid and brief action of the preformed
resistance (Lieutier, 2002). Their relative role to that of the preformed resistance
can also be modulated by various factors such as beetle behavior (gallery direction),
tree species, or climatic factors (Lombardero et al., 2000). In addition, interactions
exist between different systems. In Norway and Sitka spruce, a negative correlation
was found between the size of the phloem reaction zone and the concentration of
stone cell masses in this tissue (Wainhouse et al., 1997). At least for phenols, the
same PP cells seem to be involved in constitutive, hypersensitive and delayed
resistance (Franceschi et al., 2000).
2.2.2. Induction, specificity and involved cells

Apart from their linkage in time, there are several essential characteristics that
appear to be shared by the different degrees of induced response (Lieutier, 2002).
They are all wound reactions, eventually stimulated
m when fungi are present, they are
not specific in relation to the species of aggressor, and they generally involve
phloem parenchyma cells.
In experiments using natural and artificial attacks on Scots pine by T. piniperda
and I. sexdentatus, it has been shown that the hypersensitive reaction is a wound
reaction, induced by the mechanical stress caused by the tunneling activity of the
beetle, and that it can be considerably accelerated and amplified when a
phytopathogenic fungus is present in the gallery (Lieutier et al., 1988b, 1995). This
was also demonstrated in Norway spruce submitted to artificial infestation by
Ceratocystis polonica, a fungus associated with I. typographus (Brignolas et al.,
1995a, Franceschi et al., 1998). Lieutier (1993) suggested that this mechanism of
induction occurs in all hypersensitive reactions of conifers to attacks by bark beetles
and their associated fungi. Induced protection has also been demonstrated to occur
after pre-treatment with malt agar without fungus, although to a lesser extent than
after pretreatment with fungus (Krokene et al., 1999). This again suggests that
fungus stimulates a wound reaction. Traumatic resin duct formation is typically a
wound response which has been demonstrated to be stimulated by fungi
(Christiansen et al., 1999b; Nagy et al., 2000). Exogenous applications of methyl
jasmonate on the stems of Norway spruce and other Pinaceae, without wounding,
can trigger induced responses similar to those induced by wounding, fungal

infection or bark beetle attacks (Franceschi et al., 2002; Martin et al., 2002; Hudgins
et al., 2003a). However, during a natural beetle attack, there is always a wound. It
is thus conceivable that wounding causes the release of this phytohormone inside the
tree tissues. The induced resin flow, by definition, is a wound reaction. Fungi may
enhance it but no information is available to test this possibility.
The non specificity of defence is a consequence of the wound response. It has
been demonstrated directly for the hypersensitive reaction. Whatever the aggressors
(different beetles, different fungi, wounding,), the development pattern of the
hypersensitive reaction, as well as the associated chemical, anatomical and
histological changes are identical in a tree (Delorme and Lieutier, 1990; Lieutier et
al., 1991a; Brignolas et al., 1995a; Bois and Lieutier, 1997; Franceschi et al., 1998).
Changes in the type of aggressor elicit only variations in rapidity and extension of
the reaction. Reported here for Scots pine and Norway spruce, the same results have
been obtained in North American situations (Wong and Berryman, 1977; Müllick,
1977; Raffa and Smalley, 1995). Induced protection and formation of traumatic
resin canals in Scots pine and Norway spruce are also non specific phenomena
(Krokene et al., 1999, 2001; Nagy et al., 2000; Franceschi et al., 2000; Hudgins et
al., 2003a). It has been hypothesized that induction by wounding, eventually
followed by stimulation by fungi, and non specificity of the response are traits
common to all induced defence mechanisms off conifers against bark beetle attacks
(Lieutier, 2002).
Studied mainly in Norway spruce, PP cells interfere in many aspects of the
hypersensitive reaction (see above). Krekling et al. (2000) presented their structure
and development in detail, and Franceschi et al. (1998, 2000, 2002) generalized their
role to all cases of induced responses in conifers (except induced resin flow). PP
cells appear to play a major role in synthesis, storage, and modification of phenolic
compounds in response to wounding, for both constitutive and inducible defences
(Franceschi et al., 1998, 2000).
2.2.3. Biochemical characteristics of the tree induced response

The chemical nature of the response to attacks by bark beetles and their associated
fungi has been investigated for the hypersensitive reaction only and almost
exclusively at the phloem level. In the pines P. sylvestris and P. pinaster, terpene
concentration increases more than 100 times (Lieutier et al., 1989a, 1991a). The
relative composition in monoterpenes and resin acids varies slightly, but the main
alteration in this chemical family is an absolute increase in the concentration of all
compounds already present before attack (Delorme and Lieutier, 1990; Lieutier et
al., 1991a; Langström et al., 1992). Similar results have been obtained in North
American pines (Shrimpton, 1973a; Raffa and Berryman, 1982a; Raffa and Smalley,
1995). Only stimulation of syntheses seems to occur. On the contrary,
investigations of phenolics in both Scots pine and Norway spruce revealed
considerable changes in their relative composition (Lieutier et al., 1991b, 1996c;
Brignolas et al., 1995a). The concentration of some compounds decreases while
that of other increases, some being new for the concerned tissue. These new
142 F. LIEUTIER
compounds result from neosyntheses and not from degradation of pre-existing

products or translocation, since alteration of related enzymatic activities as well as
gene activation have been observed (Brignolas et al., 1995b; Chiron et al., 2000).
The phenolic aspects of the phloem hypersensitive response to bark beetles and their
associated fungi have not been deeply investigated in other conifers than Scots pine
and Norway spruce, but they certainly occur in most conifer species.
The energy demand to the tree is considerable during the process of
hypersensitive reaction and the source of energy used has been a matter of debate.
Sugar and starch concentrations decrease in the close vicinity of the reaction zone
(Christiansen and Ericsson, 1986; Långström et al 1992). This could indicate that
they may be used by the tree as a source of energy for responding to attacks, but also
that they may be consumed by the fungus for its growth. Most European research
conducted in Norway spruce and North American studies in pines have concluded
that there is mobilization of products from current photosynthesis (Christiansen and
Ericsson, 1986; Miller and Berryman, 1986; Christiansen et al., 1987; Christiansen,
1992; Dunn and Lorio, 1992; Christiansen and Fjorne, 1993). However, recent
experiments based on the use of labeled carbon in Scots pine pointed to an essential
role of the tree reserves (Guérard, 2001).
3. MODE OF ACTION UPON THE AGGRESSORS

The effect of preformed resin flow on the aggressors has been largely studied in
North America and few data are available from European situations. However,
since beetle – fungus - tree relationships in North America have parallel counterparts
in Europe, a transposition of the conclusions seems reasonable. The role of resin
flow would mainly be wound cleansing by flushing the wounded tissues, followed
by sealing the wound through resin crystallization (Berryman, 1972) and effect on
beetles seems mainly relevant to antixenosis, leading them to modify their behaviour
and leave quickly. Preformed resin would act against the aggressors physically,
through flushing, viscosity and crystallization rate (Vité, 1961; Cates and Alexander,
1982), or chemically through toxicity of terpenes (Reid and Gates, 1970; Raffa et
al., 1985; Paine and Hanlon, 1994; Raffa and Smalley, 1995). It can also interfere
with pheromone emission, resulting in stopping beetle aggregation (Raffa and
Berryman, 1983a). However, although fungal spores can be flushed away, fungi can
often tolerate the resin flow (Shrimpton and Whitney, 1968), whereas some beetle
species are highly resistant to it, such as D. micans in Europe (Everaerts et al., 1988;
Grégoire, 1988). Moreover, in addition to its rapid drying up, resin flow exhibits
high variability within a tree, as shown in Europe in Scots pine (Schroeder, 1990).
Consequently and because the attacking beetles are often not killed and can escape,
they can circumvent this system by finding a place on the same tree suitable for
initiating a gallery (Lieutier et al., 1995). The effect of the induced resin flow has
not been studied specifically, but it is certainly comparable to that of the preformed
one, provided that its chemical composition is the same.
The hypersensitive reaction is often said to act upon the aggressors through a
combination of both physical and chemical factors, as well as through reduced
access to nutrients. This later effect would result from both nutrient depletion in the
reaction zone and containment of the aggressors inside this zone, thus impeding
their access to nutritive tissues located outside. The physical effect would consist in
hardening of the resin impregnated tissues and resin flooding from the saturated
tissues into the galleries. Hardened tissues would become unsuitable for the boring
female and for the larvae that could hatch from already led eggs. Resin flooding
would have consequences comparable to that of the preformed and induced resin
flows, certainly complemented by an increased toxicity due to its higher terpene
content. Nevertheless, only the chemical effect has been investigated through
experimental approaches. In general, it relates to both antixenosis and antibiosis,
and results from complementary actions of compounds from several families,
mainly terpenes and phenols.
As with the preformed resin flow, research on the effect of terpenes involved in
the hypersensitive reaction to bark beetles and their associated fungi has been
mainly developed in North America. Assays with purified compounds demonstrated
that a minimum concentration is necessary for terpene toxicity and that, at
concentrations present in the reacting tissues, monoterpenes are toxic or repellent for
beetles and inhibitory for beetle associated fungi, either by contact or vapor (Smith,
1963; Cobb et al., 1968a; Shrimpton and Whitney, 1968; Bordash and Berryman,
1977; Raffa and Berryman, 1983b; Raffa et al., 1985; Bridges, 1987; Raffa and
Smalley, 1995; among others). Similar results have been obtained in Europe with I.
sexdentatus, T. piniperda and their associated fungi, regarding Scots pine
monoterpenes (Delorme and Lieutier, 1990). Although some monoterpenes, such as
limonene, may be more toxic than others (Raffa et al., 1985), all exhibit a high
toxicity for beetles and a high inhibitory effect for fungi (Delorme and Lieutier,
1990). Results combine to suggest that the effect of monoterpenes on both beetles
and their associated fungi are more due to the total quantity of these compounds
rather than to some particular ones [Berryman and Ashraf (1970), Raffa and
Berryman (1982a), Lieutier et al. (1991a), Raffa and Smalley (1995) for North
American pines and firs; Delorme and Lieutier (1990) for Scots pine]. The same
conclusion holds for resin acids as well (Långström et al. 1992).
The effects of phenolics in the context of conifer resistance to bark beetles have
been investigated mainly in Europe, in both Scots pine and Norway spruce, but no
assay has been performed on the insects themselves. They have a significant in vitro
inhibitory effect on bark beetle associated fungi by contact but, unlike terpenes, it is
remarkable that this effect is mainly due to some particular compounds, especially
those that are neosynthesized during the hypersensitive
y reaction, with some of them
acting synergistically (Brignolas, 1995; Bois and Lieutier, 1997; Bois et al., 1999;
Evensen et al., 2000). Similar inhibitory effects of phenolics of North American
pines have also been reported on Ophiostoma species (Hart and Shrimpton, 1979;
Hart, 1981). However, phenols have not been demonstrated to have the same effect
in nature (Hart and Shrimpton, 1979) and their role in conifer resistance to bark
beetles and their associated fungi remains unclear, although correlations between
phenol composition and resistance exist for both Norway spruce and Scots pine (see
below VI.1).
144 F. LIEUTIER
4. BEETLE BEHAVIOR IN RELATION TO TREE RESISTANCE

Facing such a diversity of defence systems which together present efficient
resistance to their attacks, bark beetles have evolved various behaviors to establish
in their hosts. Raffa (1991) proposed that these behavioural traits could be used to
separate beetle attack strategies, on the basis of exhausting tree defences, avoiding
resistant trees or tolerating tree defences. Derived from a preliminary suggestion
(Lieutier, 1992), Lieutier (2002) also proposed the use of beetle behavior but in
another way which leads to a different grouping of beetle species that attack living
trees into two main types of strategies: exhausting tree defences and killing the tree
vs avoiding / tolerating tree defences and keeping the tree alive.
4.1. The strategy of exhausting host defences (cooperative strategy)
4.1.1. The general model and the critical threshold of attack density
An ancient and common observation forming the basis of the model used to describe
the strategy of exhausting tree defences is that, in most bark beetles species
attacking living trees, a minimum number of attacks is necessary to kill a tree and
for successful establishment of the beetle populations, including successful
oviposition and brood development. This fact has been well known by all European
foresters for a long time and the corresponding scientific concept was first
formulated by Thalenhorst (1958) before being largely developed by North
American researchers (Safranyik et al., 1975; Berryman, 1976, Raffa and Berryman,
1983a). It implies the existence of both a threshold of attack density that must be
exceeded to allow the success off beetle attacks, and tree resistance mechanisms that
are efficient below that level. The threshold levels thus quantify tree resistance to a
given beetle species, as well as beetle aggressiveness for a given tree species
(Berryman, 1976; Raffa and Berryman, 1983a; Christiansen et al., 1987). The idea
has then been used in North America and Europe to built models of bark beetle
population dynamics (Berryman, 1976; Christiansen et al., 1987, among others).
The existence of such critical thresholds has been experimentally demonstrated in
the field under various conditions for several beetle and conifer species, as for I.
typographus in Norway spruce and T. piniperda and I. acuminatus in Scots pine in
Europe (Mulock and Christiansen, 1986; Långström et al., 1992; Långström and
Hellqvist, 1993a,b; Guérard et al., 2000a). In Europe, their level in healthy trees
ranges from 300 to 850 attacks / m² depending on species and local conditions and is
strongly influenced by tree health and genetic factors (see § 6). In North America
on Pinus ponderosa, Dendroctonus ponderosae has been reported to have a critical
threshold of attack density as low as 60 attacks / m² (Raffa and Berryman, 1983a).
In Southwestern China, the critical threshold of a Tomicus species for Pinus
yunnanensis is around 80 attacks / m² but is strongly influenced by the intensity of
previous attacks in the shoots (Lieutier et al., 2003c).
Since induced defence systems must be built rapidly at each point of attack in
order to stop the aggressors, the existence of the critical threshold is supposed to
result from the fact that the ability of the tree to rapidly mobilize its sources of
energy is limited, and the level of tree resistance is thus determined by this capacity
(Christiansen et al., 1987). The model of the strategy of exhausting tree defences is
based on these energetic considerations. The strategy of the beetle population is to
rapidly deplete the energy resources by increasing the energy demand to the tree
until a level (critical threshold of attack density) above which the tree becomes
unable to accelerate the energy mobilization. At this moment, the tree induced
defences become inefficient, brood establishment
a begins and attacks can succeed.
4.1.2. Conditions for attack success

According to the model, everything thatt stimulates and increases the energy
expenditure by the tree at the moment of beetle attack lowers the critical threshold of
attack density and is thus useful to that strategy. It is possible to recognize typically
four main characteristics in beetle biology that are important in this context
(Lieutier, 2002).
- Mass aggregation on the host tree at the time of attacks is an essential and
powerful tool for the beetle population, justifying the name of cooperative strategy
that has also been given to that strategy. Most of the time, aggregation results from
pheromones, but it can also be due to monoterpene attractants emitted by the tree
through the wounds caused by the first arrived beetles, as in the case of T. piniperda
(Byers, chapter 8). In any case, it allows a rapid increase of the number of attacks
on the host, of course necessary to reach a certain threshold of attack density, but
also forcing the tree to respond at many places simultaneously, as each local induced
reaction is stimulated by the beetle tunneling activity.
- Another biological characteristic in favor of the exhaustion strategy is related to
gallery orientation. Because the reaction develops mainly in the longitudinal
direction, longitudinal galleries should better stimulate it than transverse galleries.
- Occurrence of beetle attacks during the season of tree activity, when the tree is
able to respond, is also a biological trait adapted to that strategy. Inside that period
and referring to the growth – differentiation balance concept (Loomis, 1932; Lorio,
1986), spring attacks should even be even more efficient than summer or autumn
attacks, because they occur during a period when tree growth is maximal and thus
when less energy is available for defence, consequently favoring rapid tree
exhaustion.
- An association with a phytopathogenic fungus is often also an efficient way to
lower the threshold of attack density, since induced defences can be stimulated by
phytopathogenic fungi introduced by the beetles in their galleries (see above).
Similarly to the thresholds of attack density, by artificially mass inoculating trees
with fungi, it is possible to define critical thresholds of inoculation density, above
which tree resistance is overcome and trees are killed, while they resist and survive
below [Hornvedt et al. (1983) and Christiansen (1985a) for Ceratocystis polonica in
Norway spruce; Långström et al. (1993), Solheim et al. (1993) and Croisé et al.
(1998b) for Leptographium wingfieldii on Scots pine; Guérard et al. (2000a) for
Ophiostoma brunneo-ciliatum on Scots pine]. Values range from 400 to more than
1 000 inoculations per m². Similar results have been obtained for the North
American species (Raffa and Berryman, 1983b). Such thresholds can be used to
146 F. LIEUTIER
quantify fungus pathogenicity and to compare tree resistance levels. However, to

conclude that a bark beetle associated fungus contributes significantly to lowering
the critical threshold of attack density of its vector, one must be able demonstrate
that the stimulation of the induced defences by the fungus occurs effectively when
the fungus is introduced by the beetle itself and not only after artificial inoculations.
It has been pointed out that: 1- the frequency of association between beetles and
fungi is very variable and often far from 100 % (Kirisits, chapter 10); 2- the tree
response to one artificial inoculation depends quantitatively on the number of spores
present in the inoculum, and a minimum number must be introduced into the wound
for the fungus to be able to stimulate significantly the tree induced reaction (Lieutier
et al., 1988b; 1989). The usual method of artificial inoculation utilizes 5 mm
diameter discs of 3-week-old agar cultures (Kirisits, chapter 10). One such
inoculum introduced in a single hole contains a very high number of spores, far
above the number introduced by a beetle in its gallery (Lieutier et al., 1989a; 1995).
Because fungus pathogenicity is measured with artificial inoculations, it follows
from the two above remarks that there is no relation between beetle aggressiveness
and pathogenicity of its associated fungus (Harrington, 1993; Paine et al., 1997;
Lieutier, 2002). A vigorous induced reaction to artificial inoculation and a low
threshold of inoculation density, which reflect high fungus pathogenicity, are thus
not sufficient information to conclude that the fungus plays a role in lowering the
threshold of attack density (Lieutier, 1995; 2002). A typical example in Europe is
given by T. piniperda and its associated fungus L. wingfieldii (see below).
4.1.3. Tissues colonization and tree death

In a strategy of exceeding a defined threshold for attack, tree death occurs as an
unavoidable consequence of defence exhaustion. Since tree defences must be
exhausted before brood establishment begins, tree death develops simultaneously to
successful colonization of phloem by beetles, and both phloem and sapwood by
fungi. The mechanisms of tree death have been a matter of debate, especially in
Northern America, and it has often been concluded that fungi play a crucial role (ref.
in Paine et al., 1997). In fact, three complementary factors seem to be involved:
sapwood invasion, occlusion and cavitation by the fungi, leading to the stopping of
water transfer; phloem invasion by the beetles, leading to phloem destruction; and
resin soaking that had occurred during the development of tree defences, sometimes
resulting in the sacrifice of a considerable quantity of phloem and sapwood tissues.
A detailed discussion has been presented in Lieutier (2002).
4.1.4. The species concerned

The strategy of exhausting host defences is employed by most bark beetle species
that attack living trees. Table 1 summarises economically important European
species matching that strategy, together with some counterparts from other
continents, mainly North America, with h a presentation of their biological
Table 1: Characteristics of the beetle behaviour and role of the associated fungi during attacks, and consequences of successful attacks for the
tree, for different beetle species relatively to their attack strategies, in Europe and North America.
Beetle Region Host tree Beetle species Fungus Aggreg- Egg Attack Tole- Successful
strategy species role ation gallery / tree rance attacks kill
/ tree orienta- activity to tree
defence tion resin
t ograp
Spruces Ips typ a hus Yes Yes Longit. During Yes
Pity
t ogenes chalcograpa hus ? Yes Oblique During Yes
Pines Ips acuminatus Yes Yes Longit. During Yes
Europe Orthotomicus erosus Yes Yes Longit. During Yes
Ips sexdentatus Yes Yes Longit. During Yes
Tomicus pinipi erda No* No Longit. Before Yes
Firs Pity
t okteines curvidens ? Yes Transv. During Yes
Pines Dendroctonus ponderosae Yes Yes Longit. During Yes
North Dendroctonus frontalis
f No ? Yes Wind. During Yes
America Firs Scoly
l tus ventralis Yes Yes Transv. During Yes
Dg. fir Dendroct. pseudotsugu ae Yes Yes Longit. During Yes
Europe Spruces Dendroctonus micans No No Transv. A. time High No
Dendroctonus punctatus No No Transv. A.time High No
HOST RESISTANCE TO BARK BEETLES
North
Pines Dendroctonus valens ? No Tr + Lg A.time ? High No
America
Dendroctonus terebrans ? No Longit. A.time ? ? No
Dg. fir = Douglas fir; Longit. = longitudinal; Transv. = transversal; Wind. = winding; Tr + Lg = transversal and longitudinal; * = fungus
present but no role; A.time = any time
147
148 F. LIEUTIER
characteristics concerned with the conditions for attack success. Typical cases are
those of I. typographus in spruces and I. sexdentatus, I. acuminatus and
Orthotomicus erosus in pines, of which all biological characteristics are in perfect
accordance with the general model. All off them have aggregation pheromones and
develop mass aggregation, have longitudinal galleries, attack during the season of
tree activity (Sauvard, chapter 7), and are associated with fungi that stimulate the
development of the tree hypersensitive reactions (Kirisits, chapter 10). Typical
North American representatives are D. ponderosae and Dendroctonus pseudotsugae.
The other European species possess only some of the typical biological
characteristics but still fit the exhaustion strategy.
Pityogenes chalcographus bores oblique galleries in spruces. This particular
behavior results in stimulation of the hypersensitive reaction and in an abundant
resin flow (by cutting numerous resin ducts), both contributing to exhaustion of tree
defences. Its associated fungi have not been studied. Nevertheless, this beetle
seems to fit well with the exhaustion strategy. Pityokteines curvidens bores
transverse egg galleries in Abies alba, but this orientation is not a handicap since
resin ducts do not exist in firs. It aggregates on the attacked trees, but it is not
known if associated fungi are able to stimulate tree defences. If this was the case,
Scolytus ventralis would be its North American counterpart in Abies grandis. T.
piniperda also refers to the exhaustion strategy. However, its associated fungus L.
wingfieldii, although strongly pathogenic for Scots pine with a threshold of
inoculation density around 400 inoculations / m² (Solheim et al., 1993; Croisé et al.,
1998b), does not play any role in stimulating the tree hypersensitive reaction
(Lieutier et al., 1995), because of its very low frequency of association and also
because of certainly too low a number of spores introduced by the beetle in its
gallery (Lieutier et al., 1989a; Lieutier, 1995). Tree defences can be exhausted only
by repeated mechanical stimulation resulting from the longitudinal tunneling activity
of the beetle. Moreover, attacks take place during winter (Sauvard, chapter 7), early
before the rapid increase of tree activity in spring. All these biological
characteristics result in a very high critical threshold of attack density on healthy or
moderately weakened trees, and certainly explains why T. piniperda attacks succeed
usually on very weak and dominated trees (Lieutier, 1995). In Southwestern China,
another Tomicus species corresponds exactly to the situation of T. piniperda in
Europe and develops the same strategy, except that, during their maturation feeding
in the shoots, the maturing adults concentrate their attacks on the same trees (Ye and
Lieutier, 1997). This results in a considerable lowering of the critical threshold of
attack density on the stem, which makes this species able to kill trees by using the
exhaustion strategy during subsequent stem attacks (Lieutier et al., 2003c). In North
America, D. frontalis could correspond to a situation intermediate between P.
chalcographus (winding galleries and aggregation pheromones) and T. piniperda
(role of the associated fungus questionable).
4.2. The strategy of avoiding host defences
4.2.1. The general model and the solitary behavior

This strategy has been typically described in Europe (Lieutier, 1992, 2002) and D.
micans in Norway spruce is the best example. m There is no stimulation or
exploitation of tree’s defences to overcome its resistance. On the contrary,
everything is done to avoid the defence mechanisms, especially to minimize the
development of the hypersensitive reaction. Firstly, there is typically no association
with fungi, as demonstrated for D. micans (Lieutier et al., 1992). Secondly, since
tree exhaustion is not necessary, there is no beetle cooperation; beetles behave
individually and do not have aggregation pheromones at the adult stage (“solitary
strategy”) (Grégoire, 1988). Thirdly and typically also, maternal galleries are
transverse perpendicular to the direction of the usual development of the
hypersensitive reactions. This behavior both minimizes the development of those
reactions and also avoids contact between the boring female and toxic neo-
synthesized compounds. Nevertheless, it obliges the female to cut through a large
number of resin ducts, and thus supposes that they have a high resistance to the
preformed resin. In Norway spruce however, the preformed resin flow is very weak,
and adults of D. micans adults are highly resistant to constitutive resin (Grégoire,
1988). The consequence of egg gallery orientation is that larval galleries are
longitudinal, which supposes a high resistance of the larvae to the neo-synthesized
compounds and/or the development of special larval strategies to resist the
hypersensitive reaction. D. micans has solved this problem through both a high
tolerance of eggs and larvae to resin (Everaerts et al., 1988) and the existence of
aggregation pheromones at the larval stage (Grégoire et al., 1982), allowing larvae
of a same system to cooperate in boring a familial gallery faster than the tree
develops its reaction. A fourth typical trait in this strategy, allowed by the absence
of effects of the hypersensitive reaction on the attacking females, is that attacks can
occur at any season.
The local particularities of the tree (preformed defences), at the places where the
beetle attacks occur, play the most important role in determining the success or
failure of oviposition. This is the case for moisture and stilbene content of the
phloem (Storer and Speight, 1996), stone cell masses (Wainhouse et al., 1990,
1998a), preformed resin flow (Lieutier et al., 1992). Consequently and contrarily to
the cooperative strategy where a threshold exists above which all attacks succeed, in
the solitary strategy, attacks can succeed at one place while others can fail at another
place of the same tree (Vouland, 1991). Moreover, in that solitary strategy, as a
consequence of the non exhaustion of tree defences, the host is not killed by the
successful attacks and the whole beetle lifef cycle takes place in a living tree, making
that strategy a real parasitic one. With D. micans, tree death always occurs after
several years and several generations in a same tree (Vouland, 1991).
4.2.2. Other related situations

Only a few bark beetle species represent the solitary attack strategy and there is no
other known example than D. micans in Europe (Table 1). In North America, D.
punctatus is typically equivalent to D. micans and fits in exactly with the same
strategy. D. valens also probably refers to the strategy of avoiding host defences. It
does not have aggregation pheromones and can reproduce without killing its host
150 F. LIEUTIER
(Raffa, 1991). It carries a highly pathogenic fungus but it is not clear if this fungus
stimulates the tree induced reaction when introduced into the tree by the beetle itself.
D. terebrans resembles D. valens but has longitudinal galleries.
5. EFFECT OF HOST RESISTANCE ON BARK BEETLE POPULATION

DYNAMICS
5.1. The case of the cooperative strategy

Papers presenting a general model on the role of host resistance in bark beetle
population dynamics in the case of the cooperative strategy have concerned almost
exclusively North American species (Berryman, 1976, 1982; Coulson, 1979; Raffa
and Berryman, 1983a; Raffa, 1991). In Europe, the American model has been
applied and developed for I. typographus (Christiansen et al., 1987). These models
are based on comparisons between trees’ resistance level (in terms of critical
threshold of attack density) and real beetle attack density on trees (as a result from
current population level).
During endemic periods, the densities of attacks on trees are low and only very
weakened trees or felled trees can be successfully colonized because their resistance
level is very low or nil. The beetle population varies with the availability of this
material but, because such trees are depletedd at each beetle generation, they are in
insufficient number to sustain population increase. The population level is thus
rarely sufficient to reach the critical threshold of attack density for healthy trees and
to allow establishment on them. The reproductive gain is thus offset by losses
during the search for available hosts (Raffa, 1991). However, if large quantities of
trees become weakened or fallen, beetle populations can rapidly increase, and
eventually exceed the critical threshold of attack density of healthy trees. A
considerable quantity of material is then available for beetle reproduction,
generating a positive feed-back cycle, and the populations can continue to expand,
even if the weakened trees are depleted (Raffa, 1991). The epidemic period ends
when all suitable trees are killed or when beetle levels are too low to overwhelm
additional trees.
In Europe, many field observations corroborate these mechanisms. Following
the two hurricanes “Lothar” and “Martin” that devastated forests and felled billions
of trees throughout Western Europe in December 1999, populations of I.
typographus and I. sexdentatus have exploded in 2000, leading to extensive killing
of healthy trees in numerous places during 2001 and 2002 (Nageleisen, 2002, 2003).
Trees weakened allowing beetle establishment and population increase have also
resulted from pollution or fire (Christiansen, 1989; Langström et al., 1999).
Outbreaks often correspond to coincidences between a prolonged period of drought,
supposed to lower the resistance of living trees, and sudden abundant reproductive
material without defence (felled trees or broken branches) that favors population
increase, as for I. acuminatus in South Eastern France in 1987 (Lieutier et al.
1988a).
5.2. The case of the solitary strategy

D. micans can attack any tree and even seems to prefer healthy trees. Moreover,
successful attacks do not kill the host and, therefore, a tree successfully
f colonized is
still available for future generations. Thus a sufficient quantity of food is always
present. Its accessibility depends mainly on local preformed resistance (resin, stone
cell masses, phloem moisture and stilbenes). On the other hand, the efficacy of tree
resistance in attack failure does not depend on the population level (contrary to the
other strategy), since beetle strategy is individual and resistance based on local tree
characteristics. This density independence thus poses questions about the role of
tree resistance as a key-factor of beetle population dynamics. Rather, in the case of
D. micans at least, several field observations suggest that predators are the most
important factor (Grégoire, 1988). Tree resistance is certainly the most important
parameter that determines the success of female colonisation of the tree and
oviposition, and can thus contribute to lower the population levels during the search
for an available host, but this effect very likely concerns a constant fraction of the
beetle population. Larvae are well adapted to bore into resin impregnated phloem,
and very little mortality due to the hypersensitive reaction occurs at this stage
(Everaerts at al., 1988). Predation on eggs and larvae on the contrary seems to have
the highest impact on brood development and on variations of population levels.
There is no information on whether these comments can be applied to other beetles
using the solitary strategy.
6. VARIATIONS IN TREE RESISTANCE TO BARK BEETLES
6.1. Role of genetic factors

The genetic dependence of certain factors involved in preformed defences of
conifers has been known for a long time in both North America and Europe. This is
the case for monoterpenes and resin acids (Hanover, 1966, 1975; Bernard-Dagan et
al., 1971; Tobolski and Hanover, 1971; Baradat et al., 1975, 1978; Katoh and
Croteau, 1998; among others), total resin yield (Mergen et al., 1955; Rudinsky,
1966), resin viscosity and rate of crystallization (Mergen et al., 1955; Buijtenen and
Van Santamour, 1972; Nebeker et al., 1992), and resin flow (Nebeker et al., 1992).
Bark structure (Nihoul et al., 1989) and sap pressure (Lévieux et al., 1988) have also
been reported to be partially genetically dependent. All these parameters have often
been suggested to contribute to genetic differences in tree resistance to bark beetles
and their associated fungi, but no parallel has been established directly in these
studies between variations in the parameters and variations in tree resistance.
Between-tree genetic differences in the length of the phloem reaction zone that
develops in response to artificial aggressions have been reported in pines in both
North America and Europe (Paine et al., 1993; Lieutier et al., 1996b), but no link to
differences in tree resistance level was established. Moreover, absolute reaction
zone length does not seem a good indicator of tree resistance (see 2.1.2). Genetic
variations in the ability of the tree to synthesize terpenes after aggression have also
152 F. LIEUTIER
been mentioned in grand fir and interpreted in terms of tree resistance to bark beetles
(Katoh and Croteau, 1998), but without data on parallel variations in resistance.
Within the same conifer species, the existence of varieties or provenances more
resistant than others to bark beetle attacks was recorded several years ago, as in
Pinus elliotti vs. I. calligraphus (Wilkinson, 1979) and Abies concolorr vs. S.
ventralis (Ferrell and Otrosina, 1996). Some evidence of intra-specific genetic
differences in tree susceptibility to beetle attacks, parallel to differences in their
capacity to respond to aggressions, have also been provided in North America,
especially regarding resin exudation in Pinus radiata (Witanachchi and Morgan,
1981) and terpene synthesis in P. contorta (Raffa and Berryman, 1982a). However,
the relationships between the genetic control of tree resistance to bark beetles or
their associated fungi (defined d in terms of critical thresholds of attack / inoculation
density) and the parameters involved in resistance, have been intensively
investigated only recently, mainly in Europe, in Scots pine and Norway spruce.
Through a between clone comparison, the level of resistance of Norway spruce to
mass inoculations with C. polonica and that of Scots pine to mass inoculations with
L. wingfieldii have been demonstrated to be genetically controlled, and to vary in
parallel to the phloem phenol composition both t before attacks and in response to
these attacks (Brignolas et al., 1995b, 1998; Bois and Lieutier, 1997; Evensen at al.,
2000). In Norway spruce, these results were then extended to the whole species
through comparisons mixing clones and provenances (Lieutier et al., 2003a). In this
tree species, the diversity of constitutive phloem phenols and the ability to induce
phenol synthesis [especially (+)-catechin] in response to wounding have been
proposed as predictors of tree resistance to fungus mass inoculation, and supposedly
to bark beetles (Lieutier et al., 1996a, 2003a; Brignolas et al., 1998), whereas the
ability of the tree to synthesize pinosylvin in response to aggression was proposed as
predictor of Scots pine resistance (Bois and Lieutier, 1997). For Norway spruce, at
the end of an outbreak, the proposed parameters were validated in the field as
predictors of resistance to natural bark beetle attacks, but their validity during an
outbreak peak seemed questionable (Lieutier et al., 2003b). The PP cells, already
reported to be involved in the resistance mechanisms of Norway spruce to mass
inoculation with C polonica (see above, II.2.2), have also been observed to differ
greatly between resistant and susceptible clones (Franceschi et al., 1998). While
they are filled with dense bodies and occur in single rows in the phloem of
susceptible clones, the rows are two cells thick and the cells are 40 % more
numerous and show lighter deposits in the resistant clones. In response to fungus
inoculation, the PP cells of the resistant clones enlarge and their phenolic bodies are
considerably reduced, whereas these changes are much less marked in the
susceptible clones (Franceschi et al., 1998). In response to attack, the traumatic
resin ducts are built earlier in the resistant than in the susceptible clones (Nagy et al.,
2000). The genetic determinism of conifer resistance to bark beetles has however
never been investigated.
6.2. Variations with season and tree age

The only experiment taking into account the seasonal variations of the tree
resistance level itself (level of the critical threshold of inoculation density) was
carried out in Norway spruce (Horntvedt, 1988). It demonstrated that resistance to
mass inoculations with C. polonica is lower in summer than in spring and autumn.
Most studies related to the effect of season on the parameters of tree resistance have
been carried out on North American pines ((P. taeda, P. echinata, P. ponderosa, P.
contorta) and were related to the length of the phloem reaction zone induced by
isolated fungus inoculations. They generally referred to longer reaction zones in
summer than in spring or autumn (Stephen and Paine, 1985; Cook et al., 1986; Reid
and Shrimpton, 1971). In Europe, Lieutier et al. (1993) reported smaller reaction
zones in spring than in summer and autumn in Scots pine. In most cases, these
results have been interpreted as consistent with a lower level of tree resistance in
summer. In P. ponderosa however, Paine (1984) observed smaller reaction zones in
summer than in autumn. Tisdale and Nebeker (1992) observed an increase of the
resin flow in P. taeda between May and August.
It has often been reported that old trees are more susceptible than young ones to
bark beetle attacks but no measurement of tree resistance has been performed in this
direction. In Europe, reaction zones induced by single inoculations of Scots pine
with Ophiostoma brunneo-ciliatum have been reported to be longer and to contain
more resin in the oldest trees (Lieutier et al., 1993). In North America, Shrimpton
(1973b) in P. contorta and Raffa and Berryman (1982b) in A. grandis observed that
the resin response was maximum for middle aged trees. DeAngelis et al. (1986)
observed that radial resin duct density in P. taeda was negatively correlated to tree
age.
6.3. Silvicultural aspects
6.3.1. Effect of tree vigor and dominance

Vigor of conifers, such as lodgepole pine in North America and Norway spruce in
Europe, is positively correlated to the critical thresholds of inoculation or attack
densities, whether this vigor is expressed by dominance (Sandness and Solheim,
2002) or productivity indexes (Waring and Pitman, 1983; Mulock and Christiansen,
1986). Ponderosa pine, white spruce (Picea glauca) and white fir ((Abies concolor)
with low productivity indexes or low growth efficiency are also more susceptible to
attacks by beetles than highly vigorous trees (Larsson et al., 1983; Hard, 1985;
Ferrell et al., 1994), and dominated Scots pines are more susceptible than
intermediate or dominant trees (Cedervind et al., 2003). However, Christiansen
(1981 in Bakke, 1983) did not observe any relation between vigor of Norway spruce
and its resistance to beetle mass attacks during a mass outbreak.
Several experiments, such as fertilization, have been performed to modify tree
vigor in order to examine the consequences on tree resistance and its mechanisms.
They are presented below in 6.5.2. Very y little investigations have been done in
natural conditions to measure the effectt of tree vigor on the mechanisms of
resistance, without any artificial treatment. In loblolly pine, the density of resin
ducts was positively correlated with growth rates (DeAngelis et al., 1986),
154 F. LIEUTIER
suggesting a positive effect on the preformed defence mechanisms. However in

Scots pine, Kytö et al. (1999) did not observe any correlation between resin duct
density and preformed resin flow and, after modifying tree vigor by fertilization,
they even observed a weak negative correlation between vigor index and resin flow
or phloem constitutive phenol concentration (Kytö et al., 1998, 1999). In Norway
spruce, Baier et al. (2002) also reported, with increasing radial growth indexes, a
decrease of the constitutive resin flow, accompanied by a decrease in the cross
sectional area of resin ducts and the initial monoterpene content. However, the
effects of vigor can depend on tree activity. Lombardero et al. (2000), modulating
tree growth by combining thinning, dominance and fertilization, reported that the
constitutive resin flow in P. taeda was least during the period of rapid tree growth
(early wood production) but most during latewood production. Results seemed less
variable for the parameters related to induced defence. The induced increase in resin
flow after wounding was greatest in the fastest growing trees, even during their
season of greatest growth (Lombardero et al., 2000). After isolated fungus
inoculations, the mean total monoterpene content at the site of inoculation in grand
fir was lower in suppressed trees than in dominant trees (Raffa and Berryman,
1982b) and reaction zone length t in Scots pine was negatively correlated with
productivity indexes (Lieutier et al., 1993), results which have been interpreted as a
lower induced resistance in suppressed or low productive trees. In A. grandis, resin
production after fungus mass inoculations was greater in high-vigor trees (Filip et
al., 1989). In Norway spruce however, reaction zone length increased with
increasing radial growth indexes (Baier et al., 2002).
6.3.2. Stand density and diversity

Most studies on the effect of stocking and thinning on tree-bark beetle relationships
have been carried out in North American pine forests ((P. contorta, P. taeda, P.
echinata). In all cases, dense stocking and absence of thinning were positively
correlated to attack success or tree mortality by bark beetles (Belanger et al., 1979;
Mitchell et al., 1983; Brown et al., 1987; Bartos and Amman, 1989; Showalter and
Turchin, 1993). Thinning has been reported to increase oleoresin flow rates and tree
growth indexes over about 2 to 3 years when compared to unthinned plots (Mason,
1971; Waring and Pitman, 1985; Mitchell et al., 1983; Matson et al., 1987; Brown et
al., 1987). However, no information is available regarding the effect of thinning on
tree resistance parameters other than oleoresin exudation, and thus no demonstration
has been really provided that the decreases of beetle attacks and tree mortality after
this treatment were caused by increases off tree resistance. On the other hand, in
addition to acting on tree growth and dominance, thinning also induces significant
modifications of the forest microclimate, which have been hypothesized to be the
main factors linking beetle attacks and tree thinning (Amman et al., 1988; Bartos
and Amman, 1989; Bartos and Booth, 1994). In Europe, an integrated approach
carried out in Norway spruce forests revealed that thinning increased the primary
resin flow but did not show any effects on several other resistance parameters, such
as the preformed monoterpene content and the wound reaction development after
low density inoculation with C. polonica (Baier et al., 2002).
Very little information is available on the effects of stand diversity. In North

America, hardwood trees mixed with pines seem to interfere with infestation growth
and to decrease the mortality of pines following induced attacks by D. frontalis
(Showalter and Turchin, 1993). No effect was observed on resin flow in that
experiment. In Europe, Norway spruce trees exhibited higher primary resin flow,
lower reaction zone length and lower relative increase of resin flow in response to
low density inoculations, when growing in mixed species stands than when growing
in pure stands (Baier et al., 2002).
6.4. Relation with phytosanitary problems

The possibility that defoliators and pathogens can predispose trees to be overcome
by bark beetle attacks has been proposed for a long time in Europe (Schwertfeger,
1944; Thalenhorst, 1958; Chararas, 1962), essentially according to empirical
observations, suggesting that these primary aggressors weaken the trees, that is
depress their natural resistance. Only relatively recently, in both North America and
Europe, experiments have been conducted to quantify these observations. Among
them, many refer to tree susceptibility to beetle attacks; some have investigated the
tree resistance mechanisms themselves.
6.4.1. Mistletoe and pathogens

In North America, mistletoe, blister rust on branch and trunk, and root pathogens
((Armillaria mellea) favor infestations by bark beetles in fir and pines (Ferrell, 1974;
Tkacz and Schmitz, 1986; Rasmussen, 1987) att least for endemic populations. For
epidemic populations however, Christiansen and Huse (1980) in Scandinavia did not
find any relation between root infestation of Norway spruce by the butt rot
Heterobasidium annosum and tree susceptibility to I. typographus.
In firs infested by mistletoe, successful beetle attacks were accompanied by very
little or no resin secretions, while the only (failed) attack that occurred on healthy
trees was filled of resin (Ferrell, 1974). In P. resinosa, root disease led to decreased
resin flow (Raffa and Klepzig, 1996), to modifications of monoterpene ratios in
tissues reacting to artificial inoculations by Leptographium terebrantis, but not to
modifications of total monoterpene and phenol concentration in the unwounded
tissues (Klepzig et al. 1995). No European study has dealt with these aspects.
6.4.2. Defoliating insects

Studies dealing with defoliations have generally suggested a significant increase of
tree susceptibility to bark beetle attacks, only in heavily (90 % or more) defoliated
trees. This is the case in North America for example in Abies amabilis defoliated by
the sawfly Neodiprion sp. and then attacked by Pseudohylesinus spp. (McMullen et
al., 1981), and in A. grandis and Pseudotsuga menziesii defoliated by the moth
Orgyia pseudotsugata and subsequently attacked by S. ventralis and D. ponderosae
(Wright et al., 1984). Similar conclusions have been drawn in Scandinavia for Scots
pines defoliated by the sawfly Diprion pini and the moth Bupalus piniaria and
attacked by T. piniperda and T. minorr (Annila et al., 1999; Långström et al., 2001a;
156 F. LIEUTIER
Cedervind et al., 2003) and in Eastern Europe for Norway spruce defoliated by the
moth Zeiraphera diniana before attacks by I.typographus, I. amitinus and P.
chalcographus (Grodski, 1997). Mass inoculations on trees defoliated by B.
piniaria were also able to kill trees only when they suffered at least 90 % defoliation
(Långström et al., 2001b). Wallin and Raffa (2001) however, reported that
colonization of Pinus banksiana by Ips grandicollis increased exponentially in
relation to defoliation level by the moth Choristoneura pinus. In all cases where the
delay was considered, tree susceptibility was maximum one to two years after the
defoliation (Wright et al., 1984; Raffa et al., 1998; Cedervind et al., 2003). In
Northern Spain, Amezaga (1997) observed that the presence of pine processionary
caterpillars (Thaumetopoea pityocampa) in P. radiata and P. sylvestris stands
increased the rate of shoot pruning by T. piniperda in vigorous trees, but not in trees
where dominance was taken by side shoots, thus suggesting an interference with the
tree social status. Shoot damage during the maturation feeding of Tomicus spp. can
be compared to defoliations. In Southwestern China, the critical threshold of bole
attack density by Tomicus sp. on Pinus yunnanensis (that is tree resistance level to
bole attacks) decreases when shoot damage increases, and a critical threshold of
shoot damage (60 % damaged shoots) has been defined above which stem attacks
always succeed in killing trees (Lieutier et al., 2003c). Pruning was sometimes used
to simulate defoliations and reduce photosynthesis in Scots pine and Norway spruce.
It also increased susceptibility to bark beetles or their associated fungi (Långström
and Hellqvist, 1993; Christiansen and Fjorne, 1993).
Parameters involved in various mechanisms of resistance to bark beetles,
concerning both preformed and induced defences, can be affected by defoliations.
Resin flow rate decreased significantly in P. resinosa moderately defoliated in
controlled conditions (Raffa et al., 1998), in P. banksiana and P. sylvestris heavily
defoliated respectively by C. pinus and D. pini (Wallin and Raffa, 2001; Annila et
al., 1999), and in pruned Scots pines (Långström et al., 1993). Opposite results have
however been observed when the defoliation effect is compounded with fertilization
(Kytö et al., 1999). Monoterpene content of preformed resin can also be affected, as
in P. banksiana defoliated by C. pinus (Wallin and Raffa, 1999). Results
concerning the tree induced responses are more variable. In Abies sibirica, Vetrova
et al. (1999) in Russia indicated that all defence parameters, histologically evaluated
through the rate and intensity of response to inoculations with Leptographium sp. in
phloem and xylem tissues, are affected by defoliation due to the moth Dendrolimus
superans sibiricus. In Scots pine, no effect of defoliation or pruning was reported
on reaction zone length, fungus performances, resin acid and phenol content after
isolated inoculations with L. wingfieldii or Ophiostoma ips, or after attacks by T.
piniperda and T. minorr (Långström et al., 1993, 2001b, Croisé et al., 1998; Annila
et al., 1999). Results in North American conifers are more consistent. In A.
grandis, the monoterpene concentration in the reaction zones induced by
inoculations with T. symbioticum decreases in direct proportion to defoliation, and
during two years after defoliation (Wright et al., 1979). In P. banksiana, the phloem
induced response to artificial inoculations with O. ips is affected in its extent, its rate
of monoterpene accumulation, and the changes in monoterpene content, depending
on defoliation intensity and the time since defoliation (Wallin and Raffa, 1999,
2001).
6.5. Relation with water and nutrient availability

Because of observations by foresters and scientists, of coincidences between damage
and climatic or locality factors, the roles of drought and bad soil quality as factors
predisposing trees to bark beetle attacks has been asserted for a long time in Europe,
(Schwertfeger, 1944; Thalenhorst, 1958; Chararas, 1962) and in North America as
well (Keen, 1938; Rudinsky, 1962). In that manner, bark beetle outbreaks have
often been explained by the existence of drought periods supposed to weaken trees
(Pesson and Chararas, 1969; Lieutier et al., 1988a, as examples for Europe). Most
often, especially in experimental approaches, water stress and nutrient availability
have been considered separately.
6.5.1. Water stress

Several approaches to demonstrate and understand the relationships between water
stress and tree resistance to bark beetles have followed seasonal or diurnal variations
of tree water status, in relation to variations in tree susceptibility or defence
mechanisms. Others have attempted to experimentally manipulate water stress.
Both preformed and induced defence mechanisms have been investigated,
depending on the model of tree-bark beetle relationships that was considered. Some
experiments have considered the general resistance level of trees to attacks.
Effects on preformed defence mechanisms. Nothing has been done in Europe in this
field and the major part of the literature corresponds to studies carried out in
Southern North America on loblolly pine with reference to its susceptibility to D.
frontalis.
Studies of seasonal and daily variations in tree water status concluded that water
availability accounts for a large part in resin flow variations (Mason, 1971), that
water stress decreases it (Blanche et al., 1992), and that oleoresin exudation pressure
is related to soil and atmospheric moisture (Lorio and Hodges, 1968a). However,
Lorio and Hodges (1968b) noticedd that resin flow was not reduced until a severe soil
and atmosphere moisture stress occurred. Lorio and Sommers (1986) even
attributed the late summer increase in oleoresin yield [a phenomenon also reported
by Barrett and Bengtson (1964) on P. elliotti] to moderate water deficits at this time.
Lombardero et al. (2000) observed an increase of the oleoresin yield during the
period of latewood formation in loblolly pine, when drought conditions were
limiting tree growth. A study of rainfall conditions prevailing over 52 years in
various southern States concluded, however, that there was no relation between
rainfall and the end of epidemics of D. frontalis (King, 1972).
The first experimental attempt to manipulate tree water status and to quantify the
effect of water stress on preformed defences, was done by Vité (1961) and Vité and
Wood (1961) in California, in relation to the susceptibility of P. ponderosa to I.
confusus and D. brevicomis. They manipulated water availability to trees through
158 F. LIEUTIER
sprinkling and concluded that oleoresin exudation pressure was directly and
inversely related to water stress. In loblolly pine, several experiments were
conducted by digging trenches around trees to diminish soil water reserves (Lorio
and Hodges, 1977), by erecting shelters to prevent rain from reaching the soil (Dunn
and Lorio, 1993), or by cooling the trunk of trees with dry ice, a process supposed to
create an acute water stress (Lorio et al., 1995). In all cases, the stressed trees
showed a reduced resin flow, generally associated with a higher number of
successful attacks by the southern pine beetle, compared to the control trees.
However, in case of a mild stress, the rate of successful attacks was very low on all
trees, which was attributed to the fact that trees could adjust their water regime
(Dunn and Lorio, 1993). It was also suggested that attack success on artificially
stressed trees could depend on the water conditions during the year and tree
ontogeny (Lorio et al., 1995). Indeed, although oleoresin yield was negatively
affected in artificially stressed trees, during a wet year at the moment of earlywood
formation, attacks failed on those trees as well as on control trees but, during a dry
year at the period of latewood formation, attacks succeeded on stressed trees while
they failed on control trees. This is also in favor of the hypothesis that mild water
stress can enhance tree resistance while a severe stress can decrease it (Lorio, 1986).
This hypothesis is corroborated by the observation that, in grand fir saplings, the
constitutive terpene cyclase activity stayed unaltered during a moderate stress but
was reduced significantly during a severe stress (Steele et al., 1995).
Effects of water stress on preformed defence parameters others than resin flow
rate have been poorly investigated. In loblolly pine, the proportion of resin acids in
the xylem oleoresin of artificially stressed trees decreased (Hodges and Lorio,
1975), and soil moisture could influence the monoterpene composition (Gilmore,
1977).
Effects on induced defence mechanisms. Few experiments have been carried out to
directly measure the effects of water stress on the mechanisms of induced defence.
In North America, Ferrell (1978) observed that attacks by S. ventralis caged on the
trunk of severely water stressed A. concolorr were successful and accompanied by
little resinosis in the phloem, while similar attacks in the control trees failed due to
extensive resinosis. Cooling the bole of P. contorta with dry ice caused the
elimination of observable wound response after artificial inoculations with
Ophiostoma clavigerum (Miller et al., 1986). Steele et al. (1995) observed that
wound-inducible terpene cyclase activity in A. grandis was significantly reduced
after both a severe and a mild stress. In Europe, after a severe stress in Scots pine
saplings, Croisé and Lieutier (1993) observed a decrease of the phloem reaction
zone length and the total quantity of induced resin, in response to isolated
inoculations with L. wingfieldii and O. brunneo-ciliatum. Similarly, a slight
decrease in reaction zone length after isolated inoculations with O. ips was observed
when inoculations took place during the period of maximum stress intensity, but no
change was noticed in the phenol composition
m of the reaction zone, and fungal
growth was not affected (Croisé et al., 1998). After mass inoculations with L.
wingfieldii, Croisé et al. (2001) did not reported any change in the intensity of the
phloem induced response in 5-year-old d severely stressed seedlings, although

sapwood water conductivity decreased significantly and conspicuous damage were
observed in the sapwood.
Effects on the tree resistance level itself.

f Such effects of water stress have already
been presented above in some experiments where susceptibility to bark beetles had
been considered simultaneously with tree defence mechanisms. They were mostly
related to preformed defence and to susceptibility to D. frontalis. Other experiments
investigated the effects of water stress directly on tree resistance level, without
referring to defence mechanisms. However, because they mainly concerned bark
beetles of which the success of attacks is thought to depend on the non efficacy of
the induced defence mechanisms, one may suppose that these mechanisms were
affected by water stress.
It has been generally reported that tree resistance (indicated by the critical
threshold of inoculation density) increased with a mild stress and decreased with a
severe stress. In Europe, the levels of resistance of P. abies to mass inoculations
with C. polonica, and that of P. sylvestris to mass inoculations with L. wingfieldii,
were higher in trees submitted experimentally to several months of mild stress than
in the control trees (Christiansen and Glosli, 1996; Dreyer et al., 2002). Similarly in
Southwestern China where wet seasons alternate with dry seasons, an 18-month
study of tree water status in two plots differing in their soil water availability
revealed that P. yunnanensis resistance to mass inoculations with Leptographium
yunnanense was higher during the dry periods and in the dry plots (Ye and Lieutier,
2001). At the other extreme, several successive cycles of severe stress decreased the
level of resistance of Scots pine to mass inoculations with L. wingfieldii (Croisé et
al., 2001). These observations are in agreement with those reported for preformed
defence (Lorio, 1986; Lorio and Sommers, 1986, Lorio et al., 1995). However, no
after effect of an artificial drought repeated three years consecutively was noticed in
Norway spruce, which suggests that trees recover as soon as water is available in
sufficient quantity (Christiansen, 1992).
6.5.2. Nutrient availability

Regarding fertilization effects on conifers – bark beetles relationships, experiments
in North America have been concerned mostly with tree susceptibility to attacks,
whereas European research was focused on the mechanisms of resistance
themselves. The conclusions were generally that fertilization had no or a negative
effect, while tree growth was largely stimulated.
No effect was observed on tree susceptibility in the case of P. taeda exposed to
attacks by D. frontalis and D. terebrans, after N or NPK fertilization (Moore and
Layman, 1978; Matson et al., 1987) and for A. grandis facing S. ventralis attacks
after NPK treatment (Filip et al., 2002). In P. contorta, increasing N nutrition did
not prevent attacks by D. ponderosae until growth improvement exceeded 100 g. of
wood production per m² of foliage (Waring and Pitman, 1985). In Scots pine also,
N fertilization did not modify the ability of T. piniperda to establish egg galleries
and to cause stem damage (Löyttyniemi, 1978). However, the treatment stimulated
160 F. LIEUTIER
tree growth and increased shoot diameter, which resulted in an increase of shoot
attack density during the beetle maturation feeding, because of more suitable sized
shoots.
In Norway spruce and Scots pine, fertilization by N or other nutrients increased
the number of resin ducts but tended to decrease their density, and had no effect or
caused only a very slight decrease on the constitutive resin flow (Kytö et al., 1996,
1998, 1999; Viiri et al., 1999). In other situations however, a more important
decrease of constitutive resin flow or stem resin content was reported, following
fertilization with N, P or K, such as in Picea sitchensis (Wainhouse et al., 1998b)
and in P. taeda (Warren et al., 1999). Results are not clear with phloem constitutive
phenols, as fertilization was observed to cause no effect, a decrease or an increase of
their total concentration (Kytö et al., 1996, 1998; Viiri at al., 1999; Wainhouse et
al., 1998b; Warren et al., 1999). Little attention has been given to effects on
induced defence mechanisms. In Norway spruce, no consequence of fertilization
was observed on the induced resin flow and the length of the phloem lesion that
develops in response to inoculation with C. polonica (Kytö et al., 1996; Viiri et al.,
1999). Viiri et al. (2001) however, reported a decrease in the concentrations of total
terpenes and stilbene aglycons in this reaction zone and suggested a possible
decrease of the tree ability to defend itself against beetle attacks.
6.6. Effects of other damaging agents (Wind, lightning, fire, and pollution)
Research on effects of wind and lightning on conifer susceptibility to bark beetle
attacks has been developed exclusively on P. taeda in Southern North America. A
simulated wind stress including bending stems and pruning branches resulted in a
decrease of oleoresin flow, probably because of the decrease of leaf area due to
pruning (Fredericksen et al., 1995). Although relatively low numbers of beetles
were observed, Dendroctonus and Ips species tended to be trapped in higher
numbers near the stressed trees, but no successful attacks were observed. After
lightning, either natural of simulated, loblolly pine was also more susceptible to
attacks by D. frontalis and various other bark beetle species (Hodges and Picard,
1971; Coulson et al., 1986). Even small numbers of beetles were capable of
overcoming host defences (Flamm et al., 1993), thus demonstrating directly that the
critical threshold of attack density was considerably lowered. Lightning decreased
oleoresin pressure and flow rapidly (Hodges and Picard, 1971; Blanche et al., 1985)
but, 3 weeks after the strike, resin flow was restored while the monoterpene
composition was changed (Blanche et al., 1985).
Effects of fire have been studied in Europe after accidental fires and in North
America after accidental or prescribed fires. In all situations, incidence of fire
increases tree susceptibility to bark beetle attacks. In Spain, Amezaga (1997)
reported an increased number of shoot attacks by T. piniperda in P. radiata. Bole
attacks also are favored. In Scots pine, the fire-damaged trees were reported to be
susceptible mostly during the first two years after fire (Ehnström et al., 1995;
Långström et al., 1999) but after the big 1988 fire in Yellowstone Park, damage by
bark beetles on several conifer species was high until 1992 (Rasmussen et al., 1996).
Susceptibility to bole attacks depended on the importance of fire injury to the crown
or the bole of the trees. T. piniperda successfully attacked Scots pines with less than
25 % foliage while all attacks failed when there was more that 50 % foliage left
(Långström et al., 1999). Colonization attempts by Ips and Dendroctonus species
on fire-damaged P. ponderosa were also positively related to intensity of crown
scorch (Wallin et al., 2003). Pines with no crown damage can also be attacked by
bark beetles when the bole has been scorched (Santoro et al., 2001) and Rasmussen
et al. (1996) observed that high levels of infestations were strongly correlated with
the percentage of basal circumference of the tree that had been fire-killed. Among
the possible mechanisms of resistance that could be affected, only the resin flow was
investigated. Both constitutive and induced resin flow of P. ponderosa was
negatively related to crown scorch intensity (Wallin et al., 2003) but constitutive
resin flow of P. resinosa increased in trees with scorch boles (Santoro et al., 2001).
Pollution increased tree susceptibility to bark beetles in general but its effects
seemed to vary depending on the nature of the pollutant, the tree or the beetle
species. After photochemical oxidant injury, attacks by D. ponderosae and D.
brevicomis on P. ponderosa were positively correlated to the injury (Stark et al.,
1968). Among the killed trees, beetle attack density was higher for the less affected
trees than for the highly affected trees (Dahlsten and Rowney, 1980), which
corresponds to a higher critical threshold of attack density in the former than in the
latter ones. In Czechoslovakia, Norway spruce submitted to sulphur dioxide
pollution was more susceptible, not to attacks by I. typographus, but to attacks by
secondary bark beetles such as Pityogenes chalcographus (Christiansen, 1989). At
the Polish/Czech border, in pollution-damaged Norway spruce stands, P.
chalcographus was also the main pest and trees suffering from more than 60 %
needle loss were predisposed to attacks (Lanz et al., 1993). Regarding the resistance
mechanisms, oleoresin flow decreased butt no change was observed in the terpene
composition in P. ponderosa submitted to oxidant injury (Cobb et al., 1968; Miller
et al., 1968). Along a decreasing gradient of heavy metal pollution in Finland,
constitutive resin flow of Scots pine increased until 4 km from the pollution source
(Kytö et al., 1998). No experiment was concerned with the effect of increased CO2
concentrations on tree susceptibility to bark beetles.
6.7. Synthesis and conclusions on the role of environmental factors

Table 2 synthesizes the effects of the different environmental factors on the tree
resistance level, tree susceptibility and different parameters of the preformed and
induced defences, while separating the results obtained on European tree species
from those obtained on trees growing outside Europe (mainly North America).
6.7.1. Remarks, gaps and particularities

Before commenting on table 2, it must be mentioned that certain parameters used to
indicate the mechanisms of tree resistance should be considered with caution. This
is the case for the absolute length of the induced reaction zone after isolated
inoculations (see 2.1.2). Only the results mentioning the efficacy (e) of this reaction
162 F. LIEUTIER
Table 2: Summary of the effects of environmental factors on various parameters of conifer

resistance to bark beetles and their associated fungi, at the whole tree level and for preformed
defence mechanisms, according to studies carried out in Europe or outside Europe.
Resistance parameters
R
Environmental e Whole tree ------Preformed defenses------
g
Resis- Suscep- Resin Total Terp. Phe-
factors i
tance tibility flow terpe cyclase nols
o
level (2) nes activity
n
(1)
E + - - - -
Tree vigour
O + - -
Stand density or E - o
no thinning O + -
E +
Mixed stands
O - o
Pathogens / E o (**)
Mistletoe O + - o (m) o
E o o
L
Defo- O o o -
liation E - + - (f+)
H
O - + - -
E +
M
Water O + o- + +
E - +
S
stress O + - -
E
U
O + -
E o o- - o-
Fertilization
O o (-) - - +
E
Wind
O -
E
Lightning
O - + - (m)
E o
L
O o o
Fire
E +
H
O + -
E o
L
O o (-) o (+) -
Pollution
E +
H
O - + - o
Levels of stress: L = light or low; H = heavy or high; M = moderate; S = severe; U =

unknown intensity. Area: E = results from European tree species; O = results from trees
growing outside Europe (mainly North America). 1 = critical threshold of attack or
inoculation density; 2 = success of beetle attacks; Quantitative changes: + = increase; - =
decrease; o = no change. Qualitative changes: m = modification of the composition; ** =
epidemic populations. f+ = increase in case of interaction with fertilization
Table 2 (cont.): Summary of the effects of environmental factors on various parameters of

conifer resistance to bark beetles and their associated fungi for induced defence mechanisms,
according to studies carried out in Europe or outside Europe.
Resistance parameters
R
--------------Induced defenses-------------- e Environmental
g
Resin Tree Total Terp. Phe- I factors
flow reac- terpe cyclase nols o
tion nes activity n
(3)
-+ E
Tree vigour
+ + O
o E Stand density or
O no thinning
- - E
Mixed stands
O
E Pathogens /
O Mistletoe
E
L
m O Défo-
-(e) o -o o E liations
H
-(e) - O
E
M
- O Water
-o - o E
S
- -(e) - O stress
E
U
m O
o o - - (*) E
Fertilization
O
E
Wind
O
E
Lightning
O
E
L
o O
Fire
E
H
- O
E
L
O
Pollution
E
H
O
Levels of stress: L = light or low; H = heavy or high; M = moderate; S = severe; U =

unknown intensity. Area: E = results from European tree species; O = results from trees
growing outside Europe (mainly North America). 3 = reaction zone length or efficacy of the
reaction (e). Quantitative changes: + = increase; - = decrease; o = no change. Qualitative
changes: m = modification of the composition; * = decrease of the stilbene aglycones.
164 F. LIEUTIER
should be regarded as reliable. Total concentration of phenols, especially in the

induced reaction zone, has no relationship to tree defence ability. Indeed, both in
spruce and pines, it has been demonstrated that the tree phenol response is not
quantitative but rather qualitative, that is consists mostly in variations in the
proportions of the constituents, the concentration of certain compounds decreasing,
that of others increasing, while several others are neosynthesized (see 2.2.3). In this
context, only the quantitative variations of particular compounds or families of
compounds, those that have been demonstrated to be related to tree resistance or to
have an effect on the aggressors, can be of interest. This is the case, for example,
for stilbene aglycons, catechin, pinosylvin or pinocembrin (see 3 and 6.1).
Even regarding preformed defences, total phenol concentrations have a very
limited interest, since toxicity in this chemical family varies largely from one
compound to another (see 3). On the contrary, total monoterpene concentrations
have a meaning in terms of tree resistance, since all of them increase in response to
attacks and have toxic effects on insects and fungi (see 3). Variations in relative
content are thus less useful here. Unfortunately, in the attempts to try and connect
the chemical characteristics of the tree to its defence mechanisms in relation to
effects of environmental factors, qualitative variations have considered almost
exclusively monoterpenes. In all cases butt one, phenols were considered in relation
to their total concentration.
In table 2, results are generally clear and coherent regarding the effects of
environmental factors on tree susceptibility and the level of resistance itself,
although additional information is needed for this latter parameter, especially
concerning the silvicultural and fertilization effects. Fewer results are available
regarding the effects on resistance mechanisms, i.e. the parameters involved in
defence, but there is consistency if absolute reaction zone length and total phenol
concentration are discarded. In general, except for water stress, defoliation, and
fertilization effects, the mechanisms of induced defences have been very poorly
investigated. Moreover, the effects of fertilization on induced defence mechanisms
have been considered only in Europe, whereas North American studies have
concentrated on water stress and defoliation effects. Even for the constitutive
defences, little is known outside of resin flow variations, although terpenes and
phenols certainly play a decisive role. For all environmental factors, studies of resin
flow have been largely developed in Southern North America. European work on
that parameter concerned only fertilization and silvicultural effects. In the present
social and environmental context, the general lack of data concerning the effects of
silviculture and pollution on tree defence mechanisms against bark beetles
represents a dramatic gap. Even regarding tree susceptibility and resistance, almost
nothing is known on the effects of silviculture and tree diversity.
The effect of tree vigor on resistance may be intriguing since an increase in
resistance (or a decrease in tree susceptibility) due to high vigor, corresponds to a
decrease of the preformed defences. The balance between vigor and preformed
defence can be explained by the growth differentiation balance (GDB) hypothesis,
especially during the period of rapid growth (Kytö et al., 1999; Baier at al., 2002;
Lorio, 1986), but still the increase in resistance with vigor must be clarified. The
stimulation of the induced defence mechanisms, which could become a priority over
growth in cases of wounding (Lombardero et al., 2000) could be a reason. No effect

of fertilization has been observed on tree susceptibility although both the preformed
(resin flow and total terpenes) and induced (total terpenes and stilbene aglycons)
defences are altered (table 2 and see references in 6.5.2). This alteration has been
explained by the above mentioned hypothesis because fertilization stimulates tree
growth (Viiri et al. (2001), but tree susceptibility should increase, the more because
induced defence does not seem to be a priority over growth in that case.
6.7.2. General trends

In spite of the specific relationships reported above for some factors, there are
general trends common to several environmental factors that can be drawn from
table 2.
A dose effect is evident for several factors such as defoliation, water stress, fire
and pollution. Defoliation, fire and pollution, have a depressive effect on tree
resistance (or increase tree susceptibility), and this effect is proportional to the stress
intensity. All three factors have in common an effect on tree vitality through foliage
injury, and their intensity is quantified by the percentage of crown loss or crown
scorch. In these conditions, a dose effect f is not surprising because defence
metabolism is conditioned by photosynthetic activity, through current
photosynthesis or building of reserves. Moreover, photosynthetic activity of the
remaining foliage is probably preferentially directed towards growth rather than
defence metabolism, a priority which could also depend on the extent of foliage
injury. Unfortunately, insufficient data are available to check k if the effects on
defence mechanisms are also proportional to the stress intensity, although this seems
true at least for the effect of fire on the preformed and induced resin flows.
Although many results are difficult to interpret because several experiments have
been carried out without quantifying the stress intensity, it is also clear that a dose
effect of water stress exists. It corresponds however to a completely different
phenomenon, since mild stress increases tree resistance (or decreases tree
susceptibility) whereas a severe stress decreases it. There is no proportionality
between water stress intensity and tree resistance. On the contrary, a threshold of
stress exists on each side of which the effects are opposite. Observations on the
preformed but not the induced defence mechanisms agree with variations in tree
resistance, but too little data are available to conclude definitely on this point. The
GDB hypothesis can explain these results if we admit that tree growth stops very
rapidly, and is affected by water stress before defence, and that photosynthesis
continues until the above mentioned threshold is reached. Recent experiments
suggest that the stress threshold could be linked to predawn needle water potential
value of -1.2 MPa (Dreyer et al., 2002). This value is below that observed during
drought in temperate zones at the period of beetle flight, where generally only mild
stresses occur. This means that the reason for many outbreaks may not be a
decrease in tree resistance due to drought (Christiansen and Glosli, 1996; Dreyer et
al., 2002; Lieutier et al., 2003a).
Preformed and induced defences can vary in opposite direction with the same
factor, even under the same stress intensity. This has been mentioned above for the
166 F. LIEUTIER
effect of tree vigor (see 6.7.1). It has also been observed under a mild water stress in
A. grandis, where constitutive terpene cyclase activity is stimulated while induced
terpene cyclase activity is reduced (Steele et al., 1995). In cases of severe stress,
however, both activities are reduced. According to Lombardero et al. (2000), the
fact that constitutive and induced defence can be differentially affected by
environmental conditions could be one explanation for the existence of conflicting
results regarding environmental effects on plant anti-herbivore defences in general.
Interference between factors can modify the characteristics off the tree defences
against a given factor. For example, it has been mentioned above (see 6.3.2) that
thinning can affect tree resistance through stimulation of growth and modification of
social status, but it also modifies the forest microclimate which can have
consequences on both insect biology and tree defences. More complex interactions
may take place. Fertilization seems to be able to change the direction of the effects
caused by other factors. In the absence of any treatment, it has often been reported
that constitutive resin flow decreases when defoliation increases (see 6.4.2), but a
positive relation between resin exudation and the intensity of defoliation by D. pini
has been found in fertilized Scots pine, suggesting that defoliation stimulates resin
production in the stem (Kytö et al., 1999). Similarly, in a cross experiment
combining drought and fertilization treatments, fertilization has been observed to
moderate drought effects on tree resistance to mass inoculations of Scots pine with
O. brunneo-ciliatum (Guérard et al., 2000).
6.7.3. Explanatory theories

Several models have been proposed to explain the role of the environment on plant
secondary metabolites and its involvement in resistance to attacks by plant-feeders:
growth-differentiation balance (Loomis, 1932; Lorio, 1986; Herms and Mattson,
1992), carbon-nutrient balance (Bryant et al., 1983), plant stress hypothesis (White,
1984; Mattson and Haack, 1987), optimal allocation (Tuomi et al., 1991). All aim at
defining general mechanisms, and conifer bark k beetles and their associated fungi are
only one component of a complex approach taking into consideration results from
many experiments carried out separately with various species belonging to different
guilds and submitted to different environmental factors. It is thus not surprising that
none of these models has led to a general consensus (Koricheva et al., 1998). It is
however concluded generally that different models may apply to different guilds. In
addition, only one environmental factor is generally considered in each experiment,
and it is difficult to extrapolate to natural conditions where several factors interfere
with each others. An interesting approach already considered in some experiments
is to study only one insect guild with several environmental factors in combination.
Regarding bark beetles, I will only note that, compared to other groups of
insects, bark beetles that attack living trees form a homogeneous guild although
different life cycles and strategies can be distinguished. They have intimate
relationship with their hosts because they spend the major part of their life cycle
inside them, and because host resistance is the key factor of their population
dynamics. They thus seem an insect model favorable to test the effects of
environmental factors on tree resistance to attacks. However, the situation is
complicated by the important role played by the fungi in the relationships with the
tree. Even for this group alone, many gaps, visible in table 2, need to be filled
before trying to build a general theory. In addition, to progress in the understanding
of the mechanisms by which environmental factors affect tree resistance, it will also
be necessary to distinguish the effects that the modifications in the tree physiological
parameters have on the insect itself from those that they have on its associated fungi.
The effects resulting from the consideration of several environmental factors in
combination in controlled conditions should also give interesting information on the
mechanisms.
7. UTILIZATION OF RESISTANCE IN BARK BEETLE MANAGEMENT

This aspect has been presented recently both t from a general point of view (Lieutier,
2002) and for possibilities of utilization in Central and Western Europe (Heidger and
Lieutier, 2002). They will thus not be developed here. I will only reformulate the
major ideas and underline, among the numerous potential applications of conifer
resistance to bark beetles, the research topics that seem most likely to yield practical
applications in the context of a modern forestry.
Tree selection for resistance is a classical but still promising application. The
phenolic predictors of tree resistance that have already been proposed for Scots pine
and Norway spruce (see 6.1) could be used as resistance markers in breeding
programs, in addition to other desirable characteristics of the tree. Other predictors
belonging to the same chemical family could certainly be discovered in other conifer
species. This supposes research on the possibilities to use these predictors at the
juvenile stage of the tree. Research on possible counter-adaptations by beetles and
fungi are also needed, even if the chance for such adaptations may seem lower than
with other insect guilds (Lieutier, 2002).
In the context of global change and biological invasions, bark beetles may
encounter new hosts. Studies on factors that allow beetles and fungi to adapt to tree
resistance mechanisms will also give useful information to evaluate the risk of
damage and to help foresters to define options available for forest protection.
Regarding climatic change, detailed studies on the effects of environmental
factors, such as water stress, pollution, and fire, on tree defence mechanisms will
have practical applications in the field of risk prediction and physiological
improvement of trees by adapted silvicultural methods. Research on effects of
fertilization on tree resistance has demonstrated that this treatment can be beneficial
to forestry when considering bark beetle problems, since it increases tree
productivity without affecting the risk of damage (table 2). Similarly, clarifying the
effects of thinning, and understanding the role of tree biodiversity on tree resistance,
will also lead to improvements of silvicultural methods.
8. CONCLUSIONS
Knowledge of mechanisms of tree resistance to attacks by bark beetles and their
associated fungi has improved considerably since the pioneer papers by Vité (1961),
168 F. LIEUTIER
Reid et al. (1967) and Berryman (1972), especially during the last 30 years in North
America and the last 20 years in Europe. However, many aspects are still not
understood and need to be investigated. Questions and research prospects have been
listed and presented recently while considering the general state of knowledge of
conifer resistance to bark beetles (Lieutier, 2002). Research in relation to
environmental factors is particularly needed in the present environmental situation
and some directions have been proposed above (see 6.7 and 7). This concluding
section will provide a synopsis of the strengths and gaps in our understanding of the
mechanisms of resistance of the European conifer species to European bark beetle
species, through a comparison with the state of knowledge on the North American
species.
Research really started in Europe in the early 80’s with works developed on the
resistance of P. abies to I. typographus and its associated fungus C. polonica
(Christiansen and Horntvedt, 1983; Horntvedt et al., 1983). Resistance of P.
sylvestris to Ips and Tomicus species began to be studied later (Lieutier et al., 1988b;
Lieutier and Ferrell, 1988; Långström & Hellqvist 1988). Practically, among the
native species, only these two conifers have been considered since. The species
range considered in North America has not been much higher, the studies focusing
mainly on P. taeda (sometimes associated with P. echinata), P. ponderosa, P.
contorta and A. grandis. Much less attention has been given to Pinus pinaster,
Picea obovata and P. sitchensis (introduced) in Europe, and to Douglas fir
(Pseudotsuga menziesii), A. concolor, Pinus elliottii, Pinus radiata and Picea glauca
in North America. However, considering that there are 31 species of Pinaceae in
Europe (North Africa included) and 57 in North America (Mexico excluded)
(Debazac, 1977), the ratio of species studied is about the same in both continents.
Outside Europe and North America, at least 95 Pinaceae species live in Asia and 32
in Central or South America (Debazac, 1977). Among them, only Pinus
yunnanensis in Southwestern China has been studied t so far for the mechanisms of
resistance to bark beetles. Little has been done in conifer families other than
Pinaceae but they are not concerned with bark a beetle damage, except some species
of Cupressaceae in the Mediterranean areas. In hardwood trees, only elms (Ulmus
spp.) have been studied, but only for resistance to the fungus (Ophiostoma ulmi)
itself.
Regarding the beetle species, mainly I. typographus, I. sexdentatus, and T.
piniperda have been considered in Europe with, to a lesser extent D. micans and I.
acuminatus. In North America, the species concerned are mainly D. frontalis, D.
ponderosae, and S. ventralis, with less frequently D. brevicomis D. pseudotsugae, D.
terebrans, I. pini and I. confusus. Similarly to tree species, the ratio of studied insect
species to available species is similar on both sides of the Atlantic. However, a
considerably higher number of North American papers is published each year,
reflecting different research efforts in terms of number of scientists and institutions
involved.
All tree resistance mechanisms that have been presented in this chapter (see 2.1)
certainly exist in both regions. However, induced resin flow has been described
only in loblolly pine, while the existence of delayed resistance has been clearly
demonstrated in Norway spruce only. Hypersensitive reactions have, by far, been
much more studied than the other resistance mechanisms both in North America and
in Europe, but preformed resistance has been studied mainly in North America. The
reasons are that North America has economically important beetles both among
those species where resin flow is a major resistance factor ((D. frontalis) and in those
species where induced resistance plays the main role (D. ( ponderosae). In Europe,
except against D. micans, the major factor of conifer resistance to the economically
important European bark beetles are induced defences (see 4).
In the field of the mechanisms involved in the hypersensitive reaction, research
has depended on the topics considered and may have concentrated on either
European or North American tree species. The relative role of beetle tunnelling
activity and the associated fungi in the induction and stimulation of this reaction was
demonstrated in Scots pine and was then extended to other conifers (see § 2.2.2).
Collaboration between North American and European teams on Norway spruce
established the essential role of the P.P. cells. This role was then extended to other
kinds of defences (see § 2.2.2). The biochemical characteristics of the tree response
have been investigated mainly in North American pines for terpenes, but in Norway
spruce and Scots pine for phenols. However, little European research has dealt with
the mode of action upon the aggressors. The mechanisms of tree death and the
pathogenicity of beetle associated fungi have been studied in both areas, depending
on the beetle species considered, but still no definite explanation is available for the
former aspect.
The effects of environmental factors on tree resistance and defence mechanisms
have been investigated largely on both North American and European species, but
unequally depending on the factor considered (see 6.7 and table 2). For example,
effects of water stress and defoliation have been studied about equally, but the
fertilization effects were more thoroughly considered on Scots pine and Norway
spruce. Models on the role of host resistance in bark beetle population dynamics
have concerned almost exclusively North American species.
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Chapter 10
FUNGAL ASSOCIATES OF EUROPEAN BARK

BEETLES WITH SPECIAL EMPHASIS ON THE
OPHIOSTOMATOID FUNGI
T. KIRISITS
BOKU – University of Natural Resources & Applied Life Sciences, Vienna, Institute
of Forest Entomology, Forest Pathology & Forest Protection, Hasenauerstraße 38,
A-1190 Wien, Austria,
1. INTRODUCTION
Fungi are common and well-known associates of bark beetles (Coleoptera:
Scolytidae). The relationship between fungi and scolytids was recognized relatively
long ago. Schmidberger (1836) described an “ambrosia” in the galleries of the
wood-inhabiting bark beetle Xyleborus dispar, and Hartig (1844) discovered the
fungal nature of this “ambrosia” lining the tunnels of the insects. Likewise, Hartig
(1878) first recognized the interrelationships between insect damage, discoloration
of wood and fungi, and during his studies on blue-stain in the sapwood of conifers,
Münch (1907, 1908) observed that blue-stain in living trees and lumber is associated
with attack by bark beetles. Since these early discoveries a large number of
investigations on various aspects of the association of fungi with bark beetles have
been carried out.
Scolytids are among the most economically important pests of the world´s
forests, especially conifer forests in the boreal and temperate regions of the Northern
hemisphere (Postner 1974; Schwerdtfeger 1981; Wood 1982; Wood and Bright
1992). A considerable number of fungal associates of bark beetles are known as
forest pathogens in their own right, causing vascular wilt orr vascular stain diseases
(Webber and Gibbs 1989; Harrington 1993a, 1993b; Wingfield et al. 1993). Many
other species give rise to discoloration in the sapwood of conifers and cause
enormous losses to forestry and wood industry worldwide (Whitney 1982; Seifert
1993; Butin 1996).
Although the association between scolytids and fungi has been recognised for
more than one century, many fundamental aspects of this relationship are still poorly
181
181–235.
© 2007 Springer.
182 T. KIRISITS
known. A key question pertaining to the symbiosis between bark beetles and fungi is
that regarding the degree of dependence off the partners on each other. Many fungi
are totally dependent on their associated insects for dissemination and they have not
been found outside the bark beetle habitat (Mathiesen-Käärik 1953; Francke-
Grosmann 1967; Whitney 1982; Kirschner 1998; Six 2003). Similarly, one group of
scolytids, the ambrosia beetles, are obligatorally dependant on certain fungi, the
ambrosia fungi, for nutrition (Francke-Grosmann 1967; Postner 1974; Norris 1979;
Beaver 1989). However, the role of fungi associated with bark beetles that colonize
the phloem of trees has been the subject of cnsiderable debate, and arguments exist
both for and against the view that the insects and the fungi they carry are mutualists
(e. g. Francke-Grosmann 1967; Whitney 1982; Christiansen et al. 1987; Harding
1989; Harrington 1993a, Wingfield et al. 1995; Krokene 1996; Paine et al. 1997).
In this chapter a synthesis of the knowledge regarding the association of fungi
with bark beetles is presented. This synthesis will focus on European scolytids and it
deals mainly with fungal associates of conifer bark beetles. This is because they
have been most intensively studied, in contrast to scolytids on hardwoods where
much less knowledge is available. This review also highlights the ophiostomatoid
fungi which include the ascomycete genera Ceratocystis, Ceratocystiopsis and
Ophiostoma and related anamorph genera, causing tree diseases and blue-stain on
trees and lumber. Fungal pathogens of bark beetles are treated by Wegensteiner
(chapter 12) and are thus excluded here.
2. OVERVIEW OF THE ASSOCIATION OF FUNGI WITH BARK BEETLES IN

RELATION TO BARK BEETLE ECOLOGY
The large majority of bark beetle species fulfil most of their life cycle in the wood or
secondary phloem underneath the bark of conifer and deciduous trees (Postner 1974;
Schwerdtfeger 1981; Wood 1982; Wood and Bright 1992; Pfeffer 1995). Two major
groups, ambrosia beetles and phloeophagous bark beetles, are commonly
distinguished based on their habitats and larval feeding habits (Francke-Grosmann
1966, 1967; Postner 1974; Beaver 1989; Wood 1982; Pfeffer 1995). These two
groups differ greatly in their nutrition biology and also show fundamental
differences in their association with fungi. Another group, the phloeomycetophagous
bark beetles that feed both on phloem and on associated fungi are also considered
(Francke-Grosmann 1952, 1966, 1967; see below and 6.2.2.).
One group of bark beetles, termed “ambrosia beetles” or “xylomycetophagous
bark beetles” breeds in the wood of trees (Francke-Grosmann 1966, 1967; Postner
1974; Beaver 1989; Pfeffer 1995). The ambrosia beetles also include the platypodid
beetles (Coleoptera: Playtypodidae) with only one species, Platypus cylindrus
occurring in Europe (Postner 1974; Pfeffer 1995). Wood is a poor substrate for
nutrition of insects, since they are not able to digest lignin, cellulose and
hemicelluloses, which are the main constituents of the xylem (Francke-Grosmann
1967; Graham 1967; Beaver 1989). Ambrosia beetles have overcome this problem
through ectosymbiosis with nutritionally obligate fungi (Francke-Grosmann 1966,
1967; Graham 1967; Postner 1974; Beaver 1989; Berryman 1989; Six 2003). The
FUNGAL ASSOCIATES OF BARK BEETLES 183
larvae of ambrosia beetles feed on specific fungi, known as “ambrosia fungi” that
are transported to newly colonised trees and cultivated by the adult insects.
Although ambrosia beetles can sometimes attack and kill living trees they usually
breed on dying or recently killed trees and fresh logs and degrade timber (Postner
1974; Schwerdtfeger 1981).
The second, much larger group of bark beetles lives in the phloem of hardwood
and conifer trees. They are referred to as “phloeophagous”, “phloem-feeding” or
“true bark beetles” (Postner 1974; Schwerdtfeger 1981; Wood 1982; Wood and
Bright 1992; Pfeffer 1995). Phloem provides a nutrient-rich source of nutrition for
the insects and in contrast to ambrosia beetles most phloem-feeding bark beetles are
most likely not dependent on their fungal associates for nutrition (Francke-
Grosmann 1967; Whitney 1982; Harding 1989). However, phloem-feeding bark
beetles are commonly associated with various fungi, in particular blue-stain fungi
belonging to the ascomycete genera Ophiostoma and Ceratocystis and their
anamorphs (e. g. Mathiesen-Käärik 1953; Francke-Grosmann 1967; Whitney 1982;
Beaver 1989; Raffa and Klepzig 1992; Krokene 1996; Paine et al. 1997; Kirschner
1998; Jacobs and Wingfield 2001; Six 2003).
Some phloem-feeding bark beetles, especially on conifers, are amongst the most
economically important forest pests. Under certain circumstances these scolytids
attack living trees and cause long-lasting and destructive outbreaks. In Europe, Ips
typographus on Norway spruce is considered as the most aggressive and most
economically inportant bark beetle species (Christiansen and Bakke 1988), but there
are also many other scolytids that cause considerable damage to European forestry
(Postner 1974; Schwerdtfeger 1981)
In order to utilize living trees for breeding, bark beetles must overcome the tree´s
defence systems and kill their hosts (Postner 1974; Christiansen et al. 1987; Raffa
and Klepzig 1992; Krokene 1996; Paine et al. 1997; Lieutier 2002 and chapter 9).
Overcoming the resistance of the host tree is accomplished by a co-ordinated mass
attack of many individuals, which exhausts the anatomical and biochemical host
defenses and is followed by tree death (Christiansen et al. 1987; Raffa and Klepzig
1992; Lieutier 2002 and chapter 9). For bark beetle species that attack living trees
and kill them by this “cooperative strategy” (Lieutier 2002 and chapter 9) the
association with pathogenic blue-stain fungi has always been suspected to be of
great significance (Berryman 1972; Whitney 1982; Christiansen et al. 1987; Raffa
and Klepzig 1992; Krokene 1996; Paine et al. 1997; Lieutier 2002 and chapter 9).
Associated blue-stain fungi might help their insect vectors to overcome and kill their
host trees by contributing to exhaust the tree´s defense mechanisms (see 3.3.1. and
6.2.1.; Lieutier chapter 9). Among true bark beetles in Europe, one species,
Dendroctonus micans is unusual, because it individually attacks trees and behaves
like a true parasite that initially does not kill its host (Gregoire 1988; Lieutier 2002
and chapter 9). As part of the solitary, “defence-avoiding attack strategy” (Lieutier
2002 and chapter 9), associated blue-stain fungi do not play an important role in the
successful breeding of D. micans in living trees (Lieutier et al. 1992; Lieutier 2002
and chapter 9).
Despite the traditional distinction between xylomycetophagous and
phloeophagous bark beetles, some species seem to be intermediate between these
184 T. KIRISITS
two groups. In Europe, two species on pine, Tomicus minorr and Ips acuminatus
share characteristics of both mycetophagous and phloeophagous scolytids and one
may best refer to them as phloeomycetophagous bark beetles (Francke-Grosmann
1952, 1966, 1967; see 6.2.2.). Consequently, they are regularly associated with
Ambrosiella species that are typical ambrosia fungi of xylmycetophagous scolytids
and with blue-stain fungi in the genus Ophiostoma that are common associates of
phloeophagous bark beetles (Mathiesen-Käärik 1953; Francke-Grosmann 1952,
1967).
One form of behaviour in some phloem-feeding bark beetles has important
consequences regarding the transmission off virulent forest pathogens. Elm bark
beetles in the genus Scolytus fulfil their maturation feeding requirements on twig
crotches in the crown of trees and this leads to efficient transmission of the Dutch
elm disease pathogens Ophiostoma ulmi and Ophiostoma novo-ulmi from diseased
to healthy elm trees (Postner 1974; Webber and Brasier 1984; Webber and Gibbs
1989). Scolytus intricatus on Quercus spp. shows a similar behaviour and might thus
be an efficient vector of the oak wilt pathogen Ceratocystis fagacearum, if it were
accidentally introduced from North America into Europe (Webber and Gibbs 1989).
3. TAXONOMY, BIOLOGY AND ECOLOGY OF FUNGI ASSOCIATED WITH

BARK BEETLES
Fungi associated with bark beetles have been grouped based on various
characteristics. They have been classified as mycangial or non-mycangial,
describing whether they are disseminated in mycangia (see 4.) or not (Paine et al.
1997; Six 2003). The term “ambrosia fungi” is used for those fungal associates of
ambrosia beetles, which are cultivated in the galleries of the insects and on which
the beetles depend for nutrition (Francke-Grosmann 1967; Norris 1979; Beaver
1989). Both classifications refer to the ecology of the fungi, but do not consider their
taxonomy. The various fungi associated with bark beetles belong to the yeasts (3.1.),
basidiomycetes (3.2.), ascomyctes (3.3.) and anamorphic fungi without sexual states
(3.4.). Zygomycetes have occasionally also been reported as associates of bark
beetles (Whitney 1982; Harding 1989; Kirschner 1998; Jankowiak 2004), but they
are casual and inconsistent elements in this ecological niche and will not be treated
in detail here.
3.1. Yeasts
Yeasts are commonly associated with phloeophagous bark and ambrosia beetles
(Grosmann 1931; Siemaszko 1939; Callaham and Shifrine 1960; Francke-Grosmann
1967; Zimmermann 1973; Whitney 1971, 1982; Bridges et al. 1984; Harding 1989;
Leufvén and Nehls 1986; Furniss et al. 1990; Six 2003). Very little is known about
the taxonomy of yeasts associated with scolytids, the species assemblages occurring
with bark beetles and the effects of yeasts on the insects. Taxonomically, all yeasts
associated with bark beetles probably belong to the ascomycetes (Six 2003).
In many studies on the mycobiota of bark beetles yeasts have been recorded, but
their identity has only rarely been determined (e. g. Grosmann 1931; Bramble and
Holst 1940; Callaham and Shifrine 1960; Zimmermann 1973; Bridges et al. 1984;
Leufvén and Nehls 1986; Furniss et al., 1990; Solheim 1992b; Krokene 1996; Six
2003). Species that are associated with ambrosia
m beetles have occasionally been
reported as ambrosia fungi, thus being nutritionally important for the insects
(Francke-Grosmann 1967). They are also suspected to be nutritionally important for
phloeophagous bark beetles (Whitney 1982; Strongman 1986; Pignal et al. 1988;
Harding 1989). Yeasts have been isolated from the outer surface of adult beetles and
their immature stages as well as from the digestive tracts of larvae and mature
insects (Grosmann 1931; Leufvén and Nehls 1986; Furniss et al. 1990; Six 2003).
They are also common in the breeding galleries and pupal chambers of bark beetles
(Bridges et al. 1984). In early stages of the breeding development of bark beetles,
yeasts are among the most frequent micro-organisms that can be isolated from the
phloem and xylem adjacent to the insect galleries (Bramble and Holst 1940; Käärik
1975; Bridges et al. 1984; Kirisits 1996), but they do not display pathogenicity to
their host trees (Callaham and Shifrine 1960). In isolations directly from bark
beetles, yeasts occur more frequently than the blue-stain fungi, while the opposite is
true for isolations from the wood of bark beetle-infested trees (Furniss et al. 1990;
Solheim 1992b).
Individual bark beetle species often carry
y not only one, but two or several yeast
taxa (Callaham and Shifrine 1960; Whitney 1982; Leufvén and Nehls 1986; Six
2003). The yeasts associated with bark beetles are relatively unspecific and one
fungal species is usually associated with several insect species (Callaham and
Shifrine 1960; Six 2003). Most bark beetle-associated yeasts belong to the genera
Candida, Pichia, Hansenula, Saccharomyces and Cryptococcus (Callaham and
Shifrine 1960, Whitney 1982; Leufvén & Nehls 1986; Harding 1989; Six 2003). The
most detailed study on yeasts associated with bark beetles in Europe was carried out
by Leufvén and Nehls (1986) who studied the yeasts occurring with I. typographus.
At least six different yeasts were recorded, with Hansenula holstii and Candida
diddensii type yeasts being most prevalent (Leufvén and Nehls 1986).
3.2. Basidiomycetes
Basidiomycetes have only occasionally been mentioned as associates of bark beetles
(Siemaszko 1939; Whitney 1982; Klepzig et al. 2001a, 2001b; Six 2003), but their
diversity in this habitat may have been underestimated thus-far (Kirschner 1998,
2001). In Europe, Gloeocystidium ipidophilum was described from galleries of I.
typographus on Norway spruce in Poland (Siemaszko 1939). This fungus was not
mentioned again for a long time, but it was recently also found in Germany
(Kirschner 1998) Poland (Jankowiak 2004) and Austria (Grubelnik 1998), in the the
same niche as the one originally reported for it. A hymenomycete similar, but not
identical to G. ipidophilum was isolated from the sapwood of Picea abies infested
by I. typographus in Norway (Solheim 1992b). Heterobasidion annosum, the causal
agent of Annosum root rot (Butin 1996) has occasionally been found to be
186 T. KIRISITS
associated with bark and ambrosia beetles on conifers (Bakshi 1950; Harding 1989;
Kirschner 1998). The vector relationships between bark beetles and H. annosum are
likely only casual.
Recently, knowledge on the association of basidiomycetes with bark beetles in
Europe has been improved by Kirschner (1998, 2001) who isolated 20 kryptic
basidiomycetes from the insects or from bark beetle galleries. Most of these
basidiomycetes represent new taxa and at least some of them are suspected to be
consistently associated with bark beetles. Their trophic roles may be diverse, and
many of these newly detected basidiomycetes are likely mycoparasites or
mycophilous fungi (Kirschner 1998). A few North American bark beetle species,
partcularly Dendroctonus species and Ips avulsus appear to be intimately associated
with basidiomycetes, which is in contrast to the situation in Europe (Six 2003 and
references therein). These basidiomycetes belong to the genus Entomocorticium,
including five species known to be associated with bark beetles (Whitney et al.
1987; Klepzig et al. 2001a, 2001b; Six 2003 and references therein).
3.3. Filamentous ascomycetes

Filamentous ascomycetes have long been known as common associates of bark
beetles. Fungi belonging to the genera Ceratocystis, Ceratocystiopsis and
Ophiostoma are the most prevalent and most important associates of phloeophagous
bark beetles and they are also known to occur in the galleries of wood-inhabiting
scolytids (Mathiesen-Käärik 1953; Francke-Grosmann 1967; Zimmermann 1973;
Upadhyay 1981; Whitney 1982; Wingfield et al. 1993; Krokene 1996; Paine et al.
1997; Kirschner 1998; Six 2003). These principal fungal associates of phloem
feeding bark beetles have received mostt attention, which is not surprising
considering their economic importance as tree pathogens and agents of sapstain.
However, it is worth mentioning that diverse assemblages of other ascomycetes with
various tropic roles are associated with barkk beetles, some of which seem to have a
consistent relationship with the insects (Kirschner 1998, Malloch and Blackwell
1993). In this review, I focus on the ophiostomatoid fungi and refer to Kirschner
(1998, 2001) and Malloch and Blackwell (1993) for an overview of other
ascomycetes associated with bark beetles.
3.3.1 The ophiostomatoid fungi

Together with other ascomycetes, Ophiostoma, Ceratocystis and Ceratocystiopsis as
well as related asexual fungi in the genera Leptographium, Pesotum,
Hyalorhinocladiella, Sporothrix and Thielaviopsis are known as the
“ophiostomatoid fungi” (Wingfield et al. 1993). This common name was introduced
in the 1990s taking the similarities of these fungi into account. Ophiostomatoid
fungi associated with bark beetles are also commonly known as “blue-stain fungi”,
referring to the damage these fungi cause, namely blue, gray, brown or even black
discoloration of the sapwood of trees, mostly on conifers (Münch 1907; Lagerberg
et al. 1927; Seifert 1993; Butin 1996; Fig. 1).
Figure 1. Blue-stain in the sapwood of Norway spruce infested by the bark beetle Ips
typographus.
Blue-stain is considered as serious problem in conifer trees (Seifert 1993; Butin

1996), however, hardwoods are also affected (Butin and Zimmermann 1972;
Kowalski and Butin 1989; Kowalski 1991; Seifert 1993). On hardwoods, these fungi
more often cause vascular wilt and vascular stain diseases (Kile 1993; Harrington
1993; Brasier 2000). Sap stain is caused by fungal hyphae, which are concentrated
in the ray parenchyma cells and resin ducts of infected sapwood (Münch 1907; Liese
and Schmid 1961; Ballard et al. 1984; Seifert 1993; Gibbs 1993). Tracheids are also
colonized, especially at later stages of infection (Liese and Schmid 1961; Ballard et
al. 1982; Seifert 1993; Gibbs 1993).
Blue-stain fungi utilise assimilates stored
d in the living ray parenchyma cells of
the sapwood (Seifert 1993; Butin 1996). In contrast to decay fungi, they do not
decompose the structural components of the wood (cellulose, lignin and
hemicelluloses) (Münch 1908; Seifert 1993). The moisture content of the sapwood is
important for the development of blue-stain. Most blue-stain fungi grow at moisture
content between 30-40 % and 130-140 % of the dry weight, with different fungal
species having different requirements (Münch 1908; Lagerberg et al. 1927; Butin
1996). Pathogenic blue-stain fungi that cause stain in living trees are able to infect
fresh sapwood with high moisture content and low oxygen levels (Münch 1908;
Lagerberg et al. 1927; Scheffer 1986; Solheim 1991).
Taxonomy of the phiostomatoid fungi. Ophiostoma and Ceratocystis have many

morphological characters in common, including perithecia with globose or pear-
shaped bases and long perithecial necks (Fig. 2), evanescent asci and hyaline, one-
celled, small ascospores, which vary in their shape and possess or lack sheaths (Hunt
1956; Upadhyay 1981; De Hoog and Scheffer 1984; Wingfield et al. 1993;
188 T. KIRISITS
Harrington and Wingfield 1998; Jacobs and Wingfield 2001). Based on their
similarities Ophiostoma and Ceratocystis have been considered as synonyms for
long periods of their taxonomic history. The third related genus, Ceratocystiopsis
forms a morphologically well-defined group and is characterised by an unique
combination of features, namely relatively small ascocarps, short perithecial necks
with convergent ostiolar hyphae and sickle-shaped, sheathed ascospores (De Hoog
and Scheffer 1984; Upadhyay and Kendrick 1975; Upadhyay 1981; Wingfield
1993). There are, however, various arguments relating to whether these fungi should
be treated together with Ophiostoma.
It is now widely accepted that Ceratocystis is not closely related to Ophiostoma
and Ceratocystiopsis, despite the similarities in their perithecial characteristics (De
Hoog and Scheffer 1984; Wingfield et al. 1993; Jacobs and Wingfield 2001).
Phylogenetic studies based on analyses of the rDNA sequence data placed
Ophiostoma in a monophyletic group close to the Diaporthales, while Ceratocystis is
closely related to taxa in the Microascales (Spatafora and Blackwell 1993; Hausner
et al. 1993b; Paulin-Mahady et al. 2002). Ceratocystiopsis, though morphologically
well defined, groups phylogenetically together with Ophiostoma and these genera
have thus been synonimized (Hausner et al. 1993a). However, Ceratocystiopsis is
still widely used as genus name and it is also treated as separate from Ophiostoma in
the present review.
Figure 2. Perithecia of Ceratocystis polonica.
The similar ascocarps of Ceratocystis, Ophiostoma and Ceratocystiopsis evolved

separately from each other, likely as adaptions to the bark beetle habitat. Besides
molecular markers the separation of Ceratocystis from Ophiostoma and
Ceratocystiopsis is supported by several lines of evidence. Most distinctively, these
genera can be differentiated based on their asexual stages. Ceratocystis species have
Thielaviopsis anamorphs (De Hoog and Scheffer 1984; until very recently known as
Chalara, Paulin-Mahady et al. 2002), with endogenous conidium development by

“ring wall building” (Minter et al. 1983). In contrast, asexual stages of Ophiostoma
belong to a variety of hyphomycete genera including Leptographium, Pesotum (until
recently known as Graphium; Okada et al. 1998, 2000), Sporothrix and
Hyalorhinocladiella (De Hoog and Scheffer 1984), and conidium development is
always exogenic by “apical wall building” (Minter et al. 1982). Similarly,
Ceratocystiopsis spp. have Hyalorhinocladiella and Sporothrix anamorphs, but not
Leptographium and Pesotum states (Upadhyay 1981; De Hoog and Scheffer 1984;
Wingfield 1993). Other than these characteristics Ophiostoma and Ceratocystiopsis
are very similar, if not identical (De Hoog and Scheffer 1984; Wingfield 1993), and
therefore, subsequent discussion will deal with Ophiostoma as including
Ceratocystiopsis. There are also differences between Ophiostoma and Ceratocystis
in the development of the ascospores and the arrangement and organisation of the
asci in the perithecium (Van Wyk and Wingfield 1990; Van Wyk et al. 1993).
Species off Ophiostoma and Ceratocystis also differ in the chemical composition
of their cell walls (De Hoog and Scheffer 1984 and references therein). Ophiostoma
spp. are unusual within the ascomycetes, since their cell walls contain besides chitin
also cellulose and rhamnose (De Hoog and Scheffer 1984). In contrast, the cell walls
of Ceratocystis consist mainly of chitin and do not contain any detectable amounts
of cellulose and rhamnose (De Hoog and Scheffer 1984). In addition, Ophiostoma
and Ceratocystis differ in their tolerance to the antibiotic cycloheximide that inhibits
the protein synthesis in most eucaryotic organisms (Harrington 1981). While
Ceratocystis is very sensitive to even low concetrations of cycoheximide, species of
Ophiostoma tolerate high concentrations of this antibiotic (Harrington 1981; De
Hoog and Scheffer 1984).
Ecology of the ophiostomatoid fungi. Ceratocystis and Ophiostoma also display

differences in their ecology and their relationships with insects (Harrington 1987,
1993a; Kile 1993). Ceratocystis species colonize a variety of herbaceous and woody
plants (Kile 1993). Many species are distributed in subtropical and tropical regions
of the world and some others occur on woody plants in temperate and boreal
regions, causing blue-stain in the sapwood of conifers (Harrington 1987; Kile 1993;
Harrington and Wingfield 1998). Apart from bark beetles, a wide variety of insects
such as flies (Diptera) or nitidulid beetles (Nitidulidae) are known as vectors of
Ceratocystis spp. (Harrington 1987). Generally, Ceratocystis species have a
relatively loose and unspecific relationship with insects. This is exemplified by the
causal agent of oak wilt in North America, C. fagacearum, which is transmitted at
low frequencies by nitidulid beetles (Juzwik and French 1983). However, there are
also exceptions to this characteristic. There are three Ceratocystis species, which are
consistently associated with conifer bark beetles (Solheim 1986; Redfern et al. 1987;
Wingfield et al. 1997; Harrington and Wingfield 1998). Intriguingly, these three
species are relatively virulent pathogens (Christiansen 1985; Redfern et al. 1987;
Harrington and Wingfield 1998; Solheim and Safranyik 1997; Yamaoka et al. 1997;
1998).
190 T. KIRISITS
Species of Ophiostoma and Ceratocystiopsis and their anamorphs are, in contrast

to Ceratocystis spp., mainly distributed in temperate and boreal regions of the
Northern hemisphere (Harrington 1987, 1993a; Jacobs and Wingfield 2001). Most
of these fungi live in the phloem and in the sapwood of conifers and hardwoods and
they rarely occur on other substrates such as herbaceous plants (Hunt 1956;
Upadhyay 1981; Jacobs and Wingfield 2001). Ophiostoma spp. are predominantly
known as fungal associates of phloeophagous bark beetles, with which they often
form intimate and relatively specific relationships (Mathiesen-Käärik 1953; Whitney
1982; Paine et al. 1997; Kirschner 1998; Jacobs and Wingfield 2001). Ophiostoma
species also occur in association with ambrosia beetles (Bakshi 1950; Mathiesen-
Käärik 1953; Zimmermann 1973; Kirschner 1998), cerambycid beetles (Mathiesen-
Käärik 1953; Jacobs and Wingfield 2001; Jacobs and Kirisits 2003; Jacobs et al.
2003a), weevils (Mathiesen-Käärik 1953; Jacobs and Wingfield 2001; Viiri, chapter
17) and phoretic mites carried by bark k beetles (Bridges and Moser 1983, 1986;
Lévieux et al. 1989; Moser et al. 1989, 1997). A number of ophiostomatoid fungi
are not specifically associated with insects, but disseminated through the air or by
rain-splash inoculum (Mathiesen-Käärik 1953; Kile 1993; Dowding 1969; Gibbs
1993). These species also occur in galleries of bark beetles, in particular at late
stages of brood development, but their relationship with the insects is relatively
loose and unspecific (Mathiesen-Käärik 1953; Kirisits 1996; Kirschner 1998).
The association of blue-stain fungi with bark beetles can easily be recognized on
trees or logs infested by the insects, especially on conifers. At advanced stages of
breeding activity, blue-stain can be seen in the phloem and in the sapwood (Fig. 1)
around and underneath insect galleries. Perithecia and anamorph structures of the
ophiostomatoid fungi develop in the phloem and sapwood in and around female and
larval galleries and in pupal chambers (Fig. 3).
Blue-stain fungi are primary colonizers of the sapwood of dying and recently
killed trees. A number of studies have treated the characterstic succession of
colonization of the sapwood by blue-stain fungi, following attack by bark beetles
(Bramble and Holst 1940; Käärik 1975; Solheim 1992a, 1992b). The most virulent
blue-stain fungi are the first to grow into the fresh sapwood of trees that have been
infested by the insects. Other, less virulent blue-stain fungi follow these primary
invaders. During this temporal succession, primary and secondary invaders are
rapidly replaced by other fungi, including wood-decay fungi and saprotrophic
species (Solheim 1992b). In contrast to their pathogenic abilities, most blue-stain
fungi are poorly adapted to live and survive saprophytically in host tissues (Gibbs
and Inman 1991; Gibbs 1993; Solheim 1992b). They are thus quickly replaced by
other fungi, which are better adapted to live saprophytically.
Pathogenicity of ophiostomatoid fungi. There are a considerable number of

economically important plant and tree pathogens among the ophiostomatoid fungi
(Wingfield et al. 1993; Kile 1993a; Harrington 1993a). Among these, the most
aggressive tree pathogens are those that cause vascular wilt diseases. They are
disseminated by insect vectors or abiotic agents, infect the vascular system of living
trees, which leads to disruption of the water transport and finally to death of trees.
Figure 3. Larva of the spruce bark beetle Ips typographus prior to pupation in a pupal
chamber. Plentiful sporulation of Leptographium penicillatum is seen along the walls of the
gallery.
The best known examples of vascular wilt pathogens are O. ulmi and O. novo-ulmi
that are effectively transmitted by elm barkk beetles and have been responsible for
various pandamics of Dutch elm disease in Europe, North America and parts of Asia
(Brasier 1991, 2000; Webber and Gibbs 1989). Other examples of aggressive wilt
pathogens within the ophiostomatoid fungi include C. fagacearum, the causal agent
of oak wilt in North America (Webber and Gibbs 1989; Kile 1993), Leptographium
wageneri, which is responsible for black stain root disease on conifers in western
North America (Harrington 1993a; Viiri, chapter 17) and Ceratocystis fimbriata,
which causes vascular stain and canker diseases on a wide range of economically
important woody plants, including tree species of great economic importance (Kile
1993; Roux et al. 2000; Marin 2004). While the Dutch elm disease pathogens are
consistently associated with insect vectors, the relationships of C. fagacearum and
C. fimbriata with insects are loose and unspecific, and L. wageneri is probably
intermediate between these two extremes (Webber and Gibbs 1989; Harrington
1993a; Kile 1993; Viiri, chapter 17).
Most ophiostomatoid fungi causing blue-stain in the sapwood of conifers are
moderately or weakly virulent pathogens, or they are saprophytes that cause damage
to stored logs, timber and other wood products (Seifert 1993; Gibbs 1993; Butin
1996). However, some species display relatively high levels of virulence to their
hosts and can kill trees when inoculated at sufficiently high dosages (Horntvedt et
al. 1983; Christiansen 1985; Christiansen et al. 1987; Harrington 1993a; Paine et al.
1997; Lieutier 2002, chapter 9). Generally, bark beetle-associated blue-stain fungi
are much less virulent than the afforementioned aggressive wilt pathogens. In
contrast to typical vascular wilt pathogens, pathogenic blue-stain fungi mainly
192 T. KIRISITS
colonize the ray parenchyma cells of the sapwood which leads to disruption of the
sap flow of infected trees (Ballard et al. 1982; Horntvedt et al. 1983; Webber and
Gibbs 1989; Harrington 1993a; Paine et al. 1997; Kirisits and Offenthaler 2002).
Colonization of xylem vessels or tracheids is very limited at early stages of
pathogenesis and occurs extensively only at late stages of infection (Ballard et al.
1984; Webber and Gibbs 1989). Simultaneously to infection of the xylem the
phloem of trees is also colonized by blue-stain fungi, which can lead to bark girdling
of the host trees (Webber and Gibbs 1989). Due to the patterns of colonization of the
xylem, pathogenic blue-stain fungi have been referred to as “vascular stain
pathogens” (Webber and Gibbs 1989). The type of disease caused by these fungi has
also been called “canker stain”, because disease symptoms include both necrotic
lesions in the phloem and stain in the sapwood (Wingfield et al. 1993; Fig. 4).
Systemic vascular wilt pathogens and non-systemic vascularr stain pathogens
differ substantially in the modes of inoculation and infection as well as in their
pathogenesis. While infection of vascular wilt pathogens can start from a single
inoculation point and progresses systemically, pathogenic blue-stain fungi are
simultaneously inoculated into the host tissues during the mass attack of trees by
bark beetles (Webber and Gibbs 1989). The host tree can always resist single or low
numbers of inoculations of blue-stain
l fungi which lead to discrete necrotic lesions in
the phloem and to limited desiccation or stain in the sapwood (Redfern et al. 1987;
Lieutier et al. 1989a, 1989b; Krokene 1996; Lieutier 2002, chapter 9). However, it
has been demonstrated in mass inoculation experiments that the defense
mechanisms, in particular the induced, hypersensitive wound response of the host
trees get exhausted, which can finally result in tree death (Horntvedt et al. 1983;
Christiansen 1985; Christiansen et al. 1987; Croisé et al. 1998; Lieutier 2002,
chapter 9). After mass inoculation, necrotic lesions develop in the phloem and the
sapwood becomes blue-stained and dysfunctional (Fig. 4).
Examples of relatively virulent ophiostomatoid fungi associated with bark
beetles in Europe include Ceratocystis polonica (associated with Ips spp. on Picea
spp.; e. g. Horntvedt et al. 1983; Christiansen 1985; Solheim 1988; Harding 1989;
Christiansen and Solheim 1990; Krokene and Solheim 1998; Kirisits 1998; Kirisits
and Offenthaler 2002), Ceratocystis laricicola (associated with Ips cembrae on
Larix spp.; Redfern et al. 1987; Kirisits et al. 2000) as well as Leptographium
wingfieldii and Ophiostoma minus (associated with Tomicus piniperda on Pinus
spp.; Solheim et al. 1993, 2001; Croisé et al. 1998). Other bark beetle-associated
blue-stain fungi also display varying levels of virulence to their host trees. Most of
them also stimulate the tree´s defense reactions to some extent. However, they are
less virulent as the afforementioned blue-stain fungi and can kill trees, if at all, only
at very high inoculation dosages. Such less virulent bark beetle-associated blue-stain
fungi in Europe include Ambrosiella sp., Ophiostoma bicolor, O. penicillatum, O.
piceaperdum, O. piceae and Pesotum sp. on Norway spruce (Horntvedt et al. 1983;
Solheim 1988, Harding 1989; Krokene and Solheim 1998; Kirisits 1996, 1998), O.
canum, O. ips and O. brunneo-ciliatum on pine (Lieutier et al. 1989a, 1989b;
Guérard et al. 2000; Solheim et al. 2001) as well as Graphium laricis and O.
brunneo-ciliatum on European larch (Redfern et al. 1987; Kirisits et al. 2000).
Within the fungal assemblages of particular bark beetles there are often one or
sometimes two relatively virulent fungal associates, while other associated fungi are
less virulent. European scolytids with such patterns of virulence among fungal
associates include I. typographus, I. amitinus, I. cembrae, I. duplicatus and T.
piniperda (Horntvedt et al. 1983; Solheim 1988; Solheim et al. 1993, 2001; Kirisits
et al. 2000; Krokene and Solheim 1996, 1998).
Figure 4. Necrotic lesions in the secondary

r phloem and blue-stain in the sapwood of a
Norway spruce tree after mass inoculation with Ceratocystis polonica.
The results of various inoculation studies suggest that there is considerable

variation in the virulence of different isolates of the same blue-stain fungus. Isolates
of L. wingfieldii collected within the forest of Orléans varied greatly in their
virulence to Scots pine (Lieutier et al. 2004). Likewise, low levels of virulence and
loss of virulence have been described for isolates of C. polonica (Kirisits and
Anglberger 1998; Krokene and Solheim 2001). Recently, hypovirulence caused by
infections of dsRNA mycoviruses has been detected in isolates of C. polonica and
C. laricicola (Marin 2004). This intriguing finding raises questions about the impact
of the virus on the ecology and epidemiology of these pathogenic blue-stain fungi
and also about possible indirect effects on the relationship between the fungi and
their insect vectors.
Pathogenic blue-stain fungi are also known to be associated with North
American bark beetles, but I will not treatt them in detail here and refer to recent
overviews provided by Krokene (1996) and Paine et al. (1997). In Asia, the best-
194 T. KIRISITS
known examples of pathogenic blue-stain fungi associated with bark beetles are
C. polonica (associated with Ips typographus f. japonicus on Picea spp. in Japan;
Yamaoka et al. 2000), C. laricicola (associated with Ips subelongatus on Larix
kaempferi in Japan; Yamaoka et al. 1998) and Leptographium yunnanensis
(associated with Tomicus piniperda in China; Lieutier 2002)
3.4. Anamorphic Fungi

Among the anamorphic fungi associated with bark beetles almost all belong to the
hyphomycetes (Francke-Grosmann 1967; Batra 1967; Beaver 1989; Whitney 1982;
Kirschner 1998). Many asexual fungi have been known to be associated with bark
beetles, but often the relationship between the insects and the fungi seem to be
fortuitous and inconsistent (Zimmermann 1973; Whitney 1982; Kirschner 1998; Six
2003). However, some non-ophiostomatoid hyphomycetes are commonly associated
with bark beetles (Kirschner 1998, 2001). The way, in which these more regularly
associated hyphomycete taxa interact with their insect associates and with other
fungi in the bark beetle habitat is unknown. But they may be significant, for example
as antagonists and mycoparasites of more intimate associates such as ambrosia fungi
and blue-stain fungi (Kirschner 1998; Six 2003).
For many ophiostomatoid species that are phylogenetically related to
Ophiostoma no sexual state is known to occur and these taxa are thus known under
the generic name of their anamorph state, Leptographium, Pesotum, Sporothrix and
Hyalorhinocladiella. Among these, Leptographium species are probably best known
(Jacobs and Wingfield 2001), but there are also numerous Pesotum species that are
consistently associated with bark beetles (e. g. Mathiesen-Käärik 1953; Solheim
1992a, 1992b; Krokene and Solheim 1996; Kirisits et al. 2000). Synnematous
anamorphs of Ophiostoma have until recently been classified in the genus
Graphium, but phylogenetic studies based on sequence analyses of the rDNA placed
Graphium penicillioides, the type species of the genus Graphium, within the
Microascales (Okada et al. 1998, 2000). Graphium is thus only distantly related to
Ophiostoma, and consequently, synnematous anamorphs of Ophiostoma were
transferred to Pesotum (Okada et al. 1998, 2000). In addition to Pesotum spp., a few
Graphium species are closely associated with bark beetles (Kirschner 1998; Kirisits
et al. 2000; Jacobs et al. 2003b).
Besides a few species where teleomorphs are known, ambrosia fungi generally
belong to various genera of hyphomycetes. Major ambrosia fungi belong to the
genera Ambrosiella, Raffaelea and Fusarium (Francke-Grosmann 1967; Batra 1967;
Zimmermann 1973; Norris 1979; Beaver 1989). The principal ambrosia fungi of
European xylomycetophagous bark beetles are Ambrosiella spp. (Table 1). Analyses
of rDNA sequence data of Ambrosiella species have shown that this genus is
polyphyletic, with two lineages closely related to Ceratocystis and Ophiostoma,
respectively (Cassar and Blackwell 1996; Rollins et al. 2001, Paulin-Mahady et al.
2002). Three Ambrosiella species, including A. xylebori (the type species of the
genus), A. ferruginea and A. hartigii are related to Ceratocystis, whereas eight other
taxa, A. brunnea, A. gnathotrichi, A. ips, A. macrospora, A. sulcati, A. sulfurea, A.
tingens, and an Ambrosiella sp. associated with Hylurgops palliatus and

Polygraphus poligraphus (Krokene and Solheim 1996) show affinities to
Ophiostoma (Cassar and Blackwell 1996; Rollins et al. 2001). Similarly, Raffaelea
species have proven to be closely related to Ophiostoma (Jones and Blackwell
1998). The close phylogentic relationships of Ambrosiella and Raffaelea species to
Ophiostoma and Ceratocystis clearly demonstrate that the most common associates
of phloeophagous and xylomycetophagous bark beetles share common ancestors.
A significant characteristic of the ambrosia fungi is their pleomorphism. In the
breeding systems of the ambrosia beetles they form “ambrosial” layers along the
gallery walls, representing the “ambrosia” first described by Schmidberger (1936).
The “ambrosia” consists of a dense, palisade-like layer of hyphae, on the top of
which numerous conidia are formed in chains (Francke-Grosmann 1967; Batra
1967; Zimmermann 1973; Beaver 1989). Beetles and larvae feed on this ambrosial
layer and sporulation of the ambrosia fungi is greatly enhanced by the browsing
activity of the insects (Mathiesen-Käärik 1953; Francke-Grosmann 1967; Beaver
1989). Likewise, ambrosial growth seems to be influenced by the physical contact
between the insect and the fungus. The control of the growth form of the ambrosia
fungi by the insects may be explained by secretions of the adult beetles and their
larvae (Francke-Grosmann 1967; Beaver 1989). Slow “ambrosial” growth with
intensive sporulation may also occur in culture, and can be stimulated by cultivation
of the fungi on certain media (Francke-Grosmann 1967 and references therein; Batra
1967; Beaver 1989). However, in cultures ambrosia fungi often form fast-growing
and sterile mycelia. A third growth form is commonly observed in the mycangium
of the beetles, where ambrosia fungi form yeast-like stages (Francke-Grosmann
1967; Beaver 1989).
Ambrosia fungi are relatively sensitive to various environmental factors such as
relative humidity, moisture content of the sapwood and extreme temperatures. Many
ambrosia fungi including Ambrosiella species are extremely sensitive to desiccation
as well as exposure to high and low temperatures (Zimmermann 1973; Zimmermann
and Butin 1973). Ambrosia fungi and thus also ambrosia beetles have specific
requirements on the moisture content of the sapwood of their host trees. Generally,
this is one of the most decisive factors for establishment and successful breeding of
the insects, since the fungus cannot grow when the moisture content is too low
(Francke-Grosmann 1967). In the wood of their host trees ambrosia fungi usually
penetrate only a few mm into the xylem and their growth is usually restricted to
areas surrounding the galleries (Francke-Grosmann 1967; Zimmermann 1973).
However, Ambrosiella ferruginea, the ambrosia fungus of Xyloterus lineatus,
penetrates several cm into the sapwood off its conifer hosts and causes a reddish-
brown discoloration in the xylem (Mathiesen-Käärik 1953; Francke-Grosmann
1956a).
4. TRANSMISSION OF FUNGI
Both bark beetles and their intimately associated fungi have evolved morphological
adaptions to ensure maintainance of symbiosis from generation to generation. The
196 T. KIRISITS
most obvious adaptions of the insects for consistent dispersal of certain fungi are
specialized structures in the integument of the beetles associated with gland or
secretory cells that are used for the storage, transport and transmission of fungi.
These structures have been defined as mycangia or mycetangia (Batra 1963a;
Francke-Grosmann 1967; Beaver 1989; Berryman 1989). In the strict sense,
mycangia consist of more or less spacious tubes, pouches or cavities in the
integument lined with glandular cells that produce secretions which protect and
preserve the spores of associated fungi (Francke-Grosmann 1956a, 1956b, 1963a,
1963b, 1967; Batra 1963a; Beaver 1989; Lévieux et al. 1991; Six 2003). More
broadly defined the term mycangium refers to any structure that functions in the
transport and protection of fungi, regardless whether glandular cells are present or
not (Whitney 1982; Six 2003).
Besides protecting fungal spores from detrimental environmental influences (e.
g. drought, UV light) and effectively disseminating fungal associates to new
habitats, mycangia also act selectively towards certain fungi, since spores of
mutualistic species are favoured and detrimental or neutral symbionts are excluded
(Batra 1963a; Francke-Grosmann 1967; Beaver 1989). The fungi consistently
occurring in the mycangia (= mycangial fungi) are biologically highly or obligately
significant for the insects. Probably all mycangial fungi have a decisive role for the
nutrition of their associated insects (Francke-Grosmann 1967; Beaver 1989; Paine et
al. 1997; Six 2003).
Mycangia are commonly classified on the basis of their location on the beetles
and structural characteristics. There is a great diversity in the location, form,
structure and size of mycangia in xylomycetophagous and phloeophagous bark
beetles, which supports the view that these organs have evolved numerous times and
independently in different scolytid genera and species (Batra 1963a; Francke-
Grosmann 1967; Beaver 1989; Berryman 1989). Mycangia can be present on both
sexes, only on the males or only on the females, depending on scolytid species
(Francke-Grosmann 1967; Beaver 1989). Xylomycetophagous bark beetles
generally possess mycangia, in which they disseminate their ambrosia fungi.
Although mycangia play a primary role in dissemination of fungi by ambrosia
beetles, other means of fungal dissemination, in particular through the gut, may also
be important in this group of scolytids (Francke-Grosmann 1975; Beaver 1989).
Only a small number of the European xylomycetophagous bark beetles have
thus-far been investigated for the type off mycangium that they bear. These include
the economically important species, Xyleborus dispar, X. monographus, X. saxeseni,
Xyloterus domesticus, X. lineatus and X. signatus, as well as the introduced
Xyleborus germanus and Gnathotrichus materiarius (Table 1 and references
therein). With exception of G. materiarius where the mycangium occurs in the male,
only the females of European xyletomycetophagous scolydids possess a mycangium.
There is a considerable variation in the types of mycangia present on European
ambrosia beetles (Table 1 and references therein). In Xyloterus spp. the mycangium
consists of a pair of glandular tubes in the prothorax (Francke-Grosmann 1956a,
1958, 1967). In Xyleborus disparr and X. germanus the mycangium is represented by
intersegmental pouches located between the pro- and mesonotum (Francke-
Grosmann 1956a, 1958, 1967), while in X. monographus it consists of membranous
pouches at the base of the mandibles (Schedl 1964, Francke-Grosmann 1967).

Another type of mycangium is seen in X. saxeseni that possesses sclerotized pouches
at the base of the elytra (Francke-Grosmann 1956a, 1967). Finally, the mycangium
of G. materiarius consists of an enlargement of the precoxal cavity (Farris 1963;
Francke-Grosmann 1966, 1967).
Mycangia are also known in a number of true bark beetles, although they occur
only in a few species (Francke-Grosmann 1967; Whitney 1982; Beaver 1989; Paine
et al. 1997; Six 2003). For example, various types of mycangia occur in some, but
not all North American Dendroctonus species (Whitney 1982; Paine et al. 1997; Six
2003). In Europe, mycangia have been described for five true bark beetle species
(Table 1 and references therein). In I. acuminatus which has a
phloeomycetophagous feeding habit (Francke-Grosmann 1952; see 6.2.2.), females
possess paired membranous pouches at the base of the mandibles (Francke-
Grosmann 1963b, 1967). In the mycangium of I. acuminatus the nutritionally
important fungus, Ambrosiella macrospora is transmitted. Primitive mycangia,
consisting of secretion-filled punctures of the integument, especially on the elytra,
have been described in both sexes of Hylurgops palliatus, Hylastes aterr and
Hylastes cunicularius (Francke-Grosmann 1956b, 1963a, 1967) Likewise, puncture
pits on the mandibles, the pronotum and the elytra function as mycangia in I.
sexdentatus (Lévieux et al. 1991).
For the majority of phloeophagous bark beetles that regularly carry particular
fungi, mycangia have not been found. In these non-mycangial scolytid species
dissemination of fungi is thus suspected to occur either epizoically by conidia and
ascospores adhering to the insect´s exoskeleton or endozoically through spores
passing the gut undigested (Mathiesen-Käärik 1953; Francke-Grosmann 1967;
Whitney 1982; Furniss et al. 1990; Paine et al. 1997). Apparently, this form of
fungal transmission is as efficient as in scolytids which possess mycangia, since
relatively specific and relatively constant assemblages of fungi also occur with non-
mycangial bark beetles. However, it is also be possible that relatively simple,
unconspicuous pit mycangia, similar to those of Ips sexdentatus (Lévieux et al.
1991) may also occur in other scolytids, but have so far not been recogniszed.
Phoretic mites often also play an important role in the transmission of
ophiostomatoid fungi (Bridges and Moser 1983, 1986; Lévieux et al. 1989; Moser et
al. 1989, 1997) Some mites in the genus Tarsonemus even possess specialized
structures, called sporothecae which are organs for transmission of fungi (Moser
1985). Likewise, in some cases phoretic mites may even be more intimately
associated with a particular fungus than the bark beetles themselves. The best known
examples are D. frontalis, its hyperphoretic mites Tarsonemus krantzi and T. ips
(which both have sporothecae) and Ophiostoma minus which is more closely
associated with the mites than with the southern pine beetle (Bridges and Moser
1983; Moser 1985; Klepzig et al. 2001a, 2001b).
Fungi associated with bark beetles have also evolved adaptions to the symbiosis
with their insect partners. Morphological features of Ophiostoma, Ceratocystis and
Ceratocystiopsis such as long perithecial necks (Fig. 2) and sticky ascospores and
conidia are viewed as adaptions to the bark beetle habitat (Francke-Grosmann 1967;
Whitney 1982; Beaver 1989; Malloch and Blackwell 1993; Six 2003). Ascospores
Table 1. Ambrosia fungi of European scolytids and types of mycangia occurring in European bark beetle species
198
Bark beetle species Principal anbrosia fungus1 Type of mycangium Referecnes

Ambrosia beetles (xylomycetophagous)2
Gnathotrichus materiarius Ambrosiozima monospora3 Enlargement of precoxal cavity in male Farris 1963; Francke-Grosmann 1966,
1967
Xyleborus dispar Ambrosiella hartigii Intersegmental pouches between pro- and Francke-Grosmann 1956a, 1958, 1967
mesonotum in female
Xyleborus germanus Ambrosiella hartigii Intersegmental pouches between pro- and Francke-Grosmann 1956a, 1958, 1967
mesonotum in female
Xyleborus monographus ‘‘Yellowish moniloid fungus’ Paired membranous pouches at base of SChedl 1964; Francke-Grosmann 1967
mandible in female
Xyleborus sexeseni Ambrosiella sulfurea Sclerotized pouches in base of elytra in female Francke-Grosmann 1956a, 1967
Xyloterus domesticus Ambrosiella ferruginea A pair of glandular tubes in prothorax of female Francke-Grosmann 1956a, 1958, 1967
Xyloterus lineatus Ambrosiella ferruginea A pair of glandular tubes in prothorax of female Francke-Grosmann 1956a, 1958, 1967
Xyloterus signatus Ambrosiella ferruginea A pair of glandular tubes in prothorax of female Francke-Grosmann 1956a, 1958, 1967
T. KIRISITS
True bark beetle (phloeophagous)

Hylastes ater - Secretion-filled punctures of the integument, Francke-Grosmann 1956b, 1967
especially on the elytra
Hylastes cunicularius - Secretion-filled punctures of the integument, Francke-Grosmann 1956b, 1967
Hylurgops palliatus - Secretion-filled punctures of the integument, Francke-Grosmann 1956b, 1967
Ips acuminatus4 Ambrosiella macrospora Paired membranous pouches at base of Francke-Grosmann 1963b, 1967
mandible in female
Ips sexdentatus - Puncture pits on the proximal part of the mandible, Lévieux et al., 1991
the sides of the pronotum and the elytra
Notes: 1 See also table 2 and references therein. 2 European scolytides with xylomycetophagous feeding habits (Postner 1974; Pfeffer 1995), for which neither
the ambrosia fungus nor the type of mycangium has been investigated: Xyleborus cryptographus, X. alni, X. eurygraphus, X. dryographus, X. pfeili, X. levae.
3
references: Batra 1963b; Kischner 1998, 2001. 4 I. acuminatus is siuggested to have a “phloeomycetophagous” feeding habit (Francke-Grosmann 1952).
and conidia easily adhere to the bodies of the insects. Ascospores often possess well
developed sheaths, which may protect the spore from digestation in the gut of the
beetles (Francke-Grosmann 1967; Malloch and Blackwell 1993). Ophiostomatoid
fungi and ambrosia fungi are pleomorphic and show both mycelial and yeast-like
growth forms. In the mycangium of the beetles the fungi are usually present in their
slow-growing yeast stage (Francke-Grosmann 1967; Beaver 1989; Six 2003). The
loss of the sexual stage in almost all known ambrosia fungi and in some
ophiostomatoid fungi may also be viewed as extreme adaption to the symbiosis with
bark beetles (Six 2003).
5. ASSEMBLAGES OF FUNGI ASSOCIATED WITH EUROPEAN BARK

BEETLES
Since the discovery of the association of fungi with bark beetles numerous studies
on the mycobiota associated with European scolytids have been carried out. An
overview of the assemblages of fungi and especially the ophiostomatoid fungi
associated with xylomycetophagous (5.1.) and phloeophagous bark beetles (5.2.) is
presented.
5.1. Assemblages of fungi

f associated with xyllomycetophagous bark beetles
For six xylomycetophagous beetles that are native in Europe and for two species that
have been introduced into Europe their principal ambrosia fungi are known (Tables
1 and 2 and references therein). Their identity has not been determined for the other
seven xylomycetophagous species in Europe (Table 1) that are economically less
important. Most European scolytids with xylomycetophagous feeding habit are
associated with species in the genus Ambrosiella (Tables 1 and 2) that includes taxa
related to Ceratocystis or Ophiostoma (Cassar and Blackwell 1996; Rollins et al.
2001; Paulin-Mahady et al. 2002). Xyleborus disparr and the introduced X. germanus
live in symbiosis with A. hartigii, wheras X. domesticus, X. lineatus and X. signatus
are associated with A. ferruginea. Both A. hartigii and A. ferruginea are closely
related to species in the genus Ceratocystis (Cassar and Blackwell 1996; Rollins et
al. 2001). Ambrosiella sulfurea, which has affinities to the genus Ophiostoma
(Cassar and Blackwell 1996; Rollins et al. 2001) is transmitted by X. saxeseni. The
ambrosia fungus of Xyleborus monographus has been referred to as “yellowish
moniloid fungus” (Francke-Grosmann 1967). A Raffaelea species has also been
reported to be associated with this scolytid (Kowalski 1991). The introduced G.
materiarius is associated with a non-ophiostomatoid ambrosia fungus, the yeast
Ambrosiozyma monospora (Batra 1963b; Kirschner 1998). As seen in European
ambrosia beetles the association between the insects and their principal ambrosia
fungi is not species-specific, since several beetle species can be associated with the
same Ambrosiella species.
In addition to their principal fungal associates, ambrosia beetles are also known
to carry Ophiostoma species and other non-ambrosial ophiostomatoid fungi. These
fungi have also been proposed to represent ambrosia fungi with nutritional
200 T. KIRISITS
importance for the insects (Bakshi 1950), but most authors consider them as “weed
fungi” that are ecologically insignificant for the beetles (Francke-Grosmann 1966,
1967; Beaver 1989). The spectrum of ophiostomatoid fungi occurring together with
xylomycetophagous bark beetles comprises a considerable number of species, most
of which are generalists that occur in association with a wide range of insects on
several host trees (Table 2).
5.2. Assemblages of fungi associated with phloeophagous bark beetles

A synthesis of the numerous investigations on the assemblages of ophiostomatoid
fungi associated with phloem-feeding bark beetles in Europe is provided in Table 2.
Thus-far, 27 true bark beetle species, 23 on conifers and 4 on hardwoods have been
examined for the ophiostomatoid fungi they carry. The best-studied European bark
beetle regarding its fungal associates is I. typographus which has been included in
many investigations within its distribution range in Europe (Table 2 and references
therein) and also in Japan (Yamaoka et al. 1997). I will subsequently often refer to
this species as example.
5.2.1. Overview about ophiostomatoid fungi associated with phloeophagous bark

beetles
Ophiostomatoid fungi associated with true bark beetles in Europe mainly belong to
the genus Ophiostoma, which is represented by a large number of species (Table 2).
Several Leptographium and Pesotum species are also associated with phloeophagous
bark beetles (Table 2). A few European bark beetles transmit Ceratocystis species,
namely C. polonica and C. laricicola. Ceratocystis polonica is mainly associated
with I. typographus, I. amitinus and I. duplicatus on Norway spruce, although it is
occasionally also transmitted at low frequencies by other spruce bark beetles (Table
2). Likewise, C. laricicola is associated with I. cembrae on Larix spp. Ceratocystis
polonica and C. laricicola are unusual, since they are among the few Ceratocystis
species that are regularly transmitted by bark beetles. The only other known
example is C. rufipenni that is associated with D. rufipennis on Picea spp. in North
America (Wingfield et al. 1997). A few conifer bark beetles, including particularly
H. palliatus, I. acuminatus, I. sexdentatus and T. minorr transmit Ambrosiella species
that are phylogenetically related to Ophiostoma (Table 2; see 3.4.). Species of
Graphium as associates of bark beetles are also included in Table 2, despite the fact
Graphium is not closely related to Ophiostoma and other ophiostomatoid fungi
(Okada et al. 1998, 2000; Harrington et al. 2001). In particular, four Graphium
species are common associates of European bark beetles. These include G.
pseudormiticum associated with several pine bark beetles, G. fimbriisporum,
associated with various spruce bark beetles, G. laricis, occurring with I. cembrae on
larch and G. penicillioides, associated with Taphrorychus bicolorr on beech and
Scolytus spp. on elm (Kirschner 1998; Kirisits et al. 2000; Jacobs et al. 2003b; Table
2).
5.2.2. Intimacy of association between ophiostomatoid fungi and phloem-feeding

bark beetles
Based on the intimacy of association with ophiostomatoid fungi, scolytids can
broadly be divided into two groups. One of these groups includes bark beetle species
that are relatively loosly associated with fungi, in the sense that only a low portion
of individuals in a population carries fungi. The pine shoot beetle, Tomicus
piniperda may be a typical example for a scolytid with a relatively loose relationship
with blue-stain fungi. Although this bark beetle transmits numerous ophiostomatoid
fungi (Table 2), none of these occur at consistently high frequencies in populations
of the insect (Mathiesen-Käärik 1953; Lieutier et al. 1989b; Solheim and Långström
1991; Gibbs and Inman 1991). Even L. wingfieldii, O. minus and Hormonema
dematoides, the most consistent associates of T. piniperda are usually isolated at
relatively low frequencies, compared to other conifer bark beetle-fungus-systems
(Lieutier et al. 1989b; Solheim and Långstöm 1991; Gibbs and Inman 1991). Other
examples of conifer bark beetles with relatively loose association with fungi include
the solitary D. micans on Norway spruce (Lieutier et al. 1992), Cryphalus abietis on
Silver fir (Kirschner 1998), and Pityogenes quadridens on Scots pine (Mathiesen-
Käärik 1953) (Table 2). Among bark beetle species on deciduous trees, Leperisinus
varius on ash and Scolytus intricatus on oak infrequently disseminate unspecific
Ophiostoma species (Kirschner 1998).
The second group of bark beetles comprises species that are intimately
associated with blue-stain fungi, meaning that a large percentage of individuals (up
to 100 %) carry spores of ophiostomatoid ffungi. This does not necessarily mean that
one particular blue-stain fungus is always present at such high frequencies, but that
the majority of beetles usually carry at least one fungus out of the whole assemblage
of fungi associated with a particular bark beetle species. For conifer bark beetles
intensive association with blue-stain fungi is the rule rather than the exception. A
typical example is I. typographus on Norway spruce. A diverse assemblage of fungi
is associated with this economically extremely important bark beetle. Despite the
fact that there is a great variation in the composition of the mycobiota reported in
various investigations (see 5.2.5), all studies agree that I. typographus very
consistently and regularly carries blue-stain fungi (Table 2). The same is true for
many other conifer bark beetles, including Crypturgus cinereus, Crypturgus
pusillus, Dryocoetes autographus, Hylastes ater, Hylastes cunicularius, Hylurgops
palliatus, Hylurgops glabratus, Ips acuminatus, Ips amitinus, Ips cembrae, Ips
duplicatus, Ips sexdentatus, Orthotomicus laricis, Orthotomicus proximus,
Pityogenes chalcographus, Polygraphus poligraphus and Tomicus minorr (Table 2).
Among bark beetles on hardwoods, Scolytus spp. on elm seem to be rather
intimately associated with ophiostomatoid fungi, in particular with the introduced
Dutch elm disease pathogens O. ulmi and O. novo-ulmi and with G. penicillioides
(Table 2). However, the different Scolytus species vary greatly in their efficiency as
vectors of the Dutch elm disease pathogens, with Scolytus scolytus being the most
effective vector (Webber and Brasier 1984; Webber and Gibbs 1989; Webber 1990,
2000). On beech, the secondary Taphrorychus bicolorr may be relatively regularly
associated with G. penicillioides (Table 2).
202 T. KIRISITS
5.2.3. Elements of the mycobiota of phloephagous bark beetles

The symbiosis between ophiostomatoid fungi and bark beetles is usually not a “one
fungus – one insect” relationship. Hence, most bark beetle species are associated
with an assemblage of several fungi. Typically, some fungal species occur at high
frequencies and/or constantly together with a given bark beetle species, while others
are rare and/or casual components of the mycobiota. For example, a very high
number of fungi has been reported to occur together with I. typographus in Europe,
but many of the recorded species are generally rare in this niche or have been found
only by one or a few investigators (Table 2). Only a few species are mentioned as
relatively constant associates in the majority of the studies on the mycobiota of I.
typographus. Thus, despite different results of the various investigations (see 5.2.5.),
C. polonica, O. ainoae, O. bicolor, O. penicillatum and O. piceaperdum are
probably the most common and ecologically most significant fungi associated with
I. typographus in Europe (Table 2). Very similar patterns also occur in many other
bark beele-fungus systems (Table 2).
Table 2: Ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) in

Europe. Species of Graphium, which were formerly known as anamorphs of Ophiostoma are
also included.
Bark beetle (Host trees) a Fungus h References j

Cryphalus abietis b,f Ophiostoma piceae Kirschner 1998, 2001
(Conifers [Abies
[ alba]) (Ophiostoma piceaperdum) Kirschner 1998, 2001
Crypturgus cinereus b,e Ceratocystiopsis alba Kirschner 1998, 2001

(Conifers [Picea abies, Ceratocystiopsis minima Kirschner 1998, 2001
Pinus sylvestris]) Ceratocystiopsis minuta Kirschner 1998, 2001
Ophiostoma japonicum Kirschner 1998, 2001
(= O. arborea?)
Ceratocystis leucocarpa Kirschner 1998, 2001
Ophiostoma neglectum Kirschner 1998, Kirschner and
Oberwinkler 1999
Ophiostoma piceae Kirschner 1998, 2001
Ophiostoma cf. piceae Kirschner 1998, 2001
Ophiostoma piceaperdum Kirschner 1998, 2001
Ophiostoma stenoceras Kirschner 1998, 2001
Crypturgus pusillus b,e Ceratocystiopsis alba Kirschner 1998, 2001

(Conifers [Picea abies]) Ceratocystiopsis minima Kirschner 1998
Ceratocystiopsis minuta Kirschner 1998, 2001
Ceratocystis leucocarpa Kirschner 1998
Graphium pseudormiticum Kirschner 1998, 2001
(= G. fimbriisporum?)
Ophiostoma ainoae Kirschner 1998, 2001
Ophiostoma araucariae Kirschner 1998, 2001
Ophiostoma bicolor Kirschner 1998, 2001
(= O. arborea?)
Oberwinkler 1999
Ophiostoma cf. piceae Kirschner 1998
Table 2 continued
Ophiostoma simplex Kirschner 1998
Ophiostoma stenoceras Kirschner 1998
Ophiostoma torulosum Kirschner 1998
Dendroctonus micans b,ff Ophiostoma canum Lieutier et al. 1992

((Picea abies) (Ophiostoma penicillatum) Lieutier et al. 1992
(Ophiostoma minus) Lieutier et al. 1992
(Ophiostoma sp.) Lieutier et al. 1992
Dryocoetes autographus b,e Ceratocystiopsis alba Kirschner 1998, 2001

(Conifers [Picea abies, Ceratocystiopsis minuta Kirschner 1998, 2001
Pinus sylvestris]) Ceratocystis autographa Bakshi 1951
Graphium adustum Grosmann 1931
Graphium fimbriisporum Kirisits et al. 2000, Jacobs et al. 2003b
Leptographium guttulatum Kirisits et al. 2000; Jacobs and
Wingfield 2001; Jacobs et al. 2001a
Ophiostoma ainoae Kirschner 1998, 2001; Kirisits et al.
2000
Ophiostoma cucullatum Kirschner 1998, 2001; Kirisits et al.
2000
Ophiostoma galeiformis Bakshi 1951
(= O. arborea?)
Ophiostoma obscura
Ophiostoma neglectum Kirschner 1998; Kirschner and
Oberwinkler 1999
Ophiostoma piceae Kirschner 1998, 2001; Kirisits et al.
2000
Ophiostoma piceaperdum Kirschner 1998, 2001; Kirisits et al.
2000
Gnathotrichus materiarius d,e Leptographium sp. Kirschner 1998

(Conifers [Larix decidua, Ophiostoma araucariae Kirschner 1998
Pinus sylvestris]) Ophiostoma cucullatum Kirschner 1998
Ophiostoma obscura Kirschner 1998
Ophiostoma piceaperdum Kirschner 1998
Ophiostoma piceae Kirschner 1998
Hylastes ater b,e [Graphium (Pesotum

( ?) Mathiesen-Käärik 1953
((Pinus sylvestris) aureum]
Leptographium guttulatum Wingfield and Gibbs 1991, Jacobs and
Wingfield 2001
Leptographium lundbergii Dowding 1973; Mathiesen 1950;
Mathiesen-Käärik 1953; Jacobs and
Wingfield 2001
Leptographium serpens Wingfield and Gibbs 1991; Jacobs and
Wingfield 2001
(Ophiostoma ips) Mathiesen-Käärik 1953
Ophiostoma minus Mathiesen 1950; Mathiesen-Käärik 1953
204 T. KIRISITS
Table 2 continued
Ophiostoma penicillatum Mathiesen 1950; Mathiesen-Käärik
1953, Jacobs and Wingfield 2001
[Ophiostoma penicillatum f. Mathiesen 1950
chalcographi]
[Ophiostoma penicillatum f. Mathiesen 1950; Mathiesen-Käärik 1953
pini]
Ophiostoma piceae Mathiesen 1950; Mathiesen-Käärik 1953
(Ophiostoma piliferum) Mathiesen-Käärik 1953
Hylastes opacus b,g Graphium (Pesotum

( ?) sp. Wingfield and Gibbs 1991
((Pinus sylvestris) Leptographium guttulatum Wingfield and Gibbs 1991; Jacobs and
Wingfield 2001
Leptographium lundbergii Wingfield and Gibbs 1991; Jacobs and
Wingfield 2001
Leptographium procerum Wingfield & Gibbs 1991; Jacobs and
Wingfield 2001
Leptographium wingfieldii Wingfield & Gibbs 1991; Jacobs and
Wingfield 2001
Hylastes cunicularius b,e Ophiostoma galeiformis Mathiesen-Käärik 1953; Zhou et al.

((Picea abies) 2004
Ophiostoma olivaceum Mathiesen-Käärik 1953
Ophiostoma penicillatum Mathiesen-Käärik 1953; Jacobs and
Wingfield 2001
Ophiostoma piceae Mathiesen-Käärik 1953
Hylurgops palliatus b,e Ambrosiella sp. Krokene and Solheim 1996; Rollins et
(Conifers [Picea abies, Pinus al. 2001
sylvestris, Larix kaempferi]) Ceratocystiopsis alba Kirschner 1998, 2001
Ceratocystis autographa Bakshi 1951
Ceratocystis polonica Krokene and Solheim 1996
Graphium fimbriisporum Kirisits et al. 2000; Jacobs et al. 2003b
Graphium (Pesotum
( ?) Mathiesen 1950, Mathiesen-Käärik 1953
pyknocephalum
Graphium (Pesotum
( ?) spp. Wingfield and Gibbs 1991
Leptographium guttulatum Mathiesen 1950; Harding 1989;
Wingfield and Gibbs 1991; Kirisits et al.
2000; Jacobs and Wingfield 2001;
Jacobs et al. 2001b
Leptographium lundbergii Kotýnková-Sychrová 1966; Harding
1989; Wingfield and Gibbs 1991; Jacobs
and Wingfield 2001
Leptographium procerum Wingfield and Gibbs 1991; Jacobs and
Wingfield 2001
Leptographium wingfieldii Wingfield and Gibbs 1991; Jacobs and
Wingfield 2001
Ophiostoma ainoae Kirisits et al. 2000
Ophiostoma bicolor Harding 1989; Kirschner 1998, 2001
Ophiostoma cucullatum Kirschner 1998, Kirisits et al. 2000
Ophiostoma galeiformis Bakshi 1951
(= O. arborea?)
Ophiostoma neglectum Kirschner 1998, 2001; Kirisits,
Table 2 continued
unpublished
Ophiostoma penicillatum Mathiesen 1950; Mathiesen-Käärik
1953; Kirschner 1998; Jacobs and
Wingfield 2001
palliati] (= Leptographium
guttulatum)
Ophiostoma piceae Mathiesen 1950; Mathiesen-Käärik
1953; Harding 1989; Krokene and
Solheim 1996; Kirschner 1998, 2001;
Kirisits et al. 2000
Ophiostoma piceaperdum Davidson et al. 1967; Harding 1989;
Krokene and Solheim 1996; Kirschner
1998, 2001; Kirisits et al., 2000; Jacobs
and Wingfield 2001
Hylurgops glabratus b,e Graphium fimbriisporum Kirisits 1996; Kirisits et al. 2000; Jacobs
(Conifers [Picea abies]) et al. 2003b
Leptographium guttulatum Kirisits 1996; Kirisits et al 2000; Jacobs
and Wingfield 2001; Jacobs et al., 2001b
Ophiostoma ainoae Kirisits 1996; Kirisits et al. 2000
Ophiostoma cucullatum Kirisits 1996; Kirisits et al. 2000
Ophiostoma flexuosum Kirisits 1996; Kirisits et al. 2000
Ophiostoma floccosum Lin 2003
Ophiostoma piceae Kirisits 1996; Kirisits et al. 2000
Ophiostoma piceaperdum Kirisits 1996; Kirisits et al. 2000
Ips acuminatus c,e Ambrosiella macrospora Mathiesen 1950; Francke-Grosmann

(
(Pinus spp.) 1952, 1963b; Cassar and Blackwell 1996
Ceratocystiopsis minima Lieutier et al. 1991
Ceratocystiopsis minuta Mathiesen 1951
(Ceratocystis coerulescens) Mathiesen 1950; Mathiesen-Käärik 1953
(Graphium (Pesotum
( ?) Mathiesen 1950; Mathiesen-Käärik 1953
pyknocephalum)
Leptographium lundbergii Mathiesen 1950; Mathiesen-Käärik
1953; Jacobs and Wingfield 2001
Ophiostoma brunneo- Lieutier et al. 1991
ciliatum
(Ophiostoma canum) Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma clavatum Rennerfelt 1950; Mathiesen 1950, 1951;
Mathiesen-Käärik 1953; Francke-
Grosmann 1952, 1963b
Ophiostoma ips Lieutier et al. 1991; Mathiesen-Käärik
1953
Ophiostoma minus Rennerfelt 1950; Mathiesen 1950;
Mathiesen-Käärik 1953; Lieutier et al.
1991
1953; Francke-Grosmann 1952
Ophiostoma piliferum Mathiesen 1950, Mathiesen-Käärik
1953; Francke-Grosmann 1952, 1963
Ophiostoma sp. Lieutier et al. 1991
Ophiostoma spp. Rennerfelt 1950; Mathiesen 1950
206 T. KIRISITS
Table 2 continued
Ips amitinus b,e Ceratocystiopsis cf. alba Kirisits et al. 2000

((Picea abies, Pinus cembra) Ceratocystiopsis minuta Kirisits et al. 2000
Ceratocystis polonica Kirisits et al. 2000
Graphium fimbriisporum Kirisits et al. 2000 ; Jacobs et al. 2003b
Graphium ((Pesotum?) spp. Grosmann 1931
Leptographium lundbergii Grosmann 1931
Leptographium spp. Kirisits et al. 2000
Ophiostoma bicolor Kirisits et al. 2000
Ophiostoma brunneo- Kirisits et al. 2000
ciliatum
Ophiostoma cucullatum Kirisits et al. 2000
Ophiostoma minus Grosmann 1931
Ophiostoma penicillatum Kirisits et al. 2000
Ophiostoma piceae Kirisits et al. 2000
Ophiostoma piceaperdum Kirisits et al. 2000
Ophiostoma cf. Kirisits et al. 2000
piceaperdum
Ophiostoma piliferum Grosmann 1931
Ips cembrae b,e Ceratocystiopsis cf. alba Kirisits et al. 2000; Stauffer et al. 2001
((Larix decidua, Ceratocystiopsis minuta Kirisits et al. 2000; Stauffer et al. 2001
Larix kaempferi) Ceratocystis laricicola Redfern et al. 1987; Redfern 1989;
Kirisits et al. 2000; Stauffer et al. 2001
Graphium laricis Kirisits et al. 2000; Stauffer et al. 2001;
Jacobs et al. 2003b
Ophiostoma bicolor Kirisits et al. 2000; Stauffer et al. 2001
Ophiostoma brunneo- Redfern et al. 1987; Redfern 1989;
ciliatum Kirisits et al. 2000; Stauffer et al. 2001
(Ophiostoma fusiforme) Agayeva et al. 2004
(Ophiostoma lunatum) Agayeva et al. 2004
Ophiostoma piceae Kirisits et al. 2000; Stauffer et al. 2001
Ophiostoma cf. Kirisits et al. 2000; Stauffer et al. 2001
piceaperdum
Ips duplicatus b,e Ceratocystis polonica Valkama 1995; Krokene and Solheim
((Picea abies) 1996
Ophiostoma bicolor Valkama 1995; Krokene and Solheim
1996
Ophiostoma penicillatum Valkama 1995; Krokene and Solheim
Ophiostoma piceae Valkama 1995; Krokene and Solheim
1996
Ophiostoma piceaperdum Krokene and Solheim 1996; Jacobs and
Wingfield 2001
(Ophiostoma sp.) Mathiesen 1950
Pesotum sp. Krokene and Solheim 1996
Ips sexdentatus b,e Ambrosiella ips Siemaszko 1939; Mathiesen-Käärik

((Pinus spp.) 1953
Ambrosiella tingens Mathiesen-Käärik 1953
Graphium pseudormiticum Kirschner 1998, 2001; Kirisits,
unpublished
Leptographium sp. Lieutier et al. 1989
Table 2 continued
(= O. brunneo-ciliatum?)
Ophiostoma brunneo- Mathiesen-Käärik 1953; Lieutier et al.
ciliatum 1989, 1991; Kirisits et al. 2000
Ophiostoma clavatum Mathiesen-Käärik 1953
Ophiostoma ips Siemaszko 1939; Francke-Grosmann
1952; Lieutier et al. 1989, 1991;
Kirschner 1998, 2001; Kirisits et al.
2000
(= O. arborea?)
Ophiostoma minus Siemaszko 1939; Lieutier et al. 1989
Ophiostoma obscura Kirschner 1998, 2001
Ophiostom piceae Kirisits, unpublished
Ophiostoma sp. Mathiesen 1950; Mathiesen-Käärik 1953
Pesotum fragrans Mathiesen-Käärik 1953
Ips typographus b,e Ceratocystiopsis alba Kirschner 1998, 2001; Kirisits,

((Picea abies) unpublished
Ceratocystiopsis minuta Siemaszko 1939; Mathiesen 1950; 1951,
Kotýnková-Sychrová 1966; Käärik
1975; Solheim 1986, 1992b, 1993;
Harding 1989; Kirisits 1996; Grubelnik
1998; Kirschner 1998, 2001; Kirisits et
al. 2000; Viiri and Lieutier 2004;
Jankowiak 2004
Ceratocystis polonica Siemaszko 1939; Mathiesen 1950, 1951;
Mathiesen-Käärik 1953; Käärik 1975;
Solheim 1986, 1992a, 1992b, 1993;
Harding 1985, 1989, 1995; Furniss et
al. 1990; Krokene and Solheim 1996;
Viiri and Weissenberg 1995; Kirisits
1996; Viiri 1997; Grubelnik 1998;
Kirschner 1998, 2001; Kirisits et al.
2000; Viiri and Lieutier 2004, Salle et
al. 2003; Jankowiak 2004
Graphium fimbriisporum Morelet 1995; Kirisits 1996; Grubelnik
1998; Kirisits et al. 2000; Jacobs et al.
2003b
Graphium (Pesotum
( ?) Grosmann 1931; Siemaszko 1939,
pycnocephalum Mathiesen 1950; Mathiesen-Käärik
1953; Kotýnková-Sychrová 1966;
Jankowiak 2004
Leptograhium euphyes Jankowiak 2004
Leptographium lundbergii Harding 1989
Leptographium spp. Rennerfelt 1950; Kirschner 1998; Viiri
and Weissenberg 1995; Viiri 1997;
Viiri and Lieutier 2004
Ophiostoma ainoae Solheim 1986, 1992a, 1992b, 1993;
Harding 1989; Viiri and Weissenberg
1995; Kirisits 1996; Viiri 1997;
Grubelnik 1998; Kirschner 1998, 2001;
Kirisits et al. 2000; Viiri and Lieutier
208 T. KIRISITS
Table 2 continued
2004; Jankowiak 2004
Ophiostoma bicolor Kotýnková-Sychrová 1966; Davidson et
al. 1967; Käärik 1975; Solheim 1986,
1992a, 1992b, 1993; Harding 1985,
1989; Furniss et al. 1990; Viiri and
Weissenberg 1995; Kirisits 1996;
Krokene and Solheim 1996; Viiri
1997; Grubelnik 1998; Kirschner 1998,
2001; Kirisits et al. 2000; Viiri and
Lieutier 2004; Salle et al. 2003;
Jankowiak 2004
Ophiostoma cainii Harding 1989
Ophiostoma cucullatum Solheim 1986; Harding 1989; Kirisits
1996; Grubelnik 1998; Kirschner 1998,
2001; Kirisits et al. 2000; Viiri and
Lieutier 2004; Jankowiak 2004
Ophiostoma flexuosum Solheim 1986; Harding 1989; Jankowiak
2004
Ophiostoma floccosum Mathiesen 1950, 1951; Mathiesen-
Käärik 1953
(= O. arborea?)
(Ophiostoma minus) Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma neglectum Kirschner 1998; Kirscher and
Oberwinkler 1999
(Ophiostoma obscura) Kirschner 1998, 2001
Ophiostoma penicillatum Grosmann 1931, 1932; Goidànich
1936; Siemaszko 1939; Rennerfelt
1950; Mathiesen 1950; Mathiesen-
Käärik 1953; Kotýnková-Sychrová
1966; Davidson et al. 1967; Käärik
1975; Solheim 1986; 1992a, 1992b,
1993; Harding 1985, 1989; Furniss et
al. 1990; Viiri and Weissenberg 1995;
Kirisits 1996; Krokene and Solheim
1996; Viiri 1997; Grubelnik 1998;
Kirschner 1998; Kirisits et al. 2000;
Jacobs and Wingfield 2001; Viiri and
Lieutier 2004; Jankowiak 2004
chalcographi]
Ophiostoma piceae Grosmann 1931; Siemaszko 1939;
Rennerfelt 1950; Mathiesen 1950;
Mathiesen-Käärik 1953; Käärik 1975;
Solheim 1986, 1992b, 1993; Harding
1985, 1989; Viiri and Weissenberg
1995; Kirisits 1996; Krokene and
Solheim 1996; Viiri 1997; Grubelnik
al. 2000; Viiri and Lieuter 2004;
Jankowiak 2004
Ophiostoma piceaperdum Kotýnková-Sychrová 1966; Solheim
1986, 1992b, 1993; Harding 1989,
1995; Viiri and Weissenberg 1995;
Table 2 continued
Kirisits 1996; Viiri 1997; Grubelnik
al. 2000; Jacobs and Wingfield 2001;
Viiri and Lieutier 2004; Salle et al.
2003; Jankowiak 2004
(Ophiostoma Mathiesen-Käärik 1953
pluriannulatum)
Ophiostoma serpens Kotýnková-Sychrová 1966
Ophiostoma stenoceras Mathiesen 1950; Mathiesen-Käärik
1953; Kirschner 1998
Ophiostoma tetropii Käärik 1975; Solheim 1986, 1992b;
Viiri and Weissenberg 1995; Viiri 1997,
Kirschner 1998; Salle et al. 2003
Ophiostoma spp. Rennerfelt 1950; Mathiesen 1950;
Mathiesen-Käärik 1953; Harding 1989;
Viiri and Lieutier 2004
Pesotum fragrans Solheim 1992b
Pesotum sp. Furniss et al. 1990; Solheim, 1992a,
1992b, 1993; Krokene and Solheim
1996
Pesotum (Graphium?) spp. Harding 1985, 1989; Furniss et al. 1990;
Solheim 1992b, 1993; Viiri and
Weissenberg 1995; Viiri 1997; Viiri
and Lieutier 2004; Jankowiak 2004
Leperisinus varius b,ff (Ophiostoma quercus) Kirschner 1998

((Fraxinus excelsior)
Orthotomicus laricis b,e Ceratocystiopsis falcata Kirschner 1998

((Pinus sylvestris) Ceratocystiopsis minuta Kirschner 1998, 2001
Ceratocystis leucocarpa Kirschner 1998
Leptographium sp. Kirschner 1998
Ophiostoma bicolor Kirschner 1998, 2001
Ophiostoma cucullatum Kirschner 1998, 2001
Ophiostoma ips Kirschner 1998, 2001
(= O. arborea?)
Ophiostoma obscura Kirschner 1998, 2001
Orthotomicus proximus b,e (Ceratocstis coerulescens) Mathiesen 1950; Mathiesen-Käärik 1953

((Pinus sylvestris)
Graphium (Pesotum
( ?) Mathiesen-Käärik 1953
pycnocephalum
((Leptographium lundbergii) Mathiesen 1950; Mathiesen-Käärik
(Ophiostoma clavatum) Mathiesen-Käärik 1953
Ophiostoma ips Mathiesen-Käärik 1953
Ophiostoma minus Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma piliferum Mathiesen-Käärik 1953
(Ophiostoma sp.) Mathiesen 1950
210 T. KIRISITS
Table 2 continued
((Pesotum fragrans) Mathiesen-Käärik 1953
Pityogenes chalcographus b,e Ceratocystiopsis minuta Kirisits 1996; Kirschner 1998, 2001;
((Picea abies) Kirisits et al. 2000
(Ceratocystis coerulescens) Mathiesen 1950; Mathiesen-Käärik 1953
Ceratocystis polonica Krokene and Solheim 1996; Kirisits
1996, Kirisits et al. 2000
Graphium fimbriisporum Kirisits 1996; Kirisits et al. 2000; Jacobs
et al. 2003b
Graphium ((Pesotum?) Mathiesen 1950; Mathiesen-Käärik 1953
pycnocephalum
Leptographium sp. Kirisits et al. 2000
Ophiostoma ainoae Kirisits 1996; Kirschner 1998, 2001;
Kirisits et al. 2000;
Ophiostoma bicolor Krokene and Solheim 1996; Kirisits
al. 2000
Ophiostoma cucullatum Kirschner 1998, 2001; Kirisits et al.
2000
Ophiostoma floccosum Mathiesen 1950, 1951; Mathiesen-
Käärik 1953; Lin 2003
Ophiostoma neglectum Kirschner 1998; Kirscher and
Oberwinkler 1999
(Ophiostoma obscura) Kirschner 1998, 2001
Ophiostoma penicillatum Grosmann 1931; Goidànich 1936;
Mathiesen 1950; Mathiesen-Käärik
1953; Kirschner 1998; Jacobs and
Wingfield 2001
chalcographi]
1953; Krokene and Solheim 1996;
Kirisits, 1996; Kirschner 1998, 2001;
Ophiostoma piceaperdum Kotýnková-Sychrová 1966; Davidson et
al. 1967; Kirisits 1996; Kirschner
1998, 2001; Kirisits et al. 2000; Jacobs
and Wingfield 2001
Ophiostoma serpens Kotýnková-Sychrová 1966
Pesotum sp. Kirisits 1996; Kirisits et al. 2000
Pesotum (Graphium?) sp. Mathiesen 1950; Mathiesen-Käärik 1953
Pityogenes quadridens b,g ((Ambrosiella tingens) Mathiesen 1950, Mathiesen-Käärik 1953

((Pinus sylvestris)
Leptographium lundbergii Mathiesen-Käärik 1953; Jacobs and
Wingfield 2001
Ophiostoma canum Mathiesen 1950; Mathiesen-Käärik 1953
(Ophiostoma minus) Mathiesen-Käärik 1953
[Ophiostoma penicillatum f. Mathiesen 1950; Mathiesen-Käärik 1953
pini]
Table 2 continued
Polygraphus poligraphus b,e Ambrosiella sp. Krokene and Solheim 1996; Rollins et
((Picea abies) al. 2001
Ceratocystis polonica Krokene and Solheim 1996
Graphium pseudormiticum Kirschner 1998
Ophiostoma bicolor Krokene and Solheim 1996; Kirschner
1998, 2001;
Ophiostoma penicillatum Krokene and Solheim 1996; Jacobs and
Wingfield 2001
Ophiostoma piceaperdum Kirschner 1998, 2001; Jacobs and
Wingfield 2001
Scolytus intricatus b,f Ophiostoma quercus Kirschner 1998

(Quercus spp.) Ophiostoma stenoceras Kirschner 1998
Scolytus spp. b,e Ceratocystiopsis cf.

f falcata Kirisits and Konrad, unpublished
(Ulmus spp.) Graphium penicillioides Brasier 1990; Kirisits et al. 2000;
Kirisits and Konrad, unpublished
Ophiostoma quercus Brasier 1990; Brasier & Kirk 1993;
Kirisits et al. 2000; Kirisits, unpublished
Ophiostoma piceae Brasier and Kirk 1993; Lin 2003
Ophiostoma ulmi e. g. Siemaszko 1939; Webber and
Brasier 1984; Webber and Gibbs 1989;
Webber 1990, 2000; Brasier 1990, 1991
Ophiostoma novo-ulmi e. g. Webber and Brasier 1984; Webber
and Gibbs 1989; Webber 1990, 2000;
Brasier 1990, 1991
Taphrorychus bicolor b,e Graphium penicillioides Kirschner 1998; Kirisits et al. 2000
((Fagus sylvatica) Leptographium sp. Kirisits, unpublished
Ophiostoma cf. acericola Kirschner 1998; Kirisits et al. 2000
Ophiostoma quercus Kirschner 1998; Kirisits et al. 2000; Lin
2003
Ophiostoma piceae Lin 2003
Ophiostoma cf. stenoceras Kirisits, unpublished
Tomicus minor c,e Ambrosiella tingens Rennerfelt 1950; Mathiesen 1950;

((Pinus spp.) Francke-Grosmann 1952; Mathiesen-
Käärik 1953; Rollins et al. 2001;
Kirisits, unpublished
Ceratocystiopsis minuta Mathiesen 1950, 1951; Mathiesen-
Käärik 1953
Graphium pseudormiticum Jacobs et al. 2003b
Leptographium guttulatum Kirisits et al. 2000; Jacobs et al. 2001b;
Jacobs and Wingfield 2001
Leptographium lundbergii Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma canum Rennerfelt 1950; Mathiesen 1950,
1951; Francke-Grosmann 1952;
Mathiesen-Käärik 1953; Kotýnková-
Sychrová 1966; Kirisits et al. 2000
(Ophiostoma floccosum) Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma minus Grosmann 1931; Rennerfelt 1950;
Mathiesen 1950; Mathiesen-Käärik 1953
212 T. KIRISITS
Table 2 continued
Ophiostoma piceae Mathiesen 1950; Francke-Grosmann
1952; Mathiesen-Käärik 1953
Ophiostoma piliferum Grosmann 1931; Siemaszko 1939;
Rennerfelt 1950; Mathiesen 1950;
Francke-Grosmann 1952; Mathiesen-
Käärik 1953
(Ophiostoma Mathiesen 1950; Mathiesen-Käärik 1953
pluriannulatum)
Ophiostoma spp. Rennerfelt 1950
Tomicus piniperda b,f Ambrosiella tingens Rennerfelt 1950; Mathiesen 1950;

((Pinus spp.) Mathiesen-Käärik 1953
Ceratocystiopsis minuta Mathiesen-Käärik 1953; Kirisits et al.
2000
Ceratocystis autographa Kotýnková-Sychrová 1966
Graphium (Pesotum
( ?) spp. Gibbs and Inman 1991; Wingfield and
Gibbs 1991
Leptographium euphyes Jacobs et al. 2001a; Jacobs and
Wingfield 2001
Leptographium guttulatum Jacobs et al. 2001b; Jacobs and
Wingfield 2001
Leptographium lundbergii Mathiesen 1950; Mathiesen-Käärik
1953; Gibbs and Inman 1991; Jacobs
and Wingfield 2001
Leptographium procerum Gibbs and Inman 1991; Jacobs and
Wingfield 2001
Leptographium wingfieldii Morelet 1988; Piou et al. 1989; Lieutier
et al. 1989; Solheim and Långström
1991; Gibbs and Inman 1991;
Wingfield and Gibbs 1991; Kirisits et al.
Leptographium sp. Kirschner 1998
Ophiostoma canum Rennerfelt 1950; Mathiesen 1950;
Mathiesen-Käärik 1953; Kirschner 1998
(Ophiostoma clavatum) Mathiesen 1950; Mathiesen-Käärik 1953
Ophiostoma floccosum Lin 2003
Ophiostoma galeiformis Zhou et al. 2004
Ophiostoma huntii Gibbs and Inman 1991; Jacobs and
Wingfield 2001
Ophiostoma ips Mathiesen-Käärik 1953
Ophiostoma minus MacCallum 1922; Grosmann 1931;
Siemaszko 1939; Rennerfelt 1950;
Solheim and Långström 1991; Piou et
al. 1989; Lieutier et al. 1989; Kirisits et
al. 2000
Ophiostoma piceae MacCallum 1922; Siemaszko 1939;
1953; Solheim and Långström 1991;
Gibbs and Inman 1991; Kirschner 1998;
Ophiostoma piceaperdum Solheim & Långström 1991; Kirisits et
al. 2000
Ophiostoma piliferum Siemaszko 1939; Rennerfelt 1950;
Table 2 continued
Solheim and Långström 1991; Gibbs and
Inman 1991; Kirisits, unpublished
Ophiostoma spp. Rennerfelt 1950; Mathiesen 1950,
Mathiesen-Käärik 1953
Xyleborus dispar d,e Ambrosiella hartigii i Hartig 1844; Francke-Grosmann 1958,

(Deciduous trees, rarely also 1967, Batra 1967; Zimmermann 1973;
conifers) Cassar and Blackwell 1996
Ceratocystis (Ophiostoma) Zimmermann 1973
sp.
Xyleborus dryographus d,e Ophiostoma verrucosum Gebhardt et al. 2002

(Deciduous trees)
Xyleborus germanus d,e Ambrosiella hartigii i Francke-Grosmann 1958, 1967, Batra

(Deciduous trees and 1967; Cassar and Blackwell 1996
conifers)
Xyleborus monographus d,e “Yellowish monilioid Francke-Grosmann 1958; 1966, 1967;

(Deciduous trees [Quercus fungus” i Kirschner 1998
sp.]) Ophiostoma grandicarpa Kirschner 1998
Ophiostoma quercus Kowalski 1991
Raffaelea sp. i Kowalski 1991
Xyleborus saxeseni d,e Ambrosiella sulfurea i Francke-Grosmann 1958, 1967; Batra

(Deciduous trees and 1967; Cassar and Blackwell 1996
conifers)
Xyloterus domesticus d,e Ambrosiella ferruginea i Hartig 1872b; Francke-Grosmann

(Deciduous trees [Fagus 1956a, 1958, 1967; Batra 1967;
sylvatica, Quercus sp., Zimmermann 1973; Cassar and
Betula sp.]) Blackwell 1996
Graphium penicillioides Zimmermann 1973
Graphium (Pesotum
( ?) sp. Zimmermann 1973
Ophiostoma ambrosia Bakshi 1950
(= Ophiostoma piliferum)
Ophiostoma bacillisporum Butin and Zimmermann 1972;
Zimmermann 1973
Ophiostoma piceae Zimmermann 1973
(Ophiostoma quercus?)
Ophiostoma torulosum Butin and Zimmermann 1972;
Zimmermann 1973; Kirisits,
unpublished
Xyloterus lineatus d,e Ambrosiella ferruginea i Hartig 1872a; Mathiesen-Käärik 1953;

(Conifers [Picea abies, Larix Francke Grosmann 1956a, 1958, 1967;
decidua, Larix kaempferi]) Batra 1967; Kirschner 1998, 2001
(Ceratocystis autographa) Bakshi 1951
(Graphium pseudormiticum) Kirschner 1998, 2001
Leptographium lundbergii Bakshi 1950; Kotýnková-Sychrová
(Ophiostoma cucullatum) Kirschner 1998, 2001
(Ophiostoma galeiformis) Bakshi 1951
214 T. KIRISITS
Table 2 continued
Oberwinkler 1999
Ophiostoma penicillatum Mathiesen-Käärik 1953; Jacobs and
Wingfield 2001
Ophiostoma piceae Bakshi 1950; Mathiesen-Käärik 1953;
Kirschner 1998, 2001
Ophiostoma piceaperdum Kotýnková-Sychrová 1966; Kirschner
1998, 2001
Ophiostoma piliferum Bakshi 1950
(Ophiostoma torulosum) Kirschner 1998
Xyloterus signatus d,e Ambrosiella ferruginea i Francke Grosmann 1956a, 1958, 1967;
(Deciduous trees) Batra 1967
Notes: a Host trees of particular bark beetle species follow Postner (1974) and Pfeffer (1995). Hosts in
brackets refer to the tree species, from which insects originated for the studies on the associated fungi
and/or from which fungi were isolated. b, c, d Feeding habit of the respective bark beetle species: b
phloeophagous, c phloeomycetophagous, d xylomycetophagous. e, f, g Level of intensity of association with
ophiostomatoid fungi for the respective bark beetle species: e intimately associated, f loosely associated, g
intensity of association not precisely known. Xylomycetophagous bark beetles have always been assigned
to the group of scolytids with intimate association with fungi, since they nutritionally depend on ambrosia
fungi. h Fungal species in bold font are appraised to be commonly associated with a given bark beetles
species. Fungi in parenthesis are extemely rare elements of the mycobiota of a bark beetle species. Fungi
in brackets are of doubtful taxonomic status. i Nutritionally important ambrosia fungus. j In the case of
different reports by various authors regarding the abundance/importance of a particular fungus associated
with a particular bark beetle species, the references, which reported the fungus as relatively common
associate are printed in bold font.
Ophiostomatoid fungi vary greatly in the specifity of association with certain

bark beetle species and the occurrence on different host trees. Some fungi are
specifically associated with one or a few scolytid species on one host trees, while
others occur with a wide range of insects and even on several host trees (Table 2).
Originally, many blue-stain fungi were thought to be very specific in their
association with bark beetles (Mathiesen-Käärik 1953; Francke-Grosmann 1967,
Whitney 1982). As surveys of the mycobiota of scolytids have increased in number,
it has become clear that strict specifity of fungi regarding their associated insects is
rare and rather the exception than the rule (Table 2; Krokene and Solheim 1996;
Kirisits 1996; Kirschner 1998; Kirisits et al. 2000; Jacobs and Wingfield 2001).
Despite the finding that some blue-stain fungi are less specific than previously
believed, there are still fungal species showing a relatively narrow range of insect
associates and host trees (Table 2). This is in clear contrast to other fungi, which are
associated with a broad range of bark beetles and often occur on more than one host
tree. Typical examples for the latter fungi are Ceratocystiopsis minuta and O.
piceaperdum, which occur together with an extremely wide spectrum of European
bark beetles on at least two conifer hosts (Table 2). Despite occurring in a wide
range of niches, C. minuta and O. piceaperdum rely on their insect associates for
transmission. However, another group of blue-stain fungi consists of unspecific
species, which occur both in association with insects as well as on logs without
insect attacks, indicating that they are both transmitted by bark beetles and by air-
borne or rain-splash inoculum (Matiesen-Käärik 1953; Dowding 1969; Gibbs 1993).
Examples for such unspecific ophiostomatioid fungi include Ophiostoma piceae, O.

floccosum and O. piliferum on conifers as well as O. quercus on hardwoods (Table
2).
5.2.4. Comparisons of the fungal assemblages of different bark beetle species

The synthesis presented in Table 2 allows for qualitative and quantitative
comparisons of the differences in the whole mycobiata of different bark beetle
species occurring on the same or on different host trees. This is a question, which is
directly connected to the specifity of blue-stain fungi regarding their associated
insects and hosts discussed above. Here, I also believe that specifity of the
assemblages of fungi with individual bark beetles has previously been overestimated
(e. g. Mathiesen-Käärik 1953; Francke-Grosmann 1967) and in many cases,
differences of the mycobiota between scolytids occurring on the same host are
relatively small and often mainly quantitative. For example, various spruce bark
beetles have many elements of their mycobiota in common (Table 2). One major
quantitative difference between the various bark beetles on Norway spruce refers to
C. polonica that is more commonly associated with I. typographus, I. duplicatus and
I. amitinus, while other spruce bark beetles rarely, if at all carry this blue-stain
fungus (e. g. Solheim 1986; Harding 1989; Krokene and Solheim 1996; Kirschner
1998; Kirisits et al. 2000; Table 2 and references therein).
Certain elements of the fungal assemblages of bark beetles on pine also overlap
between individual species, e. g. Ophiostoma ips, O. brunneo-ciliatum, O. minus and
C. minuta, but there are also fungi that are relatively specific for individual scolytid
species (Table 2). For example, the mycobiota of T. minor and I. acuminatus differ
considerably, even though these two scolytids often occur together on thin-barked
parts of the bole or branches of pines. Despite some overlap, the spectrum of fungi
associated with bark beetles on different host trees (e. g. spruce, pine and larch;
Table 2) generally shows large differences, which might suggest that the host tree is
more important than the associated insects, in driving specifity and speciation of
ophiostomatoid fungi.
5.2.5. Variation in the mycobiota of bark beetles

An intriguing aspect of the association of blue-stain fungi with phloem-feeding bark
beetles is the variation of the assemblages of fungi associated with the same bark
beetle species at different localities in Europe (Table 2 and references therein).
Various factors might be responsible for this variation. Among these, the
methodology employed in different studies may often be very important. Every
method of fungal isolation is selective. Thus, the species spectrum and frequency of
fungal associates of bark beetles can vary considerably depending on the sources
and the methods of isolation employed by different researchers (e. g. Furniss et al.
1990; Krokene 1996; Yamaoka et al. 1997; Grubelnik 1998, Kirschner 1998).
Methodological factors should be considered, when comparing results of different
studies on the mycobiota of bark beetles (Table 2). In addition, mycological studies
always have a strong “human component”. Thus, the experience, skills and focus of
the researcher can have a stong influence on the outcome of a study.
216 T. KIRISITS
The investigations by Kirschner (1998, 2001) may be a good example to illustate

the influence of the isolation methods on the results of a study. Kirscher (1998,
2001) used a specific medium for isolation, consisting mainly of pieces of inner bark
of Picea abies embedded in water agar, onto which adult, living bark beetles were
placed individually. Such an isolation procedure was not used in any other study on
the mycobiota of European bark beetles and this may be the reason that numerous
fungi recorded by Kirschner (1998, 2001) have not been reported in any other
investigation.
The variation of the mycobiota of bark beetles at different localities in Europe
has been best-known for I. typographus and this scolytid is again used as an
example to illustrate this phenomenon further, although variation in the spectrum of
blue-stain fungi between different localities is also known for other bark beetle
species (see Table 2 and references therein). An extremely diverse assemblage of
blue-stain fungi is associated with I. typographus in Europe. A similar spectrum of
fungi has been reported to occur together withh this bark beetle in various parts of the
continent, but remarkable qualitative and quantitative differences in the composition
of the mycobiota of this insect between study sites have also been documented.
Differences are most obvious for the most virulent fungal associate of I.
typographus, C. polonica. Other differences in the mycobiota of I. typographus are
also well-known, in particular for O. piceaperdum (Table 2), but they will not be
discussed further here.
Thus-far, C. polonica only has been found as common associate of I.
typographus in Poland (Siemaszko 1939), Norway (e. g. Solheim 1986, 1992a,
1992b; Krokene and Solheim 1996), in samples from Belgium (Harding 1989) and
at some localities in Austria (Kirisits 1996, 2001; Grubelnik 1998; Kirisits et al.
2000). In contrast, it was not recorded at all in some studies (Rennerfelt 1950;
Kotýnková-Sychrová 1966), or occurred rarely in investigations performed in
Sweden (Mathiesen-Käärik 1953; Harding 1989), Denmark (Harding 1989), Finland
(Viiri 1997), Germany (Harding 1989; Kirschner 1998) and France (Salle et al.
2003). It was also relatively rare in a recent study conducted in Southern Poland
(Jankowiak 2004). In another French study, C. polonica occurred at moderately high
frequencies (Viiri and Lieutier 2003). While it was the dominant fungal associate of
I. typographus in South-Eastern Norway (Solheim 1986, 1992a, 1992b), C. polonica
was less frequently isolated at six localities in Central Norway (Solheim 1993).
Likewise, the fungus was rare or only moderately frequent in several study sites in
Austria, in contrast to other localities where it was the dominant fungus associated
with I. typographus (Kirisits 1996, 2001; Grubelnik 1998; Kirisits et al. 2000). It is
particularly interesting that C. polonica is the most virulent blue-stain fungus
associated with I. typographus (e. g. Horntvedt et al. 1983; Christiansen 1985;
Solheim 1988; Krokene and Solheim 1998), which gives rise to speculation about
the ecological consequences of the variation of the occurrence of C. polonica within
the distribution range of I. typographus (Harding 1989; Solheim 1993).
There is no clear geographic pattern in the occurrence of C. polonica in Europe,
since the fungus was both reported as frequent associate of I. typographus in some
studies in Northern (e. g. Solheim 1986, 1992a, 1992b; Krokene and Solheim 1996)
and Central Europe, while it occurred rarely or not at all in studies in adjacent
countries (e. g. Rennerfeldt 1950; Mathiesen-Käärik 1953; Kotýnková-Sychrova

1966; Harding 1989; Viiri 1997; Kirschner 1998). Furthermore, C. polonica has also
been found together with I. typographus f. japonicus in Japan (Yamaoka et al. 1997;
Marin 2004), which suggests that the fungus follows the distribution range of its
vectors and host trees in Eurasia. Differences in the methodology between various
studies might also explain some of the varying results concerning the mycobiota of
I. typographus (see above), and in particular those regarding C. polonica. However,
the conflicting results about the occurrence and frequency of fungi associated with I.
typographus in Europe cannot be ascribed exclusively to differences in the
methodology employed in the various studies.
It has been suggested that the population dynamics of I. typographus has a strong
influence on the incidence and frequency of C. polonica or that C. polonica may
even play a role in the initiation and development of outbreaks of I. typographus
(Harding 1989; Solheim 1993). Following this hypothesis, C. polonica occurs at low
frequencies during non-outbreak periods of I. typographus, but its frequency
increases during the course of outbreaks. As increasing numbers of healthy trees are
attacked, C. polonica gains a habitat, in which it is more competitive than other
fungal associates of the spruce bark beetle (Harding 1989; Solheim 1993). This
competitive advantage is probably due to its ability to maintain growth in the wet
sapwood of healthy trees, which contains low levels of oxygen (Solheim 1991).
Thus-far, there is only weak evidence supporting this hypothesis. Solheim (1993)
developed this theory to explain differences in the frequency of C. polonica between
South-Eastern Norway, where a severe outbreak of I. typographus occurred in the
1970s and Central Norway where the spruce bark beetle never caused large-scale
damage. However, Harding (1989) did not find obvious differences in the frequency
of C. polonica between sites varying in the outbreak status of I. typographus.
Studies in Austria also provided no support for the view that the occurrence of C.
polonica is related to damage levels by I. typographus. Here, C. polonica occurred
at low frequencies in stands outside the natural range of Norway spruce, which have
been suffering most severely during the outbreak of I. typographus since 1992
(Grubelnik 1998; Kirisits et al. 2000; Kirisits 2001). In these Austrian studies, C.
polonica was more frequently recorded at localities within the natural range of
Norway spruce. This pattern of diffusion could be due to climatic influences.
Ceratocystis polonica has a relatively low temperature maximum around 31-32°C
(Marin 2004) which may inhibit its vigour and give other fungi such as O. bicolor
with higher growth maximum (Solheim 1991) competitive advantages at localities
with high spring and summer temperatures, such as at the Austrian localities in the
foothills of and outside the Alps. This hypothesis certainly requires thorough study.
Some authors have suggested that the vigour/vitality of Norway spruce may have
a strong influence on the spectrum of fungi that are isolated from the phloem and
sapwood following aattck by I. typographus (Harding 1989; Solheim 1992b;
Jankowiak 2004). According to this view, vigorous trees may favour the
development of C. polonica, whereas other ophiostomatoid fungi are more
competitive than C. polonica on low vigorous, wind-thrown and wind-broken trees
as well as logs. This hypothesis is connected to the other hypothesis that C. polonica
increases its frequency during outbreak periods of I. typographus (Harding 1989;
218 T. KIRISITS
Solheim 1993; see above). Harding (1989) found no relationship between the
occurrence of C. polonica and the health status of Norway spruce trees. In a recent
study in Poland, C. polonica was relatively rare, but it occurred more frequently on
healthy trees compared to weakened or dead trees as well as wind-thrown, wind-
broken and trap trees (Jankowiak 2004). Despite a few hypotheses have been
suggested to explain the variation of the frequency of C. polonica as associate of I.
typographus at different localities in Europe, this phenomenon seems to be very
complex and is not fully understood thus-far. This intriguing question, therefore,
deserves continuing and careful study in the future.
6. SYMBIOSIS BETWEEN BARK BEETLES AND FUNGI

The term “symbiosis” has been used with different meanings in various scientific
disciplines, either in a strict or broad sense. For the present discourse on fungal
associates of bark beetles I follow the terminology of Whitney (1982). In its original
definition symbiosis refers to the more or less continuous living together of different
species, regardless of the benefits or disadvantages to the partners. This broad
definition includes mutualism, antagonism and other symbiotic relationships.
Mutualism, often referred to as symbiosis in its strict sense, is defined as
relationship between two separate species where both partners benefit. In
antagonistic relationships, one or both partners are detrimentally affected. The
symbiotic relationships between xylomycetophagous bark beetles and ambrosia
fungi (6.1) and between true bark beetles and fungi (6.2) are discussed below.
6.1. Symbiosis between xylomycetophagous bark beetles and ambrosia fungi

The relationship between xylomycetophagous bark beetles and ambrosia fungi
clearly represents a symbiosis, since the two partners are in close physical contact
with each other throughout their life and do not become separated at any stage of
their life histories (Francke-Grosmann 1967; Beaver 1989; Berryman 1989).
Moreover, beetles and fungi are mutualistic symbionts, which benefit from and
obligately depend on each other (Francke-Grosmann 1967; Berryman 1989).
Ambrosia fungi mainly benefit from the association with ambrosia beetles by the
consistent dissemination of fungal spores and their inoculation into new, suitable
habitats (Francke-Grosmann 1967; Norris 1979; Beaver 1989). The fungi are also
selectively protected and nourished in the beetle´s mycangium. In the galleries,
ambrosia beetles actively take care of their ambrosia fungi and protect them from
other “weed” fungi which leads to the dominance of ambrosia fungi in the galleries
of xylomycetophagous bark beetles (Francke-Grosmann 1967; Beaver 1989).
For the beetles the advantage of the association with their domesticated ambrosia
fungi is obvious. The fungi provide the only source of food for the adult ambrosia
beetles and their larvae (Francke-Grosmann 1967; Norris 1979; Beaver 1989;
Berryman 1989). Ambrosia fungi derive nutrients from the wood of their host trees,
concentrate them in their mycelium and make them available to the ambrosia beetles
that feed on ambrosial layers formed along the galleries. Apart from converting
nutrients from the wood and providing them in a nutrient form (sugars and other
carbohydrates, lipids and proteins) that can be digested by the beetles, fungi produce
and concentrate nutrients essential for the beetles that are not at all or only at very
low concentrations present in the wood. Nutritionally beneficial fungi provide a very
rich source of protein, nitrogen and amino acids to the beetles (Beaver 1989; Six
2003 and references therein). Likewise, ambrosia fungi supply the beetles with
sterols (especially ergosterol) that are very essential for growth, molting, and
reproduction (Beaver 1989; Six 2003 and references therein). The fungal diet is
probably also important for fulfilling some of the vitamin requirements of the insects
(Beaver 1989). The total nutritional dependence of the xylemycetophagous bark
beetles on their asociated fungi makes it possible to successfully rear the insects on
artificial cultures of their ambrosia fungi (Francke-Grosman 1967; Beaver 1989;
Norris 1979).
6.2. Symbiosis between phloeophagous bark beetles and fungi

As in the ambrosia beetles and their associated ambrosia fungi, the relationship
between phloeophagous bark beetles and certain fungi, mainly ophiostomatoid
fungi, yeasts and occasionallyy basidiomycetes, represents in many cases also a
symbiosis, since the partners are more or less consistently and continuously
associated with each other. Only for a short period of time, during some stages of
larval development in the phloem, insects and fungi can physically become
separated from each other, and the larvae feed ahead of the front of fungal
colonization in the phloem (Whitney 1971; Yearian et al. 1972). Contact between
them is re-established after pupation of the insects in the pupal chambers where the
fungi often form dense layers of conidiophores and sometimes also ascocarps, and
young adults become inoculated with conidia and ascospores (Whitney 1971;
Webber and Gibbs 1989; Yearian et al. 1972) (see also Fig. 3).
While the association between phloeophagous bark beetles and certain fungi
clearly fulfills the criteria of a symbiosis, there is no unequivocal agreement whether
their relationship represents mutualism (Whitney 1982; Harding 1989; Harrington
1993a; Paine et al. 1997). True bark beetles form a heterogenous group and various
species differ considerably in their nutrion biology (phloeophagous versus
phloeomycetophagous), aggressiveness, attack strategies and range of vigour of host
trees selected for breeding. It is thus reasonable to assume that there is no universal
model describing the interactions between phloem-feeding bark beetles and
associated fungi. Bark beetle species may vary considerably in their dependence on
fungi and many different forms of symbiosis may be encountered in different bark
beetle-fungal complexes.
Fungal associates of true bark beetles benefit in similar ways from the
association with their insect partners as ambrosia fungi benefit from the relationship
with xylomycetophagous scolytids (Whitney 1982; Krokene 1996; Paine et al. 1997;
Six 2003). The fungi are transmitted and inoculated to new, appropriate habitats by
the beetles. The insects not only disseminate fungal spores, but also create wounds
in the bark, and enable blue-stain fungi and other fungal associates to infect the
220 T. KIRISITS
tissues of their host trees. Many blue-stain fungi occur exclusively in association
with bark beetles and obligately depend on the beetles to be transmitted to suitable
habitats (Francke-Grosmann 1967; Krokene 1996; Paine et al. 1997; Upadhyay
1981; Kirschner 1998; Six 2003).
The ecological significance of the fungi for the bark beetles is less clear and in
most cases still not fully understood. Differentt groups of fungi may be beneficial or
inimical to the insects in various ways (Paine et al. 1997). I will discuss four modes
of action how bark beetles can gain benefits from their associated fungi:
involvement of fungi in tree killing and in exhaustion of the defense mechanisms of
the host tree during bark beetle attack (6.2.1.), nutrition (6.2.2.), protection from
detrimental fungi (6.2.3.), and involvement in pheromone production (6.2.4).
6.2.1. Involvement of fungi in tree killing and in exhaustion of the defense

mechanisms of the host during attack by bark beetles
Blue-stain fungi have long been been suspected to play an important role in killing
of conifer trees attacked by bark beetles (e. g. Nelson and Beal 1929; Nelson 1934;
Bramble and Holst 1940). Many researchers considered the involvement of the fungi
in tree killing and in exhaustion of the defence mechanisms of the host as the main
mode of action from which bark beetles benefit from the association with fungi (e. g.
Berryman 1972; Whitney 1982; Christiansen et al. 1987; Christiansen and Bakke
1988; Harding 1989; Raffa and Klepzig 1992; Krokene 1996; Paine et al. 1997).
Association with phytopathogenic fungi has also been mentioned as an important
characteristic of aggressive bark beetle species and even as a prerequisite for
scolytids to display aggressive behaviour (Christiansen et al. 1987; Krokene 1996).
The high level of virulence of some fungal associates to their host trees (see 3.3.1.)
is the primary argument in support of the hypothesis that fungi are important
components in the ability of bark beetles to kill trees (e. g. Berryman 1972; Whitney
1982; Christiansen et al. 1987; Raffa and Klepzig 1992; Krokene 1996).
However, the general importance of fungi to help bark beetles in overcoming the
defense mechanisms of the host trees has also been questioned by several authors (e.
g. Harrington 1993a; Wingfield et al. 1995; Paine et al. 1997; Lieutier 2002, chapter
9). This view is based on several lines of evidence. Here, I will mention only a few
examples of the arguments that have been presented. Harrington (1993a) considers
the virulence of ophiostomatoid fungi merely as adaption to the habitat of bark
beetles on living trees that might have been evolved as result of interspecific
competition between various ophiostomatoid fungi, but not primarily through
coevolution with bark beetles. By their fast growth, tolerance against host chemicals
and their abilty to grow under anaerobic conditions in moist sapwood, pathogenic
species gain competitive advantages over other fungal associates (Harrington
1993a). Other arguments refer to the intimacy of association between bark beetles
and associated blue-stain fungi. For example, T. piniperda is so loosely associated
with L. wingfieldii and other ophiostomatoid fungi that it is difficult to understand,
how fungi could contribute to exhaust the defence mechanisms of pine trees during
natural attack of the pine shoot beetle (Lieutier et al. 1989a; Lieutier 1993, 2002,
chapter 9). In I. typographus, the pathogenic blue-stain fungus C. polonica has been
suggested to be essential to overcome the defense mechanisms of Norway spruce

(Christiansen et al. 1987; Christiansen and Bakke 1988; Krokene 1996; Krokene and
Solheim 1998). However, the frequency of C. polonica varies considerably between
different localities and in many areas in Europe this pathogenic fungus is only rarely
associated with I. typographus (see 5.2.5.). This clearly demonstrates that the spruce
bark beetle does not obligately need C. polonica to successfully colonize living
trees. Even in areas, where C. polonica occurs rarely, I. typographus is associated
with numerous ophiostomatoid fungi, in particular O. bicolor, O. penicillatum and
O. piceaperdum (Table 2). Thus, I. typographus always transmits fungi when
attacking living host trees. However, these species are less virulent than C. polonica
(Horntvedt et al. 1983; Harding 1989; Kirisits 1998) and probably less efficient to
exhaust the defense systems of Norway spruce.
Apart from the few examples mentioned above, no attempt is made in this
chapter to extensively review the role of ophiostomatoid fungi in tree killing and in
exhaustion of the defense mechanism of the host during bark beetle attack. This is
because this aspect of bark beetle-fungus relationship has recently been extensively
treated by Lieutier (2002) and Lieutier (chapter 9) and I also refer to other recent
reviews of this topic (Whitney 1982; Harding 1989; Harrington 1993a; Raffa and
Klepzig 1992; Krokene 1996; Paine et al. 1997). I believe that the various lines of
evidence justify to assume that bark beetle species greatly differ in the dependence
on fungi to interfer with the defense mechanisms of their host trees. It is easy to
predict that the debates on the role of fungi in overcoming the defense systems of
host trees will continue in the future. Simultaneously, the conflicting views will
likely stimulate research in various scolytid-fungus-host-systems, which will
contribute to improve our current understanding of the intriguing interactions
between bark beetles, fungi and live conifer trees.
The association of the Dutch elm disease pathogens O. ulmi and O. novo-ulmi
with elm bark beetles represents a bark beetle-fungus relationship that differs from
that of conifer bark beetles with blue-stain fungi. Scolytus species transmit O. ulmi
and O. novo-ulmi during maturation feeding from diseased to healthy trees (Webber
and Brasier 1984; Webber and Gibbs 1989). These healthy trees get infected, decline
due to Dutch elm disease and become susceptible to attack by the next generation of
elm bark beetles, which breed in the barkk of diseased elm trees. The pandemics of
Dutch elm disease since the early 20th century have created large amounts of
susceptible host trees for the elm bark beetles and the fungi thus provided benefits to
the populations of these scolytids (Webber and Brasier 1984; Webber and Gibbs
1989; Webber 2000). It should be considered, however, that the association of O.
ulmi and O. novo-ulmi with Scolytus spp. is an untypical bark beetle-fungus-host
relationship, since it is driven by an introduced pathogen that came in contact with
highly susceptible host trees (Brasier 2000).
6.2.2. Nutrition
Concerning their nutritional biology, it is reasonable to further distinguish two
groups within bark beetles colonizing the phloem of trees. One group of species
feeds both on the phloem of the host trees, but also on associated fungi, and it is
222 T. KIRISITS
probably justified to describe their feeding habit as “phloeomycetphagous”

(Francke-Grosmann 1952, 1966, 1967). Some, but not all species in this group
possess mycangia in which nutritionally relevant fungi are carried (Francke-
Grosmann 1952, 1963b; Whitney 1982; Paine et al. 1997; Six 2003). These
scolytids share characteristics of true bark beetles and xylomycetophagous bark
beetles (Francke-Grosmann 1952, 1966, 1967; Six 2003 and references therein).
Within the European bark beetle fauna, two species on pine, T. minorr and I.
acuminatus have been reported to have a phloeomycetophagous feeding habit
(Francke-Grosmann 1952, 1967). The larvae of these bark beetle species create very
short galleries in the phloem and move later in the outer sapwood where they
pupate. Initially the larvae feed in the phloem, but at later stages of their
development they feed on conidia and mycelium of fungi, I. acuminatus on
Ambrosiella macrospora and T. minorr on A. tingens. The fungi form dense conidial
layers in the larval galleries of I. acuminatus and T. minor, very similar to ambrosia
fungi associated with ambrosia beetles. In I. acuminatus an oral mycangium has
been detected in which the conidia of Ambrosiella tingens are transported (Francke-
Grosmann 1963b). No mycangium has so far been found in T. minorr (Francke-
Grosmann 1952, 1963b). Scolytids with phloeomycetophagous feeding habit are
probably more numerously represented in the North American bark beetle fauna.
Although they have not explicitly referred to as phloeomycetophagous, D. frontalis
and D. ponderosae likely belong to this group, since they both possess a mycangium
and feed on phloem as well as on fungi, upon which they are largely dependent for
nutrition (Barras 1973; Klepzig 2001a, 2001b; Six 2003).
Most bark beetle species that breedd in the phloem of trees are truly
phloeophagous and thus feed mainly on the phloem of their host trees, which is a
nutrient-rich substrate. Typically, they do not possess a mycangium and are less -
and in many cases not obligately - dependent on fungal associates for nutrition,
although the fungi may provide an additional food source for larvae and teneral
adults (Francke-Grosmann 1967; Harding 1989; Whitney 1982; Six 2003). Different
groups of fungi may vary in their importance for the insects. Yeasts are suspected to
be essential as suppliers of vitamins, especially B-group vitamins (Strongman 1986;
Pignal et al. 1988; Beaver 1989; Harding 1989 and references therein), while non-
mycangial ophiostomatoid fungi are generally thought to be less, if at all, important
for nutrition of phloeophagous bark beetles (Grosmann 1931; Yearian et al. 1972;
Whitney 1982; Harding 1989; Fox et al. 1993). Some blue-stain fungi even display
antagonism against bark beetles (Barras 1970; Yearian et al. 1972; Klepzig et al.
2001a, 2001b).
The nutritional relevance of yeasts and blue-stain fungi for phloeophagous bark
beetles in Europe is poorly known, but the few studies that have been conducted so
far, suggest that the insects can be reared successfully in the absence of blue-stain
fungi, while a positive influence of yeasts cannot be excluded (Grosmann 1931;
Harding 1989; Colineau and Lieutier 1994; Simsek and Führer 1993; Simsek 1994).
Grosmann (1931) concluded that yeasts and blue-stain fungi are not obligately
needed for the development of I. typographus, since a single larva free of micro-
organisms developed into an adult insect. This conclusion is questionable, however,
due to the limited scope of the study and because the fecundity and behaviour of
progeny was not tested. Harding (1989) was able to rear I. typographus in the
complete absence of blue-stain fungi through two generations, however, yeast were
occasionally isolated from parent and offspring beetles. Simsek and Führer (1993)
and Simsek (1994) successfully reared I. typographus from eggs to mature adults on
a semi-artificial medium based on ground phloem, in which the development of
associated fungi was suppressed by fungicides. Finally, Ips sexdentatus showed
normal breeding behaviour and reproduced successfully in absence of its fungal
associates, O. brunneo-ciliatum and O. ips (Colineau and Lieutier 1993). Besides
these European studies, Yearian et al. (1972) successfully reared I. avulsus, I.
calligraphus and I. grandicollis through 3 to 4 generations in the absence of O. ips
on pine logs. In summary, the nutritional role of associated fungi for phloeophagous
bark beetles has received relatively little attention in Europe thus-far, and this topic
should, therefore, be investigated more intensively in the future.
Studies in North America have shown that certain blue-stain fungi are
antagonists of bark beetles by making the phloem unsuitable for larval nutrition or
inhibiting ovioposition of adult beetles. In phloem colonized by O. minus larval
development of D. frontalis was negatively affected in various ways, resulting in
lower reproductive success (Barras 1970; Klepzig et al. 2001a, 2001b). Similarly,
ovioposition of Ips avulsus, Ips calligraphus and Ips grandicolis was almost totally
inhibited in the phloem of pine logs that had been preinfected by O. ips (Yearian et
al. 1972). Among conifer bark beetles in Europe it is generally not known, if blue-
stain fungi could have negative effects on brood development, but Webber and
Gibbs (1989) reported that larvae of elm bark beetles (Scolytus spp.) avoided areas
of elm bark that had previously been colonized by O. ulmi. Possible antagonistic
effects of blue-stain fungi on bark beetles in Europe form an uninvestigated area of
research that deserves attention in the future.
6.2.3. Protection from detrimental fungi

The idea that mutualistic fungi protect bark beetle galleries from invasion by
detrimental fungi originally comes from D. frontalis and its associated fungi and
phoretic mites (Klepzig et al. 2001a, 2001b). In this system, the two mycangial
fungi of D. frontalis, Entomocorticium sp. and C. ranaculosus compete with the
nonmycangial and antagonistic fungus, O. minus for resources in the phloem of trees
attacked by the southern pine beetle. The two mycangial fungi, especially
Entomocorticium sp. and to a lesser extent C. ranaculosus, provide some protection
from the detrimental O. minus to the developing larvae. Other examples of such
competitive interactions are mentioned by Six (2003).
I speculate that protection of the developing broods from antagonists by
associated fungi could be important in many beetle-fungus-systems. Blue-stain fungi
quickly colonize the gallery systems and the adjacent phloem after attack by bark
beetles and likely occupy this niche at least until the young insects have left their
host trees. Thus, ophiostomatoid fungi might play a considerable role in preventing
the establishment of fungi that are deleterious to the developing larvae. This
postulate certainly requires confirmation by thorough studies.
224 T. KIRISITS
6.2.4. Involvement in pheromone production

A few studies provided evidence that fungi may be involved in the production of
pheromones (Whitney 1982 and references therein; Harding 1989 and references
therein; Six 2003). The only investigation adressing this question in an European
bark beetle-fungus system is that of Leufvén et al. (1984) who showed in laboratory
assays that yeasts associated with I. typographus can convert cis/trans-verbenol, an
aggregation pheromone of this bark beetle, to verbenone, which functions as an
antiaggregation pheromone. The abundance of yeasts increased during later phases
of bark beetle attack and this increase occured at the same time as the increase of the
amount of verbenone, which suggests that yeasts could be important in interferring
with the chemical communication of I. typographus under field conditions (Leufvén
and Nehls 1986).
Many species of Ophiostoma and Ceratocystis produce volatile metabolites that
give fungal cultures characteristic odors (Hanssen 1993). These metabolites include
short-chain alcohols and esters, mono- and sesquiterpenes as well as other
miscellaneous compounds (Hanssen 1993). The production of intensive aromas by
ophiostomatoid fungi and especially by Ceratocystis species is viewed as an
adaption to attract various insects that are unspecifically involved in dissemination
of these fungi (Kile 1993; Harrington and Wingfield 1998). It is attractive to think
that volatiles produced by ophiostomatoid fungi might also play a role in the
chemical communication of bark beetles, but so far this assumption is speculative
and requires investigation (Hanssen 1993).
7. PERSPECTIVES FOR FUTURE RESEARCH

The association of fungi with bark beetles is a fascinating example of symbiosis that
has received much attention in the past. It is easy to predict that the fungi transmitted
by bark beetles and the relationship with their associated insects and host trees will
continue to fascinate scientists in various disciplines. The fact that bark beetles are
important forest pests and that many fungal associates of scolytids cause destructive
tree diseases or are economically important agents of blue-stain, will likely help to
justify allocation of research resources to continue studying these fungi thoroughly
and in an interdisciplinary manner. Below I will present a few ideas for future
research, from a personal, very subjective perspective.
Despite tremendous research efforts in the past I feel that we still can learn a lot
about the diversity of fungi in the bark beetle habitat. So far, only a minor portion of
the 154 European bark beetle species (Postner 1974) have been examined regarding
the fungi they carry. It is, therefore, likely that a large number of ophiostomatoid
fungi and other fungi associated with bark beetles remain to be discovered, even in a
relatively well-studied region as Europe. Further surveys of ophiostomatoid species
associated with bark beetles in Europe could greatly improve the knowledge on the
taxonomy, ecology and biogeography of these fungi.
It is only a little more than a decade ago that the issue of “sibling species” within
the ophiostomatoid fungi has started to receive considerable attention (Brasier and
Kirk 1993). They represent morphologically similar or even indistinguishable fungi
that are ecologically and genetically isolated and represent different biological
species. Examples of such sibling species in Europe are O. quercus and O. piceae as
well as the bark beetle-vectored blue-stain fungi, C. polonica and C. laricicola
(Brasier and Kirk 1993; Kirisits 2001; Harrington et al. 2002; Marin 2004). Due to
the rapid progress in the development of reliable molecular markers, it is likely that
many more sibling and kryptic species within the ophiostomatoid fungi will be
identified in the near future. Genetic studies, mating experiments, studies on the host
specialization of fungi and growth experiments can be effectively combined to
provide several lines of evidence to distinguish “sibling species”. These discoveries
will also improve the understanding of speciation within the ophiostomatoid fungi
and will provide new insights in their ecology and relationships with insects.
The synthesis of studies on the fungal assemblages of European bark beetles
(Table 2) has clearly shown that remarkable variation in the composition of the
mycobiota of the same bark beetle species at different localities in Europe can occur.
Ips typographus has been mainly used as a model to illustrate this phenomenon, but
it is also documented for other European scolytids. The factors, which drive the
variation of the mycobiota of I. typographus as well as the resulting implications for
the ecology and population dynamics of the spruce bark beetle still remain poorly
known. Thus, further studies on the variation of the mycobiota of I. typographus in
various parts of Europe will represent an intriguing area for future research.
Although I have focussed on I. typographus, comparisons of the mycobiota of
scolytids in various parts of Europe are certainly also of interest for other
economically important bark beetle species. I also believe that the role of phoretic
mites associated with bark beetles in transmission of blue-stain fungi should be
further investigated, since mites have been shown to be very important in driving the
transmission and frequency of ophiostomatoid fungi in bark beetle-fungus-mite-
systems in North America (Bridges and Moser 1983, 1986; Klepzig et al. 2001a,
2001b).
The relationships between phloem-feeding bark beetles and fungi represent in
most cases a “polysymbiosis”. Typically, at least two, and often more fungal species
are consistently associated with one scolytid species. It is reasonable to assume that
different fungi interact in various ways with their bark beetle partners, with some
fungi being beneficial for the insects, while others being neutral or antagonistic
symbionts (Six 2003). Likewise, fungal associates strongly compete with each other
for space and resources in the bark beetle habitat (Klepzig et al. 2001a, 2001b).
These competitive interactions may influence the frequency of occurrence of fungal
associates, which likely also has some consequences for the insect-fungal
relationships. I think that we have presently just started to understand the
interactions between various fungal associates of bark beetles at varying ecological
situations (Klepzig et al. 2001a, 2001b; Six 2003). Therefore, the competitive
interactions between fungi associated with scolytids in vitro and in vivo form a
largely uninvestigated and highly intriguing area for future research that will provide
essential information for characterizing the bark beetle-fungus symbiosis (Klepzig
1998; Klepzig and Wilkins 1997; Klepzig et al. 2001a, 2001b; Six 2003).
Although much is already known about the phytopathogenicity of bark beetle-
associated blue-stain fungi, there is still a need for further studies. The pathogenicity
226 T. KIRISITS
of some potentially important fungal species and the ability of these fungi to
stimulate the defense reactions of their host trees should be tested, considering
especially the variation of virulence displayed by different isolates of the same
fungal species (see Lieutier et al. 2004). Likewise, the recently discovered
mycovirus-mediated hypovirulence in C. polonica and C. laricicola (Marin 2004)
offers many possibilities for future research. This includes the possible ecological
implications of dsRNA mycovirus infections on populations of these Ceratocystis
species and possible chances for implementation of biological control strategies. It
may also be very intriguing to screen other pathogenic blue-stain fungi for the
presence of dsRNA mycoviruses and to study the possible effects of the viruses on
the pathogenicity and fitness of the fungi.
Pathogenic blue-stain fungi have been an invaluable tool to study the defense
mechanisms of conifers against bark beetles and fungi (Lieutier 2002, chapter 9 and
references therein) and I look forward to the progresses in the understanding of the
resistance mechanisms of conifers that will be made in the future. In addition,
studies should consider the processes of inoculation and infection of blue-stain fungi
under natural conditions. For many conifer bark beetle species it is well established
that they carry blue-stain fungi, however, the spore load of associated fungi
transmitted by individual beetles is not known for most beetle-fungus-systems (but
see Webber and Brasier 1984; Webber and Gibbs 1989; Webber 1990, 2000). For a
few blue-stain fungi ((L. wingfieldii and O. brunneo-ciliatum) a relationship between
the number of spores inoculated and the intensity of the defense reaction has been
established (Lieutier et al. 1989a; Lieutier 1993, 2002, chapter 9), but such a
relationship has not been investigated for many other bark beetle-associated blue-
stain fungi. Both the spore load carried by the beetles as well as possible
relationships between the number of spores inoculated by the insects to the tree and
the intensity of the tree´s defense reactions are essential to understand inoculation
and infection of blue-stain fungi byy bark beetles under field conditions.
Recent reviews of the symbiosis between bark beetles and fungi, including the
present one, have proposed that there may be great differences between various bark
beetle-blue-stain fungus-systems in terms of the relevance of the fungi (Wingfield et
al. 1995; Krokene 1996; Paine et al. 1997; Lieutier 2002, chapter 9; Six 2003). In
order to improve our understanding of the relationship between bark beetles and
blue-stain fungi, additional studies should be initiated aimed at investigating the
direct effects of association with fungi for phloeom-feeding bark beetles. Whitney
(1982) proposed that the role of associated fungi for bark beetles could be revealed
by production of aseptic, microbe-free insects and by comparing them in biological
experiments with specifically fungus-inoculated insects or beetles from field
populations. The production of microbe-free insects is extremely difficult to achieve
and incudes the risk of failure. However, I believe that studies using aseptic bark
beetles will be a main approach in the future to make progress in the understanding
of the complex relationships between fungi, bark beetles and their host trees.
8. ACKNOWLEDGEMENTS
I thank Michael J. Wingfield and François Lieutier for their valuable comments and
suggestions for this chapter.
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Yamaoka, Y., Takahashi, I. & Iguchi, K. 2000. Virulence of ophiostomatoid fungi associated with the
spruce bark beetle Ips typographus f. japonicus in Yezo spruce. Journal of Forest Research, 5, 87-94.
Yearian, W.C., Gouger, R.J. & Wilkinson, R.C. 1972. Effecets of the bluestain fungus Ceratocystis ips on
development of Ips bark beetles in pine bolts. Annals of the Entomological Society of America, 65,
481-87.
Zhou, X.D., De Beer, Z.W., Harrington, T.C., McNew, D., Kirisits, T. & Wingfield, M.J. 2004.
Ophiostoma geleiformis and phylogeny of species in the O. galeiformis complex. Mycologia,
accepted.
Zimmermann, G. 1973. Vergleichende ökologisch-physiologische Untersuchungen an Ambrosiapilzen,
Assoziierten Bläuepilzen und Luftbläuepilzen.
t Dissertation, Georg-August-Universität Göttingen.
Zimmermann, G. & Butin, H. 1973. Untersuchungen über Hitze- und Trockenresistenz holzbewohnender
Pilze. Flora, 162, 393-419.
Chapter 11
RESEARCH ON PARASITOIDS AND PREDATORS OF

SCOLYTIDAE – A REVIEW
M. KENIS 1, B. WERMELINGER
R 2 & J.-C. GRÉGOIRE 3
1
CABI Bioscience Switzerland Centre, 2800 Delémont, Switzerland
2
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903
Birmensdorf, Switzerland
3
Université Libre de Bruxelles, 50 avenue F.D. Roosevelt, B-1050 Bruxelles,
Belgium
1. INTRODUCTION
Scolytidae are major forest pests in Europe. For example, Ips typographus (L.) is
considered the main pest problem in forestry in many central and northern European
countries. Consequently, there is a long tradition of forest entomology studying
various aspects of bark beetle ecology, including their natural enemy complexes,
with a view to developing control methods. In recent years, the need for the
development of sustainable pest management methods, taking into account the
whole forest ecosystem, has enhanced the interest in natural mortality factors.
Mills (1983) provided an extensive review of the natural enemies of conifer
feeding bark beetles in Europe. In contrast, natural enemies of broadleaf-feeding
species have never been reviewed. Furthermore, much research has been carried out
in the last 20 years, in particular in fields such as host/prey location or tritrophic
interactions. Other noteworthy reviews include two books by Hedqvist (1963; 1998)
on chalcid and braconid parasitoids of Scolytidae in Sweden, and a publication by
Nuorteva (1957) on parasitoids of bark beetles in Finland. Data are also available in
general parasitoid and predator catalogues such as Thompson (1943), Herting
(1973), and Noyes (2001), although these often repeat errors contained in primary
publications.
This review will focus primarily on parasitoids and predators of bark beetle
species considered to be pests of living trees in Europe, although it may also
consider relevant research in other continents. A list of these European species is
given in chapter 1. Pathogens of scolytids are reviewed in another chapter
(Wegensteiner, chapter 12).
237
237–290.
© 2007 Springer.
238 M. KENIS, B. WERMELINGER & J.C. GRÉGOIRE
2. PARASITOIDS
2.1. Parasitoid complexes
Tables 1, 2 and 3 list the hymenopteran parasitoids of European Scolytidae living on
Pinaceae, Cupressaceae and broadleaf trees, respectively. In addition to
Hymenoptera, mites can also be parasitic on eggs, larvae or pupae of bark beetles.
However, it is often difficult to properly assess the exact biology of mites, which
may either be parasites, parasitoids, predators, saprophytes or commensals. In this
review, mites will be reviewed in the predator section.
There is a large variation in the knowledge of the parasitoids of European bark
beetles. As expected, the parasitoid complexes of the most important pests have
been the target of specific studies. Parasitoids of Ips typographus have been studied,
among others, by Sachtleben (1952), Bomboschm (1954), Mills and Schlup (1989),
and Weslien (1992) and those of Tomicus piniperda (L.) and Ips acuminatus (Gyll.)
by Hérard and Mercadier (1996) and Balazy et al. (1987). Scolytus species have
been investigated as well because of their importance as vectors of the Dutch elm
disease (e.g. Beaver 1967a; Schroeder 1974; Maksimovic 1979; Merlin 1984,
Manojlovic et al. 2000a, 2000b). Phloeotribus scarabaeoides (Bernard) was studied
extensively by several authors for its importance in olive plantations (Russo 1938;
González and Campos 1990a, 1991). Hintze-Podufal and Druschke (1988), Mills
(1991) and Lozano and Campos (1991) provide significant data on the parasitoid
complex of Leperisinus varius (F.) and Eichhorn and Graf (1974) on the ambrosia
beetles Trypodendron spp. In addition, Nuorteva (1957), Hedqvist (1963, 1998), and
Mendel (1986) provide numerous rearing records for bark beetles in Finland,
Sweden, and Israel, respectively. For many a European bark beetles, however,
information on their parasitoid complex is usually restricted to parasitoid-host lists,
catalogues and general studies which provide incomplete or erroneous records. No
mention of parasitoids was found in the European literature for the following
scolytid species: Gnathotricus materiarius (Fitch), Hylastes spp., Hylurgus
ligniperda (F.), Trypodendron signatum (F.) and Xylosandrus germanus
(Blandford). Larvae of these species either live in the root system (Hylastes spp., H.
ligniperda) or in the sapwood (G. materiarius, T. signatum, X. germanus) and are
thus probably less susceptible to generalist larval parasitoids. In addition, G.
materiarius and X. germanus are exotic species recently introduced into Europe,
which may have not yet been adopted by European parasitoids.
The parasitoid complex of a particular scolytid host is difficult to evaluate
because of the cryptic habit of bark beetle larvae and because a scolytid species
usually shares the same breeding resource with a range of other insects. In most
studies, parasitoids were reared from entire logs and attributed to the most abundant
or most likely host, which resulted in many erroneous records. The most obvious
mistakes are easily detected. For example, the braconid parasitoid Eubazus
semirugosus (Nees) has often been associated with scolytids (Herting, 1973;
Hedqvist, 1998) whereas it is a common egg-prepupal parasitoid of weevils of the
genus Pissodes that cannot parasitize eggs of scolytids in galleries (Kenis and Mills,
1998). Similarly, most records of Ichneumonidae on Scolytidae are erroneous, with
PARASITOIDS AND PREDATORS OF SCOLYTIDAE 239
the exception of the large spruce species Dendroctonus micans (Kug.), which is
commonly attacked by the ichneumonid Dolichomitus terebrans (Ratzeburg)
(Grégoire 1976). However, errors are often more difficult to trace, especially when
two or more scolytid species occur simultaneously. Ideally, parasitism should be
evaluated by the debarking of infested wood, observation and determination of host
galleries and single rearing of parasitoid larvae, pupae or cocoons. Unfortunately,
only few studies were based on log dissection and individual rearing (e.g. Schroeder
1974; Mendel 1986). Another method to study parasitoids and other natural enemies
consists of the exposure of sentinel hosts for a short period of time, as was carried
out by Weslien (1992) with I. typographus.
2.2. Parasitoid guilds and general biology

A parasitoid guild can be defined by the host stage attacked, the host stage killed,
and the mode of parasitism (endo- or ectoparasitism) (Mills, 1994). Four parasitoid
guilds are found on Scolytidae.
2.2.1. Egg parasitoids

Only one true hymenopteran egg parasitoid has been undoubtedly reared from
scolytids in Europe. Trichogramma semblidis (Aurivillius) is a well-known
parasitoid of the ash bark beetle Leperisinus varius (= Hylesinus fraxini Panzer = H.
orni Fuchs) and the closely related ash species Hylesinus crenatus F. (e.g. Michalski
and Seniczak 1974; Hintze-Podufal f and Druschke 1988). It is also reported from 56
species of Lepidoptera, Diptera and Coeloptera (Noyes, 2001). However, the genus
Trichogramma is a taxonomically difficult group, and sibling species within this
complex with a narrower host range cannot be ruled out. T. semblidis was very
common on ash bark beetles in Poland, with mean parasitism rates of 11-14%
(Michalski and Seniczak 1974). Parasitoid females were found in galleries
ovipositing in freshly laid beetle eggs.
2.2.2. Egg-larval endoparasitoids

The only confirmed egg-larval parasitoid of Scolytidae in Europe is the eulophid
Entedon ergias Walker (= leucogramma (Ratzeburg)), one of the most abundant
parasitoids of broad-leaf scolytids of the genus Scolytus (Hedqvist 1963; Schroeder
1974; Merlin 1984; Yates, 1984). Other Entedon spp. have been reported from bark
beetles (Tables 1 and 3), but their biology is unknown. The biology of E. ergias has
been described in detail by Beaver (1966a) on Scolytus scolytus (F.). The female
enters the scolytid maternal gallery to oviposit in the egg. The parasitoid
development occurs internally. Parasitised larvae are usually killed in the 4th,
penultimate instar. Parasitism induces a modification of the behaviour of the
parasitised larva, which moves to the outer bark before the unparasitised ones.
Overwintering occurs as a larva in the host larva or as a pupa in the gallery. There
are one or two generations per year. E. ergias has also be studied extensively in the
USA, where it was accidentally introduced and became established on the elm
beetle, Scolytus multistriatus (Van Driesche et al. 1996)
2.2.3. Larval ectoparasitoids

Most of the parasitoids of Scolytidae belong to this guild. Two different strategies
are observed. Larval ectoparasitoids can eitherr enter bark beetle galleries to find and
parasitize host larvae ("cryptoparasitoids"), or can locate and parasitise their host
through the bark. The best known cryptoparasitoid is the holarctic Roptrocerus
xylophagorum (Ratz.), a common and polyphagous parasitoid of conifer bark
beetles. Its biology has been extensively studied, both in Europe and the USA (e.g.
Hedqvist 1963; Samson 1984; Pettersson et al. 2000; Sullivan et al. 1999). Eggs are
laid on bark beetle larvae and, occasionally, on pupae in the galleries. Two other
species, Roptrocerus mirus (Walker) and R. brevicornis (Thomson), occur on
conifers in Europe (Hedqvist 1963). They have never been studied in detail and have
been cited much less frequently and from fewer hosts than R. xylophagorum (Table
1). However, this may result from identification errors since recent studies showed
that R. mirus is nearly as frequent as R. xylophagorum, particularly on spruce
(Wermelinger 2002; M. Kenis, unpublished). The pteromalid Cerocephala
eccoptogastri Masi and several Bethylidae are mentioned as cryptoparasitoids of
scolytid larvae and pupae by Mendel (1986), and seem to be particularly abundant in
southern Europe and the Mediterranean region (Tables 2, 3) (Russo 1938; Mendel
1986). Other probable cryptoparasitoids are the species that attack ambrosia beetles
in the sapwood, Perniphora robusta (Ruschka) and Eurytoma polygraphi
(Ashmead), although their oviposition behaviour has never been clearly described.
The majority of the larval parasitoids attack their host through the bark. This
biology is encountered mainly in Braconidae and Pteromalidae, but also in
Ichneumonidae, Eurytomidae, Torymidae and Eupelmidae. Nuorteva (1957),
Hedqvist (1963, 1998) and Mills (1983) provide general overviews of the biology of
these parasitoids, but some species have been studied in greater detail, for example,
Coeloides bostrichorum Giraud, Rhopalicus tutela (Walker) and Dendrosoter
middendorffii (Ratzeburg) as parasitoids of Ips typographus (Sachtleben 1952;
Bombosch 1954; Krüger and Mills 1990; Hougardy and Grégoire 2001),
Cheiropachus quadrum (F.) and Rhaphitelus maculatus Walker on Phloeotribus
scarabaeoides (Russo 1938; Campos and Gonzalez 1990, 1991; Gonzalez and
Campos 1990b; Campos and Lozano 1994), and Dendrosoter protuberans (Nees), a
parasitoid of Scolytus species (Kennedy, 1970). The general biology is similar for
most species. Parasitoids usually locate their host by walking on the bark, paralysing
the larvae or pupae by injecting venom, and laying a single egg on the paralysed
host. Eggs and larvae develop quickly. Overwintering usually occurs as prepupae or
pupae, in the host gallery. Braconids and ichneumonids build a cocoon in the
gallery, whereas chalcids pupate directly in the host gallery. Several ectoparasitoids
act as facultative or obligatory hyper- or cleptoparasitoids on other parasitoids of the
same guild (see section 2.6 below).
2.2.4. Adult endoparasitoids

Adult parasitism is a relatively rare event in endopterygote insects. Bark beetles,
however, are frequently parasitized in the adult stage by a range of Braconidae and
Pteromalidae (Table 1). Interestingly, adult parasitism seems to be restricted to
conifer bark beetles whereas there is no record from broadleaf species, apart from
the dubious notification of Centistes cuspitatus Hal. on Leperisinus varius (Hintze-
Podufal and Druschke 1988). The most studied adult parasitoid is the pteromalid
Tomicobia seitneri (Ruschka), a frequent parasitoid of Ips typographus and,
possibly, some other Ips spp. Faccoli (2000a, 2001a) provides a review of its
biology. Females oviposit into adult beetles of various ages on the bark. Parasitized
beetles are still able to bore into the bark and lay eggs, but fecundity is reduced by
an average of 30% (Sachtleben 1952). The parasitoid kills its host and emerges from
it in the gallery. It has usually two generations per year. Overwintering occurs as a
larva in the host beetle. T. seitneri seems to be present in most I. typographus
populations and parasitism rates vary from 20% to 100% (Faccoli 2000a). T. seitneri
is often parasitized in the host beetle by another pteromalid, Mesopolobus
typographi (Ruschka) (Balazy and Michalski 1962; Seitner, in Hedqvist 1963).
Several other Tomicobia spp. are reported from conifer bark beetles in the world
(Faccoli 2001a). In Europe, T. acuminati Hedqvist is found on Ips acuminatus and
T. pityophthori (Boucek) on Pityogenes chalcographus (L.) (Hedqvist 1963;
Lobinger and Feicht 1999).
Braconid adult parasitoids all belong to the sub-family Euphorinae.
Ropalophorus clavicornis (Wesmael) is a frequently encountered parasitoid of I.
typographus (Nuorteva 1957; Hedqvist 1998; Faccoli 2001a). Its biology has been
poorly studied but seems to be very similar to that of T. seitneri (Bombosch 1954;
Nuorteva 1957; Faccoli 2001a). There is very little information on the level of
parasitism by R. clavicornis, except from Bombosch (1954) who mentions 18%
parasitism in Bavaria. In a large collection of parasitoids from spruce infested by I.
typographus in Switzerland, R. clavicornis was the main adult parasitoid, and the
third most abundant species of the whole parasitoid complex (Wermelinger 2002).
The genus Cosmophorus comprises several species apparently specialised on conifer
bark beetles. Five of them occur in Europe. Hedqvist (1998) and van Achterberg
and Quicke (2000) provide determination keys, host lists and general data on their
biology, which is apparently similar to the other adult parasitoids. Finally, another
euphorine braconid, Cryptoxilos cracoviensis (Capek and Capecki), has been reared
from adults of Cryphalus piceae (Ratz.) in Poland (Capek and Capecki 1979).
2.3. Host specificity

Host range is among the most difficult characteristics to determine in parasitoid
ecology (Shaw 1994). The literature is full off identification mistakes and erroneous
host-parasitoid associations, especially in bark beetles and their parasitoids, which
are usually associated merely because they emerge from the same logs. The most
obvious errors were removed from Tables 1, 2 and 3, but these undoubtedly still
contain many wrong associations. However, patterns in host specificity can emerge
from the most serious studies. For example, adult parasitoids and the egg-larval
parasitoid Entedon ergias are probably more specific than the majority of the larval
ectoparasitoids. E. ergias seems to be restricted to the genus Scolytus. Tomicobia
seitneri and Ropalophorus clavicornis are usually associated with I. typographus,
Tomicobia acuminati with Ips acuminatus and Tomicobia pityophtori with
Pityogenes chalcographus. The host specificity of Cosmophorus spp. is less clear,
and at least some species have been reared from several bark beetle hosts (Hedqvist
1998). The high specificity of parasitoids attacking eggs and adults could be
explained by the fact that females probably a locate their host by their aggregative
pheromone, as shown for T. seitneri (Mills and Schlup 1989; Faccoli 2000a), T.
pityophthori (Lobinger and Feicht 1999) and R. clavicornis (Faccoli 2001a). More
generally, koinobiont endoparasitoids tend to be more specific than idiobiont
ectoparasitoids because the former live in close interaction with the hormonal
system of their host.
Larval ectoparasitoids of Scolytidae are thought to be rather more host-tree
specific than host-specific, but this is highly variable. Few parasitoids are commonly
found on conifer and broad-leaf species. The main examples include Eurytomidae
(e.g. Eurytoma morio Boheman) and Eupelmidae (e.g. Eupelmus urozonus Dalman),
which are known to be facultative or obligatory hyperparasitoids, but also some
Pteromalidae such as Heydenia pretiosa Forster, r Dinotiscus colon (L.), and the
braconidd Ecphylus silesiacus (Ratzeburg), although the existence of cryptic species
cannot be ruled out. The pteromalid, Perniphora robusta, and the eurytomid
Eurytoma polygraphi are specialised in ambrosia beetles living in the sapwood, but
are found equally in conifers and broad-leaf trees. Other overlaps are probably the
result of identification errors or accidental parasitism. Within conifers or broad-leaf
trees, some parasitoids are reported to be polyphagous and to attack beetles on
various tree genera (e.g. Rhopalicus tutela, Roptrocerus spp., Dendrosoter
middendorffii), whereas others seem to be confined to a single tree genus (e.g.
Metacolus unifasciatus Forster, Coeloides abdominalis (Zetterstedt) and C.
sordidatorr (Ratzeburg) on pine, and Coleoides bostrichorum, on spruce). Some
larval ectoparasitoids are strongly linked to a host species, such as C. bostrichorum
with I. typographus, although other host records are sometimes found. However, it
remains to be seen whether the apparentt association between a parasitoid and a
particular host tree is due to the tree itself or to the host beetle, or a combination of
the two. Interestingly, when I. typographus, a typical spruce bark beetle,
occasionally attacks pine, it is followed by its whole range of parasitoids, including
those that are usually associated with spruce rather than pine, such as C.
bostrichorum, D. eupterus, T. seitneri and R. clavicornis (Turcani and Capek, 2000;
Turcani and Kenis, unpublished). Inversely, during an outbreak of the pine bark
beetle Ips sexdentatus (Boern.) on oriental spruce (Picea orientalis) in Turkey,
Schimitschek (1940) reared a parasitoid complex very similar to that usually
observed on pine, including C. abdominalis, a species usually associated with
various pine beetles.
Very few studies have focused on parasitoid host range in Scolytidae. A notable
exception is Mendel (1986) who, in Israel, collected 26 parasitoid species from 15
bark beetle species on 17 different members of the Pinaceae, Cupressaceae and

various broad-leaf families. He reared parasitoids singly from identified larval
galleries, which prevented errors in host-parasitoid associations. Interestingly, there
was little overlap between the parasitoid complexes in Pinaceae and other trees, but
the overlap was much larger between Cupressaceae and broad-leaves. All levels of
host specificity were found, from highly polyphagous species (e.g. H. pretiosa) to
species specific to a single beetle (e.g. Ecphylus caudatus Rushka on Hypoborus
ficus (Erichson), to a single genus (e.g. Entedon ergias on Scolytus spp.), or
restricted to a single tree species but polyphagous within this tree (e.g. D.
middendorffii, or R. xylophagorum in Pinus). The mechanisms leading to polyphagy
or monophagy in larval ectoparasitoids are not clear, but probably include multiple
factors such as host- and host tree location (both long range and short range), and
physical constrains such as bark thickness and host size. Host location is the subject
of the following section. The influence of bark thickness on host range has been
investigated by Manojlovic et al. (2000a) in E. silesiacus, a parasitoid of Scolytus
spp. on elm. E. silesiacus, the species living in the thickest bark, was the least
parasitized and the least preferred host.
2.4. Host location

The topics of host location and, more generally, tri-trophic interactions, have
provided some of the most interesting studies on bark beetle parasitoids in recent
years. Host location mechanisms have been studied because they are supposed to be
the key to understanding parasitoid host ranges, and also because their better
understanding would allow the development of new control methods aiming at
conserving and augmenting natural enemies in the field. In addition, Mills and his
colleagues studied host location mechanisms in Ips typographus parasitoids to
evaluate their potential as biological control agents against new hosts in North
America (Mills and Krüger, 1989; Mills and Schlup, 1989; Mills et al., 1991). The
location of bark beetles by parasitoids involves two distinct steps. Firstly, the
parasitoid must locate the host habitat, i.e. an infested tree (long-range host
location). Secondly, the parasitoid must be able to locate a particular host at a
suitable developmental stage (short-range host location).
The attraction of the adult parasitoid Tomicobia seitnerii to the aggregation
pheromone of Ips typographus was shown in field conditions by Mills and Schlup
(1989) and Faccoli (2000a). Mills and Schlup also tested pheromones of American
Dendroctonus spp., to which T. seitneri did not respond, suggesting that this host
location mechanism involves specific interactions, and may be responsible for the
higher specificity in adult parasitoids compared to larval parasitoids. Lobinger and
Feicht (1999) showed that Tomicobia pityophthori was strongly attracted by the
pheromone of its host, Pityogenes chalcographus. It is likely that other adult
parasitoids also locate their hosts using the host pheromone as kairomone, as
suggested by Faccoli (2001a) for Ropalophorus clavicornis. In contrast, it seems
that aggregation pheromones do not attract larval ectoparasitoids, as shown by Mills
and Schlup (1989) for I. typographus parasitoids. However, multistriatin, a
component of the aggregation pheromone of Scolytus multistriatus is known to be

attractive for several larval ectoparasitoids of this elm-feeding scolytid (Kennedy,
1984; Gonzales et al., 1999). The mechanisms and cues involved in long-range host
location in larval ectoparasitoids are unclear. Mills and Schlup (1989) suggested that
the cues could be emitted by the host-associated fungi. However, in a field
experiment, Rhopalicus tutela was attracted by spruce logs and isolated bark
infested with I. typographus larvae, but not by spruce wood containing the
associated fungi alone.
In Spain, Lozano et al. (2000) showed that the larval ectoparasitoids
Dendrosoter protuberans and Cheiropachus quadrum and their host, Phloeotribus
scarabaeoides are attracted by the same compounds, alpha-pinene and 2-decanone.
They suggest that these parasitoids could use these compounds to locate their host.
Mechanisms of short-range host location in larval ectoparasitoid have been
studied more extensively, especially on I. typographus and its main parasitoids
(Mills et al. 1991; Pettersson 2001a, 2001b; Pettersson et al. 2000, 2001a, 2001b).
They followed interesting observations by Ryan and Rudinsky (1962) and Richerson
and Borden (1972) on Coeloides vancouverensis (D.T.) (= C. brunnerii Vier.) and its
host Dendroctonus pseudosugae Hopkins in North America, providing evidence for
the role of sound and infra-red radiation, respectively, as cues for locating host
larvae beneath the bark. However, in a series of experiments on I. typographus
parasitoids (Coeloides bostrichorum, Dendrosoter middendorffii and Rhopalicus
tutela), Mills et al. (1991) rejected the role of sound, vibration and infrared
radiation, and showed evidence that volatile cues play the major role. However, they
were not able to isolate the source of these volatiles, nor the volatiles themselves.
Pettersson and co-authors (Pettersson et al. 2000, 2001a, 2001b; Pettersson 2001a,
2001b) confirmed the role of volatiles in host location in C. bostrichorum, R. tutela,
Roptrocerus mirus and R. xylophagorum. They revealed odour perceptive sensillae
on antennae of R. tutela (Pettersson et al. 2001a), and showed that, for all parasitoids
investigated, the attractive compounds were mainly oxygenated monoterpenes
present in infested trees. These are probably involved in both short-range and long-
range attraction, and seem not to arise from the insect hosts, but from the host-plant
complex, including associated fungi.
2.5. Dispersal, longevity and feeding behaviour in the field

Most knowledge on the biology and ecology of parasitoid adults has been gathered
from laboratory rearing (e.g. Kennedy 1970; Krüger and Mills 1990; Campos and
Gonzales 1990; 1991; Gonzales and Campos 1990b, Manojlovic et al. 2000a), or
from observations of adult behaviour on infested logs (e.g. Hedqvist 1963, Mills
1991). However, the ecology and biology of adults of bark beetle parasitoids remain
largely unknown, especially in relation to dispersal capacities, longevity in natural
conditions and feeding habits in the field. These characteristics, however, are
essential in the development of new management methods taking into account the
roles and impacts of parasitoids and other natural mortality factors. Hougardy and
Grégoire (2000) suggested that food sources such as nectar, pollen and honeydew
are available in abundance in spruce forests and that searching for food is probably
not time and energy consuming.
Dispersal behaviour could be studied using rubidium as an internal marker.
Promising results were obtained by Hougardy et al. (2003) who marked larval
parasitoids of Ips typographus by introducing rubidium chloride into spruce vascular
systems. In another recent field study, Lobinger and Feicht (1999) used traps baited
by the pheromone of Pityogenes chalcographus related to an electronic design to
study the swarming behaviour of the adult parasitoid Tomicobia pityophthori.
2.6. Competitive interactions and other mortality factors in parasitoids

Larval ectoparasitoids are often subject to hyper- or cleptoparasitism. Antagonistic
interactions between parasitoids of scolytids have been discussed by Mills (1991).
Eurytoma morio and Eurytoma arctica Thomson, polyphagous parasitoids of conifer
and broad-leaf tree scolytids, may act as primary parasitoids (e.g. Nuorteva 1957;
Hedqvist 1963; Pettersen 1976a), cleptoparasitoids (Mills 1991) and
hyperparasitoids through Braconidae and Pteromalidae (Sachtleben 1952; Nuorteva
1957). Eupelmidae of the genera Calosota and Eupelmus have been frequently
reared from logs attacked by bark beetles (e.g. Hedqvist 1963, Pettersen 1976b;
Mendel 1986) but the few data available on their biology suggest that they act
mainly as hyperparasitoids (Hedqvist 1963). Kenis and Mills (1994) observed that
Calosota aestivalis Curtis and Eupelmus urozonus, the most often cited eupelmid
parasitoids of bark beetles in Europe, parasitized cocoons of Dolichomitus terebrans
and Coeloides spp., respectively, in galleries of Pissodes castaneus De Geer (Col.:
Curculionidae) in pine logs. Rarely, primary pteromalid parasitoids may also act as
facultative hyperparasitoids of braconids, as observed with Dinotiscus eupterus on
Dendrosoter middendorffii (Sachtleben 1952).
Cleptoparasitism is probably a common behaviour among parasitoids of bark
beetles. Mills (1991) showed that females of Cheiropachus quadrum and E. morio
commonly displaced females of Coeloides filiformis Ratz. ovipositing on the ash
bark beetle Leperisinus varius. Hougardy and Grégoire (2003) observed that, on Ips
typographus, R. tutela females were able to displace C. bostrichorum from the
oviposition sites to steal the host previously located by the braconid. Hougardy
(2003) also investigated the niche partitioning mechanisms in the main parasitoids
of I. typographus, i.e. Coeloides bostrichorum, Rhopalicus tutela, and Roptrocerus
xylophagorum. She analysed between-stand, between-tree and within-tree
distributions, as well as habitat preferences and interactions with other species.
Competitive interactions among parasitoids of adults have been poorly studied.
Mesopolobus typographi is known as a hyperparasitoid of Tomicobia seitneri
(Seitner, in Hedqvist, 1963), but its biology is largely unknown.
Table 1. Parasitoids reared reared from scolytid species feeding on living Pinaceae in Europe and the Near East. xx = Particularly 246
reliable association, i.e. mentioned in at least four different studies, or obtained byy log dissection. x = other records. (xx) = Association
that appears dubious to the senior author because it comes from an unreliable study and the biology of the parasitoid makes this i
association unlikely. Totally unlikely associations are not mentioned in this table.
Tomicus minor
Dendroctonus micans
Pityokteines vorontzovi
Ips acuminatus
Ips amitinus
Ips duplicatus
Ips sexdentatus
Ips typographus
Orthotomicus erosus
Pityogenes trepanatus
Pityokteines curvidens
Pityophtorus pityographus
Tomicus piniperda2
Cryphalus piceae
Ips cembrae
Pityogenes conjunctus
Pityokteines spinidens
Polygraphus poligraphus
Tripodendron lineatum
Main references3 a, a, a, a,b a,b a, a,b a,b a a a,b b a, a, a, a,c a,b a,b a,b a,b
b b c,f c,f u g
c,f c,f b b c,d c,d b c,d c b b b c,d c,d c,d d,v
,ln c,f e,f c e,f c, c g, e,f e,f, e,f,l,m,
,g ,j c, e,f f
h,i k,l ,l ,lz ,ln g § l u
d l,n ,s
Guild1
e,f op
q,r
,ly st
wx
Braconidae
Blacus humilis (Nees) ? . . . . . . . . . . . . . . . . . . x .
Bracon instabilis (Marshall) L.ec. . . . . . . . . . . . . . . . . . (x) (x) .
B. hylobii Ratzeburg L.ec. . x . . . . . . . . . . . . . . . . . .
M. KENIS, B. WERMELINGER & J.C. GRÉGOIRE
B. osculatorr Nees L.ec. . . . (x) . . . . . . . . . . . . . . . .

B. palpebratorr Ratzeburg L.ec. . . . . (x) . . (x) . . . . . . . . . x x .
B. stabilis (Wesmael) L.ec. . . . . . . . (x) . . . . . . . . . . . .
Coeloides abdominalis (Zetterstedt) L.ec. . . xx . x. . xx .x . . . . . . . . . xx xx .
C. bostrichorum Giraud L.ec. x . . x. x x x. xx . . xx . x . . . . . x .
C. scolyticida Wesmael L.ec. . . . . . . . (x) . . . . . . . . . (x) . .
C. sordidatorr (Ratzeburg) L.ec. . . .x . . . x. (x) . . . . . . . . . xx xx .
Table 1. (cont.).
P. vorontzovi
I. amitinus
P. curvidens
T. minor
C. piceae
D. micans
I. acuminatus
I. cembrae
I.. duplicatus
I. sexdentatus
I.. typographus
O. erosus
P. conjunctus
P. chalcographus
P. trepanatus
P. spinidens
P. pityographus
P. poligraphus
T. piniperda2
T. lineatum
Cosmophorus cembrae Ruschka A.en. x . . . . . . . . . xx . . x x . (x) . . .

C. klugi Ratzeburg A.en. . . . . . . . xx . . . . . x x . xx . . .
Cosmophorus regius Niezabitowski A.en. . . . . . . . xx . . . . . . . . xx . . x
Cryptoxilos crocoviensis (Cap. & C.) A.en. x . . . . . . . . . . . . . . . . . . .
Dendrosoter flaviventris Förster L.ec. . . . . . . . . xx . . x . . . . . . xx .
(= caenopachoides Ruschka)
D. hartigi (Ratzeburg) L.ec. . . x . . . . . xx . x x . . . . x xx . .
D. middendorfi (Ratzeburg) L.ec. x x x x x x x xx xx . x . x . x x xx xx xx (x)
D. protuberans (Nees) L.ec. . . . . . . (x) . . . . . . . . . . (x) (x) .
Dendrosotinus similes Boucek L.ec. x . . . . . . . . . . . . . . . . . . .
Doryctes leucogasterr (Nees) L.ec. . . . . . . . (x) . . . . . . . . . . . .
D. mutilator (Thunb.) (= obliteratus L.ec. . . . . . . (x) (x) . . . . . . . . . . (x) .

Nees = strigztus Kokujev)
D. pomarius Reinhard L.ec. . . . . (x) . . (x) . . . . . . . . . . . .
PARASITOIDS AND PREDATORS OF SCOLYTIDAE
D. striatellus (Nees) L.ec. . . . . . . . . . . . . . . . . . . (x) .

Ecphylus caudatus Ruschka L.ec. x . . . . . . . . . . . . . . . . . . .
E. hylesini (Ratzeburg) L.ec. . . x . . . . x . . xx . . x x x xx x . .
E. silesiacus (Ratzeburg) L.ec. x . . . . . . . . . x . . . x x . . . .
Heterospilus sicanus (Marshall) L.ec. x . . . . . . . . . . . . . . . . . . .
Lysitermus pallidus Förster L.ec. . . . . . . . . . . . . . . . . xx . . .
247
248
Table 1. (cont.).
P. vorontzovi
I. amitinus
P. curvidens
T. minor
C. piceae
D. micans
I. acuminatus
I. cembrae
I.. duplicatus
I. sexdentatus
I.. typographus
O. erosus
P. conjunctus
P. chalcographus
P. trepanatus
P. spinidens
P. pityographus
P. poligraphus
T. piniperda2
T. lineatum
Lestricus secalis (L.) ? . . . . . . . (x) . . . . . . . . . . . .

(= Cenocoelus agricolator L.)
Ontsira antica (Wollaston) L.ec.. . . (x) . . . . . . . . . . . . . . (x) .
O. imperator (Haliday) L.ec.. . . . . . . . . . . . . . . . . . (x) (x) .
Perilitus rutilus (Nees) A.en. . . . . . . . . . . . . x . . . . . . .
Ropalophorus clavicornis (Wesm.) A.en. . . . x . . . xx . . . . . . . . . . . .
Spathius brevicaudis Ratzeburg L.ec. . . (x) . . . . (x) . . (x) . . . . . . . (x) .
S. exarator (L.) L.ec. . . . . (x) . . (x) . . . . . . . . . (x) . .
S. rubidus Rossi L.ec. . . . . . . . . . . . . . . . . . (x) . .
Ichneumonidae
Dolichomitus terebrans (Ratz.) L.ec. . xx . . . . . . . . . . . . . . . . . .
Neoxorides collaris (Gravenhorst) L.ec. . (x) . . . . . . . . . . . . . . . . . .
Xorides irrigatorr (F.) L.ec. . (x) . . . . . . . . . . . . . . . . . .
Pteromalidae
Cheiropachus quadrum (F.) L.ec. . . (x) (x) . . (x) x . . (x) . . . . . . (x) (x) .
Dinotiscus aponius (Walker) L.ec. . (x) . . . . (x) (x) . . . . . . . . . . (x) .

D. colon (L.) L.ec. . . xx . . . . . . . . . . . . . . xx x .
Dinotiscus eupterus (Waljer) L.ec. x . x x . . (x) xx . x xx . . x x x xx (x) . .
Heydenia pretiosa Forster L.ec. . . x . . . . xx xx . . . . . x . . xx . .
Macromesus amphiterus Walker L.ec.? . . . . . . . . . x x . . . . . . . . .
Table 1. (cont.).
I. acuminatus
I. amitinus
P. curvidens
P. vorontzovi
I. cembrae
T. minor
C. piceae
D. micans
I.. duplicatus
I. sexdentatus
I.. typographus
O. erosus
P. conjunctus
P. chalcographus
P. trepanatus
P. spinidens
P. pityographus
P. poligraphus
T. piniperda2
T. lineatum
Mesopolobus typographi (Ruschka) A.en. (h). . . x x . . . xx . . x . . . . . x . (x) .

Metacolus azureus (Ratzeburg) L.ec. . . x . . . . . xx x x . . . . . . x xx .
M. unifasciatus Forster L.ec. . . xx . . . . (x) xx . . . . . . . . xx xx .
x
Perniphora robusta Ruschka L.ec. c.? . . . . . . . . . . . . . . . . . . .
x
Platygerrhus affinis (Walker) L.ec.? . . . . . . . . . . . . (x) . . . . . . .
Psychophagus omnivorus (Walker) (h) ? . . . . . . . (x) . . . . . . . . . . . .
Pteromalus abieticola Ratzeburg ? . . . . . . . . . . x . . . . . . . . .
P. puparum (L.) ? . . . . . . . . . . . . (x) . . . . . . .
(
Rhaphitelus ladenbergii (Ratz.) L.ec. . . . . . . . . . . . . . . . . . . (x) .
Rhopalicus guttatus (Ratzeburg) L.ec. . . . . . . . (x) . . . . . . . . . . x .
R. quadratus (Ratzeburg) L.ec. . . xx xx . . . . . . xx . . . . . . xx xx .
R. tutela (Walker) L.ec. . x xx xx . xx xx xx . . xx . x . . . x xx xx .
Roptrocerus brevicornis Thomson L.ec.c. . . xx . . . . . . . xx . . . . . . xx xx .
R. mirus (Walker) L.ec.c. . . . . . . . xx . . x . . . . . x . x .
R. xylophagorum (Ratzeburg) L.ec.c. xx . xx xx x xx . xx xx . xx . x x x . x . xx .
Tomicobia acuminate Hedqvist A.en. . . xx . . . . . . . . . . . . . . . . .

T. pityophthori (Boucek) A.en. . . x . . . . . . . x . . . . . . . . .
T. seitneri (Ruschka) A.en. . . x x . x . x . . . . . . . . . . . .
Eulophidae
Aprostocetus hedqvisti Graham ? . . . . . . . . . . . . . . . . . x . .
249
250
Table 1. (cont.).
P. vorontzovi
I. acuminatus
I. amitinus
P. curvidens
I. cembrae
C. piceae
D. micans
I.. duplicatus
I. sexdentatus
I.. typographus
O. erosus
T. minor
P. conjunctus
P. chalcographus
P. trepanatus
P. spinidens
P. pityographus
P. poligraphus
T. piniperda2
T. lineatum
Entedon methion (Walker) E-L.en.? . . x . . . . . . . . . . . . . . . . .

E. pinetorum Ratzeburg E-L.en.? . . . . . . x . . . . . . . . . . . . .
Eupelmidae
Calosata aestivalis Curtis L.ec. (h) . . . . . . . . xx . . . . . . . . . . .
Eupelmus urozonus Dalman L.ec. (h) . . x . . . . x . . . . . . x . x . . .
Eurytomidae .
Eurytoma abieticola Ratzeburg L.ec.? . . . . (x) . . (x) . . . . . . . . . . . .
E. arctica Thomson L.ec. . . xx x . . x xx . . x . . . . . . xx xx .
E. blastophagi Hedqvist L.ec. . . . . . . . xx . . . . . . . . . . . .
E. crassinervis Thomson L.ec.? . . . . . . . (x) . . (x) . . . . . . . . .
E. morio Baheman L.ec. . . x . . . . xx xx . xx . . . . . . . . .
E. polygraphi (Ashmead) L.ec.? . . . . . . . (x) . . . . . . . . . . . xx

(= spessivtsevi Bouc. & Novicky)
E. rufipes Walker L.ec.? . . . . . . . . . . . . . . . . . . (x) .

1
r
Parasitoid guilds: L.ec. = Larval ectoparasitoid; L.ec.c. = Larval ectoparasitoid, cryptoparasitoid; E-L.-en. = Egg-larval endoparasitoid; (h) = Essentially hyperparasitoid. See text
for more details.
2
Includes data of the cryptic species T. piniperda and T. destruens
3
Referesces: a: Noyes (2001); b: Herting (1973); c: Mills (1983); d: Hedqvist (1963); e: Hedqvist (1998); f: Thomson (1943); g: Faccoli (2000b); h: Hedqvist (1967); i: Capeck &
Capecki (1979); j: Grégoire (1976); k: Voolma (1986); l: Nuorteva (1957); m: Hérard & Mercadier (1996); n: Grodski (1997); o: Bombosch (1954); p: Faccoli (2001a); q:
Hougardy & Grégoire (2003); r: Mills & Schlup (1989); s: Pettersen (1976a); t: Sachtleben (1952); u: Mendel (1986); v: Eichhorn & Graf (1974); w: Weslien (1992); x:
Wermelinger (2002); y: Balazy et al. (1987); z: Schimitschek k (1940); §: Capek (1955).
Predators and diseases are also responsible for mortality in bark beetle
parasitoids. Many generalist predators, such as clerid beetles and dolichopodid flies,
feed indiscriminately on botht hosts and parasitoids (Mills 1983), but their impact on
parasitoid populations has never been measured. Very little is known on pathogens
of bark beetle parasitoids, although researchers often observe dead parasitoid larvae
and pupae in galleries (M. Kenis, unpublished). Winter mortality is important.
Faccoli (2002) measured mortality rates of 47-48 % in C. bostrichorum and R.
xylophagorum in Italy. In Colorado, the winter mortality rate of Dendrosoter
protuberans varied between 79 and 89 % (Hostetler and Brewer 1976). The
mortality factors could not be firmly established, although low temperatures were
suspected to play a major role, especially in D. protuberans.
Table 2. Parasitoids reared from scolytidd species feeding on living Cupressaceae in

Europe and the Near East. xx = Particularly reliable association, i.e. mentioned in at least
four different studies, or obtained by log dissection. x = other records. Totally unlikely
associations are not mentioned in this table. Records from Ruschka (1916), Lichtenstein and
Picard (1920), Herting (1973), Mendel (1986), and Noyes (2001).
Guild1 Phloeosinus Phloeosinus Phloeosinus

armatus bicolor thujae
Braconidae
Dendrosoter protuberans (Nees) L.ec. xx xx .
Hecabolus sulcatus Curtis L.ec. . x x
Heterospilus incompletus (Ratzeburg) L.ec. . . x
Pteromalidae
Cerocephala eccoptogastri Masi L.ec.c. xx xx .
Heydenia pretiosa Forster L.ec.c. xx xx .
Metacolus unifasciatus Forster L.ec. xx xx x
Rhaphitelus maculatus Walker L.ec. xx xx x
Rhopalicus quadratus (Ratzeburg) L.ec. . . x
Eulophidae
Entedon ergias Walker E-L.en. . x .
Eupelmidae
Calosota aestivalis Curtis L.ec. (h) xx xx .
Eurytomidae
Eurytoma morio Boheman L.ec. xx xx x
Bethylidae
Cephalonomia hypobori Kieffer L.ec.c. . xx x
1
Parasitoid guilds: L.ec. = Larval ectoparasitoid; L.ec.c. = Larval ectoparasitoid, cryptoparasitoid; E-L.-
en. = Egg-larval endoparasitoid; (h) = Essentially hyperparasitoid. See text for more details.
Table 3. Parasitoids reared from scolytid species feeding on living broad-leaved trees in Europe and the
252
Near East. XX = Particularly reliable association, i.e. mentioned in at least four different studies, or
obtained by log dissection. X = other records. (X) = Association thatt appears dubious to the senior author
because it comes from an unreliable study and the biology of the parasitoid makes this association unlikely.
Totally unlikely associations are not mentioned in this table.
Guild1
crenatus
Hylesinus
varius2
Phloeotribus
scarabaeoides
intricatus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
ratzeburgi
Scolytus
dispar
Leperesinus
scolytus
Scolytus
Trypodendron
Xyleborus
domesticum
Main references3 a,b,c a,b,c a,j, a,b,d, a,b, a,b,d a,b a,b,e a,b, f,u
e,f g,h,i k,l f, m, d, e e,f,n, ,d,e, ,f,o,p, d,u
s, v o,p,q,r f,s q,t
Braconidae
Bracon caudatus Ratzeburg L.ec. . (x) . . . . . . . .
B. obscuratorr Nees L.ec. . (x) . . . . . . . .
B. palpebratorr Ratzeburg L.ec. . . . (x) . . . . . .
B. ratzeburgii Dalla Torre L.ec. . (x) . . . . . . . .
B. stabilis Wesmael L.ec. xx xx . . . . . . . .
B. tenuicornis Wesmael L.ec. . . x . . . . . . .
Centistes cuspidatus (Haliday) A.en.? . x . . . . . . . .
Coeloides abdominalis (Zetterstedt) L.ec. . (x) . . . . (x) . . .
C. filiformis Ratzeburg L.ec. xx xx xx . . . . . . .
C. melanotus Wesmael L.ec. x xx x . . . . (x) . .
C. scolyticida Wesmael L.ec. . x . . . xx x xx . .

C. sordidatorr (Ratzeburg) L.ec. . . . (x) . . . . . .
C. subconcolor (Russo) L.ec. . x xx . . . . . . .
C. ungularis Thomson L.ec. . . . . . . xx . . .
Dendrosoter ferrugineus (Marshall) L.ec. . . x . . . . . . .
D. protuberans (Nees) L.ec. xx xx xx x . xx x x . .
Table 3. (cont.).
Guild1
crenatus
Hylesinus
varius2
Phloeotribus
Leperesinus
scarabaeoides
intricatus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
ratzeburgi
Scolytus
scolytus
Scolytus
dispar
Trypodendron
Xyleborus
domesticum
Doryctes undulatus (Ratzeburg) L.ec. . . . (x) . . . . . .

(=brachyurus Marshall) .
Doryctes pomarius Reinhard L.ec. . . . . . x . x . .
D. rex Marshall L.ec. . . . . . . (x) . . .
Ecphylus eccoptogastri Ratzeburg L.ec. . . xx . . xx . x . .
E. hylesini (Ratz.) L.ec. (x) (x) . . . . . . . .
E. silesiacus (Ratzeburg) L.ec. . . xx x . xx . x . .
Hecabolus sulcatus Curtis L.ec.? . (x) . . . . . . . .
Meteorus consimilis (Nees) ? . . . . . x . . . .
M. obfuscatus (Nees) ? . . . . . . x x . .
Monolexis fuscicornis Förstrer (=Hecabolus L.ec.? . . x . . . . . . .
doderoi (Mantero))
Ontsira imperatorr (Haliday) L.ec. . . . . . . (x) . . .
Rhoptrocentrus piceus Marshall L.ec.? . . x . . . . . . .

Spathius brevicaudis Ratzeburg L.ec. . (x) . x (x) x . . . .
S. curvicaudis Ratzeburg L.ec. . . . . . x . . . .
S. exaratorr (L.) L.ec. (x) (x) . . . (x) . . . .
S.rubidus (Rossi) L.ec. . (x) x . . x . . . .
253
254
Table 3. (cont.).
Guild1
crenatus
Hylesinus
varius2
Phloeotribus
Leperesinus
scarabaeoides
intricatus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
ratzeburgi
Scolytus
scolytus
Scolytus
dispar
Trypodendron
Xyleborus
domesticum
Ichneumonidae
Nematopodius formosus Gravenhorst ? . . . . . . . . . (x)
(= Pseudopimpla anisandri (Fahringer))
Pteromalidae
Acrocormus semifasciatus Thomson L.ec.? . . . xx . . . . . .
Agrilocida ferrierei Stephan L.ec.? . . . . . xx . . . .
Cerocephala cornigera Westwood L.ec.c.? . xx xx . . x . . . .
C. eccoptogastri Masi L.ec.c. . x xx . . xx . . . .
Cheiropachus obscuripes Brues L.ec. . (x) . . . . . . . .
C. quadrum (F.) L.ec. . xx xx xx x xx x xx . .
Cleonymus obscurus (Walker) L.ec.? . . . . . . . x . .
Dinotiscus aponius (Walker) L.ec. x xx . . x x xx x . .
D. colon (L.) L.ec. . . x . . . xx . . .
Dinotiscus eupterus (Walker) L.ec. . x . . . . . (x) . .
Habritys brevicornis (Ratzeburg) L.ec.? . . . . . . . . x x

Heydenia pretiosa Förster L.ec. . x xx . . xx x . . .
Perniphora robusta Ruschka L.ec.c.? . . . . . . . . xx xx
Platygerrhus ductilis (Walker) L.ec.? . . . x . . . . . .
P. maculatus Erdös L.ec.? . . . x . . . . . .
Table 3. (cont.).
Guild1
crenatus
Hylesinus
varius2
Phloeotribus
Leperesinus
scarabaeoides
intricatus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
ratzeburgi
Scolytus
scolytus
Scolytus
dispar
Trypodendron
Xyleborus
domesticum
Pteromalus brunnicans Ratzeburg L.ec.? . . . . . . . x . .

Rhaphitelus ladenbergii Ratzeburg L.ec. . (x) . x . x . . . .
R. maculatus Walker L.ec. . x xx x . xx . x . .
Rhopalicus tutela (Walker) L.ec. . (x) . x . (x) . (x) . .
Roptrocerus mirus (Walker) L.ec.c. . . . (x) . . . . . .
R.xylophagorum Ratzeburg L.ec.c. . . . (x) . . . . . .
Theocolax formiciformis Westwood ? . (x) . . . . . . . .
Trigonoderus cyanescens (Förster) ? . . . (x) . . . . . .
T.princeps Westwood ? . . . . . . x . . .
Eulophidae
Aulogymnus bivestigatus (Ratzeburg) ? . x . . . . . . . .
Baryscapus hylesini Graham ? . x . . . . . . . .
Entedon armigerae Graham E-L.en.? . . . . (x) . . . . .
E.ergias Walker E-L.en. . . . xx xx xx xx xx . .

E.tibialis (Nees) E-L.en.? . . . x . . . . . .
Euderus albitarsis (Zetterstedt) ? . . . (x) . . . . . .
Stenomesius rufescens (Retzius) ? . . (x) . . . . . . .
Eupelmidae
Calymmochilus russoi Gibson ? . . x . . . . . . .
255
256
Table 3. (cont.).
Guild1
crenatus
Hylesinus
varius2
Phloeotribus
Leperesinus
scarabaeoides
intricatus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
ratzeburgi
Scolytus
scolytus
Scolytus
dispar
Trypodendron
Xyleborus
domesticum
Eusandalum merceti Bolivar & Pieltrain (h) . . . . . x . . . .

Eupelmus aloysii Russo L.ec. (h) . . x . . . . . .
E. annulatus Nees L.ec. (h)? . . . . . . x . . .
E. urozonus Dalman L.ec. (h) . x x x . . . . . .
E.vesicularis (Retzius) L.ec. (h) . x x . . . . . . .
Eurytomidae
Bruchophagus maurus (Boheman) L.ec.? . . . . . x . . . .
Eurytoma aloisfilippoi (Russo) L.ec. . x xx . . . . . . .
E. arctica Thomson L.ec. x xx . . . x . . . .
E.eccoptogastri Ratzeburg L.ec. . (x) . . . . . . . .
E.flavoscapularis Ratzeburg L.ec. . x . . . . . . . .
E.morio Boheman L.ec. x xx xx x x xx . x . .
E. polygraphi (Ashmead) L.ec.? . . . . . . . . xx .
(= spessivtsevi Bouc. & Novicky)
Torymidae
Torymus arundinis (Walker) L.ec.? . x . . . . . . . .
T. hylesini Graham L.ec.? x . . . . . . . .
Trichogrammatidae
Trichogramma semblidis Auriv. E.en. xx xx . . . . . . . .
Table 3. (cont.).
Guild1
crenatus
varius2
Phloeotribus
scarabaeoides
intricatus
ratzeburgi
Hylesinus
Leperesinus
Scolytus
laevis
Scolytus
multistriatus
Scolytus
Scolytus
scolytus
Scolytus
dispar
Trypodendron
Xyleborus
domesticum
Bethylidae
Cephalonomia cursorr Westwood L.ec.c.? . . xx . . . . . . .
C. hypobori Kieffer L.ec.c. . . xx . . xx . . . .
Laelius elisae (Russo) L.ec.c.? . x xx . . . . . . .
Plastanoxus westwoodi (Kieffer) L.ec.c.? . . xx . . . . . . .
Sclerodermus brevicornis Kieffer L.ec.c.? . . x . . . . . . .
S. domesticus Latreille L.ec.c. . . . . . xx . . . .

1
Parasitoid guilds: E.en = Egg endoparasitoid; L.ec. = Larval ectoparasitoid; L.ec.c. = Larval ectoparasitoid, cryptoparasitoid; E-L.- en. = Egg-
larval endoparasitoid; A.en. = Adult endoparasitoid; (h) = Essentially hyperparasitoid. See text for more details.
2
Many records from Hylesinus fraxini Panzer, synonym with Leperisinus varius (F.)
3
References: a: Noyes (2001); b: Herting (1973); c: Michalski and Seniczak (1974); d: Hedqvist, 1963; e: Hedqvist, 1998; f: Thomoson,
(1943); g: Mills (1991); h: Hintze-Podufal and Druschke (1988); i: Lozano and Campos (1991); j: Russo (1938); k: Mendel (1986); l: Gonzales
and Campos (1990); m: Markovic and Stojanovic (1996); n: Manohlovic (2000); o: Maksimovic (1979); p: Merlin (1984); q: Schroeder (1974);
r: Mendel (1986); s: Nuorteva (1957); t: Beaver (1967a); u: Eichhorn and Graf (1974); v: Yates (1984)
257
3. PREDATORS
Predators are defined as carnivorous organisms killing several prey during their
development. Since most problems with bark beetles occur in conifers, most
investigations on predators were carried out on conifers, and little information is
available on predators of Scolytidae on broad-leaf trees. In general, predators have a
larger range of prey species than parasitoids. They can be efficient antagonists
because many species are more mobile and active during wintertime than their prey.
Like parasitoids, many predators are known to locate their prey by semiochemicals,
i.e. by bark beetle pheromones or tree volatiles. They are the first to arrive at newly
infested trees - often concomitantly with their prey - while most parasitoids arrive
later (Stephen and Dahlsten, 1976; Ohmartt and Voigt, 1982; Linit and Stephen,
1983). Insect predators do not seem to prefer specific tree parts, but rather colonise
the lower parts of bolts (Wermelinger 2002), in contrast to parasitoids, which often
prefer the upper parts of a tree where the bark is thinner (Ball and Dahlsten 1973;
Stephen and Dahlsten 1976; Gargiullo and Berisford 1981; Wermelinger 2002).
Many insect predators produce only one generation per year (Nicolai 1996).
3.1. The predatory taxa

Many species have been found associated with bark beetle galleries but only a few
are definitely known to forage on living eggs, larvae, pupae, or adults of bark
beetles. Many species may be facultative predators, preying also on other subcortical
taxa, and others may be solely scavengers. Most predatory species belong to the
Coleoptera and Diptera. Some important coleopteran families include Cleridae,
Rhizophagidae, and Trogossitidae (=Ostomidae). Many species of other families are
also associated with bark beetles. Among the Diptera, the Dolichopodidae and
Lonchaeidae are the most relevant families.
Furthermore, predatory bugs in the heteropteran family Anthocoridae suck on
juvenile and adult scolytids. A few species of Raphidiidae (Neuroptera) live in their
larval stage in the brood galleries of bark beetles and feed on scolytid larvae. There
are also mite species that are predatory or parasitic on eggs and larvae of scolytids.
The only relevant vertebrate group foraging on bark beetles is the woodpeckers.
Previous compilations of insect predators were provided by Herting (1973) and
Mills (1983). The present synopsis mainly reviews the literature of the last five
decades including also that on woodpeckers. The most important taxa are discussed
in more detail below while a comprehensive list is given in Table 4.
3.1.1 Coleoptera (beetles)

Beetles are among the most important and most investigated predators of scolytids.
Both their larvae and adults may feed on prey larvae or adults. They usually show
less specificity for prey or tree species than parasitoids. Many predators are attracted
by prey-emitted pheromones, modulated by tree volatiles (Erbilgin and Raffa 2001).
Predacious beetles in conifers often respond to alpha-pinene and ethanol (Schroeder
and Weslien 1994). In addition, they can detect anti-aggregation pheromones such
as verbenone emitted by bark beetles. This is hypothesised to deter predators

specialised on early successional scolytid species and to be indifferent or attractive
to generalist predators (Lindgren and Miller, 2002). Among the most extensively
investigated beetle species are Thanasimus spp. (Cleridae), Rhizophagus spp.
(Rhizophagidae), and Nemosoma elongatum (L.) (Trogossitidae).
Cleridae (checkered beetles). This family includes two genera, among which three
species of Thanasimus Latreille are known to be predators of bark beetles (Table 4).
Among these, T. formicarius (L.) has been the most intensively studied.
Experimental studies showed that it can reduce a brood of Tomicus piniperda by
81% (Schroeder 1997) and a brood of Ips typographus by 18% (Mills 1985).
However, in field exclusion experiments involving Ips typographus japonicus
Niijima, its impact was somewhat mixed with that of intraspecific competition
(Lawson et al. 1997). T. formicarius starts flying early in the season, and forages
throughout the summer, attacking a wide range of prey. In Germany, the females
oviposit from early April to late August (Gauss 1954). This author mentions more
than 20 species of bark-beetle prey in the following genera; Ips, Pityogenes,
Tomicus, Polygraphus, Hylesinus, Hylastes, Scolytus and Dendroctonus. The
predators are attracted to their prey byy their aggregation pheromones (Bakke and
Kvamme 1978, 1981; Köhnle and Vité 1984; Tømmerås 1988). Tømmerås (1985)
observed that predator antennae have receptors keyed to a high number of prey
pheromones [(+)- and (-)-ipsdienol, (S)-cis-verbenol, (-)-ipsenol, (+)-lineatin, (-)-
verbenone, exo-brevicomin, frontalin, etc] and host-tree volatiles [(+)- and (-)- -
pinene, myrcene, terpineol, limonene, -pinene, camphor, pino-camphone, (+)- and
(-)-linalol]. This sometimes resulted in high catches in pheromone traps (up to a 1:4
T. formicarius : Ips typographus ratio according to Bakke and Kvamme 1978).
Responding to the pheromones and host-tree volatiles, the predators land on the
k beetles and oviposit on the bark surface. T.
attacked trees, feed on the attacking bark
formicarius was caught in equal numbers in pine stands attacked the previous year
by Tomicus piniperda and in unattacked stands, suggesting that they are extremely
mobile (Schroeder 1997). Their appearance early in the year and their response to
aggregation pheromones allows them to be one of the first species to colonise bark-
beetle broods (Lawson et al. 1997; Hérard and Mercadier 1996). T. formicarius' high
impact can be explained by its high fecundity (106 eggs/female: Dippel et al. 1997),
and high voracity; one adult consumes 3 adult Ips typographus per day (Gauss
1954), and each larva consumes 44 to 57 prey larvae during its whole larval life
(Mills 1985; Hérard and Mercadier 1996; Dippel et al. 1997). Predator densities
attacking I. typographus were estimated at 1.3 to 11 larvae/1000 cm² (Mills, 1985;
Thalenhorst 1958). Combining these larval prey consumption figures with
associated predator densities, we conclude that the larvae of T. formicarius kill 57 -
627 I. typographus larvae per 1000 cm². For comparison, I. typographus density has
been estimated at 84 – 189 individuals/1000 cm2 by Hougardy and Grégoire (2000)
and 227/1000 cm2 by Gonzalez et al. (1996). Adult T. formicarius live for 4-10
months and the life cycle takes one year (Gauss 1954) or two years in Scandinavia
(Schroeder 1999a). The beetles overwinter either as prepupae or as young adults in

pupal niches within the bark.
Rhizophagidae (root-eating beetles). The family is represented among bark-beetle

associates by the genus Rhizophagus Hrbst. Vogt (1966) lists 14 European species,
most of which live under the bark of conifers or broadleaves. R. depressus (F.) and
R. disparr (Payk.) are associated with Trypodendron lineatum, Pityogenes
chalcographus, Ips typographus, Ips acuminatus, Ips sexdentatus, Dendroctonus
micans, Tomicus piniperda, T. minorr (Kolomiets and Bogdanova 1980) or respond
to the pheromones of these species and/or to ethanol (Byers 1992; Kubisz 1992).
They are probably only partly predacious, although there is documented evidence
for predation. Hanson (1937) observed in the laboratory a single adult R ferrugineus
(Payk.) consuming 79 eggs of Hylastes sp. Hérard and Mercadier (1986) found that
the larvae of R depressus are partly mycetophagous or saprophagous, and partly
predacious on T. piniperda (the larvae consumed 14 prey larvae, the adults 1 prey
larva; all stages were also observed to feed on bark-beetle eggs). A similar
observation was made by Merlin et al. (1986) on Rhizophagus disparr Gyll., which
grew and developed either when reared on fungal cultures or when provided with
living or dead bark beetle larvae. Schroeder (1996) found in an exclusion
experiment that R. depressus reduced T. piniperda broods by 41%.
The biology and feeding habits of Rhizophagus grandis, one of the rare examples
of a specific predator, are much clearer, because of the wide interest in this insect as
a biological control agent against Dendroctonus micans. Except for specificity, the
major features of R. grandis' life cycle are probably similar to those of the other
species. The adults find the prey brood chambers using chemical clues (Wyatt et al.
1993; Tømmerås et al. 1984; Grégoire et al. 1992); this prey location mechanism is
so finely tuned that a high proportion of the prey broods is eventually discovered
(Fielding et al. 1991b; Van averbeke and Grégoire 1995). Oviposition is regulated
both by chemical stimuli and inhibitors (Baisier 1990; Grégoire et al. 1991). Adults
and larvae feed on the eggs, larvae, pupae and callow adults of the prey. The larvae
aggregate on wounded prey but, when food is scarce, they become cannibalistic
(Baisier et al. 1984; Baisier 1990). Merlin et al. (1984) observed that, during its
whole larval life, each individual R. grandis consumes the equivalent of one fully
grown D. micans larva. The prepupae become photopositive, leave the brood
chambers and pupate in the ground or in the bark at the stem base of the trees. There
is at least one generation per year (King et al. 1991).
Trogossitidae (bark-gnawing beetles). Most trogossitids live underneath the bark.

However, there is only one species reported to be predatory on scolytids, i.e.
Nemosoma elongatum. This is a well-known and widespread predator foraging on a
wide range of bark beetles on both conifers and broadleaf trees (cf. Table 4). It is
most often found associated with Pityogenes chalcographus in spruce and
considered to be a very important predator of this bark beetle. The predator's biology
and ecology have been investigated quite extensively (Baier 1991; Wigger 1994;
Dippel 1995, 1996; Dippel et al. 1997). The adults are attracted by kairomonal cues
and boring dust of bark beetles. Its long-term abundance is, with a time lag, closely
related to that of P. chalcographus (Kopf and Funke 1998) while its seasonal
phenology shows much variation (cf. Baier 1991; Wigger 1996). However, in
spring, oviposition of both prey and predator start at the same time. In P.
chalcographus pheromone baited traps N. elongatum can reach up to 20 % of the
total catches (Wigger 1996). Trogossitid predators of bark beetles respond to single
kairomone compounds (Billings and Cameron 1984; Köhnle and Vité 1984).
Staphylinidae (rove beetles). A large number of species have been described

associated with bark beetles, or were caught in bark beetle pheromone traps.
However, they feed on a wide range of prey species and the precise biology is often
unclear. The fact that they can be rearedd on bark beetles in the laboratory does not
mean that they actually forage on bark beetles in the field. Some may also feed on
tree sap (Nuorteva 1956). The most frequent staphylinid predators are Nudobius
lentus (Grav.) and Placusa spp. (Rauhutt et al. 1993). They forage facultatively on
bark beetles and their larvae. N. lentus is frequently found in pheromone traps for
spruce bark beetles.
Histeridae (hister beetles). The histerids most frequently associated with bark
beetles in Europe are Platysoma spp. and Plegaderus spp. They are attracted to
pheromone traps of spruce bark beetles (Rauhutt et al. 1993) as well as to plant
volatiles (Schroeder and Weslien, 1994). The foraging behaviour of Eblisia minor
(Rossi) (= Platysoma frontale Paykull) was studied in more detail (Hérard and
Mercadier 1996). During the three larval stages it consumed an average of 44
scolytid larvae. The adults are also predacious.
Nitidulidae (sap beetles). Various species of Epuraea, Glischrochilus and other

genera are reported to be attracted to scolytid pheromones (Zumr 1983; Rauhutt et al.
1993; Faccoli 2001b) or to plant volatiles (Schroeder and Weslien 1994). Both their
adults and larvae may feed on eggs of bark beetles or other prey (Nuorteva 1956;
Schroeder 1999). Many species are endangered and recorded on red lists.
Tenebrionidae (darkling beetles). Only a few tenebrionids exhibit a predatory

feeding behaviour. Various Corticeus species are facultatively predacious on eggs
and larvae of bark beetles (Nuorteva 1956; Goyer and Smith 1981; Smith and Goyer
1982; Hérard and Mercadier 1996). Corticeus fraxini (Kug.) was reared in the lab
and some life history parameters were investigated (Hérard and Mercadier 1996).
Both its larvae and adults are predacious. They respond to prey pheromones (Rauhut
et al. 1993).
There are a few additional coleopteran families which include bark beetle predators.
Within the Colydiidae, two Aulonium and one Bitoma species have been reported
from European scolytids. Although the Carabidae are a large predatory group, only
Dromius and Calodromius species are frequently found associated with bark beetles.
Various species from other predatory families are attracted by either prey- or host
tree semiochemicals: Salpingus planirostris (F.) (Salpingidae) was found in high
numbers in pheromone traps for spruce bark beetles (Rauhutt et al. 1993). Pytho
depressus (L.) (Pythidae) was strongly attracted by the host tree volatiles alpha-
pinene and ethanol (Schroeder and Weslien 1994). Further coleopteran families with
potential bark beetle predators are Laemophloeidae, Mycetophagidae, and
Silvanidae (see Table 4).
3.1.2 Diptera (flies)

Most predatory Diptera feed on bark beetles in their larval stage. They often
outnumber other subcortically living predatory taxa (Morge 1961). On the other
hand, their prey consumption is usually lower than that of beetles. They do not feed
exclusively on bark beetles but also on larvae of cerambycids, curculionids, other
Diptera and Hymenoptera. The main families are described below. Other dipteran
taxa occasionally associated with bark beetles are found in Table 4.
Dolichopodidae (long legged flies). The most relevant genus is Medetera. The adult
flies are predatory on small insects with a soft integument (Nuorteva 1956; Lieutier
1979; Nicolai 1995a). Mating occurs on the infested trunks and the females deposit
their eggs in bark crevices and under scales of bark beetle infested trees (Hopping
1947). Medetera dendrobaena Kowarz produces up to 120 eggs per female (Dippel
et al. 1997). This species is mono- to bivoltine. The arrival of dolichopodids on
infested logs occurs shortly after colonisation by bark beetles but their presence and
oviposition extends through the summer (Stephen and Dahlsten 1976; Lieutier 1979;
Nicolai 1995c).
Most species are known to prey on scolytid larvae, pupae, and teneral adults.
They overwinter in the larval stage and emerge simultaneously with the bark beetles
(Beaver 1966c; Lieutier 1979). Winter mortality in the maggots can be substantial
(Hopping 1947; Nuorteva 1959; Beaver 1966c). Medetera has been found to be
associated with many bark beetle species in different tree species (cf. Table 1; Capek
1957; Nuorteva 1959; Ounap 1992b). The genus is not necessarily restricted to
scolytid diets but also feeds on other taxa. The prey consumption of M. dendrobaena
showed a functional response, i.e. prey consumption increased with increasing bark
beetle density (Nicolai 1995b). When prey is abundant, dolichopodids kill more prey
than necessary (Beaver 1966c). With low prey supply they can act cannibalistically.
The impact of dolichopodid flies on scolytid survival is discussed controversially
in the literature. Bark beetle mortality imposed by Medetera species was assessed to
be minor (Mills 1986) and to be independent of Medetera densities (Mills 1985). At
low densities the access of dolichopodid larvae to bark beetle larvae may be
restricted by intact pieces of phloem (Nagel and Fitzgerald, 1975). However, they
can reach densities of up to 10 larvae per 100 cm2 (Dippel et al. 1997) and cause
mortality rates of 70-90 % (Hopping 1947; Nuorteva 1959).
Lonchaeidae (lance flies). Among the Lonchaeidae, only the genus Lonchaea lives
subcortically (Morge 1963). The feeding behaviour of these species is
controversially discussed in the literature. They are often considered to be
saprophagous or coprophagous (Lieutier 1979). Most species of this genus,
however, have developed from saprophagous to predatory behaviour. Morge (1961,
1963) and Hérard and Mercadier (1996) investigated extensively the predatory
behaviour of these species. They are specialised in colonising certain species and
conditions of trees rather than in preying on specific species of bark beetles. More
species live in broadleaves than in conifers. Lonchaea species occur in smaller
numbers and feed on detritus rather than on living bark beetle larvae (Morge 1961).
In conifers, however, some species are known to be obligatory predators, occurring
in high numbers. They can feed on eggs, larvae, and adults as well (Morge 1967).
Like the Dolichopodidae, they are very voracious, killing more prey individuals than
they can eat. When prey individuals are rare, cannibalism occurs. (Hérard and
Mercadier 1996).
Pallopteridae (pictured-wing flies). Toxoneura usta (Meigen) is known to forage on

scolytid larvae (Morge 1967; Martinek 1977; Chandler 1991). It is able to feed on
eggs, larvae, pupae, and even adult bark beetles, killing many more prey than it can
actually eat (Morge 1967). It is not specialised on any particular tree or prey.
Asilidae (robber flies). Asilid flies are not specialised predators of bark beetles.
However, scolytids may be among their prey (Wichmann 1956; Dennis 1979). The
adult flies insert their stylet before or behind the pronotum or between the elytra,
inject paralysing saliva into the body and suck up the liquefied contents. Their larvae
are predacious on other subcortical insect larvae (Wichmann 1956).
3.1.3 Other insect groups

Among the Heteroptera, the predatory behaviour of Scoloposcelis species and
Xylocoris cursitans (Fallén) (Anthocoridae) has been studied in some detail
(Heidger 1994; Hérard and Mercadier 1996; Dippel et al. 1997). Both larvae and
adults are very voracious, killing more prey than they can consume (Hérard and
Mercadier 1996). Scoloposcelis pulchella can produce two generations per year.
They respond to the same lures as their prey (Heidger 1994).
The larvae of some Raphidioptera prey on or underneath the bark. A few species
of Raphidiidae are known to forage non-specifically on cerambycids, bark beetles
and other subcortically living organisms (Schimitschek 1931; Wichmann 1957).
They may be able to access scolytid galleries only after the bark is loosened, e.g. by
maturation feeding of bark beetles or by woodpeckers (Wichmann 1957). For further
predatory insects see Table 4.
3.1.4 Acari (mites)

Mites can be associated with bark beetles in two ways. The first group feeds on
substrates other than living bark beetles, e.g. fungi or nematodes. Therefore, some of
these may even be beneficial to bark beetles (Hirschmann and Wisniewski 1983).
These mites depend in a phoretic way on bark beetles, i.e. in a given stage they
attach themselves to the emerging bark beetles and use them as transport vehicles to
reach new habitats. The second group is parasitic or predacious on various scolytid
stages. Adult females and deutonymphs may be phoretic as well.
In general, the ecology of acarine species associated with bark beetles is poorly
understood. It may range from mutualistic to parasitic behaviour with all possible
combinations of the two. Many mites are parasites rather than predators. A large
number of mite species has been found associated with European bark beetles
(Hirschmann 1971; Hirschmann and Wisniewski 1983; Kielczewski et al. 1983;
Moser and Bogenschütz 1984; Moserr et al. 1989), but only a few are known to
actually feed on scolytids. In a study on Ips typographus, some 30 % of trapped
beetles carried an average of 3 phoretic mites (Moser and Bogenschütz 1984).
Common acarine predators such as Iponemus spp. and Paracarophenax spp. are
known to be specialised on bark beetle eggs, whereas Pyemotes spp. and
Digamasellus spp. feed on larvae and pupae. Some adults are commensals while
their larvae feed on eggs (Hintze-Podufal and Druschke 1988). Adult bark beetles
are not attacked (Moser 1975). The mites are transported to new habitats by adult
beetles beneath their elytra or attached to the thorax or elytral declivity. Egg
parasites seem to be more host specific than larval parasites (Lindquist 1969). Many
species are specific in terms of habitats rather than in terms of hosts (Lindquist
1970). The impact of mites on bark beetle population dynamics is largely
unexplored but often considered substantial. Mortality by Pyemotes spp. and
Iponemus spp. reached up to 90 % (Gäbler 1947; Lipa and Chmielewski 1977;
Kielczewski et al. 1983; Moserr et al. 1989).
3.1.5 Aves (birds)

Among birds, the woodpeckers (Picidae) are the most important predators on
scolytids. Most quantitative studies have been made in America, mainly in
Dendroctonus spp. infestations. In Europe species like the black (Dryocopus martius
L.), the great spotted (Dendrocopos majorr (L.)), and the three-toed woodpecker
(Picoides tridactylus (Hemp. and Ehr)) are commonly observed foraging on bark
beetles on conifers (Schimitschek 1931; Nuorteva 1956; Pechacek 1994) and on
broadleaves (Yates 1984). In general, they seem to prefer larger prey species than
scolytid larvae or beetles (Nuorteva and Saari 1980). In an American study, 89 % of
Table 4. List of European predatory species, their host trees, and their bark beetle preys.
Observation type represents character of information: f= observed feeding on respective prey
or prey found in faeces, a= associated in galleries or on bodies of respective prey, s= attracted
to semiochemicals (pheromones or allelochemicals). Killing rate denotes prey consumption or
killing by the respective predator (A= adult, L= larva), an asterisk indicates unclear feeding
behaviour. For a summary of further older data see Herting & Simmonds (1973) and Mills
(1983). Coleopteran taxonomy follows basically Freude et al. (1965-1998)
Table 4
Host
Predator
Dendroctonus micans
Hylurgops palliatus
Ips acuminatus
Ips cembrae
Ips typographus
Orthotomicus erosus
Polygraphus poligraphus
Taphrorychus bicolor
Ips sexdentatus
Pityogenes calcaratus
Scolytus intricatu
Other species
Scolytus spp.
Tomicus spp.
Trypodendron lineatum
tree Killing rate References1
Observation type
COLEOPTERA
Carabidae
Calodromius spilotus (Ill.) Pn . . . . x . . . . . . . . x . . a 22
(=Dromius quadrinotatus)
Dromius quadrimaculatus (L.) Pn . . . . x . . . . . . . . x . . a 22
Carabidae spp.* Pn . . . . . . . . . . . . . x . . a 36
Cleridae
Allonyx quadrimaculatus (Sch.) Pn . . . . . . . . . . . . . x . . a 22

Thanasimus femoralis (Zett.) . . . . . x . . . . . . . . . . s 77
T. formicarius (L.) Pc,Fr x . x . x x . . x . . x . x . x a,f,s 44-57 larvae/L 11,15,18, 21,22,23,
2.9 adults/A/day 45, 46, 63, 67,68,70,
74-109 adults/A 72,76
T. rufipes (Brahm) Pc . . . . . x . . x . . . . . x . a,s 63, 76
Colydiidae
Aulonium ruficorne (Ol.) Pn . . x . x . x x . . . . . . . x a,f,s 22, 40, 41

A. trisulcum (Fourcr.) Ul . . . . . . . . . . . x . . . . a 1
Bitoma crenata (F.) Pn . . x . x . . . . . . . . x . . a 22
Histeridae
Eblisia minorr (Rossi) (=Platysoma Pn . . x . x . . . . . . . . x . . a,f 44 larvae/L 22
frontale) 1.5 larvae/A/day
265
Paromalus parallelepipedus (Hbst) Pn . . . . . . . . . . . . . x . . a,s 36, 37, 38, 63

Table 4 (cont.)
266
Predator Host Obs
Spp
I. typ.
T. bic.
T. lin.
I. cem.
I. sex.
T. spp.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
tree tye Killing rate References1
Platysoma angustatum (Thunb.)* Pn,Pc . . x . x x x x x . . . x x . a,s 22,36,40,42,63
(=Cylister ferrugineum)
P. elongatum (Thunb.)* Pn .. . . . . . x x . . . . . . . . a 22, 42
P. lineare (Er.)* Pn,Pc . . . . . x . . x . . . . x x . a,s 63, 67
Plegaderus discisus Er. Pn .. . . . . . x x . . . . . . . . s 40, 42
Plegaderus vulneratus (Panz.) Pn,Pc .. x . . . x . . . . . . . x x a,f,s 18,37,55,63, 67,7
78
Laemophloeidae
Cryptolestes fractipennis Motsc Pn .. . . . . . . . . . . . . x . . a 22
C. spartii (Curt.) Pn .. . . . . . x x . . . . . x . . a 42
Placonotus (Laemophloeus) Fa x . . . . . . . . . . . x . . . a 20
testaceus (F.) .
Mycetophagidae
Litargus connexus (Fourcr.) Pn .. . x . x . . . . . . . . x . . a 22
Nitidulidae .
Epuraea angustula Sturm Pc .. x . . . . . . . . . . . . . x a 55
E. laeviuscula (Gyll.)* Pc . . . . . . . . . . . . . . x . a 55
= pusilla (Ill.))
E. marseuli Rtt. (=E. Pn . x x . x x . . x . . . . x x . a,f,s 23 eggs/L/day 22,36,55,67,68,77
E. pygmaea (Gyll.) Pc . . . . . x . . . . . . . . . x a,f,s 9 eggs/L/day 55,77,78
E. rufomarginata (Steph.) Pn . . x . x x . . . . . . . x . . a,s 22,87
E. silacea (Hbst.) Pn . . x . x . . . . . . . . x . . a 22
E. thoracica Tourn.* Pc,Pn . x x . . x . . . . . . . x . . a 55,78
E. unicolorr (Ol.) Fa . . . . . . . . . . . . x . . . a 20
Epuraea spp.* Pn,Pc . x . . . x . . x . . . . x x . a,f,s 18,55,63,67,70,78
87
Glischrochilus quadripunctatus (L.)* Pn,La,Pc .. . . x . . . . . . . . . x . . a,f,s 18,36,55,64,67
(=quadripustulatus (L.))
Table 4 (cont.)
Predator Host Obst
Spp
I. typ.
T. bic.
T. spp.
T. lin.
I. cem.
I. sex.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
tree ye Killing rate References1
G. hortensis (Fourcr.)* Pc . . . . . x . . x . . . . . x . s 63
Ipidia binotata (Rtt.) Pn . . . . . . . . . . . . . x . . a 22
(= Quadrimaculata Quensel)
Pityophagus ferrugineus (L.) Pn,Fa . . . . . x . . . . . . x x . . a,s 36,53,67,77
Pythidae
Pytho depressus (L.) Pn . . . . . . . . . . . . . x . . s 67
Rhizophagidae (=Monotomidae)
Rhizophagus bipustulatus F. Pc,Pn,Fr . . . . . x x x . . . . . x . x a,s 23,29,36,40,42
R. cribratus Gyll. Pc,Pn . x . . x x . . . . . . . . . x a 27
R. depressus (F.) Pn,Pc x x x . x x . . x . . . . x x . a,f,s 14 larvae/L 18,22,27,29,38,55
1 larva/A/day 63,67,68,87
16 eggs/A/day
R. disparr (Payk.) Pn,Pc x x x . x x . . . . . . . x x . a,f,s 15 eggs/L/day 18,27,29,36,44,55
63,76,78
R. ferrugineus (Payk.) Pn,Pc . x x . x x . . . . . . . x . x a,s 79 eggs/A 7,19,22,55,67,77,
87
R. grandis Gyll. Pc,Pn x . . . . . . . . . . . . . . . a,f,s 1 larva/L 6,13,14,16,17,25,
26,27,43,73,74,84
R. nitidulus (F.) Pn . . . . . . . . . . . . . x x x a,s 29,36,63,64
R parvulus Payk. Pc . x . . . . . . . . . . . . . . s 29
R. perforatus Er. Fr,Ul . . . . . . . . . . . x . . . x s 29

R. puncticollis Sahlb. Pc . . . . . . . . . . . . . . . x s 27
Salpingidae
Rabocerus foveolatus (Liungh) Pc . . . . . x . . . . . . . . . . a 76
R. gabrieli (Gerh.) Pc . . . . . x . . . . . . . . . . a 76
Salpingus (Rhinosimus) planirostris F. Pc . . . . . x . . x . . . . . x . s 63
S. (Rhinosimus) ruficollis (L) Pc . . . . . x . . x . . . . . x . s 63
267
Table 4 (cont.)
268
Predator Host Obst
T. lin.
Spp
I. typ.
T. bic.
T. spp.
I. cem.
I. sex.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
Sphaeriestes (Salpingus) castaneus Panz Pc . . . . . x . . x . . . . x . s 63
Silvanidae
Silvanus bidentatus (F.) Pn . . x . x . . . . . . . . x . . a 22
S. unidentatus (F.) Pn . . x . x . . . . . . . . x . . a 22
Staphylinidae
Aleochara sparsa Heer Pc . . . . . x . . x . . . . . x . s 63
Metoponcus brevicornis (Er.) Ab . . . . . . . . . . . . . . . x s 8
Nudobius lentus (Grav.) Pn,La,Pc . x . x . x . . x x . . . x . x a,f,s 18,36,55,58,63,64
70,78,87
Phloeonomus spp.* Pn,Pc . x . . . x . . . . . . . x . . a 38,55,78
Phloeopora testacea (Mannh.) Pc,Pn . x . . . x . . . . . . . x . . a 55,70
Phloeostiba lapponicus (Zett.)* Pc . x . . . . . . . . . . . . . . a 55
Placusa adscita Er. Pn . . x . x . . . . . . . . x . . a 22
P. atrata (Mannh.) Pc,Be . x . . . . . . . . . x . . . x a,f 55
P. depressa Maekl. Pc . x . . . x . . x . . . . x x x a,s 2 eggs/L/day 18,38,55,63
P. tachyporoides (Waltl.) . . . . . x . . . . . . . . . . s 87
Quedius laevigatus Gyll. Pc . x . . . x . . . . . . . . . . a,s 7 larvae/A/day 55,87
Q. plagiatus Mannh. Pc . . . . . x . . . . . . . . . . s 78
Staphylinidae spp.* Pn,Pc, La . . . . . x . . x . . . . x x . a,s 36,38,55,63,64,77
78
Tenebrionidae
Corticeus fraxini Kug Pn . . x . x . . . . . . . . x . . a,f 93 larvae/L 22
1 larva/A/day
C. (Hypophloeus) linearis F.* . . x . x x . . x . . . . . x . a,s 18,22,63
C. longulus Gyll.* Pn . . . . . . . . . . . . . x . . 62
C. pini Panz.* Pn . . . . . . x x . . . . . . . . a 42
C. suberis (Luc.)* (= rufulus Ros.) Pn . . . . . . x x . . . . . . . . a 42
Table 4 (cont.)
Predator Host Obst
Spp
I. typ.
T. bic.
T. spp.
T. lin.
I. cem.
I. sex.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
C. unicolor* (Pill. Mitt.) Pn . . . . . . x x . . . . . . . . a 42
Trogossitidae
Nemosoma elongatum (L.) Pc,Al, . . . . . x . . x . . . x . . x a,f,s 1-2 beetles/A/day 2,3,10,11,20,28
Pn,Fa 30-45 42,63,69,70,75,81
larvae+pupae+ 82,87
teneral beetles/L
DERMAPTERA
Forficulidae
Forficula auricularia L. . . . x . . . . . . . . . . . . f 64
DIPTERA
Asilidae
Laphria flava (L.) Pc . . . . . x . . . . . . . . . . f 79
Choerades (Laphria) gilva (L.) Pc . . . . . x . . . . . . . . . . f 7 beetles/A/day 79
Tolmerus (Machimus) atricapillus Pc . . . . . x . . . . . . . . . . f 79
(Fallén)
Dolichopodidae
Dolichopus sp. Qu . . . . . . . . . . x . . . . . a 85
Medetera ambigua (Zett.) Pc,Pn . . . . x x . . . . . . . . . . a 32
M. adjaniae (Goss.)(=breviseta Par.) Pc . x . . . x . . x . . . . . . x a 46,56,76,78
M. dendrobaena Kowarz Pc,Fa . . . . . x . . x . . . x . x . a,s 0.5-10 larvae/L/day 11,52,53,54
M. dichrocera Kowarz Pc,Pn . x . . . x . . x . . . . x . . a,f 55,56

M. excellens Frey La,Pc . . . x . x . . . . . . . . . . a,f 64,76,78
M. impigra Collin Ul,La,Fa . . . . . . . . . . . x x . . . a,f 4-7 larvae/L 4,20
M. infumata Loew Pn,Pc . . . . . x . . . . . . . x . . a,s 55,77
M. melancholica Lundb.* Al,Pn . . . . . . . . . . . . . . . x a 55
M. nitida (Macqu.) Ul . . . . . . . . . . . x . . . x a,f 7-11 larvae/L 4,66
M. obscura Zett.* Pn . x . . . . . . . . . . . x . . a 55
269
Table 4 (cont.)
270
Predator Host Obst
Spp
I. typ.
T. bic.
T. spp.
T. lin.
I. cem.
I. sex.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
M. pinicola Kow. (=nuortevai Thun) Pn,Pc . x . . . x . . . . . . . x . . a 55,56,76
M. setiventris Thun. Pc,Pn . x . . . . . . x . . . . . . x a 55
M. signaticornis Loew Pc,Pn . . . . x x . . . . . . . . . . a 18,32,55,59,70,72
76,77,78
M. striata Parent Pn . . . . . . x x . . . . . . . . a 42,55
M. thunebergi Negrob. Pc,Pn . . . . x x . . . . . . . . . . a 32
M. vagans Beck.* (=fennica Thun.) Pc . . . . . x . . . . . . . . . x a 55
Medetera spp. Pc,Pn,Ab . x . . . x x x x x x . x . . x a,f 7-20 3,20,22,40,54,55
Qu,Fa larvae+pupae/L 56,58,65,78,85,86
1 larva/L/day
Empididae
Drapetis sp. Pn . . x . x . . . . . . . . x . . a 22
Lonchaeidae
L. bruggeri Morge Con . . . . . x . . . . . . . . . . a 48,76,78
L. collini Hackman Con . . x . x . . . . . . . . x . . a,f 1 larva/L/day 22,48
L. fugax Becker Pc . . . . . x . . . . . . . . . . a 70
L. helvetica MacGowan Pc . . . . . x . . . . . . . . . . a 76
L. laticornis Meigen* Ab . . . . . . . . . . . . . . . x a 8
L. scutellaris Rondani Pc . . . . . x . . . . . . . . . . a 48,76
L. seitneri Hendel Con . . . . . . . . . . . . . . . . a 48
L. zetterstedti Becker* Pc,Pn . . . . x x . . . . . . . . . . a 32,48,76

Milichiidae
Madiza glabra Fallén* La . . . x . . . . . . . . . . . . a 64
Muscidae
Phaonia gobertii (Mik)* Pn,La . . . x . x . . . . . . . . . . a 32,64
Phaonia sp. Pn . . . . x x . . x x . . . x . . a,f 22,58
Pallopteridae
Predator
Palloptera ustulata Fallén . . . . . x . . . . . . . . . . 34
Toxoneura (Palloptera) usta (Meig.) Con . . . . . . . . . . . . . . . . a,s 9,49,70,76
Stratiomyidae
Zabrachia minutissima (Zett.)* . . . . . x . . . . . . . . . . a,s 77
Z. tenella (Jaenn.)* . . . . . . . . . . . . . . . a 35
HETEROPTERA
Anthocoridae
Lyctocoris campestris (F.) Pn . . . . . . . . . . . . . x . . a 22
Scoloposcelis obscurella (Zett.) Pn . . x . x . . . . . . . . x . . a 4.7 larvae/L/day 22
25 larvae/A/day
S. pulchella (Zett.) Pn,Pc . x x . x x x x x x . . . x . . a,f 39-144 larvae/L 11,21,22,40,42,58
Xylocoris cursitans (Fallén) Pn . . x . x . . . . . . . . x . . a,f 44 larvae/L 22
4 larvae/A/day
HYMENOPTERA
Formicidae
Formicidae spp. . . . . . . x . . . . . . . . x f 39,83
NEUROPTERA
Chrysopidae
Chrysoperla carnea (Steph.) Pc . . . . . x . . . . . . . . . . a 76
ODONATA
Anisoptera spp Pn . . x . . . . . x x . . . x x x f 30
RAPHIDIOPTERA
Raphidiidae
Dichrostigma (Raphidia) flavipes Pc . . . x . x . . . . . . . . . . a 64,80
(Stein)
Phaeostigma (Raphidia) notata (F.) Pc . . . x . x . . . . . . . . . . a 64,80
Phaeostigma sp. Pn . . . . x . . . . . . . . x . . a 22
271
Table 4 (cont.)
272
Predator Host Obst
Spp
I. typ.
T. bic.
T. spp.
T. lin.
I. cem.
I. sex.
D. mic.
H. pal.
I. acu.
O. ero.
P. cal.
P. cha.
P. pol.
S. int.
S. spp.
Puncha ratzeburgi (Brau.) Pc . . . . . x . . . . . . . . . . a 76
ACARI
Acarophenacidae
Paracarophenax ipidarius (Redik.)* . . . x . x . . . . . . . . . x a 24,50,51
Ascidae
Lasioseius ometes Oud. . . . . . . . . . . . . . . x . a 71
Proctolaelaps fiseri (Vitzt.) . . . . . . . . . . . . . . x . a 71
P. pini Hirsch. . . . . . . . . . . . . . . x . a 71
P. xyloteri Sams. . . . . . . . . . . . . . . x . a 71
Digamasellidae
Dendrolaelaps apophyseosimilis . . . . . . . . . . . . . . x . a 71
Hirsch
Dendrolaelaps spp. . . . . . . . . . . . . . . x . a 71
Pyemotidae
Pyemotes dryas (Vitzt.) . . . . . x . . x x . . . . . . a 24,50,51
P. herfsi (Oud.) . . . . . . . . . . . x . x . . a 24
P. scolyti (Oud.) Ul . . . . . . . . . . . x . . . . a,f 5,12,24,33
Tarsonemidae
Iponemus gaebleri (Schaar.) . . . . x x . . . . . . . . . x a 24,31,50,51
Uropodidae
Trichouropoda bipilis (Vitzt.) Fr . . . . . . . . . . . . . . . x a 23

ARANEAE
Erigonidae
Troxochrus nasutus Schenkel . x . . . . . . x . . . . . . . a 47
AVES
Fringillidae
Fringilla coelebs L. . . . . . x . . . . . . . . . . f 72
Table 4 (cont.)
Predator Host Obst
Spp
I. typ.
T. bic.
I. cem.
I. sex.
T. spp.
T. lin.
D. mic.
H. pal.
I. acu.
O. ero.
S. spp.
P. cal.
P. cha.
P. pol.
S. int.
Picidae
Dendrocopos majorr (L.) La,Qu . . . x . . . . . . x . . . . . f 64,60
Dryocopus martius L. La . . . x . . . . . . . . . . . . f 64
Picoides syriacus (Hemp. & Ehr.) Pn,Ol,Pr . . . . . . x x . . . x . x . . f 39
Cu,Ul
P. tridactylus (L.) Con . . . . . x . . . . . . . . . x f 1200 adults/day 57,61
(estimate)
Picoides sp. Qu . . . . . . . . . . x . . . . . 85
1
References: 1 Allen (1975); 2 Baier (1991); 3 Baier (1994); 4 Beaver (1966); 5 Beaver (1967); 6 Bergmiller (1903); 7 Byers (1992); 8 Capek (1957); 9 Chandler (1991); 10
Dippel (1996); 11 Dippel et al. (1997); 12 Doberski (1980); 13 Fielding and Evans (1997); 14 Fielding et al. (1991b); 15 Gauss (1954); 16 Grégoire et al. (1991); 17 Grégoire et
al. (1992b); 18 Grodzki (1997); 19 Hanson (1937); 20 Harz and Topp (1999); 21 Heidger (1994); 22 Herard and Mercadier (1996); 23 Hintze-Podufal and Druschke (1988); 24
Kielczewski et al. (1983); 25 King et al. (1991); 26 Kobakhidze (1965); 27 Kolomiets and Bogdanovaa (1980); 28 Kopf and Funke (1998); 29 Kubisz (1992); 30 Labedzki
(1989); 31 Levieux et al. (1989); 32 Lieutier (1979); 33 Lipa and Chmielewski (1977); 34 Martinek (1977); 35 Matile (1993); 36 Mazur (1973); 37 Mazur (1975); 38 Mazur
(1979); 39 Mendel (1985); 40 Mendel (1988); 41 Mendel et al. (1989); 42 Mendel et al. (1990); 43 Merlin et al. (1984); 44 Merlin et al. (1986); 45 Mills (1985); 46 Mills
(1986); 47 Moor and Nyffeler (1983); 48 Morge (1963); 49 Morge (1967); 50 Moser and Bogenschütz (1984); 51 Moser et al. (1989); 52 Nicolai (1995c); 53 Nicolai (1996); 54
Nicolai et al. (1992); 55 Nuorteva (1956); 56 Nuorteva (1959); 57 Otvos and Stark (1985); 58 Ounap (1992a); 59 Ounap (1992b); 60 Pavlik (1999); 61 Pechacek (1994); 62
Pishchik (1980); 63 Rauhut et al. (1993); 64 Schimitschek (1931); 65 Schopf and Köhler (1995); 66 Schröder (1974); 67 Schroeder and Weslien (1994); 68 Schroederr (1996);
69 Schumacher and Pohris (2000); 70 Seitner (1924); 71 Strube and Benner (1984); 72 Thalenhorst (1958); 73 Tømmerås et al. (1984); 74 Wainhouse et al. (1992); 75
Wegensteiner and Führer (1991); 76 Wermelinger (2002); 77 Weslien and Schroeder (1999); 78 Weslien (1992); 79 Wichmann (1956); 80 Wichmann (1957); 81 Wigger (1993);
82 Wigger (1996); 83 Wilkinson et al. (1978); 84 Wyatt et al. (1993); 85 Yates (1984); 86 Zinovjev (1957) [in Morge (1961)]; 87 Zumr (1983°;
2
Host trees: Ab: Abies; Al: Alnus; Be: Betulus; Con: Conifers; Cu: Cupressus; Fa: Fagus; Fr: Fraxinus; La: Larix;
i Ol: Olea; Pc: Picea; Pn: Pinus; Pr: Prunus; Qu:
Quercus;Ul: Ulmus
273
the prey in the gizzard of three-toed woodpeckers were larvae of buprestid beetles
(Otvos and Stark 1985) while in a German study, the faeces of the same species
consisted of 89 % of I. typographus (Pechacek 1994). When foraging on bark beetle
broods, woodpeckers prefer the later and larger instars (Kroll and Fleet 1979). At the
same time, they also devour predatory and parasitic insects living underneath the
bark.
Indirect effects of woodpecker activity by puncturing, loosening and removing
bark can cause more bark beetle mortality (due to desiccation, other predation,
diseases) than direct woodpecker foraging (Moore 1972; Otvos 1979). They can
debark large proportions of infested trunks
r (Hintze-Podufal and Druschke 1988).
Only a fraction of the brood in bark flakes dropping to the ground survives to
emergence (Kroll and Fleet 1979). Mortality imposed by woodpeckers may vary
significantly among single trees, ranging from 5 to 70 % (Shook and Baldwin 1970;
Moore 1972; Massey and Wygant 1973; Berryman 1976; Amman 1984; Pavlik
1999). They are most significant in endemic situations, in local outbreaks, or during
the decline of an outbreak (Otvos 1979). Woodpecker impact is highest in the upper
tree parts where bark beetle densities are highest, during winter and spring (Moore
1972). Woodpecker populations are positively influenced by bark beetle outbreaks.
4. QUANTITATIVE ASSESSMENT OF PARASITOIDS AND PREDATORS

AND THEIR ROLES IN THE POPULATION DYNAMICS OF SCOLYTIDAE.
It is difficult to quantify the effects of predators on bark beetles. The consumption of
prey in the field is hard to measure, and predators may not only forage on the target
bark beetle, but also on other subcortical insects, including predators and parasitoids
(Mendel et al. 1990) and therefore reduce the overall detrimental effect on a bark
beetle population. For example, Thanasimus formicarius is an important mortality
factor for Medetera larvae (Nuorteva 1959).
In contrast, most studies on parasitoids of Scolytidae have provided some
quantitative evaluations of parasitism, either as parasitism rates, or as relative
abundance of parasitoid species. Parasitism rates varying from 0 to 100% have been
found. However, parasitism rates and consumption rates are poor indicators of the
real impact of natural enemies on bark beetle populations. Several authors state that
natural enemies do not play an important role in regulating bark beetle populations
(e.g. Sachtleben 1952; Bombosch 1954; Faccoli 2001a) whereas a few others affirm
the contrary (e.g. Mendel 1987), but few of these statements are based on solid data.
To better evaluate the impact of parasitoids and predators on bark beetle
populations, various methods have been used, such as consumption rate based
assessments (e.g. Dippel et al. 1997; Wermelinger 2002), life table analyses, and
natural enemy exclusion experiments. Life tables are not easy to construct for bark
beetles because of the problem of overlapping
a generations. On the other hand, their
cryptic biology may facilitate population studies because the cause of death and the
stage at which it occurs can usually be assessed through regular bark examination.
Furthermore, the effect off population densities on mortality y factors can be assessed
easily because sample logs can be considered as separate populations, with different
beetle densities. In his study on Scolytus scolytus in the UK, Beaver (1966b, 1967b)
was among the first to use a life table (or, better, population table) approach to
assess the various mortality factors on bark beetles and their role in population
regulation. He stated that populations are likely to be regulated by different
mechanisms at different population densities. Among the main mortality factors
were subcortical predators (mainly Medetera spp.) and larval ectoparasitoids
(mainly Coeloides scolyticida Wesmael). Predators showed a density-dependent
response at low beetle densities, but became inversely density-dependent at higher
densities. In contrast, the ectoparasitoids showed a density-dependent response only
above a certain host density. This suggests that subcortical predators have regulatory
power at low beetle densities whereas ectoparasitoids compensate at high densities,
together with other factors such as intraspecific competition. The roles of
woodpeckers and the egg-larval endoparasitoid Entedon ergias were less clear.
Similar studies on Leperisinus varius (Lozano et al. 1993, 1994) and Phloeotribus
scarabaeoides (Lozano et al. 1996a, 1996b) showed that populations were regulated
by density-dependent larval mortality, due to larval competition and ectoparasitism.
However, in both bark beetles, larval parasitism alone tended to show an inversely
density-dependent response. Other similar studies
t were made in North America. In a
time-series analysis of populations and antagonists of the North American bark
beetle Dendroctonus frontalis Zimmermann, delayed density dependency was
shown (Turchin et al. 1999), suggesting that antagonists are more important during
the decline phase of an outbreak than at the beginning. This is supported by another
study on Dendroctonus ponderosae Hopk. that assigned predators (except clerids)
and parasitoids a more significant role in epidemics than in endemic situations
(Amman 1984). In a two-year study during an Ips typographus infestation in
Switzerland, Wermelinger (2002) observed that predators were more abundant in the
first year, at the peak of bark beetle density, whereas parasitoids dominated in the
second year, when overall beetle mortality increased and populations collapsed.
Mills (1986) and Mills and Schlup (1989) produced basic partial life tables of I.
typographus in Switzerland and Germany. They suggested that clerid predators
Thanasimus spp. and larval ectoparasitoids had a significant influence on brood
survival. They showed that parasitism may vary with tree height (e.g. parasitism by
braconids being much higher at the top of the tree), although the relation between
parasitism and bark thickness was unclear. Wermelinger (2002) also found higher
parasitism on I. typographus at the top of the tree than at the bottom.
Natural enemy exclusion experiments provide an elegant method to better assess
the impact of natural enemies on bark beetle populations, but have rarely been
carried out in Europe. Notable exceptions are the works by Weslien (1992) and
Schroeder and Weslien (1994) who, in Sweden, observed a reduction of I.
typographus and Tomicus piniperda populations of 83-89% compared to caged
populations where parasitoids and predators were excluded. Related studies in
North America also showed that parasitoids and predators can reduce bark beetle
populations to a similar extent (e.g. Linit and Stephen 1983; Riley and Goyer 1986).
5. UTILISATION OF PARASITOIDS AND PREDATORS IN BIOLOGICAL

CONTROL PROGRAMMES
Although the justification of most studies on parasitoids was their potential use in
biological control strategies against scolytids, only few biological control
programmes have been implemented. The most important has been the biological
control of Dendroctonus micans in Georgia, Turkey, UK and France.
D. micans, originally a Siberian species, has been increasing its range
continuously during the 20th century, and most of the time it was closely followed by
Rhizophagus grandis. The impact of this predator was observed very early in
Germany, after the establishment of both species (Bergmiller 1903). The first
biocontrol programme involving R. grandis was developed in the Georgian SSR,
after Dendroctonus micans invaded the region during the 1950s (Kobakhidze 1965).
A small number of adult and larval predators was imported from Czechoslovakia,
released in 1963 and established successfully in the local D. micans infestations. By
1970, 54,000 predators had been released (Tvaradze 1976), and by 1976 a series of
rearing units was established, producing insects on logs infested with D. micans.
From Georgia, D. micans progressed into Turkey, where a biocontrol programme
has also been implemented.
In 1983, as D. micans was progressing through the French Massif Central, a
Belgian-French programme was developed (Grégoire et al. 1985). Semi-artificial
rearing methods using an artificial diet and oviposition stimulants were established
and, in the period 1983-1991, 659 sites (12,275 ha; public as well as private forest)
had been treated, usually with rather large releases (500-1000 pairs/site). The sites
situated at the borders of the infested area were treated first, to take advantage of the
lower pest density there, and to try limiting the spread of the pest. During 1983-99, a
total of 530.000 insects were produced and released. Predator establishment and
impact were closely followed in a series of permanent plots and in more temporary
surveys. The predator releases were always followed by establishment and, within 6-
8 years, by the collapse of the bark-beetle populations (see e.g. Van averbeke and
Grégoire 1995). At present, D. micans is still expanding (Aveyron, Orne), justifying
the need for further releases. A potential development is the monitoring of pest and
predator movements using kairomone traps that attract R. grandis (Grégoire et al.
1992).
Also in 1983, following the discovery of D. micans in the north-west of England
and in Wales (Bevan and King 1983), a rearing and release programme started in the
UK (Fielding et al. 1991; Evans and Fielding 1994; Fielding and Evans 1997).
Combined with internal quarantine procedures and the deployment of a pest-free
zone around the infested area, predators were released in all sites. In order to cover
as many sites as possible, release rates were adjusted to 10-50 pairs/site (average: 57
individuals/site). Between 1984 and 1995, 156,400 insects were released in 2,741
sites (public and private forest). Establishment of R. grandis and subsequent control
of D. micans was observed at the same rates as elsewhere. As D. micans is still
expanding, the biocontrol programme is continuing.
Finally, R. grandis is also being used in a neo-classical biological control
programme against a close relative of D. micans, D. valens, a north-American
species which invaded China in the late 1990's. Following promising laboratory
results (Miller et al. 1987), R. grandis is presently being mass-reared in China for
releases in the Shanxi Province (Yang Zhong-qi, pers. comm.).
The programme against D. micans was the only classical biological control (i.e.
the introduction and establishment of exotic natural enemies to control a pest), that
has ever been carried out against scolytids in Europe, mainly because few exotic
scolytids have invaded Europe, and these are, presently, not the most damaging
species. Conversely, European parasitoids have often been considered for release
against European scolytids that have established in other parts of the world. Several
parasitoids of the European elm bark beetle, Scolytus multistriatus, vector of the
Dutch elm disease, were introduced into North America, either accidentally
(Entedon ergias and Cheiropachus quadrum) or intentionally (Dendrosoter (
protuberans, Ecphylus silesiacus andd Coeloides scolyticida, but only D. protuberans
became established) (Van Driesche et al. 1996). A full evaluation of the biological
control programme was not made. The pteromalid parasitoid Rhopalicus tutela and
several predators, Thanasimus formicarius, Rhizophagus dispar, R. bipustulatus and
R. ferrugineus, were introduced against Hylastes aterr in New Zealand, after its
accidental introduction from Europe, despite the fact that these natural enemies were
rarely, or never found in association with H. aterr in Europe. Only T. formicarius
became established, but its incidence appears limited. (Faulds 1989). Metacolus
unifasciatus, Dendrosoter chaenopachoides and several predators were released
against the European Orthotomicus erosus in South Africa (Kfir 1986). D.
chaenopachoides became established and is now spreading (Tribe and Kfir 2001).
T. formicarius was sent from Germany to the US in 1882-83 against
Dendroctonus frontalis, but this attempt did not succeed (Moeck and Safranyik
1984). Later, Mills and his colleagues (e.g. Mills 1985; Mills and Schlup 1989;
Krüger and Mills 1990; Mills et al. 1991) studied the parasitoids and predators of
European conifer bark beetles in relation to potential biological control of
Dendroctonus spp. in North America. T. formicarius was sent to Canada for
laboratory studies and rearing (Safranyik et al. 2002). It was decided not to release it
because of its possible impact on other bark-beetle competitors of D. ponderosae,
and because laboratory experiments had demonstrated thatt crossbreeding with the
native T. undatulus to produce fertile hybrids was possible. Later on, in 1995-96, T.
formicarius was again considered for classical biological control, against Tomicus
piniperda in the US. However, its introduction was postponed because of its
possible impact on non-target prey and the risk of competitive displacement of
native predators (Haack et al. 1997). Interestingly, T. formicarius was also
introduced in 1908 from Great-Britain into Sri Lanka against Xyleborus fornicatus
on tea, but was never retrieved from the field (Clausen 1978).
Programmes to conserve or augment parasitoids and predators of scolytids have
never been seriously attempted in Europe, with the notable exception of mass
releases of parasitoids against the small elm bark beetle, S. multistriatus, in Granada,
southern Spain, as part of integrated management of Dutch elm disease (González et
al. 1999). Over 1 million specimens of seven parasitoid species were released from
1995 to 1997. Parasitism increased from 6 to 20 %, and, at the same time, the level
of tree infection and of bark beetle populations decreased substantially, but it is not
clear whether the release of parasitoids played any role in these decreases.
In Sweden, Weslien (1992) observed that less than 10% of Ips typographus
populations overwinter in logs, whereas the large majority of its natural enemies do.
He suggested that log removal after the emergence of bark beetles in summer should
be avoided, to preserve parasitoids and predators. Similarly, to control the olive
beetle Phloeotribus scarabaeoides, in southern Spain, González and Campos (1991)
suggested removal of infested wood in late June, just before the emergence of the
beetle, when most of the parasitoids have already emerged.
Kairomones may be used to attract natural enemies and augment their impact.
Schroeder and Weslien (1994) used logs baited with ethanol and alpha-pinene to
attract antagonists of T. piniperda, and observed a significant reduction of beetle
populations compared to unbaited logs. Grégoire et al. (1992) and Pettersson
(2001a, 2001b) determined that oxygenated monoterpenes present in infested trees
play an important role in host/prey location in Rhizophagus grandis on
Dendroctonus micans and in parasitoids of I. typographus, respectively, y and
suggested the use of these compounds to enhance the role of natural enemies.
Control methods may be detrimental to parasitoids and predators and efforts
should be made to limit these detrimental effects. Weslien and Schroeder (1999)
observed that predators were more numerous in unmanaged than in managed spruce
stands. Similarly, the application of pheromone traps may pose a problem in
integrated bark beetle management. Since many predators and parasitoids react to
the same semiochemicals as their prey or host, commercial pheromone traps may
trap out significant amounts of these beneficials (Nebeker et al., 1984). For
pheromone traps against bark beetles it was calculated that the Nemosoma
elongatum individuals caught in the traps would have eaten a multiple of the number
of bark beetles caught in these traps (Baier 1991; Wigger 1993; Schumacher and
Pohris 2000). Optimised blends of semiochemicals and application times may
minimise such detrimental effects (Raffa 1991; Aukemaa et al. 2000).
6. CONCLUSIONS AND FUTURE RESEARCH

Parasitoids and predators have been studied more extensively in bark beetles than in
any other forest insect pests in Europe, which illustrates the significance of
Scolytidae in European forestry. Substantial progress was made in recent years in
the understanding of various aspects of the ecology of parasitoids, such as host
location, competitive interactions, etc. However, many gaps in our knowledge
remain. First of all, most studies concentrated on a few scolytid species whereas the
natural enemy complex of many others is largely unknown. This probably reflects
the relative importance of the different pest species. However, most natural enemies
are not host- or prey-specific and a better knowledge of the natural enemies of
secondary pests would help in understanding the natural control of the primary
pests, which can lead to the development of control strategies. Secondly, there is
wide variation in knowledge of the differentt groups of natural enemies. In general,
parasitoids have been more extensively studied than predators, although there is no
evidence suggesting that parasitoids are more important natural regulators than
predators. Among parasitoids, adult parasitism has been much less investigated than
parasitism on larvae. Most studies on predators focused on Thanasimus formicarius
and Rhizophagus grandis, whereas the biology, ecology and impact of other species
and groups remain largely unknown. More generally, the role of natural enemies in
the population dynamics of scolytids needs to be better assessed, to evaluate their
importance as regulatory factors and to develop strategies to enhance their impact.
Despite extensive research on the natural enemies of scolytids, few attempts
have been made to use this knowledge in biological control strategies, with the
notable exception of the Dendroctonus micans/Rhizophagus
/ grandis programmes.
Classical biological control (i.e. the introduction of an exotic natural enemy into a
new area for permanent control) is better used against exotic species and, thus, is not
targeted for the main scolytid pests in Europe. However, because of the increase of
international wood trade, introductions of exotic bark- and wood boring insects are
rising worldwide. New introductions are expected in Europe, both from other
continents and other European regions (e.g. many European bark beetles, including
Ips typographus, are still absent from the British Isles). Classical biological control
could be envisaged as part of management strategies against new introduction.
Biological control by augmentation (i.e. regular releases of laboratory
reared/produced natural enemies) is technically possible, since many parasitoids and
predators can be mass reared, but it will probably never be economically profitable
in forestry, given the large areas involved and their low productivity. However, it
may be considered for protection of particularly valuable trees, such as the elm trees
of the Alhambra in Granada (González et al. 1999), or in orchards (e.g. Phloeotribus
scarabaeoides and Leperisinus varius in olive groves). Biological control by
conservation (i.e. the conservation and enhancement of native natural enemies
already present on-site) is probably the most promising strategy against scolytid
pests. Forestry practices could be modified d to favour the action of native parasitoids
and predators and to enhance the natural control of forest pests. Various techniques
have been suggested, based on, for example, wood removal dates, use of
kairomones, etc. (see section 5, above), and many more could be developed. These
strategies, however, require an excellent knowledge of the biology and ecology of
parasitoids and predators. More data still need to be gathered on many traits, such as
natural enemy impact and population dynamics, host location mechanisms, biologies
of adult parasitoids and predators in the field, specificity and interactions with
alternative hosts and prey, etc. Furthermore, since such strategies would have to be
adapted to particular regions and field situations, they would rely on the skills of
foresters and other forest practitioners, who would have to be trained specifically for
these tasks.
Taxonomy and identification of natural enemies is another field that would need
more research. There is a serious lack of knowledge, particularly in the systematics
of parasitoids attacking bark beetles. There are too few specialists in Europe, too
many groups of parasitoids that are not properly covered, and the identification keys
are not accessible for applied entomologists. A correct identification of natural
enemies is an essential component of any biological control programme.
7. ACKNOWLEDGEMENTS
We thank Lisa Bartels and Magali Rohner for their editorial work and Massimo
Faccoli and an anonymous reviewer for their constructive comments on the
manuscript. M. Kenis and B. Wermelinger were supported by grants from the Swiss
Federal Office for Education and Science (C98.0042 and C99.0116).
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Chapter 12
PATHOGENS IN BARK BEETLES
R. WEGENSTEINER
of Forest Entomology, Forest Pathology & Forest Protection, Hasenauerstraße 38,
A-1190 Wien, Austria
1. INTRODUCTION
Insect pathology is the science of diseases in all kind of insects, including pests,
beneficials or indifferent species. Knowledge of pathogen occurrence in useful
insects, like honeybees or silk worms, and in insect vectors of human disease,
provided the impetus for the development of insect pathology. The scope of insect
pathology covers the whole field of diseases in insects including aetiology,
symptomatology, epizootiology, and the structural, chemical and functional
alterations that result from diseases.
Comprehensive information is given by several authors on morphological
features and action of different entomopathogens (Weiser, 1961a; Müller-Kögler,
1965; Weiser, 1966, 1977; Krieg, 1986; Levine, 1988; Adams and Bonami, 1991;
Entwistle et al., 1993; Tanada and Kaya, 1993; Hunter-Fujita et al., 1998; Boucias
and Pendland, 1998; Becnel and Andreadis, 1999; Butt at al., 2001). But,
entomopathogens are also known to play a major role in the population dynamics of
many important forest insects. Outbreaks of phytophagous forest insects are very
often terminated by pathogens, and they are responsible for rapid decline and
collapse of local insect populations. Therefore, entomopathogens have potential for
microbial control programmes through inoculative, inundative or augmentative
releases (Lacey and Goettel, 1995).
2. PATHOGENS AND THEIR ACTION

In microbial insect diseases, pathogens invade and multiply in insects and spread to
infect other specimens. Pathogens can be transmitted to insects horizontally by
contact, ingestion, and by vectors, and vertically from parents to their offspring
291
291–313.
© 2007 Springer.
292 R. WEGENSTEINER
(transovum transmission). Pathogens can be non-cellular, infectious agents: viruses,

prokaryotic forms: bacteria and eukaryotic forms: fungi and protozoa. All these
pathogens may cause infections. They can be separated into potential pathogens
(incapable of invading the host without assistance of external factors) and facultative
pathogens (do not require an insect weakened by external factors), they need a
certain medium for replication, and most of them are bacteria and fungi. Obligate
pathogens require live insect hosts for survival and replication (which occurs
intracellularly), e.g. viruses, some fungi and microsporidia (protozoa). Some
pathogens are able to release exotoxins which open the host for infections (catabolic
and anabolic substances; of. bacteria and fungi), others produce endotoxins confined
to the infectious unit (e.g. Bacillus thuringiensis) with the same function. The
method of entry of pathogens varies with the type of pathogen. Fungi generally
invade through the integument (contact insecticides), whereas viruses, bacteria and
protozoa enter their host primarily through the mouth (peroral).
Infectivity is the ability of a pathogen to produce an infection, whereas virulence
is the disease producing power of a pathogen to overcome the host defense
mechanisms and to kill the host. The infection in insects may vary from latent or
inapparent (no signs of disease ), chronic (symptoms are possible, but no mortality)
and acute (symptoms most obvious, mortality). Chronic and latent infections can
become acute infections by the action of stressors. The course of infection by
pathogens after invasion of an insect host up to the time of death is described by the
“incubation period” (period from invasion off pathogen to the development of first
symptoms), then by the beginning and height of disease (clearly visible symptoms),
followed by death. Many pathogens continue to grow and reproduce (form spores or
persistent cysts) after the death of an insect (e.g. bacteria and fungi). However,
definite symptoms allowing indication of disease are not visible in all cases. In
addition, the termination of a chronic disease may involve the recovery of an insect
due to its immune responses. Several different pathogens (and non-pathogenic
organisms) can occur within the same host insect and they may interact with each
other. The interaction may result in independent coexistence, complementarity or
interference.
Preliminary diagnosis (cursory examination of a dead insect) is normally
followed by a tentative diagnosis (macroscopic and microscopic examinations of the
diseased specimen), both lead to a definite diagnosis of pathogens, based on
laboratory and field data and comparison with information from the literature.
Physical examinations by use of optical and electron microscopes and molecular
studies of pathogens are the basis for all further studies. After this laboratory studies
must be conducted to isolate, culture and study the biology of pathogens.
Completing all these steps allows evaluation of impact of pathogens on their hosts,
and extensive bioassays are necessary before use of pathogens in biological control.
PATHOGENS IN BARK BEETLES 293
3. TAXONOMY, SYSTEMATICS AND BIOLOGY OF PATHOGENS
3.1. Viruses
Virus particle (virion) morphology is an important character in assigning a virus to a
taxonomic group. A virion is composed of a protein shell (capsid) that surrounds the
nucleic acid. The capsid provides the virion with morphological and functional
properties, the nucleic acid with the genetic constituent, and both together form the
nucleocapsid. Each virus has only one type of nucleic acid, either DNA or RNA. In
some groups (Baculoviridae, Entomopoxviridae, Reoviridae) the nucleocapsids are
occluded in a crystalline protein matrix (occlusion body). This occlusion body
contributes to the stability and persistence of the virions when they are released from
the host into the environment. When a host consumes the occlusion body, the
protein matrix dissolves in the midgut, releasing the virions which attach to the
membranes of the microvilli and cross these membranes. The virions are taken in by
a process of fusion, they begin to replicate viral RNA or DNA in the cytoplasm, e.g.
entomopoxviruses (EPV) or cytoplasmic polyhedrosis virus (CPV), or in the
nucleus, e.g.: nuclear polyhedrosis virus (NPV) or granulosis virus (GV). One
important feature of insect viruses is that they are obligate pathogens and most of
them are relatively host specific. Virus infections
f are usually very contagious and
cause mortality.
3.2. Bacteria
Bacteria are unicellular organisms but lack of defined nucleus (Procaryotes). They
may have rigid cell walls or they are without cell walls. Some species produce
resistant endospores. Bacteria are the most common microorganisms associated with
insects, most of them developing extracellularly except for the pathogenic
Rickettsia. Many cause no diseases to insects, but a significant number are important
pathogens. Bacterial infections in insects can be classified as bacteremia (bacteria
multiply in the insect’s haemolymph without production of toxins), septicemia
(bacteria multiply in the insect haemocoel and produce toxins) and toxemia (bacteria
produce toxins killing the insect and are confined to the gut lumen). Bacteria infect
insects mostly through the mouth and digestive tract (taken in together with food).
Within the digestive tract, the bacteria produce enzymes. These enzymes may
damage the cells of the gut wall and enable the bacteria to enter the haemocoel and
may act on tissues in the haemocoel. The majority of non-sporeforming bacteria are
facultative pathogens whose pathogenicity depends on stress conditions affecting the
insect host.
Many of the insect pathogenic bacteria occur in the family Bacillaceae; Bacillus
thuringiensis in particular, has received considerable attention as a microbial control
agent. Members of the family Bacillaceae produce endospores and are gram-
positive, motile or nonmotile rods. They are aerobic or facultatively aerobic and
usually produce a catalase. They multiply as vegetative cells. The vegetative cell,
294 R. WEGENSTEINER
when it begins to produce a spore, is called a sporangium. During sporulation they

produce parasporal bodies within the sporangium containing an endotoxin.
Different subspecies of B. thuringiensis are known to be pathogenic to different
insect orders . One type is known to be pathogenic to Lepidoptera, another one to
(aquatic) Diptera and a third one to Coleoptera, and they are classified in different
serotypes.
3.3. Fungi
Entomopathogenic fungi can be found within the Zygomycota, Ascomycota and
Deuteromycota. Up to now, mainly species of the Deuteromycota (can be grown on
artificial media) were tested with regard
d to their efficacy to pest insects.
Most of the Entomopathogenic fungi form m superficial growth on the surface of
their hosts where they produce conidia. Their growth and development are limited
mainly by the external environmental conditions, in particular, high humidity or
moisture and adequate temperatures for sporulation and spore germination. The
infectious units are the conidia (and hyphal
y bodies). The fungi gain access to the
insect mainly through the integument. The development of a mycosis can be
separated into three phases: 1. adhesion and germination of the spore on the insect’s
cuticle, 2. penetration of the integument into the haemocoel and 3. development of
the fungus, which generally results in death of the insect, ending with sporulation on
the surface of the cadaver. Host specificity of entomopathogenic fungi varies
considerably, some of them infecting a broad range of insect hosts (e.g. Beauveria
bassiana infects at least 100 different insect species).Virulence of isolates may also
have a high degree of specificity.
3.4. Protozoa
Entomopathogenic protozoa are minute unicellular organisms, they are members of
the protozoan phyla: Rhizopoda, Apicomplexa, Microspora, Zoomastiginia and
Ciliophora . The highly pathogenic forms occur in the protozoan phylum
Microspora, particularly those that invade the haemocoel and different tissues and
develop intracellularly. They may cause severe acute infections in insects, but some
produce only inapparent or chronic infections, which nonetheless may play an
important role in regulating insect populations.
The majority of the protozoa enter the insect by the way of the mouth and
digestive tract. The infective stage is generally a spore or a cyst. Those protozoa that
remain in the lumen of the digestive tract are attached to the midgut epithelium or
enter appendages associated with the digestive tract (gregarines). Others penetrate
into the haemocoel and develop within cells of various tissues and organs (e.g.
apicomplexa and microspora). Microsporidia possess unicellular spores, containing
a uninucleate or binucleate sporoplasm, and an extrusion apparatus always with a
polar filament and a polar cap; they do not have mitochondria. They are obligate
pathogens and multiply only in living cells, causing economically serious diseases in
beneficial and pest insects. Therefore, microsporidia are the most promising
protozoa for use in microbial control. But, the rest of protozoa, other Apicomplexa,
(Neogregarina and Coccidia) are also efficient pathogens of insects.
4. PATHOGENS IN BARK BEETLES

Many pathogens have been described from different insect species, whereas
pathogens in bark beetles are still not very well investigated and there are only a few
articles summarizing the current knowledge (Postner, 1974; Mills, 1983; Bathon,
1991; Nierhaus-Wunderwald, 1993; Stephen et al., 1993; Fuxa et al., 1998).
Furthermore, there is a great lack in knowledge of the action of pathogens in bark
beetles worldwide in spite off the presumed potential of pathogens in controlling bark
beetle populations.
4.1. Viruses
The Ips typographus Entomopoxvirus was the first record of a virus disease in the
most important European spruce bark beetle species, Ips typographus, occurring in
the cells of the midgut epithelium (Weiser and Wegensteiner, 1994; Wegensteiner
and Weiser, 1995). Information on the prevalence of the ItEPV in different I.
typographus populations (varying from 0.0 to 3.6%) is presented by Wegensteiner et
al. (1996). This virus is presumed to be different from all former described
entomopoxvirus type A (Zizka et al., 2001). Discoidal inclusion bodies are released
with faeces and the infection appears in adult beetles where it destroys the gut
epithelium. The virus seems to be absentt in America. Only from Northern China
there are two reports of an entomopoxvirus in Dendroctonus armandi (Fan et al.,
1987; Tang and Fan, 1990). In North America Sikorowski et al. (1996) found five
different virus-like particles in Dendroctonus frontalis which were not connected
with evident disease and similar to different virus types but no entomopoxvirus.
Haidler (1998) found the ItEPV in I. typographus from a locality in the Austrian
central Alps, Händel (2001) found the ItEPV not only in I. typographus but also in I
amitinus; furthermore, he found indications of a Baculovirus (in the nuclei of
midgut epithelium) and of entomopoxvirus-like spheroids in the cytoplasm of the
midgut epithelium of Polygraphus poligraphus. The common occurrence of ItEPV
in I. typographus was reported from different sampling plots in a planned national
park area in Austria (Gasperl, 2002).
Up to now, there are no papers concentrating on the efficacy of these virus
infections on their hosts. Preliminary field experiments showed successful
introduction of the ItEPV in an Ips typographus field population (Pultar and Weiser
1999). Experiments infecting Scolytus scolytus larvae with the Oryctes baculovirus
produced inexplicable results on the presence of virus particles which were different
from those inoculated, but in any case infections had no significant influence on
mortality of beetles (Arnold and Barson, 1977). At the moment, there is no evidence
of transmission of the Ips typographus Entomopoxvirus to Scolytus spp. or other
bark beetle species of deciduous trees.
296 R. WEGENSTEINER
4.2. Bacteria
Relatively few papers deal with entomopathogenic bacteria in bark beetles. Chararas
(1955, 1962) and Pesson et al. (1955) were the first to report bacteria in bark beetles
from Europe; some of the bacteria ((Aerobacter scolyti and Escherichia
klebsiellaeformis) were found to cause high mortality (up to 100%) in Scolytus
multistriatus within 72 hours (Pesson et al., 1955). Lysenko (1959) found bacteria in
Ips curvidens (Serratia marcescens) and in Xyloterus lineatus (Pseudomonas caviae,
Pseudomonas septica, Cloaca cloacae and Bacillus coagulans). Novak (1960) found
Pseudomonas septica in Trypodendron lineatum. Balazy (1966) reports the
occurrence of several bacteria in different bark beetle species from Poland, without
precise identification. Later some of these bacteria (Bacillus subtilis, Bacillus
pumilus, Enterobacter cloacae, Enterobacter aerogenes, Flavobacterium sp.,
Corynebacterium sp.) were found to occur in Scolytus multistriatus in Australia
(French et al., 1984). Inspection of Anisandrus disparr produced evidence of
numerous bacteria (Enterobacter agglomerans, Pseudomonas chlororaphys,
Xanthomonas maltophilia, Staphylococcus lentus, Vibrio alginolyticus, Bacillus
subtilis, Pseudomonas cepacia, Erwinia rhapontici, Erwinia rubrifaciens,
Pasteurella haemolytica, Bacillus megaterium,
e Pseudomonas alcaligenes,
Pseudomonas paucimobilis, Bacillus thuringiensis, Acinetobacter calcoacetius) and
other microorganisms (Canganella et al., 1994). Even in North America there are
few records dealing with bacteria in bark beetles, from laboratory colonies (Wood
1961) and from field populations (Doane, 1960; Jouvenaz and Wilkinson, 1970;
Moore, 1971, 1972). Serratia marcescens caused high mortality in S. multistriatus
larvae within a four day period and was highly correlated with the number of larvae,
which was interpreted as a crowding effect (Doane, 1960). In one population of
adult I. calligraphus from Florida the incidence of S. marcescens was high (45.7%)
due to ingestion of contaminated phloem in old logging debris or to contact between
crowded adults during the predispersal, maturation-feeding period (Jouvenaz and
Wilkinson, 1970). Most of these reports refer to isolates from beetles dead in their
galleries in the bark. There is no evidence off any transmission of bacterial infections
with eggs and in larvae. Most cases were characterised by a multiple mixed bacterial
flora, without evidence of any specific strain.
The occurrence of Bacillus thuringiensis in Ips typographus and Dendroctonus
micans is reported from Georgia, where activity of the bacterium is thought to
correlate with the activity of β-exotoxin in the bacterial preparation Bitoxibacillin
used (Imnadze, 1978). Infection experiments with Bacillus thuringiensis var.
insectus against Ips subelongatus worked partly, but most probably also as a
consequence of exotoxins (Gusteleva, 1982a, b). Tomalak et al., (1988) found
Gram-negative bacteria in the fat body of all inspected Hylurgopinus rufipes from
Canada, but with no apparent pathological effects in the host. Testing different
bacteria (Bacillus thuringiensis var. thuringiensis, Bacillus alvei, Bacillus cereus,
Pseudomonas syringae) against Scolytus scolytus- and S. multistriatus- larvae
worked partly, with mortality up to 91.3% depending on inoculation dose (Jassim et
al., 1990). Further experiments confirmed possible contaminations during laboratory
evaluation, because Bacillus thuringiensis was not effective against Ips calligraphus
and Dendroctonus frontalis, but a bacterial metabolite alone was very effective
(Cane et al., 1995) when applied to laboratory colonies. Bacillus thuringiensis var.
tenebrionis caused no significant mortality in adultt Ips typographus in field tests,
spraying bark surface of spruce logs before beetles colonised the log sections
respectively after beetles colonisation (Novotny and Turcani, 2000).
4.3. Fungi
In a similar extent as bacteria, pathogenic and saprophytic fungi are common in dead
beetles, in many cases this development is without growth of fungi on surface of
dead beetles.
In comparison with other pathogens, many records can be found dealing with
entomopathogenic fungi in bark beetles, first reviewed by Müller-Kögler (1965). A
number of investigations show the occurrence of fungi in bark beetle field
populations, several different fungal species were found, including Beauveria
bassiana and Spicaria (Paecilomyces) sp. which are those mentioned most
frequently.
As a consequence of numerous references the occurrence of different
entomopathogenic (mainly Deuteromycete) fungi in different bark beetle species is
listed in chronological order.
Beauveria bassiana in: Hylastes aterr (Petch, 1932), Ips typographus, Ips duplicatus
(Karpinski 1935), Ips typographus (Siemaszko, 1939), Ips typographus (Neuzilova,
1956), Scolytus multistriatus (Doane, 1959), Scolytus ratzeburgi, Scolytus
multistriatus, Scolytus scolytus, Scolytus laevis, Polygraphus poligraphus,
Hylurgops palliatus, Hylastes ater, Hylastes opacus, Dryocoetes
r autographus,
Leperesinus fraxini, Ips typographus, Ips amitinus (Balazy, 1962, 1965, 1966;
Balazy et al., 1967), Blastophagus piniperda (Nuorteva and Salonen, 1968),
Hylastes aterr (Leatherdale, 1970), Trypodendron lineatum (Magema et al., 1981),
Ips acuminatus (Balazy et al., 1987), Ips typographus (Landa et al., 2001),
Leperesinus varius (Kirschner, 2001).
Beauveria caledonica in: Crypturgus pusillus, Dryocoetes autographus,

Gnathotrichus materiarius, Hylurgops palliatus, Ips typographus, Orthotomicus
laricis, Pityogenes chalcographus, Polygraphus poligraphus (Kirschner, 2001).
Paecilomyces farinosus in: Ips typographus (Neuzilova, 1956), Ips typographus

(Balazy et al., 1967), Trypodendron lineatum (Kirschner, 2001), Ips typographus
(Landa et al., 2001).
Paecilomyces fumosoroseus in: Ips typographus (Landa et al., 2001).

298 R. WEGENSTEINER
Paecilomyces variotii in: Leperesinus varius (Chararas, 1957), Dryocoetes

autographus (Chararas, 1962).
Verticillium lecanii in: Crypturgus pusillus (Balazy, 1962), Polygraphus

poligraphus (Balazy, 1963), Scolytus intricatus, Scolytus kirschii, Polygraphus
poligraphus, Hylesinus crenatus, Ips typographus (Balazy, 1973; Landa et al.,
2001).
Mucor hiemalis in: Trypodendron lineatum (Magema et al., 1981).
Tolypocladium cylindrosporum in: Pityogenes chalcographus (Kirschner, 2001).
In all cases cited it is evident that Deuteromycete fungi are able to kill all stages
of bark beetles when the fungus has free access to the cuticle, but do not interfere
with the developmental stages (eggs, larvae, pupae, callow adults) during their
development in sterile conditions of galleries in fresh bark (in the tree).
Infections with other fungi are rare, there is one case of an Ascomycete,
Metschnikowia typographi in Ips typographus (Weiser and Wegensteiner, 1998), Ips
typographus and Ips amitinus (Händel, 2001; Weiser et al., 2003), the infection is
under further investigation.
The importance of high humidity for infection of bark beetles (larvae and adults)
with Deuteromycetes and for growth of conidia on cadavers is mentioned by several
authors (Doane, 1959; Schvester, 1957; Balazy, 1963). The possible role of vectors
(e.g. predators, parasitoids) in spread of infection through transmission of fungal
spores within bark beetle galleries was mentioned in early investigations (Karpinski,
1935; Doane, 1959). Many fungi were found in galleries of bark beetles (31
different species) from different tree species, and even iff beetles were not present in
their galleries, several of them were known as entomopathogenic fungi (Beauveria
bassiana, Beauveria caledonica, Conidiobolus coronatus, Paecilomyces farinosus,
Tolypocladium cylindrosporum and Verticillium lecanii), B. bassiana, B. caledonica
and P. farinosus were the most abundant species (Kirschner, 1998, 2001; Landa et
al., 2001).
Novak and Samsinakova (1962) performed laboratory and field tests with B.
bassiana against Trypodendron lineatum and they were able to show high efficacy
of laboratory isolates especially to larvae (100% mortality in 6 to 8 days) but also to
adults (100% mortality in 12 days).
Several studies have focused on efficacy comparison off different fungal species
in bark beetles. Artificial infection was successful with Verticillium lecaniii in
Scolytus scolytus larvae (Balazy, 1963). Action of Verticillium lecaniii was also
tested in the laboratory against Scolytus scolytus larvae by Barson (1976), but
especially high mortality was caused in S. scolytus larvae by Beauveria bassiana
(Barson, 1977), an inoculum of 1x106 spores was determined as the LD50 after 5
days (at 23°C and 100% relative humidity). Comparison of the efficacy of B.
bassiana and P. farinosus in adult I. typographus and in S. ratzeburgi larvae

revealed better infections using B. bassiana (Balazy, 1966). Nuorteva and Salonen
(1968) found B. bassiana infection rates in B. piniperda up to 62.5%, but infection
rates decreased with increasing time of exposure of conidia on the bark surface.
All developmental stages of Pityogenes chalcographus (larvae, pupae, adults)
were sensitive to B. bassiana infections in a laboratory study (especially larvae and
pupae) depending on inoculation dose (in 3 to 10 days up to 100% mortality). In
addition, abiotic conditions favouring efficacy of B. bassiana were higher
temperature (especially 25°C), bark humidity (45%) in breeding systems and
particularly air humidity in incubation vessels (especially 91%). Furthermore,
horizontal transmission of the infection was observed within breeding systems, and
the number of eggs laid was significantly reduced in infected females (Wulf, 1979,
1983).
Doberski (1981a, b) tested the pathogenic effects of different strains of
Beauveria bassiana, Metarhizium anisopliae and Paecilomyces farinosus to Scolytus
scolytus larvae, with B. bassiana being the most virulent species. Indirect
inoculation of adult beetles via treatedd bark was found to be successful for B.
bassiana and M. anisopliae. Successful infections in larvae were found at
temperatures down to 2°C with B. bassiana and P. farinosus. In the case of M.
anisopliae the minimum temperature for infection was 10°C; B. bassiana and d M.
anisopliae were successful even at low humidities (from 100% to 51%), and P.
farinosus only from 100% to 86% humidity. Unknown factors essential for
germination of B. bassiana on the cuticle of Dendroctonus ponderosae were
presumed by Hunt et al. (1984). Gusteleva (1984) reports controversially the high
sensitivity of adult Ips subelongatus to Beauveria bassiana (89% mortality) but
observed no effect on larvae.
Matha and Weiser (1985) tested a commercial B. bassiana preparation (Boverol)
via indirect inoculation of beetles exposing them to spore treated filter paper and
were able to show that this method caused 100% mortality in I. typographus. In
addition, they were able to transfer the infection from dead beetles overgrown with
fungus to healthy ones by accidental contact, but mortality was not as high as
through contact with preparation on filter paper.
When Houle et al. (1987) tested different fungal species and different fungal
strains against Scolytus multistriatus, they found B. bassiana, M. anisopliae and
Paecilomyces fumoso-roseus produced 100% mortality att high inoculation dosages,
whereas other fungal species tested were not as effective (Cordyceps militaris,
Hirsutella thompsonii, Nomuraea rileyi, Verticillium lecanii, Paecilomyces
farinosus).
Temperature, humidity, spore formulation and spore dose dependent effects of
Beauveria bassiana to Trypodendron lineatum were tested in the laboratory, and the
results were similar to those from tests with other bark beetle species (Prazak, 1988,
1991, 1997). Different test conditions caused 36% to 55% mortality in most cases,
while only a few experiments lead to mortality rates higher than 80%. Transmission
of B. bassiana from inoculated male beetles to healthy female beetles was successful
and caused 20% reduction of egg laying. Treatment of the bark surface resulted in
300 R. WEGENSTEINER
reduced number of egg niches (up to 44%) depending on applied spore

concentration. Treatment of soil resulted in high mortality of hibernating offspring
beetles (88% to 100% mortality). In additional tests, infection rates were high in P.
chalcographus and Hylastes cunicularius, but relatively low in Hylurgops palliatus
(Prazak, 1988).
Testing pathogenic effects of Beauveria bassiana, Beauveria brongniartii and of
one more B. brongniartii strain (syn. B. tenella) to Ips typographus showed high
virulence particularly of B. bassiana (4.8 days mean life span); even contact of I.
typographus with B. bassiana treated bark for one minute caused 60% mortality, or
contact of healthy beetles with cadavers of I. typographus with fungal conidia on
their surface caused high infection rates (98.6%). Infection rates differed at three test
temperatures (13°, 23° and 33°) but were always high (78% to 100%)
(Wegensteiner, 1992). Inoculation dose and temperature were also shown to be very
important factors for the action of B. bassiana in I. typographus (up to 100%
infection), and even contact of I. typographus with B. bassiana treated bark led to
infection rates up to 97% (Wegensteiner, 1996). Laboratory tests exposing
Polygraphus poligraphus to B. bassiana or B. brongniartii treated bark pieces
showed that B. bassiana caused higher infection rates (72%-100%) than B.
brongniartii (69.6%-81.4%). Furthermore, testing th, effects of temperature and B.
bassiana inoculation dose in P. poligraphus brought similar results as found in I.
typographus (87% to 100% infection) (Wegensteiner, 2000).
The efficacy of Metarhizium anisopliae was tested against adult Pityogenes
chalcographus, when direct inoculation of beetles caused high mortality (95.3%),
and inoculation via treated bark resulted in 26.8% infection (Pehl and Kehr, 1994).
Markova (2000) tested the effects off B. bassiana, M. anisopliae, P. farinosus and V.
lecanii to I. typographus; the most pathogenic species was M. anisopliae (100%
mortality in 4 days) and the least pathogenic one was V. lecanii (still causing 90%
mortality).
However, B. brongniartii and Metarhizium anisopliae were never identified from
field collected bark beetles.
In field populations the importance of entomopathogenic fungi is mentioned,
especially for P. farinosus and B. bassiana (Balazy, 1968). Fungal pathogens were
found in all developmental stages even if the percentage of infection and the
proportion of reduction of beetle population was estimated to be relatively low.
Bychawska and Swiezynska (1979) performed field experiments spraying B.
bassiana on trap logs to infect Tomicus piniperda; this treatment caused no
significant infection in T. piniperda, and different abiotic conditions (rain, snow,
insolation) were identified as major problems reducing viability of germs in field
conditions. In a further experiment infested trap logs were sprayed with B. bassiana
suspension then covered with a polyethylene foil to improve climatic conditions and
to infect the emerging callow adults of T. piniperda with B. bassiana; this procedure
was successful and resulted in 71 to 100% infection (Lutyk and Swiezynska, 1984).
In all reported cases there is no mention of mortality in larvae during their
development in fresh phloem of trees.
Some special laboratory experiments were performed simulating hibernation of

I. typographus in litter, which caused 70% mycosis at 20°C, 17°C and 12°C after 28
days, 35 days and 41 days respectively. Furthermore, field experiments were carried
out with the special aim of using B. bassiana against I. typographus during
hibernation in litter, and these resulted in promising infections (Hallet et al, 1994).
These results were confirmed by a further study, but B. bassiana-infection rates
were high even in the control group, due to the natural presence of B. bassiana in the
soil of all experimental plots (Arbesleitner, 2002) similar to the observations of
Hallet et al. (1994). Kreutz (1995) found only B. bassina in I. typographus after
hibernation in the soil.
Testing the virulence of B. bassiana against I. typographus by the way of
inoculative release via B. bassiana-containing pheromone traps (catch – inoculate –
release technique) were very promising, since this inoculation mode caused high
infection rates (70.7 to 96.7%) and a significantly reduced life span of beetles
(several beetles died within the nuptial chamber) plus a reduction of length of
maternal galleries (Vaupel and Zimmermann, 1996; Kreutz et al., 2000a, b; Kreutz,
2001).
4.4. Protozoa
Fuchs (1915) was the first to describe protozoan diseases in Ips typographus, with
the identification of two protozoan species, Telosporidium typographi and
Gregarina typographi. In most of the investigations adult beetles were inspected, in
the majority of cases from field collected specimens.
Weiser (1954, 1955, 1961a, 1966, 1977) was the first to summarize the
knowledge on protozoa in bark beetles. Purrini and Führer (1979) were the first who
tested laboratory infections of bark beetles with protozoa. Sprague (1977) and
Levine (1988) included the protozoan species described from bark beetles in their
systematic compendium of microsporidia.
Rhizopoda, Amoebina
The occurrence of a rhizopodan species was mentioned, first determined as a
variety of Malamoeba locustae (Purrini, 1978a, b), and later described as
Malamoeba scolyti, in the cells of the midgut epithelium and of the Malpighian
tubules of Dryocoetes autographus (Purrini, 1980). Purrini and Führer (1979) were
able to show that Malamoeba scolyti is also infective to Pityogenes chalcographus
(6.0% to 26.0% infection of tested beetles). Kirchhoff (1982) and Kirchhoff and
Führer (1985) found M. scolyti in Hylurgops palliatus field populations too and they
investigated the effects of this pathogen by artificial infection in the lab. Kirchhoff
and Führer (1990) found a significant reduction of life span of infected D.
autographus (at 20°C, time to death: 5 to 7 weeks post infection, compared with 3 to
4 months in control beetles), and successfully transferred the infection to several
other bark beetle species ((Hylurgops palliatus, Hylastes ater, Tomicus piniperda,
Polygraphus poligraphus, Pityogenes chalcographus, Pityogenes bidentatus,
Pityogenes calcaratus, Ips typographus, Ips laricis, Ips acuminatus, Ips
sexdentatus,); but they also mentioned that it can be some inhibition in manifestation
302 R. WEGENSTEINER
of disease in case of nematode presence in the gut of I. typographus and D.

autographus (Kirchhoff, 1982; Kirchhoff and Führer, 1990). The whole life cycle of
M. scolyti in D. autographus was described by Purrini and Zizka (1983).
Wegensteiner (1994), Wegensteiner et al. (1996) and Händel et al. (2001) found
Malamoeba scolyti in the gut of Ips typographus from different localities in Austria.
M. scolyti was found in Dryocoetes autographus and Ips typographus, but also in
Hylurgops glabratus from a locality in the Austrian Alps, even if in a small number
of beetles (Haidler, 1998). Händel (2001) mentioned in his study the occurrence of
M. scolyti in Ips typographus, Hylurgops palliatus, Dryocoetes autographus and for
the first time in Hylastes cunicularius from several localities in Austria. Totally new
was the observation of Malamoeba scolyti in Ips acuminatus from Austria (Zitterer,
2002).
Besides this species, there is only one more passing mention of an Endamoeba
sp. in Pityogenes calcaratus (Purrini and Halperin, 1982).
4.5. Apicomplexa, Eugregarinida

Fuchs (1915) first described Gregarina typographi occurring in the midgut lumen of
Ips typographus. Theodorides (1960) found Gregarina typographi occurring in Ips
sexdentatus. Different gregarines are mentioned from several bark beetle species in
the compendium of Geus (1969): Gregarina piktyokteinidis in Pityokteines
curvidens (Rauchalles i. litt., in Geus 1969), Gregarina hylastidis in Hylastes ater,
Hylastes cunicularius andd Hylastes opacus (Rauchalles i. litt., in Geus, 1969),
Gregarina typographi in Dryocoetes autographus (Geus, 1969), Gregarina
pityogenidis in Pityogenes bidentatus (Rauchalles i. litt., in Geus, 1969) and
Acanthospora crypturgi in Crypturgus pusillus (Geus, 1969).
Inspecting Ips typographus in Austria brought evidence of Gregarina typographi
in the beetles from some of the differentt localities (Wegensteiner, 1994). A further
study, including more sites, showed that G. typographi can be found in I.
typographus from many localities in Austria and the Czech Republic, in some cases
at high prevalence (up to 43.8%) (Wegensteiner et al., 1996). Inspecting the
pathogens of bark beetles living associated on spruce brought evidence of Gregarina
hylastidis in Hylastes cunicularius and most probably of Gregarina cf. typographi in
Hylurgops glabratus, in Pityogenes chalcographus and in Ips amitinus (Haidler,
1998; Händel, 2001); in addition, they also found G. typographi in I. typographus
and in D. autographus. An undescribed Gregarina sp. was observed in the midgut
lumen of Tomicus minorr from Austria (Kohlmayr, 2001). Gregarina typographi
could be found frequently in I. typographus from a national park area, and partly in
a very high proportion of inspected beetles (up to 63.9%) (Gasperl, 2002). During
inspection of Ips acuminatus a Gregarina sp. was found in the gut lumen of adult
beetles from Austria and Norway (Zitterer, 2002).
4.6. Apicomplexa, Neogregarinida

The first to report a neogregarinid species, Telosporidium typographi, in Ips

typographus was most probably Fuchs (1915) who argued that the impact of this
infection on the beetles can be an important mortality factor.
Weiser (1955) first described the occurrence of Menzbieria chalcographii in
Pityogenes chalcographus. Purrini and Führer (1979) performed infection
experiments with M. chalcographi in P. chalcographus and showed that beetles
from different localities were not in all cases sensitive to this infection (0.0% to
12.0% infection), and artificial infection worked only in beetles without nematodes
in the gut. Ophryocystis dendroctoni was found in the Malpighian tubules of
Dendroctonus pseudotsugae (Weiser, 1970). Mattesia schwenkei was described
from the adipose tissue of Dryocoetes autographus (Purrini, 1977) and of Hylurgops
glabratus (Purrini, 1978b). Purrini (1978b, 1980) found Menzbieria chalcographi in
Dryocoetes autographus, in H. glabratus and in Hylurgops palliatus. Ophryocystis
hylesini was found in the Malpighian tubules of Hylesinus fraxini (Purrini and
Ormieres, 1981). A first indication of the occurrence of Ophryocystis sp. in the
Malpighian tubules of Pityogenes calcaratus is given by Purrini and Halperin
(1982). The presence of spores of a new neogregarine in the adipose tissue was
recorded for Ips typographus from a nature reserve in Germany (Wegensteiner and
Weiser, 1996a), the spores were identified as similar to those spores which Fuchs
(1915) described as Telosporidium typographi. Morphological features of this
neogregarinid species indicatedd that it is most probably a Mattesia sp. (Zizka et al.,
1997, 1998). This Mattesia sp. was found only in very few I. typographus from a
national park area in Austria (Gasperl, 2002). Not concise data are given on the
occurrence of an unidentified neogregarinid species in Pityophthorus pityographus
(Haidler, 1998) and in Pityogenes chalcographus (Händel, 2001). Another
neogregarinid species, similar to Mattesia sp. in I. typographus, was found in Ips
acuminatus from one locality in Norway (Zitterer, 2002).
4.7. Microspora
Three types of microsporidia are represented in bark beetles of conifers:
Chytridiopsis sp. with thick walled spherical pansporoblasts filled with 16 or more
spherical spores, infecting the cells of the midgut epithelium. Nosema typographi
with single binucleate spores mainly in the fat body and Malpighian tubules, and
Unikaryon sp. respectively Canningia sp. with single uninucleate spores mainly in
the cells of the midgut epithelium, the Malpighian tubules and the ovariols of adult
beetles. The genera Stempellia and Pleistophora are infecting scolytids of deciduous
trees, they have ovoid spores connected in groups of 8 – 16 or in irregular masses in
the cells of the midgut epithelium and other tissues.
Weiser (1954a, b) was the first to describe Chytridiopsis typographi (formerly
Haplosporidium typographi) from the gut epithelium of Ips typographus, and in the
American species Dendroctonus pseudotsugae (Weiser, 1970); in the same paper
Nosema dendroctoni is described for D. pseudotsugae. Nosema typographi was
described by means of light microscopy from the adipose tissue of Ips typographus
(Weiser, 1955), and later this investigation was completed by an electron
304 R. WEGENSTEINER
microscopy study (Weiser et al., 1997). Nosema typographi was also found in
Hylurgops palliatus (Purrini, 1978b). Furthermore, Weiser (1961b) described a
microsporidium, Nosema curvidentis, from Pityokteines curvidens, which occurred
mainly in the adipose tissue, the hypodermis and connective tissues.
Stempellia scolyti was found by Weiser (1966) mainly in the midgut of Scolytus
scolytus, S. multistriatus, Scolytus pygmaeus and Scolytus ensifer. Lipa (1968) found
Nosema scolyti in the same four Scolytus species (in the midgut, in Malpighian
tubules and in haemocytes). Weiser (1968) described Plistophora scolyti in Scolytus
scolytus and mentioned a double infection with Nosema curvidentis in the gut wall
and in oenocytes. A microsporidium similar to Stempellia scolyti in size, but
different in development was found in Scolytus scolytus from Kosovo (Purrini,
1975).
There are only two mentions of the occurrence of Unikaryon minutum in an
American bark beetle, Dendroctonus frontalis (Knell and Allen, 1978), and later it
was found again in differentt populations occasionally att high prevalence (4.3% to
55.0% infection) in the same host (Bridges, 1987).
Nosema typographi and Helicosporidium parasiticum were mentioned briefly to
occur in Hylurgops palliatus (Purrini, 1980).
Pleistophora xyloteri was described as occurring in the gut wall of Trypodendron
domesticum, and Nosema dryocoetesi in the adipose tissue of Dryocoetes
autographus (Purrini and Ormieres, 1981). Nosema calcarati was found in the
gonads of Pityogenes calcaratus (Purrini and Halperin, 1982).
In further investigations Chytridiopsis typographi was found to infect Hylastes
cunicularius too (20% infection) (Purrini and Weiser, 1984). Dates on spore
dimorphism of Chytridiopsis typographi from I. typographus are mentioned in the
study of Purrini and Weiser (1985); in the same paper there is a passing mention
(without precise data) that Chytridiopsis typographi was also found in Ips laricis and
in Hylurgops glabratus from Germany. A study concentrating on the pathogens in
Ips typographus brought evidence of several microsporidia in this species,
Chytridiopsis typographi was found in many localities in Austria and the Czech
Republic in prevalence up to 27.7% (Wegensteiner, 1994; Wegensteiner et al., 1996;
Skuhravy, 2002). Considerable distinctions were found in infection rates of I.
typographus field populations (from pheromone trap catch), varying in different
years depending upon date of sampling within a year (1.0% to 80.0% infection), in
comparison with several consecutive laboratory generations (22.1% to 67.5%
infection) (Wegensteiner and Weiser, 1996b,). Chytridiopsis typographi and
Nosema typographi were found in Ips typographus from a nature reserve in
Germany (Wegensteiner and Weiser, 1996a). Laucius and Zolubas (1997) found
Chytridiopsis typographi also in Ips typographus from Lithuania. Studies on
associated spruce bark beetles from a site in the central Alps of Austria showed that
Ch. typographi also can be found in Hylastes cunicularius, Hylurgops glabratus,
Pityophthorus pityographus, Pityogenes chalcographus, Ips typographus and Ips
amitinus (Haidler, 1998), results which were confirmed in a further study for the
species Pityogenes chalcographus, Ips typographus and Ips amitinus (Händel,
2001). Chytridiopsis sp. seems to be a non-specific pathogen infecting several bark

beetle species of conifers.
Canningia spinidentis was described from the adipose tissue, the Malpighian
tubules, muscles and connective tissues of Pityokteines spinidens (Weiser et al.,
1995). Unikaryon montanum was found in the adipose tissue, the Malpighian
tubules and the ovaries of Ips typographus (Weiser et al., 1998).
Host specificity of Nosema typographi and Unikaryon montanum is unclear at
the moment especially with regard to associated (in the same tree) living bark
beetles. Not identified microsporidia were mentioned by Haidler (1998) for
Hylurgops glabratus, Hylurgops palliatus, Dryocoetes autographus, Pityogenes
chalcographus and Ips amitinus. Händel (2001) was able to find Nosema typographi
in Ips typographus and a Nosema sp. in Hylurgops palliatus, and Unikaryon
montanum in Ips typographus, respectively undescribed Unikaryon spp. in
Pityogenes chalcographus, Ips amitinus and in Polygraphus poligraphus. The
Unikaryon sp. in Polygraphus poligraphus, found in the midgut cells, in gut muscles
and in Malpighian tubules was described later as Unikaryon polygraphi (Weiser et
al., 2002). Analysis of Ips typographus from different sampling plots in a planned
national park in Austria brought evidence of Chytridiopsis typographi in the beetles
of most plots, but Nosema typographi and Unikaryon montanum were found only in
the beetles from one sampling plot (Gasperl, 2002). Chytridiopsis sp. (probably
Chytridiopsis typographi) was found in Ips acuminatus from Austria, Czech
Republic and from Norway (Zitterer, 2002).
Kohlmayr (2001) and Kohlmayr et al. (2003) report the occurrence of Canningia
tomici in the cells of the midgut epithelium, the adipose tissue and in the gonads of
Tomicus piniperda from Austria, Czech Republic, Poland, Finland and from USA.
5. CONCLUSIONS
Until recently, the numerous reports of the occurrence of pathogens in bark beetles
were mostly confined to morphological description of the pathogens. Relatively few
papers concentrated on the effects of natural or artificial infections in the hosts.
Horizontal transmission of pathogens is likely to be promising only between female
and male beetles of the parental generation, especially in polygamous species,
simply because of a bark beetle’s life pattern. Vertical pathogen transmission from
beetles of the parental generation to beetles of the filial generation is also
conceivable (trans ovum or in the course of maturation feeding). Infections
transmitted in eggs evidently remain unapparent till maturation of beetles into
adults. However, all efforts to find progressing infections in larvae and callow adults
failed. Natural per os infection in larval stage most probably doesn’t occur because
all the economically most important bark beetle species normally feed in a sterile,
not contaminated medium (phloem or xylem), and larvae of most of these species
avoid contact with other individuals. Investigations of the occurrence or prevalence
of pathogens in a bark beetle population vary widely due to the sampling period
(time of the year), host generation (parental or filial generation), and mode of
sampling (collecting beetles out of logs by hand, collecting beetles from a
306 R. WEGENSTEINER
pheromone trap or collecting beetles emerging through a longer period from logs),
and thus may influence the significance of results of infection data.
The evaluation of pathogenic effects in bark beetles can be tentatively only, there
are no precise records of numbers of dead beetles in the field (with regard to natural
mortality). Infections in bark beetles are not manifested by the way of deformation,
change of colour or surface, or of behaviour of infected animals; only fungal
infections are forming surface covers on dead animals.
There is uncertainty in indication of mortality of bark beetles with different
infections, but infected animals must have a loss of expectation of life even dead
bark beetles are not present in high numbers in the galleries, maybe they die during
swarming.
For microbial control it is necessary to inoculate the target insects sufficiently
(per os, via cuticle or trans ovum) to ensure successful infection. The time window
for this process, especially for artificial infection, is normally very short for bark
beetles, due to the relatively short swarming periods of beetles. After this, beetles
live hidden in the bark and are “protected” against inoculation, with the exception of
horizontal transmission between the breeding partners or of vertical pathogen
transmission. One possibility could be the use of pheromone traps, attracting beetles
to the traps and inoculating them with infectious material. Furthermore, use of
microbials against bark beetles can raise similar questions as in other cases,
concerning the possible side effects of pathogens in other insects, especially natural
enemies. Till now, there is no knowledge on non target infectivity of pathogens of
bark beetles to other insects including their predators and parasites, and there is no
knowledge of ability of migrating nematodes or mites to provide transport for any
bark beetle pathogen. In addition, the type of pathogen and control t strategy can be
aimed at short term control or can fulfil a longer term regulatory effect. In case of
entire absence of one pathogen species in the bark beetle population of a region, an
inoculative release of such a pathogen could be a good option.
Viruses could be very interesting for microbial control measures, especially from
the point of selectivity and effectiveness, as known from other insect species. At the
moment there is a lack of knowledge on infection process and efficacy of viral
infections, but the distribution of propagules in faecal pellets, could be useful for
field application (autodissemination). Even though several reports deal with bacteria
in bark beetles, no bacterium is known at the moment to act effectively in bark
beetles. Fungal pathogens look to be very promising candidates for microbial control
of bark beetles. A large number of pathogenic fungi have been described in bark
beetles and several were found to cause rapida mortality in laboratory experiments,
and may act as very efficient control agents. However, some of the
entomopathogenic fungi have the disadvantage that they act rather non-specifically.
Protozoa, especially microsporidia are known for their relatively slow action, but as
obligatory pathogens and as occasional vertically transmitted pathogens, this group
may be very important for long term regulation strategies.
Evaluating the efficacy of single pathogens is relatively easy based on laboratory
tests, but it is more of a problem to estimate actions of pathogens under field
conditions, and interactions between different pathogens and of pathogens with
other natural enemies (predators, parasitoids) is equally problematic. Survival of

resistant stages of pathogens in the environment of the host’s habitat is an important
point. Furthermore, most of the pathogens have a limited capacity to disperse by
their own action and must rely on physical and biotic factors for their dispersal.
Even if the number of pathogens isolated from bark beetles is relatively high,
few studies have dealt with practical control aspects using microbials in bark beetle
field populations. Therefore, there remains a great need to identify and measure the
scope of pathogens influencing bark beetle populations.
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Part 2
Bark Weevils
Chapter 13
TAXONOMY AND SYSTEMATICS OF BARK

WEEVILS
G. LEMPÉRIÈRE 1, A. MANTILLERI 2 & C. CONORD 1
1
Université Joseph Fourier, UMR CNRS 5553, Grenoble
2
Muséum National d'Histoire Naturelle, 55 rue Buffon, 75005, Paris
1. RECENT STATUS OF THE FAMILY CURCULIONIDAE

The family Curculionidae includes the majority of species described from the
Curculionoidea and it can be considered as the most derived taxonomic group of the
super-family which is also part of the most derived group among the Coleoptera.
During the second half of the last century, the concept of the Curculionidae family
changed with Crowson (1955) including a large number of taxa which are now
omitted from the group ; however he first formally mentioned the Scolytidae and
Platypodidae as sub-families. Later on, the use of cladistic methods further clarified
relationships between different groups of weevils.
Entire groups were then separated from the Curculionidae. It was the case for the
Dryophthoridae (=Rhynchophoridae) (Morimoto, 1962a, 1962b, 1976), and the
Ithyceridae that form a monospecific group (Morimoto, 1976; Sanborne, 1981).
After a study using the male genitalia, the Erirhinidae, Brachyceridae,
Cryptolaryngidae and Raymondionymidae were separated from the Curculionidae
Thompson, 1992). At the present time, only species that present male genitalia with
a gonatocera type are considered as Curculionidae. In the Curculionidae sensu
stricto, males have a manubrium which is smaller than the spiculum gastrale. If the
spiculum gastrale is absent, then the rostrum is also absent. The Platypodinae do not
follow this pattern because in this group, the sclerification of genitalia is very thin
and the spiculum gastrale is not visible. This new way of looking at Curculionidae
has been used by Alonso-Zarazaga and Lyal (1999) in their world catalogue of
families and genera of Curculionoidea.
317
317—330.
© 2007 Springer.
318 G. LEMPÉ RIÈ RE, A.M. MANTILLERI & C. CONORD
2. EXTERNAL MORPHOLOGY
A fundamental feature of the Curculionidae is the absence of specific external
characters and the only apomorphism that allows definintion of the Curculionidae
clade is based on a single character off the male genitalia. However, the
Curculionidae have a very unique shape.
The head is produced into a rostrum of very variable length and form. It can be
long and pointed in the genus Curculio or short and wide in the Otiorrhynchus. The
rostrum can be turned-down on the prosternum in the Cryptorhynchinae. The
antennae are located on the rostrum and are geniculate after the scape and have a
variable number of articles between 9 and 11. Eyes are present except for the
Torneuma that live in the soil or in cavities or caves.
The thorax: the prothorax is variable and can present a furrow to screen the
rostrum. The mesothorax is also variable with a scutellum which can be visible or
not and the elytra that are dorsally attached to this segment. The metathorax is
hidden by the elytra and the membranous wings are attached to it. Its ventral part
shows furrows that can vary according to the sex. Legs are also variable and tarsi are
usually cryptopentamere with four visible articles.
The abdomen consists of 9 segments with segments 8 and 9 modified and
forming the sclerified parts of the sexual organs. On the dorsal part, 7 segments are
visible under the elytra. On the ventral part, only 5 segments are visible, the two
missing segments being reduced and included in the metathorax. The first two
visible segments are more or less joined.
3. INTERNAL MORPHOLOGY
The digestive system is divided into three parts: the stomodeum with the oesophagus
including the crop and the proventricle , the mesenteron and the proctodeum. The
mesenteron often shelters symbiotic bacteria that have a cellulolitic role (Buchner,
1933). The proctodeum is connected to the excretory system which is composed of
the Malpighian tubules. There are six Malpighian tubules in the Curculionidae. The
classic respiratory system is composed of tracheae with access to the environment
through spiracles located on the thorax and the abdomen. The circulatory system
does not show real vessels and the « blood »fills up the general cavity and is put in
motion by a dorsal propulsive vessel. The nervous system is divided into a central, a
visceral and a peripheral system (Hoffmann 1950). The central system is formed by
a brain composed of three pairs of ganglia that innervate the eyes, the antennae and
the labrum and a double chain of ventral ganglia. The visceral system includes
dorsal ganglia that innervate the dorsal vessel, the genitalia and the spiracles. The
peripheral nervous system consists of hypodermic cells located at the base of
sensory hairs that cover the tegument. The muscles are well developed and complex.
Cephalic and thoracic muscles connected with mandibles for the first and legs and
wings for the second are very strong. There are also muscles in the abdomen that are
used during oviposition. Male genitalcopulatory sacs are composed of two testicles,
TAXONOMY AND SYSTEMATICS OF BARK WEEVILS 319
the accessory glands, the vas deferens, the seminal vesicles, the ejaculatory duct and
the aedeagus with the spiculum gastrale, tegmen and penis. Female genitals include
ovaries, acrotrophic ovarioles, the oviduct, the copulatory sac, the spermatheca, the
uterus, the vagina and the genitalia (ovipositor, spiculum ventrale and 8th abdominal
tergite).
4. PHYLOGENETIC ANALYSIS
Most recent works on the phylogeny of Curculionidea (Farell et al. 2002 ;
Marvaldi et al, .2002) using molecular analysis and new morphological data (larval
characters, internal morphology) and including a large number of samples of
Curculionidae in the analysis, show a weak resolution of the relationships within the
family.
For instance, it is not certain that the traditional Adelognatha and Phanerognatha
groups are monophyletic (Marvaldi, 1997).
The species of weevils listed as BAWBILT (Bark and Wood Boring Insects in
Living Trees) belong to the family Curculionidae. Recent work on the phylogenetic
relationships in weevils (Wink et al., 1997) mentions the two subfamily groups
Adelognatha and Phanerognatha for the species of Curculionidae. They have male
genitalia of the gonatocere type. Those species belong to the following six
subfamilies Cossoninae Schoenherr 1825 (genus Brachytemnus), Cryptorhynchinae
Schoenherr 1825 (genus Cryptorhynchus), Curculioninae Latreille 1802 (genus
Anthonomus), Mesoptiliinae Lacordaire 1863 (genus Magdalis) and Molytinae
Schoenherr 1823 (genera Hylobius, Pissodes, Trachodes) for the Phanerognatha
clade and Entiminae Schoenherr 1823 (genus Otiorrhynchus, Strophosoma) for the
Adelognatha clade (Lacordaire 1866). This last group is probably monophyletic with
several synapomorphies based on larval characters (Marvaldi, 1997) as well as
molecular characters (Wink et al,. 1997) or a combination of both (Marvaldi et al.,
2002). It is one the subfamilies of Curculionidae which is strongly supported
phylogenetically.
Curculioninae and Hylobiinae are heterogenous groups and their position in the
Curculionidae is not yet resolved.
The following status for the list of species could be proposed as below:
- Adelognatha
- Subfamily: Entiminae Schoenherr 1823
- Tribe: Otiorhynchini Schoenherr 1826
- Genus: Otiorrhynchus Germar 1822 (type species:Curculio rhacusensis
Germar 1822)
- Synonymies: Pachygasterr Germar, 1817 non Meigen,1803;
Loborhynchus Dejean, 1821; Panaphilis Dejean,1821;
Loborhynchus Schoenherr, 1823 non Dejean, 1821 ;
Otiorrhynchus Germar, 1824 non Germar, 1822.
- Sub-genera: Otiorrhynchus (s.st.) Germar 1824
Dorymerus Seidlitz, 1890
Tourniera Stierlin, 1861

Postaremus Reitter, 1912
- Species:
- O. (s.st.) arcticus Germar 1824
- Synonymy: O.(s.st.) monticola Germar 1824
- O. (s.st.) nigerr Fab.1775
- O. (Postaremus) nodosus MÅller 1764
- Synonymy: O.dubius Strîm,1783; the name dubius is still valid.
It is now among the sub-genus (Postaremus) Reitter, 1912.
- O .(Tourniera) ovatus L.1758
- O. (Dorymerus
( ) singularis L.1767
- Tribe: Brachyderini Schoenherr, 1826
- Genus: Strophosomus Schoenherr, 1823 (type species: Curculio
melanogrammus Forster, 1771). Strophosomus is not the
valid name for this species and Strophosoma Bilberg, 1820
must be used.
- Synonymies: Judolus Dejean, 1821; Strophosomus Schoenherr, 1823;
Bryssus Dejean, 1821; Strophosomum Gistel, 1856.
- Species:
- S. (s.st.) melanogramma Forster 1771
- Synonymies: S.(s.st.) coryli F., 1775; S.(s.st.) illibata
Boh.,1833; S.(s.st.) obesa Thoms., 1868 non Marsham,
1802; S.(s.st.) fagi Chevrolat, 1865.
- Species:
- S. (s.st.) capitata De Geer 1775
- Synonymies: S. (s.st.) obesa (Marsham, 1802); S.(s.st.) coryli
Boh.1840 non Fabricius 1775; S. (s.st.) fulvicornis Walton,
1846; S. (s.st.) desbrochersi Tournier, 1876; S. (s.st.) grisea
Tournier, 1876
- Phanerognatha
- Subfamily: Cossoninae Schoenherr, 1825
- Tribe: Onycholipini Wollaston, 1873
- Genus: Brachytemnus Wollaston, 1873 (type species: Rhyncolus
porcatus Germar, 1824).
- Species:
- B. porcatus Germar, 1824
- Tribe: Rhyncolini Gistel, 1856
- Species:
- R. (s.st.) aterr (Linnaeus, 1758)
- Subfamily: Cryptorhynchinae Schoenherr, 1825
- Tribe: Cryptorhynchini Schoenherr, 1825
- Genus: Cryptorhynchus Illiger, 1807 (type species: Curculio lapathi
Linnaeus, 1758
- Synomynies: Aracnipus Dejean, 1821; Arachnipes Villa & Villa, 1833;
Cryptorhynchidius Pierce, 1919; Eupterus Fiedler,
1941;Cryptorrhynchobius Voss, 1965
- Species:
- C .lapathi Linnaeus, 1758
- Subfamily: Curculioninae Latreille, 1802
- Tribe: Anthonomini Thomson, 1859
- Genus: Furcipes Bedel, 1884 (type species: Curculio rectirostris
Linnaeus, 1758). This name is not valid. It is a replacing
name for the genus Furcipus Desbrochers, 1868 which is
valid. Furcipes Bedel is then a synonym of Furcipus
Desbrochers which has a priority as being older. Furcipus
is a subgenus of the genus Anthonomus Germar, 1817.
- Genus: Anthonomus Germar, 1817
- Synomyny: ((Furcipes) Bedel, 1884
- Species:
- A. rectirostris L., 1758
- Subfamily: Mesoptiliinae Lacordaire, 1863
- Tribe: Magdalini Pascoe, 1870
- Genus: Magdalis Germar 1817(type species: Curculio violaceus L.,
1758
- Subgenera: - Magdalis Germar, 1817
- Aika Barrios, 1984
- Dagmalis Kìno & Morimoto, 1960
- Edo Germar, 1819
- Laemosaccidius Smreczynski 1972
- Odontomagdalis Barrios, 1984
- Panopsis Daniel, 1903
- Panus Schoenherr, 1823
- Porrothus Dejean, 1821
- Synomynies: Thamnophilus Schoenherr, 1823; Magdalinus Germar,
1843; Scaradamyctes Gistel, 1848.
- Species:
- M. violaceus L., 1758.
- Subfamily: Molytinae Schoenherr 1823
- Tribe: Hylobiini Kirby, 1837
- Sub-tribe: Hylobiina Kirby, 1837
- Genus: Hylobius Germar, 1817 (type species: Curculio piceus De Geer,
1875)
- Subgenera: - Hylobius Germar, 1817
- Synonymy: Hypomolyx LeConte, 1876,
- Callirus Dejean, 1821 (type species: Curculio abietis

L., 1758
- Synomynies: Hylobitelus Reitter, 1923; Polyaunbus Kìno, 1934.
- Species:
- H. abietis L.1758
- H. pinastri Gyll.1813
- Tribe: Pissodini Gistel, 1856
- Sub-tribe: Pissodina Gistel, 1856
- Genus: Pissodes Germar, 1817 (type species: Curculio pinii L.1758)
- Synonymy: Piniphilus Dejean, 1821
- Subgenera: Pissodes Germar, 1817 Epipissodes Voss, 1956
- Species:
- P. castaneus (DeGeer, 1775)
- P. harcyniae (Herbst, 1795)
- P. piceae (Illiger, 1807)
- P. pini (L.1758)
- P. piniphilus (Herst.1797)
- P. scabbricollis Miller, 1859
- Tribe: Acicnemidini Lacordaire, 1866
- Genus: Trachodes Germar, 1824 (type species: Curculio squamifer
Paykull, 1800)
- Synonymies: Blastophila Gistel, 1856; Metrachodes Marshall, 1948
- Subgenera: - Trachodes Germar, 1824
- Species:
- T. hispidus (L., 1758)
- Atrachodes Morimoto, 1962
The names and synonymies of the species as well as the names of authors
together with the dates have to be clearly and carefully mentioned and identified in
order to avoid any misinterpretation as recently observed in evolutionary works on
bark beetles (Kelley et al., 1999).
5. GEOGRAPHICAL DISTRIBUTION
With 9 genera and 22 species, the BAWBILT weevils are among the largest beetle
families recorded in Europe. The geographical distribution of most species has not
been fully covered and information is fragmentary for the majority of them.
5.1. Adelognatha
5.1.1. Genus Otiorrhynchus:

This is one of the largest weevil genera in Europe and it is represented in the
BAWBILT list with 5 species.
O. (s.st.) arcticus is known to be a subalpine or alpine species with records from

the Pyrenees and the Massif Central (Hoffmann, 1958). Adult weevils live under
mosses and stones and the larvae feed on the roots of various herbaceous plants and
sometimes on the roots of young seedlings as recently mentioned on larch in Iceland
(Halldorsson et al., 2000).
O .(s.st.) nigerr and O. (Postaremus) nodosus are mentioned as pests in forest
nurseries, specially on spruce and pine seedlings in central and eastern Europe and
in Sicily (Hoffmann, 1958). More recently O. (s.st.) nigerr has been recorded in
northern Europe (Lunderstadt, 1981) while O. (Postaremus) nodosus was causing
problems to natural regenerations of Scots pine in Lapland (Suoheimo, 1984).
O. (Tourniera) ovatus is also a pest of forest nurseries. This species is
polyphagous and widely distributed throughout Europe and present in North
America. Damage has been mentioned in the past on spruce plantations and in forest
nurseries in Czechoslovakia (Srot, 1979)and in the German Democratic Republic
(Bogs and Braaschd, 1988). Adult weevils feed on flowers of various plants.
O. (Dorymerus
( ) singularis larvae are rhizophagous (Schauermann, 1977). Adult
weevils are polyphagous and feed on beech, alder, walnut, spruce, pines. This
species is recorded from western and Central Europe, in Baden-Wurtemberg for
instance where it has damaged young oak and lime plantations (Bogenschutz, 1982).
5.1.2. Genus Strophosoma:

There are 6 species in Europe all parthenogenetic. Two of them are harmful to
forestry.
The larvae of S. melanogramma feed on roots of various herbaceous plants and
also on beech and oak while the adults ffeed on leaves, shoots and buds of various
plants including oak, walnut, maple, hawthorn, pine.
Recent damage has been recorded in forestt nurseries and reforestation sites, in
the UK (Parry, 1983; Parry et al., 1990; Stork et al., 2001), but also in southern
Sweden on beech, oak and Norway spruce (Lîf, 2000; Prieme et al., 2000), in the
mountain regions of Germany (Biernath et al., 1996), in central France (Lemperiere
pers obs.). Outbreaks of the weevil were mentioned in the Czech Republic in 1995
on beech, Norway spruce and Sorbus aucuparia (Urban, 1995).
The larvae of S. capitata feed on the roots of heather and ericaceous plants and
the adults on oak, beech, arbutus, hornbeam.
Damage is recorded from central France on oak (Rougon et al., 1995), from
Norway on Scots pine planted after forest fires (Solbraa, 1983). In Poland, several
observations mention damage on young Scots pines (Szmidt and Stachowiak, 1980,
Stachowiak, 1991, 1992) but also on hazelnuts (Gantner, 2001) and birch plantations
(Korczynski, 2001).
5.2. Phanerognatha
5.2.1. Genus Brachytemnus

Adults and larvae of B. porcatus live on firs, spruces and pines like Pinus maritima,
P .laricio, P. halepensis of the Mediterranean area. The insect is also mentioned
from central Europe (Hoffmann, 1958).
5.2.2. Genus Cryptorhynchus

The poplar weevil C .lapathi is the only species of the genus in northern and central
Europe. It is also found in Siberia and Japan (Hoffmann, 1958).
Larvae and adults live in the wood of Salicaecae and Betulaceae : Salix caprea,
S. viminalis, S. purpurea, S. triandra, S. fragilis ; Populus alba, P. canadensis, P.
virginiana, P. nigra, P. tremula.
Adults feed on the bark while larvae tunnel in the inner bark. Damage is
recorded on young trees as well as mature stands all over Europe with records from
Italy on poplars (Allegro 1989, 1990, 1997; Arru, 1977; Cavalcaselle and Allegro,
1986; Giorcelli and Allegro, 1999; Lapietra and Allegro, 1987, 1990; Montermini et
al., 1998; Pollini, 1990; Verenini, 1984), from Spain on Salix (Anton, 1979; Sabate
and Rojo, 1982), from south-east and south-west France on poplar plantations
(Attard, 1978, 1979), from Croatia (Jodal, 1987) and Hungary (Prenner et al., 1983;
Szontagh, 1985). In central Europe the weevil is more polyphagous with records on
Salix in Poland (Czerniakowski, 2001) and southern Russia (Maksimenko et al.,
2001) on Alnus (Chlodny, 1982) in Poland and on Norway spruce in
Czechoslovakia (Kristek, 1989). In the north west of Europe the weevil was
observed on poplar in the Netherlands (Moraal, 1996) and Salix viminalis in Ireland
(Neeman and Kennedy, 1989).
5.2.3. Genus Anthonomus

A .rectirostris is found in northern and central Europe and also found in Siberia and
Japan. Larvae feed in the kernel of many wild and cultivated cherry trees : Cerasus
padus, C. avium, C. vulgaris (Holighaus and Dahlbender, 1995).
5.2.4. Genus Magdalis

M.violaceus is known from Central and 'boreal' Europe, Switzerland, the Italian
Alps and Belgium and live on Picea excelsa and Abies pectinata. It could be
considered as a saproxylic weevil as living on dying or dead trees and/or dead parts
of trees (branches).
Pupal chambers penetrate deep in the wood as in Pissodes species (Hoffmann,
1958).
5.2.5. Genus Hylobius

Of the four species of the genus found in Europe, H. abietis and the somewhat
smaller H .pinastri are very hard to tell apart. They feed on the cambium and bark of
many conifers. H. abietis is very common in Europe from Siberia to northern Spain
and its distribution and spread are referred to sylvicultural practices (clear cuttings
and reforestation programmes).It is considered as the worst pest of young conifers.
There are numerous records of the presence of the insect in its distribution zone,
from Siberia (Gourov, 1994), Russia (Charitonova, 1965, Lur'e, 1966), the nordic
countries (Bejer-Petersen et al., 1962), including Norway (Christiansen 1971),
Sweden (Eidmann, 1964 , 1971, 1981; Langström, 1982; Nordenhem, 1989),
Finland (Langström, 1985), Eastern Europe including Bulgaria (Cankov, 1970), the
Czech Republic (Zumr and Stary, 1994), Poland (Sierpinski, 1972; Szmidt and
Korczynski, 1983) , the north west of Europe with the Netherlands (Elton, 1964), the
United Kingdom (Stoakley, 1968; Bevan, 1987), Belgium (Nef, 1992), France (
Hoffmann, 1958; Malphettes, 1966),
H.pinastri is less abundant and has a more Nordic distribution ( Eidmann, 1974,
Lindelow et al., 1993; Langström, 1982). H. piceus is observed on larch and Scots
pine, in Siberia, northern Europe, (Eidmann, 1974; Langström, 1982). This rare
species is known from the Alps in the region of the Queyras (Lemperiere, pers.
obs.).
5.2.6. Genus Pissodes

The genus is represented by 8 species in Europe. This genus comprises some
forestry pests.
P .castaneus is known from southern France (Lieutier et al., 1997), Turkey
(Tozlu, 2001), Moldova (Poiras, 1991) and Russia (Kulinich and Orlinskii, 1998) on
different pine species as a secondary pest.
P.harcyniae was recorded as a secondary pest on Pinus silvestris, Picea excelsa,
Abies pectinata. It is mentioned as rare in eastern and southern France (Hoffmann,
1954) but is more common in central Europe ( Kula and Zabecki, 1997, 2000).
P.piceae lives on silver firs and sometimes on spruce and is primarily a montane
species. It is common in all the mountains of continental Europe where it can cause
damages on ailing and weaken trees. It is mentioned in Italy (Tiberi, 1997,
Moriondo and Tiberi, 2000), in the eastern part of the Carpathian mountains in
Romania (Simionescu, 1995; Simionescu et al., 1998), in Poland (Podlaski, 1996,
2002; Starzyk, 1996), in Bulgaria (Tsankov, 1994) and central France (Lemperiere,
1987).
P .pini is common in central and southern Europe, in the Alps on Scots pines
where it feeds on the top of trees. It is also mentioned on Pinus uncinata in the
Pyrenees (Hoffmann 1954) and in Germany (Habermann and Geibler, 2001)
.P. piniphilus is known from central Europe, in Germany (Habermann and
Geibler, 2001), in Austria (Cecht and Tomiczek, 1996), in Poland (Kurowska and
Falencka-Jablonska, 1994, Witrylak, 1995) and northern Europe, in Estonia (Luik,
1994; Voolma, 2001), Finland (Pappinen and Weissenberg, 1996) and also Russia
and Siberia (Bogdanova, 1998; Demakov, 1994, 1996, 1998; Maslov et al., 1999) on
Scots pine and Abies nordmanniana. The insect develops on dying trees (Karoles,
1992) and is considered as rare in France (Hoffmann, 1954).
P scabricollis is known as a secondary pest on spruce in central Europe
(Oppermann, 1985).
5.2.7. Genus Trachodes

This genus holds half a dozen of not very well known species. T .hispidus lives in
the thin and dry branches of oak, beech and birch. They are recorded from Northern
Europe, Switzerland and Belgium (Hoffmann 1958).
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Pissodes piniphilus (Herbst) (Coleoptera, Curculionidae) in Estonia. Journal of Forest Science, 47
(Special Issue 2, 171-73.
Wink, M., Mikes, Z. & Rheinheimer, J. 1997. Phylogenetic relationships in weevils (Coleoptera:
Curculionoidea) inferred from nucleotids sequences of mitochondrial 16S rDNA.
Naturwissenschaften, 84, 318-21.
Witrylak, M. 1995. Biologia, ekologia i znaczenie gospodarcze wgryzonia jodlowca Cryphalus piceae
(Ratz.) (Coleoptera, Scolytidae) w gorskich drzewostanach Lesnego Zakladu Doswiadczalnego w
Krynicy. Sylwan, 139, 51-66.
Woods, S.L. 1986. A reclassification of the genera of Scolytidae (Coleoptera). Great Basin Naturalist
Memoirs, 10, 1-126.
Zumr, V. & Stary, P. 1992. The occurence of the large pine weevil Hylobius abietis L., in individual
forest zones. Forest Ecology and Management, 51, 251-58.
Chapter 14
GENERAL BIOLOGY AND LIFE CYCLES OF BARK

WEEVILS
K.R. DAY 1, G. NORDLANDER

R 2, M. KENIS 3 & G.
HALLDORSON 4
1
University of Ulster, Coleraine, Northern Ireland, UK-BT52 1SA, UK
2
Swedish University of Agricultural Sciences, P.O. Box 7044, S-750 07 Uppsala,
Sweden
3
CABI Bioscience Laboratory, 1 Chemin des Grillons, CH-2800 Delémont,
Switzerland
4
Forest Research Station, Mogilsa Mosfellsbaer, IS-270, Iceland
1. INTRODUCTION
The large pine weevil, Hylobius abietis (L.) is the single most important insect pest
of reforestation in northern and western Europe. The number of scientific papers
published annually on this insect continues to increase in response to the need to
find long-term solutions to the problems it causes. Its common name in English
suggests that it is one of the larger weevils found feeding on conifers. Adults are
about 8-14mm long (Eidmann 1974). The large pine weevil breeds in conifer
stumps but feeds on conifer seedlings, so its reputation as a pest is greatest in
countries which employ clear-cut plantation forestry.
Other species of Hylobius, H. pinastri Gyll. and H. piceus De G. occur in large
parts of Europe (Eidmann 1974; Långström 1982). The biology of H. pinastri is
similar to that of H. abietis (Nordlander 1990), although H. pinastri appears to
prefer moist areas dominated by spruce (Långström 1982; Nordlander 1990).
Hylobius pinastri is moderately abundant in Scandinavia and makes up about a
quarter of the weevil population (with H .abietis) in Estonia (Luik and Voolma
1989). Hylobius piceus is less common and mostly found in moist forests, almost
never on clear-cuttings. It breeds in the root collar of living conifer trees and the
adults are seldom observed feeding on seedlings (Eidmann 1974; Å. Lindelöw pers.
comm.). A fourth European species, Hylobius transversovittatus (Goeze), lives in
the roots of a perennial plant Lythrum salicaria, and is hence of no interest in this
331
331–349.
© 2007 Springer.
332 K.R. DAY, G. NORDLANDER, M. KENIS & G. HALLDORSON
context, but is used for biological control of its introduced host in the United States
(Kok et al. 1992).
Several other economically important species of the genus Hylobius occur
outside Europe ((H. assimilis Boheman, H. congener Dalla Torre et al., H. pales
(Herbst), H. radicis Buchanan, H. warreni Wood, and H. xiaoi Zhang). Lynch
(1984) reviews the biology of the pales weevil ((H. pales) and Cerezke (1994) the
biology of H. warreni in North America. There are clearly differences between
members of the genus according to where they breed. H. radicis, H. warreni and H.
xiaoi breed in the root collar region or lower stem of healthy hosts and assimilis in
small, living lateral roots, whereas H. pales and H. congenerr breed in roots of dying
or recently dead trees, just as H. abietis does.
Eight Pissodes species occur in Europe (Kudela, 1974). Pissodes castaneus De
Geer (= notatus F. ), P. pini (L.) and P. piniphilus (Herbst) attack pine stems. They
are widely distributed in Europe and, for P. castaneus, in North Africa. Pissodes
piceae (Illiger) is a pest of fir stems and occurs throughout the distribution of its
host, Abies alba. Three species feed on spruce stems; P. harcyniae (Herbst) is
distributed from France to Siberia and Scandinavia, P. scabricollis (Miller) occurs in
Central and eastern Europe, and P. gyllenhali (Sahlberg) is found mainly in
Northern Europe. The eighth species, P. validirostris (Sahlberg) attacks pine cones
and will not be included in this review.
Kudela (1974) provides a review of the knowledge on the biology and ecology of
the eight Pissodes spp. until the late 1960’s. Since then, new information has been
provided for P. castaneus, mainly in Southern France (Carle, 1967, 1973, 1974;
Alauzet, 1972a, 1972b, 1973, 1977, 1984, 1985, 1986; Lauga and Alauzet, 1983).
Observations were made also on P. piceae in France (Lempérière and Malphettes,
1987; Lévieux et al., 1994) and Poland (Starzyk, 1996; Podlaski, 2002), and on P.
piniphilus in Estonia (Riis, 1975; Luik, 1994). In the last 30 years, no research has
been published that specifically focused on the biology of P. pini and the three
spruce Pissodes spp., which demonstrates their minor importance as forest pests.
The genus Otiorrhynchus is a homogenous group divided into four subgenera
and includes around a thousand species throughout the world. The distribution of the
genus is related to cold and temperate climates in both hemispheres (Lempérière,
1999). The weevils are wingless and nocturnal and most species are
parthenogenetic. The larvae are serious pests in agriculture and forestry in many
countries in Europe (Dolmans 1992). Four Otiorrhynchus species: O. arcticus
(Fabr.), O. nodosus (Müller), O. singularis (L.) and O. sulcatus (Fabr.) are
recognised as BAWBILT species. The black vine weevil, Otiorrhynchus sulcatus,
which is a pest in nurseries, the clay coloured weevil, O. singularis, which is a pest
in nurseries and forest regeneration and O. arcticus andd O. nodosus which are pests
in afforestation (Bejer-Petersen 1979; Bevan 1987; Van Tol 1993; Harding et al.
1998; Halldórsson et al. 2000). There exists an extensive literature on the black vine
weevil, especially the biology of the larvae, (Montgomery and Nielsen 1979;
Stenseth 1976,1979), whereas the other species have received much less attention.
Much of the information, given below, on the biology of these insects is therefore
based on existing knowledge of the black vine weevil.
BIOLOGY AND LIFE CYCLES OF BARK WEEVILS 333
2. HYLOBIUS ABIETIS
2.1 Adult feeding

The adult pine weevil feeds on the young stem of a conifer transplant where there is
no competition with Hylastes species, which mainly feed from the root collar down
(Scott and King 1974). While this represents the sole source of economic damage
from the weevil, conifer seedlings do not constitute its main food supply. Extensive
feeding also occurs in the crowns of mature coniferous trees and on their roots
(Örlander et al. 2000, 2001). Where such trees are present as shelterwood, this
reduces the attention weevils give to seedlings (Örlander et al. 2001; Nordlander et
al. 2003a, b). Seedlings with a stem diameter of 3-8mm at planting are more
vulnerable to damage by pine weevils than larger seedlings (Thorsén et al. 2001).
Irrespective of stem diameter, mortality due to pine weevil feeding is generally
higher for seedlings than for cuttings (Hannerz et al. 2002). Previous damage on
seedlings strongly increases the risk of subsequent attack by pine weevils due to the
release of attractive host volatiles (Nordlander 1991; Björklund et al. 2003). The
likelihood of attack is also strongly affected by the environment immediately around
the seedling. Both humus and vegetation provide cover for pine weevils and
encourage feeding in their presence, whereas seedlings in bare mineral soil are
largely avoided as food sources (Christiansen and Bakke 1971, Björklund et al.
2003; Örlander and Nordlander 2003).
A pine weevil eats about 0.2 cm2 of bark per day (Pohris 1983; Bylund et al.
2004), but this depends on the species of conifer, the depth of bark and temperature.
Given twigs of Pinus sylvestris, a preferred host, a pine weevil may consume an
average of 0.36 cm2 per day at 20oC, five times as much bark surface area as at 10
o
C, nearly twice as much as Picea abies (at 20oC) and more than ten times the bark
of Fraxinus exelsiorr (Leather et al. 1994). Although the weevil may consume bark
of broadleaved trees (Manlove et al. 1997), they are usually ignored when an
alternative conifer is available. Differentt conifer species provide food of varying
quality, e.g. the preoviposition period has been shown to vary between 11.8 and 15.5
days at 20oC depending on the conifer species consumed by the females (Wainhouse
et al. 2001). The feeding rate and amount of bark removed depend upon weevil size
and total nitrogen content of bark (lower N means more bark is consumed). Also,
not all bark material removed is consumed (Wainhouse et al. in press).
2.2 Behaviour and dispersal

The pine weevil is strongly affected by air temperature, humidity and light
(Christiansen and Bakke 1971; Havukkalaa and Selander 1976). The activity of
weevils is stimulated by increases in temperature up to 25 oC (Christiansen and
Bakke 1968; Pohris 1983). This may affect their feeding rate in parts of the forest
environment which are differentially shaded (Örlander et al. 2000; Nordlander et al.
2003b). Light and humidity reactions are largely dependent on the physiological
(reproductive) stage of H. abietis (Havukkala and Selander 1976). Female weevils
avoid both high and low humidities, but are generally hygronegative and more so
than males (Havukkala 1979). In areas with high humidity, spatial displacement is
brought about by an increase in walking speed and decrease in the amount of turning
per unit time (Havukkala 1980). Under uniform humidity and temperature
conditions pine weevils move faster on mineral soil (sand) than on organic humus
(Kindvall et al. 2000), possibly to avoid being exposed to excessive solar radiation
(Björklund et al. 2003) or to the increased risk of predation during daylight hours. In
the field, a stable diurnal rhythm of locomotor activity is maintained, but modified
by weather conditions. Sibul et al. (1999) found that weevils were relatively passive
at noon but increased their activity in late afternoon. The periods of greatest activity
were correlated with high relative humidity (85-95%) and a moderately warm
temperature (17-21oC) which generally corresponded to twilight periods (Sibul et al.
1999). During a hot period, the activity of weevils in an exposed site was limited to
twilight and dark hours (Christiansen and Bakke 1971).
Migration by flight is an important way in which the pine weevil moves within
large forest mosaics, where clear-cut patches appear regularly as part of the forest
exploitation regime. In Scandinavia, weevils leave overwintering sites in spring at
temperatures > 8-9 oC and the flight period occurs during late May and early June
(Eidmann 1968; Solbreck and Gyldberg 1979). The proportion of male and female
weevils with well-developed flight muscles is already high at the beginning of May
in field populations and flight muscle development is completed ahead of sexual
maturation (Nordenhem 1989). Eggs start to develop in the oviducts during the
spring migration period (Christiansen 1971a), and after a short time of feeding all
females are in the reproductive phase (Örlander et al. 2000).
Figure1. Adult Hylobius abietis in flight

i (photographed by Niklas Björklund)
Under good conditions for migratory flight (Fig 1), individual weevils will
undertake most of their flight activity, including their longest flights, in the first 10
days of their migratory period (Solbreck k 1980). They respond positively to light and
readily climb upwards to initiate flights. There seems to be quite a range of variation
in flight duration among individuals, so that some may fly for half an hour and
others not at all. Weevils are able to fly when temperatures exceed 18-19 oC and at
low wind velocity of 3-4 m s-1 (Solbreck and Gyldberg 1979). It appears that at take-
off, pine weevils head into the prevailing wind, then turn to fly downwind
continuing to fly upwards, thus reaching heights of 30-50m, above the canopy of the
forest. Most flight is undertaken at wind speeds of < 3 m s-1. Indirect estimates of
flight distance, deduced from knowledge of flight duration and direction in relation
to air movement, have been made by Solbreck (1980). The estimates for an
experimental population form a frequency distribution which suggests that 50% fly
1.5 km during the entire flight period, while some individuals are capable of
covering 80 km. Nilssen (1984) trapped H. abietis in Finland at least 30km from its
nearest source, and possibly a source 85km away, from whence it may have arrived
with wind assistance.
During the migratory phase, host volatiles are used by weevils to locate areas
with an abundance of freshly felled coniferous trees (Nordlander et al. 1986;
Nordenhem and Eidmann 1991). Flight muscle degeneration follow the flight
period, so that most older weevils lack flight muscles (Nordenhem 1989). As the
migratory phase ends, weevils tend to become photonegative.
2.3 Reproduction and oviposition

The pine weevil is synovigenic. Reproductive maturation in female weevils is
signalled by a progression and later a demise in the status of the reproductive system
(Christiansen 1971a). Recognisable stages in the reproductive cycle are:
1a Juvenile (prereproductive) – short ovarioles, no oocytes
1b Developing juvenile – extended ovarioles, developing oocytes
2 Fertile – large ovarioles, oocytes in oviducts, corpora lutea present
3 Senile– extended ovarioles, no oocytes, corpora lutea present
4 Redeveloping - extended ovarioles, developing oocytes, corpora lutea present
These stages are illustrated in Christiansen (1971a) and Nordenhem (1989).
Pine weevils meet and copulate often (Nordlander et al. 1986; Tilles et al. 1988).
No sex pheromone that bring the sexes together have been found in the pine weevil
(Nordlander et al. 1986; Tilles et al. 1986; Zagatti et al. 1997), but there is a close-
range mating stimulant present on the body surface of females and young males
(Tilles et al. 1988). In courtship, these function in concert with stridulation and
tactile signalling by the male (Selander and Jansson 1977; Selander 1978).
Eggs are reported to be laid singly or in irregular groups in niches excavated in
the bark below ground level (Eidmann 1974; Scott and King 1974). However,
Nordlander et al. (1997) show that eggs are laid in the bark of roots mainly when the
surrounding soil is likely to dry out. More consistently, eggs are laid in the soil and
first instar larvae migrate to the bark of conifer roots. Two explanations for this
behaviour are 1) that eggs avoid conspecific cannibalism or predation, or 2) newly
hatched larvae are better than adults at locating suitable larval feeding sites
(Nordlander et al. 1997).
Under laboratory conditions, most eggs were laid near the surface of the soil
(moist sand) to depths of 10cm, with only 8% laid at depths of 40-60 cm (Pye and
Claesson 1981). In peat soil in the field a considerable proportion of the eggs were
found under the main roots at about 20-30cm below the surface (Nordlander et al.
1987). However, in a hard-packed substrate found in the field, oviposition occurred
entirely within 5cm of the surface (Pye and Claesson 1981). Larval populations have
been found mostly within 5cm of the surface,
f with only 2% below 15cm (Henry and
Day, 2001).
The following terminology (Bejer-Petersen et al. 1962; Nordenhem 1989) is
used to denote the age of clear-cuttings in which breeding occurs. (A) is the growing
season immediately following cutting, and (A+1), (A+2) etc. are subsequent years.
Oviposition by migrant weevils on first year (A) breeding substrate occurs in the
summer months, between June and August (Lekander et al. 1985). The preferred
temperature for oviposition is 22oC (Christiansen and Bakke 1968). The frequency
of eggs laid is unimodal during this period with a peak in late June (Nordlander et al.
1997) or somewhat earlier or later depending on prevailing climate. Reproduction
ceases in August, coincides with a sudden drop in weevils caught by traps
(Nordenhem 1989), and is probably inducedd by decreasing daylength (Örlander et
al. 1997). No eggs are found in the oviducts in autumn and the oocytes that are
present in the ovarioles are smaller than those in early summer (Christiansen 1971a).
Such weevils, if they survive winter hibernation, are destined to resume
vitellogenesis and ovulation in the following year. Fat reserves may be lower, and
therefore fertility may also be lower, in the second season.
The realised fecundity of female pine weevils during the first season has been
estimated to be approximately 70 eggs (Bylund et al. 2004). The fecundity of
weevils depends on female size and the bark species on which adult feeding has
taken place. Three or fourfold differences in fecundity (22-71 eggs) were reported
by Wainhouse et al. (2001). Both subsequent egg and larval size and egg shape were
also affected by conifer species; egg volume varied between 0.405 – 0.470 mm3.
Feeding by larval stages and particularly maturation feeding by adult female weevils
are key factors in reproductive success.
2.4 Larval feeding

Pine weevil larvae feed under the bark of roots of recently killed or dying conifer
trees and in fresh stumps. Their rate of development and mortality is dependent on
the conifer species acting as host (Thorpe and Day 2002). The effects of host species
are discussed in Chapter 16.
Freshly hatched larvae migrate from ovipostion sites in soil to suitable feeding
sites in bark (Nordenhem and Nordlander 1994, Nordlander et al. 1997). Older
larvae can also move between roots (Nordenhem and Nordlander 1994), a behaviour
which represents a trade-off between improved larval food and the risks of predation
by ground beetles (Salisbury and Leather, 1998).
The larva makes a long tunnel with irregular orientation, and which increases in
diameter with larval size (Schwerdtfeger 1970). Feeding occurs in the cambial
region and the larva constructs ventilation ducts to the surface (Scott and King
1974). In thick-barked roots pupal chambers may be found in the bark, but where the
bark is thin, the larva excavates an oval chamber inside the wood, and closes the
entrance hole with a plug of small chips resulting from its boring activity. The fully
grown larva may be 9.5-16mm in length (Kangas 1959). Generally, the larvae tunnel
downwards after hatching where they may be better protected for overwintering
(Pye and Claesson 1981) although the depth to which they go may depend on
substrate and climate (Henry and Day 2001).
2.5 Duration of development and longevity

There are five larval instars (Bejer-Petersen et al. 1962; Christiansen 1971b). The
rate of development from egg to pupa varies with temperature; in warm dry
conditions, an egg laid in the spring (A) may become a fully developed final instar
larva by late autumn in the UK (Scott and King 1974). This developmental schedule
may produce an adult weevil by late May in the following year (A+1), although
cooler temperature commonly delay emergence until July to September. In the
Nordic countries most affected by the pine weevil (Denmark, Sweden, Norway and
Finland), the duration of development tends to be longer than in the UK, but usually
the time between generations is two years (Bejer-Petersen et al. 1962). Three or four
year life cycles are associated with cooler climates of northern Scandinavia. The
time of oviposition (earlier or later in the summer) is partly responsible for the
pattern of subsequent larval development and whether the life cycle is completed in
one, two or three years (Lekander et al. 1985). Temperature of the breeding
substrate ultimately determines the length of the developmental period. Whether a
breeding site is shaded or insolated can result in the developmental time being
amplified to two years rather than one (Bakke and Lekander 1965; Bejer-Petersen
1975; Kuziemska-Grzeczka 1984). Shelterwood can significantly prolong larval
development. Von Sydow and Örlander (1994) found earlier emergence of pine
weevils on sites with less than 80 shelter trees ha-1 than on sites with denser shelter
trees.
Facultative pre-pupal diapause experienced by larvae in pupal chambers, is
induced when final instar larvae are exposed to temperatures below a threshold of
21oC (Eidmann 1963, 1964; Christiansen 1971b). Termination of diapause has not
been studied in detail, but diapause of larvae developing at 12 oC appears to be
broken 6 months after oviposition (Christiansen 1971b).
It is alleged that adult weevils of the new generation may appear and reproduce
already in year A+1 in the UK (Scott and King 1974). In southern Scandinavia the
new generation weevils either emerge and feed in late summer year A+1 or they
remain in the pupal chamber until spring A+2 (Nordenhem 1989). In both cases they
remain prereproductive until just after migration to new sites in year A+2 (Örlander
et al. 2000). As oviposition occur also on yearr A+1 by weevils of the parent
generation that have overwintered, new generation weevils appear also in late
summer year A+2 and in spring year A+3 (Nordlander 1987; Nordenhem 1989).
Adult abundance varies throughout the year according to these patterns of
emergence and migration to sites with fresh breeding material (Örlander et al. 1997).
Typically, weevils are most abundant during the summer year A, in summer and
autumn year A+1, and in spring year A+2. Due to oviposition year A+1 and delayed
development of part of the population pine weevils are often abundant on clear-
cuttings until year A+3 (Örlander et al. 1997)
2.6 Overwintering
Diapause occurs in the final larval instar and its incidence depends on the
temperature experienced during this stage (Eidmann 1963, 1964). Larvae that have
reached the final instar before autumn will overwinter in diapause. Younger larvae
hibernate in a quiescent state and reach the final instar in the following summer
(A+1) when pupal development is completed. In northern Scandinavia the larvae
may pass through yet another winter in diapause. Overwintering larvae tolerate
temperatures of –12 oC on average, and can survive temperatures as low as –19 oC
(Luik and Voolma 1989). The supercooling point is generally higher than that for
bark beetles and they do not survive prolonged periods at -15 oC (Luik and Voolma
1989). However, with a snow covering on the ground for insulation, there is
generally likely to be little mortality in their natural environment in most regions.
Overwintering of adults takes place eitherr in the pupal chamber or in the litter by
those adults that have left the pupal chamber already in late summer and spent some
time feeding before hibernation (Nordenhem 1989). Adults that have already been
reproductive for one season may overwinter in the litter several times and reach an
age of up to four years (Eidmann 1979).
2.7 Monitoring and Population Studies

There have been no published studies off pine weevil population dynamics, although
frequent attempts have been made to monitor populations of adults at clear-cut sites
during the period of conifer transplant vulnerability to attack. Freshly cut billets of
coniferous trees have proved successful in attracting weevils in proportion to their
abundance (Långström 1982; Wilson and Day 1995, 1996; Wilson et al. 1996; Zumr
and Stary 1993). Örlander et al. (1997) argue that there are drawbacks with this
method; natural host material can vary in its attraction to weevils, weevils are not
arrested permanently, and standardisation of recorded weevils is problematic. To
overcome these problems, Nordlander (1987) has introduced a more standardised
approach based on a chemically-baited, covered pitfall trap (Nordlander 1990; Zumr
and Stary 1994; Lindelöw et al. 1993). The use of this bait also has a drawback in
that pre-reproductive weevils emerging in late summer are not attracted to the traps
(Nordenhem and Eidmann, 1991). However, it aappears that this can be advantageous
in enabling separate monitoring of a parent population in decline at a time when it is
present alongside a new generation of adults (Örlander et al. 1997). To catch pine
weevils in all phases in a fairly well standardized manner one may use the covered
pitfall traps baited with equally-sized stem or branch pieces taken from one tree
individual (Nordenhem and Eidmann 1991; Nordlander 1991).
An emergence trap devised specifically for use with pine weevils emerging from
stumps on spruce clear-cuttings, provides a method for monitoring temporal patterns
of emergence and for estimating on-site overwintering densities of weevil
populations (Moore 2001). The trap is highly efficient at capturing weevils,
regardless of their age, and has been used as an alternative to stump excavation for
the estimation of emergent adult population density (Moore et al. 2003).
Relative measures to estimate larval population density have been devised and
calibrated by examining bark on excavated stumps (Henry 1995; Henry and Day
2001). Samples of bark of known surface area within 10 cm of the soil surface and
within 70 cm of the trunk, could be used to estimate a known fraction of the larval
population (Henry and Day 2001). More recently absolute estimates of larval
populations have been made (Moore et al., 2003) and time of year and time of
felling were both shown to influence population size, spatial distribution and
development in stumps, as well as emergence from stumps. In this study ‘potential’
adult emergence was estimated to be between 46,400 and 170,825 H.abietis ha-1.
This is in close agreement with other estimates of adult population density on clear-
cuttings in the UK, reaching levels between 150,000 ha-1 (Heritage 1996) to 220,000
ha-1 (Leather et al. 1995) Absolute estimates of immigrant weevil populations on a
fresh clear-cutting and an adjacent shelterwood (A+1) in Sweden, have resulted in
much lower densities, about 14,000 weevils ha-1 (Nordlander et al. 2003a).
3. PISSODES
S SPP.
3.1 Host range and host tree preference

All European Pissodes spp. are restricted to a single host tree genus, unlike some
North American species, e.g. P. strobi (Peck) or P. nemorensis, which commonly
attack pine and spruce species (O’Brien, 1989). There are, however, single reports of
P. castaneus on spruce and larch, and of P. pini on spruce (Kudela 1974). Within the
host genus, Pissodes spp. are usually rather polyphagous. For example, although P.
piceae was originally restricted to silver fir, Abies alba, it is now commonly found
on introduced fir species, A. grandis, A. nordmanniana and A. nobilis. P. castaneus
and P. pini are found on nearly all pine species within their distribution range.
Nevertheless, Carle (1973) and Alauzet (1984) found significant differences in the
reproductive performance of P. castaneus fed and reared on different pine species.
P. piniphilus seems to be restricted to Scots pine, Pinus sylvestris and, occasionally,
to white pine, P. strobus. The natural host of the three spruce-feeding Pissodes spp.
is the Norway spruce, Picea abies, but it is not known whether they also attack
introduced spruce species.
Very little is known of the chemical interactions between Pissodes spp. and their
host trees in Europe. Blanc and Blanc (1975) studied the effects of pine extracts on
P. castaneus behaviour. They showed that feeding behaviour was stimulated by
phenolic substances contained in the xylem and bark. Host selection and host
resistance mechanisms have been much more studied in North America on P. strobi
(e.g. Mehary et al. 1994; Sahota et al. 1998). Since these studies have important
implications in the development of IPM strategies against P. strobi, similar
investigations should be carried out for European species.
Pissodes spp. also show preferences in the age of the host tree. P. castaneus is
known to prefer young (4-15 year old) pine trees, P. piniphilus is mainly found on
30-40 year old pine trees, and P. piceae and P. harcyniae prefer old trees (Kudela
1974). However, for each Pissodes sp. trees of various ages are commonly attacked.
It is generally agreed that European Pissodes spp. are secondary pests, i.e. they
prefer weakened or freshly-killed trees. For example, P. castaneus outbreaks are
usually associated with pine decline in combination with other insects or pathogens.
It was shown that it prefers to attack trees previously weakened by the scale
Matsucoccus feydauti Duc (Carle 1973, 1974) and the rust Cronartium flaccidum
(Alauzet 1972a, 1984). Pissodes. piceae, P. pini and P. piniphilus are known to
attack mainly weakenedd trees or trees previously attacked by bark beetles (Kudela
1974; Riis 1975; Luik 1994). Pissodes piniphilus and P. harcyniae are particularly
abundant in stands affected by air pollution (Kudela 1974). However, there are
consistent observations of Pissodes spp. attacking apparently healthy trees, in
particular P. castaneus, P. piniphilus, P. piceae, and P. harcyniae, especially when
present in high density (Kudela 1974; Alauzet 1984; Starzyk 1996). More studies
should focus on the real pest status of Pissodes spp., and in their exact role in the
decline of conifers in Europe.
3.2 Adult biology

The biology and ecology of Pissodes adults have been poorly studied, especially in
the field. In the laboratory, freshly emerged P. castaneus adults feed first on the bark
of twigs (maturation feeding) (Carle 1967). Branches and stems are used by older
adults. Sexes are morphologically similar, but can be distinguished by the structure
of the abdomen and the snout (Carle 1967; Starzyk 1996). Mating is frequently
observed, including during oviposition. Adults are believed to be long-lived (e.g.
Hierholzer 1954; Bukzeeva 1965), but field data on survival are lacking. Carle
(1973) kept adults alive for up to 587 days in natural conditions in southern France.
Carle (1967, 1973), Blanc and Blanc (1975) and Alauzet (1984), provide data on
various other aspects of the biology of P. castaneus adults in laboratory conditions,
such as temperature resistance, feeding habits,
a fecundity, etc. These data are not
available for the other Pissodes spp.
3.3 Oviposition and fecundity

Pissodes spp. lay their eggs in holes bored in the bark by the female. Ovipositor
holes are often found in wounds or cracks in the bark. In most species, eggs are laid
in groups of one to five (Kudela 1974) although broods of P. piceae are usually
larger. In Poland, Starzyk (1996) observed up to 35 eggs per hole, with an average
of 13, whereas, in Germany, Haeselbarth (1962) found a maximum of 15 eggs, with
an average of 4.1 eggs per hole. Fecundity was investigated for P. castaneus only.
Lauga and Alauzet (1983) and Alauzet (1984) measured a mean potential fecundity
of over 500 eggs per female. The fecundity was influenced by rearing temperature
and food quality. The ecological optimum for fecundity was calculated at 16-17°C.
In constant rearing conditions, P. castaneus females showed two egg-laying cycles,
a short one (4-8 days) and a long one (20-60 days), with temperature-dependent
durations.
3.4 Larval and pupal stage

All weevils of the genus Pissodes for which larval stages have been studied have
four larval instars. This includes the European P. castaneus (Carle 1967; Alauzet
1984), P. piceae (Haeselbarth 1962) and P. validirostris (Roques 1976) and several
American species (listed in Alauzet 1984). Hierholzer (1954) and Bukzeeva (1965)
mention five larval instars in P. piceae and P. castaneus, respectively, on the basis
of head capsule measurements showing five distinct peaks. In factt the last two peaks
represent healthy fourth instar larvae and larvae parasitized by Eubazus spp. (Hym.:
Braconidae), which tends to have a strongly reduced size (Haeselbarth 1962; M.
Kenis, unpublished data). Carle (1967), Alauzet (1984), and Hierholzer (1954)
provide measurements of the head capsule width and duration in rearing, for each
instar of P. castaneus and P. piceae, respectively.
Pissodes larvae burrow feeding tunnels in phloem and cambium. At the end of
the fourth larval instar, the larvae excavate a pupal cell in the surface of the wood.
The pupal cell is covered with shredded wood fibre, and is typical for Pissodes spp.
Sometimes, the pupal cell is built more deeply in the sapwood, particularly in P. pini
in pine trunks, or in P. castaneus when this latter attacks the top of young pine trees,
where the bark is very thin. Larvae parasitized by Eubazus spp. tend to build their
pupal chamber in the bark, closer to the surface,
f in particular in fir or pine trunks
with a thick bark (M. Kenis, unpublished data)
3.5 Life cycle

The phenology of Pissodes spp. varies with species and climatic conditions. The
stem-feeding European species usually develop without obligatory diapause, as
shown in laboratory rearing (Carle 1967 and Alauzet 1984 for P. castaneus; Kenis,
1994 and unpublished data for P. castaneus, P. pini, and P. piniphilus). However, in
the field, Carle (1974) and Alauzet (1986) observed a facultative diapause in the
fourth instar larvae of P. castaneus, possibly induced by temperature and
photoperiod conditions. Kenis (1994) showed intraspecific variations in P. pini in
Switzerland. Lowland populations developed without diapause, both in the field and
in the laboratory, whereas mountain populations from the Alps had more than 80%
of their individuals entering into an obligatory diapause in the last larval instar when
reared in the laboratory. When larvae were collected in the field in autumn and
incubated in the laboratory, nearly 100% of the larvae remained in diapause. This
diapause in mountain populations was considered as an adaptation to the particular

climatic conditions in cold areas, where P. pini has a two-year cycle.
P. castaneus shows the largest variability in phenology, probably due to its wide
ecological and geographic distribution in Europe and North Africa. The most
complete studies on P. castaneus phenology are from Carle (1973, 1974) and
Alauzet (1977, 1984) in southern France. They describe life cycles that vary from
site to site and year to year. In general, however, there are overlapping generations,
and from one to two generations a year, with adults and last instar larvae as the main
overwintering stages. Other studies in southern Europe are reviewed by Alauzet
(1984), which also describe various phenological patterns. In other European
regions, P. castaneus has usually one generation per year, or even one per two years
in northern Europe, with either young adults or mature larvae overwintering (see
Kudela 1974, Carle 1974, and Alauzet 1984, for review). However, observations in
central Europe showed that, in single populations, overlapping generations is the
rule and both larvae and adults overwinter (M. Kenis, unpublished data).
The life cycle of P. piceae is less variable, probably because it is strictly
confined to silver fir, a European tree with a rather limited ecological and climatic
range. In central France (Lempérière and Malphettes 1987) and Bavaria
(Haeselbarth 1962), the life cycle is as follows. Eggs are laid in spring or early
summer. The final instar overwinters in its pupal cell and pupates in spring, and
adults emerge in late spring and in summer, but will oviposit in the following year
only. However, Lévieux et al. (1994) in Central France, and Starzyck (1996) in
Poland state that pupation and adult emergence can also occur in late summer and
autumn, if eggs are laid early in the year, suggesting that P. piceae does not have an
obligatory diapause in the larval stage.
There is no detailed study on the phenology of other stem-feeding Pissodes spp.
in Europe. P. pini, P. piniphilus and the three spruce-feeding species are believed to
be usually univoltine, but the life-cycle can last two years at high latitudes (Kangas
1938; Kudela 1974) or altitudes (Kenis 1994). Both adults and larvae can
overwinter, and generations partly overlap.
4. OTIORRHYNCHUSS SPP.
4.1 Adult biology

Otiorrhynchus adults feed for 5-8 weeks before oviposition starts and feeding is
most extensive during the pre-oviposition and early oviposition periods (Stenseth
1976; Moorhouse et al. 1992; Palm 1996). Adults are known to be even more
polyphagous than the larvae. They feed on the leaves and bark of trees and plants.
Leaf notching by black vine weevil (O.sulcatus) adults is of concern for ornamental
plant growers (Bevan 1987; Van Tol 1993) and ring-barking by clay coloured
weevil (O.singularis) adults is a significant problem in reforestation (Bejer-Petersen
1979; Bevan 1987). All species, except O. arcticus, are predominantly
parthenogenetic, but males of all the other species are known from the southernmost
part of the distribution area.
4.2 Oviposition and fecundity

Otiorrhynchus spp. deposit their eggs in the soil or leaf litter at the base of their host
plants (Palm 1996). Oviposition is mostly in mid or late summer, but may continue
until there is a hard frost (Nielsen 1989). Oviposition usually lasts for several weeks
and is broken into distinct oviposition cycles (Moorhouse et al. 1992). Fecundity is
dependent upon temperature, photoperiod food quality and the age of the weevils
(Evenhius 1978; Garth and Shanks 1978; Moorhouse et al. 1992). Overwintering
weevils start laying eggs earlier than newly emerged adults and lay more eggs
(Tanigoshi et al. 1999), however, reduced egg viability of overwintering black vine
weevil females has been recorded (Stenseth t 1976). Fecundity of weevils seems to
be related to host nutritional quality (Moorhouse et al. 1992) as well as to host plant
type. Hanula (1988) observed that black vine weevils reared on Taxus produce more
eggs than weevils on a different diet. The egg production is normally in the range of
150-300 eggs/weevil, but an individual black vine weevil has been recorded laying
as many as 2101 eggs (Nielsen and Dunlap 1981; Moorhouse et al. 1992).
4.3 Larval and pupal stage

The eggs hatch in 2-3 weeks, i.e. in the late summer or autumn, and the young larvae
burrow into soil where they can be found throughout the plant root zone feeding on
the fine roots (Evenhuis 1978). A drop in the soil temperature, signals them to move
deeper into the soil where they overwinter. The larvae overwinter in the soil and
resume feeding on roots in the early spring. At this stage they cause the heaviest
damage as the overwintering larvae prefer larger roots and may girdle the main stem
killing the plants. The larvae are polyphagous; more than 100 plant species have
been identified as potential host plants of black vine weevil larvae and the other
species are also known to be polyphagous (Wagner and Negley 1976; Masaki et al.
1984; Palm 1996). Larvae pupate in May and June and adults emerge in June and
July (Garth and Shanks 1978; Stenseth 1976). However, the larvae of O. nodosus
and O. arcticus continue their development throughout the summer after the first
overwintering and pupate in the early summer after a second overwintering (Larson
and Gígja 1959). The exact number of larval instars is uncertain. The larvae pupate
inside an earthen chamber and the adults emerge from the pupae after 2-3 weeks
(Nielsen 1989; Moorhouse et al. 1992; Palm 1996).
4.4 Life cycle

The black vine weevil Otiorrhynchus sulcatus and the clay coloured weevil
O.singularis are univoltine, whereas O. arcticus and O. nodosus are perennial at
least in the northernmost part of the distribution area (Larsson and Gígja 1959;
Bevan 1987; Van Tol 1993). All species overwinter as larvae in the soil, but the
adult weevils also overwinter to some extent. After a period of feeding in the spring
or early summer the larvae pupate and the adults emerge about two weeks later. The
larvae of the black vine weevil and the clay coloured weevil pupate in early spring
and adult clay coloured weevils start to emerge in March-April, whereas adult black
vine weevils start to emerge in May-June (Stenseth 1976; Nielsen 1989; Garth and
Shanks 1978). The larvae of O. arcticus and O. nodosus pupate in the early summer
and the weevils emerge in late June (Larsson & Gígja 1959; Halldórsson 1994). Egg
laying is generally in mid or late summer, following a period of pre-ovipositional
feeding.
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abietis (L.) larvae (Col., Curculionidae). Journal of Applied Entomology, 120, 397-403.
Nordlander, G. 1987. A method for trapping Hylobius abietis (L.) with a standardised bait and its
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weevil Hylobius abietis to underground sources of host volatiles. Entomologia Experimentalis et
Nordlander, G., Nordenhem, H. & Bylund, H. 1997. Oviposition patterns of the pine weevil, Hylobius
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Nordlander, G., Örlander, G. and Langvall O. 2003b. Feeding by the pine weevil Hylobius abietis in
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strains of Heterohabditis sp. and Steinernema sp. and the fungus Metarhizium anisopliae in nursery
stock. Med. Fac. Landbouww. Univ. Gent, 58/2a.
von Sydow. F. & Örlander, G. 1994. The influence of shelterwood density on Hylobius abietis (L.)
occurrence and feeding on planted conifers. Scandinavian Journal of Forest Research, 9, 367-75.
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Curculionidae). Proceedings off the Entomological Society of Washington, 78, 240-62.
Wainhouse, D., Ashburner, R. & Boswell, R. 2001. Reproductive development and maternal effects in the
pine weevil Hylobius abietis. Ecological Entomology, 26, 655-61.
Wainhouse, D., Boswell, R.. & Ashburner, R Maturation feeding and reproductive development in adult
pine weevil, Hylobius abietis. Bulletin of Entomological Research, in press.
Wilson, W.L. & Day, K.R. 1995. The comparative effectiveness
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larch billets, for the estimations of pine weevil ((Hylobius abietis L.) density indices. Journal of
Wilson, W.L. & Day, K.R. 1996. Variation in the relative abundance of the large pine weevil among
Sitka spruce plantation sites. Forestry, 69,169-71.
Wilson, W.L., Day, K.R. & Hart, E.A. 1996. Predicting the extent of damage to conifer seedlings by the
pine weevil ((Hylobius abietis L.): a preliminary risk model by multiple logistic regression. New
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Zagatti, P., Lempérière, G. & Malosse, M. 1997. Monoterpenes emitted by the large pine weevil,
Hylobius abietis (L.) feeding on Scots pine, Pinus sylvestris L. Physiological Entomology, 22, 394-
400.
Zumr, V. & Stary, P. 1993. Baited pitfall and flight traps in monitoring Hylobius abietis (L.) (Col.
Curculionidae). Journal of Applied Entomology, 115, 454-61.
Zumr, V. & Stary, P. 1994. Seasonal occurrence of Hylobius abietis (L.) (Col., Curculionidae) in different
forest environments of a model area. Journal of Applied Entomology, 118, 361-64.
Chapter 15
SEMIOCHEMICALS IN THE LIFE OF BARK FEEDING

WEEVILS
F. SCHLYTER
Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 ALNARP,

Sweden
1. INTRODUCTION
There is a strong taxonomic bias and limitation in the literature on the BAWBILT
group of bark feeding weevils in general and on the reactions to semiochemicals in
particular. All are conifer feeding species.
Of the 11 species of weevils on the BAWBILT list, only one species, the large
pine weevil Hylobius abietis, has been studied in regard to host selection and the
chemical signals mediating the orientation to and selection of the host plant for
feeding, sex-recognition, and egg-laying. In addition, recent work on anti-feedants
has focused entirely on this species. Thus, while there is some information on the
Palearctic H. pinastri and Pissodes spp and from the Nearctic on Pissodes spp and
H. pales and other root-weevils, this chapter will deal almost exclusively with the
large pine weevil, Hylobius abietis (L.).
2. ORIENTATION BY ADULTS AND LARVAE TO THE HOST

The orientation on different scales in the life of pine weevils relates to different
resources –ecological entities depending on the life-cycle (Trädgårdh 1913; Bejer-
Petersen et al. 1962). The orientation of pine weevils could be seen as a series of
behavioural steps on different spatial scales. The steps span from orientation over
the landscape towards habitat by flying adults at km-scale to the larval feeding
migrations at cm-scale (Fig. 1). Migration to new patches by adults is mandatory as
the larval feeding destroys the substrate (bark of conifer roots) in one or a few years.
The steps are discussed below in sequence in relation to stimuli from habitat,
breeding trees, feeding patches, mates etc.
351
F. Lieutier et al. (ed.), Bark and wood boring insects in living trees in Europe, a synthesis,
351–364.
© 2007 Springer.
352 F. SCHLYTER
Scale Animal Signal Activity

type
Repro- Negative RESOURCE
Maturing
g ductive Larvae signal
Egg-laying
Habitat Maturation
MT (EtOH)
feeding
(Land-
NHV ?
scape) CONIFERS &
STUMPS
Maturation &
MT
sustenance
Tree NHV & other feeding
non-host
compounds FRESH BARK
MT & EtOH Egg-laying

Stump
(Roots) Vn? DYING BARK
Ontogenetic
MT & (developmental)
EtOH(?) feeding
Bark patch
DYING BARK &
FREE SPACE
Figure 1 – Level of behavioural steps at different scales in Hylobius abietis. MT)

Monoterpene hydrocarbons (like α-pinene, see Figure 2), EtOH) ethanol (and probably other
stress-induced volatiles), NHV) Non-host Volatiles. See text for references.
2.1. Breeding adults: Habitat

At the largest scale (1 –10 km), the weevil needs to navigate the forest landscape
when migrating to find a habitat suitable for breeding (Fig. 1). The suitable habitat is
patches of conifer forest where dying roots are available as part of trees or as fresh
stumps (felling areas in modern forestry).
In Scandinavia this migration is done by long distance flights (Solbreck 1980)
guided by olfactory cues. That the long distance orientation in fact occurs towards
odour sources, rather than to general landscape features, is evidenced by the large
numbers of weevils observed in the artificial industrial landscapes of large sawmills
processing conifer logs (Solbreck and Gyldberg 1979). Interestingly, this evidence is
strong only in North and East Europe.
Fresh, uninfested spruce and pine logs are by themselves attractive to flying H.
abietis, proving a wide sense primary attraction to the host plants (sensu Schlyter &
Birgersson 1999; attraction to volatiles from healthy hosts, stress-induced volatiles
like ethanol need not be present) (Tunset et al.; 1993, Brattli et al. 1998). It is not
clear how important ethanol is at this larger scale, but it probably play some role as
it is active in flight traps (Lindelöw et al. 1992). Early on, Mustaparta (1973)
conclusively showed the existence of neurones in single sensilla on the antenna that
physiologically respond to host volatiles and their relation to behaviour (Mustaparta
1975). Wibe and co-authors (Wibe and Mustaparta 1996; Wibe et al. 1996, 1997,
SEMIOCHEMICALS IN THE LIFE OF BARK WEEVILS 353
1998) showed neurones in single sensilla with high specificity to many host volatiles
(Wibe et al. 1998; Mustaparta 2002), mostly monoterpene hydrocarbons like α-
pinene (Fig. 2). A more comprehensive study of behavioural responses to attractant
candidates (Muller and Gunther 1991) is under way (Roten et al. 2002).
2.2. Breeding adults: Adult feeding patches (trees) by odour and other modalities
At the next step of scale (1 –100s m) when the insect is present in the suitable
habitat, adults must find spaced large mature trees (10 –100m scale) or densely
planted small seedlings (1 –10 m scale) for feeding. After landing in the suitable
habitat or emerging from the breeding substrate (for most individuals today: the
clear-cuts of modern forestry) the adults need not only to locate the egg-laying sites.
They also need live host-plants for maturation and sustenance feeding to fill their
demand for the long egg-laying and mating period (Fig. 1).
The adults feed mostly in the crown of mature trees in and nearby felling areas –
recently quantified by Örlander et al. (2000). This feeding on larger trees causes
little or no harm as it is small in relation to the bark biomass of mature trees.
Unfortunately for forestry production, the adults feed not only on the mature trees
but as well on the small seedlings (transplants) planted in the clear-cuts. The feeding
of a single weevil at a seedling stem base may consume a large part of bark of the
stem and may easily ring-bark the transplant. This is where their economic damage
occurs.
Insects normally integrate olfactory, visual and tactile cues for the purpose of
finding (mainly) host plants for feeding (Finch 1986; Chapman and deBoer 1995;
Schoonhoven et al. 1998). Apart from olfaction, visual cues are indicated for H.
pales (Hunt and Raffa 1991). Probably, the large trees are located on the larger scale
(felling area vs. edge, 10 –100 m) by visual cues, possibly directly in flight when
coming into the habitat (Örlander et al. 2000), and the feeding sites found by tactile
cues. The densely planted small seedlings might be encountered to a large degree by
random walks (Björklund et al. 2002), but host odour, enhanced by feeding scars
effluvia, aids the adults in finding the transplants for feeding (Tilles et al. 1986b;
Nordlander 1991). Furthermore, there is an effect on beetle movement in orientation
to seedlings if they stand surrounded by mineral soil or humus (Kindvall et al.
2000). A a pure mineral soil makes weevil movements faster and the animal less
likely to stay on a mineral soil patch (Kindvall et al. 2000), interfering with host
finding. However, also host acceptance at very close range is interfered with and in
the field the mineral soil partly protects transplants from feeding (Björklund et al.
2002).
2.3. Breeding adults: Breeding patches and mate recognition

Location by reproductive adults of breeding patches like stumps and roots takes
place on a m –dm-scale, while mate recognition occurs on the smallest scale of mm
to cm. While the physical scale and the chemical compounds differ, the chemical
senses, mainly olfaction, is the modality for these steps.
354 F. SCHLYTER
2.3.1. Long distance

The longer distance orientation to breeding patches does not seem to differ from that
of many other bark- and wood-living beetles. In particular, some root infesting bark
beetles can be attracted to and sampled by the same signals ((Hylastes spp: Eidmann
et al. 1991; Erasmus and Chown 1994; Erbilgin et al. 2001). The weevil breeds in
dying roots of conifers, such as those of storm-felled or cut trees, and does not
appear to have a long-distance pheromone (Tilles et al. 1988; Zagatti et al. 1997) in
spite of some early indications to that effect (Mustaparta 1974, 1975). As in Tomicus
piniperda bark beetles (Byers et al. 1985), feeding beetles on Scots pine ((Pinus
sylvestris) logs enhance attraction somewhat over uninfested logs, but no more than
can be explained by the increased release of host odours (Tilles et al. 1986b; Zagatti
et al. 1997). The attraction of long-horn beetles (cerambycids), bark weevils
(curculionids), and non-aggressive bark beetles to combinations of conifer volatiles
and ethanol is well established (Fig. 2, Moeck 1970; Klimetzek et al. 1986;
Schroeder 1988; Byers 1992; Lindelöw et al. 1992; Erasmus and Chown 1994).
Attraction to ethanol alone or in combination with odours from stressed hosts occurs
also in long-horns and bark beetles living in hardwoods (Montgomery and Wargo
1983; Dunn and Potter 1991). In dying stems, roots, or logs the release of ethanol
(Moeck 1970) and other low-molecular products is due to anaerobic stress (Graham
1968; Davies 1980; Kimmerer and Kozolowski 1982; Kelsey 1996; Kelsey and
Joseph 1997; Kelsey 2001) or decay fungi (Gara et al. 1993). These stress signals
make the host material more attractive. It should be noted that the stress reaction in
living tissue in stumps (vonSydow and Birgersson 1997) is the key ethanol
production mechanism, while the microbial degradation of killed tissue is less
important (Kelsey 2001).
A stress-induced primary attraction seems active in the pine weevil, shown by
the synergism between ethanol and conifer host volatiles (Tilles et al. 1986a;
Nordlander 1987). A study in Scandinavia by Lindelöw et al. (1992) showed that H.
abietis was the only species attracted consistently not only to combinations of host
monoterpenes and ethanol, but also to ethanol itself, indicating a preference for
strongly stressed (dying) host roots (Fig. 1). This is proof of stress-induced primary
attraction (sensu Schlyter and Birgersson 1999), agreeing well with the status of the
dying breeding substrate. Ecologically similar weevils and scolytids –breeding in
conifer roots– have broadly similar responses to turpentine, α-pinene, ethanol, and
their combinations (Fig. 2). A combination of turpentine and ethanol is generally
attractive (Lindelöw et al. 1993). Among weevils, only H. abietis was attracted to
ethanol alone, whereas H. pinastri was the only species not significantly attracted to
ethanol plus spruce turpentine (Lindelöw et al. 1993).
2.3.2. Final location

At the final step in location of breeding patches, a short distance orientation (dm-
scale) occurs to individual roots (of stumps) for egg-laying (Fig. 1). Weevils walk
on the forest floor (litter) and dig through the soil towards the stress signals from
roots, as described in laboratory studies by Nordlander et al. (1986). Older stumps
will release not only hydrocarbon monoterpenes and ethanol, butt also oxygenated
monoterpenes like verbenone, which in larger doses inhibits attraction to host

material (Lindgren et al. 1996). Whereas breeding success differs among conifer
hosts both for Hylobius abietis (Thorpe & Day 2002) and for Nearctic Hylobius
(Hunt et al. 1993), attraction to different host by reproductives have been little
studied.
Normal host constituents Stress induced
OH
(1S,5S)-α-Pinene (1R,5R)-α-Pinene ∆3-Carene Ethanol
Taxa attracted
Hylobius Hylobius Hylobius Hylobius abietis
Tomicus Tomicus Tomicus (Tomicus)
Dendroctonus spp Dendroctonus spp D. valens Hylastes spp
Cerambycidae Cerambycidae Cerambycidae Dendroctonus spp
Cerambycidae
Figure 2 – Kairomonal attractants in weevils and other BAWBILTs. Figure redrawn from
Schlyter and Birgersson (1999). For most root feeding beetles, like Hylobius and Hylastes,
and those breeding in substrates of dying host tissue there is a synergism between
monoterpenes and ethanol.
2.3.3. Mate recognition

Another type of final step is the recognition by males of their female sex partners at
close distance (cm- or mm-scale). The short-range contact sex-recognition
pheromone is partly characterised as a long-chain, low volatile extractable
compound from the female cuticle (Tilles et al. 1988).
2.4. Larval orientation to feeding patches

A basic piece of the biology, the normal egg-laying site, was only recently
discovered in Swedish studies. Most of egg-laying is in fact not directly on the host
bark but in the soil near roots (field: Nordlander et al. 1997). Even the small 1st
instar larvae may migrate for 5 cm through soil to the feeding substrate (lab:
Nordenhem and Nordlander 1994). Larger larvae may also leave over-crowded sites
and migrate through soil to other parts of the root (Nordenhem and Nordlander
1994), which may increase survival in spite of an increased risk of predation
(Salisbury and Leather 1998). The signal used by the larvae is the same as for adults
orienting to dying roots; monoterpenes (α-pinene) and ethanol (Fig. 1, Nordenhem
and Nordlander 1994).
2.5. Non-breeding adults

356 F. SCHLYTER
The responses to olfactory stimuli in the phases of the adult life cycle reflect the
seasonal needs, egg-laying plus food orr food only, respectively (Nordenhem and
Eidmann 1991). The non-breeding (pre-reproductive) adults are more attracted to
fresh host material or monoterpene mixtures with no ethanol added, whereas
breeding adults require older material with ethanol emission (Nordenhem and
Eidmann 1991; Malphettes et al. 1994; Zumr et al. 1995). A similar pattern was
found in the Nearctic Hylobius radicis Buchanan, H. assimilis Boheman, H. pales
(Herbst), and Pachylobius picivorus (Germar). The non-reproducing animals were
found only in passive traps, while reproductively mature individuals of all species
were found in terpene + ethanol traps (Hoffman et al. 1997).
3. HOST ACCEPTANCE IN ADULT FEEDING

The preference for conifers is far from absolute, the adults have been observed
feeding on both coniferous and broad-leaved tree species (Scott and King 1974) and
appear to be more an oligophagous than a monophagous species. The insects have
been presented to a number of woody plant species where they showed a preference
in the order: P. sylvestris >> B. pendula >> P. abies >> F. excelsiorr > A.
pseudoplatanus (Leather et al. 1994; Manlove et al. 1997). Recently, Månsson &
Schlyter (2003) showed in no-choice tests that the outer bark was contacted and
removed in 35 of 38 spp offered from 25 plant families. However, in 17 spp the
inner bark was not accepted for feeding, indicating that while regarded as food by
the insects, these species had anti-feedant qualities in their inner bark causing the
weevils to starve rather than to feed for 48 h. Also in the field, feeding on non-
conifer seedlings like Fagus and Quercus occurs frequently (Löf 2000). Such
feeding damage may, however, be intermixed with damage from short-snouted
weevils (Otiorrhynchus scaberr L. and Strophosoma melanogramma Forst.), that
feed predominantly on angiosperm seedlings (Löf 2000). At the weevil densities
prevailing today in forestry, there is also evidence for a strong random component in
the contact of the weevils with seedlings. Judging from frequent catches in traps
surrounding intact spruce seedlings, most seedlings will be visited within 2.5 cm by
a weevil once a week (Björklund et al. 2002). Such random plant contacts may
partly explain the feeding on non-hosts (Löf 2000).
Several single components from Pinus host bark have, somewhat surprisingly,
been implicated as anti-feedants or repellents (Dethier et al. 1960) for adult pine
weevil feeding (Fig. 3). Nordlander (1990, 1991) reported limonene, a monoterpene
hydrocarbon, as inhibitor of attraction to the host. Lindgren et al. (1996) quantified
the inhibition of feeding in response to the oxygenated monoterpene verbenone as
did Klepzig and Schlyter (1999) for carvone, another monoterpene ketone. Bratt et
al. (2001) reported anti-feedant activity of a new natural product, ethyl 2,3-
dibromo-3-phenylpropanoate, –a halogenated phenylpropanoid derivative from P.
contorta. The fact that these and several other components coming from host tissue
(Klepzig and Schlyter 1999) are active as negative signals for feeding is puzzling. It
could be explained by the testing at unnaturally high doses and/or by the testing
alone without the full complimentary blend of other host signals. Non-host bark
may, naturally, yield more of anti-feedant compounds (Månsson 2001, Månsson &
Schlyter 2003, Månsson et al. 2004)
A type of deterrent pheromone found in the faeces laden material added by the
ovipositing female over the egg and egg-niche, in cases where egg-laying occurs
directly on the bark, has been tentatively reported (Nordlander 1999). An anti-
feedant component (methyl-3,5-dimethoxybensoate)
y from the faeces material has
been reported as field active (Nordlander et al. 2000a; Nordlander 2001).
However, not only strict semiochemicals may be active chemicals in weevil host
selection. Sahota et al. (2001) showed negative post-ingestive effects, probably
toxic, on ovarian growth in Pissodes strobi of extracts from resistantt Picea
sitchensis.
O
CH3O
OCH3
1 5
OCH3
O
2 6 H
O OCH3
O
3 7 Br O
Br
O
O
4 8
OH
Figure 3 – Molecules with reported anti-feedant activity of different origin: Left column those
found in host Pinus sylvestris tissue ((1: (R
(R)-Limonene, Nordlander 1990; 2: Verbenone,
(R)-(+)- and (S)-((−)-Carvone, Klepzig and Schlyter 1999). Right
Lindgren et al. 1996; 3 & 4: (R
column from other sources ((5: Beetle faeces, Aromatic ester, Nordlander et al. 2000, 6: Non-
hosts, Aromatic aldehyde, Eriksson et al. 2002; 7: Pinus contorta, halogenated
phenylpropanoid,d Bratt et al. 2001 8: Non-host Tilia cordata, Nonanoic acid, Månsson et al.
2004). [FS1]
4. OPTIONS FOR CONTROL BY SEMIOCHEMICALS

The actual problem for production forestry occurs during the subsistence feeding by
older adults and maturation feeding by young adults on seedlings. Direct control
must aim at either diminishing weevil populations or preventing feeding on the
small transplants. A control program will also need accurate forecasting or
monitoring of weevil distribution and abundance to predict damage.
358 F. SCHLYTER
4.1. Pheromones and kairomone attractants

Conventionally, semiochemical attractants have had three major applications;
monitoring, mass-trapping, and mating-disruption. For the boll weevil ((Anthonomus
grandis Boh.) and for K K-selected palm weevils (Rhynchophorus and Metamasius
spp) a mass-trapping with aggregation pheromones have been reported as efficient
(Plato et al. 2000, Oehlschlager et al. 2002). As the pine weevil has no long-range
pheromone, the options for a competitive attractant useful in mass-trapping or
disruption are bleak. Pheromones are species-specific signals produced only by the
insect, often multi-component and active at very low levels. In contrast, a kairomone
(host odour) signal is especially in conifer-inhabiting species nott very specific and
field-active only a rather high rates of release (Byers et al. 1985; Tilles et al. 1986a,
b). These rates can never compete with the same compounds, released en masse
from host materials that are abundant in the suitable habitat, in attracting any major
proportion of the population. The short-range sex-recognition pheromone found in
adult females (Tilles et al. 1988) will, due to the short range of action (mm –cm) be
of little use for a conventional semiochemical usage.
Only for the monitoring trapping has kairomone bait and walk-in traps for use in
clear-cuts been developed (Nordlander 1987). The synergistic bait of α-pinene and
ethanol (Tilles et al. 1986a) is, however, best suited for mature (egg-laying period)
weevils only (Nordenhem and Eidmann 1991; Malphettes et al. 1994). For North
American root weevils (Fettig et al. 1998, Rieske 2000) as well as for H. abietis
(Zumr and Stary 1992, Wilson and Day 1995), an increase of catch or attraction is
reported of fresh host logs or barkk over synthetic monoterpenes alone.
However, the relation between weevil damage and weevil catch in pitfall traps is
not straightforward and may only exist at the end of the season (Nordlander 1987).
In a large and well-replicated long-term study, problems existed in relating insect
catches to feeding damage over a 6-year period, and only at 2 years was the
correlation significant (Örlander et al. 1997).
4.2. Allomonal antifeedants and repellents

Schlyter and Löfqvist (1998) and Leather et al. (1999) suggested that deterrents and
pre-ingestive anti-feedants (sensu Månsson 2001) could be used, relying on
techniques developed for several other insects (Koul 1993, Frazier and Chyb 1995).
So far, there are few formal papers published on laboratory tests of European
Hylobius in spite of intensive research efforts (Beitzenheineke and Hofmann 1992;
Klepzig and Schlyter 1999; Bratt et al. 2001). The use of ‘neem’ formulations
(Schmutterer 1995) has been tested in Hylobius spp (Beitzenheineke and Hofmann
1992; Salom et al. 1994, 1996; Klepzig and Schlyter 1999, Sibul et al. 2001), but
with the exception of Sibul et al. (2001) there is little success. Several papers in
'grey literature' report more or less successful
f applications in the field of a few
compounds (Schlyter 1998, 2001; Schlyter et al. 2000, 2004b; Fojtik et al. 2000;
Nordlander et al. 2000b; Nordlander 2001; Sibul et al. 2001). The compounds
reported are rather diverse but mostly volatiles (Fig. 3).
Whereas satisfactory efficacy has been reported in several cases, a major

problem seems to be the formulation for extended field activity (Sjödin et al. 2001;
Löfqvist et al. 2002a). Nevertheless, patents have now been granted or applied for a
number of anti-feedants/repellents and the formulation of these (Nordlander et al.
2000a; Löfqvist et al. 2002b).
CONCLUSIONS
Two very general conclusions can be made based on the available literature:
- Signals for orientation (kairomone volatiles) are relatively well known and
practically useful in the field. Even so, work remains on the behavioural activity of
several host monoterpenes.
- Host acceptance signals in adult feeding (both feeding stimulants and inhibitors)
are little known, in spite of work in several applied projects with allomonal anti-
feedants (Nordlander et al. 2000b; Smitt 2002).
Several specific future research issues include:

1- Why are young conifer seedlings so little resistant to adult weevil attacks, which
seem so important in modern forestry? One reason might be that the selection
pressures (predation) over the life of the seedling are quite diverse and the weevil
defence is not the only concern. Nystrand and Granström (2000) showed several
other mortality factors: seed predation by carabids ((Pterostichus, Calathus) and
predation by slugs ((Arion) as the most important factors for young – juvenile
(weeks) seedlings. Mortality of juvenile seedlings was not related to catches of pine
weevils in their study. Are these small trees physiologically incapable of resistance
or are selection pressures too variable during the life of the tree to affect traits
expressed during the seedling period?
2- Direct control by population reduction by semiochemical mass-trapping is not
possible. Monitoring by kairomone baited walk-in traps could be more accurate in
regions that have less dispersal by flight than in Scandinavia.
3- Adult feeding decisions is partly by contact chemoreception and can be re-
directed. Research on the anti-feedants structure-activity and formulations may well
provide a key element for seedling protection.
4- Compared to the well-studied kairomone responses of predatory Coleoptera (e.g.
Erbilgin and Raffa 2001; Schroeder 2003) and parasitoid Hymenoptera (Pettersson
2001) attacking conifer bark beetles, essentially nothing is known about
semiochemical responses in bark weevil predators or parasitoids.
5- Sex recognition pheromone identification would allow new avenues of testing a
low-volatile compound for behavioural modification. How would males and females
react to a small host plant that smells like a sexually active female?
ACKNOWLEDGEMENTS
Comments on earlier drafts by Drs J. Löfqvist, G. Nordlander, K. Sjödin, and M.
Faccoli are much appreciated. Computer generated molecule structures are courtesy
360 F. SCHLYTER
of Dr K. Sjödin, Mid-Sweden University, Sundsvall. The author was supported by

the project “Protection of conifer seedlings against Hylobius pine weevils by
allomones” in the program “Pheromones and Kairomones for Control of Pest
Insects” funded by MISTRA (The Foundation for Strategic Environmental
Research).
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Experimentalis & Applicata, 80, 39-42.
Wibe, A., Borg-Karlson, A.K., Norin, T. & Mustaparta, H. 1997. Identification of plant volatiles
activating single receptor neurons in the pine weevil ((Hylobius abietis). Journal of Comparative
Physiology a-Sensory Neural and Behavioral Physiology, 180, 585-95.
Wibe, A., Borg-Karlson, A.-K., Persson, M., Norin, T. & Mustaparta, H. 1998. Enantiomeric composition
of monoterpene hydrocarbons in some conifers and receptor neuron discrimination of α-pinene and
limonene enantiomers in the pine weevil, Hylobius abietis. Journal of Chemical Ecology, 24, 273-87.
Wilson, W.L. & Day, K.R. 1995. The Comparative Effectiveness
f of Chemical Traps, and Fir, Spruce and
Larch Billets, for the Estimations of Pine Weevil ((Hylobius abietis L) (Col, Curculionidae) Density
Indexes. Journal of Applied Entomology, 119, 157-60.
vonSydow, F. & Birgersson, G. 1997. Conifer stump condition and pine weevil ((Hylobius abietis)
reproduction. Canadian Journal of Forest Research-, 27, 1254-62.
Zagatti, P., Lemperiere, G. & Malosse, C. 1997. Monoterpenes emitted by the large pine weevil, Hylobius
abietis (L.) feeding on Scots pine, Pinus sylvestris L. Physiological Entomology, 22, 394-400.
Zumr, V. & Stary, P. 1992. Field Experiments with Different Attractants in Baited Pitfall Traps for
Hylobius abietis L (Col, Curculionidae). Journal of Applied Entomology, 113, 451-55.
Zumr, V., Stary, P. & Dostalkova, I. 1995. Comparison of Seasonal Responses of Hylobius abietis (L)
(Col, Curculionidae) to Chemical and Natural Lures in Baited Pitfall Traps. Anzeiger Fur
Schadlingskunde Pflanzenschutz Umweltschutz, 68, 166-68.
Örlander, G., Nilsson, U. & Nordlander, G. 1997. Pine weevil abundance on clear-cuttings of different
ages: A 6- year study using pitfall traps. Scandinavian Journal of Forest Research, 12, 225-40.
Örlander, G., Nordlander, G., Wallertz, K. & Nordenhem, H. 2000. Feeding in the crowns of Scots pine
Chapter 16
HYLOBIUS ABIETIS
S – HOST UTILISATION AND
RESISTANCE
D. WAINHOUSE
Forest Research, Alice Holt Lodge, Wrecclesham Farnham, Surrey GU10 4LH,
United Kingdom
1. INTRODUCTION
The pine weevil, Hylobius abietis, breeds predominantly in the bark of roots of
felled conifers and occasionallyy in moribund trees or in logs in contact with the soil.
In unmanaged forests, these resources are unpredictable in time and space and
usually scarce, except after relatively rare events such as extensive windblow. H.
abietis is therefore, expected to occur at low density in its natural habitat. In
managed forests, where clearfelling at the end of a rotation is the silvicultural norm,
high weevil populations develop on the abundant root-stumps left in the ground.
Hylobius abietis is therefore a ‘silvicultural’ pest whose population size is
determined to a large extent by the availability of breeding sites (Eidmann 1979).
The size of weevil populations is one of the main factors determining the extent of
mortality of young conifers planted after clearfelling in central and northern Europe.
But emphasis on the quantitative aspects of root-stump availability as a determinant
of population size tends to obscure possible qualitative variation, both between and
within host species, in their ‘suitability’ for larval development. The ‘quality’ of the
resource is also likely to change over time, depending on such site-related factors as
rainfall, temperature and rate of fungal decay. Weevil population dynamics and
abundance could therefore be influenced by qualitative as well as quantitative
variation in their breeding resource.
The young conifers used in replanting clearfell sites are vulnerable to attack by
adult weevils that emerge from the root-stumps. Weevils are large relative to the
transplants and because they feed on the bark of the main stem, relatively small
amounts of damage can be lethal. Mortality of unprotected d young conifers on
reafforestation sites is normally high (Långström & Day, chapter 19), giving the
impression that most plants are very susceptible to weevil attack. However, because
weevil population densities and therefore rates of attack on transplants are so high,
365
365–379.
© 2007 Springer.
366 D. WAINHOUSE
any underlying differences in susceptibility, both within and between species are
likely to be obscured. This is an importantt point because even relatively low levels
of resistance can be of value in pest management, allowing for example a reduction
in the amount of insecticide needed to protect plants (van Emden 1991). In the
following sections of this Chapter, evidence for ‘residual’ resistance in root-stumps
affecting the survival and development off larvae and for resistance in seedlings
affecting the amount of adult feeding is reviewed.
2. ‘RESISTANCE’ OF ROOT-STUMPS TO LARVAE

In conifer bark, preformed defences such as resin and lignified stone-cell-masses, as
well as the induced dynamic wound response can be highly effective in preventing
colonisation of the bark of living trees by bark beetles and weevils (Christiansen and
Horntvedt 1983; Grégoire 1988; Phillips and Croteau 1999; Raffa and Berryman
1987; Wainhouse et all 1990). In the intact root-stump left in the ground after felling,
preformed and possibly also induced defences could remain effective and reduce
establishment success of H. abietis larvae for a period after felling. Evidence for the
residual effects of resistance mechanisms present in the living tree comes from both
field and laboratory experiments showing that there are within and between species
differences in the quality of stumps as a breeding resource for weevils. Because it is
difficult to work with root-stumps, most experiments have been done with logs cut
from the lower stem of mature trees. It is a reasonable assumption however, that the
bark of these logs is similar to that on the main body of the root-stump which
contains most of the bark resource on which larvae feed.
Pine, the presumed natural host, is generally more favourable for larval
development than spruce. Larvae develop more slowly on buried logs of Norway
spruce than of Scots pine (Bejer-Petersen et al 1962), more weevils tend to emerge
from root-stumps of pine than spruce (von Sydow and Birgersson 1997) and adults
from spruce appear to have a lower fecundity and a shorter adult life span than those
emerging from pine (Guslits 1970). Species such as larch appear to be highly
unfavourable for larval development (Wainhouse et all 2001; Thorpe and Day 2002).
The flow of resin from bark has been suggested as a cause of larval mortality
especially in pines (Wainhouse et al 2001) and in Sitka spruce, physical defence in
the form of lignified stone-cell-masses within the bark can reduce the growth rate of
larvae (Fig 1).
Indirect evidence for the importance off ‘residual’ resistance comes from the
observation that larval size influences survival on different conifer hosts. Egg size in
H. abietis is influenced both by female size and by the quality of the food resource
during maturation feeding (Wainhouse et all 2001). The large larvae that hatch from
large eggs survive better than smaller ones when inoculated onto logs of different
conifer species (Fig 2). This suggests that preformed defences in the bark were still
active after felling and that small larvae were most susceptible to their effects.
Competitive interactions between larvae in root-stumps may be an additional cause
of mortality of small larvae (Nordenhem and Nordlander 1994).
H. ABIETIS – HOST UTILIZATION AND RESISTANCE 367
Figure 1. Mass of Hylobius abietis larvae developing on logs of Sitka spruce for 106 days.
Larvae feeding in bark that contained high concentrations of lignified stone-cell-masses were
much smaller than those from bark which contained no stone-cell-masses (From Thorpe and
Day, 2002).
Figure 2. Predicted survival of larvae of Hylobius abietis of different initial mass when
inoculated into the bark of logs of different conifer species (From Wainhouse et al 2001).
These different experiments show that conifer root-stumps are not simply a
‘passive’ breeding resource. They suggest that the number of weevils emerging from
clearfell sites for a given level of initial attack is likely to be affected not only by the
368 D. WAINHOUSE
tree species previously occupying the site but also by the ‘age’ of the root-stump i.e.
the time since felling. During the early phase of root-stump colonisation, when
‘residual’ resistance is most likely to be effective, larval mortality could be
relatively high. Field experiments are however, needed to verify this.
3. RESISTANCE OF YOUNG CONIFERS TO ADULT FEEDING

Female weevils emerge from root-stumps with undeveloped ovaries in which eggs
develop only after a period of maturation feeding (Fig 3) (Munro 1928; Nordenhem
1989; Leather et all 1999; Örlander et all 2000). Initial feeding is likely to be on the
bark of transplants, although weevils also feed on the bark of branches and twigs
within the crown of mature conifers and on the bark of logs and brash left on site
after felling operations. In the laboratory, this period of maturation feeding can be
relatively short. For example, when weevils fed on the bark of different seedling
conifers, the first mature eggs were formed after 12-16 days (Wainhouse et all 2001).
In this study, variation in the rate of reproductive development was most likely due
to differences in the nitrogen content of the bark of the different conifer species.
To be of practical value, resistance in young conifers would need to be expressed
through a reduction in the amount of feeding or an increase in the ability of the
plants to tolerate and recover from a given level of feeding damage. Most methods
for quantifying the amount of feeding have been developed for field use where the
emphasis has been on visual estimation of damage categories (Eidmann and
Lindelöw 1997 and references therein). In quantifying attack, there has naturally
been much emphasis on lethal damage estimated by simple methods that allow large
sample sizes. Methods that classify damage as absent, moderate or heavy can be
subjective however, and make it difficult to compare different studies where plants
may vary in size and age or where the differences in the amount and distribution of
feeding are relatively small.
3.1. Variation in damage to young conifers

Nearly all studies on variation in feeding
f damage on young conifers have
concentrated on the role of plant phenotype or on the influence of the local
environment. However, a number of different factors can interact to determine
damage levels (Eidmann and Lindelöw 1997). Factors that have been reported to
affect the amount of feeding on transplants include the method of nursery production
(Selander et all 1990; Selander 1993; von Sydow 1997), plant size (Eidmann 1969;
Selander 1993; Thorsén et all 2001), scarification of soil around the transplants
(Långström 1985; von Sydow 1997), insolation (von Sydow and Örlander 1994) and
the presence of branches and other felling residues around the plants (Selander
1993). It is also possible that factors referred to collectively as transplant ‘stress’
could influence susceptibility to weevil attack (Kauppi 1984; McKay 1997; South &
Zwolinski 1997). This can make it difficult not only to identify resistance traits but
also to compare field studies in which different species, plant age, plant production
systems, insecticide treatment and planting sites have been used. Results exclusively
from field assessments of damage can therefore be difficult to interpret in terms of

plant resistance.
Figure 3. Ovaries dissected from (a) a recently emerged, immature female and (b) one
containing two mature eggs (m) ready for laying. Note difference in approximate scale. (See
Nordenhem (1989) for discussion)
3.1.1. Species differences and the influence of nursery production method

There have been few comparative studies of species susceptibility to attack, but in a
trial of three-year-old bare-rooted spruce and pine of similar lower stem diameter,
von Sydow and Örlander (1994) found no differences between them in feeding rate
or damage. However, some laboratory experiments with seedling plants suggest that
pine may be more tolerant of attack (section 3.2.2., Fig. 7)
370 D. WAINHOUSE
Plants that are mass-produced for use in reafforestation programmes are usually
‘containerised’ or cell-grown under protected cultivated or are open-grown bare-
rooted plants. Comparing attack rates on these different plant types is not
straightforward, because they can vary in physical characteristics such as stem
diameter, amount or distribution of foliage or bark thickness as well as in their
response to site conditions and transplantation stress due to differences in root-shoot
ratio.
Conifer transplants are sometimes assumed to be more susceptible to weevil
attack than naturally regenerated plants but again, there have been few detailed
comparisons. Selander et all (1990) demonstrated that nursery-produced Scots pine
seedlings planted close to naturally occurring ones of similar size were more
frequently attacked, had higher mortality and tended to recover less well from
sublethal damage. However, none of the natural seedlings were lifted and replanted
so it is not possible to determine whether the differences were due to ‘nursery
production method’ or to a ‘transplantation effect’. The effects of transplantation are
known to be complex, affecting in particularr the water relations of the plant (Burdett
1990; Margolis and Brand 1990) but there is also evidence of effects on secondary
chemicals. In 3-year-old pines that had recently been replanted, terpene
concentration in needles and stems initiallyy increased by around 30% compared with
similar ‘control’ pines that had been planted one year earlier. By the end of the
growing season however, concentrations were lower than in controls (Sallas et al
1999). The initial effects were attributed to the negative influence of planting on
photosynthesis, which reduced the overall carbon budget, and to possible effects of
drought stress.
When methods of nursery production are compared, several studies have
indicated that in both spruce and pine, bare-rooted transplants have higher survival
rates than containerised ones (Selander et all 1990; Selander 1993; von Sydow 1997)
(Fig 4). In an interesting comparison between containerised cuttings and seedlings
of Norway spruce of similar stem diameter, seedlings were in general, more
frequently attacked, were more likely to be girdled and had higher mortality rates
than cuttings (Hannerz et all 2002) (Fig 5). These differences were attributed in part
to the thicker bark and presence of needles on the stem base of cuttings.
The effect of fertilisation on levels of attack has been investigated by Selander and
Immonen (1991). In transplanted fertilisedd or unfertilised 2-yr-old containerised
Scots pine seedlings, the area of wounded bark on those fertilised with NPK was
approximately three times higher than seedlings fertilised with PK, N or those left
unfertilised. This variation in response to fertiliser composition is difficult to
interpret without some analysis of the nutritional or secondary chemical ‘quality’ of
the bark on which the weevils were feeding. As well as altering the nitrogen
concentration in the bark of young conifers, nitrogen fertilisation also reduces the
concentration of preformed carbon-based defences such as resin and polyphenols
(Wainhouse et al 1998). These effects are broadly explained by resource-availability
theories of plant defence that predict that nitrogen fertilisation stimulates growth and
so limits the amount of carbon available for synthesis of secondary chemicals. In
general therefore, fertilised plants are expected to be less well defended in the short
term (Herms and Mattson 1992).
Figure 4. Survival of bare-rooted (¨(¨) and containerised (Ÿ)Scots pine and Norway spruce
planted after felling without an intervening fallow period. The young trees had been treated
with insecticide at planting. A was the firstt growing season after felling (From von Sydow
1997).
3.1.2 Effect of plant size

Larger plants, i.e. those with a bigger stem
m diameter, are in general less likely to be
killed by weevil attack. One of the main reasons for this is that the probability of
girdling is lower in larger plants (Selander 1993; Örlander and Nilsson 1999;
Thorsén et all 2001). Larger plants however, tend to accumulate more feeding
372 D. WAINHOUSE
damage (Eidmann 1969), but appear to be able to recover from it more readily than
small plants. In one extensive study, thousands of containerised Norway spruce
seedlings were planted out in southern Sweden and their fate monitored for up to 7
years (Thorsén et all 2001). Prior to planting, experimental plants had been grown
for different lengths of time at different densities and in different sized containers so
Figure 5. Mortality of Norway spruce cuttings and seedlings on clearfells of different age
located in southern Sweden. Some of the sites were scarified before planting (From Hannerz
et al 2002).
that when planted out, they differed in stemm diameter, height and age. It was clear
from this study that mortality caused by weevil feeding was reduced as stem
diameter increased, independently of other effects. Seedlings of 8-10 mm diameter
suffered the least damage and there was also evidence that faster growing
transplanted seedlings suffered only light damage.
3.2. Resistance mechanisms

Resistance mechanisms are usually considered in relation to their effects on the
survival, development or behaviour of insects, or in relation to the plants ability to
tolerate attack (Painter 1951, 1958; Kogan and Ortman 1978). Most studies of
‘resistance’ to weevil feeding in young conifers have examined the effect of
phenotypic variation on damage levels. There have been no systematic studies of
genetic variation in resistance and only a few studies have investigated possible
resistance mechanisms. With some knowledge of the underlying mechanisms of
resistance to feeding by H. abietis in young conifers, it would be easier to interpret
the observed variation in attack in relation to plant phenotype.
3.2.1 Effects of preformed defences on orientation and feeding behaviour

The ability of weevils to detect components of resin has been demonstrated in
several electrophysiological studies in which olfactory r receptors responsive to
different monoterpenes and sesquiterpenes have been described (Mustaparta 1975a,
b; Wibe and Mustaparta 1996; Wibe et all 1996, 1997, 1998). For most of these
chemicals, the behavioural response of weevils and their possible role in finding and
accepting hosts is generally unknown. Where behavioural studies have been done,
interpretation is complicated by the likely role of monoterpenes in both adult
maturation feeding and location of root-stumps for oviposition and also by apparent
changes in responsiveness during the reproductive cycle (Nordenhem and Eidmann
1991; Lindelöw et all 1993). The monoterpene, α-pinene, which is released from
both root-stumps and transplants is attractive to weevils (Selander et all 1973, 1974;
Kalo et all 1974; Mustaparta 1974; Mustaparta 1975b (but see Müller and Haufe
1991)). The response to Į-pinene released from root-stumps however, is synergised
by ethanol which is released naturally from host material under anaerobic conditions
(Nordlander et all 1986; Tilles 1986a; Nordlander 1987, 1990; Lindelow et all 1993;
Kelsey 1994). The fact that ‘wounding’ of bark either mechanically or through
active feeding by weevils, increases its attractiveness to H. abietis, is further
evidence of the important role of volatile monoterpenes in host finding (Tilles
1986b; Nordlander 1991; Zagatti et al 1997).
Some monoterpenes however, may be repellent or inhibitory. Limonene and
myrcene for example have been found to inhibit the attractive response to Į-pinene
(Nordlander 1990, 1991; Zumr and Starý 1992) and limonene is known to be toxic
or repellent to bark beetles and weevils (Raffa et all 1985; Werner 1985; Lindgren et
al 1996). Monoterpene composition in conifers is under genetic control (Phillips and
Croteau 1999) and the concentration of limonene is known to vary among pine and
spruce populations (Yazdani and Nilsson 1986; Nerg et all 1994). This suggests the
possibility that monoterpene composition could play a role in resistance by affecting
the behavioural response of weevils to transplants. However the high intraspecific
variation in monoterpene composition and strong environmental influence on
concentration in young conifers (Kalo et all 1974; Nerg et all 1994) suggests that
resistance mechanisms affecting weevil host finding are likely to be of little practical
significance.
Once plants have been located, weevil feeding behaviour could be affected by
resin or other secondary chemicals within the bark. Several host and non-host
chemicals have been observed to affect the feeding behaviour of weevils (Table 1),
but in general, there is little evidence of the natural occurrence of feeding inhibitors
or repellents in the bark of young conifers.
374 D. WAINHOUSE
Table -1. The effect of some chemicals on the feeding behaviour of adult Hylobius abietis
Chemicals affecting Origin Response Reference

adult feeding behaviour
Acetophenone glycoside ramets of Pinus negative correlation Lieutier et

sylvestris clones with feeding all 1996
damage
Ethyl-trans-cinnamate, bark of antifeedants Bratt et al

Ethyl 2,3-dibromo-3- lodgepole pine 2001
phenyl-propanoate
Verbenone commercial or feeding deterrent Lindgren et

microbial all 1996
breakdown of
host tissues
Coumarin, carvone, commercial feeding deterrent Klepzig &

verbenone, limonin, Schlyter
borneol, 4-allyanisole 1999
3.2.2. Induced resistance, wound repair and tolerance.

The effect of induced changes in bark on resistance to further feeding and the ability
of transplants to recover from sublethal damage has been examined in several
studies of artificial wounding. Mechanical wounding of the stems of 1-year-old
Pinus sylvestris seedlings causes an increase in the overall concentration of resin
acids in areas immediately adjacent
d to the wound within about 3 days, apparently as
a result of de novo synthesis in affected tissues (Gref and Ericsson 1985). In further
experiments, Ericsson et all (1988) wounded pine seedlings on one side of the main
stem and waited until it was almost completely healed by formation of callus tissue
before exposing the plants to weevils in a bioassay. Where weevils had access to
both wounded and unwounded seedlings, wounded seedlings were attacked first,
apparently because weevils were attracted to monoterpenes released from the
incompletely closed wounds. However on the wounded plants, most feeding
occurred on the unwounded side suggesting that the risk of girdling had been
reduced (Fig 6). Reduced feeding on the wounded side was attributed to the higher
induced concentration of resin acids. Some feeding however, occurred above the
wound on the wounded side of the stem apparently due to the higher concentration
of carbohydrates and other nutrients that accumulated because the wound blocked
downward transport. These results indicate that weevils are sensitive both to the
nutritional and defensive status of the bark on which they feed.
Evidence of species variation in tolerance of attack also comes from laboratory
experiments with wounded seedlings. When one year old Scot s pine and Norway
Figure 6. The effect of mechanical stem wounding on subsequent feeding damage by Hylobius
abietis. The wounds made on one side of the stem had largely callused over at the start of the
experiment but weevils feed most on the unwounded side. Data summed over two experiments
(From Ericsson et al., 1988).
spruce seedlings were partially girdled on the lower stem by a mechanical wound,
mortality was found to be much higher in spruce than in pine (Långström and
Hellqvist 1989) (Fig. 7). If the tolerance observed in this experiment could be
demonstrated under field conditions and the main factors influencing it identified,
this resistance trait could be of considerable practical significance.
4. HOST PLANT RESISTANCE IN THE MANAGEMENT OF PINE WEEVIL

Several studies of larval development suggest that ‘residual’ resistance contributes
to between and within species variation in larval survival and growth rate. If root-
stumps are most ‘resistant’ immediately after felling, the offspring of weevils
attacking immediately after a spring clearfell may have lower survival than those of
weevils attacking root-stumps of trees felled some months earlier. Field experiments
are therefore needed to determine whether for a given level of attack, the total
population emerging from spring clearfells is less than that from sites clearfelled
when weevil attack does not occur for several months.
Most mass-produced conifer transplants appear to be generally susceptible to
high levels of attack by H. abietis. Different methods of nursery production and in
376 D. WAINHOUSE
particular, plant size affect the survival of transplants on clearfell sites. Studies of
resistance mechanisms indicate a possible role for induced resistance and tolerance
but further studies are needed to confirm this and to show how plant phenotype
influences resistance expression. With increasing restrictions on insecticide
application in forests, the use of plants able to resist at least moderate levels of
weevil attack will be essential for the development of an effective Integrated Pest
Management programme against this important European pest.
Figure 7. Mortality of pine and spruce seedlings planted out for one year after partial
girdling of the stem. Plants were two years old at the end of the experiment, with stem
diameters ranging from 3-3.9 mm (From
F Långström and Hellqvist 1989).
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Chapter 17
FUNGI ASSOCIATED WITH HYLOBIUS ABIETIS

S AND
OTHER WEEVILS
H. VIIRI
Finnish Forest Research Institute, Juntintie 40, FIN-77600 Suonenjoki, Finland
1. INTRODUCTION
Many weevils (Coleoptera: Curculionidae) carry fungal spores to their host trees.
According to Leach (1940), an insect can be considered to be a vector if it 1) is
consistently associated with an infected plant in the field, 2) visits healthy host
plants under conditions when infection is possible, 3) carries pathogen inoculum
with it in the field, and 4) is able to transmit the pathogen to a healthy plant under
controlled conditions. Most of the well-known weevil-fungus associations are from
North American species carrying root-rot or staining fungi. The association of
European weevils with fungi has so far not been reviewed extensively, and research
focused solely on transmission of fungi is scarce. In many cases associations
between weevils and fungi have been found as extra information in investigations
set up to study different topics, e.g. spread of the pathogenic root-rot fungus
Heterobasidion annosum coll. (Fr.) Bref.
In weevils, association with fungi is closely connected with the phloephagous
feeding guild, which involves feeding on the fresh, highly nutritive phloem and
inner bark. The weevils that make large patches of feeding scars with their chewing
mouthparts are the possible inoculum agents of harmful fungi. During their
emergence from pupal chambers and galleries, most weevils are contaminated both
internally and externally with fungal spores.
Generally, for transmitting fungi, bark beetles are more important than weevils
(Whitney 1982; Harrington 1988; Beaver 1989). Very few true Curculionidae have
developed a mutualistic association with fungi (Bright 1993). Consequently, none of
the weevils have mycangia or similar structures for transporting fungi. This suggests
that primitive Curculionidae did not require fungi to aid in host discovery and
utilisation and thus followed a different evolutionary pathway (Bright 1993). The
most harmful European weevil, the large pine weevil Hylobius abietis L., feeds on
seedlings but breeds mainly in stumps and roots. Overall, it is questionable whether
381
381–393.
© 2007 Springer.
382 H. VIIRI
there are any direct benefits for large pine weevil about fungal associates, as they
compete for the same resources.
Disparate genera of ophiostomatoid fungi have evolved similar structures as
adaptations to insect dispersal. From the standpoint of fungi, reliable spore dispersal
and inoculation to a suitable habitat are crucial.
r Further, direct penetration through
the cell walls is an effective method of dispersal. Most fungi associated with
European weevils seem to be only slightly or moderately pathogenic and are
introduced to stressed trees. Among the few exceptions are the highly pathogenic H.
annosum (Jørgensen and Beier Petersen 1951; Laine 1977) and the causal agent of
resin-top disease Peridermium pini (Pers.) Lév (Pappinen and von Weissenberg
1994a, b, 1996). The prevalence of insects and fungi varies, and in European
weevils it seems that the opportunity for contact with pathogenic fungi is occasional
and occurs when population density is high.
In Europe the number of pathogenic weevil-disseminated root diseases in pole-
size and mature conifers is lower than in North America. It appears that the root-
collar zone, used e.g. by Hylobius warrenii Wood (Cerezke 1994) and Hylobius
pinicola (Couper) in the boreal forest in Canada, seem to be used less effectively in
Europe than in North America. The unique type of wilting disease, black-stain root
disease, spread by root-feeding insects and caused by the fungus Leptographium
wageneri (Kendrick) Wingfield has limited occurrence in Europe compared to
Western North America where the disease commonly occurs (Morelet 1986).
Further, in the genus Hylobius there are seven species in North America, whereas in
Europe there are only four species, of which only three live on conifers. In Europe,
we have no harmful species of the genus Steremnius or Pachylobius. Nevertheless,
among the European curculionids there are some potential fungal vector candidates
(Table 1).
2. BLUE-STAIN FUNGI ASSOCIATED WITH EUROPEAN WEEVILS
2.1. Hylobius abietis

Species off Leptographium are anamorphs of Ophiostoma H. & P. Sydow
(Ascomycetes). Although some of these species are associated with transmission by
specific bark beetles, most of them are associated with a broad group of bark beetles
and curculionids. Leptographium procerum (W.B. Kendr.) Wingf. is known to be
distributed worldwide, mostly in pines and spruce. It has been isolated e.g. from
Canada, Croatia, England, Finland, France, New Zealand, Norway, Poland, South
Africa, Sweden, and the USA (Kendrick 1962; Hallaksela 1977; Halambek 1976;
Jacobs and Wingfield 2001). The fungus, when inoculated into two-year-old Pinus
strobus L. seedlings, caused mortality (Halambek 1976).
In Europe, the fungus does not have a well-recognized insect vector; but both sexes
of the large pine weevil have been found to carry L. procerum (Lévieux et al.
1994a). Fungal spores are located on the dorsal and lateral sides of the pronotum,
especially anteriorly. Sticky masses of spores are situated in cuticular depressions
associated with the pronotal setae. According to Piou (1993), 3-47% of the emerging
FUNGI ASSOCIATED WITH WEEVILS 383
large pine weevils and 18 % of the seedlings killed by pine weevil were infected
with L. procerum. In addition, in France the staining fungi Leptographium
wingfieldii Morelet (7%), Ophiostoma canum (Münch) H. & P. Sydow (2%) and O.
piliferum (Fries) H. & P. Sydow (1-3%) have been detected in low frequencies on
emerging pine weevils (Piou 1993). Furthermore, Leptographium alethinum Jacobs,
Wingf. & Uzunovic has been isolated from the galleries of the pine weevil in
England and Scotland. This species has recently been distinguished from L.
procerum by the absence of rhizoids (Jacobs et al. 2001). The pathogenicity,
distribution and overall significance of L. alethinum or the other possible stain-fungi
associates of pine weevil are not known. The structural variation of the
conidiophores, however, suggests the presence of various fungi (Lévieux 1994a).
2.2. Pissodes weevils

In France, about 10 % of the Pissodes piceae Illiger individuals carry O. canum and
O. ips (Rumb.) Nannf., indicating a low rate of infestation on fir (Lévieux 1994b).
The largest patches of spores were located on the sides of the pronotum and
sometimes on the elytra and rostrum. Ophiostoma minus (Hedgcock) H. & P.
Sydow, Ophiostoma pini, Ceratocystiopsis minuta (Siem.) Upad. Kendrick, O.
piceae (Münch) H. & P. Sydow, O. pluriannulata (Hedgcock) H. & P. Sydow, O.
stenoceras (Robak) Melin & Nannf. and Aureobasidium pullulans (de Bary) Arnaud
have sometimes been found associated with Pissodes pini L. (Mathiesen-Käärik
1953, 1960). O. minus is found sporadically with a number of bark beetles and thus
its association with P. pini cannot be included among the specific associations
(Mathiesen-Käärik 1960.)
According to Löyttyniemi and Uusvaara (1977), Pissodes larvae found in pine
and spruce logs did not cause discoloration during six weeks of storage. If the logs
were felled in southern Finland at the beginning of July or earlier, some logs became
partly blue by the end of September, especially in the vicinity of the pupal chip cells.
In the same study, most of the weevil individuals caught in window traps were P.
pini; only a few specimens of P. piniphilus (Herbst) and P. harcyniae (Herbst) were
trapped, but there is no direct evidence of specific fungal transmission.
3. VECTORS OF DECAY FUNGI

Larvae of the large pine weevil have been detected in the roots of Scots pine
infected with the root-rot fungus H. annosum (Jørgensen and Beier Petersen 1951;
Laine 1977). In the field, seedlings killed by root-rot are often wounded by the
gnawing of pine weevils. Even small fruiting bodies are sometimes found around
feeding scars made by the pine weevil (Laine 1977). H. annosum has been isolated
from the excrement of large pine weevils collected in the field in Czech Republic
(Kadlec et al. 1992). Furthermore, both the mycelium and the conidia of H.
annosum have survived in viable condition through the digestive tract of the large
pine weevil (Nuorteva and Laine 1972; Dušin 1979). However, on the basis of these
experiments, it is unclear whether mycelium actually survived through the pine
384
Table 1. Root- and phloem-feeding weevils (Coleoptera: Curculionidae) and associated fungi.
Insect Fungus References

Hylobius sp. Leptographium procerum Jacobs et al. 2001
Hylobius abietis Heterobasidion annosum Nuorteva & Laine 1968; Laine 1977; Kadlec et al. 1992
Leptographium alethinum Jacobs et al. 2001
Leptographium procerum Piou 1993; Lévieux et al. 1994a
Leptographium wingfieldii Piou 1993
Graphium canum Piou 1993
Ophiostoma piliferum Piou 1993
Hylobius pales Leptographium procerum Lackner & Alexander 1982; Wingfield 1983; Lewis & Alexander,
1986; Alexander et al. 1988; Klepzig et al. 1991; Nevill &
Alexander, 1992a,b,c
H. VIIRI
Ophiostoma ips Klepzig et al. 1991

Ophiostoma piceae Nevill & Alexander 1992a,c
Graphium sp. Klepzig et al. 1991; Nevill & Alexander 1992a
Hylobius radicis Ophiostoma ips Klepzig et al. 1991
Leptographium procerum Wingfield 1983; Alexander et al. 1988; Klepzig et al. 1991
Leptographium terebrantis Wingfield 1983; Klepzig et al. 1991
Graphium sp. Klepzig et al. 1991
Hylobius assimilis Leptographium procerum Wingfield 1983; Alexander et al. 1988
(=H.
= rhizophagus) Leptographium terebrantis Wingfield 1983
Pachylobius picivorus Leptographium procerum Wingfield 1983; Klepzig et al. 1991
Pissodes spp. Ophiostoma ips Klepzig et al. 1991
Leptographium procerum Livingston & Wingfield 1982; Lewis & Alexander 1986
Armillaria mellea Livingston & Wingfield 1982
Table 1. (continuation)
Insect Fungus References

Pissodes approximatus Leptographium procerum Lackner & Alexander 1982; Alexander et al. 1988
Pissodes castaneus Armillaria spp. Ehnström & Axelsson 2002
Cronartium flaccidum Alauzet 1972
Ophiostoma spp. Lévieux et al. 1994b
Pissodes fasciatus Leptographium wageneri Witcosky & Hansen 1985; Witcosky et al. 1986a; Witcosky 1989
Pissodes nemorensis Leptographium procerum Lackner & Alexander 1982; Nevill & Alexander 1992a b,c
Ophiostoma piceae Nevill & Alexander 1992a,c
Graphium sp. Nevill & Alexander 1992a
Pissodes piceae Ophiostoma canum Lévieux et al. 1994b
Ophiostoma ips Lévieux et al. 1994b
Pissodes pini Ophiostoma minus Mathiesen-Käärik 1953, 1960
Heterobasidion annosum Kangas 1938; Jørgensen & Beier Petersen 1951; Nuorteva &
Laine, 1968; Laine 1977
Leptographium procerum Kendrick 1962; Livingston & Wingfield 1982
FUNGI ASSOCIATED WITH WEEVILS
Leptographium lundbergii Mathiesen-Käärik 1953

Aureobasidium pullulans Mathiesen-Käärik 1960
Pissodes piniphilus Peridermium pini Kangas 1934; Pappinen & von Weissenberg 1994a,b
Lachnellula pini (Brunch.) Kangas 1938
Dennis
Ceratocystiopsis minuta Mathiesen 1951
Steremnius carinatus Leptographium wageneri Witcosky & Hansen 1985; Witcosky et al. 1986a; Witcosky 1989
385
386 H. VIIRI
weevil digestive tract or whether the mycelium was originally contaminated with the
conidia.
It has been suggested that a succession of fungi in roots wounded by Hylobius
begins with the hyphomycetes or by other fungi usually not considered capable of
causing extensive decay in wood and that later succession is followed by the decay
fungi (Whitney 1961). Thus, in the Great Lakes region, H. annosum and Armillaria
spp. have not been isolated from declining red pine, Pinus resinosa Ait. stands
associated with the complex of scolytids, curculionids, Leptographium and
Ophiostoma fungi (Klepzig et al. 1991; Erbilgin and Raffa 2002). Most decay fungi
(except for Armillaria and some others) infect the stump from a cut surface. They
grow relatively slowly down to the roots and in the early phases of colonization
probably do not affect the suitability of the substrate for insect breeding. Nor are the
larger roots, where the pine weevil breeds, reached rapidly by the soil fungi that
penetrate the thin roots (von Sydow 1993). Consequently, it seems that the large
pine weevil and most weevils breed without fungal interaction.
In Finland, larvae and pupae of Pissodes pini have been detected at the stem base
of H. annosum- infected Scots pine (Nuorteva and Laine 1968). Fruiting bodies of
H. annosum have also been found near the feeding wounds of P. pini (Nuorteva and
Laine 1968; Laine 1977). In Denmark, Jørgensen and Beier Petersen (1951) have
found P. pini gnawing trees infected by H. annosum. However, in all these cases it is
unclear whether P. pini attacked trees weakened by root rot or whether the weevil
fed first and root rot came later. Of the European Pissodes species, on some
occasions P. pini has been speculated to be a primary pest on mature conifers.
4. VECTORS OF RESIN TOP DISEASE

The pine-top weevil, P. piniphilus, is considered to a important pest in Europe.
However, the primacy of P. piniphilus has not yet been solved. Tomicus piniperda
and Tomicus minorr often attack trees where P. piniphilus has been breeding in a
previous year (Ehnström and Axelsson 2002). The pine-top weevil and the small-
banded pine weevil, Pissodes castaneus (De G.), often breed in pines that are
weakened by resin-top disease caused by a rust pathogen Peridermium pini (Kangas
1934; Kudela 1974). On Pinus pinasterr Ait. the association of P. castaneus with
resin top disease caused 62% mortality, whereas mortality was lower in trees
infected by the fungus alone (Alauzet 1972). However, also in all these cases it is
unsure whether host trees were weakened by the fungus before weevil breeding or
whether the fungus was disseminated after the weevil arrived.
Pappinen and von Weissenberg (1994a) found a positive correlation between P.
piniphilus pupal chambers and disease frequency. The weevils were associated with
stands that were heavily infected by the resin-top disease. The presence of canker
favoured the breeding of P. piniphilus, while the number of pupal chambers was
largest in the region of the canker. P. piniphilus has been found to carry spores in
both field and laboratory conditions (Pappinen and von Weissenberg 1994b).
Weevils were able to carry spores and infect healthy trees with spores while the time
of weevil emergence and the development of new aecia were overlapping (Pappinen
and von Weissenberg 1994a, b).
In a feeding test, P. piniphilus preferred diseased branches significantly more
than healthy branches (Pappinen and von Weissenberg 1996). Furthermore, weevil
feeding increased the germination off P. pini aeciospores on pine phloem and needle
extracts. Especially in rust fungi, insect transfer leads to cross-fertilization, brings
one mating type to another and results in high levels of local genetic diversity (Hunt
1985; Webber and Gibbs 1989; Hamelin 1996). Thus the migration and breeding
habits of weevils may affect the incidence of disease on host trees.
5. ROOT DISEASES IN NORTH AMERICA
5.1. Black-stain root disease

Leptographium wageneri, which causes black-stain root disease, is characterized by
dark staining in the roots and lower stem of mature conifers. L. wageneri colonizes a
tree tangentially along the growth rings and thus only along the actively conducting
xylem tracheids of the roots and stems, whereas radial growth is minor (Harrington
and Cobb 1983). The disease fulfils the requirements of wilting disease by blocking
water transport and finally leading to a decrease in the terminal growth of infected
trees (Witcosky and Hansen 1985). Black-stain root disease is thought to be a native
disease of Douglas-fir Pseudotsuga menziesii (Mirb.) Franco in western North
America. There are three recognized host-specialized varieties, L. wageneri var.
wageneri M.J. Wingf., which is pathogenic to pinions, the variety ponderosum T.C.
Harr. & F.W. Cobb, which specializes on western hard pines, and the variety
pseudotsugae T.C. Harr. & F.W. Cobb, which causes black-stain on Douglas-fir and
hemlock species (Harrington and Cobb 1986; Zambino and Harrington 1989).
A root-feeding bark-beetle, Hylastes nigrinus (Mannerheim), and the root-
feeding weevils Steremnius carinatus (Boheman) and Pissodes fasciatus LeConte
are among the primary vectors (Harrington et al. 1985; Witcosky and Hansen 1985;
Witcosky et al. 1986a; Hansen et al. 1988). In infected areas, apparently low
numbers of vector insects, up to 5%, may be infested with L. wageneri during
emergence and dispersal (Harrington et al. 1985; Witcosky et al. 1986a). S.
carinatus causes, in particular, the tree-to-tree spread of the pathogen around
established infections, while wounds caused by y P. fasciatus are encountered less
frequently on diseased trees (Hansen et al. 1988). Adults of S. carinatus are
flightless, and P. fasciatus feeds only on dead and dying trees, which restricts their
ability to spread root pathogens. However, both weevils carry L. wageneri in the
field, transmit the fungus to host trees, and feed or oviposit on susceptible hosts
under conditions suitable for transmission of L. wageneri, thus fulfilling the
postulates of the vector hypothesis (Leach 1940; Witcosky and Hansen 1985;
Witcosky et al. 1986a).
Black-stain root disease is most often found in 5- to 30-year-old plantations that
have been pre-commercially thinned (Harrington et al. 1983, 1985; Hansen et al.
1988; Witcosky et al. 1986a, b). Clear cutting and thinning activities increase weevil
388 H. VIIRI
populations at such sites (Harrington et al. 1985; Witcosky et al. 1986a, b). Even in
the absence of vector activity, the fungus can cause mortality of seedlings and large
trees through root graft transmission (Hessburg and Hansen 1986; Harrington 1988).
In areas with high risk of black-stain root disease, thinning should be avoided or
done immediately after the flight period so that the host material can age and lose
much of its attractiveness (Witcosky et al. 1986b; Witcosky 1989). Forest
management has created favourable conditions for root-feeding insects and for the
fungus causing black-stain root disease.
Damage due to the black-stain root disease in thinned stands has been suggested
to be a result of the behavioural preferences of its insect vectors. Large areas of
young susceptible stands have increased the occurrence of root disease. The fungus
L. wageneri does not have cellolytic enzymes for penetration of cell walls. Different
host-specialized varieties of black-stain fungi attack Douglas-fir and lodgepole pine
Pinus contorta Dougl. ex Loud. All these features together indicate that the fungus
is able to adapt to different habitats; and they make black-stain root disease
extremely harmful, if it manages to spread into managed forests in Europe.
5.2. Leptographium terebrantis

Leptographium terebrantis Barras and Perry is, together with L. procerum, among
the causal agents of red pine decline on P. resinosa in the United States. L.
terebrantis causes the black-staining of primary roots, lesions in the phloem and
resin-soaking areas in the lower stem and root-collar (Harrington and Cobb 1983;
Raffa and Smalley 1988). The typical symptoms in a forest are openings formed by
dead and diseased trees in various stages of decline. This fungus is weakly
pathogenic and colonizes, in particular, stressed or wounded conifers. L. terebrantis
and L. wageneri are more virulent than L. procerum (Harrington and Cobb 1983;
Wingfield 1983, 1986).
The fungus is associated with various bark beetles, D. terebrans Oliver, D.
valens LeConte and Hylurgops porosus (LeConte) (Harrington and Cobb 1983;
Owen et al. 1987); but it has also been isolated from trees infested by the root-collar
weevil H. radicis Buchanan (Wingfield 1983; Klepzig et al. 1991). However, in the
absence of L. procerum Wingfield (1983) could not isolate L. terebrantis from any
of the trees infested by the root-collar weevil. Thus, the role of the fungus in this
disease is speculative – neither of the abovementioned fungal agents have been
shown to cause the disease independently.
5.3. Procerum root disease

Leptographium procerum is common on pines and is speculated to cause white pine
root decline on P. strobus. The symptoms are presence of resinous streaks from
roots to stem base, sapwood discoloration, decreased shoot growth and needle
wilting. The weevils and bark beetles transmit the fungus from infected
f trees to the
roots of healthy but stressed trees. L. procerum is considered to be a weak wound
pathogen that is unable to kill seedlings when wound-inoculated into a stem
(Harrington and Cobb 1983; Wingfield 1983). The pathogenicity of this species has
been a matter of substantial debate (Jacobs and Wingfield 2001). The discrepancy
may be caused by different inoculation methods, variation in the pathogenicity of
fungal strains or simply that the fungus is not a primary pathogen.
Leptographium procerum is associated with several root and root-collar infesting
insects in the eastern parts of North America. Mainly the pine-reproducing weevils,
Hylobius pales Herbst, H. radicis, H. assimilis (Bohemann) ((H. rhizophagus M., B.
& W.), Pachylobius picivorus (Germar) and Pissodes nemorensis Germar, carry L.
procerum (Wingfield 1983; Lewis and Alexander 1986; Alexander et al. 1988;
Raffa and Smalley 1988; Nevill and Alexander 1992b, c). Furthermore, L. procerum
is found in the galleries of Pissodes approximatus Hopkins (Herbst) on pine
(Wingfield 1983; Alexander et al. 1988). Under controlled conditions, weevils seem
to transmit L. procerum to fresh white pine bolts more effectively than bark beetles
do (Lewis and Alexander 1986). In addition, L. procerum is commonly isolated
from surface-sterilized H. radicis, H. pales and P. picivorus, and less frequently
from D. valens (Wingfield 1983).
As the pathogen spreads throughout the root collar, the infected tissue becomes
more suitable for weevil oviposition and breeding. H. pales and P. nemorensis
normally oviposit in stressed or diseased trees, not on healthy ones, as H. radicis
does. H. radicis causes symptoms on pines similar to those associated with white
pine root decline, although it seldom infests five-needle pines (Wingfield 1983,
1986). Wingfield (1983) isolated L. procerum from roots that had been recently
damaged by weevils, but not from roots damaged during previous years and already
decaying. Furthermore, the low recovery of the fungus from the soil suggests
dissemination by the insect (Lewis et al. 1987). Leach’s postulates about the
vectorship are fulfilled when weevils transmit L. procerum. At first, weevils are
associated with diseased trees (Leach 1940; Lackner and Alexander 1982; Wingfield
1983, Nevill and Alexander 1992b). Secondly, weevils are found with their host
trees during their whole life cycle (Raffa and Klepzig 1996). Furthermore, H. pales
and P. nemorensis weevils carry L. procerum in the field (Wingfield 1983) and
finally, weevils are able to transmit the fungus to a healthy plant (Lackner and
Alexander 1982; Lewis and Alexander 1986; Nevill and Alexander 1992c). It is
important to note that Leach's postulates relate to the vectorship – but Koch's
postulates are a prerequisite to show primary pathogenicity – for L. procerum and L.
terebrantis (in the field) this has never been achieved.
6. CONCLUSIONS
The ecological role of root-feeding weevils and the fungi with which they are
associated is obscure. If weevils are associated with fast-growing pathogenic fungi,
they compete for the same nutrient resources. This points out what Berryman (1989)
has suggested that co-adaptation of the weevils with fungal pathogens is not an
evolutionarily stable strategy.
In L. wageneri, the sexual state of Ophiostoma wageneri (Goheen and F.W.
Cobb) T.C. Harr. has been found only in the galleries of Hylastes; thus it is possible
390 H. VIIRI
that the fungus needs root-inhabiting insects to bring the compatibility types
together (Goheen and Cobb 1978). Whether lack of a functional sexual state is an
indication that the weevils play some role in dissemination of root-infecting
pathogens, is a highly speculative idea.
On white pine it has been demonstrated that adult weevils locate and oviposit on
trees with roots diseased by L. procerum in advance of bark beetles (Nevill and
Alexander 1992b). Whether European root-feeding weevils play a special role in
inhabiting weakened seedlings and trees before the bark beetles remains to be
solved.
The phrase “out of sight, out of mind” describes well the role of subterranean
and sub-cortical insects in many ecosystems (Hunter 2001). In many cases,
delimitation of species for instance within Leptographium is difficult and requires
studies on the ultra-structure of fungal spores. Difficulties in identification may have
inhibited detection of associated fungi. Both in the assessment of root-feeding insect
abundance and their possible fungal associates, there is a clear gap in our
knowledge.
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Chapter 18
PARASITOIDS, PREDATORS, NEMATODES AND

PATHOGENS ASSOCIATED WITH BARK WEEVIL
PESTS
M. KENIS 1, R. WEGENSTEINER
R 2 & C. T. GRIFFIN 3
1
2
of Forest Entomology, Forest Pathology & Forest Protection, A-1190 Wien, Austria
3
National University of Ireland, Maynooth, Co. Kildare, Ireland
1. INTRODUCTION
Among the main bark weevil pests in Europe, Hylobius abietis L. and Pissodes spp.
have been thesubject of several major studies regarding the biology, impact and use
of their natural enemies. In particular, parasitoids and nematodes of H. abietis, and
parasitoids of pine and fir Pissodes spp. have been extensively studied. In contrast,
very little has been done on Cryptorrhynchus lapathi L., and nothing on Hylobius
pinastri (Gyllenhal), or on Otiorrhynchus spp. in the forest environment, probably
reflecting their lower importance in forest protection.
2. HYLOBIUS ABIETIS
2.1. Parasitoids
Compared to other bark and wood boring insects, H. abietis has a very limited
parasitoid complex. Eight to ten parasitoid species are recorded from the weevil, but
no single study on the life history of H. abietis mentioned more than three
parasitoids (e.g. Munro 1929; Hanson 1943; Elton et al. 1964; Gerdin and Hedqvist
1985; Henry 1995) (Table 1). This restricted parasitoid complex is probably due to
the fact that larvae are concealed beneath soil and thick bark and, thus, are not
accessible to polyphagous parasitoids attacking other bark weevils or bark beetles in
conifers.
395
395–414.
© 2007 Springer.
396 M. KENIS, R. WEGENSTEINER & C.T. GRIFFIN
Table 1. Parasitoids recorded

d in the literature from Hylobius abietis and their biology.
Names in bold refer to frequent parasitoids reported
e from a least three different studies.
Other names were mentioned in only one study. References are in the text..
Biology
Hym. Braconidae
Allodorus lepidus (Haliday) Egg-larval koinobiont endoparasitoid ?
Aspilota sp. Adult endoparasitoid, very unlikely record.
See text
Bracon hylobiii Ratzeburg 1 Larval idiobiont ectoparasitoid
Perilitus areolaris Gerdin & Adult endoparasitoid
Hedqvist2
Hym. Ichneumonidae
Dolichomitus tuberculatus Larval (and pupal?) idiobiont ectoparasitoid
(Geoffroy)
Stenarella gladiatorr (Scopoli) Unknown, but very unlikely record. See text
Hym. Pteromalidae
Tomicobia sp. Adult endoparasitoid
Dipt. Phoridae
Megaselia plurispinulosa Zetterstedt Larval koinobiont endoparasitoid ?
1
Some records as Bracon brachycerus Thomson, probably a misidentification
2
Some records as Perilitus rutilus (Nees), probably a misidentification
Adults are commonly attacked by Perilitus areolaris Gerdin and Hedqvist

(Hym.: Braconidae) (Gerdin and Hedqvist 1985; Starý et al. 1988). Earlier studies
mentioned Perilitus rutilus (Nees) as parasitoid of H. abietis adults (e.g. Schindler
1964; Novák 1965; Slizynski 1969), but recent taxonomic studies (Starý et al. 1988;
Haeselbarth 1999) suggested that P. rutilus was a misidentification of P. areolaris,
which is known only from H. abietis, whereas P. rutilus is a parasitoid of weevils of
the genera Sitona and Phytonomus. Schindler (1964) provides data on the life cycle
of P. areolaris (as P. rutilus) in Germany. The parasitoid has two generations per
year on H. abietis. It overwinters as a larva, in the adult weevil or in a cocoon. One
to nine specimens emerge from a single host. Impact on beetle populations is
difficult to measure for adult parasitoids. Schindler (1964) found 1-4% parasitism in
field-collected samples in Germany, and Novák (1965) 15-16% in Czechoslovakia
but, given the long life span of beetles, the short life of parasitized beetles and the
two generations per year of parasitoids, the percentage of beetles eventually killed
by the parasitoid is probably much higher. Further details on the biology of P.
areolaris, such as larval development, mating and oviposition behaviour, are given
in Slizynski (1969) and Gerdin and Hedqvist (1985). Schindler (1964) mentions
Aspilota sp. (Hym.: Braconidae) as a rare parasitoid of adult H. abietis, but this
record is very dubious because Aspilota species are known to parasitise Phoridae
(Diptera). Långström (1972) also observed two parasitoids of adult H. abietis in
Finland, Pygostolus sp. (Hym.: Braconidae) and Tomicobia sp. (Hym.:
Pteromalidae). Since only larvae were obtained, Pygostolus sp. may be a
NATURAL ENEMIES OF BARK WEEVILS 397
misidentification for Perilitus areolaris. Tomicobia spp. are known parasitoids of

Scolytidae and Curculionidae, but have not been reported elsewhere from H. abietis.
H. abietis larvae are attacked by att least two parasitoids, Dolichomitus
tuberculatus (Geoffroy) (Hym.: Ichneumonidae) and Bracon hylobiii Ratzeburg
(Hym.: Braconidae). D. tuberculatus has often been reared from H. abietis, but
always at low level (e.g. Munro 1929; Hanson 1943). Little is known of the biology
of this parasitoid on H. abietis. It has also been reared from the weevil C. lapathi
(see below) and from Cerambycidae (Fitton et al. 1988; Kenis and Hilszczanski,
chapter 21) and, as other Dolichomitus species, it is most certainly an idiobiont
ectoparasitoid of mature larvae or pupae.
B. hylobii is by far the most important and the most studied parasitoid of H.
abietis. It is a gregarious ectoparasitoid of H. abietis larvae. Females lay four to 12
eggs on the weevil larvae. Laboratory experiments showed that females laid more
eggs and spent much more time on larger larvae than on smaller larvae. Only larvae
heavier than 100 mg were parasitized (Henry and Day 2000). In the laboratory,
females gave rise to a maximum of 93 offspring and up to 17 host larvae were
parasitised by a single female (Henry 1995). B. hylobii has five larval instars
(Munro, in Hedqvist 1958). The last larval instar builds a cocoon in which it
overwinters. Pupation and adult emergence occur in spring. In the UK, it was
observed causing 30% parasitism in pine (Munro 1929) and an average of 47 % in
Sitka spruce (Henry and Day 2001), but has a non-uniform distribution within sites.
It was long assumed that B. hylobii is able to attack only larvae that occur at the
level of the ground (Hedqvist 1958) and, therefore, would be incapable of
parasitizing the majority of larvae that live under the bark deeper in the soil.
However, a recent study (Henry and Day 2001) showed that, on Sitka spruce in the
UK, most host larvae were reachable by B. hylobii. Parasitized larvae were found at
depths of up to 15 cm and, on average, occurred at greater depth than healthy larvae.
B. hylobii seems to be rather specific. The only other hosts known are weevils of
the genus Pissodes (Hedqvist 1958). A closely related species, Bracon brachycerus
Thomson has been reported from H. abietis (see Hedqvist 1958; Herting 1973,) but
Hedqvist (1958) supposes that these were misidentificatons for B. hylobii.
The use of B. hylobii as a biological control agent has often been discussed.
Munro (in Hedqvist 1958) was the first to suggest its use as a mean of control. More
recently, Henry and Day (2000, 2001) proposed and tested several control methods
involving augmentation or conservation of B. hylobii. Some 40,000 adult parasitoids
were reared in the laboratory and released onto forest clear fells in their first two
summers. Parasitism in these plots was three times higher than in control plots
(Henry and Day, 2001). However, the prospects of using B. hylobii in inundative
releases are limited by the high costs usually related to mass production of specific
parasitoids. Henry and Day (2000, 2001) also suggest sylvicultural methods to
increase the impact of B. hylobii, which could be used in combination with other
control methods. For example, B. hylobii will lay fewer eggs on smaller larvae, thus
parasitizing higher numbers of small larvae than large larvae. Therefore, they
anticipate that increasing resistance in the larval weevils’ feeding substrate may have
not only a direct effect on weevil mortality but also an indirectt effect through an
increase in parasitism rate. Provision of food

f for parasitoid adults has also been
suggested. Finally, some forest site conditions known to reduce the level of
parasitism, such as brash heaped on site after felling and needle litter lying over
bark, could be easily modified to favour the activity of B. hylobii. However, more
studies are needed, particularly on host-location behaviour and on reproduction in
the field, to properly assess the possible impact of these methods.
A few other larval parasitoids were mentioned on single occasions in the
literature. Allodorus lepidus Haliday (Hym.: Braconidae) was cited by Györfi (in
Herting 1973), but we have found nothing on the status and biology of this species.
Bramanis (1930) mentions Steranella gladiatorr (Scopoli) (as Mesostenus gladiator)
(Hym.: Ichneumonidae) on H. abietis larvae or pupae in pine stumps in Latvia, with
a parasitism rate of 3.5%. This record is also doubtful because Steranella species are
usually parasitoids of aculeate Hymenoptera. In Sweden, Trägardh (1931) observed
Megaselia plurispinulosa Zetterstedt (Dipt.: Phoridae) on H. abietis larvae in spruce
stumps. Up to 54% of the larvae were found parasitized in one sample, with about 8
to 10 phorid larvae per host. It remains to be seen, however, whether it is a true
parasitoid or a scavenger, as are the great majority of Phoridae. However, it belongs
to a genus which is known to include several parasitoids of various insect orders
(Disney 1994). Furthermore, the structure off its mouthparts suggests a truly parasitic
behaviour (Trägardh 1931).
2.2. Predators
Little is known of predators of H. abietis. Reviews by Escherich (1923), Eidmann
(1974) and Leather et al. (1999) provide lists of possible vertebrate and invertebrate
predators, but nothing is known of their actual impact. Several birds have been
observed feeding on larvae and adults, among which woodpeckers seem to be the
most important (Eidmann 1974). Many insect predators were encountered in and
around pine stumps attacked by H. abietis (list in Leather et al. 1999) but only few
were observed feeding on the weevil. Notable exceptions are Laphria sp. (Dipt.:
Asilidae), which was observed attacking adults, several Carabidae and Elateridae
(Coleoptera), feeding on larvae and adults, and fly larvae, possibly of the genus
Brachyopa (Dipt.: Syrphidae) found beside cadavers in larval galleries (Escherich
1923). The feeding habit of H. abietis larvae probably protects them against
generalist predators. However, larvae may be caught when migrating from one food
source to another. Experiments showed that, during migration, larvae are vulnerable
to carabid predators (Salisbury and Leather 1998). But the real impact of predators
in the field still needs to be evaluated.
2.3. Pathogens
Up to now the occurrence of pathogens in Hylobius abietis and closely related
Hylobius species has been poorly studied, in spite of the importance of these forest
pest insects. In Europe some reports have focused on the occurrence and action of
entomopathogenic fungi in H. abietis but few authors have reported the occurrence
of Protozoa. Pathogens have not been better studied in other species of the genus
Hylobius, including the North America species. A few papers have focused on
entomopathogenic fungi, and only one on a protozoan disease (in H. pales (Herbst):
Walstad et al. 1970, Walstad and Anderson 1971, Schabel 1976, 1978, Schabel and
Taft 1988; in H. rhizophagus Millers: Goyer and Benjamin 1971).
The results of early attempts to use the entomopathogenic fungus Beauveria
bassiana (Bals., Vuill.) against H. abietis in laboratory and field tests were not
always in agreement, and some of them were not very promising (Novák and
Samsinakova 1964, Samsinakova and Novák 1967, Waldenfels 1975).
Investigations on the occurrence of entomopathogenic fungi in field populations of
H. abietis showed that B. bassiana can be found in H. abietis adults (Gerdin, 1977).
In laboratory experiments, B. bassiana was tested against adult H. abietis and it was
shown that high temperatures (> 30°C) were unfavourable (compared to 13° and
23°C). Inoculation with spore suspension led to higher infection rates compared to
inoculation with dry spore powder (Wegensteiner and Führer 1988). The same study
showed that sustained contact with B. bassiana-treated spruce bark caused high
infection rates, and even limited contact of beetles with B. bassiana-treated bark for
three days resulted in 100% infection, but with a long survival time of beetles (81.8
days). A comparative study of the efficacy of B. bassiana and two Beauveria
brongniartii (Sacc., Petch.) strains showed differences in incubation time but high
infection rates with all tested isolates (Wegensteiner 1989). Inoculation of H. abietis
via fortuitous contact with spores of B. bassiana or B. brongniartii on fungus-
overgrown beetles resulted in short survival time and high infection rates. This
observation indicates the importance of a host passage, which is known to increase
virulence (Wegensteiner 1992).
Metarhizium anisopliae (Metschn., Sorokin) has been reported to be very
effective against H. abietis, achieving 100% mortality within 9 days, but significant
strain-dependent differences were found in H. abietis, as well as differences in
susceptibility of H. abietis compared to other insect species (Markova and
Samsinakova 1990, Markova 2000). Some of these authors have mentioned that the
tough, thick cuticle of H. abietis can be an exceptional problem for the effectiveness
of entomopathogenic fungi, at least in prolonging the time to host death.
Pathogens other than fungi are reported from adult beetles. Gregarina hylobii
(Fuchs) was found in the midgut lumen of H. abietis, and Ophryocystis hylobii
(Purrini & Ormieres) in the Malpighian tubules (Fuchs 1915, Geus 1969, Purrini and
Ormieres 1982). Nosema hylobii (Purrini) was described from the cells of the
midgut epithelium of H. abietis (Purrini 1981). All those investigations were basic
studies and concentrated on populations in Germany. Nothing is known of the
effects of these pathogens on their hosts.
2.4. Nematodes
There is little evidence that parasitic nematodes are an important cause of natural
mortality of forest weevils, but entomopathogenic nematodes (Rhabditida:
Heterorhabditidae and Steinernematidae) have potential as inundative biological

control agents of Hylobius abietis.
Nematodes from three orders (Tylenchida, Diplogasterida and Rhabditida) have
been reported from Hylobius abietis larvae. Up to 10% off insects collected in
Denmark harboured Allantonema miribile Leuckart (Tylenchida: Allantonematidae),
a parasite of the body cavity (Bovien 1937), but Wülker (1923) reported that A.
miribile was not particularly pathogenic to pine weevils. Dirhabdilaimus leuckarti
Fuchs (Diplogasterida: Diplogasteroididae) was isolated from dead or moribund
“white, flaccid” larvae of H. abietis in Sweden, but when cultured and tested in the
laboratory was unable to cause disease in H. abietis larvae (Pye and Burman, 1977).
Diplogasterr sp. (Diplogasterida: Diplogasteridae) was found in almost half of the
dead H. abietis larvae field-collected in Sweden, but could not be confirmed as the
cause of death (Gerdin 1977). Most members of the genus feed on dead material.
Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis spp.) are
parasites of insects that normally kill the host and develop in the resulting cadaver.
Their natural hosts include the soil-dwelling stages of many insect species. They are
also in commercial use for the control of several insect pests worldwide.
Steinernema feltiae Filipjev was isolated from m H. abietis in the Czech republic
(Mracek et al. 1993); both adult and larval weevils were infected (Z. Mracek, pers.
comm.). Entomopathogenic nematodes may in certain circumstances result in
epizootics (Peters 1996). Epizootics have not been reported in H. abietis, but up to
30% of Hylobius pales sampled in North Carolina were infected with a Steinernema
sp. (Thomas 1970).
Due largely to their mutualistic association with entomopathogenic bacteria
(
(Xenorhabdus spp. and Photorhabdus spp., respectively), Steinernema spp. and
Heterorhabditis spp. can result in rapid death of their insect hosts, and mass
production is possible on a large scale for inundative application (Burnell and Stock
2000; Gaugler 2002). They have several other attributes that make them suitable as
biological control agents, including safety to humans, plants and non-target
organisms, and active host finding by the infective juvenile (making cryptic hosts,
such as pine weevil larvae in tree stumps, potential targets). Entomopathogenic
nematodes are applied inundatively, and recycling in the host environment is of
secondary importance.
Field trials against adult Hylobius abietis in Sweden and H. congenerr in Canada
showed that treating young seedlings with Steinernema spp. reduced damage due to
adult weevils (Pye and Pye 1985; Eidt et al. 1995). However, extensive field trials in
Scotland by the Forestry Commission using nematodes on containerised and bare
root planting stock did not produce significant reduction in H. abietis feeding
damage to the plants (Brixey 1997). Inadequate control of adult weevils might be
due to failure of nematodes to survive at adequate numbers throughout the Hylobius
feeding season, or may be accounted for by poor susceptibility of the adult weevils
to entomopathogenic nematodes (a dose of 8,800 infective juvenile nematodes/insect
was required to kill 50% of adult weevils (Collins 1993).
Early work in Sweden demonstrated the susceptibility of pine weevil larvae to
Steinernema carpocapsae Weiser (Pye and Burman 1978) and preliminary field
trials showed that application of this nematode had the potential to suppress numbers
of weevils in stumps (Burman et al. 1979). In Scottish field trials, up to 70% of the
population within treated stumps were infected and killed by nematodes (Brixey
1997). More extensive area-wide trials conducted in Scotland by the Forestry
Commission confirm that S. carpocapsae, applied as a spot treatment to stumps,
shows promise for area-wide suppression of H. abietis populations (S. Heritage, pers
comm. 2002). Both the Swedish and Scottish work has concentrated largely on a
single species of nematode, S. carpocapsae. In recent trials in Ireland,
Heterorhabditis downesi Stock, Griffin and Burnell was the most successful of four
nematode species tested in reducing numbers of adult pine weevil emerging from
treated pine stumps (Dillon 2003). Stumps treated with this nematode produced an
average of 8 adult weevils compared to 146 emerging from untreated stumps.
Entomopathogenic nematodes on their own are unlikely to provide adequate control
of pine weevil populations, but they may form an important component of an
integrated pest management system for this pest.
3. PISSODES
S SPP.
3.1. Parasitoids
In the last 40 years, several extensive studies have been published on parasitoids of
five of the eight European Pissodes spp. The pine trunk species Pissodes castaneus
De Geer was studied by Alauzet (1982, 1987), Mills and Fisher (1986), Kenis and
Mills (1994, 1998), Kenis et al. (1996) and Kenis (1996, 1997). Parasitoids of the
two other pine trunk species, P. pini (L.) and P. piniphilus (Herbst) were
investigated by Mills and Fisher (1986), Kenis and Mills (1994, 1998) and Kenis et
al. (1996). The parasitoid complex of the fir trunk species P. piceae (Illiger) was
studied by Haeselbarth (1962), Mills and Fisher (1986), Kenis and Mills (1994,
1998) and Kenis et al. (1996). P. validirostris (Salhberg), inhabiting pine cones, was
the target of important studies by Annila (1975), Roques (1975), Mills and Fisher
(1986), Kenis and Mills (1994, 1998), Kenis et al. (1996) and Kenis (1996, 1997). In
contrast, very little has been done on the parasitoid complex of spruce trunk species,
P. harcyniae (Herbst), P. scabricollis Miller and P. gyllenhalii Gyllenhal, apart from
some old parasitoid records (e.g. Lovaszy 1941; Zinovev 1958). However,
unpublished data on parasitoids of P. harcyniae are provided in Table 2.
Table 2 shows the parasitoid complex of Pissodes spp. in Europe. P.
validorostris, a pest of pine cones, is included in this review for comparison with
congeneric species attacking conifer trunks. Only larval or pupal parasitoids are
known. In all Pissodes spp., parasitism is usually dominated by braconids of the
genera Eubazus and, to a lesser extent, Coeloides. In Pissodes castaneus however,
the ichneumonid Dolichomitus terebrans (Ratzeburg) or the pteromalids Rhopalicus
tutela (Walker) and R. guttatus (Ratzeburg) are occasionally more abundant than the
braconids (Kenis and Mills, 1994). In general, parasitism on Pissodes spp. is higher
than in other bark and wood boring beetles. Parasitism rates above 50% are
common, whereas such high levels are rarely observed in Scolytidae, Cerambycidae
or Hylobius abietis. These high rates can be explained by the accessibility of

Pissodes eggs and larvae. Most parasitism is due to the egg-larval koinobiont
parasitoids Eubazus spp. which have easy access to eggs in Pissodes feeding holes.
Such egg-larval parasitism rarely afflicts Scolytidae, the eggs of which are hidden in
galleries. The other parasitoids are all larval idiobiont ectoparasitoids and are usually
also known from other bark and wood beetles. However, larvae of Pissodes weevils
are particularly accessible because of their large size -compared to other bark
beetles- and their proximity to the bark surface -compared to wood boring beetles.
The biology, ecology and taxonomy of the braconids Eubazus spp. and
Coeloides spp. have been the focus of several studies. Eubazus spp. were
investigated in detail by Haeselbarth (1962) on P. piceae, by Alauzet (1987) on P.
castaneus, by Annila (1975), by Roques (1975) on P. validirostris and by Kenis et
al. (1996) and Kenis and Mills (1998) on all Pissodes spp. Eubazus spp. attacking
Pissodes spp. are specific to this genus and, perhaps, to the genus Magdalis
(Achterberg and Kenis, 2000). They lay their eggs in Pissodes eggs, develop inside
the host larva, and kill their host in the prepupal stage. Then, they build a cocoon in
which to pupate under the bark or in the cone. Until recently, the taxonomy of the
genus Eubazus was confusing. Several species had been described in the past, in
many genera (Eubadizon, Brachistes, Allodorus, Calyptus), but many studies on
Pissodes parasitoids had suggested that a single species attacks all European
Pissodes spp. (Haeselbarth 1962; Annila 1975; Roques 1975; Alauzet 1982; Mills
and Fisher 1986). Very recently, Kenis and his co-workers (Kenis et al. 1996; Kenis
and Mills 1998) used morphometric, molecular and bio-ecological characters to
show the occurrence of three sibling species, each of them m being largely specialised
in different hosts and microhabitats. E. semirugosus (Nees) is a parasitoid of those
Pissodes spp. which develop in pine and spruce trunks, E. robustus (Ratzeburg)
primarily attacks P. validirostris in pine cones and is occasionally found attacking
Pissodes spp. in pine trunks, and the newly described species E. abieticola
Achterberg and Kenis attacks only P. piceae in fir trunks. The taxonomy of the
Eubazus spp. attacking Pissodes spp. throughout the world was revised by
Achterberg and Kenis (2000). Interesting intraspecific variability in developmental
responses was found in Eubazus spp. Mountain biotypes of E. semirugosus and E.
robustus were found to have an obligatory diapause, in contrast to lowlands biotypes
of the same species that were reared on the same hosts without diapause (Kenis et al.
1996). This variation is regarded as an adaptation to the phenology of their hosts in
different climatic conditions. Indeed, the phenology of Eubazus populations is
usually well synchronized with that of the corresponding Pissodes populations.
Three Coeloides spp. are found on Pissodes spp. (Haeselbarth 1967; Kenis and
Mills 1994). C. sordidatorr (Ratzeburg), synonymous with C. melanostigma Strand
and C. stigmaticus Hellén, is a major parasitoid of all pine-feeding Pissodes spp. It
is also known from pine scolytids, cerambycids and buprestids (Haeselbarth 1967),
but records from Pissodes spp. are much more frequent. In contrast, C. abdominalis
(Zetterstedt) is a well-known parasitoid of pine bark beetles (Haeselbarth 1967;
Mills 1983), but it has also been reared in sizeable numbers from P. castaneus and
P. pini (Alauzet 1982, 1987; Kenis and Mills 1994). Finally, C. forsteri Haeselbarth
is a rarer species, which has been reared exclusively from P. pini, P. piceae, P.
piniphilus and P. harcyniae (Haeselbarth 1967; Kenis and Mills 1994). Details on
the biology of C. sordidatorr are given in Annila (1975), Roques (1975), Alauzet
(1987) and Kenis (1996, 1997). C. abdominalis was studied by Alauzet (1987) on P.
castaneus and by Nuorteva (1957) on Scolytidae. The biology of C. forsteri on P.
piceae was described by Haeselbarth (1962) as Coeloides sp. All Coeloides spp. are
idiobiont ectoparasitoids of late instar larvae in feeding galleries. They paralyse and
oviposit on Pissodes larvae through the bark. Parasitoid larvae develop quickly and
build a cocoon in which they overwinter. One or two generations per year
arerecorded by most authors, although Alauzet (1987) counted up to four
generations in southern France. True diapause in C. sordidatorr was observed in the
cocoon stage and was induced by short day photoperiod on the mother and by low
temperature on larvae (Kenis 1997). In an attempt to develop rearing methods for C.
sordidator, Kenis (1996) analysed the factors affecting sex ratio in laboratory
rearing. Three factors were found to influence sex ratio: the host age, the age of
ovipositing females, and the host of origin. Male-biased sex ratios were observed
with young hosts, young females and with C. sordidatorr strains originally from P.
castaneus. Female-biased sex-ratios were observed with older hosts, older females
and with strains from P. validirostris. Competitive interactions between C.
sordidatorr and E. semirugosus were studied by Kenis (1997). C. sordidatorr did not
discriminate between healthy larvae and larvae containing E. semirugosus larvae
suggesting that C. sordidator, and probably other ectoparasitoids, have a negative
impact on E. semirugosus populations. Haeselbarth (1962) made similar
observations with Eubazus abieticola and Coeloides forsteri.
Other braconids have occasionally been reported from Pissodes spp. Bracon spp.
were reared from P. piceae, P. pini and P. castaneus. (Frediani, 1957, Haeselbarth
1962, Alauzet 1982; Kenis and Mills 1994). B. palpebratorr Ratzeburg, B.
praetermissus Marshall and B. hylobii have been mentioned as species, but the
genus is in need of revision. Another species, Spathius rubidus (Rossi), was also
reared in low numbers from P. castaneus, P. pini and P. validirostris (Annila 1975;
Roques 1975; Alauzet 1982; Kenis and Mills 1994, M. Kenis, unpublished)
The ichneumonid Dolichomitus terebrans (Ratzeburg) is frequently associated
with P. castaneus and has also been reared from P. harcyniae, P. pini, P. piniphilus
and P. piceae. The few observations available on the parasitoid complex of P.
harcyniae suggest that D. terebrans is a dominant species in this complex. It is also
known from the scolytid Dendroctonus micans (Kugelann) (Gregoire 1976) as well
as from several microlepidoptera (Aubert 1969), but several of these records may
result from identification errors. In North America, a sub-species, D. terebrans
nubilipennis (Viereck), occurs, which seems to be restricted to Pissodes spp.
(Carlson 1979). D. terebrans is an ectoparasitoid attacking larvae, prepupae or
pupae in pupal cells. In P. validirostris, it is replaced by three other pimpline
ichneumonids, Exeristes ruficollis (Gravenhorst), Scambus sudeticus (Glowacki)
and S. sagax (Hartig) (Roques 1975; Kenis and Mills 1994). A recent paper (Starzyk
1996) provides a list of ichneumonids supposedly reared from P. piceae in Poland:
Baranisobas ridibundus (Gravenhorst), Coleocentrus caligatus (Gravenhorst),
Scambus brevicornis i (L.) and Atract

t odes sp. Since none of these species are known
to attack Curculionidae, these records have to be considered cautiously.
The pteromalids Rhopalicus tutela (Walker), R. guttatus (Ratzeburg) and
Metacolus unif ifasciatus Foerster are ectoparasitoids on larvae in galleries and are
frequently found on P. castaneus. R. tutela has also been occasionally found on P.
pini, P. piniphilus, and P. harcyniae (Kenis and Mills 1994, Kenis, unpublished). R.
guttatus was sometimes reared from pine cones (Hedqvist 1963; Roques 1975),
suggesting that it also attacks P. validirostris. However, Roques (1975) found it
mainly in cones attacked by Dioryctria mutatella Fuchs (Lep.: Pyralidae). M.
unifasciatus is usually associated with pine scolytids whereas R. tutela is a
polyphagous species attacking a large number of bark beetle species (Mills 1983)
and its abundance on Pissodes spp. probably depends on the density of its alternate
hosts in the environment. Its biology, particularly host location mechanism, has been
intensively studied on the scolytid beetle Ips typographus (L.) (e.g. Krüger and Mills
1990; Pettersson 2001; Pettersson ett al. 2001).
Two species off Eurytoma spp. are reared from Pissodes spp. Pissodes
validirostris is often heavily attacked by E. annilai Hedqvist (Annila 1975; Roques
1975). Roques (1976) showed that E. annilai (in Roques mentioned as E. waachtli)
is a cleptoparasitoid of the ichneumonids Scambus spp. E. annilai and E. wachtli
Mayr are occasionally reared from P. castaneus, but their biology is not known.
Kenis and Mills (1994) suggest that they may act as clepto- or hyperparasitoids. An
unidentified Eurytoma sp. has been reared in high numbers from P. harcyniae in
Poland (M. Kenis, unpublished)
Two eupelmids, Calosota aestivalis Curtis and Eupelmus urozonus Dalman were
reared from P. castaneus by Frediani (1957) (as C. vernalis Curtis) and Kenis and
Mills (1994). Whereas Frediani describes them as primary parasitoids, Kenis and
Mills reared them from cocoons of D. terebrans and Coeloides spp., respectively.
Finally, Alauzet (1982) mentions the tarsonemid mite Pediculoides ventricosus
Newport as a parasite of P. castaneus pupae in southern France. However, its
biology and incidence on P. castaneus have not been fully assessed.
High rates of parasitism observed in nearly all studies suggest an important
impact on weevil populations. However, mostt studies on parasitoids were rather
descriptive and no serious attempt has been made to evaluate the real impact of these
parasitoids on the population dynamics of their hosts, or to develop methods to
conserve or augment parasitoids. This perhaps reflects the relatively low importance
of Pissodes spp. in European forestry compared to, e.g., bark beetles or Hylobius
abietis. Ironically, the largest study on parasitoids of Pissodes spp. in Europe was
carried out for the biological control project against the North American Pissodes
strobi, a pest that is far more serious than any of its eight European congenerics
(Kenis and Mills 1994; Hulme and Kenis 2002). Only two authors briefly explore
the potential of parasitoids for the control of Pissodes spp. in Europe. Haeselbarth
(1962) suggests that fir trees infested by P. piceae be cut in spring, between the
emergence period of the parasitoids and that of the weevil. Annila (1975) suggests
strategies to conserve parasitoids of P. validirostris in pine seed orchards in Finland.
Table 2. Parasitoids of Pissodes spp. in Europe, with level of abundance: xxx = Dominant in
at least two studies or samples, and present in >50% of the studies/samples; xx = Dominant
in at least one study/sample or present in >50% of the studies/samples; x = Present in at least
two studies/samples or rearedd for sure from Pissodes sp. by M. Kenis. Based on reviews by
Mills and Fisher (1985), Kenis and Mills (1994) and unpublished surveys by M. Kenis from
1993-1998.
Pissodes species
validirostris
piniphilus
harcyniae
castaneus
Biology1
Parasitoid species
piceae
pini
Hym.: Ichneumonidae
Dolichomitus terebrans (Ratzeburg) L. ec. xxx x x x xxx
Exeristes ruficollis (Gravenhorst) L. ec. x
Scambus sagax Hartig L. ec x
Scambus sudeticus (Glowacki) L. ec. xx
Hym.: Braconidae
Bracon hylobii Ratzeburg L. ec. x x
Bracon praetermissus Marshall L. ec. x
Undetermined Bracon spp. L. ec. x x x
Coeloides abdominalis (Zetterstedt) L. ec. x x
Coeloides forsteri Haeselbarth L. ec. x x x xx
Coeloides sordidatorr (Ratzeburg) L. ec. xxx xx xxx xx
Eubazus abieticola Achterberg & Kenis E.-L. en. xxx
Eubazus robustus (Ratzeburg) E.-L. en. x x xxx
Eubazus semirugosus (Nees) E.-L. en. xxx xxx xxx xxx
Spathius rubidus (Rossi) L. ec. x x x
Hym.: Pteromalidae
Metacolus unifasciatus Foerster L. ec. xx
Rhopalicus guttatus (Ratzeburg) L. ec. xx x x x
Rhopalicus tutela (Walker) L. ec. xx x x xx
Hym.: Eupelmidae
Calosota aestivalis Curtis L. ec. (h) x
Eupelmus urozonus Dalman L. ec. (h) x
Hym.: Eurytomidae
Eurytoma annilai Hedqvist L. ec. x x
Eurytoma wachtli Mayr L. ec. x
Undetermined Eurytoma spp. L. ec. x xx
Acari: Tarsonemidae
Pediculoides ventricosus Newport P. ec. x
1
Biology: L. ec. = Larval idiobiont ectoparasitoid; E.-L. en. =Egg-larval koinobiont endoparasitoid; P. ec.
= Pupal ectoparasite; h = Facultative hyperparasitoid.
Should new control methods against Pissodes spp. be needed, the biology and
ecology of Pissodes parasitoids are sufficiently known to apply this knowledge to
the development of control methods. Similarly, this knowledge could be useful in
case a European Pissodes species becomes invasive in another part of the world,
such as P. castaneus which was introduced into Uruguay and Argentina (Abgrall et
al. 1999). Then, some parasitoids, in particular the specific Eubazus spp., could be
considered as valuable control agents.
3.2. Predators, nematodes and pathogens

Other natural enemies of Pissodes spp. have been studied in much less details than
parasitoids. Undoubtedly, the most important predators are woodpeckers. These are
particularly important for the large species P. piceae and P. pini attacking mature fir
and pine trees. Quantifying their impact is difficult, but Haeselbarth (1962) suggests
that, often, over 50% of overwintering larvae of P. piceae are destroyed by
woodpeckers. Nuorteva and Saari (1980) observed similar damage on P. pini larvae
overwintering in their pupal cell. Fir, pine and spruce trunks debarked by
woodpeckers are a good indication of the presence of Pissodes spp. (M. Kenis,
unpublished).
Insect predators are not considered important mortality factors in European
Pissodes spp. in contrast to North America, where Lonchaea corticis Taylor (Dipt.:
Lonchaeidae) is the main natural enemy of Pissodes strobi (Peck) (Hulme and Kenis
2002). Alauzet (1982) mentions Thanasimus formicarius (L.) feeding occasionally
on young, emerging adults, whereas eggs and feeding larvae are difficult to reach. T.
formicarius has been extensively studied as a predator of bark beetles (Kenis,
Wermelinger and Grégoire, chapter 11). Lonchaeid flies (Haeselbarth 1962),
Nudobius lentus (Gravenhorst) (Col.: Staphylinidae) and Xylophagus cinctus (De
Geer) (Dipt.: Xylophagidae) (Starzyk 1996) were found attacking P. piceae, but
nothing is known of their importance.
Tylenchid nematodes of the genera Sphaerulariopsis (Sphaerularidae) and
Neoparasitylenchus (Allantonematidae) (Siddiqui 2000) are associated with
Pissodes spp. It is notable that these genera also parasitise bark beetles, in which
they may cause pathological effects (Kaya 1984). Other authors reported nematodes
in Pissodes larvae and adults (e.g. Haeselbarth 1962), but nothing is known of the
impact of these nematodes. The potential of entomopathogenic nematodes as a
biological control agent for European Pissodes species has received little attention,
but Laumond et al. (1979) showed that Pissodes castaneus larvae and pupae were
very susceptible to Steinernema carpocapsae in the laboratory.
Dead larvae, pupae and teneral adults are sometimes found covered by fungi
(Haeselbarth 1962; M. Kenis, unpublished), but their identity and role in weevil
mortality has never been investigated. In contrast, dead larvae have often been
observed enveloped in the growing mycelium of Armillaria spp., in particular in P.
piceae (Starzyk 1996) and P. castaneus (M. Kenis, unpublished). Inundative
biological control using pathogens has never been tested against Pissodes spp. in
Europe.
4. CRYPTORHYNCHUS LAPATHI
To our knowledge, no specific studies have focused on the natural enemy complex
of C. lapathi. Old parasitoid records are summarised in Szalay-Marzsó (1962) but,
among the dozen parasitoid species listed in this publication, most are impossible to
accept as parasitoids of C. lapathi. The only investigations on the life history of C.
lapathi and its parasitoids are found in Strojny (1951), who described the
oviposition behaviour of the ichneumonid Dolichomitus tuberculatus (Geoffroy) on
C. lapathi larvae in willow branches, and in Szalay-Marszó (1962), who briefly
described parasitism by the ichneumonid Perosis sp. (probably, but not certainly,
Schreineria sp.) on 5th instar larvae. But there is no information on the abundance of
these parasitoids. Since the review of Szalay-Marzsó (1962), only Schimitschek
(1964) mentioned the braconid Bracon immutatorr Nees, var. austriaca Fahringer, as
a larval parasitoid, but does not provide any data on its abundance and biology.
Szalay-Marzsó (1962) also briefly mentions predation by tits on adults, and by
woodpeckers on larvae. Nothing is known about pathogens or nematodes under
natural conditions; however, the potential of entomopathogenic nematodes for the
control of Cryptorhynchus lapathii was tested by Cavalcaselle and Deseo (1984).
5. OTIORRHYNCHUS
S SPP.
No studies have focused on natural enemies of Otiorrhynchus arcticus Germar and
O. nodosus (Müller), the two species of this large genus considered as seedling pests
in northern Europe. However, information on their potential natural enemy complex
can be gathered from the numerous data on natural enemies of other Otiorrhynchus
spp. in horticulture. Lists of parasitoids are found in Herting (1973), Tschorsnig and
Herting (1994) and Noyes (2001). Parasitoids of adult weevils belong to the genera
Perilitus and Pygostolus (Hym.: Braconidae), Dirhicnus and Tomicobia (Hym.:
Pteromalidae), Pandelleia, and Rondania (Dipt.: Tachinidae), and Megaselia (Dipt.:
Phoridae). Predators are reviewed by Herting (1973) and include the genera Cerceris
(Hym.: Sphecidae), Broscus and Carabus (Col.: Carabidae), Histerr (Col.:
Histeridae) and Formica (Hym.: Formicidae). In general, the parasitoid and predator
complexes of Otiorrhynchus spp. are rather limited, and no attempt has been made
to use these natural enemies as biological control agents.
In contrast, parasitic nematodes are important natural enemies of Otiorrhynchus
spp. In Finland, natural populations of Steinernema feltiae killed 20% of
Otiorrhynchus dubius (Ström) and O. ovatus (L.) larvae in strawberries (Vainio and
Hokkanen 1993). Natural infections of O. sulcatus by entomopathogenic nematodes
(Steinernema carpocapsae S. feltiae and Heterorhabditis megidis Poinar, Jackson
and Klein have also been reported (Poinar 1986; Peters 1996). Numerous trials have
demonstrated the success of entomopathogenic nematodes for the control of
Otiorrhynchus spp. (particularly O. sulcatus (F.)) infesting hardy ornamentals and
soft fruits (e.g. Klingler 1988; Landi 1990; Deseo and Costanzi 1987; Mracek et al.
1993; Fitters et al. 2001), and several nematode-based products are sold for this
purpose. Trials in Ontario demonstrated the potential of heterorhabditids for control
of O. sulcatus and O. ovatus in forest nurseries, provided soil temperatures were
adequate (Rutherford et al. 1987). Considering the success of parasitic nematodes
against Otiorrhynchus spp. in horticulture, it would be highly desirable to evaluate
their potential against O. arcticus and O. nodosus in nurseries and plantations in

northern Europe.
The main pathogens reported from Otiorrhynchus species (O. ligustici (L.), O.
ovatus, O. dubius, O. sulcatus) are entomopathogenic fungi, which can be found in
both larvae and adults of field populations, in some cases at high incidence (Marchal
1977, 1989). Therefore, the potential of such fungi to control Otiorrhynchus was
tested: Metarhizium anisopliae and Beauveria brongniartii caused highest mortality
of weevil larvae in laboratory and field tests (Workshop of the IOBC Study Group
“Insect Pathogens and Insect-parasitic Nematodes” 1987 in Versailles 1989). B.
brongniartii was reported to cause high mortality (up to 100%) of O. sulcatus in the
lab and in the greenhouse (Coremanns-Pelseneer and Nef 1986, Tillemans et al.
1987). Various M. anisopliae strains were found to be effective (62% to 100%
mortality) against O. sulcatus larvae in ornamentals (Zimmermann 1981,
Sellenschlo 1984, Gillespie and Moorehouse 1989, Moorhouse et al. 1993a, 1993b).
In addition, M. anisopliae was found to be also very effective under field conditions
against O. ovatus and O. dubius larvae, whereas B. bassiana was less effective
(Vainio and Hokkanen 1993). All of these results indicated the potential of
entomopathogenic fungi for control of pest weevils in ornamentals, nurseries and
various agricultural crops; today there are several commercial products on the
market.
6. CONCLUSIONS
The information available on natural enemies of bark weevil pests in Europe varies
with pest species and natural enemy category. The best studied systems are
parasitoids of Hylobius abietis and Pissodes spp. The parasitoid complex of these
insects is well known and the biology and ecology of their main parasitoids have
been extensively studied. However, the role of parasitoids and other natural enemies
in regulating weevil populations remains unclear. The impact of parasitoids is likely
to be higher in Pissodes spp. than in H. abietis. Pissodes weevils are unusual among
bark and wood-boring insects by suffering from high rates of parasitism. This is
largely due to the specific egg-larval parasitoids Eubazus spp. Predators and
pathogens have been less investigated. Even for the best studied systems, however,
the impact and role of natural enemies on pest populations are not clearly
understood.
Until now, little effort has been made to use these natural enemies in biological
control programmes. Classical biological control, i.e. the introduction and
establishment of an exotic natural enemy, has little prospect of success because the
best targets for classical biological control are exotic pests whereas the main bark
weevils in Europe are native. Inundative and conservation biological control are
more promising strategies. Entomopathogenic nematodes and entomopathogenic
fungi are used as biological pesticides against weevils in horticulture, and the
techniques could be adapted to related forest pests. Particularly good targets would
be Otiorrhynchus species and H. abietis. Promising results have already been
achieved against H. abietis using entomopathogenic nematodes, but more research is
needed before obtaining commercially competitive products. Parasitoids and

predators show little prospects as inundative biological control agents because of the
high production costs and the large areas involved in forestry. In contrast,
sylvicultural methods could be developed, or modified, to enhance natural
populations of parasitoids and predators, and increase their impact on the target
pests. Such methods have already been suggested, in particular against H. abietis,
but, so far, they have not been implemented.
7. ACKNOWLEDGEMENTS
We thank Mark Shaw and an anonymous reviewer for their useful comments on the
manuscript. M. Kenis was supported by the Swiss Federal Office for Education and
Science (project C99.0116).
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Zoologiceskij Zurnal, 37, 379-94.
Chapter 19
DAMAGE, CONTROL AND MANAGEMENT OF

WEEVIL PESTS, ESPECIALLY HYLOBIUS ABIETIS
B. LÅNGSTRÖM 1 & K.R. DAY 2
1
Swedish University of Agricultural Sciences, P.O. Box 7044, S-750 07 Uppsala,
Sweden
2
University of Ulster, Coleraine, Northern Ireland, UK-BT52 1SA, UK
1. INTRODUCTION
This part of the BAWBILT synthesis deals with bark feeding weevils that cause
damage and mortality, mainly to newly planted conifer seedlings in Europe. The
species listed in the damage & control database are summarised in Table 1 giving
their estimated aggressiveness and extent for the reporting countries. The large pine
weevil, Hylobius abietis (L.) (Col., Curculionidae) is the most important species in
this group. The weevil breeds in fresh conifer stumps and feeds on young seedlings,
and consequently this or related species have become major pests wherever clear-
felling and subsequent replanting is practiced in forestry. In Europe, H. abietis is
sometimes accompanied by the lesser pine weevil Hylobius pinastri (Gyll.), but this
species is considered much less important than H. abietis, and little is known about
its feeding behaviour. Hence, all pine weevil damage is normally attributed to
H.abietis, and this will be the case in this overview as well. There is also a third and
fairly rare conifer-related species, Hylobius piceus (DeG.) that occasionally may
attack seedlings, but this species is not related to clear-fellings as it mainly lives in
the roots of senescent conifers.
Within the genus Pissodes, several species also damage the bark of conifers, but
in contrast to Hylobius where the adult is the damage-causing agent, either larvae or
adults may feed on the bark of live seedlings (or young trees). The most destructive
species in this group is the white pine weevil, Pissodes strobi (Peck.) in North
America (Alfaro et al. 1995), but there is nothing similar, which occurs in Europe,
neither in biology nor destructiveness. Pissodes pini (L.), and especially Pissodes
castaneus (DeG.) may occasionally kill young conifer saplings by their adult feeding
activity, but this damage is negligible compared to the Hylobius problem. These
Pissodes-weevils may, however, cause substantial mortality to weak or senescent
415
415–444.
© 2007 Springer.
416 B. LÅNGSTRÖM & K. DAY
pine trees by ovipositing into the lower stem, whereafter the developing brood
colonizes the phloem and eventually kills the tree. Thus, this damage
physiologically resembles that of bark beetles, and there is a third and possibly more
aggressive species on pine, Pissodes piniphilus, attacking the upper stem in the same
way. Similarly, Pissodes harcyniae (Hrbst.) attacks dying Norway spruce trees and
P. piceae (Hbst.) occurs on true firs ((Abies sp.).
Weevil larvae of the genus Otiorrhynchus are well known pests on garden crops
like strawberries, but a few species also attack conifer seedlings. Problems have
mainly occurred in conifer nurseries, where e.g. O. nodosus (Müller) has devastated
seedling crops on several occasions in Scandinavia (Harding et al. 1998). Damage
reports from forest sites are rare except from Iceland, where the same species
together with O. arcticus (Fabr.) has caused substantial mortality to planted larch
seedlings (Halldorsson et al. 2000).
In contrast to all the above-mentioned species which all are related to conifers,
Cryptorhyncus lapathi is the only weevil attacking broad-leaved trees that has been
included in the BAWBILT database. The reported aggressiveness varies between
countries from low to high, and so too does the reported extension of damage. A
summary of the information included in the database for all these weevils is given in
Table 1.
The substance of this review will entirely focus on the damage, control and
management of the large pine weevil, H. abietis.
2. HYLOBIUS DAMAGE HISTORY

Linneaus (1767) described the large pine weevil as Curculio abietis in 1758, but did
not recognise it as a pest (in contrast e.g. to Tomicus piniperda), as forests were not
really managed at that time. During the 19th century, and with the advent of
commercial forestry, H. abietis became established as a major forest pest in
Germany (Ratzeburg 1839), Sweden (Holmgren 1856), Finland (Blomqvist 1883)
and England (Ormerod 1890). In Escherich’s book “Forstinsekten Mitteleuropas”
(1923), 38 pages are devoted to discussing the damage and control of this species.
At that time, much attention was given to different trapping methods used to reduce
the number of weevils and hence to reduce seedling mortality. Physical seedling
protection using barriers were in use, and different, mainly badly-smelling,
chemicals were tested to deter weevils from feeding on the seedlings. Toxic
substances for seedling protection were tested but not much used.
Nearly fifty years later, Eidmann (1974) summarized the Hylobius problem in
Schwenke’s ”Die Forstschädlinge Europas”, and gave a comprehensive review of
the countermeasures that are totally dominated by the use of insecticides for seedling
protection. In the 1950s, DDT became the main way to control pine weevil damage
and was routinely used in most European countries until the late 1970s. DDT was
banned for seedling protection and other uses in forestry, first in Sweden in 1975,
and soon many countries followed. In most countries another chlorinated
hydrocarbon, lindane or gamma-cyclohexane, soon replaced DDT for seedling
protection. During the 1980s, permethrin and later other synthetic pyrethroids
DAMAGE AND CONTROL OF WEEVIL PESTS 417
replaced the chlorinated hydrocarbons for Hylobius control. In addition, some

countries also used (and still use) systemic insecticides for seedling protection,
whereas this practice has never been permitted in most countries.
The cheap and efficient Hylobius control provided by insecticides has inhibited
the development of other control strategies. After the DDT ban in 1975, Sweden
temporarily invested in the development of alternatives (Eidmann 1979). As lindane
was never registered for seedling protection in Sweden, a 2-4 year fallow period,
that was known previously to reduce weevil damage, was adopted as the main
strategy to avoid excessive seedling damage. Soil scarification was also found to
reduce seedling damage besides its other beneficial effects, but nobody understood
why seedlings in mineral soil suffered less damage than seedlings in humus. During
these years, feeding deterrents were tested but with poor results, whereas physical
barriers preventing the weevils from reaching the seedlings were more successful.
Two concepts, the TENO collar (Lindström et al. 1986) and the stocking (Eidmann
and von Sydow 1989) were made commercially, and several other ideas developed
and tested. Thus, there was an integrated pest management approach based on
replacing insecticides with physical barriers and silvicultural countermeasures.
These attempts to replace insecticides in seedling protection, as well as research
plans to improve seedling resistance aspects against weevil damage for inclusion
into the IPM system, all collapsed when permethrin was registered for seedling
protection in 1980, as reviewed by Långström (1998).
During the 1990s there has been an increasing public concern about the use of
insecticides in forestry, mainly but not exclusively, in northern Europe. In Sweden,
the situation is getting acute (again!) as the registration of permethrin will end in
2003. Despite ambitious research (see below), no alternatives can fully replace
insecticides in Hylobius-control yet, and hence cypermethrin was recently (April
2003) registered for the period until the end of 2005 to bridge the gap between
permethrin and control techniques not involving insecticides. A similar concern
about insecticides in forestry is growing in the rest of Scandinavia and UK although
the situation is less acute than in Sweden. In 2002, a decision was taken in Denmark
to refrain from protecting seedlings with insecticides in state forests (H.P. Ravn,
pers. comm.). During the last decades, there has also been a lot of debate throughout
Europe about the practice of clear-felling, and with increasing pressure and FSC-
certification of forest products, the chemical protection of seedlings is now part of a
much bigger issue. Hence, the research needs for a necessary development of
integrated pest management strategies without chemical insecticides are the focus of
recent review papers on the large pine weevil problem (Långström 1998; Leather et
al. 1999; Fjelstad-Pedersen and Ravn 2000).
Facing the threat of loosing insectides for Hylobius control again, the Swedish
foresty and research agencies have in recent years funded research for Hylobius
control that is not based on insecticides. Two major programs, one aiming at
replacing insecticides with antifeedants (Schlyter and Löfqvist 1998), and the other
aimed at taking the above-mentioned silvicultural IPM concept further by testing
and combining different countermeasures in order achieve good seedling survival at
acceptable costs (Nordlander 2001). In the UK, a similar environmental concern has
lead to large research investments in biological control of Hylobius using pathogenic
nematodes for suppression of weevil populations (Brixey 1997). Another line of

biological control of Hylobius, also aimed at population suppression, is pursued in
Poland where positive results have been obtained by treating stumps with the fungus
Phlebiopsis gigantea, which is antagonistic to the root rot Heterobasidion annosum,
and also deprives the pine weevil larvae of their food (Skrzecz 1996).
Altogether, the Hylobius situation in Europe is serious, as acceptable seedling
protection against weevil damage is an absolute imperative for efficient forest
management. From an economic point of view, there is, at least not for Scandinavian
forestry with slow growth rates and long rotation periods, no room for costly
seedling protection. If planting costs become excessively high, modern forestry
practice will have to be abandoned and replaced with low-intensity forestry relying
Table 1. Aggressiveness and extension ( A/E ) of BAWBILT weevils in different countries

according to the reported information in the damage & control database
Country H abi H pin P sp. P cas P pin P pph P pic P har O sul O sin C lap
Aus ***/** **/* **/* ***/**
Bel **/** */* */* */*
Est ***/*** ***/** */* */** **/**
Fra */*** */*** */***
Ger ***/** **/***
Hun ***/** ***/** ***/***
Ire ***/*** */* */**
Ita */* */* */*
Lit ***/**
Pol ***/*** ***/** **/*** **/** **/**
Por */* */* */*
Rom ***/*** */* */* **/** */* ***/**
Slo ***/*** */* */** */*
Spa **/** **/**
Swe ***/***
Swi **/* */* */** **/*
Net */* */* **/**
UK ***/*** */* */* */* */*
Aus=Austria, Bel=Belgium, Est=Estonia, Fra=France, Ger=Germany,Hun=Hungary, Ire=Ireland,

Ita=Italy, Lit=Lithuania, Pol=Poland, Por=Portugal, Rom=Romania, Slo=Slovakia, Spa=Spain,
Swe=Sweden, Swi=Switzerland, Net=The Netherlands, UK=The United Kingdom
H abi = Hylobius abietis, H pin = Hylobius pinastri, P sp. = Pissodes sp., P can = Pissodes castaneus,
P pin = Pissodes pini, P pph = Pissodes piniphilus, P pic = Pissodes piceae, P har = Pissodes harcyniae, O
sul = Otiorrhynchus sulcatus, O sin = Otiorrhynchus singularis, C lap = Cryptorhynchus lapathi
on natural regeneration and small-scale operations. This will have detrimental

effects on the national income in countries like Finland and Sweden.
3. CURRENT HYLOBIUS-DAMAGE IN EUROPE

Compiled data in the BAWBILT damage & control database clearly show that
Hylobius abietis is one of the highest ranked forest pests in Europe. Only Estonia
has given information on the pest status and control of Hylobius pinastri, in addition
to that given for H. abietis. We know, however, that H. pinastri causes some
damage at least in Germany (Escherich 1923), Latvia (Ozols 1967), Finland
(Långström 1982), Sweden (Nordlander 1990), and Estonia (Sibul 2000). In the
following text, however, no attempt is made to separate the damage by the two
species, and everything is attributed to H.abietis.
In the BAWBILT database, many countries rank the aggression as high and the
geographical extent of damage as high (Table 1). There are, however, some
inconsistencies between these rankings and the reported control measures indicating
that a deeper analysis of the Hylobius-problem was needed. Hence, a request for
more details on the damage and control of this pest was sent out to the BAWBILT
community in early 2002. Most countries replied and a more detailed and consistent
pattern emerged, as summarized in Table 2.
Today, Hylobius abietis is mainly a problem in northern and eastern parts of
Europe. Typically, countries using clear felling and planting as their main forest
management strategy are reporting the worst pine weevil problems. This finding is
not new, but it is interesting that countries that have abandoned this practice, like
Germany and the Netherlands, report that Hylobius used to be a problem. In
Switzerland, Hylobius is not a problem as forestry there has long since been based
on dimensional cutting and natural gap regeneration. Hylobius is not a problem in
southern Europe either, but the reasons for this are not clear.
The extent of the Hylobius-problem is difficult to assess from the database as
figures are not comparable. When the host area available for the weevils is given, it
may mean the total conifer forest area in the country or the annual cutting area, or
anything in between. It is, however, evident that the situation differs tremendously
between countries, as the annual reforestation area threatened by Hylobius ranges
from a few hundred (Hungary) to more than 100 000 hectares in Finland and
Sweden. The damage estimates are also confusing as they reflect the present
situation with the widespread use of insecticides for seedling protection. For
example, France reports small problems but is treating 15 million seedlings with
insecticides (of 65 million planted), whereas the UK reports 30-100% mortality
unless seedlings are properly protected. In Finland, ca 150 million conifer seedlings
are planted annually on ca 100 000 ha off which approximately 70-80 million
seedlings are protected with insecticides and even then the estimated Hylobius-
related mortality is ca 10 % (valued at ca 5-10 million Euro per annum). The figures
for Sweden are even higher: ca 100 million seedlings are chemically protected out of
ca 300 million planted. Without proper protection seedling mortality in southern
Sweden would approach 100%, whereas in northern Sweden, losses can be kept at
Table 2. Known and estimated damage and economic losses (Millions of Euro) caused by Hylobius abietis in Europe
420
Country BAWBILT Annual Seedlings Mortality (%) if Annual loss (ME) Main Alternat. Monitor. Reference
Agr. Extent host area planted protected no with with without control Strateg.
1000 ha (millions) (millions) protec. protect. insect. insect. strategy
Austria *** ** 16 80 15 40-60 15 pyr ffp, pb no H.Krehan
Belgium ** ** BAWBILT
Czech Repub. *** ** 15 50 25 < 50 2-3? 0.4 2 pyr prev ffp, pyr surv,traps M.Knizek
Denmark *** ** 5 1 0.7 50-100 5 0.2 3 pyr ss,pb,sh surveys HP.Ravn
Estonia *** *** 27 14 ? pyr ffp, sow surveys K.Voolma
Finland *** *** 150 150 80 10 6 pyr ss H.Viiri
France * *** 65 15 0-70 1 0.3 pyr, car none none FX.Saintonge
Germany *** ** 2 f
few f
few NR H.Niemeyer
Hungary *** ** 0.1 12 5 10-30? < 10 < 0.05 0.05-0.2 pyr, car none none F.Lakatos
Iceland No Hylobius
Ireland *** *** 8 20 20 50-90 10 3.2 ? pyr none none D.Ward
Italy * * small NR none none M.Faccoli
Lithuania *** ** 7 ss questionn BAWBILT
Norway *** *** 20 40 25-30 0-80 0-20 2 7 pyr ss,fp none E.Christiansen
B. LÅNGSTRÖM & K. DAY
Poland *** *** 30 240 100-150 <60 < 10 0.1-0.5 pyr, car many traps I.Skrzecz
Portugal * * small 8 none variab none none none M.Branco
Romania *** *** 6 25 25 50-80 10-15 < 0.1 0.5 pyr f
fp surveys N.Olenici
Slovakia *** *** 15 pyr, car surveys BAWBILT
Spain ** ** 100 BAWBILT
Sweden *** *** 200 300 100 20-100 < 20 15-20 pyr ss,fp,pb B.Långström
Switzerland ** * v. small 1 none small 0 0 NR f
fp no B.Forster
The Netherl. * * small NR (pyr) no L.Moraal
U.K. *** *** 15 4 4? 30-100 2 17 pyr, car none R.Moore
pyr = pyretroids; car = carbamates; NR = natural regeneration; ss = soil scarification, mounding; fp = fallow period 1-3 years; pb = physical barrier
tolerable levels (<20%) by using silvicultural countermeasures (see below). A

conservative estimate of replanting and other costs relating to Hylobius-damage is in
the range 15-30 million Euro annually in Sweden (Weslien 1998). Recently, the
Swedish National Forest Board estimated that the annual cost for the Swedish forest
industry for refraining from the use of insecticides for pine weevil control would be
ca 60 million Euro per year (Thuresson et al. 2003). In Poland, as many as 240
million seedlings are planted on 30 000 ha, anda half of these are treated. The cost
estimates differ, however, largely between counties as Poland reports much lower
losses than Finland and Sweden despite similar planting activity. In relation to the
above-mentioned facts, no reliable economic loss estimates can be made for the
BAWBILT community unless we get better data input here. However, current best
estimates of the total costs incurred by the BAWBILT community, if insecticides
were not employed for plant protection, might be in the region of 140 million Euro
per year.
4. CURRENT CONTROL METHODS IN USE IN EUROPE

In the BAWBILT damage & control database, control strategies are grouped into
different categories with several subheadings. This is a general system for the whole
database and many options are not relevant for the Hylobius-problem. The grouping
of the options is questionable in some cases, e.g. using a fallow period is clearly a
silvicultural management option, but here it is classified as ”other control strategy”.
Also, most countermeasures against the large pine weevil are preventative, i.e.
applied prior to the damage occurrence, and hence very little is direct control in the
real sense of the word. The available information for Hylobius control is compiled in
Table 2.
4.1 Use of insecticides

In most countries practicing forestry based on clear-felling and planting, chemical
protection of conifer seedlings prior to planting is the main way to control the pine
weevil problem. In Finland, Poland and Sweden, ca 300 million seedlings altogether
are treated annually, and this constitutes the major part of all treated seedlings
planted within the BAWBILT area. Countries like Austria, Czech Republic, France,
Ireland, Norway and Romania constitute a second group with 15-25 million
seedlings treated, whereas countries like Estonia, Hungary, Lithuania and UK plant
a few million seedlings, but protect most of them with insecticides. Most of the
chemical seedling protection is in fact damage prevention, as it is applied routinely
prior to planting. Direct control by treating planted seedlings at the planting site in
cases of heavy weevil attack (top-up treatment) occurs occasionally at least in
Sweden and in Ireland, but is not the main method of insecticide application. In
Austria, seedlings are often treated twice in two consecutive years, as the protective
effect does not last long enough (Rudolf Wegensteiner, pers comm). The same
practice is common in Ireland too (Declan Ward, pers comm).
Synthetic pyrethroids are mostly used but systemic insecticides (carbosulfan) are
also occasionally used in some countries although they are forbidden in others
(Table 3). As was mentioned above, only permethrin has been allowed for seedling
protection in Sweden and that use is coming to an end in 2003. Recently,
cypermethrin and imidacloprid were registered for seedling protection in Sweden,
but only for a two-year-period. Hitherto Ireland, Norway and UK have also relied on
permethrin although carbosulfan is also registered, but not much used, in the UK.
The same applies to bensultap (Bancol) in Norway. In the other countries, two or
more pyrethroids are used, and Poland and the Netherlands also allow carbosulfan to
be used for seedling protection.
Table 3. Insecticides registered for control off damage caused by Hylobius abietis in Europe
Country Synthetic pyretroids Carbamates Other

perm cyperm a-cyperm esfen delta lambda pyr carbo
Austria yes yes yes
Belgium
Czeck rep.
Denmark yes yes yes
Estonia yes yes
Finland yes yes yes
France yes yes Mar-Susc
Germany yes yes yes
Hungary yes Dimecron
Iceland
Ireland yes
Italy
Lithuania
Norway yes
Poland yes yes yes Mar-Susc
Portugal
Romania yes yes
Slovakia
Spain
Sweden yes yes Merit
Switzerland
The Netherlands yes yes
United Kingdom yes Mar-Susc
4.2 Physical protection

As the weevils approach the seedlings by walking (see e.g. Björklund et al. 2003),
prevention of the weevils’ access to the seedlings by physical barriers is an old idea
(for different concepts, see Escherich 1923). With the ban of DDT in 1975 in
Sweden, these old ideas gained a revival resulting in the TENO-collar and the plant
stocking that for a few years were semi-commercially produced (Lindström et al.
1986; Eidmann and von Sydow 1989) but they became obsolete with the registration
of permethrin in 1980. During the 1990s a multitude of new and old concepts for
physical protection have been tested. Some of these, like the idea of covering the
lower stem with a waxy coating (”Bugstop
” ”) have reached semi-commercial scale,
but there are still application problems related to phytotoxic effects due to heating.
Another approach based on a paper cylinder covered with slippery Fluon®-coating
gives good protection (Eidmann et al. 1996), but is difficult to mechanise. Several
other concepts of physical protective ”shelters” have been developed and tested with
variable results (Hagner and Jonsson 1995; Örlander and Petersson 1998; Petersson
et al. 2004). The barrier concept is still a viable idea providing that the application
can be mechanised, and the current workk in this field is reported below.
Elsewhere in Europe, there has been little interest in physical barriers for
seedling protection, but some of the Swedish concepts have been tried on a small
scale in several countries (Beitzen-Heineke and Kolbe 1987; Zumr and Stary 1995).
In Austria, another old concept has been taken up again resulting in ””Hylobex”, a
stem-coating containing stone meal, which is on the market and used to some extent.
4.3 Trapping-out and population suppression

For more than 100 years, different ways of suppressing the weevil population have
been tried, generally with poor results. Escherich (1923) reports a number of
approaches based on trap logs, trap ditches, and bark pieces all of which, it is
claimed, attract large numbers of weevils. Some of these techniques are still useful
either as tools to monitor weevil populations (Långström 1982; Voolma 1994;
Wilson and Day 1995), or in combination with insecticides to suppress weevil
numbers. Nordlander (1987) developed an efficient weevil trap baited with host
odours, but simultaneously concluded that trapping out weevils would require an
unrealistic trapping effort. Nevertheless, some countries like Poland (Skrzecz 2003)
and Romania (Olenici and Olenici 1994) include trapping-out in their control
strategy.
Debarking of stumps was also practiced as a weevil suppression technique, but is
now abandoned as laborious and inefficient (Elton et al. 1964). Stump pulling was
tried in Sweden during the 1980s, mainly for reasons other than Hylobius-control,
but the remaining thin roots were found to support a substantial weevil population so
the effect on Hylobius was small (Anon. 1978). Other stump treatment approaches
are dealt with below.
An unanswered but interesting question in n this context is whether the current
large-scale use of insecticides is having an effect on the local weevil populations. If
so, we can expect even larger problems in a future without chemical seedling
treatment. This topic will be addressed below.
4.4 Silvicultural countermeasures
4.4.1 Choice of reforestation method

As was mentioned above, the pine weevil problem is very much related to the
practice of clear-felling and planting. There is clear evidence showing that pine
weevil problems are smaller in natural regeneration than in plantations (Juutinen
1962). The main reason for this is probably the timing in seedling development as
compared to weevil occurrence, i.e. most weevils have disappeared from the site
when the self-sown seedlings grow up. The number of natural seedlings is also often
high enough to allow for a substantial mortality without open patches in the seedling
stand. One can, however, often find heavily attacked natural seedlings with healed
feeding scars all along the stem that still are alive and growing well, while similar
sized newly planted seedlings suffer heavy mortality. Hence, naturally regenerated
seedlings display a higher resistance to weevil damage than planted ones.
Consequently, natural regeneration is often a good strategy to avoid Hylobius-
damage at sites where it can be practiced, but old spruce stands are often unstable
and natural regeneration hence risky. In Norway, for example, nearly all Scots pine
is naturally regenerated, and hence pine weevil damage is mainly a spruce problem
there (E. Christiansen pers. comm.).
Seeding is not used anywhere on a larger scale, but is more similar to natural
regeneration than planting when it comes to pine weevil problems (Juutinen 1962).
In central Europe, many countries follow the practice used in Switzerland, and
nowadays also Germany and the Netherlands, which is a form of forestry based on
dimensional cutting and natural gap regeneration that creates no large clear-fellings
and hence no weevil problems. This kind of forestry, however, requires a certain
type of site, and cannot be practised everywhere.
4.4.2 Fallow period

The use of a fallow period is based on the fact that pine weevil damage is highest
during the first years after the final felling (see eg Christiansen 1971; Doom and
Frenken 1980; Långström 1982; Örlander et al. 1997). Hence, by waiting until the
weevils have disappeared from the site, i.e. 2-4 years depending on the length of the
development period, pine weevil damage can be avoided. This time lag is the most
likely reason that self-sown seedlings suffer little Hylobius-caused mortality. In
northern parts of Europe, where the generation period is more than 2 years, there is
also a 1-2 year gap between the occurrence of the parent and young beetles
(Långström 1982), that can be exploited by the forester for planting in the second
year after the final felling. During the years between the ban of DDT and the
registration of permethrin, Swedish forestry relied mainly on the fallow period for
minimizing Hylobius-damage (Eidmann 1979). It has also been used to some extent
elsewhere in Europe (at least in Austria, Finland, Norway and Poland), but has never
been popular for two reasons: weed problems and increased rotation length.
Nowadays, it seems to be more or less abandoned in most countries, except in
northern Sweden where a 1-year delay in planting is still common practice.
4.4.3 Soil scarification

Soil scarification is beneficial for newly planted seedlings in several ways, but it was
observed many years ago that weevil damage was less frequent on seedlings
standing openly in mineral soil (Ormerod 1890; Lekander and Söderström 1969;
Christiansen and Sandvik 1974). The observation was originally interpreted as a
case of ”agoraphobia” (i.e. fear of open space), and more recent studies indicate that
weevils do not avoid the mineral soil but walk faster and straighter than in humus
(Kindvall et al. 2000). This may reduce risks of predation or desiccation. It is clear
that the decision to feed on a seedling is taken in the very close vicinity of a plant
(Björklund et al. 2003). Soil scarification has been adopted as a standard procedure
in Scandinavian forestry, and much work has been done to create the optimal
technique both for seedling establishment as such, and as a countermeasure against
weevil damage. None of the other BAWBILT countries, however, mentions this as
an option against the large pine weevil. In western Ireland, the re-growth of
vegetation is so rapid on clear-cuts that there is a very real possibility of scarified
patches losing their protective effect before seedlings outgrow their vulnerability
(KR Day, pers.comm.).
4.4.4 Shelter trees and alternative food

The large pine weevil is highly polyphagous and known to feed on most woody
plants, although thin conifer bark is preferred food (Escherich 1923; Leather et al.
1994). On fresh clear-cuttings, the logging waste provides alternative food for a
while but it soon dries out, and then there remains little else than the newly planted
seedlings for the weevils to feed upon. Fairly recently, von Sydow and Örlander
(1994) reported that seedlings were less damaged under shelter woods than in clear-
fellings despite the fact that trap catches were similar. Obviously, weevil activity
was either lower in the shade of the shelter trees, or there were other food sources. It
was further found that weevils feed in tree crowns during the main flight period in
early summer but not thereafter (Örlander et al. 2000). Seedlings also suffered less
damage if extra food (i.e. fresh branches) was experimentally added to the plots
(Örlander et al. 2001). In addition, it has recently been found that weevil damage
was twice as high in clear-fellings than in shelterwoods at the same population
density (Nordlander et al. 2003a), and that seedlings growing close to stand edges
were less damaged than those further out on the open site (Nordlander et al.
2003b).When feeding budgets were calculated for the pine weevil it became obvious
that seedlings constitute a minor proportion of the total food consumption (Bylund
and Nordlander 2001). In the shelterwoods, the main food supply has been
suggested be the living roots of the shelter trees (Nordlander et al. 2003a, b), and
thereby the ”shelter-tree-effect” was clarified. This may in turn at least partly
explain why weevil damage is minimal in the gap-regeneration forestry practised in
central Europe.
4.4.5 Seedling properties

It is common knowledge that large seedlings resist/tolerate more pine weevil
damage than small ones. It is also well known that healthy seedlings in good
physiological condition stand more damage than newly planted seedlings suffering a
planting shock. The choice of appropriate planting stock and the timing of the
planting operation are common practice among foresters, but as will be shown
below, there is much more to learn and to implement here.
4.5 Biological control

Biological control is not used against the large pine weevil in any BAWBILT
country, except for Poland where stump treatment with a fungus is becoming part of
the control strategy (see below under biocontrol). In the UK, there is also a great
interest in using nematodes for stump treatment, and hitherto more than 100 ha have
been treated on a semi-commercial scale as will be discussed below (Stuart
Heritage, pers. comm.)
4.6 Integrated control

Only Poland and Sweden are implementing some kind of an IPM strategy against
the large pine weevil. Elements of that can, however, be traced in other countries as
well although the ”tool box” used is basically limited to the choice of a reforestation
option and/or use of chemical seedling protection. In 2002, Denmark took a large
step towards IPM of Hylobius by accepting a policy implying that insecticides
should not be used on state lands. The Danish policy is much influenced by Swedish
work on silvicultural countermeasures to prevent weevil damage (H.P Ravn, pers.
comm.) Use of shelter trees and soil scarification are main components in this
strategy (see below). In the UK, an ambitious pest management program is under
development, where the Forestry Commission is planning to replace insecticides
with an IPM program where risk assessment, population suppression using
nematodes and increased seedling resistance are key elements (Wainhouse et al.
2002).
The Polish strategy seems to be based on including the whole tool-box.
According to Skrzecz (1997), chemical seedling protection is supplemented with
providing alternative food (traps, trap barks or twig bundles), use of more resistant
seedlings (i.e. large and containerized seedlings), and lately stump treatment using
Phlebiopsis gigantea to prevent root rot and to reduce weevil production. Traps are
also used for monitoring weevil populations, and presumably the control options are
chosen based on the critical levels of trap catches. Fallow period and trap ditches
were used earlier, but are now abandoned.
The current Swedish strategy for integrated pest management of the large pine
weevil is based on combining physical seedling protection with silvicultural
countermeasures. The viability of this concept was tested in a large scale field
experiment where four plots (soil scarification, shelter trees, both treatments, and
neither treatment) were compared at 10 sites (Petersson and Örlander 2003). In order
to maximise the weevil pressure, no fallow period was used. At each plot, spruce
seedlings from the same seed lot were planted with one of the following treatments:
no seedling protection, waxy stem coating (”Bugstop”), Fluon®-coated cylinders
(”Hylostop”), and permethrin twice (prior to planting and next year at the site). After
three field seasons, ca 90 % of the control seedlings were dead, whereas shelter trees
and soil scarification alone reduced the mortality to 60 and 25 %, and in combina-
Figure 1. Two typical reforestation sites in northern Europe: above, a sitka spruce plantation
in Northern Ireland (photo: Keith Day), and below a reforestation site with few seed trees in
central Sweden (Photo: Claes Hellqvist)
tion to ca 15%. The use of physical barriers alone reduced mortality to ca 50%, i.e.
better than shelter trees but worse than soil scarification). Combining ”Bugstop”
with both silvicultural measures resulted in a mortality of a few percent, that was
fully comparable with that obtained from insecticide treatment alone. Although this
experiment does not fully represent field practise, it shows that pine weevil damage
can be handled without insecticides, but probably at a high cost.
5. SEARCH FOR ALTERNATIVES IN SEEDLING PROTECTION
5.1. New insecticides

There is little work reported on replacement of the currently dominating synthetic
pyrethroids for seedling protection with new insecticides. The main reason for this is
that few believe that possible new insecticides may be environmentally safer or
politically more acceptable than the pyrethroids. Rather recently, Bancol (bensultap)
which is derived from marine organisms (annelids), has been tested in Denmark and
Norway, and found to be fairly efficient against the pine weevil. It has been used for
seedling protection to some extent in Norway (Kohmann 2000), but its use will
come to an end in 2003 (E. Christiansen pers. comm). Currently, two other
insecticides (Fipronil and Imidacloprid) are being tested in Denmark and Sweden (P.
Christensen, pers. comm.). The latter was recently registered in Sweden for a two-
year-period (2004-05).Bensultap and fipronil are also being tested in Hungary (F.
Lakatos pers. comm.)
In the UK, novel application techniques based on the electrodyn sprayer
conveyor have been developed (Heritage et al. 1997). A drive plant feeder (conveyer
sprayer system) has led to better deposition of lambda-cyhalothrin, decreased
volume used, improved economy of use and better safety (Rose 2002).
Recent studies indicate that pyrethroids also seem to repel weevils (Heritage and
Johnson 1997). Weevils can clearly detect pyrethroids, the effect of which is to
depress feeding rates while the mortality suffered by weevils exposed to normal
doses with which plants are pre-treated, is low (Rose 2002).
In Estonia, neem and some other plant extracts have been tested for seedling
protection against the pine weevil, but mostt of these are antifeedants rather than
toxic substances and the results have generally been poor (Luik et al. 2000).
5.2 Physical protection

The idea of preventing the walking pine weevil from reaching the seedling dates
back to the beginning of the previous century when Berger (1904, see Escherich
1923) reported a collar made of metal with hinges, that was applied around a
seedling and moved to a new plantation after a few years. This idea was later turned
into the TENO-collar that was used in the late 1970s (ca 9 million altogether) in
Sweden (Lindström et al. 1986). The collar was soon followed by the plant stocking
(Eidmann and von Sydow 1989), and a cylindrical barrier called “Hylostop” coated
with fluon£ i.e. polytetrafluoroethylene (Eidmann et al. 1996) that is still being
tested and improved. There are a number of other candidates that have been or are
being tested (Fig. 2), but none of them is close to practical application yet (Hagner
and Jonsson 1995; Örlander 1998; Nordlander et al. 2001, Petersson et al. 2004).
The other idea for physical barriers is based on applying a protective coating to
the lower stem of the seedling prior to planting. This has also been tried before
(Escherich 1923), but new materials have provided new opportunities. A latex-based
coating was tried fairly early in the Czech Republic (Zumr and Stary 1995), and was
also found to give good seedling protection in Sweden but technical application
Figure 2: Four different types of physical barriers for seedling protection against pine weevil
damage, that have shown promising results in field tests in Sweden: upper left, ”KANT-
skyddet” a plastic collar with a brim preventing access to the seedling; upper right
”Hylostop” a paper cylinder with a slippery coating of Fluon£ at the upper end preventing
weevils from climbing the shelter; lower left ”Bugstop” a mineral wax sprayed on the lower
stem to protect it against weevil feeding; and lower right, ”Conniflex” consisting of mineral
particles of defined size in a flexible carrier sprayed on the lower stem (all pictures taken by
Claes Hellqvist).
problems have halted the further development of this idea (Örlander and Peterson
1998) Large experiments have been carried out in Sweden with waxy coatings of
”Bugstop” that give good protection against weevil damage but application without
phytotoxic effects seems difficult to achieve, and these problems that have not yet
been fully resolved (Örlander 1998; Hellqvist 2001). For the time being, the most
promising approach is a coating called “Conniflex” that contains small hard mineral
particles of a given size in a water-soluble and flexible carrier (Nordlander et al. in
prep.) This concept is based on a similar principle as the Austrian Hylobex-coating
which has been available on the market for some time (Rudolf Wegensteiner pers.
comm.). Conniflex is now commercially available and half a million of seedling
have hitherto been treated in Sweden. Altogether, physical barriers are, as such,
more expensive than a traditional insecticide treatment and the mass application
involves different technical problems that need to be solved. Despite massive
investments in Sweden in some of the ideas mentioned above, none of the concepts
is yet ready for practical use on a large scale. Hence, physical barriers cannot fully
replace insecticides for seedling protection against pine weevil damage yet.
5.3 Antifeedants
Feeding deterrent substances have been tried against the pine weevil long before
insecticides were available (Escherich 1923). Pine oil and garlic are among those
substances that have had a documented seedling-protecting effect against the pine
weevil (Eidmann 1987; Luik et al. 2000). Another is carvone that among others is
tested in a large research program aiming at finding antifeedants against H.abietis
(Schlyter and Löfqvist 1998; Klepzig and Schlyter 1999). There are also some
natural seedling substances with repellent or antifeedant activity but these are
discussed under the resistance heading.
It was recently observed that the weevil female covers the ovipostion site with
faeces containing a chemical compound with extremely strong antifeedant activity
(Nordlander 2001). The substance is identified and has been tested in large scale
field trials with good seedling-protecting results. Difficulties with finding a suitable
carrier in combination with phytotoxic effects indicate, however, that this is not the
ultimate seedling protection as it seemed. Hence, with all efforts made in Sweden in
this field during the last decade, antifeedants
f are far from offering a worthy
substitute for insecticides for protection of conifer seedlings against the large pine
weevil.
As was mentioned above, the pine weevil problem is very much related to the
practice of clear-felling and planting, and some countries have solved their weevil
problems by abandoning this practice. In other countries, this is not possible for
ecological or economic reasons, and there other measures like using a fallow period,
soil scarification and or shelter trees offer some help, but the main strategy is still to
protect the seedlings with insecticides. There seems to be little, if any, work on
developing new or improved silvicultural countermeasures against weevil damage in
Europe, except for Sweden. Even there, the focus is mainly on creating the optimal
mineral soil patch around the seedling (Petersson and Örlander 2001). Current work
indicates that the quality of the patch is more important than the size, i.e. a few cm
of fresh mineral soil around the seedling is enough, and the protective effects
deteriorate after the first field season (Örlander & Nordlander 2003). One concept
being pursued is artificial mounding where a ”cow dung heap” consisting of a cup of
a sandy slurry is placed on the soil together with the seedling (Göran Örlander pers.
comm.).
As the newly planted seedlings are not the main food resource for the weevils
(Bylund and Nordlander 2001, Bylund et al. in press), all measures providing
alternative food sources for the weevils can release the weevil pressure on the
seedlings (Örlander et al. 2001). The positive effect of shelter trees should most
likely be ascribed to the fact
f that their living roots may constitute an important food
source for the adult weevils (Nordlander et al. 2003a, b).
In northern Scandinavia, there may also be something to gain from the timing of
the planting operation if the main emergence period of the new generation is known
(cf. Långström 1982). In southern Sweden, however, weevil pressure is high
throughout the first 3-4 years, and hence there is no ”window” for planting there
(Örlander et al. 1997; Örlander and Wallertz 1999).
Seedling properties are also part of the silvicultural concepts but these are
discussed separately below. Altogether, we need to know much more about the
feeding behaviour of the weevils before we can start to further modify silvicultural
countermeasures. At present, we can see that they are important components in
future insecticide-free management plans against H. abietis.
7. SEEDLING PROPERTIES - HOST RESISTANCE

Hylobius abietis (and presumably H. pinastri as well) is a highly polyphagous
species (Escherich 1923; Leather et al. 1994), and adult feeding may take place on
most woody plants in its environment. Thin conifer bark on seedlings or larger trees
is, however, preferred food. Host recognition and utilization are discussed in
chapters 15 and 16, so here we focus on physical and physiological host properties.
It is common knowledge that large seedlings resist/tolerate more pine weevil
damage than small ones. In a comparative study, Eidmann (1969), however,
concluded that large seedlings were more resistant, but they were also clearly more
attacked than smaller ones. In Swedish forestry practice, large 4-yr old spruce
seedlings are commonly used for planting in areas with high weevil abundance.
Spruce seedlings with a stem base diameter exceeding 10 mm suffered low and
acceptable losses, but producing and planting such large large seedlings becomes
prohibitively expensive, and hence other means are needed to control the weevil
problem (Thorsen et al. 2001). Pine seedlings are not kept that long in nursery, and
are hence smaller when planted, and consequently often suffer heavy losses from
weevil damage unless properly protected.
Earlier it was noted that pine weevil problems are smaller in natural regeneration
than in plantations. The main reason for this is probably the timing in seedling
development as compared to weevil occurrence, i.e. mostt weevils have disappeared
from the site when the self-sown seedlings grow up. The number of natural
seedlings is also often high enough to allow for a substantial mortality without open
patches in the seedling stand. One can, however, often find heavily attacked natural
seedlings with healed feeding scars all along the stem that are still alive and growing
well, while similar sized newly planted seedlings suffer heavy mortality. In a series
of Finnish experiments, Selander et al. (1990) demonstrated that self-sown seedlings
of pine were less attacked and tolerated more damage than comparable planted
seedlings. It has also been shown that watering and fertilization affect the feeding
preference of the pine weevil (Selander and Immonen 1992), and furthermore that
levels of nitrogen and phosphorus in the phloem affected seedling susceptibility to
weevil damage. Other studies point in the same direction to the importance of
physiological status of the seedling for its chances of surviving an insect attack
(Wainhouse et al. 1998, 2000, 2004). This relates to the possibility of the plant
repairing feeding scars by wound healing, but also to its ability to defend itself by
deterring the weevils. It is obvious that that a well-established seedling with all
physiological processes functioning has a larger potential for defense and wound
healing than a newly planted seedling in physiological imbalance due to the planting
shock.
The conventional wisdom that large and vigorous seedlings should be used to
reduce weevil damage is still true, but there is some interesting input coming from
different directions. One promising trait under development in Sweden is the use of
very small (< 5cm) seedlings for planting. Compared to conventional seedlings,
these small seedlings suffer much less mortality altogether and especially due to
pine weevils (Lindström and Hellqvist 2001). There are probably two mechanisms
involved: first, these small seedlings may, to a larger extent escape detection by the
weevils, and second, their establishment is fast with an amazing root and shoot
development in their first field season. This opens up interesting perspectives for
timing of planting with respect to weevil abundance.
Another contribution to the importance of seedling vigour comes from Iceland,
where larch seedlings with established mycorrhiza at the time of planting were less
vulnerable to feeding damage by Otiorrhynchus-larvae (Halldorsson et al. 2000).
This again emphasizes the role of seedling vigour, in this case a functioning water
and nutrient uptake, for the resistance properties of seedlings. In the case of the
white pine weevil, P. strobi, a systematic program to screen progeny in resistance is
well advanced, with resistant seedlings commercially available (Alfaro et al. 2002).
Vegetatively propagated cuttings constitute another possible trait for improved
plant survival, as the physical bark properties (texture, and presence of needles etc.)
seem to encourage less weevil feeding than on comparable seedlings (Hannerz et al.
2002). Almost nothing is known about the role of the genetic make up of the
seedlings or cuttings for their susceptibility to weevil damage, but observed
morphological differences between differentt genetic origins are alone interesting
enough for further studies. In addition, Alfaro et al. 2002 have indicated that the
presence of high numbers of thick-walled sclerid cells in the phloem, prevents
weevils attack on spruce shoots
During recent decades, bark beetle researchers have made major advances in
understanding resistance mechanisms of conifers against bark beetles (Lieutier
2002) and the terminal weevil (Alfaro et al.2002), as detailed elsewhere (Lieutier,
chapter 9). The emerging pattern is a complex network of interacting physiological

and chemical processes that are under genetic control. Basically, tree defences
operate on three levels where preformed or primary defences (resin duct resin,
polyphenolic parenchyma cells, lignin-containing stone cells) seem to aim at halting
the intruder while the second line of defence consisting of an induced reaction
(lesion formation, traumatic resin ducts) is mobilized and if successful enclosing the
intruder in necrotic tissue isolated from the living tissue by a wound periderm. The
third defence level occurs in trees surviving an attack and consists of an acquired
resistance (that may or may not be systemic) that results in an elevated resistance
against later stem attacks during the same or next season (Krokene et al. 1999,
2000). Some of this knowledge should be applicable to conifer seedlings fending off
stem attacking insects like the pine weevils as well, and a few approaches in this
direction have been made.
The pine weevils seem to feed differently on seedlings growing more or less to
their full potential. On self-sown seedlings weevil damage often occurs as many
small feeding scars, whereas large and coalescing feeding areas mainly occur on less
vital i.e. newly planted seedlings. It is tempting to interpret these observations as an
expression of a behavioural response of the weevils to a different strength in the
primary resin flow. Furthermore, it has been observed that weevils avoid feeding on
wound tissue, resulting from previous feedingf scars (Selander and Kalo 1979;
Ericsson et al. 1988), which represents some kind of an induced defence reaction.
Even more interesting is the fact that seedlings responded to a topical application of
methyl-jasmonate by forming traumatic resin ducts not only locally but in a systemic
way (Franceschi et al. 2002). When exposed to pine weevil attack these seedling did
better than untreated ones but at a high cost, as height growth was retarded by the
methyl-jasmonate treatment (E. Christiansen pers.comm.)
The chemical basis of conifer resistance to stem-attacking insects seems to be
very complex and is far from understood. The role of terpenes and polyphenols in
this context is reviewed in chapter 9 with regards to bark beetles, and much less is
known for seedlings fending off e.g. pine weevils. Terpenes are important in the host
finding of the pine weevils (Tilles et al. 1986; Nordlander 1991), and H.abietis has
chemoreceptors for these on their antennae (Wibe et all 1996). Limonene has been
shown to inhibit the attraction of pine weevils to α-pinene (Nordlander 1990).
Terpenes are also known to be toxic to the weevils, but it has been difficult to relate
resistance to the monoterpene composition of the seedlings (Selander and Kalo
1979). Thorpe (1999) found great variation in concentrations of resin, polyphenols,
carbohydrates and nitrogen when comparing different host materials for the pine
weevil in the UK. She also observed that both larval development and adult feeding
correlated positively with concentrations of carbohydrates and resin, whereas
correlations were negative for nigrogen and polyphenols in clonal seedlings of Sitka
spruce (Picea sitchensis). In Scots pine, wound tissue with elevated resin acid
content has been found to deter H. abietis from feeding (Ericsson et al. 1988). Some
phloem phenolics may also be involved in pine defenses against pine weevils
(Lieutier et al. 1997). Recently, Bratt et al. (2001) isolated a bromine compound
with antifeedant properties from bark of lodgepole pine ((Pinus contorta) that does
not occur in Scots pine. Verbenone, which is known as a component in bark beetle
pheromones that normally are synthesized from host material, has also been
demonstrated to have a feeding deterrent action on the pine weevil (Lindgren et al.
1996). These scattered observations indicate that there is much more to explore in
host chemistry of conifer seedlings that could also relate to host resistance properties
against generalist feeders like the pine weevils.
Figure 3. Left: Feeding scars at the base of a pine seedling caused by the large pine weevil ;
note absence of resin exudation indicating low seedling vigour (photo: Niklas Björklund);
right: healed feeding scar at the base of pine seedling showing successful recovery from
weevil damage (Photo: Bo Långström).
The roles of the genetic make up, physiological condition, morphological

properties and defense chemistry of seedlings in avoiding and/or sustaining attack
by pine weevils should hence be studied in a more systematic way, as seedling
properties will probably be important components in future pest management
systems.
8. NATURAL ENEMIES AND BIOLOGICAL CONTROL OF HYLOBIUS

Due to their concealed way off life, larvae of the pine weevils are not much exposed
to predators or other natural enemies. As discussed in chapter 18, a few species of
insects, fungi or other microorganisms coexist with the weevil larvae in the dying
roots of conifer stumps. Some of these may cause larval mortality by competing for
food, others may use Hylobius-larvae as their food source. In the former group we
find some root-colonizing fungi and insects, in the latter group we have at least one
braconid, Bracon hylobii (Hedqvist 1958; Henry and Day 2001), and some
nematodes parasitizing weevil larvae as well as entomopathogenic fungi
(Wegensteiner and Führer 1988) and microsporidia (Purrini 1981; Purrini and
Ormieres 1982).
Adult pine weevils are long-lived and seem to have few natural enemies during
their adult lifetime. One braconid (Perilitus areolaris) seems to be specialized on H.
abietis (Gerdin and Hedqvist 1985), and this species may be an important mortality
factor in the adult stage as it seemed to be abundant in adult weevils one year after
clear-cutting in Sweden (Bylund in prep.). The species is also reported from the
Czech Republic (Stary et al. 1988), but from Poland as Perilitus rutilus (Slizynski
1969; Korczynski 1984). In Finland, a braconid, Pygostolus sp. was regularly found
together with larvae of the genus Tomicobia sp. (Hym., Pteromalidae) in the
abdomen of adults of H. abietis (Långström 1972). Pygostolus falcatus is reported
from Otiorrhychus ovatus in Finland and from other curculionids elsewhere in
Europe (Suomalainen 1942; Schindler 1964), but the species found in pine weevils
is so far unidentied. As only larvae were found, it cannot be excluded that
Långström’s (1972) findings may as well have been P. areolatus. The parasitism by
Tomicobia and Pygostolus was observed at several sites but seldom exceeded 10 %
(but only large larvae were noted).
None of these bio-control agents has so far been used in forestry practice, but
several ongoing projects, aiming at finding alternatives for insecticides in weevil
control, explore possibilities of including biological control in IPM-systems for pine
weevils. In most cases, the concept is to suppress weevil populations at least locally
and thereby to reduce seedling damage. Regardless of the technique used, there is
no evidence so far that suppression of Hylobius-populations is a really viable
approach, at least not on the landscape level.
Pine weevil larvae are sensitive to the quality of their food (root phloem), and
hence manipulation of this resource may be a possible way to reduce weevil
populations. Early efforts to debark the stumps down to ground level have been
abandoned as inefficient and laborious (Elton et al. 1964). Treatment of fresh
stumps in order to retard or accelerate microbial colonization had little effect on
weevil production (von Sydow and Birgersson 1997). In a Polish study, Skrzecz
(1996) found a negative correlation between the presence of P. gigantea and the
number of Hylobius-larvae in Scots pine roots. Laboratory experiments also showed
that Hylobius-females were repelled from sticks inoculated with P. gigantea
(Skrzecz and Moore 1997). As this fungus is common in pine and spruce stumps
(von Sydow 1993), and is nowadays commercially used (Rotstop£), at least in
Scandinavia, for stump treatment against the root rot ((Heterobasidion annosum), the
study was repeated in Sweden using Rotstop and another root-colonizing fungus,
Resinicium bicolor. Unfortunately, no effects were seen on Hylobius performance in
the field and contradictory results were obtained in the laboratory (Rothpfeffer
2000). As colonized roots produced few weevils, the main problem was slow
dispersal and growth of the fungi into the roots from the stump surface. Similar
negative results are reported from Scotland (Skrzecz and Moore 1997), and hence
this option may not work in a colder climate (see also Creevey 1999).
Entomopathogenic nematodes represent another approach for suppressing weevil
populations that is currently intensively studied in the UK and Ireland (Armendariz
et al. 2002, and references therein). Already in the 1970s, Pye and Burman (1977)
had tested the pathogenicity of the nematode Neoaplectana carpocapsae against
larvae of H. abietis, and demonstrated substantial weevil mortality in stumps treated
with a nematode suspension (Pye and Pye 1985). The practical interest for this
method has, however, been low in Sweden, and hence no further development has
taken place. In contrast, good results against seedling damage by Hylobius congener
have been reported from Canada when seedling roots were treated with nematodes
prior to planting (Eidt et al. 1995).
9. MONITORING, RISK ASSESSMENT AND SUPPRESSION OF WEEVIL

POPULATIONS
Prophylactic use of pesticides or routine employment of silvicultural and other
measures to protect seedlings, is likely to be wasteful if the challenge from Hylobius
is sporadic and patchy, with many areas experiencing low damage levels without
treatment. While this might rarely be the case for clear cut plantation forestry in
northern Europe (Örlander and Nilsson 1999), it remains possible that the correct
identification of lower risk sites might enable focusing of the most cost-effective
preventative measures on sites with the highest risk from weevil attack.
Ever since the large pine weevil became a reforestation problem, different trap
devices have been designed and used to suppress weevil populations, but generally
with poor results. Escherich (1923) reports a number of approaches based on trap
logs, trap ditches, bark pieces that all may attract large numbers of weevils. In
Sweden, Sylven (1927) caught ca 100 weevils per trap in a season, and concluded
that 100-200 traps per ha were needed for trapping out the population. This implies a
population size of tens of thousands of weevils per ha. The few existing estimates
range from a few thousand (Eidmann 1997) to 40 000 weevils per ha (Ozols 1967).
Even higher larval populations are reported from Sweden (Anon. 1978) and Russia
(Charitonova 1965). Currently, a mark-recapture study in Sweden reported similar
population levels (ca 14000 adult weevils per ha) on a clear-cut and a shelter tree
site (Nordlander et al. 2003b.) Similar studies in UK (Moore unpublished) are being
evaluated and hence better population estimates will shortly be available for that
region as well. Judging from studies based on relative trap catches, large differences
can be expected between sites and regions (Ozols 1967; Långström 1982; Voolma
2000, 2001).
Knowing the abundance and mobility of the weevils, population suppression is a
difficult task, as the efforts have to be coordinated over large areas to have a chance
to be successful. The probability for success is small in a forested landscape like the
Nordic where clear cuts are more or less evenly distributed in time and space.
Hence, suppression of the weevil population has never really been considered an
option in this part of Europe. It may, however, work in a less forested landscape
where clear cuts are relatively small and far apart like in the UK, where weevil
suppression using nematodes is currently given serious consideration (Brixey 1997).
The Polish approach with stump treatment using a fungus (Skrzecz 1996), that was
mentioned above is also aiming at population suppression, but no results on the
population level have been reported yet.
One interesting question in this context is whether the current large scale use of
insecticides for seedling protection is having an effect on the local weevil
populations. Nowadays, we know that the weevils locate most, if not all, planted
seedlings at the site (Björklund et al. 2003), and hence get in contact with the
insecticide. In Finland, on average, one dead pine weevil per seedling was found in
the humus below lindane-treated seedlings (Långström 1972), but more than 10
weevils were found around the most attacked seedlings (Långström, unpubl. data).
Considering that population estimates indicate that the ovipositing Hylobius
population is below, rather than above, 20 000 weevils per hectare (Eidmann 1997;
Nordlander et all 2003b), and that ca 2000 insecticide-treated seedlings normally are
planted per hectare, many weevils are likely to encounter the insecticide, and there
should hence be a substantial reduction in the parent weevil population at treated
sites. It is unclear and probably not very y likely that a reduction in parent beetle
numbers really affects the size of the nextt generation, but the possibility cannot be
excluded and should be studied. The situation may, however, be different with the
pyrethroids, as they do not always seem m to kill the long-lived weevils (Rose 2002).
Nowadays, weevil traps or trap billets are mainly used for monitoring purposes. eg
in Poland, 10 weevils per trap is considered a critical number in a monitoring
procedure using 5-10 traps per ha (Skrzecz 2003). In Romania, however, trap barks
treated with insecticides are deployed at 100-400 pieces per ha at high-damage sites
(Olenici, pers comm.). The use of weevil traps (or billets) for monitoring purposes
is, however, also complicated by the factt that catches do not always match with
seedling damage (Szmidt and Korczynski 1983; Nordlander 1987; von Sydow 1997;
Örlander et al. 1997). The reason for this is still unclear, but is probably linked to
weevil behaviour.
Hence, risk assessments based on trap catches are poor estimators of the actual
hazard for seedling damage. In Northern Ireland, Wilson et al. (1996) developed a
model based on site characteristics that gave clear guidance for identifying high-risk
sites (Day and Leather 1997). The key variables were simple (size and age of
planted area, previously planted or not, and planted or self-seeded) and apparently
relevant for those conditions, but probably irrelevant for Scandinavian conditions. In
an unpublished M.Sc. thesis, Pullinen (1989) built a logistic model for predicting the
hazard for an individual seedling to become attacked by pine weevils, and found that
the planting spot (i.e. mineral soil or humus), distance to humus, micro-topography
and surrounding vegetation had the best explanatory power in south-western
Finland. Selander (1993) applied a proportional hazard model to a data set of
seedlings followed over 5 years, and found that the girdling damage had the greatest
effect on survival, whereas logging slash, seedling type and diameter also influenced
the rate of survival. In Denmark, high-risk areas have been roughly identified based
on site (light soils) and forestry (much conifer plantation and high cutting activity)
variables (Fjelstad-Pedersen and Ravn 2000), and in Sweden such work is in

progress (Johansson and Långström in prep.).
10. CONCLUSIONS
Despite substantial research efforts in different parts of Europe during more than
100 years, much more work is needed before the current routine use of insecticides
for seedling protection can be replaced by integrated pest management strategies
that do not rely of chemical seedling protection. Recent Swedish work indicates that
it is possible to achieve adequate seedling protection by combining silvicultural
methods with physical barriers, albeit at a higher cost than with insecticides. Major
break-throughs in bark beetle and shoot weevil research open up interesting avenues
of work towards increasing seedling resistance against weevil damage. Recent and
current work on natural enemies point to several different approaches for population
suppression. Although this is not an easy way to go, stump treatment with fungi or
nematodes as well as exploitation of adult parasitoids deserve further attention.
Recent work has uncovered astonishing facts about weevil behaviour (such as
oviposition and larval migration in the soil), and there is little doubt that we need to
know much more about weevil behaviour and dispersal in order to develop new pest
management strategies, and even more so if we attempt to suppress weevil
populations. As weevil control without insecticides will be more costly and more
site-specific, there is a large need for risk rating systems that at least can identify
high- and low-risk areas with reasonable accuracy.
11. ACKNOWLEDGEMENTS
We are grateful to all BAWBILT colleagues for their generous contribution to this
overview of the damage and control of the large pine weevil in Europe. We also
thank Erik Christiansen, Beat Forster, Iwona Skrzecz, Ferenc Lakatos, Kaljo
Voolma and Declan Ward for valuable comments on the text, and Claes Hellqvist
for technical assistance in editing text and pictures .
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Part 3
Buprestids & Longhorns

Chapter 20
BIOLOGY, ECOLOGY AND ECONOMIC IMPORTANCE

OF BUPRESTIDAE AND CERAMBYCIDAE
H.F. EVANS 1, L.G. MORAAL 2 & J.A. PAJARES 3
1
Forest Research, Alice Holt Lodge, Wrecclesham, Farnham, Surrey, GU10 4LH,
UK.
2
ALTERRA, Wageningen University and Reesearch Centre, PO Box 47, NL-6700
AA Wageningen, The Netherlands
3
Escuela Técnica Superior de Ingenierías Agrarias. Universidad de Valladolid, Avda.
Madrid, 44. E-34004. Palencia, Spain.
1. INTRODUCTION
Most jewel beetles (Coleoptera: Buprestidae) and Longhorn beetles (Coleoptera:
Cerambycidae) are xylophagous species, although a few buprestids mine leaves and
some cerambycids live on the roots of herbs. Some species are phloem feeders and
reside entirely within the bark, while others are xylem feeders and feed both in the
phloem and within the wood. Most of the species attack dying or dead trees, and are
ecologically important components in the insect community that utilises and
contributes to degradation of dead wood. Many species have also declined and
become endangered due to the lack of breeding material in parts of Europe.
However, some species are able to invade healthy of weakened trees, eventually
killing them due to girdling of the phloem system as a result of extensive larval
feeding under the bark. Therefore some of the Buprestidae and Cerambycidae are
considered to be damaging to living trees. Even if they are not lethal to standing
trees, the secondary economic effects on naturally damaged or felled timber can be
considerable.
2. BUPRESTIDAE
This family includes about 15,000 species that are mainly distributed in the warm
parts of the globe and are easily recognised by their often bright metallic colour
which gives rise to the common name jewel beetles. The family comprises about 200
species in Europe, of which 48 species reach northern Europe. The buprestids have
447
447–474.
© 2007 Springer.
448 H.F. EVANS, L.G. MORAAL & J.A. PAJARES
an enormous range in size, shape and coloration. Some species are narrow and
elongate while others are quite flat and roundish. The variability in coloration is very
wide, from entirely black species to species bearing all the colours of the spectrum,
often brightly metallic (Bilý, 1982).
2.1. Morphology and biology
2.1.1. Morphology of adult Buprestidae

The head is short and vertical with biting mouthparts. The eyes are oval, elliptical or
reniform, sometimes projecting beyond the outline of the head. The antennae are
moderately long. In most species, the abdomen is completely covered by the elytra
which have longitudinal grooves, or rows off punctures, or longitudinal keels. Minor
morphological differences between the two sexes occur frequently, and may
exceptionally be very pronounced. More detailed information can be found in Bilý,
1982 and Schönherr, 1974.
2.1.2. Morphology of Buprestidae larvae

The larvae of buprestids are dorso-ventrally flattened, segmented, almost hairless,
usually with the thoracic part of the body very enlarged. It is possible to distinguish
several morpho-ecological types of larvae (Bilý, 1982; Schönherr, 1974).
Figure 1: The larva of Agrilus biguttatus makes zigzagging galleries in living oak trees; the
last abdominal segment terminates in a pair off minute black-brown horns. (Photo: Alterra /
A. van Frankenhuyzen).
2.1.3. Biology and ecology of the Buprestidae

Adult buprestids are diurnal, sun-loving beetles. The majority of the beetles are
oligophagous, developing only in a single tree genus or in several related genera.
The females place their eggs singly or in small groups into ridges of bark or wood.
The eggs are covered with a secretion which hardens.
BUPRESTIDAE AND CERAMBYCIDAE 449
2.1.4. Host selection and life cycle

Most buprestids are tree specialists. They are dependent on living, but weakened,
trees. When the trees are growing vigorously, the larvae tend to be destroyed by
plant defence mechanisms such as formation of callus. However, the phloem and
xylem only remain suitable for larval development for a relatively short time once
the trees are dead. This restricts the period of vulnerability of a given tree to a
relatively narrow window when the trees are in a suitably weak condition to support
colonisation and larval development. Apparently the females are able to detect
suitable trees, weakened by water stress (drought or flooding), root damage by biotic
(e.g. voles, fungal infection, etc.) or abiotic (physical damage during soil cultivation,
wind movement of the stem and roots, excess application of fertilisers, etc.) or
defoliation leading to general stress, including loss of photosynthetic and
transpiration capacity. Some species such as Agrilus viridis are even able to detect
parts of trees which are not healthy; such as bark zones with heat cancer (sun
damage) of beech trees.
Figure 2: Dead tree with old larval galleries of Agrilus biguttatus (Photo: Alterra / Leen
Moraal)
The typical life cycle of buprestids will span one or, exceptionally two years. Adult
emergence takes place in the spring (usually May or June in temperate, northern
hemisphere regions) and is characterised by y D-shaped emergence holes in the bark
of trunk and/or branches. Adults feed on foliage, pollen or nectar initially then
females lay eggs on the bark surface or within cracks and crevices. After egg hatch,
the neonate larvae move to the phloem and commence feeding and pass through
several instars (usually four) before the winter. Pupation takes place in the spring
just prior to adult emergence.
In experiments on the interaction of Agrilus suvorovi (A. populneus) and poplars,
Arru (1962) found that trees with lower moisture content (MC) in the bark were
more selected for egg deposition. Even differences of 4% lower MC were detected
by the female. No egg deposition occurred in more desiccated bark. However apart
from the moisture content of the bark, other factors, such as chemical substances,
could be involved in detecting suitable hosts (Arru, 1962). Phaenops cyanea is able
to determine the suitability of host trees in a stand with variable crown densities and
tends to attack trees with thinner crowns (Apel et al, 2000). The needles of these
trees had significantly lower dry weights and water contents and increased proline
contents compared with more resistant trees. The latter had higher concentrations of
condensed tannins such as procyanidins and vanillin. Other species of buprestid
show extreme sensitivity to infrared, which enables them to detect and colonise fire-
damaged trees. In Melanophila acuminata this is achieved by infrared-sensitive
sensillae in the antennae (Gronenberg & Schmitz, 1999).
2.1.5. Host plant resistance

In the USA, the buprestid Agrilus bilineatus attacks oak trees that have been
weakened by prior environmental or biotic stress. Oaks that attracted large numbers
of individuals or that were successfully colonized by the pest produced significantly
less callus than did non-attacked trees when experimentally wounded. It is suggested
that callus formation may limit the establishment of small larvae that feed slowly in
the cambial region. The results indicate that current theory regarding relationships
between increased tree stress and decreased allocation of energy reserves to radial
growth and defence against phloem borers may be an oversimplification. It is
suggested that tree growth and the defensive response of phloem tissues may be
limited more by the rate of carbohydrate utilization or by changes in source-sink
relationships than by storage levels. Callus formation and the synthesis of
allelochemicals in wounded phloem may be under the same control as cambial
activation, which is mediated by plant growth regulators and can be influenced by
environmental conditions (Dunn et al., 1990).
The glycoside rhododendrin was found in the inner bark of a large number of
Betula spp. in the USA. Rhododendrin was naturally hydrolysed to rhododendrol
when trees or branches were under drought stress. Rhododendrol may act as a
stimulant to oviposition by the bronze birch borer, Agrilus anxius, in white-barked
species. Selection and breeding, of borer-resistant trees should emphasize those
species or individuals found to produce little or no rhododendrin (Santamour &
Lundgren, 1997).
2.2. Economic importance of the Buprestidae

North European buprestids have not been regarded as economically important (Bilý,
1982), whereas in the central and southern parts of Europe these beetles can be very
destructive. However, it is expected that global warming will increase the
vulnerability of forests to insect attack. There is evidence for this in warm-loving
Agrilus spp. and Phaenops cyanea in Germany (Wulf, 1995).
A summary of records from BAWBILT database on damage and control
includes a range of buprestids pests (Table 1).
Table 1. Buprestidae considered to be damaging to trees.
Insect species Tree species Pest area

Agrilus angustulus Quercus Hu
Agrilus ater (A. sexguttatus) Salix, Populus
Agrilus elongatus Quercus
Agrilus biguttatus Quercus Cz, Fr, Ge, It, NL, Pl,
(A. pannonicus ) Sl,
Agrilus sinuatus Broadleaves
Agrilus sulcicollis Quercus, Fagus, Castanea
Agrilus suvorovi Populus Hu, Sl
Agrilus viridis Broadleaves It, NL, Ro
Chrysobothris affinis Quercus
Coroebus florentinus Quercus, Castanea It, Pr, Sp
(C. bifasciatus)
Coroebus undatus Quercus, Fagus Pr, Sp
Lampra rutilans Tilia
Melanophila picta Populus, Salix Pr, Sp
Palmar festiva (Lampra f.) Cupressaceae
Phaenops cyanea Pinus Cz, Ge, Hu, Pl, Ro, Sl,
(Melanophila cyanea) Sw
Cz: Czech Republic; Et: Estonia, Fr: France; Ge: Germany; Hu: Hungary ; It: Italy; NL: the Netherlands;
Pl: Poland; Pr: Portugal; Ro: Romania; Sl: Slovakia; Sp: Spain; Sw: Switzerland
2.3. Case studies
2.3.1. Coroebus florentinus (C. bifasciatus)

Coroebus florentinus affects oak trees in the
Mediterranean region. C. florentinus is considered a
primary pest attacking old trees, causing wounding
and death of branches and shoots but not killing the
trees; damage by growth losses and by affecting
tree shape is rated of medium importance.
Considered of low aggressivity and having a low to
medium distribution, control measures seem to be
practised only in Spain, where visual surveys
indicate affected branches which can be pruned
before adult emergence.
Figure 3: Adult of Coroebus florentinus. Photo: Juan A

Pajares.
Specific biology: Females lays eggs in June-July in the bark of young healthy
branches of various species of oak, often near the tips of the current year's growth of
twigs. The larvae feed at first on the acorns, later boring downwards into the
branches, first in the cambium layer and later by boring a gallery that may reach a
length of 1.5 m, towards to the base of the branch. When it is fully grown, the larva
bores an almost complete ring under the bark. This cuts the flow of sap and leads to
desiccation and death of the whole distal part of the branch. Larvae live between 20
months and four years. Deterioration of cork oak and evergreen oak may be
considerable, particularly on young trees under the canopies of older trees. This
damage is serious on young trees, which may be almost completely affected, but
mature healthy trees recover after the infested branch drops off and, sometimes,
when the larval galleries are occluded by scar tissue (Dajoz, 2000; Solinas, 1974).
2.3.2. Coroebus undatus (in cork oaks)

C. undatus is a primary pest attacking cork oaks of all ages in the Iberian Peninsula.
Although it does not usually kill the trees, it causes significant wounding,
particularly in the cork producing tissues, leading to important economic losses in
the amount and quality of the cork harvested. Rated as of low aggressivity and low
to medium distribution, no control measures against this pest are taken currently.
Specific biology: Soon after adult emergence in May and June, C. undatus females
lay their eggs, individually or in small groups, in bark crevices on the lower part of
the stem, but also in the bases of the main branches. Egg hatch occurs in two or
three weeks and young larvae penetrate the cork reaching the cork generating layer,
where they bore long S-shaped galleries, up to 2 m. long and 3-4 mm. wide, filled
with dark, packed frass. After five larval instars, mature larvae bore into the cork
layer and excavate pupal cells where later they become adults that leave the trunk
through elliptical emergence holes and move to the crowns to feed on the leaves.
Generation development usually takes two years, but a sizeable proportion of the
individuals may complete their life cycle in one year (Romanyk and Cadahía, 1992).
Economic damage in cork oaks arises from larval galleries affecting the new
cork layer and the “mother layer” of cork generating tissues; also pupation cells
within the cork greatly decrease its quality and value. Repeated attacks result in the
weakening of the tree and may lead to its death. Increasing attacks by Coroebus
species in the Iberian Peninsula are associated with holm and cork oak decline
occurring during the last decade. Although in many areas of Spain oak decline has
been primarily linked to infection by the soil pathogen Phytophthora cinnamomi
(Brasier et al., 1993), this decline is assumed to be the result of the combined actions
of several factors, especially unusual prolonged drought periods. Coroebus species
are among the main insect pests involved in the decline syndrome. Mortality of oaks
weakened by oak decline and infested by C. undatus has been observed also in
Germany, where increasing abundance of this formerly rare species of buprestid has
been related to favourable climatic conditions (Kontzog, 2001). Attack intensity by
this species is also dependent on site and stand characteristics. For example, damage
was found to be higher at lower altitudes and on south facing slopes in France
(Merle and Attié, 1992) and in denser stands with thicker understories in Spain
(Soria et al., 1992).
2.3.3. Agrilus species

Agrilus spp infesting broadleaves, especially A. biguttattus and A. viridis on Quercus
and Fagus, are generally considered secondary species which may attack all ages but
prefer older trees. In a few cases, however, Agrilus beetles are rated as primary
pests. It seems that situations or criteria for the type of impact are different among
countries. In central and western Europe these insects can kill the trees directly,
while in the Mediterranean area damage is confined to wounding and death of
branches and shoots. Agrilus spp have been implicated as important agents in the
decline of oak trees in Europe (Moraal and Hilszczanski, 2000) and North America
(Muzika et al., 2000). In some cases, they may also contribute to the spreading of
oak diseases in stem and branches (Vannini et al., 1996); in Hungary, death of oaks
is reported to be caused by a fungus associated with A. angustulus.
The type of damage resulting from these pests is also variable among European
countries. Even when tree death is caused directly by the insect, economic damage is
rated mainly at a medium level, which also applies to damage leading to timber
degradation and growth losses. It has been also observed that attacks by the most
damaging species follow weakening of the trees by insect defoliation or by the
raising of the water table and poor drainage in the soil. Even though some of the
Agrilus species are considered responsible for tree death on weakened trees, control
strategies are applied rarely. Occasional preventive burning and insecticide
application to felled trees are indicated in a few cases, but silvicultural management
is the most common strategy. Selective thinning is carried out as an occasional
control measure in many countries, whereas forest sanitation is either a main or an
occasional practice in some. Clear felling and/or pruning are applied only
occasionally in some countries. Silvicultural choice as a main tactic is applied in
Poland against A. biguttatus, where it is considered to be a primary pest causing tree
death. Prevention by control of preceding defoliation is also practised in Germany
against this pest. No other control tactics are so far applied in Europe, except very
few instances of occasional trapping out of the beetles in trap trees or logs. Most of
the countries monitor these insects through visual surveys/sampling carried out
occasionally in the forest. Several countries also employ questionnaires, but only in
one case were these used routinely. No monitoring at all is performed in the
countries where these insects are considered of minor impact. Risk rating and
decision support systems are absent from management practices, although a local
risk model for A. biguttatus is used in Germany.
Agrilus viridis: Outbreaks sometimes occur on beech, especially following hot and
dry years. Galleries of this species are found mainly under those parts of the bark
exposed to the sun at the southern edges of woodlands. It is therefore difficult to
make a distinction between damage done by y the beetle and that caused by drought
and insolation (Dajoz, 2000). In the past this beetle has destroyed large areas of
young beech one year after planting (Schönherr, 1974).
Agrilus biguttatus ((A. pannonicus). In Europe, oak decline is in general associated

with a complex of biotic and abiotic stress factors, such as repeated insect
defoliation, fungi, late winter frost and drought (Moraal & Hilszczanski, 2000).
Some of these primary stress factors are reversible and oaks may recover. However,
stressed oaks may be attacked by this species of buprestid beetle such that the trees
may be killed before they are able to recover from the original stress factors. A.
biguttatus has caused losses from a few thousand m3 in Slovakia to hundreds of
thousands m3 in France during the 1990s. In Poland, timber losses by all pests in
broadleaves, including A. biguttatus, amounted to more than 2 m m3 in the same
period. A. biguttatus is also considered the more aggressive and extended species
within the genus, particularly in western and central Europe.
Specific biology: The larvae excavate galleries under the bark of weakened trees,
which are killed through girdling. The beetle deposits groups of eggs, mainly on the
south-side of the bark of living trees and show a preference for larger trees with
thick bark. The larvae excavate long, zigzagging galleries under the bark. Relatively
vigorous trees can ward off early larval feeding by wound reactions, which show as
dark cracks with slime flux. Warm summers in combination with a large supply of
weakened trees are assumed to favour this thermophilic insect (Hartmann & Blank,
1992, 1993).
Agrilus sulcicollis and A. angustulus. In several countries these species also play a
role in oak decline. To reduce the population of the beetle, a feasible countermeasure
might be the removal of those stems which are heavily infested with larvae. Non-
infested trees, which are already dead for more than one year, or dead trees with
evidence of the beetles' exit holes, may be left in the stands for their contribution in
the development of dead wood fauna. Long-term measures include increasing age
structure, and developing the shrub and under-storey layers to provide shady
conditions that decrease the susceptibility of the trees for infestation (several authors
in: Moraal & Hilszczanski, 2000).
Specific biology: These species prefer to infest upper parts of the stems,
branches and smaller sized host trees.
2.3.4. Phaenops cyanea (Melanophila cyanea)

Among buprestids attacking conifers, Phaenops cyanea is a pest causing damage to
Scots pine pole stands in several European countries. Whether considered primary or
secondary, it does cause tree death directly in most cases. Aggressivity of this pest is
rated high in western-central countries, where it is widely distributed, whereas in
Eastern Europe it appears less aggressive and scarcer. It is one of the most serious
pests of pine in Poland, mainly in older stands weakened by biotic agents (insects
and root fungi) and abiotic agents (industrial pollution, fluctuation of the level of
groundwater, fires) (Sowinska et al., 2000). In the Nordic countries, seed trees that
are exposed after cutting are colonised in hot, dry summers. P. cyanea was the main
insect pest involved in a massive dieback of Pinus sylvestris in Germany in 1969-
1971, for which the primary cause was root rot as a result of abnormally high water-
table during 1965-69. This was the first occurrence of P. cyanea in pest proportions
in the region. Freshly felled stems (with or without crowns), when laid on sunny
places, were found to be very attractive as trap logs and more so than girdled trap
trees (Dengler, 1975). In Sweden, this buprestid can kill draught-stressed trees on
shallow soils during hot summers, but it has also been occasionally observed to
attack sun-exposed seed trees (Ehnström & Axelsson 2002).
Specific biology: This species attacks the lower stem of Scots pine logs or standing
weakened trees. At least in northern Europe, it prefer sun exposed sites, and was not
uncommon in fire-damaged trees (Ehnström et al. 1995). In southern France, trap
logs of Pinus halepensis, were preferred over Scots, black and maritime pine
(Lieutier et al. 1997).
Economic damage by this insect is important, ranking from medium to high
levels, particularly due to timber degradation but also to growth losses or even tree
mortality, though estimates of it are provided just in one case. Preventative strategies
based on physical treatments, including debarking, burning or processing, are
occasionally implemented in half of the countries where it is considered a pest. As
with other buprestids, silvicultural management is the control option applied most
frequently, particularly by selective thinning, clear felling and forest sanitation.
Pruning and silvicultural choice are also practised sometimes. Occasional spraying
of felled trees and trapping out beetles in trees or logs are complementary measures
observed in some cases. Most countries involved do carry out occasional monitoring
of this species, mainly through visual surveys, but also using trap trees and
questionnaires. In Poland, a forecast method has been proposed using a risk index of
threat to stands based on glued belt trap catches (Sowiska, 2000), but in Germany
only a risk rating model is used locally; also in this country a pest prediction model
for simulating P. cyanea population dynamics has been developed (Groll et al.,
1993).
Poplars are affected by two buprestid species. Agrilus suvorovi (A. populneus) is
a primary pest of pole trees in Hungary, quite aggressive and distributed, causing a
moderate degree of tree death and growth losses, but only occasional surveys and
selective thinning are applied as control measures; low damage to poplar transplants
by this species is also reported from Slovakia. Melanophila picta is a pest of poplar
transplants in the Iberian Peninsula associated to low vigour trees growing in
unsuitable sites, where it may cause their death. Sanitation, chemically spraying of
standing trees and planting in proper sites are practices occasionally used.
2.4. Conclusions on Buprestidae

Buprestids are considered mostly secondary species that may attack trees of all ages,
but more commonly at pole and older stages. Their type of impact may vary from
wounding trees and causing death of shoots and branches to directly killing the trees.
In many species attacks are associated with previous weakening of trees due to
drought, repeated defoliation, infection by pathogens, unsuitable sites for healthy
growth or a combination of these. Economic damage caused by buprestids is
generally rated to be moderate but reaches high levels in some cases, arising from
tree death, growth losses or timber/cork degradation. However, quantitative data are
rarely offered and damage estimations appear to be based more on qualitative
assessment. Consistent with being classed as secondary, buprestids are usually
classed as of low aggressivity, even though in some countries A. biguttatus and P.
cyanea are considered fairly aggressive. Geographic distribution is quite variable,
depending on the particular pest and country, appearing frequently of local
importance, with some having larger distributions.
Regardless of the damage caused, strategies for controlling these beetles seem to
be scarce or non-existent. No preventative measures are carried out in the majority
of cases, but silvicultural management is by far the main option employed in
Europe, especially by means of selective thinning and sanitation, but only in a few
instances are these applied more than occasionally. Chemical spraying to standing or
felled trees and trapping out in trees aand logs are used sporadically, and no
biological control tactics appeared mentioned in any case. Occasional monitoring of
buprestids seems to be carried out in most countries, mainly through visual
surveys/sampling and, to a lesser extent, questionnaires. Risk rating models and
decision support systems seem far from being integrated in buprestid pest
management in Europe. By contrast, many buprestid species have received
considerable interest from conservation biologists. Many species are red-listed in
several countries, and buprestids are good indicators of biodiversity in the
communities of saproxylic insects. Hence, buprestids are currently attaining more
significance as biodiversity components than as forest pests. In contrast with
longhorn beetles (see below), a few buprestid species are rated as pests in one part
and red-listed in another part of Europe, indicating that great care must be taken in
classifying the pest status and in carrying out any control measures against this
family of BAWBILT organisms.
3. CERAMBYCIDAE
The longhorn beetles, with about 25,000 species, are one of the largest groups of
Coleoptera. Most of the species can be found in tropical and subtropical regions.
European longhorn beetles are divided in the two families Cerambycidae and
Vesperidae and include about 550 species, although there is a distinct decrease from
South to North in the number of species (Bense, 1995). In northern Germany 26% of
the species are associated with broadleaved trees and 50% with coniferous trees
(Dajoz, 2000). Cerambycid beetles, together with representatives of other saproxylic
families are good biological indicators of woodland biodiversity. Only a few species
are damaging to living trees, although they may also be technical pests causing
cosmetic damage by boring into the wood, thus reducing its value as premium
timber. As with the buprestids, many species of longhorn beetles have declined due
to changes in forest practice that tend to leave less dead wood in the woods, and are
hence red-listed in many countries. A few species are rare or even protected in some
countries, and considered as pests in other parts of Europe. For example, Cerambyx
cerdo is protected in the whole of Europe and is a “strictly protected species” in the
Bern Convention and in the Nature 2000 directive. However, it is not always
infrequent and its status may vary from rare (e.g. in Sweden (Ehnström & Axelsson
2002) and in the Netherlands (Huijbregts 2003)), to common (e.g. France (Dajoz
2000)) and it is, therefore, listed as occasionally attacking living trees in Table 2.
However, it is not listed as a pest in the BAWBILT database. Another example, is
Monochamus urussovi, which is rare in northern Sweden (Ehnström & Axelsson
2002), but one of the most important pests in Siberia (Isaev 1995, Vetrova et al.
1999).
3.1. Morphology and biology
3.1.1. Morphology of adult Cerambycidae

These beetles are called longhorns because of their often long antennae, especially in
males. Cerambycidae mostly have elongate and almost cylindrical bodies. They vary
greatly in length: from a few mm up to 55 mm for Cerambyx cerdo. For more
detailed information see Bense, 1995; Bilý, 1982 and Hellrigl, 1974.
3.1.2. Morphology of Cerambycidae larvae

The larvae have a soft and depigmented integument; the legs are reduced or lacking.
Cerambycid larvae that live in the phloem are compressed like those of buprestids;
those that bore their galleries in xylem have cylindrical bodies. For more detailed
information see Bense, 1995; Bilý, 1982 and Hellrigl, 1974.
3.1.3. Biology and ecology of the Cerambycidae

Most of the species usually infest only particular areas of the plants such as roots,
stems (wood, cambial zone, bark), branches or twigs. The conditions of the
substratum (nutrient content, humidity, temperature) are of great importance. These
factors are decisive for infestation. Some species are monophagous (Tetropium
gabrieli in Larix), some are oligophagous (Saperda spp. in Populus and Salix) while
other ((Leiopus nebulosus) are polyphagous in many different tree-species. An
adaptation towards either conifers or broadleaf trees exists in most cases (Bense,
1995).
The adults of many species visit flowers where they feed on nectar and pollen,
while others carry out feeding on bark in the crowns of trees. The mating can take
place on the flowers or on the host plants. The eggs (one egg or a group of eggs) are
usually deposited under bark or in cracks in the wood with the help of the ovipositor.
Some species (Saperda and Monochamus spp.) gnaw excavations into the wood and
deposit a single egg in this hollow. During larval development, which mostly lasts 1-
3 years, several larval stages (for example, up to 14 in laboratory rearing of
Anoplophora glabripennis) are passed through, ending with pupation within
characteristic pupal cells in the host tree (Bense, 1995).
3.1.4. Host finding in the Cerambycidae

Cerambycid adults are well adapted to locate suitable host trees, particularly if they
respond to volatiles produced by dying or recently dead trees, especially in those
attacking conifers. For example, in common with other wood borers, Monochamus
adults are attracted to pine monoterpenes (Erbilgin and Raffa, 2000), and this has led
to some commercial wood borer baits being developed to simulate the odours of a
stressed or dying tree which release host monoterpenes, usually α-pinene, and
ethanol. Recently, addition to host
volatiles of ipsenol and ipsdienol or of
blends containing several bark beetle
pheromone components resulted in
increased attraction of several North
American Monochamus to traps
(Allison et al., 2001, 2003). Other
species, such as Anoplophora
glabripennis, are attracted to living and
stressed trees by host volatiles but also
use visual and tactile clues to determine
the suitability of the host tree. Bark
texture, leaf characteristics and other
factors, such as the density of the trees,
all contribute to host selection in this
genus of beetles (Wang et al, 2000).
Figure 4: Monochamus galloprovincialis adult
on pine bark. Photo: Fernando Ibeas
3.1.5. Host plant resistance

There is evidence that certain tree species are more resistant than others for the same
wood boring insect. One of the key components is the indirect effect of drought
stress that changes the chemical and physical nature of the tree, thus making it more
attractive and, after colonisation, more susceptible to beetle attack. Key among the
defence strategies employed by trees is sap or resin flow and its chemical
composition.
In the case of Saperda populnea there are significant differences in population
sizes on different poplar strains. This finding was positively correlated with
dissolvable total sugar and water content in branches, but no significant correlation
was found with total nitrogen and protein nitrogen content. Amino acid content
differed significantly between poplar strains but was not correlated with S. populnea
population size (Gao et al., 2001).
There are several studies on host resistance in relation to the larvae of the
cerambycid Phoracantha semipunctata on Eucalyptus. Larvae achieved a larger size
in fresh logs, which may offer a fitness advantage because of higher resource
quality. However, greater infestation of that material also increases the probability
of mortality from competition among larvae. The results suggest that there are
potential ecological interactions among food quality, host resistance, natural
enemies, and competition that must be considered in evaluating the population
dynamics of this species in native and novel environments (Paine et al., 2001).
Another study investigated the relative susceptibilities to P. semipunctata of 12

Eucalyptus species in two plantations in California (Hanks et al., 1995). The trees in
these plantations were stressed by water deficit resulting from a prolonged drought.
Some tree species appeared to be resistant to the borer. Survival of trees was
influenced by fine scale moisture variation resulting from slope and irrigation
effects. Resistance characteristics of these Eucalyptus species did not correlate with
taxonomic relatedness or bark characteristics but were those that are most tolerant of
drought in Australia. Larvae were unable to colonize the bark of logs that were
maintained at high moisture content, but were able to colonize the bark of dry logs
and artificially water-stressed trees that had reduced bark moisture content. It is
proposed that bark moisture content plays a critical role in the resistance of
Eucalyptus trees against colonization by larvae of P. semipunctata (Hanks et al.,
1991).
For the Asian Longhorn Beetle, Anoplophora glabripennis, it has been shown
that glycoside and phenolic acid contents of the bark were related to insect resistance
in Poplar trees. In particular, Populus tomentosa was more resistant than P. alba
(Wang et al., 1995).
3.2. Economic importance of the Cerambycidae

About 20% of the European longhorn beetles are of forestry importance or are of
interest, as technical pests, for the timber industry. Within this range of species,
there is a difference between those attacking living trees (Saperda, Cerambyx,
Monochamus, Tetropium, Anoplophora and d Phoracantha), species attacking dying
wood with bark still attached and species attacking dry wood. The last two genera
are introduced pests in Europe, and are potentially invasive species requiring special
attention. The same applies to the genus Monochamus as potential vector of the pine
wood nematode that was recently found in Portugal. Most species are secondary and
exploit either sick or recently felled trees, but some secondary species may
occasionally kill weakened trees as well. For example, Arhopalus rusticus was often
regarded as the cause of mortality of fire-damaged Scots pine trees in Sweden
(Ehnström et al. 1995). Cerambycids that live on decayed wood are more
polyphagous than those that feed on recently dead trees. For more detailed
information see Hellrigl (1974). In judging pest status, regional differences occur.
Some cerambycids are pests in one region but are very rare or even protected by law
elsewhere.
In the BAWBILT questionnaires, a number of more or less damaging species of
Cerambycidae on trees throughout Europe is mentioned in table 2:
3.3. Case studies
3.3.1. Anoplophora glabripennis.

This species, called the Asian longhorn beetle in Europe and North America, is part
of a complex of species in the genus Anoplophora, many of which cause damage to
living trees. They are widely distributed in China and SE Asia but have also attacked
Table 2. Cerambycidae considered to be damaging to trees.
Insect species Trees species Pest area

Acanthocinus aedilis Pinus
Arhopalus rusticus Pinus It, Pr
Arhopalus tristis Pinus, Picea
Aromia moschata Salix, Acer
Callidium violaceum Picea
Cerambyx cerdo Broadleaves
Cerambyx scopolii Quercus
Cerambyx welensii (C.velutinus) Quercus Pr, Sp
Ergates faber Pinus, Picea, Abies, Cedrus
Isarthron castaneum Picea
Isarthron gabrielis Larix
Lamia textor Salix, Populus Hu, Ro
Leiopus nebulosus Broadleaves
Molorchus minor Pinus, Picea
Monochamus galloprovincialis Pinus, Picea It, Pr, Ro
Monochamus sartor Pinus, Picea, Abies Hu, Ro, Sl
Monochamus sutor Pinus, Picea Hu, Ro, Sl
Oberea linearis Carpinus, Juglans
Oberea oculata Salix
Phoracantha semipunctata Eucalyptus,Angophora, It, Pr, Sp
Cupressus
Phymatodes testaceus Broadleaves
Plagionotus arcuatus Quercus
Pogonochaerus fasciculatus Pinus, Picea, Abies, Larix
Prinobius scutellaris Broadleaves
Prionus coriarius Quercus
Pyrrhidium sanguineum Quercus
(Callidium s.)
Rhagium bifasciatum Quercus
Rhagium inquisitor Pinus, Picea, Abies
Rhagium mordax Broadleaves
Saperda carcharias Populus, Salix Et, Fr, Hu, It, NL, Ro, Sl, Sp
Saperda populnea Populus, Salix Fr, Hu, NL, Ro, Sl, Sp
Semanotus laurasi Thuja
Tetropium castaneum Picea Cz, Et, It, Ro, Sl, Sw
Tetropium fuscum Picea Et, Ro
Tetropium gabrieli Larix Cz, Ge, Hu, Sl, Sw
Toxotus cursor Conifers
Cz: Czech Republic; Et: Estonia, Fr: France; Ge: Germany; Hu: Hungary ; It: Italy; NL: the Netherlands;
Pl: Poland; Pr: Portugal; Ro: Romania; Sl: Slovakia; Sp: Spain; Sw: Switzerland
trees in the USA (Haack et al, 2002) and in Austria (Tomiczek et al, 2002). Those
species known to be damaging include A. glabripennis, A. chinensis (=A.
= malasiaca)
(recorded in Italy) and A. macularia. The latter two species are fairly polyphagous
but are most damaging on citrus and various fruit trees, as well as ornamental trees,
whereas A. glabripennis is more a problem on forest and shelterbelt trees, including
the genera Populus, Acerr and Salix (Lingafelter & Hoebeke, 2002). A recent
taxonomic revision by Lingafelter & Hoebeke (2002) has clarified the synonymy of
several species within the genus. The experience with A. glabripennis has illustrated
the risks of movement of pests in international trade; there have been many
examples of interception of members of this genus in packing wood associated with
goods imported from China. Most European countries as well as Canada, USA,
Australia, New Zealand and South Africa, have reported interceptions and the cases
of USA and Austria, where there have been infestations on living trees in the
receiving countries. Eggs are laid in egg slits arising from female feeding on the
bark; there is usually one egg per slit. Larvae go through several instars feeding on
the phloem and it is the girdling of the branches and, sometimes, the stems that lead
to damage and mortality. The mature larvae bore into the wood and form a U-shaped
gallery, culminating in a pronounced pupal chamber, accompanied by production of
copious wood shavings. Exit holes made by the adults are completely round.
CLIMEX® analysis of the ecoclimatic suitability of Europe for A. glabripennis
indicates that the climate of most of southern and central parts of Western Europe is
suitable for establishment and, therefore, damage by this species (MacLeod et al,
2002, 2003).
Several measures for controlling this insectt have been studied in China, where it
is an important pest of poplar plantations. In field tests, planting the highly resistant
Melia azedarach together with the highly attractive Acer negundo within poplar
plantations greatly reduced damage to poplars (Sun et al., 1990). Biological control
trials using the entomopathogenic fungi Beauveria bassiana and B. brongniartii,
cultured in non-woven fabric strips, gave moderate population reduction in poplar
stands (Zhang et al., 1999). Chemical control has been also applied against this pest,
resulting in good control by directly injection of insecticide into larval galleries or
by spraying it in contact-breaking microcapsules (Pan Hua, 2001).
The recent introduction of this pest has caused great concern in the United
States. Estimates of the proportions of urban tree populations at risk range from 12
to 61%, and national maximum potential impact has been set at 1.2 billion trees
killed and monetary losses amounting to $669 billion (Nowak et al., 2001).
Eradication campaigns have been attempted by the felling of thousands of infested
trees and further chipping and incineration, although chipping alone has been
demonstrated to be sufficiently effective (Wang et al., 2000). Studies of adult
dispersal in their native range have indicated
d that effective surveys for adult beetles
and infested trees should cover a minimum distance of 1,500 m from previously
attacked trees (Smith et al., 2001). Rearing protocols and predictive models of
invasion are also being developed in North America as part of the eradication and
management strategies for this pest, (Dubois et al., 2002). There has been little
progress in developing biological control methods and current strategies for
eradication in the USA rely on survey, tree felling and destruction or use of the
insecticide imidacloprid to kill the larval stages in standing, living trees (Haack,
2003).
3.3.2. Phoracantha semipunctata.

The Eucalyptus longhorned borer P. semipunctata is native to Australia and has
become established in most of the regions of the world where its Eucalyptus host
trees have been introduced. It was first detected in Europe in 1969 (Sardinia, Italy)
later being found on the Italian peninsula (1975), Portugal (1980) and south of Spain
(1981).
P. semipunctata is a primary insect infesting water stressed eucalyptus stands at
the pole and older stages in southern Europe. In general, attacks result in significant
economic damage from tree mortality, timber degradation and from
aesthetic/recreational impacts, although no quantitative evaluation is available.
Ranked as having low aggressivity, its distribution is restricted to eucalyptus
plantations in the Mediterranean area. Physical debarking of colonised trees is the
main preventative measure practised in Spain, and a range of silvicultural tactics,
such as selective thinning, clear felling, forest sanitation and silvicultural choice are
occasionally applied in the affected countries.
t In addition, biological control by
parasitoids has been employed occasionally in Portugal and is soon to be
implemented in Spain. Visual surveys or trapping are commonly employed to
monitor this pest, and local or regional risk rating models are utilised sometimes.
General biology: Adults are active during the hours of darkness, resting under litter,
loose bark or bark crevices during the day. They feed on flowers of vigorous trees
but reproduce on stressed, weakened trees. Both sexes congregate on stressed trees
or cut logs where males locate and identify females by antennal contact, which
results in larger males having greater reproductive success due to their greater
antennal spread and to their dominance in fighting off other males (Hanks et al.,
1996). Mated females lay some 300 eggs each, in batches of 10 to 110, under loose
bark, bark crevices or in the undersides of logs. After a few days, eggs hatch and
neonate larvae penetrate the bark and bore feeding galleries along the cambium
layer, consuming phloem and primary xylem. Mature larvae leave the frass filled
galleries in the bark, entering into the sapwood to burrow pupal cells isolated from
the outside by a plug of packed frass. After some 10 to 15 days, new adults chew
their way out of the tree, leaving typical elliptic emergence holes (Romanyk and
Cadahía, 1992).
The number of generations is depending on climate, but one complete (spring-
summer) and a partial second (autumn-winter) generation are typical in the Iberian
Peninsula. In warm areas, development time from egg to adult emergence is quite
short, averaging 3 moths, with a range of 2 to 15 months (Gonzalez, 1992). In
southern Europe, adults are continuously present from early spring to late autumn;
emergence and dispersal is extended for several months and require periods of mean
air temperatures above 15ºC (Gonzalez, 1992), with dispersal distance increasing
with temperature (Hanks et al., 1998). In the laboratory, cold treatments to larvae
delayed adult emergence and resulted in a more synchronised flight, but had no
effect on survivorship or longevity, suggesting that cold tolerance of larvae would
allow spreading of this species into most areas occupied by eucalyptus (Hanks et al.,
1991).
Host location: Several studies have been carried out to elucidate the role of host
volatiles in host location by this species. In field tests, logs and leaves of Eucalyptus
globulus attracted males and females to traps (Barata et al., 1992) and in other
laboratory and field experiments, logs originating from damaged trees attracted
more adults and received more eggs by y females than those from vigorous trees;
significant differences were also found between odour bouquets released by
damaged and undamaged trees. It was hypothesised that long range attraction might
be mediated by terpene compounds, whereas host selection and oviposition would
be affected by odours indicating host tissue damage (Paiva et al., 1993).
In wind tunnel trials, host odours emanating from a log of E. globulus affected
walking and flight behaviour of adults in both sexes, inducing a more directed
upwind movement leading to the insects landing on the target, whereas no attractive
responses were observed when the adults were presented with a visual stimulus in
the absence of host odours (Barata and Araujo, 2001). Further studies have
suggested that both sexes are able to detect a large number of plant volatiles,
including terpenoids and non-terpenoids, from host and non-host trees, employing
them to discriminate between plant species through narrowly tuned olfactory
receptor cells (Barata et al., 2000). Responses from single receptor neurones to host
(E. globulus) and non-host (Pinus pinaster, Olea europaea) odours, obtained by GC-
SCR, showed that olfactory neurones seemed specialised for detection of one or two
related compounds. Although most of them responded to host and non-host
compounds, a few neurones fired specifically when exposed to volatiles from just
one species, suggesting that plant odour information could be conveyed to the brain
in P. semipunctata by two parallel routes, single channels for specific odorants and
multiple channels for other compounds (Barata et al., 2002; Lopes et al., 2002).
Host resistance: Environmental stresses, particularly water deficits, predispose

eucalyptus trees to infestation by P. semipunctata. During drought years this insect
colonises and kills standing trees at a higher rate than in its native habitat. When the
relative susceptibilities to attack were examined in droughtt stressed eucalyptus trees
of different species, resistant species were not taxonomically related but they did
correspond to the most drought tolerant species in their native range (Hanks et al.,
1995).
Resistance of trees to attack by the eucalyptus woodborer has been attributed to
several factors. Recently hatched larvae failed to survive when introduced in
vigorous standing eucalyptus trees or in watered logs, whereas many were able to
colonise dry logs and root-pruned trees. Bark moisture content was correlated with
such differences (Hanks et al., 1991). In artificially infested, water stressed potted
trees, reduced water potentials were associated with susceptibility to colonisation by
neonate larvae; in trees and logs with high bark moisture, larvae were unable to bore
into the cambium and were restricted to feeding on poorer quality tissues beneath
the bark surface (Hanks et al., 1999). Field tests with groups of water stressed, rain-
fed or irrigated trees, found that larval mortality was lower in the former group and
appeared to be related to bark moisture content; higher concentration of soluble
sugars in the bark of stressed trees was also found, accounting for the higher weight
gains of larvae growing in these trees. However, water stress effects on insect
performance were non linear, indicating the existence of a bark moisture threshold
above which larvae survival decreased (Caldeira et al., 2002).
“Kino” exudate, a dark gummy polyphenolic flow emanating from parenchyma
tissues after mechanical or insect injuries to bark, has been also implicated in
eucalyptus resistance. Although dead larvae covered by kino might be seen in tree
galleries, several studies could not conclude that it was a main defensive mechanism
against borer attack (Hanks et al., 1991; 1995; Caldeira et al., 2002), but it may
serve as a barrier zone against micro-organisms (Tippet et al., 1983).
Damage and control: P. semipunctata can colonise trees from very young, 4-5 cm
diameter, to mature. Larval activity in the phloem and cambium layers often leads to
complete girdling of the stem, resulting in tree death, although older and larger trees
may survive a first attack. Besides tree mortality, economic damage by timber losses
in harvested trees might be considerable and impact on eucalyptus recreational and
aesthetic values in urban landscapes are also important in some areas.
Monitoring of P. semipunctata populations in eucalyptus plantations can be
carried out by regular sampling of eggs in trap logs with bark incisions (Gonzalez,
1984) or pinned loose bark pieces (Cillié and Tribe, 1991) to induce oviposition on
them. A model for predicting adult emergence based on accumulated heat units has
been developed for southern Spain (Gonzalez, 1992). The risk of tree mortality can
be reduced by selection of more resistant eucalyptus species, although this would be
dependent also on the specific adaptation of the species to particular environment
conditions. In Morocco, a list of 99 eucalyptus species classed by their relative
resistance to attack within three different climatic regions was provided as a guide in
the silvicultural choice for plantations (El-Yousfi, 1992).
Silvicultural management has been the main control strategy applied against this
pest. The planting and management of plantations to reduce tree stress and to
promote vigorous growth is the main measure employed. Debarking of recently
felled trees, selective thinning and sanitation of attacked trees are also among the
tactics used commonly. Attracting large numbers of beetles to insecticide treated
trap logs has occasionally been successfully used in Spain and Portugal.
Although some early attempts at parasitoidd introduction were made, integration of
this approach in the management of this pest has only recently been introduced. Since
the discovery of the encyrtid Avetianella longoii (Siscaro, 1992), this egg parasitoid has
been the subject of promising biological control programmes against P. semipunctata,
being implemented in several countries (Paine et al., 1995; Hanks et al., 2001). This
species has also been tested on eggs of the other eucalyptus woodborer, P. recurva, but
oviposition and development on this host was lower than in P. semipunctataa (Luhring
et al., 2000). Several studies have been conducted in Australia to select larval
parasitoids for biological control; the braconids Syngaster lepidus and Callibracon
limbatus were found to be dominant, host specific on eucalyptus woodborers and
broadly distributed and are being introduced as biological control agents in California
(Paine et al., 2000; Hanks et al., 2001). Recently, protocols for mass rearing of S.
lepidus and of the gregarious Jarra phoracantha a has been developed there for
continuous production and release against P. semipunctata

a and P. recurva
a (Millar et
al., 2002).
3.3.3. Monochamus spp.

This genus is notable because of its role as the vector for the pine wood nematode,
Bursaphelenchus xylophilus, which is the causal organism of pine wilt disease, a
major tree killer in the Far East. The transmission of the nematodes to susceptible
dying or dead trees occurs during female oviposition. Extensive tree mortality in
Japan and China is associated with the presence of highly susceptible tree species,
suitable vector species and a high summer temperature. Pest risk assessments have
been carried out to determine the risks to Europe, and it is concluded that the
nematode would undoubtedly survive in Europe, but that tree mortality is likely only
in the warmer southern countries, such as in Portugal where an outbreak has been
observed. Methods to prevent transfer of nematodes to Europe are discussed in
relation to European Union legislation (Fielding & Evans, 1996).
In south and eastern Europe, three species of Monochamus are classed as
secondary pests attacking pole and older tree ages of pines, spruces or firs, generally
not killing their hosts but causing wounding and timber losses. Economic damage
from these insects is mainly through timber degradation (technical damage) and is
rated mainly as medium, although in Romania a it reaches much higher levels, with
120,000 m3 of timber and 90,000 ha affected by M. sutorr and M. sartorr in the
1990’s. Social impact arising from damage and reduction of the
recreational/aesthetic value of timber due to M. galloprovincialis, is also of medium
importance in Portugal. Apart from their known effects in Europe, the potential roles
of Monochamus species as vectors of the pine wood nematode (Bursaphelenchus
xylophilus) in Europe are of enormous relevance. Transmission of the nematode by
M. galloprovincialis between trees has already been demonstrated in Portugal,
where the nematode was first discovered in 1999 (Mota et al, 1999; Sousa et al,
2001).
In general Monochamus species are considered off low aggressivity with a
restricted geographical distribution, except for M. sartorr in Romania, where it seems
to be highly aggressive and quite extensively distributed, attacking weakened
standing trees or fallen trees previously infested by bark beetles. Prevention of
attack by physical debarking of trees, forest sanitation, chemical spraying on felled
trees and trapping out beetles are the main measures carried out in that country
against Monochamus pests. Monitoring by questionnaires and selective thinning are
the only measures occasionally implemented in other European countries.
In contrast to the situation in Europe, where Monochamus urussovi is rare, this
species alone and together with the Siberian silk moth (Dendrolimus
( sibiricus) have
caused disastrous tree mortality in Siberian spruce and fir forests (Isaev
1995,Vetrova et al., 1999). Hundreds of thousands of hectares have been devastated,
and the maturation feeding of the adult beetles on the twigs alone has rendered the
trees susceptible to stem attack in a self-perpetuating vicious circle. As far as
known, the pine wood nematode is not involved in this process.
Monochamus spp. are among the most destructive technical pests causing timber
degradation in North America log yards. Annual losses attributable to large wood
borers have been estimated to be $CAN43.6 m in British Columbia alone (Allison et
al., 2001). Recent work on attractive baits, based on host volatiles and bark beetle
pheromones (Allison et al., 2001, 2003), together with an improved trap design
(Groot and Nott, 2001; Morewood et al., 2002) could lead to an efficient device for
monitoring and mass-trapping of these pests.
In Japan, the Japanese pine sawyer M. alternatus is the main vector of the pine
wood nematode, responsible for the spreading of the nematode which, combined
with highly susceptible tree species and high temperatures, has resulted in massive
tree mortality from pine wilt disease (Mamiya, 1988). Several studies have been
conducted to integrate efficient biological control tactics with classical sanitation
and removal of infested trees, using the predator Trogossita japonica (Ogura and
Hasada, 1995), the nematode Steinernema carpocapsae (Yamanaka, 1994) and the
fungi Beauveria bassiana and B. brogniartiii (Shimazu, 1994) as control agents.
Diverse delivery methods for B. bassiana have been tested, including wheat-bran
pellets (Shimazu et al, 1992), mass-release of Cryphalus fulvus (Coleoptera:
Scolytidae) beetles as vectors (Kinuura et al., 1999) and non-woven fabric strips; the
latter technique applied to trees and logs obtained a high larval mortality (Shimazu
et al., 1995) and reduced longevity and oviposition of emerged adults (Okitsu et al.,
2000), proving that it could be suitable for practical use.
The discovery of pinewood nematode in Portugal t in 1999 has resulted in
considerable activity in thatt country to determine both the extent of the infestation
and also to introduce an eradication programme. Measures to identify, fell and
destroy trees showing wilt symp m toms have been in place since 1999 and are included
in a national eradication programme under the acronym PROLUNP
(http
tp://
/ www.dggf.
f min-aggricultu
t ra.ppt/
t/prolunpp/html/home-fi
f nal.htm). An affected zone,
surrounded by a buffer zone has been delineated and all trees showing symp m toms of
wilt are felled and some (affected zone) orr all (buffer zone) are assessed for the
presence of the nematode. Research into the vector relationships in Portugal t have
revealed that M. galloprovincialis i , which is the representative off the genus in the
southern partt of Porttugal, has taken on the role of vector for the nematode (Sousa et
al, 2001).
3.3.4. Tetropium spp

Three species of Tetropium longhorns affect spruce and larch stands in north and
central Europe. Rated as secondary pests attacking pole and older stages, their
impacts range from wounding to directly causing tree death, depending on the
species and country considered. The larch longhorn, T. gabrieli will attack dying or
severely stressed standing trees such as those affected by the root rot fungi
Armillaria spp. or Fomes spp. Eggs are laid in the bark during the summer and the
larvae initially tunnel beneath the bark but penetrate into the wood later in the year
(Speight & Wainhouse, 1989). T. gabrieli lives on larch, but females can be induced
to lay their eggs on pine and spruce, on both of which larvae grow normally (Dajoz,
2000). T. gabrieli wounds and generally kills its hosts in north and central Europe,
causing economic damage arising from tree death and timber degradation. In
Switzerland, it also has considerable impacts by reducing the roles of trees in
protection from avalanches and from erosion; even though its economic impact is of
medium importance; however, no quantitative estimates are provided. Although less
widely distributed than T. castaneum, it seems more aggressive, even highly
aggressive in Germany, where during dry and hot summers, population build-ups
occur on felled trees, leading to attacks on living neighbouring stands.
T. castaneum causes significant economic damage attributable to tree death,
growth losses and timber degradation in Switzerland and Romania; in the latter it
affected 180,000 ha and 225,000 m3 of spruce in the 1990s, where attacks by this
species were related to bark beetle and weevil attacks and an associated fungus.
Although regarded as aggressive in Romania, T. castaneum is generally ranked as
minor in the other countries, although it is widely distributed. A third species, T.
fuscum is reported as a pest of lesser importance in a few BAWBILT countries. In
Finland, T. fuscum and T. castaneum were earlier considered major mortality factors
of senescent Norway spruce trees (Juutinen 1955), but with intensified forestry their
importance in Nordic forestry has decreased. The recent finding of T. fuscum in
Canada (Halifax, Nova Scotia) where it appears to be killing weakened trees
indicates that, given suitable conditions, it can be damaging (Smith & Humble,
2000). Preventative strategies against Tetropium pests are quite widespread among
the more affected countries. The strategies include, as the main measure, debarking
although covering felled timber, processing and burning are also employed on
occasion. Silvicultural management, whether it is clear felling, selective thinning or
forest sanitation, is also applied in these countries, but not as a main practice. A few
cases of insecticide application to felled trees and direct trapping out in trees or logs
are also reported. Population monitoring and forecasting of these longhorns is not
common practice in Europe, but several countries carry out occasional
surveys/sampling or distribute questionnaires. Even less frequently a simple risk-
rating model, based on percentage off attacked trees, may be applied.
3.3.5. Saperda carcharias and S. populnea

These are wood-boring beetles on poplar and willow in many parts of Europe. S.
carcharias produces galleries in the wood in an upward direction with a length of
about 25 cm. It acts either as a primary or a secondary pest, affecting poplar
plantations mainly in the pole and older stages. Generally it does not kill the trees,
but causes wounding of trunks. Economic damage arising from timber degradation
or even growth losses is regarded as moderate, with figures averaging 2-3,000 ha or
4,000 m3 affected during the last decade in some countries. In Finland, hybrid aspen
was found to be particularly sensitive to attack by Saperda (Löyttyniemi 1972).
Other types of damage, such as recreational or aesthetic impact, death of transplants
and risk of trees falling during rainstorms in roadside plantations where tree
structure has been weakened by high larval activity, may be of particular relevance
in certain countries. The degree of aggressive attack and extension of the range of
this pest is quite variable among countries, generally being ranked from low to
medium.
Common in amenity areas, S. populnea produces galls on the branches. Populus

tremula and P. alba are especially affected. S. populnea is a primary pest in many
areas, causing wounding and death of branches and shoots to poplar transplants or
even complete mortality. Distortion of tree shape, which is of medium importance,
is the main economic damage resulting from this insect, but growth losses and, to a
lesser extent, tree death and timber degradation are also noted occasionally.
Quantitative estimates are scarce, but it may have affected 2-4,000 ha of plantations
in some east European countries during the 1990s. Although poorly documented,
massive attacks of S. populnea in plantations of hybrid aspen in southern Sweden in
the 1950s (Brammanis 1963), in fact terminated the plans to grow hybrid aspen for
the match industry in Sweden. Considered to have variable aggressivity, from low to
high, its presence also ranges from local to widely distributed.
Quarantine or preventative measures are not applied for controlling these species
of Saperda, except for very few instances of movement restriction and burning.
Again, silvicultural management seems to be the main control strategy used in
Europe, mostly through selective thinning and forest sanitation applied regularly
through the life of the forest crop. Other measures such as clear felling, site
preparation or even pruning are less widespread and only used occasionally.
Chemical insecticide spraying on standing trees against adults is also employed
infrequently in several countries. In Italy, good results in preventing adult movement
and oviposition were obtained using stem barriers made of an aqueous dispersion of
teflon applied to the basal meter of trees (Allegro, 1990). Occasional monitoring by
visual surveys/sampling is carried out in the majority of countries, but a local risk
model is used only in Romania.
3.3.6. Cerambyx welensii

In the Iberian peninsula, Cerambyx welensiii is a secondary pest causing wounding in
holm and cork oak stands, particularly those stressed or weakened by drought, or
suffering decline for unknown reasons. Significant effects on tree shape, protective
and recreational values, or even tree death are assigned to this insect, which has
affected more than 20,000 ha during the lastt decade in Spain. Of low aggressivity
but widely distributed, this pest is mainly managed through selective thinning,
pruning and sanitation of oak stands, whereas visual surveys and occasional
deployment of light traps are used for population monitoring.
3.4. Conclusions on Cerambycidae

In summary, bark and wood boring cerambycids in Europe form a group of species
considered mainly to be secondary pests, although some are classed as primary.
They are generally of low aggressivity and have restricted geographical ranges. The
majority would be included in the stressed host species category (sensu Hanks,
1999), attacking woody plants that are severely stressed, often near to death, by
drought or by the actions of other organisms. However, a few such as A.
glabripennis and Saperda spp, could be classed as damaging to healthy hosts or
weakened hosts, ovipositing only in growing trees that are fully vigorous or
weakened in some way, but not to a significant extent that could lead to tree
mortality. Impacts produced by longhorn larvae on pole and older trees are mainly
wounding and death of branches, but in some cases, tree mortality may directly
result from beetle attack. Main economic damage is derived from their impacts on
timber quality, frequently considered as of medium significance, but a lack of
quantitative estimates makes it difficult to provide specific information on this
aspect. Although of lesser overall importance, impact by tree death is also a serious
threat in certain species. Other types of economic impact of decreasing relevance
produced by these longhorn beetles are loss of volume increment, impacts on tree
shape and reduction of recreational, aesthetic and protective values.
Among control strategies, preventative measures are rarely applied against these
insects, though occasional physical treatments, generally by debarking or even
burning, are used for the most damaging species. In many cases, when damage is
regarded as low or even medium significance, no management is practised against
these pests. However, basic silvicultural management through selective thinning
and/or forest sanitation is generally applied in the most affected countries, even
though only in half of the cases are these measures regularly conducted. Insecticide
spraying on felled or standing trees and, to a lesser extent, trapping out of insects in
trees and logs, are tactics complementary to sanitary felling that may be used
occasionally in some countries. Many of them do carry out non-routine surveys for
monitoring of cerambycid pests, but there are very few examples of simple, local
risk models utilised in their management. The arrival of pinewood nematode,
B. xylophilus, in Portugal has increased the interest in Monochamus spp. and has
resulted in improvements to the monitoring and management of M. galloprovincialis
in the Iberian Peninsula.
4. OVERALL CONCLUSIONS
- Most of the European Buprestidae and Cerambycidae are of secondary importance,
because many of them only infest trees which are weakened by severe drought or
defoliation, etc. Many of these species have declined in numbers and are rare, red-
listed or even protected in parts of Europe.
- Some tree species are more resistant than others
t to boring insects, but often this is
related to environmental factors, such as the incidence of drought, rather than
intrinsic genetic resistance. Some insect species are attracted by secondary plant
metabolites but the quantities of these may be linked to the state of health of the tree,
especially when extrinsic factors such as drought, wind damage, etc. are involved.
- The maintenance of healthy, vigorous trees is always the best defence against
insect attack. This can involve irrigation where possible and necessary, possible use
of fertilizers and the removal of infested trees and, particularly, the growing of tree
species and seed origins appropriate to the particular site and climate of the area.
- Sustainable forestry practices should diminish the factors which cause poor
physiological condition of the trees. On dry sites certain broadleaved trees could be
replaced by more adapted trees e.g. pine. Long-term measures should also include
broadening the age structure by encouraging natural regeneration, formation of
mixed forests and developing the shrub and underwood layers. This underwood
produces organic material, and by this, improving the formation of good organic
soil. Furthermore, underwood provides shade on the tree trunks which can decrease
the susceptibility of the trees for infestation by sun loving borers, especially the
Buprestidae. Care should be taken in carrying out thinning and harvesting because
of changes to microclimate and potential mechanical damage to the remaining
standing trees.
- For the majority of buprestid and longhorn species conservation issues are
important elements of sustainable forestry with the aim of maintaining a high
biodiversity. Thus, a crucial question in forest management is how to provide
suitable brood material for rare species without risking increased population levels
of pest species. This is a major challenge for research in forest protection and
conservation.
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Chapter 21
NATURAL ENEMIES OF CERAMBYCIDAE AND

BUPRESTIDAE INFESTING LIVING TREES
M. KENIS 1 & J. HILSZCZANSKI 2
1
2
Department of Forest Protection, Forest Research Institute, 00-973 Warsaw,
Poland
1. INTRODUCTION
Several species of Cerambycidae are known to attack living trees in Europe.
Conifers are attacked by Tetropium castaneum L., T. fuscum F., T. gabrieli Weise,
Arhopalus rusticus (L.), Monochamus galloprovincialis (Olivier), M. sartorr (F.) and
M. sutorr (L.). Broadleaved trees are damaged by Saperda populnea (L.), S.
carcharias (L.), Lamia textorr (L.), Cerambyx cerdo L. and C. velutinus Brullé.
Among Buprestidae, the following European species are associated with living trees:
Agrilus angustulus (Illiger), A. biguttatus (F.) (= pannonicus Piller and
Mitterpacher), A. populneus Schaeffer (= suvorovi Obenberger), A. viridis (L.),
Coraebus florentinus (Herbst), Coraebus undatus (F.), and Melanophila picta Pallas
on broad-leave trees, and Phaenops cyanea (F.) on conifers.
Although many studies have investigated various aspects of the biology,
ecology, damage and control of these insects, the information on their natural
enemies is surprisingly limited. Hardly anything is known of their associated
pathogens and nematodes, and knowledge of predators is usually limited to non-
quantified observations. Parasitoids have received more attention, particularly in a
few target host species, e.g. Tetropium spp., Saperda spp. and A. viridis. However,
most of these studies are old, often incomplete, and confined to a limited geographic
area. Other species (e.g. Monochamus spp, L. textor, Cerambyx spp., C. undatus, M.
picta, A. angustulus), have never been the target off specific studies. In most cases,
information on parasitoids is restricted to unreliable host-parasitoid records in
catalogues or taxonomic books. Tables 1-3 list most species mentioned as
parasitoids in the literature in Europe. A preliminary sorting has been made in the
tables to separate dubious records from reliable data, but this list probably still
contains numerous errors.
475
475–498.
© 2007 Springer.
476 M. KENIS & J. HILSZCZANSKI
In addition, exotic cerambycid species have recently invaded Europe; these

include the Australian Phoracanta semipunctata F, attacking eucalypt plantations in
southern Europe, and Anoplophora chinensis (Forster) and A. glabripennis
(Motchulsky), newly introduced Asian pests of broadleaves. These species have
been also introduced elsewhere in the world and, as such, have been the target of
biological control programmes including specific studies on their natural enemies.
2. CERAMBYCIDAE
2.1. Conifer feeding species
2.1.1. Arhopalus rusticus

There has been no specific study on the natural enemies of this pine and spruce-
feeding beetle. A few records are found in the literature (Table 1), some more
reliable than others. The most often cited parasitoid of A. rusticus is the
ichneumonid Odontocolon dentipes (Gmelin) (e.g. Herting 1973; Aubert 1969;
Slama 1998; Hilszczanski 2002). This species is commonly found on A. rusticus in
old pine forests, with apparently two generations per year (Hilszczanski,
unpublished). Another reliable record is the ichneumonid Dolichomitus mesocentrus
(Gravenhorst) (Dominik 1958; Kinelski 1971), a common species found on different
wood borers on conifers. The other records are less verifiable. Some are very
doubtful, such as the ichneumonids Poemenia notata Holmgren, a parasitoid of
sphecid wasps, and Xorides fuligator (Thunberg), a parasitoid usually reared from
broadleaved trees.
Several Polish authors briefly mention predators of A. rusticus. Dominik (1958)
suggested that the larvae of the asilid fly Laphria gibbosa (L.) was one of the main
natural enemies of A. rusticus, attacking mainly larvae. He also mentioned
woodpeckers, badgers and wild boars looking for larvae in decaying stumps.
Wiackowski, (1957) and Slama (1998) cite elaterids of the genera Athous,
Melanotus and Elater, and the histerids Plegaderus saucius Erichson and Paromalus
parallelepidus (Herbst) as potential predators of larvae and pupae.
2.1.2. Monochamus galloprovincialis

Very little is known of the natural enemies of this pine feeding species. Until
recently, M. galloprovincialis was considered to be of secondary and minor
importance because it attacks mainly dying orr stressed trees. However, it is regarded
as the main vector of the recently introduced pine wood nematode in Portugal
(Sousa et al. 2001) and, as such, will probably attract more attention in the near
future. Until now, there has been no specific study on the parasitoids of M.
galloprovincialis. The braconids Atanycolus genalis (Thomson) and Meteorus corax
Marschall are the most reliable record listed in Table 1. A. genalis is a very common
and widespread species found on many cerambycid species feeding on conifers
(Filippenkova 1971, as A. initiator F.; Tobias 1986). M. corax has been mentioned
as a parasitoid of M. galloprovincialis by Tobias (1986) and Martikainen and
NATURAL ENEMIES OF CERAMBYCIDAE AND BUPRESTIDAE 477
Koponen (2001), but little is known of its biology. Other recent records include
undetermined species. Campadelli and Dindo (1994) mention a solitary, unidentified
ichneumonid parasitoid on larvae in Italy, and Tomminen (1993) an undetermined
tachinid on larvae in Finland. Apart from woodpeckers, predators and pathogens are
not known (Slama 1998).
2.1.3. Monochamus sartor and M. sutor

These two closely related species are found
f mainly on spruce and, occasionally, on
pine, over a large part of Europe. As is the case for their congeneric species M.
galloprovincialis, predators and pathogens are not known, and the only records of
parasitoids are found in host-parasitoid lists and in taxonomic books, which often
contain many doubtful host-parasitoid associations. The list of parasitoids provided
in Table 1 includes species that are well-known parasitoids of spruce Tetropium
spp., such as the braconids Helconidea dentatorr (F.) and Atanycolus genalis
(Schimitschek 1935, 1964; Capek 1985; Tobias 1997), which may attack
Monochamus spp. in the same spruce logs. Other possible records include the
braconid Iphiaulax impostor (Scopoli), often cited as parasitoid of both species
(Herting 1973; Capek 1985; Tobias 1986), or Dolichomitus tuberculatus
(Fourcroy) (Schimitschek, 1935, 1964), a polyphagous ichneumonid parasitoid of
large xylophagous beetles in conifer logs. Three species of the genus Rhyssa are also
mentioned (Schimitschek 1935; Aubert 1969). Rhyssa spp. are usually associated
with siricid wood wasps but it seems that they may also attack cerambycids
(Schimitschek 1929, who observed cocoons in galleries of Tetropium gabrieli), and,
thus, their association with Monochamus spp. cannot be totally ruled out.
2.1.4. Tetropium castaneum and T. fuscum

These two species are closely related. They both attack spruce logs, co-occur in
most parts of the distribution of spruce in Europe, have a very similar biology, and
are very difficult to identify at the larval stage. Consequently, they tend to share the
same parasitoid complex, and records attributed to one species might in fact concern
the other species. Tetropium spp. are the only European conifer cerambycids of
which the parasitoid complex is rather well known, thanks to specific studies. In
particular, Juutinen (1955) published an extensive work on T. castaneum and T.
fuscum in Finland, including a good description of their parasitoid and predator
complexes. Similarly, Schimitschek (1929) described the natural enemy complex of
T. fuscum (and T. gabrieli) in Moravia and Austria, and Wettstein (1951) provided
some information on parasitism of T. fuscum in Austria. These studies contain
reliable host-parasitoid records and some aspects of the impact and biology of
parasitoids. However, since these are old publications, parasitoid identification is
confusing. In Table 1, we mention the presently accepted taxonomic identities, but
misidentifications in the original studies are possible.
The most important parasitoid of spruce Tetropium spp. is undoubtedly the
braconid Helconidea dentator. In Schimitschek (1929), Wettstein (1951) and
Juutinen (1955), it was by far the main parasitoid (e.g. 84% of all parasitoids in
Finland). It is mainly known as a parasitoid of Tetropium spp. (including T. gabrieli
on larch), but host records also include other longhorn beetles in the genus
Monochamus (Table 1).
Table 1. Parasitoids of European Cerambycidae living in fresh conifer wood. XX = mentioned as reared
from the host in a study specifically focused on the host or parasitoid; (XX) = As XX, but parasitoid
identification appears doubtful to the authors; X = Recorded in a catalogue, host-parasitoid list,
taxonomic publication or from a non-specific study; (X) As X, but parasitoid identification or host-
association appear doubtful to the authors.
Monochamus Gallo-
Monochamus sartor
Monochamus sutor
provincialis
castaneum
Arhopalus
Tetropium
Tetropium
Tetropium
rusticus
gabrieli
fuscum
Main host trees Pinus Pinus Picea Picea Picea Picea Larix
Picea Pinus
Main references1 2,3,5, 2,6,25 2,3 13,19 2,10,11 2,9,10 1,2,4,8,
7,11, 13,19 20,23 13,14 11,13,14 11,12,13
13,14 25 16,17 15,16,18 14,18,19
17,23 19,23 19,20,21 20,21,22
25 24,25 23,25,26 23,25
26 27
Ichneumonidae
Clistopyga sauberi Brauns (X)
Coleocentrus caligatus Gravenhorst X
Deuteroxorides elevatorr (Panzer) (X)
Dolichomitus aciculatus (Hellén) X
D. dux (Tschek) XX
D. imperatorr (Kriechbaumer) X XX
D. mesocentrus (Gravenhorst) XX X X XX XX
D. populneus (Ratzeburg) X
D. sericeus (Hartig) XX
D. terebrans (Ratzeburg) X
1
D. tuberculatus (Geoffroy) X X X X1
Helcostizus restaurator (F.) X1 X1 X
Ischnoceros caligatus (Gravenhorst) X XX
Lissonota buccatorr (Thunberg) (X)
Neoxorides collaris (Gravenhorst) XX XX XX
N. nitens (Gravenhorst) X
Odontocolon appendiculatum Grav. (X)
O. dentipes (Gmelin) XX (X)
(= pinetorum (Thomson))
O. quercinum (Thomson) (X)
O. spinipes (Gravenhorst) XX
Odontocolon sp. X
Perithous divinatorr (Rossi) (X)
Podoschistus scutellaris (Desv.) (X)
Poemenia hectica (Gravenhorst) X1 X1
P. notata Holmgren (X) (X) (X)
Rhimphoctona lucida (Clément) XX
R. megacephalus (Gravenhorst) (X) X X (X)
(= austriacus (Tschek))
R. obscuripes (Holmgren) X
R. pectoralis Kriechbaumer X
Table 1. (cont.)
Monochamus
Monochamus
Monochamus
provincialis
castaneum
Arhopalus
Tetropium
Tetropium
Tetropium
rusticus
gabrieli
fuscum
sartor
Gallo-
sutor
R. teredo (Hartig) X X XX
(=xoridoidea
= (Strobl))
R. xoridiformis (Holmgren) X X XX XX
Rhyssa amoena Gravenhorst (X)
R. persuasoria (L.) (X) (X) XX
Townesia tenuiventris (Holmgren) (X)
(=antefurcalis Thomson)
Xorides aterr (Gravenhorst) (X) (X) (XX) (X)
X. brachylabis (Kriechbaumer) X XX XX XX
X. ephialtoides (Kriechbaumer) (X)
X. fuligator (Thunberg) (X)
X. irrigator (F.) XX X XX
X. praecatorius (F.) X XX
X. propinquus (Tschek) X
Braconidae
Atanycolus denigrator (L.) X X XX
A. genalis (Thomson) (=initiator F.) X X X XX XX
A. ivanowi (Kokujev) X
(=sculpturatus Thomson))
A. neesii (Marschall) X X XX
Coeloides forsteri Haeselbarth X
Doryctes leucogaster (Nees) X
D. mutillatorr (Thunberg) X X XX
(= obliteratus (Nees))
D. undulatus (Ratzeburg) X
Helcon angustator Nees X X
(= redactorr (Thunberg))
H. tardator Nees (X)
Helconidea dentatorr (F.) X X XX XX XX
Iphiaulax impostorr (Scopoli) X X
Meteorus corax Marshall X
Ontsira antica (Wollaston) X X
O. imperatorr (Haliday) X X
Tachinidae
Billaea adelpha (Loew) X
B. triangulifera (Zetterstedt) XX XX XX
Undetermined Tachinidae X
1
Recorded from Tetropium sp. on spruce
2
References: 1: Achterberg (1987); 2: Aubert (1969); 3: Capek (1985); 4: Chrystal and Skinner (1931);
5: Dominik (1958); 6: Filippenkova (1971); 7: Fitton et al. (1988); 8: Gorius (1955); 9: Hedqvist (1967);
10: Hedqvist (1998); 11: Hellrigl (1974); 12: Hellrigl (1985); 13: Herting (1973); 14: Hilszczanski
(2002); 15: Hilszczanski (unpublished); 16: Juutinen (1955); 17: Kinelski (1971); 18: Schimitschek
(1929); 19: Schimitschek (1935); 20: Schimitschek (1964); 21: Schimitschek (1967); 22: Skrzypczynska
and Król (1974). 23: Slama (1998); 24: Thompson (1943); 25: Tobias (1986); 26: Wettstein (1951); 27:
Wichmann (1955).
Among ichneumonids, Rhimphoctona xoridiformis (Holmgren) and Xorides

brachylabis (Kriechbaumer) are also major parasitoid of Tetropium spp.
(Schimitschek 1929; Juutinen 1955). X. brachylabis appears strongly associated
with the genus Tetropium (Aubert 1969; Hilszczanski 2002) whereas very little
information is available on the host range of R. xoridiformis. Neoxorides collaris
(gravenhorst) is also abundant and often cited from both spruce Tetropium spp. in
the whole Europe (Schimitschek 1929; Juutinen, 1955; Aubert 1969; Kinelski 1971;
Herting 1973; Slama 1998; Hilszczanski, unpublished). Schimitschek (1929), and
Juutinen (1955) also mention as frequent parasitoids the ichneumonids Xorides
praecatorius (F.), X. aterr (Gravenhorst) (although often confused with X.
brachylabis), and Odontocolon spinipes (Gravenhorst), the braconid Atanycolus
genalis (as A. initiator) and the tachinid Billaea triangulifera (Zetterstedt), which
has also been observed by Wettstein (1951). Other reliable records are the
ichneumonids Rhimphoctona teredo (Hartig) and Xorides irrigatorr (F.), reared by
Hilszczanski (2002) in Poland, and mentioned by Schimitschek (1935) and
Wichmann (1956) in Austria and Germany. Hedqvist (1998) reared the braconids
Ontsira antica (Wollaston) and O. imperatorr (Haliday) from both species in
Sweden, whereas Doryctes mutillatorr (Thunberg) and D. leucogasterr (Nees) are
mentioned by several authors (Herting 1973; Tobias 1997; Hedqvist 1998; Slama
1998), Finally, several Dolichomitus spp. are frequently mentioned in the literature
(Table 1) (e.g. Schimitschek 1929, 1935, 1967; Slama 1998), but the taxonomy of
this ichneumonid genus is confusing, and the list probably contains
misidentifications. A certain record is D. sericeus (Hartig), reared from T. fuscum by
Hilszczanski (unpublished) in Poland.
Although all parasitoids parasitising Tetropium spp. kill their hosts at the larval
stage, they have different biologies, described by Schimitschek (1929) and Juutinen
(1955). Some of the hymenopteran parasitoids oviposit into young larvae,
overwinter inside them, then in spring kill their host and build a cocoon in the pupal
gallery in the wood. This biology is encountered in H. dentator, and probably
Rhimphoctona spp. In contrast, Ichneumonidae of the sub-families Xoridinae
(
(Xorides spp., Odontocolon spp.), Pimplinae (Dolichomitus
( spp., Neoxorides spp.),
and the braconids Atanycolus spp., oviposit on larvae in the inner bark, develop
externally on paralysed larvae, and build a cocoon, in which they overwinter,
between the bark and the wood. The tachinid B. triangulifera also lives
endoparasitically and puparia are found in the pupal gallery in the wood (Juutinen
1955). Schimitschek (1929) also provides further information on the biology of the
main parasitoids such as the period of adult emergence, and a detailed description of
all developmental stages, including cocoons.
Parasitism rates are not negligible. Averages of 42.6% and 20.3% have been
observed in southern Finland, for both spruce species. In Moravia/Austria,
Schimitschek (1929) found, for T. fuscum and T. gabrieli together, about 20%
parasitism in the first year, but the rate increased to 51 and 75 % in the second and
third years, after he had left on site the logs with the highest parasitism rates. In the
same two years, host population levels had dropped 20-fold. However, it is not clear
whether this strategy of parasitoid conservation was responsible for the increase in
parasitism and the collapse of host population. Wettstein (1951) found only 6.5%
parasitism in Austria, but this was on a single, heavily attacked log.
Predators, nematodes and fungi are mentioned in Schimitschek (1929) and
Juutinen (1955) for T. fuscum, and Juutinen (1955) and Slama (1998) for T.
castaneum. The three authors mention woodpeckers as the most important predators
of Tetropium spp. In Finland, Juutinen observed that an average of 20% of the
galleries were opened by woodpeckers. Schimitschek (1929) observed the black
woodpecker ((Dryocopus martius L.) feeding on Tetropium spp. in larval and pupal
galleries, as well as on parasitoid larvae and cocoons. Among insect predators, the
following species were found feeding on Tetropium spp. on spruce: Thanasimus
formicarius (L.) (Col.: Cleridae) in Finland, Moravia/Austria and Poland, Athous
subfuscus Müller (Col.: Elateridae) Palloptera usta (Meigen) (Dipt.: Pallopteridae)
and Raphidia xanthostigma Schummel (Neur.: Raphidiidae) in Finland, Rhaphidia
notata F., Inocellia crassicornis (Schummel) (Neur.: Rhaphidiidae), and Forficula
auricularia L. (Derm.: Forficulidae) in Austria. Schimitschek (1929) gives a
detailed description of the biology and morphology of the earwig and the
Raphidiidae. All these insects are known as polyphagous predators of various bark
and wood boring insects. Mites on adults and nematodes in larvae were mentioned
by both Schimitschek (1929) and Juutinen (1955), but their exact role could not be
assessed. Finally, Juutinen (1955) found about 1% of Tetropium larvae killed by
unidentified fungi. However, it was not clear whether these fungi were really
entomophagous or saphrophitic. A higher mortality was caused by competition with
Armillaria mellea (Vahl), whose mycelium was often found overwhelming
Tetropium larvae and pupae.
2.1.5. Tetropium gabrieli

This species is taxonomically and biologically close to T. castaneum and T. fuscum,
but it is found exclusively on larch. The most complete study on its natural enemy
complex has been carried out by Schimitschek (1929) in Moravia and Austria, and
additional information is found in Chrystal and Skinner (1931) in England, Gorius
(1956) in Germany, Hellrigl (1985) in northern Italy, and Slama (1998) in former
Czechoslovakia. Parasitism in Central Europe is rather similar to that observed in
spruce Tetropium spp. Schimitschek (1929) observed, as main parasitoids, the
braconid H. dentator, and the ichneumonids N. collaris and X. brachylabis, three
parasitoids that also dominated in the same area on T. fuscum. Other important
parasitoids were X. irrigator, Atanycolus denigratorr (L.), A. neesi (Marschal), and
Rhyssa persuasoria (L.). The latter is a parasitoid usually associated with siricid
woodwasps. Schimitschek reared it from T. gabrieli larvae, but in England Chrystal
and Skinner (1931) observed that R. persuasoria emerging from larch logs
containing T. gabrieli larvae were in fact always associated to the woodwasp Sirex
cyaneus F. In Germany, Gorius (1956) found H. dentator, X. irrigator, R.
xoridiformis and the braconid Doryctes mutillatorr as main parasitoids. In Italy,
Hellrigl (1985) also reared H. dentator, but it was dominated by Rhimphoctona
lucida (Clément), an ichneumonid reared in low numbers in Austria by
Schimitschek (1929), and by the tachinid Billaea triangulifera, which has also been
obtained from spruce Tetropium spp. in Finland by Juutinen (1955) and in Germany
by Wettstein (1951). Other reliable records include the ichneumonids Ischnoceros
caligatus (Gravenhorst), reared from T. gabrieli in Czechoslovakia and Poland
(Slama 1998; Hilszczanski 2002), Dolichomitus spp. reared from larvae in Austria,
Germany and Czechoslovakia, despite probable species misidentifications
(Schimitschek 1929, 1935, 1967; Gorius 1956; Slama, 1998), and A. genalis (as
initiator) (Gorius 1956; Slama 1998). T. gabrieli has been introduced into England
in the early 20's century, where it is attacked by two parasitoids, X. brachylabis and
X. irrigatorr (Chrystal and Skinner 1931). A eupelmid, Calosota acron (Walker) (as
C. anguinalis Ruschka) was found as hyperparasitoid in X. brachylabis cocoons.
The biology and morphology of most of these species is described in
Schimitschek (1929) (see above in the paragraph on spruce Tetropium spp.). In
addition, Chrystal and Skinner (1931) provide a detailed study on the biology of X.
brachylabis and X. irrigator, including flight periods, mating and oviposition
behaviour, description of developmental stages and host specificity. Both species lay
their eggs through the bark on paralysed larvae in galleries. The parasitoid develops
quickly on the host larva and the last instar larva builds a cocoon in the inner bark,
in which it overwinters. Laboratory screening tests on other longhorn beetles suggest
that X. brachylabis is specific to Tetropium but X. irrigatorr was reared from
longhorns Acanthocinus griseus (F.), Rhagium inquisitor (L.) and Obrium brunneum
(F.) (Hilszczanski 2002). Parasitism in England varied from 16 to 59.5%. In Italy
parasitism at emergence was 41.5 and 68% at two sites (Hellrigl 1985). In
Austria/Moravia, Schimitschek (1929) observed 20% parasitism in T. gabrieli and T.
fuscum, but a parasitoid conservation programme increased parasitism rates to 51
and 75% in the following years.
Schimitchek (1929) observed the same polyphagous predators feeding on larvae
of T. gabrieli as in T. fuscum: the black woodpecker, the earwig Forficula
auricularia, the raphidiid Inocelia crassicornis, the beetles Malachius bipustulatus
(L.) and Thanasimus formicarius, and undertermined dipteran larvae. Gorius (1956)
emphasises the role of woodpeckers as natural enemies and estimated that between
10 and 20% of the larvae and pupae were eaten by woodpeckers. In this study, the
raphidiid Raphidia notata was the main insect predator, whereas the earwig F.
auricularia and the flies Palloptera usta and Lonchaea zetterstedti Becker (Dipt.:
Lonchaeidae) were also observed preying on larvae and pupae.
2.2. Broadleaf feeding species
2.2.1. Saperda populnea and S. carcharias.

The small poplar longhorn, S. populnea is probably the most damaging native
cerambycid in Europe and, as such, it has been the target of many studies. However,
information of its natural enemy complex is usually restricted to lists of parasitoids
and predators reared as part of general studies. Table 2 lists the parasitoids of S.
populnea cited in the literature. This list does not include old records which are
particularly dubious, e.g. from Scheidter (1917). However, Table 2 still contains
many errors, which result either from identification mistakes or wrong host-
parasitoid associations. Most studies on natural enemies of S. populnea in the last

40 years cite the same few parasitoid and predator species (Brammanis 1963, in
Sweden; Kailidis 1964, in Greece; Schneiderowa 1968, in Poland; Strojny and
Czaplicka 1975, in Poland; Pulkkinen and Yang 1984, in Finland; Tsankov and
Georgiev 1991, in Bulgaria; Georgiev 2001, in Bulgaria; Smith et al. in press, in
Europe), but only Pulkkinen and Yang (1984) provide details on the biology of
parasitoids and predators. Postner (1954) studied S. populnea in Germany and listed
many parasitoid species, but he did not mention which species were obtained from
his own rearing.
Natural enemies of the large poplar longhorn, S. carcharias, have been less
investigated. Among the few studies are Schneiderowa (1961, 1968) in Poland and
Srot (1983) in Czechoslovakia. These studies tend to show that there is a large
overlap between the natural enemy complexes of the two species.
Eggs and 1stt instar larvae of S. populnea and S. carcharias are attacked by the
eulophids Euderus albitarsis (Zetterstedt.) and E. caudatus Thomson. Mature larvae
of E. albitarsis have been recovered by Pulkkinen and Yang (1984) in egg-chambers
of S. populnea where they overwinter, but also in the mine of a first instar larva,
suggesting that it may also attack young instars. Smith et al. (in press) also reared E.
albitarsis from 1stt instars in Finland. It is a polyphagous parasitoid, also recorded
from Scolytidae, Lepidoptera and other insects (Noyes 2001). E. caudatus is known
only from eggs of S. populnea and S. carcharias, and is particularly abundant on the
latter. Schneiderowa (1961) observed up to 17% egg parasitism in Poland and Srot
(1983) an average parasitism of 6.5% in the Czechoslovakia. In Italy, a programme
was developed to screen insecticides, used against 1stt instar larvae of S. carcharias,
for their harmfulness on E. caudatus (Arru, 1972).
The tachinid fly Billaea irrorata (Meigen) was found to be the main larval
parasitoid of S. populnea, from northern to southern Europe (e.g. Postner 1954;
Brammanis 1963; Strojny and Czaplickaa 1975; Pulkkinen and Yang 1984; Tsankov
and Georgiev 1991; Georgiev 2001). B. irrorata is an endoparasitoid killing its host
in the prepupal stage. Larvae, emerging from the dead host larvae in the host pupal
chamber prepare a way out for the adult before pupating (Pulkkinen and Yang
1984). Parasitism by B. irrorata was about 4% in Finland (Pulkkinen and Yang
1984) and 9-19% in Bulgaria (Tsankov and Georgiev 1991). Interestingly, B.
irrorata has never been recorded from S. carcharias, suggesting that it is rather
specific. In their monograph on European tachinids, Tschorsnig and Herting (1994)
cite only the cerambycids Oberea spp. as other hosts.
Other important larval parasitoids of S. populnea include the braconids Iphiaulax
spp., and the ichneumonids Dolichomitus spp. Species of these two genera are
idiobiont ectoparasitoids, i.e. they oviposit through the bark on previously paralysed
host larvae. Iphiaulax spp. parasitise mid-instar larvae in the first year, whereas
Dolichomitus spp. seem to attack later instars in the second year (Pulkkinen and
Yang 1984; Georgiev 2001; Smith et al. in press). Iphiaulax impostorr was recorded
from many regions in Europe, from Greece (Kailidis 1964) and Bulgaria (Tsankov
and Georgiev 1991; Georgiev 2001) to Sweden (Brammanis 1963), with parasitism
rates below 3%. However, another, unidentified Iphiaulax sp. has been reared in
Finland, with a parasitism rate of 1% (Pulkkinen and Yang 1984), and Postner
(1954) mentions I. multiarticulatus (Ratzeburg). Many Dolichomitus spp. have been
cited as parasitoids of S. populnea (Table 2), but the two most regular and reliable
records are D. populneus (Ratzeburg) and D. messorr (Gravenhorst). In particular, D.
populneus has been reared from most studies, but parasitism was usually low (e.g.
2.3% in Finland (Pulkkinen and Yang 1984), 0.5-1.7% in Bulgaria (Tsankov and
Georgiev 1991)), except in Germany where Funke (1957, in Pulkkinen and Yang
1984) observed up to 70% parasitism by D. populneus or closely-related species.
Larvae of S. carcharias are also parasitised by D. populneus and D. messor, but not
by Iphiaulax spp. In a study in Czechoslovakia, the main larval parasitoid of S.
carcharias was the ichneumonid Ischnoceros rusticus (Geoffroy), but larval
parasitism remained low (about 5.5%) (Srot 1983). Records of all other parasitoids
of Saperda spp. listed in Table 2 have to be viewed with caution.
Among predators, the most investigated species is the Dipteran odiniid Odinia
xanthocera Collin, a major mortality factor in Finland (Pulkkinen and Yang 1984;
Yang, 1984). Eggs are laid at the entrance of the host tunnel. Hatching larvae enter
the tunnel and feed first on larval frass of S. populnea, whereas older larvae feed on
the cerambycid pupae. It also preys on the weevil Cryptorhynchus lapathii (L) in the
same host tree. In Finland, O. xanthocera killed about 10.5% of the S. populnea
population. Other insect predators mentioned in the literature include Staphilinidae
(Coleoptera), Pentatomidae and Reduviidae (Heteroptera), Asilidae and
Chloropidae, (Herting 1973; Smith et al. in press) but, in most cases, these insects
have been found in the beetle galleries and their predatory behaviour has not been
verified.
Woodpeckers (e.g. Dendrocopos majorr or D. minor) have been often observed
feeding on S. populnea and S. carcharias. (e.g. Brammanis 1963; Strojny and
Czaplicka 1975; Srot 1983; Pulkkinen and Yang 1984; Tsankov and Georgiev
1991). The level of predation varies from 9-10% in Finland and Czechoslovakia
(Pulkkinen and Yang 1984; Srot 1983) to 54-71% in Bulgaria (Tsankov and
Georgiev 1991). However, Pulkkinen and Yang (1984) rightly point out that the
foraging behaviour of woodpeckers further weakens the main shoots attacked by S.
populnea, causing them to break.
Diseases have been only occasionally mentioned as natural enemies of Saperda
spp. Srot (1983) observed that about 13% of the larvae of S. carcharias in
Czechoslovakia were killed by Pseudomonas septica. In Greece, up to 3% of S.
populnea larvae died from a fungal disease (Tsankov and Georgiev 1991).
In general, mortality rates attributed to natural enemies of Saperda spp. do not
exceed 20-30%. Other mortality factors are sometimes considered more important.
For example, in Czechoslovakia, healing responses of the host tree to the oviposition
wounds killed 56% of the eggs and 61% of the newly hatched larvae (Srot 1983).
However, the additional mortality caused by natural enemies should not be
neglected. Further studies are needed to better assess the proper impact of natural
enemies in the population dynamics of Saperda spp.
2.2.2. Lamia textor

Natural enemies of this poplar-feeding beetle have never been the target of any
particular study. The only records in the literature are the ichneumonid Dolichomitus
messorr (Herting 1973; Aubert 1969) and the tachinid fly Billaea adelpha (Loew)
(Tschorsnig and Herting 1994) (Table 2). Nothing is known of their impact and
biology.
2.2.3. Cerambyx cerdo and C. velutinus

To our knowledge, there is no information available in the literature on the natural
enemies of C. velutinus, a minor pest of oak in southern Europe. C. cerdo is a rare
and protected species in most of Europe. However, it attacks living trees and it is
considered a pest in some regions, such as Romania and North Africa. The most
often cited parasitoid of C. cerdo is the encyrtid egg parasitoid Oobius rudnevi
(Novicki) (Noyes 2001). Other parasitoids include the ichneumonids Dolichomitus
imperatorr (Slama 1998) and D. tuberculatus (Herting 1973). In his review, Hellrigl
(1974) lists several other parasitoids, most of which are doubtful records.
2.3. Exotic species
2.3.1. Phoracantha semipunctata

The eucalyptus borer, P. semipunctata is an Australian species feeding on trunks of
Eucalyptus spp. It was introduced in most parts of the world in which eucalypts have
been planted, e.g. southern Africa, North Africa, North America, and southern
Europe. In its region of origin, P. semipunctata is attacked by a large range of
natural enemies, especially parasitoids (Austin et al. 1994). In Europe and North
Africa, few natural enemies were observed. Avetianella longoii Siscaro (Hym.:
Encyrtidae), an Australian egg parasitoid was found in Portugal, Italy and Spain
(Siscaro 1992; Mansilla-Vazquez et al. 1999). A. longoi was introduced as a
biological control agent in California (Hanks et al., 1996) and South Africa (G.
Tribe, personal communication). Another egg parasitoid, Platystasius transversus
Thomson (Hym.: Platygastridae) was reared from P. semipunctata in Morocco
(Fraval and Haddan 1988). Ants are consideredd as important natural enemies both in
Morocco (Haddan et al. 1988) and Portugal (Way et al. 1992). A biological control
programme against P. semipunctata is presently carried out in California using
parasitoids from Australia (Millar et al. 2002).
2.3.2. Anoplophora spp.
Two Asian species of Anoplophora, both attacking a large range of broadleaved
trees, have been recently introduced accidentally into Europe. A. chinensis (= A.
malasiaca Thomson) was found recently in Italy, and is considered to be established
(Colombo and Limonta 2001). A. glabripennis was observed attacking trees in
Austria (Krehan 2002) and France (F. Lieutier, pers. comm.) and is presently the
target of eradication programmes, but its establishment in Europe has not been
confirmed. Both species have also been recently introduced in the USA. Until
recently, very little was known on the natural enemies of these two pests in their
region of origin. However, following the recent introduction of A. glabripennis to
North America, a biological control programme is being developed, and natural

enemies are presently being evaluated in Asia, as well as in Europe on other
cerambycids (Smith et al., 2002). In China, the entomopathogenic nematodes
Table 2. Parasitoids of European Cerambycidae living in fresh broadleaf trees. XX = mentioned as

reared from the host in a study specifically focused on the host or parasitoid; (XX) = As XX, but
parasitoid identification appears doubtful to the authors; X = Recorded in a catalogue, host-parasitoid
list, taxonomic publication or from a non-specific study ; (X) As X, but parasitoid identification or host-
association appear doubtful to the authors. The mostt doubtful host-parasitoid associations, including all
associations with Saperda populnea originating from Scheidter (1917) were not included in the table.
Cerambyx cerdo
Lamia textor
carcharias
populnea
Saperda
Saperda
Main host trees Quercus Populus Populus Populus
Main references1 1,5,6,7 1,6,18 1,3,6,7 1,2,3,4,6,7
12 10,11 8,9,11,13
13,14 15,16,17,18
Ichneumonidae
Absyrtus vicinator (Thunberg) (= luteus Holmgren)n (X)
Apechthis capulifera (Kriechbaumer) (X)
Coelichneumon impressor (Zetterstedt) (X)
Deuteroxorides elevatorr (Panzer) X
(= albitarsus (Gravenhorst))
Dolichomitus agnocendus (Roman) X
D. cognator (Thunberg) X
D. imperator (Kriechbaumer) X X X
D. mesocentrus (Gravenhorst) X
D. messor (Gravenhorst) X X XX
D. populneus (Ratzeburg) X XX
D. terebrans (Ratzeburg) X
D. tuberculatus (Geoffroy) X X
Echthrus reluctatorr (L.) (X)
Ephialtes manifestatorr (L.) X X
Ischnoceros caligatus (Gravenhorst) X
(= seticornis (Kriechbaumer)
I. rusticus (Geoffroy) (= filicornis (Kriechb.)) XX
Liotryphon crassisetus (Thomson) (X)
L. punctulatus (Ratzeburg) (X)
Mastrus rufobasalis (Habermehl) (hyperpar.?) (X)
Medophron afflictor (Gravenhorst) (hyperpar.?) (X)
Megarhyssa perlata (Christ) (X)
(=clavata (F.) = gigas (Laxmann))
M. superba (Schrank)
( (X)
Neoxorides nitens (Gravenhorst) X
Orthocentrus fulvipes Gravenhost (X)
Podoschistus scutellaris (Desvignes) X
(=wahlbergi (Holmgren))
Rhimphoctona grandis (Fonscolombe) X
(= Pyracmon fulvipes (Holmgren))
Rhyssa amoena Gravenhorst (X)
R. persuasoria (L.) (X)
Table 2. (cont.)
Lamia textor
carcharias
Cerambyx
populnea
Saperda
Saperda
cerdo
Stenomacrus pusillatorr Aubert (X)
(= pusillus (Holmgren))
Townesia tenuiventris (Holmgren) (X)
Virgichneumon monostagon (Gravenhorst) (X)
Xylophrurus augustus (Dalman) (X)
X. lanciferr (Gravenhorst) (= disparr Thunberg) (X)
Braconidae
Atanycolus denigratorr (L.) X
A. neesii (Marschall) X
Bracon discoideus (Wesmael) X
Iphiaulax impostorr (Scopoli) XX
I. multiarticulatus (Ratzeburg) X
Iphiaulax sp. XX
Ontsira longicaudis (Giraud) X
Encyrtidae
Oobius rudnevi (Novicky) XX
Eulophidae
Euderus albitarsis (Zetterstedt) XX
E. caudatus Thomson XX X
Tachinidae
Billaea adelpha (Loew) X
B. irrorata (Meigen) XX
Pales pumicata (Meigen) (X)
Triarthria setipennis (Fallèn) X
Calliphoridae
Rhinophora lepida Meigen (X)
1
1: Aubert (1969); 2: Brammanis (1963); 3: Delplanque (1998); 4: Georgiev (2001); 5: Hellrigl (1974);
6: Herting (1973); 7: Noyes (2001); 8: Postner (1954); 9: Pulkkinen and Yang (1984); 10: Schnaiderowa
(1961); 11: Schnaiderova (1968); 12: Slama (1998); 13: Smith et al. (2003); 14: Srot (1983); 15: Strojny
and Czaplicka (1975); 16: Tobias (1986); 17: Tsankov and Georgiev (1991); 18: Tschorsnig and Herting
(1994)
Steinernema spp. and Heterorhabditis spp. have been tested against A. glabripennis,
with some success (e.g. Liu et al. 1992). Interestingly, an egg parasitoid,
Aprostocetus sp. (Hym.: Eulophidae) has been found associated with A. chinensis in
Italy, and is presently investigated for its biological control potential against
Anoplophora spp. in North America (Smith et al. in press).
3. BUPRESTIDAE
3.1. Conifer feeding species
3.1.1. Phaenops cyanea

Parasitoid records for this important pest of pine trunks are rather numerous (Table
3), but only few of them are reliable. The ichneumonid Xorides depressus
(Holmgren) is often cited as parasitoid of P. cyanea (Aubert 1969; Hilszczanski

2002). It was found associated with mature larvae of P. cyanea and Nothorhina
punctata (F.) (Col.: Cerambycidae) inhabiting Scots pine bark (Hilszczanski 2002).
Adults are found on pine trunks infested by P. cyanea in September-October
(Hilszczanski, unpublished). Filipenkova (1971) mentions three braconid parasitoids
in Russia, Coeloides sordidatorr (Ratzeburg) (as C. melanostigma Strand), usually
associated with weevils of the genus Pissodes (Kenis 1997), Doryctes mutillatorr and
Atanycolus genalis (as A. initiator, see Tobias, 1986), the latter two being
responsible for up to 80-90% parasitism in Russia, in a pine stand that had recently
burned. All other records must be considered with great caution. Some of them are
obvious errors, such as the ichneumonid Poemenia notata, a well-known parasitoid
of sphecids (Hym. Sphecidae) nesting in empty beetle galleries, or the braconid
Ascogaster varipes Wesmael, which belongs to a genus exclusively associated with
Lepidoptera.
Predators have been reported in Russia by Kolomiec and Bogdanova (1980),
who observed Thanasimus formicarius, T. rufipes Brahm. (Col.: Cleridae),
Xylophagus cinctus (De Geer) (Dipt.: Xylophagidae), Zabrachia minutissima
(Zetterstedt) (Dipt.: Stratiomyidae) and Lonchaea collini Hackman (Dipt.:
Lonchaeidae) on larvae and Laphria gilva (L.). (Dipt. Asilidae) on adults.
3.2. Broadleaf feeding species
3.2.1. Coraebus undatus and C. florentinus

Nothing is known of the natural enemies of C. undatus, whereas knowledge on
natural enemies of C. florentinus is limited to a single study carried out in Italy by
Solinas (1974) who investigated mortality factors at different developmental stages.
About 25% of eggs were eaten by unknown predators and about 10% destroyed by
an unidentified egg parasitoid. Second aand third instar larvae were frequently
parasitised by the braconid Spathius radjabii Fisher, which has one generation per
year and overwinters in a cocoon in the host gallery. Fourth and fifth instar larvae
were parasitised at lower intensities by two braconids, an unidentified species of the
subfamily Braconinae, and a species tentatively determined as Bracon maculiger
Wesmael (= variatorr Nees). Finally, last instar larvae were attacked by a large
ichneumonid wasp, cited by Solinas (1974) as Cryptus maculipennis Dufour, but
this name was not found in the most recent ichneumonid nomenclature. It attacks
mature instars in early spring in pupal cells and builds a cocoon in which it
overwinters. Up to 50% of the C. florentinus larvae were parasitised by this
ichneumonid, which was considered by Solinas (1974) to be one of the factors
causing the collapse of host populations. He mentioned that C. maculipennis has
also been recorded as a parasitoid of C. florentinus in France by De La Perraudière
(1902, in Solinas 1974). Solinas also mentions woodpeckers and the wasp Cerceris
bupresticida Dufour (Hym.: Sphecidae) as predators of larvae and adults,
respectively, as well as fungi, bacteria aand viruses on larvae, but he does not provide
any further details.
Other parasitoids recorded as parasitoids of C. florentinus in the literature are the

ichneumonid wasp Rhimphoctona megacephalus (Gravenhorst), the braconid
Polystenus rugosus Foester (as Eucorystes aciculatus (Reinhard)) (Herting 1973)
and the eupelmid Eusandalum ibericum (Bolivar & Pieltrain) (Thompson, 1943).
Table 3. Parasitoids of European Buprestidae living in fresh wood. XX = mentioned as reared from the
host in a study specifically focused on the host or parasitoid; (XX) = As XX, butt parasitoid identification
appear doubtful to the authors; X = Record in a catalogue, taxonomic book, host-parasitoid list or from
a non-specific study ; (X) As X, but parasitoid identification or host-association appear doubtful to the
authors.
Melanophila
angustulus
florentinus
populneus
biguttatus
Phaenops
Coraebus
Agrilus .
Agrilus
Agrilus
Agrilus
cyanea
viridis
picta
Main host trees2 Q Q Po BL Q, C Po, S Pi
Main references1 9,11 5,7,91 7,12 1,4,7,8 2,7,12 3,5,7 5,6,7
12 1,12 15 9,10 17 9,12 9,11
18,19 11,12 16 12,21
20,22 13,14 22
21,23
Ichneumonidae
Atractogaster semisculptus Kriechbaumer X
Bathyplectes sp. (X)
Cryptus maculipennis (Dufour)3 XX
Deuteroxorides elevator (Panzer) XX
(= albitarsus (Gravenhorst))
Dolichomitus imperatorr (Kriechbaumer) (X) X
Dolichomitus sp. XX
Foersteria puber (Haliday) (X)
(= flavipes Szépligeti)
Isadelphus gallicola (Bridgman) X
(=Cecidonomus nigriventris (Thomson))
Poemenia notata Holmgren (X)
Rhimphoctona megacephala (Gravenhorst) X
R. pectoralis Kriechbaumer (X)
Xorides depressus (Holmgren) XX
X. irrigator F. (X)
X. praecatorius (F.) XX
Xylophrurus augustus (Dalman) (X)
(=dentatus Taschenberg)
Braconidae
Ascogaster varipes Wesmael (X)
Atanycolus genalis (Thomson) XX
(=initiatorr F.)
A. ivanowi (Kokujev) X
A. neesii (Marshall) X XX X
A. sculpturatus (Thomson) (X)
Bracon variator Nees (XX)
(=maculigerr Wesmael)
Coeloides abdominalis (Zetterstedt) X
C. scolyticida Wesmael X
C. sordidatorr (Ratzeburg) XX
(= melanostigma Strand)
Dimeris (=Pambolus) mira (Ruthe) (X)
Table 3. (cont.)
Melanophila
angustulus
florentinus
populneus
biguttatus
Phaenops
Coraebus
Agrilus .
Agrilus
Agrilus
Agrilus
cyanea
viridis
picta
Doryctes leucogasterr (Nees) (X)
D. mutillatorr (Thunberg) (X) X
D. undulatus (Ratzeburg) (X) (X)
(= brachyurus Marschall)
Helcon claviventris Wesmael (XX)
Iphiaulax impostorr (Scopoli) XX
Microgaster globata (L.) (X)
Ontsira antica (Wollaston) X
O. longicaudis (Giraud)
Pareucorystes varinervis Tobias X
Polystenus rugosus Förster XX X
(= Eucorystes aciculatus (Reinhard)
Spathius brevicaudis Ratzeburg XX
S. curvicaudis Ratzeburg XX (XX)
S. depressus Hedqvist X
S. lignarius (Ratzeburg) X (X)
S. melanophilae Fisher X
S. phymatodis Fisher X
S. polonicus Niezabitowski X
S. radjabii Fisher XX
S. radzayanus Ratzeburg X (XX)
S. rubidus (Rossi) X X
Undetermined Braconinae XX
Eulophidae
Baryscapus agrilorum (Ratzeburg) X XX XX
B. hylesini Graham X
Entedon ergias Walker X
Euderus agrili Boucek XX X
Quadrastichus misellus (Delucchi) XX
Tetrastichus heeringi Delucchi XX
T. murcia (Walker) X
(= trichops Thomson)
Eupelmidae
Calosota vernalis Curtis (XX)
C. aestivalis Curtis X
Eusandalum elongatum (Ruschka) (X)
E. ibericum Bolivar & Pieltrain X
E. walkeri (Curtis) X
Pteromalidae
Aggelma agrili Boucek X
Aggelma spiracularis (Thomson) (X)
Agrilocida ferrierei Steffan X
Apelioma pteromalinum (Thomson) (X)
Heydenia pretiosa Förster (X)
Oodera formosa (Giraud) XX X
Rhopalicus guttatus (Ratzeburg) (X)
Trichomalus sp. X
Table 3. (cont.)
Melanophila
angustulus
florentinus
populneus
biguttatus
Phaenops
Coraebus
Agrilus .
Agrilus
Agrilus
Agrilus
cyanea
viridis
picta
Trigonoderus cyanescens Förster (X)
Encyrtidae
Oobius zahaikevitshi Trjapitzin X
Chalcididae
Cratocentrus fastuosus Masi X
Tachinidae
Freraea gagatea Robineau-Desvoidy XX
(= Gymnophania nigripennis B. & B.)
1
References: 1: Schimitschek (1935); 2: Thompson (1943); 3:Fisher (1966); 4 Schimitschek (1967); 5:
Aubert (1968); 6: Filippenkova (1971); 7: Herting (1973); 8: Kolomiec and Bogdanova; 9: Tobias, 1986;
10: Tschorsnig and Herting (1994); 11: Hedqvist (1998): 12: Noyes (2001); 13 Kamp (1952); 14:
Heering (1957); 15: Arru (1962); 16 : Kailidis (1968); 17 : Solinas (1974); 18: Shaw (1988); 19: Moraal
and Hilszczanski (2000); 20: Moraal and van Achterberg (2001); 21: Hilszczanski (2002); 22:
Hilszczanski (unpublished); 23 : Schimitschek (1964).
2
Q = Quercus; Po = Populus; BL = Broadleaves; C = Castaneus; S = Salix; Pi = Pinus
3
Probably Chirotica maculipennis (Gravenhorst)
R. megacephala is a parasitoid usually associated with Cerambycidae in conifer

trunks, and E. aciculatus is a well-known parasitoid of Agrilus viridis (see below).
3.2.2. Melanophila picta

Data on natural enemies of M. picta are restricted to a few parasitoid records (Table
3). In Greece, Kailidis (1968) reared three larval parasitoids, the ichneumonid
Dolichomitus sp. and the braconids Iphiaulax impostorr and Spathius curvicaudis
Ratzeburg, with parasitism rates of 12, 13 and 25% respectively at one sample site,
and no parasitism at a second site. But no details on their biology were provided.
Another reliable record is the braconid Spathius melanophilae Fisher, which was
first described from specimens emerged from M. picta in Spain (Fisher 1966). Other
records include the ichneumonid Atractogaster semisculptus Kriechbaumer (Aubert
1969), which is probably a hyperparasitoid, the braconid Atanycolus ivanowi
(Kokujev) in Russia (Tobias 1986), and the Chalcididae Cratocentrus fastuosus
Masi, in Morocco (Herting 1973). The only mention of predators is in Kailidis
(1968) who observed the green woodpecker Picus viridis feeding on larvae.
3.2.3. Agrilus angustulus

A. angustulus is the least studied species of the four Agrilus spp. treated in this
review. However, it should be noted thatt misidentifications are frequent in Agrilus
spp. in Europe, especially at the larval stage, and many records of A. viridis and A.
biguttatus, the two most common species, may actually refer to other species.
Only three parasitoid records were found for A. angustulus (Table 3), without
any information on biology or abundance. The braconid Spathius rubidus (Rossi)
(Tobias 1986; Hedqvist 1998) is a polyphagous species attacking mainly Anobiidae

and Buprestidae larvae (Hedqvist 1998), sometimes also recorded from
Curculionidae (Kenis and Mills 1994). The pteromalid Agrilocida ferriereii Steffan
was described from one male emerged from a log containing A. angustulus. Since
then, it has been reared from Scolytus multistriatus Marsham (Col.: Scolytidae) in
Israël (Mendel 1986) and from Anthaxia sp. (Col.: Buprestidae) in Turkey (J.
Hilszczanski, unpublished). Finally, the Eupelmid Eusandalum walkeri (Curtis) is
known only from A. angustulus (Noyes 2001).
3.2.4. Agrilus biguttatus

The most frequently cited natural enemy of A. biguttatus is the braconid larval
parasitoid Spathius curvicaudis (e.g. Shaw 1988; Hedqvist 1998; Moraal and
Hilszczanski 2000; Moraal and van Achterberg 2001). S. curvicaudis is a gregarious
parasitoid of mature larvae, with up to 14 cocoons developing on a host larva (Shaw
1988). Moraal and van Achterberg (2001) found a parasitised host larva in the
overwintering cavity in the bark in the summer, whereas healthy larvae usually
reach the bark only in autumn. They speculate that S. curvicaudis induces the larva
to bore through the bark earlier, to allow easier emergence of the adult parasitoid.
Another reliable parasitoid record for A. biguttatus is Deuteroxorides elevator
(Panzer) which has been reared from a larval gallery of A. biguttatus (J.
Hilszczanski, unpublished), and is a parasitoid associated mainly with wood-boring
beetles infesting oak logs. Other records listed in Table 3 are less reliable. However,
some of them are also recorded from other Agrilus spp. and could equally attack A.
biguttatus. Spathius rubidus is also mentioned as a parasitoid of A. angustulus.
Another braconid, Atanycolus neesi is a well-known parasitoid of A. viridis, and the
eulophid Baryscapus agrilorum (Ratzeburg) is also known from A. populneus.
Predators of A. biguttatus have never been studied in detail. Moraal and
Hilszczanski (2000) mention woodpeckers and Herting (1973) lists the clerid beetle
Thanasimus formicarius.
3.2.5. Agrilus populneus

A single study (Arru 1962) on A. populneus includes data on natural enemies. He
mentions four parasitoids of A. populneus in Italy. The braconid Spathius polonicus
Niezabitowski, for which no other host in known, the pteromalid Oodera formosa
(Giraud), and the two eulophids Euderus agrili Boucek and Baryscapus agrilorum,
three species known from other Agrilus spp. (Noyes 2001). B. agrilorum, a
gregarious species with up to 16 individuals per brood, was by far the most abundant
species. It had one generation per year and was well synchronized with its host. Arru
(1962) considered that parasitism was not an important mortality factor, but he did
not provide any level of parasitism. In addition, Noyes (2001) lists another eulophid,
Baryscapus hylesini Graham, as a parasitoid of A. populneus, and Arru (1962)
mentions woodpeckers as predators on larvae and pupae.
3.2.6. Agrilus viridis

This species is by far the most studied buprestid in Europe. Several studies have
focused on its life history, of which a few included investigations on its natural
enemy complex. Consequently, a substantial number of parasitoid records have been
found in the literature (Table 3). However, it is possible that some of these records
refer to other Agrilus spp. because identifying Agrilus spp. is difficult and forest
entomologists tend to use the name A. viridis when the identity is uncertain.
The two most complete studies on mortality factors in A. viridis populations have
been carried out in Germany by Kamp (1952) and Heering (1957). Most details are
provided for parasitoids, but predators are also mentioned. Kamp (1952) mentions
substantial rates of larval parasitism (from 11 to 67%) whereas Heering (1957)
observed lower rates (6.5% on average, but variations from 0 to 95% from site to
site). In Heering (1957), about 95% of all parasitoids reared from A. viridis belonged
to three eulophid species, Tetrastichus heeringi Delucchi (50%), Baryscapus (as
Tetrastichus) agrilorum (35%) and Quadrastichus (as Tetrastichus) misellus
(Delucchi) (10%). Kamp (1952) found B. agrilorum and a Tetrastichus sp., which
could be T. heeringi. These eulophid wasps are gregarious ectoparasitoids of larvae
in galleries, with up to 28 specimens per host larva (average 3 to 5), but Kamp
(1952) also observed egg parasitism by Tetrastichus sp. Egg parasitism was about 3
to 4%. Other larval parasitoids reared from A. viridis in Germany include the
braconids Atanycolus neesi, Polystenus rugosus (as Eucorystes aciculatus), Spathius
brevicaudis Ratzeburg, S. radzayanus Ratzeburg (identity doubtful) and the
ichneumonid Xorides praecatorius, also reared by J. Hilszczanski (2002) in Poland.
Doryctes undulatus (Ratzeburg) has been reported as parasitoid of A. viridis in
Russia (Kolomiec and Bogdanova 1980). Kamp (1952) and Heering (1957) also
reared the eupelmid Calosota vernalis Curtis (likely a misidentification for C.
aestivalis Curtis), probably a hyperparasitoid through braconid cocoons. In addition,
Kamp (1952) reared the tachinid fly Freraea gagatea Robineau-Desvoidy (as
Gymnophania nigripennis B. B.) in larval galleries of A. viridis. F. gagatea is
known as a parasitoid of carabid beetles (Tschorsnig and Herting 1994). The other
parasitoid records listed in Table 3 are less reliable, or undoubtedly wrong, such as
Microgaster globatus (L.), a parasitoid belonging to the braconid sub-family
Microgastrinae, which only includes parasitoids associated with Lepidoptera.
Kamp (1952) and Heering (1957) also mention observations of predators. Kamps
(1952) cites birds (woodpeckers and nuthatch), Lonchaea chorea (F.) (Dipt.:
Lonchaeidae), and Lasius nigerr (L.) (Hym.: Formicidae) feeding on larvae and
prepupae. He also found in larval galleries the clerid beetle Thanasimus formicarius
and Rhaphidia sp. (Neur.: Rhaphididae). Heering (1957) observed woodpeckers
feeding on larvae, and tits and nuthatches picking eggs. He also suggested slugs as
egg predators. Among insects, Asilidae (Diptera) were observed preying on adults.
Eggs were eaten by the ant L. nigerr and, to a lesser extend, by the clerid T.
formicarius and Tomoxia biguttata Gyllenhal (Col.: Mordellidae).
4. CONCLUSIONS AND FUTURE RESEARCH

The knowledge of natural enemies of cerambycid and buprestid pests in Europe
varies with species and regions. Some species such as Saperda spp., Tetropium spp.
and Agrilus viridis have been relatively well covered whereas most other species
have been very poorly studied. This discrepancy is only partly explained by the
relative importance of the pest species in forestry. Traditionally, applied forest
entomology was more developed in central and northern Europe than in southern
Europe, and it is not surprising that very little is known of natural enemies of species
occurring more typically in southern Europe, such as Cerambyx velutinus,
Monochamus galloprovincialis, Coraebus spp., etc. Until recently, these pests were
considered of minor importance in forestry. However, the importance of M.
galloprovincialis is likely to increase because it is considered to be the main vector
of the newly introduced pine wood nematode in Portugal, and new control methods
will have to be developed, including those involving natural enemies.
Even the most complete studies on natural enemies of cerambycid and buprestid
beetles in Europe are usually restricted to the description of larval parasitism. Egg
and adult parasitism, as well as predators and pathogens, have been largely
neglected. Obviously, forest management would benefit from a better knowledge of
natural enemies. Firstly, a quantification of the impact of natural enemies is
desirable, e.g. though life tables and population dynamics studies, to understand the
absolute and relative importance of natural enemies, as well as their variation in time
and space. Then, a better knowledge of the influence of environmental factors on
natural enemies and parasitism should allow the development of cultural practices
that would enhance their impacts. These studies should be made at ecosystem level
rather than at pest level. For example, cerambycids and buprestids attacking living
or freshly cut trees share part of their natural enemy complexes with other
xylophagous beetles living in dead wood. Thus, it is likely that management
methods related to logging waste and dead wood removal will have an influence on
the population dynamics of the target pests.
Wood-boring beetles are particularly prone to introduction and establishment
into new regions, as shown by the recent introductions of Anoplophora spp. and
Phoracantha semipunctata in various parts of the world, of T. fuscum in Canada
(Smith and Hurley 2000), and of the emerald ash borer, Agrilus planipennis
Fairmaire, an Asian species, in the USA (McCullough and Roberts 2002). These
examples also show that, in their new environment, insects often become more
damaging than in their region of origin. Beetles enter new countries in logs, nursery
stock and, especially, solid wood packing material, such as pallets, crating or
packing blocks. Considering the continuous increase in world trade, Europe will
probably face new introductions in the near future, and, at the same time, European
beetles will become invasive elsewhere. Therefore, improved international
collaboration is desirable, firstly to develop quarantine and containment methods
and, secondly, to build up collaborative research programmes on sustainable control
methods, including a better knowledge of natural enemies, for biological control
purposes.
5. ACKNOWLEDGEMENTS
We thank Hugh Evans for his comments on the manuscript and Franck Hérard for
literature on Saperda spp. M. Kenis was supported by the Swiss Federal Office for
Education and Science (project C99.0116).
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Part 4
“Non-Coleopteran”
BAWBILT organisms
Chapter 22
“NON-COLEOPTERAN INSECTS”
B. LÅNGSTRÖM 1, K. HELIÖVAARA 2, L.G. MORAAL 3, M.

TURýÁNI 4, M. VIITASAARI 2 & T. YLIOJA 5
1
The Swedish University of Agricultural Science, P.O. Box 7044, S-750 07 Uppsala,
Sweden
2
Department of Applied Biology, P.O. Box 27, FIN-00014 University of Helsinki,
Finland
3
ALTERRA, Wageningen University and Research Centre, PO Box 47, NL-6700 AA
Wageningen, The Netherlands
4
Forest Research Institute Zvolen, Research Station Banská Štiavnica, Slovak
Republik
5
Finnish Forest Research Institute, Vantaa Research Centre, P.O. Box 18, FIN-
01301 Vantaa, Finland
1. INTRODUCTION
B. Långström
By definition the BAWBILT concept includes all insect species that attack and
damage the main stem of living trees. Apart from beetles, which are dealt with in
parts 1-3, there is a number of xylophagous species in other insect orders that are
part of the BAWBILT community. Some of these are listed in the damage & control
database, but as a result of their unclear or variable pest status, reporting to the
database is inconsistent and incomplete (table 1). There are also some species related
to the listed ones that could and perhaps should have been included, but since no
country has done so they are not there.
Despite the few records in the database, it is easy to conclude that these ”non-
coleopteran pests” are of much less importance in Europe than e.g. bark beetles and
pine weevils. Hence, these species do nott deserve the same attention as the
economically important ones, but totally ignoring them would result in an
incomplete BAWBILT synthesis. Furthermore, a few of these species have become
major pests in other parts of the world after accidental introduction to new
501
501–538.
© 2007 Springer.
502 LÅNGSTRÖM et al.
continents. Thus, a selected number of representatives of these very different pest

categories are treated
d in this chapter.
Table 1. Aggresiveness and extention of non-coleopteran" BAWBILT pests according to the
reported information in the damage & control database
Coun- Rhy Dio Cos Zeu Par Ses Syn Sir Sir Uro Ara Phy
try buo spl cos pyr tab api myo cya juv gig cin bet
Bel */* */* */* */* */* */*
Est **/* */* */* */*
**/*
Fin
*
*/* */*
Fra
** **
***/* **/ **/* **/
Hun **/*
** ** ** **
***/*
Ire */* */*
**
*/* ***/* ***/
Ita */* */** */** **/*
* ** **
Lit */*
Por */* */* */* */* */*
*** ***/ **/ ***/ ***/*
Rom ***/* ***/*
/* * * ** *
Slov */** */* */*
Spa */* */* */** */*
**/** **/**
Net */* */* */***
* *
UK */* */* */* */* */* */* */*
* , ** or *** = low, medium orr high aggressiveness/extention
Bel = Belgium, Est = Estonia, Fin = Finland, Fra = France, Hun = Hungary, Ire = Ireland, Ita = Italy, Lith
= Lithuania, Por = Portugal, Rom = Romania, Slo = Slovakia, Spa = Spain, Net = The Netherlands, UK =
The United Kingdom
Rhy buo = Rhyacionia buoliana, Dio spl = Dioryctria splendidella, Cos cos = Cossus cossus, Zeu pyr =
Zeuzera pyrina, Par tab = Paranthrene tabaniformis, Ses api = Sesia apiformis, Syn myo = Synanthedon
myopaeformis, Sir cya = Sirex cyaneus, Sir juv = Sirex juvencus, Uro gig = Urocerus gigas, Ara cin =
Aradus cinnamomeus, Phy bet = Phytobia betulae
From an economic point of view, we are dealing with basically two kinds of
problems. Firstly, damage to the leader shoot(s) of growing young trees leads to
growth losses and later to reduced timber quality due to stem crooks and internal
defects. This kind of damage is mainly caused by larvae of microlepidoptera (see
below), but the damage caused by the pine bark bug ((Aradus cinnamomeus, see
below) also belongs to this category. There are also a few sawfly species (like
Nematus ericssoni on larch and different Pristiphora species on spruce and larch)
which normally feed on the foliage, but which also may cause this kind of damage,
but these are not included here as they were not listed in the database. Shoot damage
is also caused by some beetles (Tomicus sp, Saperda populnea etc), which are
treated elsewhere in this volume.
NON-COLEOPTERAN INSECTS 503
The second type of damage is technical damage to the lower stem of older trees
leading to degraded timber value due to feeding tunnels in the wood. Typical
examples here are goat moths and clearwings (see below), some longhorn beetles
(see part 3) and the very special case with the dipteran Phytobia betulae (see below).
The siricid wasps (horntails) form a special case of this group, as they are mainly
timber pests that occasionally attack living trees (see below). Wood-dwelling ants
like the genus Camponotus could also be included here, as well as termites in the
Mediterranean area, but as they were not listed in the database they are also omitted
here.
Among Hemiptera, we have a few species that can be considered BAWBILT
insects, and of these Aradus cinnamomeus is reported as a pest in the damage &
control database. Under certain circumstances the feeding damage of this species
may lead to reduced growth and eventually to tree death. Several aphids and scale
insects, like Matsucoccus feytaudi and Pineus pini on pine and Cryptococcus
fagisuga on beech may cause substantial tree mortality, but none of these was
included in the database, and they are hence omitted here.
Among Lepidoptera (moths) we have species belonging to different families
causing shoot or stem damage in living trees. The largest and probably most diverse
group of species is the one causing damage to terminal shoots and by so dying
eventually reducing the timber value by causing external or internal defects. Nearly
all conifer species are exposed to this kind of damage but problems of economic
importance are reported from pine only. The pine shoot moth ((Rhyacionia buoliana)
is probably the most well known and economically important of the tortricids
causing this kind of damage. The species has become established in North America
as well, and is known there as the European pine shoot moth. Among related species
causing shoot damage in pine that all used to be included in the genus Evetria, we
have Petrova resinella, and R. pinicolana. At least in Scandinavia, similar damage
can be done by pyralid moths like Dioryctria mutatella (and occasionally D.
abietella in years when spruce cones are scarce). Of these species, only R. buoliana
was listed in the damage & control database, and hence only this species is included
below. There is another Dioryctria species, namely D. sylvestrella, which deserves
attention in this context. This species is causing substantial stem damage to
Maritime pine in south-western France by causing stem cancers at the base of the
branches where the larva is developing. Similar damage is also done by the tortricid
Laspeyresia pactolana, and related species, but this damage is presumably of low
economic importance.
Among broad-leaved trees, shoot damage in poplars caused by clearwing moths
of the family Sesiidae is probably the most common and important pest case. In this
context, Paranthrene tabaniformis is the principal species although other clearwings
may cause similar damage in other hosts. Another clearwing species Sesia apiformis
causes damage to the lower stem of poplars by tunnelling and destroying the wood.
Even better known are the larvae of the goat moth Cossus cossus and the leopard
moth Zeuzera pyrina that commonly tunnel the wood of preferably senescent trees
of different broad-leaved species.
Among Hymenoptera, we have the horntails (Siricidae) with the following

species listed in the database: Urocerus gigas, Sirex cyaneus and Sirex juvencus. In
Europe, they are mainly timber pests (and hence not really BAWBILT species) but
they may also attack living trees via mechanical wounds. As the siricids convey
pathogenic fungi into the wood, they may cause tree mortality as well. For unknown
reasons the globally most important species, Sirex noctilio, is not listed in the
database. This has been a big problem on radiata pine in Australia and New Zealand
where it was accidentally introduced in the beginning of the last century.
Finally, among dipterans we have the peculiar damage caused by Phytobia
betulae in living birch trees that later shows up as spectacular brown stripes in the
veneer cut from birch logs. This is mainly a problem for the Finnish veneer industry.
In conclusion, the following species are selected as the most important
organisms representing “non-coleopteran” BAWBILT species:
Hemiptera: Aradus cinnamomeus

Lepidoptera: Rhyacionia buoliana, Dioryctria sylvestrella, Cossus cossus, Zeuzera
pyrina, Paranthrene tabaniformis, Sesia apiformis
Hymenoptera: Siricidae (Urocerus gigas, Sirex noctilio, Paururus juvencus)
Diptera: Phytobia betulae
2. ARADUS CINNAMOMEUS, THE PINE BARK BUG

K. Heliövaara
2.1 Taxonomy and systematics

The flat bugs of the family Aradidae (Heteroptera) constitute a well defined family
of the Aradoidea (Gyllensvärd 1964) and contain eight closely related subfamilies.
The only economically significant species belongs to the genus Aradus, whose
members are usually called the bark bugs. Adult pine bark bugs are 3.5-4.5 mm long
but only 0.75 mm thick. Adults are brown, but small nymphs are bright red. When
disturbed, pine bark bugs secrete a characteristic smell of pear.
2.2 General biology

Aradus cinnamomeus has a two-year life span in most parts of Europe; in northern
Europe close to the tree limit, the life span is three years (Brammanis 1975,
Heliövaara and Väisänen 1987). Eggs are laid in May, nymphs hatch in June, and
reach the fourth instar during the first summer. After hibernation at the base of the
tree or in surrounding litter (Brammanis 1975), the bugs become adult in July-
August, after which they hibernate. It is not until the following spring that the bugs
mate and begin egg-laying (Tropin 1949, Brammanis 1975).
The two-year life span of the pine bark bug has led to periodicity and a unique
biogeographical pattern of distribution. In most of Europe, there seem to be two
major alternate-year populations that live in different geographical areas (Heliövaara
and Väisänen 1987). For instance, the bugs reproduce in even-numbered years in
eastern Finland and eastern Sweden, and in odd-numbered years in western parts of
these countries.
2.3 Host finding

Aradus cinnamomeus displays exceptional wing polymorphism. Most females (ca.
97 %) are brachypterous. The proportion of macropterous females is usually 3%, but
it may increase as living conditions on the host tree worsen. Males are
”stenopterous”, i.e., their hemelytra reach almost the tip of the abdomen but are
greatly narrowed in their apical three-quarters. Only the few macropterous females
can fly. Migration takes place in August on warm, sunny days, just after the final
molt.
2.4 Natural enemies

Generally, 25 % of the laid eggs are parasitized by a scelionid wasp, Telenomus
aradi Kozlov (Heliövaara et al. 1982). Parasitoids of nymphs or adults are not
known. Other invertebrate predators include Raphidia (Neuroptera) larvae, a bdellid
mite Bdella longicornis (L.), and spiders such as Philodromus fuscomarginatus
Degeer, Clubiona subsultans Thorell, Drapetisca socialis (Sundevall), Micaria
subopaca Westring, Salticus cingulatus (Panzer) and Moebilia penicillata
(Westring). However, spiders only rarely seem to eat pine bark bugs (Hokkanen et
al. 1987).
2.5 Associated organisms

The fungal feeding of aradids has been confirmed repeatedly, with the possible
exception of the only economically important species, the pine bark bug Aradus
cinnamomeus Panzer. This species pushes its stylets into phloem, cambium and
xylem tissues of living pine saplings, disturbing their growth. However, it is possible
that even this species utilizes some fungi living on pine (Usinger and Matsuda
1959).
2.6 Damage and control

The pine bark bug is a pest of pines. In central and eastern Europe the pine bark bug
has long been regarded as a harmful pest of pines. It has caused serious damage,
especially in pine stands planted in nitrogen-poor sandy soils in the Ukraine,
Byelorussia, Latvia, and Poland (Tropin 1949).
Pine bark bugs live in crevices in the bark of the trunk. Both adults and nymphs
suck sap with their highly specialized piercing mouthparts from the young tissues
surrounding the cambium, thus disturbing the conduction of fluids in the tree.
Presence of the bugs in large numbers causes noticeable growth retardation,
yellowing of needles, and withering of the pine (Tropin 1949, Brammanis 1975).
Several chemical and biological methods including systemic insecticides and

fungal diseases have been used with variable results in the control of Aradus
cinnamomeus. The bug seems to be a tenacious species with a high resistance to
chemicals, and the results obtained with a wide range of chemicals have not been
encouraging. Forest fertilization has been tested as a control method against the pine
bark bug, but the results are contradictory. No real progress has yet been achieved in
the biological control of the pine bark bug.
Because no single effective method of controlling Aradus cinnamomeus is yet
available, the use of several prophylactic silvicultural practices probably gives the
most favorable results. As the bugs thrive best in warm and light conditions, high
stocking densities should be used in pine stands in potential damage areas. The
structure of a resistant pine stand should be even and dense without gaps, and heavy
early thinnings should be avoided (Brammanis 1975, Hokkanen et al. 1987).
2.7 References
Brammanis, L. 1975. Die Kiefernrindenwanze, Aradus cinnamomeus Panz. (Hemiptera-Heteroptera). Ein
Beitrag zur Kenntnis der Lebensweise und der forstlichen Bedeutung. Studia Forestalia Suecica 123:
1-81.
Gyllensvärd N. 1964. A key to Swedish Aradidae (Hem. Het.) with figures of the male genitalia.
Opuscula Entomologica. 29: 110-116.
Heliövaara, K., E. Terho, and M. Koponen 1982. Parasitism in the eggs of the pine bark-bug, Aradus
cinnamomeus (Heteroptera, Aradidae). Annales Entomologici Fennici. 48: 31-32.
Heliövaara, K. & Väisänen, R. 1987. Geographic variation in the life-history of Aradus cinnamomeus and
a breakdown mechanism of the reproductive isolation of allochronic bugs (Heteroptera, Aradidae).
Annales Zoologici. Fennici. 24: 1-17.
Hokkanen, T., K. Heliövaara, and R. Väisänen 1987. Control of Aradus cinnamomeus (Heteroptera,
Aradidae) with special reference to pine stand condition. Communicationes Instituti Forestalis
Fenniae 142: 1- 27.
Tropin, I. V. 1949. The pine bark bug and its control. Goslesbumizdat, Moscow, 55 pp. (in Russian).
Usinger, R. L., and R. Matsuda 1959. Classification of the Aradidae (Hemiptera-Heteroptera). British
Museum (Natural History), London.
3. RHYACIONIA BUOLIANA, EUROPEAN PINE SHOOT MOTH

þ
M. Turþáni
3.1 Taxonomy & systematics

The European pine shoot moth ((Rhyacionia buoliana Denis & Schiffermüller,1775)5
belongs to the family Tortricidae, subfamily Olethreutinae, genus Rhyacionia
Hübner, 1813. The species was described as Tortrix buoliana by Denis &
Schiffermüller in 1775. Other species of the genus are: R. pinicolana (Doubleday,
1849), R. pinivorana (Lienig & Zeller, 1846), R. duplana (Hübner, 1813) and R.
piniana (Herrich-Schaffer, 1851) which all occur on pine in Europe.
Figure 1. Upper left: current expanding pine shoot attacked by Rhyacionia buoliana; upper
right: severely stunted pine sapling following several years of repeated attacks by R. buoliana
in the uppermost shoots; lower left;. young pine tree after several years of shoot attacks
leading to a lasting bend on the stem; lower right: distroyed timber quality due to attack by R.
buoliana decades ago (all pictures taken by Bo Långström).
3.2 General biology

The European pine shoot moth occurs throughout Europe and parts of Asia where it
is a major pest of pine plantations. It has also been brought to North America in
1914 and later to South America (Chile), where is a pest on Pinus radiata and P.
contorta.
The damage is done by larvae, which bore in shoot and bud tissue. Adults
emerge during June-July, and the moths are active around sunset but usually do not
fly during cool or wet days. Air temperatures below 12 °C inhibit flight. Female
moths lay eggs on host pines that may be scattered over a large area. Eggs hatch in
one to two weeks, and the new larvae begin feeding by mining needles first, and
then they move into the buds. The larvae spend the winter under a resin/silk shelter
between the buds or in buds. The following spring the larvae continue feeding in the
buds or move into the expanding shoots which become tunnelled, distorted and often
killed. Attacks frequently occur in young trees (below 30 years of age). All pines are
attacked, but Pinus sylvestris appears to be especially susceptable. Developing
shoots are tunnelled and killed. Pupation occurs in shoots and lasts two to three
weeks in late spring. There is only one generation per year.
3.3 Host finding

Little is known about the host finding of this species, but according to Tsankov &
Kostov (1985), R. buoliana appeared in the third year after plantation establishment,
and reached maximum numbers in plantations that were 5-6 years old. Smelyanets
(1995) observed that the pest spread from weakened to more resistant groups
amongst the pines.
3.4 Host resistance

Generally, pine species that have high resin yields are highly resistant to the R.
buoliana. In the series Lariciones, Pinus nigra is most likely to provide highly
resistant material. Pinus resinosa has significantly lower resistance than the other
pines in the series. According to Turþáni (1988), Pinus nigra was significantly more
resistant in conditions of central Slovakia in areas influenced by strong air pollution.
Infestation of Pinus sylvestris buds reached 18.5 to 24.3 %, whereas in Pinus nigra
only 0.5 to 2.8 % of the buds were attacked. Growth of P. nigra was not much
affected in spite of the fact, that chronical outbreak of R. buoliana occured there,
whereas the attacks caused bushy growth in P. sylvestris in these polluted areas.
Smelyanets (1977) considers that the essential oils of pine trees regulate their
resistance to R. buoliana and act as a protective system warding off infestation.
They act through the physiological processes of the insect in the larval stage.
Investigations in the Ukraine showed differences in the constitution of the
haemolymph of larvae that had fed on trees of different degrees of resistance, as
evidenced by different contents of essential oils in the buds. The results of the same
author showed that the parameters characterising the level of physiological condition
of the trees and consequently their resistance to insect attack differed widely,
particularly the intensity of resin exudation from cut shoots, the resin pressure in the
trunks, the content of beta -pinene, limonene and phellandrene in the needles, and
the content of camphene and other terpenoids in the shoots (Smelyanets 1978).
A relationship between damage caused by R. buoliana and Blastesthia turionana
and genetic forms of Scots pine with seeds of different colours has also been found
(Rostovtsev, 1979). Only 22.9 % of plants of the black/brown seed form were
damaged, whereas the corresponding figure was 94.9% for the brown/black seed
form. In general, the dark-seeded forms are more resistant to tortricids attack. In
field studies conducted in the Ukraine, infestation by Rhyacionia buoliana on Scots
pine trees produced an immune response (an increase in the concentration of
essential oils). However, not all trees in study plots produced high concentrations of
essential oils, allowing small populations of R. buoliana to survive and act as
reservoirs for future outbreaks (Smelyanets 1996).
The influence of the summer climate both on resin production and population
increase is important both in Europe and in North America. In drought years the
trees produce little resin and are thus unable to repel the shoot moth larvae.
Consistently, R. buoliana populations are high in areas where the period May to July
is dry. Summer temperatures also influence the duration of development from
oviposition to the 3rdd instar (5-14 weeks). Then in a warm summer, the third instar
larvae attack the newly formed buds, whereas in a cool summer the larvae attack
after the buds are protected by well-developed resin canals.According Tsankov et al.
(1979) considerable differences were found between the provenances of P. nigra in
their resistance to the insect. The least resistant provenances were of Corsican
origin, but these also exhibited rapid rates of growth and may be used for
afforestation in areas where wood volume production rather than stem quality is
important.
3.5 Natural enemies

Natural enemies play an important role in R. buoliana population dynamics. Over
100 parasitoids and predators have been identified worldwide. Important parasitoids
are braconids Glypta resinanae Htg. and Scambus brevicornis Grav. Other larval
parasitoids are the braconid Orgilus obscuratorr (Nees), and the ichneumonids
Eulimneria rufifemurr (Thoms.) and Temelucha interruptorr (Grav.). T. interruptor
was disclaimed as a cleptoparasitoid detrimental to the potential impact of O.
obscuratorr (Tarwacki 1998).
Orgilus obscuratorr is a specific larval parasitoid with a high fecundity and an
efficient host finding ability that permits it to avoid both superparasitism and very
low host density situations. In contrast, T. interruptorr is a more general parasitoid of
Microlepidoptera and while it also has a high fecundity it is inefficient at host
finding and oviposits most successfully in host larvae previously attacked by O.
obscurator. Both parasitoids attack young host larvae and only develop further when
the host larvae approach maturity.
According to Zerova et al. (1989) there are also some other parasitoids: Scambus
calobatus (Grav.), Pimpla turionellae L., Lissonota dubia Hgn. , Lissonota folii
Thom., Bracon stabilis Wesmael, Meteorus inctericus Nees, Charmon extensorr L.,
Microdus rufipes Nees, Apanteles lineipes Wesmael, Habrocytus semotus Walker,
Trichogramma telengai Sorokina. Tarwacki (1998) mentioned two species of
ichneumonid parasitoids ((Pristomerus orbitalis Hgn. and Scambus sagax Htg.)
which were reared from larvae and pupae of two tortricids ((R. buoliana and
Blastesthia turionella ) and one tineid ((Exoteleia dodecella). The pupa was the most
frequently attacked stage. Tsankov (1998) observed that the most common
parasitoids of R. buoliana on Pinus nigra and P. sylvestris in Bulgaria were
Exeristes roboratorr F. and Campoplex submarginatus Cresson. Low winter
temperatures, below –25 °C, negatively affect the abundance of Rhyacionia
buoliana, and especially important are periords of low temperatures which follow
warm periods, when resistance of overwintering larvae is small. The reduction of
abundance is, however, not long-lasting as the abundance usually reaches normal
levels in two years.

The larval feeding results in dead buds and shoots, but damaged terminal shoots
often survive although they are badly bent. This leads to reduced growth, but even
worse are the lasting stem crooks that destroy the timber value of the butt log.
Abundant and repeated attacks lead to bushy trees with no main stem, and it may
take years for these trees to eventually recover to normal height growth. Even so, log
quality will remain low due to internal timber defects.
Damage is considerable in plantations of Christmas trees or nursery plants,
when killed terminals cause bushy growth that may render nursery plants or
Christmas trees unmarketable. Forest stands on poor soils, or areas influenced by air
pollution are mainly damaged. The highest aggressiveness was recorded in central
Europe (Hungary, Romania and Slovakia). Out of this centre, other spots with
higher aggressiveness were recorded d in Ireland and The Netherlands.
There are three points in the life cycle of R. buoliana when insecticides can be
effective – migrating larvae (early spring), adults (early summer) and newly hatched
larvae (early summer). Accurate timing of insecticide application is critical for
satisfactory control. In recent years some succes has been achieved with summer
applications targeted at adult and young larvae. These applications can be timed
with help of pheromone traps. Spraying is done one week after the 1stt adults are
detected in pheromone traps. Moth activity lasts about 4 weeks.
Ecological prevention has been studied by Rodziewicz & Kolk (1980), who
found that intersowing with lupins reduced the numbers of pine buds and shoots
damaged by R. buoliana by 2/3.. The ability of Trichogramma dendrolimi, T.
telengai (both originating from Bulgaria) and T. nerudai (native Chilean species) to
parasitize on ova of Rhyacionia buoliana (insect pest of Pinus radiata) was
investigated by Cerda & Gerding (1999).
Tiberi et al. (1988) investigated the effectiveness of the mating disruption

technique for control of Rhyacionia buoliana. Based on the results of catches in
pheromone traps and percentage infestation, the results from the first year indicated
that this method was effective in reducing the population of the tortricid. It is
suggested that possible immigration of mated females from neighbouring pine
stands might have reduced the effectiveness of the treatment. In 1988, the population
of the pest had increased by only 6% in the treated pine stand compared with 38% in
the untreated one. In small isolated areas of pine stands surrounded by broadleaf
trees mass trapping using pheromone traps (pheromone E9-12Ac + 12Ac 1:1 in dose
1000 µg) with 5-10 m spacing could also be used (Turþáni 1988).
3.7 References
Cerda R., C. & Gerding P., M. 1999. Biological control of Rhyacionia buoliana Den et Schiff
(Lepidoptera: Tortricidae) with Trichogramma spp. Agro-Ciencia, 15, 279-83.
Rodziewicz, A. & Kolk, A. 1980. Effect of perennial lupins on the density of Rhyacionia buoliana and
other insects in young Scots pine plantations. Sylwan, 124, 23-30.
Rostovtsev, S. A. 1979. Damage by pine shoot moths to forms of Scots pine differing in seed colour. Lesnoe
Khozyaistvo, 9, 63-64.
Smelyanets, V. P. 1977. Mechanisms of plant resistance in pine trees, Pinus sylvestris. 1. Indicators of
physiological state in interacting plant-insect populations.
a Zeitschrift fur Angewandte Entomologie, 83,
225-33.
Smelyanets, V. 1995. Cascade form of process at arising of an aggressive biotype of the winter pine shoot
moth ((Rhyacionia buoliana Schiff., Lepid. Tortr.). 1. Heterogeneity of the main parameters in a pest
population and in a protective system of the pine as a base of mechanism of forming of initial
aggressive groups of the pest. Archives of Phytopathology and Plant Protection, 29, 317-25.
Smelyanets, V. 1996. Dynamics of trophical niches of the winter pine shoot moth (Rhyacionia buoliana
Schiff., Lepidoptera: Tortricidae) and response of the protective system of the Scots pine to the
affection. 2. Response of the protective system of the Scots pine to affection by the winter pine shoot
moth. Archives of Phytopathology and Plant Protection, 30, 421-28.
Smelyanets, V. P., Lopatina, N. V. & Koveshnikova, I. V. 1978. Changes in the fat-body and haemolymph
of larvae of the pine budworm overwintering after feeding on pine trees differing in resistance. Zakhist
Roslin, 24, 95-102.
Tarwacki, G. 1998. Pine tortricids (Tortricidae) and their parasitoids in the Forest Experimental Department
(LZD) at Rogów. Sylwan, 142, 89-95.
Tiberi, R.; Covassi, M. & Roversi, P. F. 1988. Use of the confusion method against Rhyacionia buoliana
(Den. et Schiff.) in young pine stands in central Italy (Lepidoptera, Tortricidae). Redia, 71, 356-68.
Tsankov, G. 1988. The ichneumonoid parasites of the European pine shoott moth caterpillars in Bulgaria
(Hymenoptera: Ichneumonoidea). Advances in parasitic Hymenoptera research: Proceedings of the II
Conference on the Taxonomy and Biology y of Parasitic Hymenoptera, 391-94
Tsankov, G.; Kostov & K. D. 1985. Pest-resistance and growth of Scots pine provenances outside their
natural range at Rabisha, Belogradchik forest. Gorskostopanska Nauka, 22, 23-30.
Tsankov, G.; Buchvarov, D. & Kostov, K. D. 1979. The resistance to Rhyacionia buolianaa of seedlings of
Pinus nigra a of different provenances in the trial plantation at Sirakovo village, Khaskovo region.
Gorskostopanska Nauka, 16, 70-80.
Turþáni, M. 1988: Survey of occurence and harmless of Rhyacionia buoliana in polluted area close to
Žiar nad Hronom. Diploma thesis, 1-46.
Zerova M.,D., Seregina L.Ya., Tolcanic V.I. & Kotenko A.G. 1989: The annotated list of entomophagous
insect of the Tortrix viridana L. (Lepidoptera, Tortricidae) in the south-west of the European part of
the USSR.Infomation journal of IOBC – east palaearctis section, p. 18-53.
4. DIORYCTRIA SYLVESTRELLA
þ
M. Turþáni

Dioryctria sylvestrella (Ratzeburg 1840) belongs to family Pyralidae, subfamily
Phycitinae, genus Dioryctria Zeller, 1846. The species was described as Dioryctria
sylvestrella by Ratzeburg in 1840, but has also been known as Dioryctria
splendidella (Herrich-Schäffer 1848) which is a junior synonym. Other species of
the genus are: D. abietella (Dennis et Schiffermuller, 1775), D. simpliciella
Heinemann, 1863 and D. schuetzeella Fuchs, 1899, which cause damage to cones.
4.2 General biology

D.sylvestrella occurs throughout Europe, northern Africa and large part of Asia. It is
more common in southern part of the distribution area, where is one of the important
pests of pine plantations. In Europe it occurs up to the arctic circle.
This species is feeding on pines (cones, shoots, buds and stems) and less
frequently on spruce. It is one of the major pests of Maritime pine (Pinus pinaster).
Female moths lay eggs on fast growing pine trees, and fertilised or highly productive
stands experience severe damage. In central Europe, the species is often found at
sites infested by Endocronartium (=Peridermium
= ) pini and E. strobi (Szujecki
1995). The larvae also damage stems of young trees that have suffered previous
mechanical damage. Within a stand of maritime pine, trees attacked by D.
sylvestrella showed no spatial aggregation and clusters of 66 trees proved to be an
optimum sampling unit for determining overall percentage infestation. The larva is
pink or greenish in colour, and the larvae make galleries into floem and provoke
resin production, which is mixed with frass. The activity of the larva slows down in
the autumn and the larva overwinters in the gallery. The flight period is July and
August, when the species can be taken at light. It is also a sporadic migrant.
4.3 Host finding

It appears that the most productive stands are most infected by D. sylvestrella. Trees
with the best radial growth are attacked first. It is suggested that larval penetration in
the inner bark is aided by any bare tree surface (linked wounds or cut branches) as
well as the presence of a thin bark; and that the quality and quantity of inner bark
affects larval growth (Carisey et al. 1994).
4.4 Host resistance

Maritime pine susceptibility to this insect is evidently related to the terpene
composition (Jactel et al. 1994). The level of attack on pruned trees increased
strongly with the intensity of pruning, showing a significant positive correlation with
the number of pruning wounds. The removal of dead branches did not result in any
increase of infestation. The infestation of pruned trees had no contagious effect

towards neighbouring unpruned trees. The majority of the attacks were located in
the vicinity of the branch insertion, and in 2- to 3-year-old internodes. In the second
year, the percentage of pruned re-attacked trees continued to show a significant
positive correlation with the severity of pruning.
r Jactel et al. (1999) found that tree
susceptibility was positively and genetically correlated with tree diameter. Infested
trees contained significantly more terpinolene and the regression between percentage
of attacked trees and mean proportion of terpinolene per family was significant.
The infestation dynamics of D. sylvestrella is also related to fertilisation of the
Maritime pine. Fertilised trees exhibit significantly greater tree growth and higher
infestation rates than control. The rate of infestation also showed a significant
positive correlation with the mean percentage of terpinolene. The distribution of
infested tree frequencies indicated, that both tree pruning, which creates bark
wounds, and tree vigour, which increases bark cracking, could simultaneously
increase wood resin flow, thus enhancing tree attractiveness.
4.5 Natural enemies

Mainly species of Braconidae and Ichnemonidae attack D. sylvestrella. The braconid
Itoplectis cristatae Momoi was recorded as a parasitoid in Japan. Several other
parasitoids of D. sylvestrella have been found, including the genus Macrocentrus
(Colombo & Eördegh 1995). The ichneumonid Macrocentrus resinellae L. also
often infests this pest. Macrocentrus abdominalis Fabr. is a major natural enemy of
D. sylvestrella in China, and M. watanabei also plays an important role. Other
species of genus Macrocentrus were also found to be parasitoids of this species: M.
linearis Nees, M. nitidus Wesmael, M. sylvestrellae van Achterberg. Scambus
capitator Aubert and Venturia robusta (Hym., Ichneumonidae) are known as
parasitoids of the D. abietella larvae. Among insect predators, the genus
Ancistrocerus spp. (e.g. Ancistrocerus ichneumonideus Ratz. and A. gazella Panzer)
was recognised as feeding on larvae. These small vasps collect paralysed larvae and
bring them to rearing chambers into nest. There are also some indirect indications
about the role of birds in predation of larvae and pupae.

The highest aggressiveness was recorded in the southern Europe (France and Italy).
Lower extension of damage was found in Spain and Portugal. Jactel et al. (2002)
described, that the percentage of trees infested was significantly lower in the pine
stands bordered by broadleaved stands than in the pine stands surrounded by other
pine stands, and in the former, D. sylvestrella infestation showed a significant
logistic increase with distance from the stand edge. This could be due to effects of
resource concentration or natural enemy attack. These results suggest that the
conservation or restoration of non-productive mixed-species stands adjacent to
intensively managed plantations is a useful preventive method for pest management
in forest monocultures.
Application of insecticides against newly laid eggs or newly hatched larvae

reduces damage from 66 –100% to 0-20%. Timely sanitation fellings of heavily
infested tree is recommended.
Direct and indirect selection using terpinolene as a biochemical marker could be
used for increased host resistance, but genetic gains for tree resistance have to be
weighed against possible genetic losses in tree growth.
4.8 References
Carisey, N.; Menassieu, P.; Baradat, P.; Lemoine, B. &Lévieux, J. 1994. Sensitivity of maritime pine
((Pinus pinasterr ) to attack by the pine moth Dioryctria sylvestrella (Lepidoptera, Pyralidae) in a
range of site conditions. Relationships to certain growth characteristics. Annales des Sciences
Forestières, 51, 67-75.
Colombo, M. & Eördegh, F. R. 1995. Dioryctria sylvestrella Rtz. (Lep., Pyralidae) in nursery of Pinus
cembra . Informatore Fitopatologico, 45, 38-40.
Hirose, Y. & Nozato, K. 1975. Habitat specificity in three sympatric species of pine shoot moths. Kontyu,
43, 40-48.
Jactel, H.; Menassieu, P. & Raise, G. 1994. Infestation dynamics of Dioryctria sylvestrella (Ratz.)
(Lepidoptera: Pyralidae) in pruned maritime pine ((Pinus pinasterr Ait.). Forest Ecology and
Jactel, H.; Kleinhentz, M.; Raffin, A. & Menassieu, P. 1999. Comparison of different selection methods
for the resistance to Dioryctria sylvestrella Ratz. (Lepidoptera: Pyralidae) in Pinus pinasterr Ait
Physiology and genetics of tree-phytophage interactions. International Symposium, Gujan, France,
31 August-5 September, 1997, 137-49.
Jactel, H.; Goulard, M.; Menassieu, P. & Goujon, G. 2002. Habitat diversity in forest plantations reduces
infestations of the pine stem borer Dioryctria sylvestrella . Journal of Applied Ecology, 39, 618-28.
Szujecki, A. 1995. Forestry entomology. Wydawnictwo SGGW Warszawa 1995, 2 Volumes.
5. COSSUS COSSUS, THE GOAT MOTH

þ
M. Turþáni

Cossus cossus, Linnaeus 1758 belongs to family Cossidae, subfamily Cossinae,
genus Cossus Fabricius, 1793. This species was described by Linnaeus in 1758. All
species of this family feed inside the stems or roots of woody plants.
5.2 General biology

Cossus cossus infests many fruit trees (apple, cherry, pear, plum, olive) and other
deciduous trees such as sweet chestnut (Castanea), elm (Ulmus), oak (Quercus),
poplar (Populus), chestnut (Aesculus
( ), lime (Tilia), maple ((Acer) and willows (Salix
spp.).
The egg is elliptical 1.2 x 1.7 mm, reddish-brown with a black longitudinal
stripe. They are laid in groups of 15-50 eggs in crevices in the trunks or in wounds
in the bark. A female lays about 500-1200 eggs with a maximum of 2000. The larva
takes 3-4 years to develop in the wood of the tree and then it hibernates in the wood
Figure 2. Upper left: large amounts of boring dust exuded from poplar tree under attackd by
Cossus cossus (photo: G. Csoka); upper right: resting adult of Zeuzera pyrina (photo: G.
Csoka); lower left: fullgrown larva of C. cossus (photo:M. Zubrik; lower right: large larva of
Z. pyrina (photo: G. Csoka)
or sometimes outside the trunk in the soil. A mature larva reaches a length of 90 to
100 mm. The young caterpillar is carmine pink; the colour is darker and more
pronounced in older individuals. The ventral surface is lightt yellow, the head black
with powerful mandibles. Larva changes colour prior the pupation. The young
larvae feed jointly beneath bark, and after the 1stt hibernation in the wood. Frass and
faeces are ejected out of the larval galleries which are elliptical and often vertically
oriented. Up to several tens of larvae could feed within one tree. The later instars are
able to migrate from one to another tree. Glands joined to the mouthparts secrete a
smelly substance, that resembles the smell of old leather, vinegar or poor quality
wine. The pupa is 50 to 60 mm long, with groups of sharp spicules, which enable it
to crawl towards the opening of the gallery just before emergence. Pupation occurs
in spring, and the adults fly in early summer, laying eggs in deep cracks in the bark.
Emergence of moth follows 3-4 weeks after pupation. The adult is a large moth of
70 to 80 mm wingspan, greyish coloured, with a massive body covered in hairs. The
forewings have a dull appearance; the hind wings are grey and hairy on their basal
part. Flight period is at June – July after sunset. During day-time specimens rest on
trunks relying on their mimicry coloration.
5.3 Host finding

The female moth prefers older and bigger, often wounded trees. The eggs are
deposited in the wounds in the bark this enables the young larvae to invade the tree
easily. Damage by C. cossus is very common in roadside trees. This is partly
attributed to the damage caused by mowing machines to the trunks.
5.4 Host resistance

Some resistance appeared by planting resistant and non-resistant tree species in an
alternating pattern (interplanting). Thus, Tilia interplanted with Picea or Pinus
suffers little from attack by Zeuzera pyrina, to which it is otherwise susceptible, and
Acerr interplanted with Ailanthus seems resistant to C. cossus.
5.5 Natural enemies

The tachinid Xylotachina diluta (Meigen) is a specific parasitoid of C. cossus larvae.
Up to 15% of the larvae were found to be parasitized by this tachinid. The larvae are
also parasitized by other tachinids species such as Nilea lethifera Pand. and
Phorocera assimilis Fall. Other parasitoids are the ichneumonids Dicaelotus
pussilatorr Grav., Stenarella gladiatorr Scop., Lissonota setosa Fourcr. and
Herpestomus arridens Grav. The adults of C. cossus are frequently attacked by owls
and bats (Szujecki 1995).
Larval diseases are caused by Spicaria cossus Petsch. Also Bacillus thuringiensis
was isolated from larvae of C. cossus (Grassi & Deseö 1984). Several nematode
species were found on C. cossus in the Tashkent region (Zemlyanskaya & Lysikova
1976). In Turkey, the larvae were found to be a host of Verticillium lecanii. Virus
infection by Borrelinavirus cossi and Entomopoxvirus (Vagoiavirus) cossi) is

considered to be the main mortality factor in C. Cossus populations, sometimes
more than 50% of the larvae are infested (Weiser 1996).

From the BAWBILT database it was derived that the highest aggressiveness of C.
cossus was recorded in southern and south-eastern Europe (Italy and Romania).
Lower aggressiveness was found in Hungary and The Netherlands – where poplar
plantings are also common. The larval tunnels interfere with sap circulation, this
makes the branches or trunks susceptible to breakage in the wind and sometimes the
tree is killed; although the moth usually attacks trees, which are wounded by traffic
and mowing activities. In situations with an overpopulation of too many larvae
within one tree, some of the full-grown larvae may leave the tree and crawl to
another tree. These full-grown larvae are able to invade into healthy, non-wounded
trees.
Survey of pest abundance is done by assessment of damage to the trees. The
number of males captured by pheromone traps can also be used. Control should be
done by removal of the heavily infested trees from forest stands. It is necessary to
burn or transport the felled trees out of the forest stands, because older larvae are
able to finish development in the felled trees or they can migrate to surrounding
living trees (Novotný & Zúbrik 2002).
Control measures should be preventive, owing to the difficulty of killing the
larvae within their galleries. Chemical control consists of sprays of insecticides on
the base of the tree and on the surrounding soil against ovipositing females and
newly hatched larvae. However, in many countries, the use of insecticides in urban
trees and forests is not sustained. The use of the fungus Beauveria bassiana causes
mortality of C. cossus in lab conditions but an appropriate method of field
application is not yet possible.
Ecological control using pheromone dispensers can be done with a pheromone
blend Z3-C10Ac+Z5-C12Ac at a 4:1 ratio. The mating disruption method applied in
apple orchards, showed an encouraging confirmation. In orchards, the percentage of
infestation in the trunks decreased within the treated field year by year compared
with the initial level and the level of infestation in the control fields. It thus seems
possible to achieve sufficient control, and to keep the pest below a damaging
threshold with a . Regarding the mass trapping method, any statistical difference
between 5 and 10 traps/ha managed was relieved. The trap type used was the
pyramidal funnel with wings in eyes height (Pasqualini & Natale 1999).
Several species and/or strains of steinernematidd and heterorhabditid d nematodes
have been tested for efficacy against the larvae of the C. cossus, both in laboratory
and field conditions. Some of the tested nematodes (Steinernema glaseri, S. feltiae
"100" and "1192" strains) proved to be very effective in the bioassays, but they
provided a poor control when applied locally in the larval galleries. S. feltiae strain
(not tested previously in the laboratory)r gave the best control, though still poor
(25%) in the localized applications carried out (Rovesti 1989).
5.7 References
Grassi, S. & Deseö, K. V. 1984. Distribution of Bacillus thuringiensis Berl. and prospects of using it in
plant protection. Atti Giornate Fitopatologiche, 425-33.
Novotný, J. & Zúbrik, M. 2002 Biotic Pests of Slovakian forests. Gerlach Slovakia, 1-206.
Pasqualini, E.; Natale, D. 1999. Zeuzera pyrina and Cossus cossus (Lepidoptera, Cossidae) control by
pheromones: four years advances in Italy. Bulletin OILB/SROP, 22:9, 115-24.
Rovesti, L. 1989. Experiments with entomoparasitic nematodes against Cossus cossus L. (Lepidoptera:
Cossidae). Difesa delle Piante, 12, 23-32.
Szujecki, A. 1995. Forestry entomology. Wydawnictwo SGGW Warszawa, 2 Volumes.
Weiser, J. 1996 Insect diseases. Academia, Nakladatelství þeskoslovenské akademie vČd Praha.
Zemlyanskaya, A. I. & Lysikova, E. A. 1976 The nematodes of insect pests of decorative plantations and
of forests in the Tashkent area. Ekologiya i biologiya paraziticheskikh chervei zhivotnykh
Uzbekistana., 48-54.
6. ZEUZERA PYRINA, THE LEOPARD MOTH

þ
M. Turþáni

Zeuzera pyrina belongs to family of Cossidae, subfamily Zeuzerinae, genus Zeuzera
Latreille, 1804. The species was described byy Linnaeus in 1761. All species of this
family feed in stems or roots of woody or herb species.
6.2 General biology

Zeuzera pyrina infests a large number of shrubs and tree species such as apple, pear,
plum, cherry, olive, pomegranate (Punica granatum), quince, black currant, currant,
Citrus, vine, oak (Quercus), ash ((Fraxinus), willow (Salix), lime (Tilia), plane
(Platanus), beech ((Fagus), poplar (Populus), maple ((Acer), tamarisk (Tamarix), etc.
The female adult has a 50 to 60 mm wing span, this is 35 to 40 mm for the male.
The thorax is white and hairy with 6 blue spots. The abdomen is relatively long. The
wings are white, sprinkled with small metallic blue spots. It does not feed and its
lifespan is extremely short, from 8 to 10 days. The female mates soon after it has
emerged. The female lays about 1,000 eggs deposited in clusters on the trees,
preferably in places where the female can insert her ovipositor (crack, old larval
gallery); it can occasionally lay eggs in the ground. The egg is oval-shaped, about 1
mm, with a light yellow to bright salmon colour. Its embryonic development lasts 7
to 23 days. The mature larva is 50 to 60 mm, bright yellow with numerous small
black points on each segment. The head and the thoracic plates are shiny black. The
caterpillars at first remain clustered in a silky cocoon from which they eventually
disperse at dawn or at dusk. They bore into the tips of branches and shoots, and
move downwards to attack the young parts of the tree (twigs, spurs, pouches, central
veins and leaf peduncles on certain shrubby species).
The caterpillars generally move around, to penetrate lower in the twigs and
branches. After several migrations, the larvae attack the largerr branches and the
trunk, in which they form ascending galleries under the bark, later in the wood. The
entry holes of the larvae are marked by small heaps of saw-dust and frass (in the
shape of small cylinders) accompanied by sap a outflows, particularly visible on the
large branches, typically at a stage where the damage is already very advanced.
The life cycle is annual in the southern part of Europe; it lasts 2-3 years in the
northern regions. The adults generally appear from the beginning of June to August.
In the Mediterranean region, the flight takes place from April to October. The young
caterpillars, attached to a silk thread, can be carried by the wind. This mode of
dispersal is often found in young stands; it also occurs on trees situated close to
hedges and thickets. In spring, the larva continues boring its gallery in the wood,
often in the centre of the branch. Pupation occurs from April to July. According to
Katlabi (1992) the flying period of Zeuzera pyrina is from late August to November
in Syria.
6.3 Host finding

The female prefers older and bigger trees, often weakened, particularly in dry years
and on dry soils. Damage by Z. pyrina is often found on roadside trees. This is partly
attributed to the damage of the bark caused by mowing machines. Healthy trees
resist attacks better (favourable influence of irrigation and of a balanced mineral
supply).
6.4 Host resistance

There are some indications of resistance. According to Lagunov (1981) green ash
((Fraxinus pennsylvanica) was damaged more frequently and severely (25% vs. 7%)
than hybrid ash ((F. excelsior x F. pennsylvanica). Survival of young larvae
artificially applied to current-year shoots was 90-97% on green ash and 57-77% on
hybrid ash. The shoots of green ash contained more starch and less Ca and Mg than
those of the hybrid ash. This suggests that starch is responsible for the greater
susceptibility of green ash. Preliminary observations with various walnut ((Juglans
regia) varieties show promising levels of tolerance to Zeuzera pyrina (Monastra et
al. 1997) Also interplanting with resistant and non-resistant species shows some
relationships e.g.: Tilia interplanted with spruce or pine suffered little from attack by
Z. pyrina, to which it is otherwise susceptible.
6.5 Natural enemies

Campadelli (1998) found as parasitoids several species e.g.: Ichneumonids:
Neoxorides nitens (Grav.), Dolicomitus messorr (Grav.), Diadegma terebrans
(Panz.), Pristomerus vulneratorr (Panz.), Braconids: Dolichogenidea laevigata
(Ratz.), Helcon sp. Chalcidids: Perilampus tristis Mayr, Diptera: Megaselia
praecusta (Schmith), Odinia meijerei Collin. Also braconids Apanteles lacteipennis
Curt., Apanteles albipennis Nees., Apanteles laevigatus Ratz., ichneumonids
Ichneumon abeillei Berth., Schreineria zeuzerae Ashm., Horogenes punctoria
Roman, chalcidids Elasmus ciopkaloi Nov., Euderus sp., Copidosoma truncatellum

Dalm., Elasmus albipennis Thoms., Elasmus schmidti Ruschka, Elachertus
nigritulus Zett., are known as parasitoids of Z. pyrina. Disney & Campadelli (1997)
describedd Megaselia zeuzerae sp. nov. as a parasitoid of the larvae of Zeuzera
pyrina.
Among the predators, mainly birds are known: Dendrocopos major, D. minor,
Picus viridis, Pediculoides ventricosus Berl. Furthermore there are some fungi such
as Aspergillus parasiticus, Mucor hiemalis and Fusarium solani known to be
pathogenic to larvae of Zeuzera pyrina.

Trees weakened by leopard moth attacks are frequently subject to other xylophagous
pests such as hornet clearwing moth (Synanthedon myopaeformis), goat moth
(Cossus cossus) and bark beetles. Furthermore, the old larval galleries serve as a
refuge to the woolly aphid (Eriosoma lanigerum), which thus partially escapes from
chemical treatments.

The highest aggressiveness was recorded in central and south-eastern Europe
(Hungary and Romania) in Danube basin. This species seems to be less important
than its bigger relative Cossus cossus. The seriousness of the attacks varies
according to the age of the plantations on young trees: 1 caterpillar is enough to kill
a tree; 3-year-old trees can lose part of their structure. The attacked trees become
extremely vulnerable to wind damage and the central axis system is permanently
affected. Therefore, results clearly indicate the mating disruption technique used is
working very well and effectively should protect the heavily infested stands against
Z. pyrina (Sarto 1999).
Current control practices include either manual killing of larvae inside their
galleries by introducing a flexible wire into it, a time consuming, labour intensive
and therefore costly procedure, or wide spectrum insecticide applications against
adults. Due to the prolonged adult emergence period, however, and the short
residual activity of the insecticide sprays, a large number of applications is required
throughout the active period of the insect (about three to four months) for an
effective control, resulting in undesired environmental side effects of such
applications.
Guario et al. (2001) compared the effectiveness of insecticides, pruning and
disposal of infested branches, and pheromone traps to control Zeuzera pyrina in
olive groves in Italy. The insect was controlled by application of triflumuron,
teflubenzuron, hexaflumuron and azinphos-methyl. t Following 2 applications (at 20
and 25 days), the initial infestation of 75% of the trees was reduced to 3-6%.
Hexaflumuron, azinphos-methyl and teflubenzuron were the most effective. In
another study (Pasqualini et al. 1999), horticultural (pruning), mechanical (removal
of larvae) and chemical (spraying) treatments were evaluated for their efficiency
against Zeuzera pyrina. The results showed 16-20, 64-69 and 60-81% reduction of
infestation for the three treatments, respectively. When the treatments were applied
for two successive years, the respective reduction increased to 32, 82 and 74-86%.
Simon et al. (1999) describe control of Zeuzera pyrina by the use of Bacillus
thuringiensis.
Some experiments with nematodes Saleh & Abbas (1998) e.g.: Steinernema
riobravae [S. riobrave ], S. abbasi, S. carpocapsae S2, Heterorhabditis sp. SAA1
and S. feltiae, were done in Egypt. Laboratory experiments showed that the larvae of
Z. pyrina were highly susceptible to the nematode infection and produced more
infective juveniles (IJ) within a shorter time than the pupae. The tested nematodes
caused 87.5-100% larval mortality within 48 hours at a dose of at least 20 IJ/larva.
Bioassays were conducted to determine the susceptibility of Zeuzera pyrina to
different spore conc. of Metarhizium anisopliae. The fungus was highly virulent
against the larval stage of Z. pyrina . The percentage mortalities were 49.4, 100 and
100 for 3rd-instar larvae and 35, 90 and 100 for 6th-instar larvae at 105, 106 and 107
spores/ml conc. resp., 7 days after treatment. The results suggested the possibility of
using M. anisopliae to control Z. pyrina.
6.7 References
Campadelli, G. 1996. Some parasitoids of Zeuzera pyrina L. (Lep., Cossidae) in Emilia-Romagna.
Bollettino dell'Istituto di Entomologia `Guido Grandi' della Universita degli Studi di Bologna, 50,
127-31.
Disney, R. H. L. & Campadelli, G. 1997. A new species of Megaselia Rondani (Diptera: Phoridae) reared
from a moth larva (Lepidoptera: Cossidae) in Italy. Bollettino dell'Istituto di Entomologia `Guido
Grandi' della Universita degli Studi di Bologna, 51, 63-68.
Guario, A., Marinuzzi, V., Milella, G., Alfarano, L. & Falco, R. 2001. Chemical control of Zeuzera
pyrina in olives. Informatore Agrario, 57, 63-65.
Katlabi, H. S. Y. 1992. Flying period of leopard moth adults (Zeuzera pyrina L.) in olive trees in Syria.
Olivae, 41, 32-36.
Lagunov, A. G. 1981. Effect of the chemical constituents of ash wood on the severity of damage by
Zeuzera pyrina L. Biologicheskie Nauki, 12, 32-34.
Monastra, F., Limongelli, F. & Barba, M. 1997. European walnut germplasm from Caserta. Options
Méditerranéennes. Série B, Études et Recherches, 16, 41-48.
Pasqualini, E., Civolani, S., Vergnani, S. & Natale, D. 1999. IPM improvement on pome fruit orchards in
Emilia-Romagna (Italy). Bulletin OILB/SROP, 22, 111-20.
Saleh, M. M. E. & Abbas, M. S. T. 1998. Suitability of certain entomopathogenic nematodes for
controlling Zeuzera pyrina L. International Journal of Nematology, 8, 126-30.
Sarto i Monteys, V. 2001. Control of leopard moth, Zeuzera pyrina L., in apple orchards in NE Spain:
mating disruption technique. Bulletin OILB/SROP, 24, 173-78.
Simon, S., Corroyer, N., Getti, F. X., Girard, T., Combe, F., Fauriel, J. & Bussi, C. 1999. Organic
farming: optimization of techniques. Arboriculture Fruitière, 533, 27-32.
7. SESIIDAE, CLEARWING MOTHS

L.G. Moraal

The family of Sesiidae (clearwing moths) are unusual wasp-like moths with partly
clear (scale-less) wings and a distinct fan-like anal tuft of scales. The larvae are stem
borers in shrubs and trees. In Europe, about 15 species can cause more or less damage
on trees in orchards, cities and forests, and more information about the Sesiidae can be
found in Lastuvka & Lastuvka (2001). The genera Paranthrene Hübner 1819
(Sciapteron Staud.) and Sesiaa Fabr. 1775 are the most important ones. Both genera
have only a few species; the most important r are the Poplar clearwing moth,
Paranthrene tabaniformis Rott. and the Hornet clearwing moth, Sesia apiformis
(Clerck). In this chapter, information is given on these two species.
7.2 Paranthrene tabaniformis - Poplar clearwing moth
7.2.1 General biology

The poplar clearwing moth, Paranthrene tabaniformis Rott. (syn. Sciapteron
tabaniformis) is a common and destructive pest of young poplars. The insect is widely
distributed in Europe, Asia, North America and northern Africa. The larvae bore
tunnels in the wood and cause loss of vigour and structural weakness of the stems.
Young trees may break, thus resulting in malformed, bushy or dead trees. In The
Netherlands, seasonal flight pattern of P. tabaniformis shows considerable variation.
Trapping studies in various parts of the Netherlands in 1984-86 with the pheromone
(3E,13Z)-3,13-octadecadien-1-ol, showed considerable variation in seasonal
occurrence. The flight period lasted from late May to mid-September (i.e. longer
than usually stated). Positive correlations were found between catches and climatic
factors such as maximum or mean daily temperatures. Flight activity of males
occurred chiefly at mid-day (Moraal et al., 1988). Eggs are laid on the stems near
wounds or crevices in the bark. The neonate larvae quickly bore into the stems,
producing galleries in the wood. The larvae hibernate in the trees for 1-2 times;
Rearing on artificial media suggest that the number of hibernations is not genetically
fixed in regional races, but that temperatures
t are important (Moraal, 1989c). More
details on the bionomics can be found elsewhere (e.g. Moraal, 1988, 1989c; 1996;
Moraal et al, 1993; Schnaiderova, 1980; Schwenke, 1978; Srot, 1966).
7.2.2 Host finding

It is well known that adult females have a preference to deposit their eggs on poplars
wounded by pruning, mowing, bark diseases such as Dothichiza populea, chafing of
metal or plastic tree guards, and fraying by roe deer. These wounds possibly release
volatile constituents that attract the females. Therefore, it is important to avoid any
wounding of the trees. For instance, pruning of young trees should not be carried out
prior to and during the flight period. The moths are very lively and are fast flyers over
Figure 3. Upper left: adult and chrysalis of Sesia apiformis; upper right: larval galleries of S.
apiformis; lower left: adult and chrysalis of Paranthrene tabaniformis; lower right: broken
shoot with gall of P. tabaniformis (all pictures taken by ALTERRA)
large distances; they can easily migrate from older forests into nurseries and young
plantations where they can cause large problems (Moraal et al., 1993).
7.2.3 Natural enemies

Not all infestations will result into severe damage. In The Netherlands it was found
that, up to 55% of the P. tabaniformis larvae, can be parasitized by Apanteles
evonymellae (Braconidae) (Moraal, 1987). In Bulgaria, the mortality of the larvae by
A. evonymellae varied from 2.4 to 35.4%, while the average mortality of hibernating
larvae caused by the parasitoid Eriborus terebrans was 4.7% (Georgiev, 2001a,b).
During an experiment in the summer of 1986, fresh eggs of P. tabaniformis,
oviposited on paper strips, were attached to one-year-old poplars in a nursery in the
Netherlands. In September, 18 females of Telenomus phalaenarum (Hym.:
Scelionidae) were reared from these eggs. This nursery was adjacent to a mixed
forest: we have tried to detect any egg-parasitization in large monotonous poplar
plantations, but we could not find parasitized eggs. This suggests that vegetation
diversity could be favourable to the pest's natural enemies (Moraal, 1989b).
7.2.4 Damage and control

Serious damage caused by P. tabaniformis can occur in those situations where large
areas are planted with young trees. This occurred in The Netherlands in the new
polders, on formerly sea bottom, during the seventies and eighties. In China, it was
reported that in the eighties, mega-areas of ten thousands hectares of land were
afforested and that many trees were attacked (Miao et al., 1987, 1989). For certain
areas in Europe, it is foreseen that large areas of land will be withdrawn from
agriculture. The planned utilization of this land will include reforestation and the
planting of woody crops for biomass and timber production using fast growing
species such as poplar. This could induce large-scale problems in the future.
Control by mass-trapping in the field. In China, mass trapping by using the sex
attractant (3E,13Z)-3,13-octadecadien-1-ol, was evaluated in field studies during 3
years. The results indicate that the population densities reduced from about 0.3 to
0.01 larvae/tree. Here, 15 traps/ha were used for mass trapping in lightly to
moderately damaged forests, 30 traps/ha were used in heavily damaged forests and
4-8 traps/ha were used for a suppressive measure throughout the year (Du et al.,
1985). Also in China, as a cheaper alternative by avoiding expensive installation of
traps, smearing of tree stems with a sticky pheromone paste, was used to control P.
tabaniformis. The area under control covered 267 000 ha, and the average
percentage of infested trees decreased from 8.2% to <1% (Miao et al., 1989). In The
Netherlands, the sex attractant was applied during 3 years in 'lure and kill' and 'mass
trapping' experiments to prevent infestations in young poplar plantations. However,
although the number of males was reduced, there was no statistically significant
decrease in infestations by comparison with untreated plots (Moraal et al., 1993).
Chemical control in the nursery. It is recommended, to plant sound plant material

without hibernating P. tabaniformis larvae inside the stems, from the nursery to a
new plantation. Therefore, it is necessary to require an effective preventive chemical
control in the nurseries. Flight period of P. tabaniformis, and thereby the period of
egg depositing, can take place during the whole summer. This means that one-year-
old poplars in the nursery can be infested with larvae of different ages. Small larvae
can be overlooked very easily, and trees together with hibernating larvae, can be
planted out in the field and thus create heavy infestations on this new location in the
subsequent years. It is therefore necessary, to require an effective preventive
chemical control in the nursery. The spraying of Permethrin was effective as fluid
(250 g/litre) or 25% wettable powder at dosages of 50 cm3 or 50 g/100 litres carrier:
5 treatments from early June to August gave complete control (Wouters, 1979).
Monitoring of the flight with sex-attractant baited traps is considered to be very
useful for timing this control. Nevertheless, newly planted sound poplars, can be
infested in their new plantations, by migrating moths from adjacent older poplar
stands (Moraal et al., 1993).
Control with biological agents. In experiments, the nematode Neoaplectana

carpocapsae was sprayed in aqueous suspensions, on young infested poplar stems,
or injected into larval boreholes. Even at the lowest dosage (250 nematodes/ml) the
larvae were killed in each gallery (Wouters, 1977). The fungus Beauveria bassiana
was applied in suspensions in the larval boreholes; this resulted in a control up to
50% (Cavalcaselle, 1975). However, the methods as mentioned above are very
labour-intensive and therefore very costly.
Resistance and tolerance of poplars. Certain secondary plant metabolites such as

phenol glycosides could play a role in the chemical defence against herbivores,
because they may have feeding deterrent or toxic properties (Augustin et al., 1993).
However, the small neonate larvae of P. tabaniformis can crawl over distances up to
140 cm, to find a suitable place to invade the tree. They bore easily into the young
stem, through wounds, lenticels or at the rough surface near the crotch of a twig.
Within one hour, they have disappeared inside the stem (Moraal, 1994). We have no
information if the neonates ingest some amountt of the bark tissue, before reaching the
xylem. If they do not, they probably bypass the plant's chemical defence system. In the
literature, we could not find statistical reliable data to designate clones to be more or
less resistant.
Tolerance is often confused with a low or moderate level of genetic resistance.
However, tolerance does not affect the population dynamics of the pest but does raise
the threshold level of the plant. For example: during experiments in 1988, the clone
'Florence Biondi' had relatively more infestations than 'Robusta'. However, in 1989
and 1990 it was almost the reverse. The recovery of 'Florence Biondi' may be
attributable to this clone's ability to grow
w faster than 'Robusta' during the first years
after planting. Rapid growth during the first years after planting has the advantage that
larval galleries are overgrown more rapidly, and therefore the risks of stem snapping
decreases strongly (Moraal, 1996; Moraal et al., 1993).
It has to be kept in mind that infestations may show interaction between clonal
resistance or tolerance and local conditions such as climate, soil characteristics,
quality of nursery material and distribution of the insect. Also Noh et al. (1994)
found significant differences among 25 genotypes of poplar against borers, such as
the Osier weevil, Cryptorrhynchus lapathi, but tolerance was more affected by
environmental factors than by genotype.
Fewer problems in vigorous trees. Wounded trees may release volatile constituents,
which attract the females. Therefore, it is important to avoid any wounding. For
instance, pruning of trees should not be carried out prior to and during the flight period
of the moth. Vegetation diversity could play an important role to suppress insect pests.
It makes the environment less favourable to the pest and more favourable to the pest's
natural enemies. In areas with a high infection pressure of P. tabaniformis, we
recommend to stimulate a rapid growth of the poplars during the first years, because
larval galleries are overgrown more rapidly. This can be achieved by planting on
suitable locations and by using clones which are known as rapid starters. Also
application of fertilizers can be an important preventive measurement to keep the trees
vigorous.
7.3 Sesia apiformis - hornet clearwing moth
7.3.1 General biology

The Hornet clearwing moth, Sesia apiformis (Clerck) ((Aegeria apiformis; Trochilium
apiformis) (Lepidoptera: Sesiidae) is the largest member of the family of clearwing
moths in Europe. The young larvae tunnel in the cambial layer and later in the wood
of the trunk and major roots of mainly Populus. The larvae live beneath the bark for
2-3 years. The mature larva is 30-40 mm long; the body is yellowish-white with a
large reddish-brown head. The last winter is spent in a cocoon of bark scrapings just
under the bark or, less commonly, in the earth near the tree. The larva pupates in the
cocoon in the following spring. Adults emerge from mid-June to mid-July, rarely in
August, and leave an exit hole about 8 mm in diameter, near the base of the trunk.
The 2-3 cm long empty pupal cases can be found around the base of the tree up to
about 60 cm height (Schwenke, 1978; Arundell & Straw, 2001). The date of the
adult emergence depends on temperature and occurs from May to June. The adults
live for several weeks and pairing occurs after a few days in the crowns of the trees.
During the daylight, the adults are not very
y active; the activity takes place during the
night. The females lay their eggs (1400-1500 each) on the lower parts of the trunks
near the soil (Kolomoets et al., 1978). However, according to Schwenke (1978) the
female is sitting on the basal part of the trunk or on low branches and let fall her
small eggs on the ground or they glide into the crevices in the rough surface of the
trunk.
The neonate larvae are very mobile and enter the trunks at or below soil level
forming galleries 20-50 cm long. Development from egg to adult lasts 2 years. The
larva hibernates twice in the lower parts of the trunk. For pupation, the larvae gnaw
their way to the surface of the trunk. Pupation takes place between late April and
mid-May (Kolomoets et al., 1978; Schwenke, 1978).
7.3.2 Host finding

The moth does not seem to have a limitation in the preference on the age of the
trees. The attacks can occur on 2-year-old
d trees, as well as on 30-year-old trees.
There was no preference in the direction of the empty pupal cases, because many
were facing to the north and others to the south. Attacks also occur in trees,
surrounded by dense vegetation around the base of the tree, and even in trees, which
bases covered on all sides by Hedera helix. In general, trees surrounded by dense
vegetation showed more infestations than trees surrounded by mown grassland.
There could be more predation of pupae when vegetation is very low. Therefore,
egg-laying females may select trees surrounded by vegetation to reduce this threat
(Coleman & Boyle, 2000).
7.3.3 Host plants

The moth is widely distributed in Europe; Populus tremula is attacked in the north
and in the east, while a diversity of species is infested in the south (Schwenke,
1978). The insect is common on Populus (and occasionally on Salix, Tilia, Betula
and Fraxinus) in amenity areas and forests. The physical damage caused by S.
apiformis to the trunk has been described by several authors, but less information is
available on the role of the moth in causing dieback in the crown, or its ability to
attack and kill healthy trees. However, attacks have been described for a longer time
without any fatal effects (Arundell & Straw, 2001). In the U.K. it was found that
Populus x euramericana showed the highest rates of infestations while P. alba, P.
nigra var. Italica and P. canescens showed less or no signs of infestations. However,
despite the lack of Sesia-infestations, P. canescens had an average of 37% crown
dieback. So, in certain cases the dieback is not caused by the attacks (Arundell &
Straw, 2001).
Poplar trees showing severe dieback, defoliation or death within a growing
season, have been reported during recent years from eastern England. Here, many of
the trees were attacked by S. apiformis. Because of the larval activities, this might be
the cause of the decline in tree health. A survey in 1999 of 801 poplar trees showed
a correlation between the amount of dieback and the number of exit holes in the
trunk. However, a significant number of trees showed severe dieback but no
infestations. The data demonstrate that dieback in many trees cannot be attributed to
S. apiformis. Up to 53% of trees with severe dieback occurred in shelterbelts, and
many of these sites were situated on reclaimed land or other man-made substrates.
The area where dieback has been most prevalent is one of the hottest and driest parts
of the UK, and the reports of dieback in poplar and the apparent increase in S.
apiformis activity, follow particular dry springs and early summers in 1995 and
1996. The available evidence suggests that the deterioration in the health of poplars
in this region is not caused directly by S. apiformis, but by a combination of climate
and human influences (Arundell & Straw, 2001).
7.3.4 Natural enemies

For S. apiformis only a few parasitoids have been described such as Cryptus
pseudonymus Tschek. and Meniscus setosus Four (Ichneumonidae), but apparently
they are not very important as natural enemies (Schwenke, 1978). Leskia aurea
(Tachinidae) was reared from some mature larvae of S. apiformis infesting the
trunks of Populus in Italy (Campadelli, G. 1986).
7.3.5 Damage and control

Extensive tunnelling by S. apiformis destroys the cambial layers and outer wood in
the lower portion of the trunk. In small trees, less than 10-years old, the tunnels can
permeate the whole cross-section. Trees with such extensive damage are susceptible
to breakage at ground level. In larger trees, the larvae tunnel mainly around the
periphery and the tunnels do not cut very deeply into the wood (Schwenke, 1978).
The symptoms are presence of exit holes, sometimes with old pupal cases,
remaining in the hole at the base of trunks, lines of sawdust at the foot of the tree
and deep galleries with a circular section. Infestation is less likely to be the principal
factor causing structural instability in larger trees. However, damage by the larvae
facilitates the entry of fungi and other organisms that cause decay. The maintenance
of healthy, vigorous trees is always the best defence against insect attack. This can
be done by irrigation where necessary and the use of fertilizers. In case of heavy
infestation one could fell the trees and remove the stumps and destroy the larvae.
Control is difficult when the larvae are deep in their galleries. In extreme cases high
value trees can be sprayed at the start of insect flight and repeated again every 2-3
weeks during the flight period. A possible confusion can occur with the Poplar
clearwing moth, Paranthrene tabaniformis and the Osier weevil, Cryptorhynchus
lapathi on young trees. On older trees the infestations could be confused with those
from the Goat moth, Cossus cossus and the Large poplar longhorn beetle, Saperda
carcharias (Arundell & Straw, 2001; Schwenke, 1978).
7.4 References
Arundell, J.C. & N.A. Straw. 2001. Hornet clearwing moth (Sesia apiformis Clerck) and dieback of
poplars in Eastern England. Arboriculture Journal 25, 235-53.
Augustin, S., C. Courtin & A. Delplanque. 1993. Poplar clones effect on development, mortality and
fecundity of Chrysomela (Melasoma) populii L. and Chrysomela tremulaee F. (Col., Chysomelidae).
Journal of Applied Entomology 116,: 39-49.
Campadelli, G. 1986. [Biological notes on little known Diptera Tachinidae]. Bolletin Società
Entomologia Italia 118, 161-66.
Cavalcaselle, B. 1975. Possibilite d'emploi de produits a base de Beauveria bassiana (Bals.) Vuill. contre
les larves de quelques insectes xylophages. XXVII International Symposium on Phytopharmacy and
Phytiatry. Mededelingen Faculteit Landbouw Rijksuniversiteit Gent. 437-42.
Ceianu, I., D. Radoi and E. Constantinescu, 1967. [Paranthrene tabaniformis: studies on its biology and
control]. Institutul de Cercetari Forestiere, Bucharest.
Coleman, D.A. & M.K. Boyle. 2000. The status and ecology of the hornet moth, Sesia apiformis (Clerck)
(Lepidoptera: Sesiidae), in suburbanr South London. British Journal of Entomology Natural History
13, 99-106.
Du, J.W., S.F. Xu, X.J. Dai & X. Zhang. 1985. [Strategies for control of poplar clearwing moth
Paranthrene tabaniformis Rott. by mass trapping]. Shanghai Institute Entomology Control 5, 19-24.
Georgiev, G., 2001a. Notes on the biology and ecology of the parasitoids of the poplar clearwing moth,
Paranthrene tabaniformis (Rott.) (Lep., Sesiidae) in Bulgaria. I. Apanteles evonymellae (Bouche,
1834) (Hym., Braconidae). Journal of Applied Entomology 125, 141-45.
Georgiev, G., 2001b. Notes on the biology and ecology of the parasitoids of the poplar clearwing moth,
Paranthrene tabaniformis (Rott.) (Lep., Sesiidae) in Bulgaria. II. Eriborus terebrans (Gravenhorst,
1826) (Hym., Ichneumonidae). Journal of Applied Entomology 125, 289-92.
Kolomoets, T.P., A.M. Sinelnikova, V.M. Kovalenko & N.V. Danilkina. 1978. [The great poplar
clearwing]. Zashchita-Rastenii 1: 36.
Lastuvka, Z. & A. Lastuvka. 2001. The Sesiidae of Europe. Apollo Books, Stenstrup.
Miao, J.C., G.Y. Li, W.F. Xia & X.L. Li. 1989. [A study on the control of Paranthrene tabaniformis by
stem smearing with sticky pheromone paste]. Forest Science Techniques 8, 28-30.
Moraal, L.G., 1987. [[Apanteles evonymellaee fauna n. sp., a new parasitoid of the poplar clearwing moth,
Paranthrene tabaniformis (Hymenoptera: Braconidae; Lepidoptera: Sesiidae)]. Entomologische
Berichten Amsterdam 47, 137-39.
Moraal, L.G., 1988. [Monitoring of the poplar clearwing moth Paranthrene tabaniformis Rott.) with sex
attractant baited traps]. Nederlands
a Bosbouwtijdschrift 60, 43-49.
Moraal, L.G., 1989a. [Poplar clearwing moth, Paranthrene tabaniformis Rott., preventive control in the
nursery with carbofuran]. Nederlands Bosbouwtijdschrift 61, 70-78.
Moraal, L.G., 1989b. [Telenomus phalaenarum fauna nov. spec., as an egg parasitoid of the poplar clearwing
moth, Paranthrene tabaniformis (Hymenoptera: Scelionidae; Lepidoptera: Sesiidae)]. Entomologische
Berichten Amsterdam 49, 65-68.
Moraal, L.G., 1989c. Artificial rearing of the poplar clearwing moth, Paranthrene tabaniformis. Entomologia
Experimentalis et Applicata 52, 173-78.
Moraal, L.G., C. van der Kraan and H. van der Voet. 1993. Studies on the efficacy of the sex attractant of
Paranthrene tabaniformis Rott. (Lep., Sesiidae). Journal of Applied Entomology 116, 364-70.
Moraal, L.G., 1994. The effect of the game deterrent Wöbra on attacks by the poplar clearwing moth,
Paranthrene tabaniformis Rott. (Lep., Sesiidae). Anzeiger für Schädlingskunde, Pflanzenschutz und
Umweltschutz 67, 72-73.
Moraal, L.G., 1996. Evaluation of infestations by the poplar clearwing moth, Paranthrene tabaniformis
Rott. In: Proceedings 20th Session of the FAO International Poplar Commission, Budapest, October
1-4.
Noh, E.R., S.K. Lee and H.S. Park. 1994. [Tolerance of Populus davidiana a clones to poplar borers]. Forest
Genetics Research Institute 30, 24-29.
Schnaiderova, J., 1980. [Kleiner Pappelglasschwärmer, Paranthrene tabaniformis Rott.]. Prace Inst.
Badawczego Lesnictwa, Warszawa nr.
Schwenke, W., 1978. Die Forstschädlinge Europas. 3. Schmetterlinge. Parey, Hamburg.
Srot, M., 1966. [Einige Erkenntnisse aus der bionomie des kleinen Pappelschwärmers, Paranthrene
tabaniformis Rott., in der CSSR und seine Bekämpfung]. Prace Vulhm 32.
Wouters, L.J.A., 1977. [the use off parasitic nematodes on the control of larvae of the poplar clearwing
moth]. Populier 14, 59-60.
Wouters, L.J.A., 1979. [The control of larvae of the poplar clearwing moth on nurseries]. Populier 16, 39-
40.
8. SIRICIDAE (HORNTAILS)
M. Viitasaari & K. Heliövaara
8.1 Taxonomy and systematics

The extant taxa of Siricoidea belong to one single family, the Siricidae, and those of
Xiphydrioidea to the single family Xiphydriidae. Representatives of Siricidae are
here called horntails, and those of the Xiphydriidae wood wasps, following Quicke
(1997).
The extant taxa of the family are divided into the subfamilies Siricinae and
Tremicinae. There are more than 100 living world species. Most species are native
to the northern forests; southern extensions reach northern Africa (in central Africa
there are two species), northern Central America, Cuba, New Guinea, Indonesia, and
northern India. Introduced species are known in Australia, New Zealand, Brazil,
Chile and South Africa. No living Siricidae are native to South America, but a
siricid fossil is found in Paleocene shales in Patagonia, Argentina. This indicates that
the Siricinae were once much more widespread than they are now (Fidalgo & Smith
1987). The southernmost occurrence of living, native Siricidae in the Western
hemisphere is northern Central America which coincides with the southern extent of
the northern lineages of Conifers.
In the northern parts of Europe are represented the genera Urocerus (by three
species), Sirex (three species), Xeris (one species) and Tremex (one species) are
represented in the northern parts of Europe. The three first genera are conifer-
feeders, Tremex is associated with deciduous trees.
8.2 General biology

Horntails are in flight in late summer aand autumn, and their copulation takes place in
tree-crowns. Females lay eggs often before copulation, these eggs producing males.
Horntails oviposit in weakened trees, frequently also in newly felled logs.
Females drill deep into tree trunks to oviposit and at the same time inject mucus and
arthrospores of a symbiontic fungus. The injected mucus has phytotoxic effects; this
is demonstrated especially in Sirex noctilio (e.g. Spradbery 1973). The number of
eggs laid depends on the size of the female. In average the ovaria contain 250600
eggs, but as many as 1000 eggs are counted in a female of Urocerus augur
(Scheidter 1923). However, all eggs will not be laid.
Siricids live in symbiosis with basidiomycete fungi, and females carry spores of
the fungi and introduce the spores into host trees during oviposition. The insect-
fungus associations often damage or kill trees. In the Xiphydriidae, the presence of
reservoirs of symbiont fungi was confirmed by Kajimura (2000).
The round gallery of a horntail larva is filled with fine, packed powder. The
drying patterns in the top and base of a tree affect the proportions of larvae, which
tunnel either up or down the tree. For the same reasons, the larvae, which originated
from eggs deposited in the same drill shaft can emerge as adults at the same time but
be of very different sizes. Therefore the length and shape of the larval gallery is
related more to the performance and degree of invasion of the fungus than to the
larvae. Moulting may follow the attainment of a particular minimum size and be
attained without obligatory turning, as claimed by Rafes (1960). However, moulting
is accompanied by a change in direction iff the larvae encounter resin pockets, dense
branch nodes or other larval galleries (Madden 1981, on Sirex noctilio). Pupation
takes place in the larval gallery, usually a few centimeters from the trunk surface.
The pupation stage lasts a few weeks; the young adult gnaws its way out and often
remains in the gallery at the exit for a long time before leaving. The round exit holes
of various sizes remain visible in the bark. The development from egg to adult takes
1җ5 years (Nuorteva 1969). According to Escherich (1942), the development may
take even 6 or more years, because emerged horntails may appear in new buildings
made of wood or containing processed timber, several years after the construction of
the building. They are able to pierce solid obstacles, even lead plates (Pax 1921,
Escherich 1942).
Figure 4. Left: pupa of female horntail (Urocerus gigas) in pupal chamber, note hardly
visible frass-filled larval tunnels in the wood; right: log in cross section with abundant larval
galleries of horntails (both pictures taken by Kari Heliövaara )

Every horntail species carries only one symbiotic fungus species, but the same
fungus can be symbiotic with other horntail species. The symbiont of many siricids
is unidentified or uncertain. The fungus symbiosis is considered species specific in
principal, but because of some conflicting information it needs a final verification.
Wyniger (1974) used ordinary dried yeast for instant rearing of horntail larvae in
cooked sawdust.
A few species of the wood-rottening basidiomycetes of the genus Amylostereum
(Peniophoraceae) have been reported as symbionts of the conifer-feeding Siricinae:
Amylostereum areolatum (Fr.:Fr.) Boidin, Amylostereum chailletii (Persoon: Fries)
Boidin,,Amylostereum laevigatum (Fries : Fries) Boidin.
Of these fungi, A. areolatum (Chaill.) Boid. is known only in connection with
Sirex; A. chailletii (Pers.) Boid. occurs with Sirex and Urocerus (Gaut 1970, Talbot
1977), and A. laevigatum .with two species of Urocerus according to Tabata & Abe
(1997, 1999a).
Two species of basidiomycetes (Polyporaceae) are proposed as symbionts in the
genus Tremex (Francke-Grosmann 1938, 1939; Stillwell 1964, 1965); of those,
Cerrena unicolorr (Fr.) Murr. was isolated from the mycangia of Tremex longicollis
in Japan (Tabata & Abe 1995).
In the Xiphydriiidae the genus Xiphydria may have a shared symbiotic fungus,
but its identification is not verified. Francke-Grosmann (1967) reported a fungus
resembling the ascomycete Daldinia concentrica (Bolt.) Ces. and de Not., as the
symbiont of some European species of Xiphydria. Kajimura (2000) discovered
mycangia and mucus in adult female Xiphydria ogasawarai Matsumura woodwasps
in Japan; the females examined carried a single unidentified fungal species in their
mycangia. According to Sinadskij (1967), the imperfect fungus Melanconium
bicolorr Nees, was isolated from the tunnels of Konowia betulae, but perhaps it only
contaminated the culture?
The mucus and the fungus together have a phytotoxic effect in the wood, causing
resin flow (Spradbery 1973). This attracts more females to oviposit in the particular
tree.
8.4 Natural enemies

There are several parasitoid species in the larvae of the horntails. Some insect
parasitoids of horntails localize the eggs (Ibaliidae: Ibalia) or larvae
(Ichneumonidae: Rhyssa) of the hosts by the smell of the symbiotic fungus,
Amylostereum areolatum being more attractive to Ibalia than A. chailletii
(Spradbery 1974). In addition, the parasitic nematode Beddingia siricidicola
(Neotylenchidae) is of importance

Siricids are insects of economic importance in forestry. Most siricids attack only
damaged or dying trees, and native species are secondary pests, which are not
regarded dangerous. Because the larval tunnels are filled with tightly packed
powder, the damage is often recognized only during further processing of sawn
timber. Xiphydriids do not damage soft wood timber before the subsequent summer
after the egg laying in Fennoscandian conditions (Löyttyniemi & Uusvaara 1977).
An introduced species can cause severe damage as seen in the case of Sirex
noctilio. This species is rather harmless in Europe, but is able to kill relatively
healthy trees in Australia, South America and South Africa, aided by its phytotoxic
mucus and the symbiotic fungus (e.g. Spradbery 1973). The most destructive
outbreak occurred between 1987 and 1989 in the states of South Australia and
Victoria; more than 5 million Pinus radiata trees with a royalty value of A$10-12
million were killed (Haugen et al. 1990).
S. noctilio is the only horntail known to be able to kill rather healthy trees, and in
an outbreak of this species a high number of drills may remarkably weaken pine
trees. The flight period is in Europe in autumn, when the metabolism of trees is
minimal. In Australia the flight period is in MarchApril, during the growing season
of Pinus radiata. This may explain the importance of S. noctilio in the Australian
region (Spradbery 1973). Another apparent factor is the stress of the introduced
Pinus radiata in the hot and dry Australian climate. A National Sirex Fund was
established in Autralia in 1962 to finance survey, research, and eradication work in
an attempt to prevent further spread. Control of Sirex populations established in a
plantation is achieved by biological means using the parasitic nematode Beddingia
siricidicola (by artificially inoculating nematode cultures into Sirex-attacked trees
whence they sterilise, and are carried by the emerging Sirex adults), and parasitoid
wasps (Elliott et al. 1998). B. siricicola was first used in the biological control of
Sirex noctilio in Australia and New Zealand, by rearing and distributing the
mycetophagous cycle (Bedding & Akhurst 1974, Zondag 1979). The nematodes
inhibit the development of the ovaria and extensively diminish the number and size
of eggs. Silvicultural treatment of P. radiata plantations by thinning to maintain or
improve tree vigour is a key factor in preventing Sirex establishment or keeping
damage within acceptable levels.
8.6 References
V җ Berlin.
Escherich, K. 1942. Die Forstinsekten Mitteleuropas V.
Fidalgo, P. & Smith, D.R. 1987. A fossil Siricidae (Hymenoptera) from Argentina. Entomological News
98, 63-җ66.
Kajimura, H. 2000. Discovery of mycangia and mucus in adult female xiphydriid woodwasps
(Hymenoptera: Xiphydriidae) in Japan.- Annals of the Entomological Society of America 93, 312-17.
Madden, J.L. 1981: Egg and larval development in the woodwasp Sirex noctilio F.җ Australian Journal of
Zoology 29: 493-506.
Madden, J.L. & Coutts, M.P. 1979. The role of ffungi in the biology and ecology of woodwasps
(Hymenoptera: Siricidae). In: Insect-fungus symbiosis. Nutrition, mutualism and commensalism.җ
Batra, L.R. (Ed.), New York.
Madden, J.L. & Coutts, M.P. 1988. Sirex in Australasia. In: Dynamics of forest insect populations.җ A.A.
Berryman (Ed.), Plenum Press. New York and London.
Nuorteva, M. 1969. Beobachtungen über die Taxonomie und Bionomie von Urocerus gigas (L.) und
Sirex juvencus (L.) (Hym., Siricidae). Annales Entomologici Fennici 35: 160-68.
Pax, F. 1921. Beobachtungen über Beschädigungen
i von Bleikammern durch Holzwespen.җ Jahresheft des
Vereins für Schlesische Insektenkunde zu Breslau.
Quicke, D. 1997. Parasitic wasps. Chapman & Hall, London.
Rafes, P.M. 1960. Type of galleries of siricids and regularities in the behaviour determining the form of
its galleries in wood. Doklady Akad. Nauk SSSR 132: 478-480.
Scheidter, F. 1923. Zur Lebensweise unserer Holzwespen. Z. Schädlingsbekämpfung, Berlin 1: 89-98.
Spradbery, J.P. 1973. A comparative study of the phytotoxic effects of siricid woodwasps on conifers.-
Annals of Applied Biology 75: 309-20.
Spradbery, J.P. 1974. The responses of Ibalia species (Hymenoptera: Ibaliidae) to the fungal symbionts of
siricid wood wasp hosts. Journal of Entomology (A) 48: 217-22.
Spradbery, J.P. 1977 The oviposition biology of siricid woodwasps in Europe. Ecological Entomology 2:
225-230.
Spradbery, J.P. 1990. Predation of larval siricid woodwasps (Hymenoptera: Siricidae) by woodpeckers in
Europe. The Entomologist 109: 67-71.
Spradbery, J.P. & Kirk, A. 1978. Aspects of ecology of siricid woodwasps (Hymenoptera, Siricidae) in
Europe, North Africa and Turkey with special reference to the biological control of Sirex noctilio F.
in Australia.җ Bulletin of Entomological Research 68: 341җ-59.
Spradbery, J.P. & Kirk, A. 1981. Experimental studies on the responses of European siricid woodwasps
to host trees.җ Annals of Applied Biology 98: 179-185.
Tabata, M. & Abe, Y. 1997. Amylostereum laevigatum associated with the Japanese horntail, Urocerus
japonicus.- Mycoscience (Japan) 38, 421-27.
Tabata, M. & Abe, Y. 1999. Amylostereum laevigatum associated with a horntail, Urocerus antennatus.-
Mycoscience (Japan) 40, 535-39.
Talbot, P.H.B. 1977. The Sirex-Amylostereum-Pinus association.җ Annual Review of Phytopathology 15:
41җ-54.
Talman, P.N. 1948. O rogohvostah Sirex gigas L. I Xanthosirex tardigradus Ced. (Hymenoptera,
Siricidae). Entomol. Obozr. 30, 82 -87.
9. PHYTOBIA BETULAE
Tiina Ylioja

All extant species within the genus Phytobia Lioy (formerly Dizygomyza Hendel
(subgen. Dendromyza Hendel)) within family Agromyzidae (Diptera) feed within
the cambial cylinder of woody plants (Spencer 1976). Phytobia spp. in Europe feed
e.g. on Betula, Alnus, Salix, Populus, Corylus, Carpinus, Sorbus, Malus, Crataegus,
Prunus and Quercus (Spencer 1973, Barnes 1933, von Tschirnhaus 1992, 1993, Lee
1953). Over 50 Phytobia species have been described in the world and many tree
species demonstrate typical larval galleries of Phytobia spp., but often the link
between the insect and the host is unknown (Spencer 1973). Von Tschirnhaus (1992,
2000) synonymized Phytobia betulae Kang. with P. cambii Hendel, a species that
feeds on Salicaceae and is reported from willow and poplar plantations (Barnes
1933, Moraal 1986). Allozyme studies in Finland, however, demonstrate the
existence of a separate species that feeds in Betula sp. and Alnus sp. (Nyman et al.
2002) referred as Phytobia betulae according to Kangas (1935). P. cambii and P.
betulae are similar both in their morphology and biology.
9.2 General biology

P. betulae is univoltine and adults emerge in early summer (Kangas 1935). Adults of
P. betulae are black and ~ 4 – 5 mm long (Kangas 1935). Females oviposit into the
new current year’s shoots within the crowns of birch trees ((Betula pendula Roth and
B. pubescens Ehrh.). They position a single egg with their ovipositor under the soft
bark. Eggs are white and oval. The duration of egg stage is ~ 1 week. After hatching,
larvae mine towards the stem and downwards in the stem within the layer of
differentiating xylem in the cambial cylinder (Ylioja et al. 1998). Larval tunnels are
filled with brown parenchyma tissue and can be extremely long (17 m), typically
reaching the base of the trees (Ylioja et al. 1998). The tunnels become up to 3-4 mm
wide as larvae grow. Larvae are slender, cylindrical, white or transparent (early
instar). Larval mandibles both have two teeth, the two on the left about half in length
than those in the right. Last instar (3rd) measures 15 – 20 mm. Narrow larval tunnels
are difficult to detect up in the canopy where they start from. Typical larval tunnels
Figure 5. Upper left: ovipositing female off Phytobia betulae (photo: J. Lehto); adult
(photo: J. Lehto); upper right: larval gallery with almost invisible larva of P. betulae (photo:
J. Lehto); lower left: typical old and dark-brown longitudinal larval galleries in the veneercut
from an infested log (photo: J. Lehto); lower right:
i cross section of birch tree with cut larval
galleries in many annual rings indicating a long period of attacks (photo: M. Rousi).
contain short side-branches that are more frequent at the distal end of the tunnels
(Ylioja et al. 1998). If trees are short, larvae reverse their direction and mine
upwards and again downwards at the stem base and in the roots until they are ready
to pupate. Larvae come out through the bark in late summer or early autumn, at the
base of the stem or roots and pupate under the litter layer or deeperr in the soil. Pupae
overwinter. Barrel shaped puparium m is light-yellow or whitish.
As the life cycle repeats itself year after year larval tunnels create a record
within the annual rings of the host tree of the past abundance of larvae. Larval
tunnels visible in stem cross-sections are referred to in the literature as 'pith flecks',
'parenchyma flecks' or 'medullary spots'.
9.3 Host finding

Phytobia betulae is common throughout Finland and elsewere in Scandinavia. This
may indicate that their dispersal is efficient. Host finding is not a well known
process. Vision and olfaction and gustation likely play roles. After landing on a
shoot, females test the shoot with their ovipositor, behaviour that has been described
also for P. cambii (Coutin et al. 1990). Successful ovipositions (from which larvae
hatch) are concentrated on fast growing shoots in the upper parts of crowns (Ylioja
et al. 2002).
9.4 Host resistance

Trees of all ages can be attacked by P. betulae. No mechanisms for resistance
against P. betulae are known. Fast growth of trees benefits P. betulae: fast growing
birch genotypes are susceptible and environmental factors that enhance growth (e.g.
silvicultural practices, site quality, fertilizers) increase susceptibility (Ylioja et al.
2001, 2002, Ylioja and Rousi 2001). Years with high radial growth are especially
suitable for P. betulae larvae (Ylioja et al. 1999). Fast growing trees may provide
more suitable feeding material than slow growing trees or the quality of plant tissue
improves for the herbivore. Furthermore, if radial growth lasts longer in fast
growing trees than in slow growing trees, it allows more time for larvae to finish
their development. Absolute abundance of P. betulae in a tree increases until trees
reach the age of ~30 years, and declines as trees grow older (Ylioja et al. 1999).

Associated organisms for P. betulae are not known. Barnes (1933), however,
described an inquiline gall midge Profeltiella dizogymyzae sp. n. (Cecidomyidae) in
larval tunnels of P. cambii. There has been some concern that Phytobia sp. could
introduce plant pathogens (bacteria and ffungi) either via oviposition or the resulting
larval tunnels.
9.6 Natural enemies

Pupae of P. betulae have been parasitized by two species of Braconidae

(Hymenoptera), Symphya hians Nees. and Symphya ringens Hal., and one species of
Ichneumonidae, Cremnodes atricapillus Grav. (Moraal, 1987). Parasitoids place
their eggs probably into eggs or first instar of P. betulae. Predation on pupae has not
been studied. Presumably pupae under the litter layer and within the soils are
vulnerable to predation, e.g. by small mammals, predatory insects, and ground-
feeding birds.

Brown coloured larval tunnels are an aesthetic defect in birch wood used for
furnishings, interior design and carpentery, including furniture, floorings, doors,
panels, plywood, veneer and wooden ornaments and objects. P. betulae is harmful in
Scandinavian countries, especially in Finland, where 15% of the growing stock is
birch and there is a long traditon in processing birch. Larval tunnels lower the
quality and value of finished products and affect the efficient use of raw material.
The economic significance of P. betulae is appreciable when otherwise superior raw
material has to be downgraded due to larval tunnels. Special quality logs that are
free of P. betulae have much higher value than ordinary birch logs. On the other
hand, compared to the whole use of wood in Finnish Forest Industry the proportion
affected by P. betulae is small. Of the annual use of birch in Finland, 2% is used as
saw timber and 11% is used in plywood industry; in the latter, only a part of the
products are aimed for furnishings.
P. betulae is a common species that occurs at relatively low numbers and
without conspicuous outbreaks: e.g., 6 - 38 larvae tree-1 year-1 in a 47-year-old birch
stand (Ylioja et al. 1999). The damage it causes cannot be recognized from the
outside appearance of birch trees. P. betulae does not weaken trees for secondary
pests. Larval tunnels do not affect the physical strength of wood, but may weaken
very thin veneer. The latter has been mentioned with respect to P. cambii tunnels in
poplar used for cheese boxes in France (Régnier 1952).
There are no known methods for control of P. betulae. Growing birch mixed
with conifers has been suggested to decrease damage. Conifers could interfere with
host finding, but the lower density of larval tunnels in birch grown in mixed stands
appears to be related to decreased growth of the birch trees among conifers. Old
birch trees have most of the outer rings free of larval tunnels especially in the lower
stem, which increases the yield of veneer that is free of P. betulae tunnels.
9.8 References
Barnes, H. F. 1933. A cambium miner of basket willows (Agromyzidae) and its inquiline gall midge
(Cecidomyidae). 1933. The Annals of Applied Biology 20, 498-519.
Coutin, R., Martinez, M & Gumez, J.-L. 1990. Comportement de ponte sur Populus des femelles de
Phytobia cambii (Hendel), (Diptera, Agromyzidae). 2. Conference Internationale sur les Ravageurs
en Agriculture. 4-5-6 Decembre 1990, Versailles. Annales ANNP, Paris (France) 2, 651-54.
Kangas, E. 1935. Die Braunfleckigkeit des Birkenholzes und Ihr Urheber Dendromyza (Dizygomyza)
betulae n. sp. Vorläufige Mitteilung. Comm. Inst. For. Fenn. 22, 31 pp.
Lee, N. R. 1953. Note on a plum cambium miner (Agromyzidae). in: Rep. E. Malling Res. Sta. for 1952.
Martinez, M., Gumez, J.-L. & Munnier, P. 1985. Un ravageur mal connu: la mouche mineuse du
cambium des peupliers. Phytoma 372, 51-53.
Moraal, L.G., 1987. [Cremnodes atricapillus, a new parasitoid of the cambium miner, Phytobia cambii,
with notes on Symphya spp. (Hymenoptera: Ichneumonidae; Diptera: Agromyzidae)].
Entomologische Berichten Amsterdam 47, 5-8.
Nyman, T., Ylioja, T. & Roininen. H. 2002. Host-associated allozyme variation in tree cambium miners,
Phytobia spp. (Diptera: Agromyzidae). Heredity 89, 394-400.
Régnier, R. 1952. Importance des degats de la mineuse du cambium du peuplier pour l'industrie du
deroulage. in: Transactions of the IXth International Congress of Entomolygy, Amsterdam, August
17-24, 1951, Volume I.
Spencer, K. A. 1973. Agromyzidae (Diptera) of economic importance. Series Entomologica vol. 9. Dr. W.
Junk. B. V. Publishers, The Hague.
Spencer, K. A. 1976. The Agromyzidae (Diptera) of Fennoscandia and Denmark. Fauna Entomologica
Scandinavica. Vol. 5. Scandinavian Science Press Ltd. Klampenborg, Denmark.
von Tschirnhaus, M. 1992. Minier- und Halmfliegen (Agromyzidae, Chloropidae) und 52 weitere
Familien (Diptera) aus Malaise-fallen in Kiesgruben und einem Vorstadtgarten in Köln. Decheniana-
Beihefte 31, 445-97.
von Tschirnhaus, M. 1993. Minierfliegen (Diptera: Agromyzidae) as Malaise-Fallen in spezifishcen
Pflanzengesellschaften: Ein Weinberg der Ahr-Eiffel in Entwicklung zu einem Felsenbirnen-Gebüsch
(Cotoneastro-Amelanchieretum). Beiträge Landespflege Rheinland-Pfalz 16, 481-534.
von Tschirnhaus, M. 2000. Agromyzidae. In: Die historische Dipteren-Sammlung Carl Friedrich Ketel
Revision einer zwischen 1884 und 1903 angelegten Sammlung von Zweiflüglern (Diptera) aus
Meckelnburg-Vorpommern. Ziegler, J. & Menzel F. (Eds.) Nova Suppl. Ent. Berlin.
Ylioja, T., Hinkkanen, S., Roininen, H. & Rousi, M. 2002. Oviposition and mining by Phytobia betulae
(Diptera: Agromyzidae) in genotypes of European white birch ((Betula pendula). Agricultural and
Ylioja, T., Roininen, H., Ayres, M. P., Rousi, M. & Price, P. W. 1999. Host-driven population dynamics
in an herbivorous insect. Proc. Natl. Acad. Sci. USA. 96, 10735-40.
Ylioja, T. & Rousi, M. 2001. Soil fertility alters susceptibility of young clonal plantlets of birch ((Betula
pendula) to a dipteran stem miner. Écoscience 8, 191-98.
Ylioja, T., Saranpää, P., Roininen, H. & Rousi, M. 1998. Larval Tunnels of Phytobia betulae (Diptera:
Agromyzidae) in Birch Wood. J. Econ. Entomol. 91, 175-81.
Research needs and priorities
for Europe
Chapter 23
GENERAL CONCLUSIONS AND RESEARCH

PRIORITIES FOR BAWBILT ORGANISMS IN EUROPE
R 1, K.R. DAY 2, H.F. EVANS 3 & B. LÅNGSTRÖM 4

F. LIEUTIER
1. Université d’Orléans, B.P. 6759, F-45067 Orléans Cedex, France

2. University of Ulster, Coleraine, Northern Ireland, UK-BT52 1SA, UK
3. Forest Research, Alice Holt Lodge, Wrecclesham Farnham, Surrey GU10 4LH,
UK
4. Swedish University of Agricultural Sciences, P.O. Box 7044, S-750 07 Uppsala,
Sweden
As surmised in the introductory chapter, studies of BAWBILT organisms has been

for a long period characterized by scattered research effort in several languages all
over Europe with few opportunities for interactions accompanied by duplications of
research in some areas, and the persistence of gaps in others. Nevertheless, with
presently more than 200 experts working in the BAWBILT fields, the research
potentialities are high in Europe, although unequally distributed among the different
countries as far as the forest area is concerned (Battisti and Faccoli, chapter 2). The
present synthesis evidently reflects this diversity of approaches. Many advances
have been made in all fields of BAWBILT research, but this has been uneven. We
present below the weighing up of this synthesis and propose research priorities for
Europe in the field of BAWBILT organisms. We will first discuss each group
separately and will then conclude with proposals regarding research fields that
deserve to be developed through European collaboration in the coming years.
1. BARK BEETLES
Because of their high economic impacts, a considerable research has been devoted
to bark beetles in Europe during the last 30 years, which has resulted in very
significant progress in the knowledge of bark beetle biology in general, their
taxonomy and phylogeny, their communication systems, and their relations with the
host tree, other living organisms (associated fungi and pathogens, parasitoids,
predators, etc.) and abiotic factors. Synthetic theories have been developed
regarding their population dynamics and the risk of damage. Practical applications
541
541–552.
© 2007 Springer.
542 F. LIEUTIER, K. DAY, H. EVANS & B. LÅNGSTRÖM
have been proposed from these different research fields and some have been tested
in nature, but results are far from enabling the construction of general models and
integrated methods to evaluate damage risks and control beetle population levels
preventatively or curatively. Considerable work is needed in each of these fields, as
well as their interrelations since all the above-mentioned factors interact with each
other in bark beetle population dynamics. Moreover, investigations at the level of
individual organisms are still necessary to understand the detailed mechanisms of
the interactions, while the comprehension of population dynamics relies on studies
at the population level.
European bark beetle species and their relative systematic position need to be
defined in detail by sequencing specific regions of the DNA in phylogenetic studies,
in relation to morphological characters. For phylogeography, fast evolving genetic
markers, such as microsatellites, are needed to analyse questions related to recent
past and quarantine aspects (Stauffer, chapter 6). Only a few have been (recently)
isolated for bark beetles. Genetic studies will also be very useful to evaluate the
possibilities of beetle adaptation to new hosts (climatic change, introductions) or to
selected hosts (resistance). In taxonomy, the morphological characters of the
immature stages of many species are still unknown (Knizek and Beaver, chapter 5).
Although the most damaging species have been intensively studied, progress in
the understanding of their life cycles is needed. Indeed, as a consequence of
scattered research teams, most life cycles have been described in relation to
conditions in a particular region. This progress is needed especially in the field of
the effects of environmental factors and their interactions on the life cycles (for
example, temperature and photoperiod). It would allow the construction of models
applicable in large areas of Europe. (Sauvard, chapter 7). The model of bark beetle
population dynamics proposed for the aggregative species, built at the tree level, is
difficult to use in forest management. The reasons refer to the facts that areas
occupied by bark beetles are poorly known, due to difficulties in appreciating their
spatial distribution at the forest scale, and that no good estimator of population
levels is available (Sauvard, chapter 7). The only available estimate is the level of
damage, which is not accurate and utilizable only at an epidemic level. Also,
although the key factor (tree resistance, see Lieutier, chapter 9) has been the subject
of many studies, several other parameters of the population dynamics are still poorly
understood (mortality during dispersal, role of sister broods). The role of insect
quality is completely unknown. Capacities for modelling population dynamics of
European bark beetle species is much lower than for North American species, due to
lack of models regarding the different parameters of the dynamics (Sauvard, chapter
7). Approaches managing space-time data, such as G.I.S., will be very useful to
better understand bark beetle population dynamics, if they develop in parallel to
bark beetle population modelling.
Chemical communication is an important aspect to consider in the scope of
managing bark beetle populations and their damage to host trees. There is still a lot
to do in nearly all fields of the chemical ecology of the insect-insect and insect-plant
relationships (Byers, chapter 8). Promising new fields especially need to be
developed with regard to practical applications. These include the roles of
GENERAL CONCLUSIONS AND RESEARCH PRIORITIES 543
semiochemicals in tri-trophic interactions, and the role of non host compounds in

relation to beetle behaviour.
Knowledge of the mechanisms of conifer resistance to European bark beetles has
increased considerably during the last 20 years, but still many aspects are not
understood (Lieutier, chapter 9). The respective roles of the various defence
systems are not very clear. Information on several points of the defence
mechanisms themselves is needed, not only for the recently described systems
(induced resin flow and induced resistance), but also for the preformed defences and
the hypersensitive reaction (Lieutier, chapter 9). Sapwood defences are very poorly
understood, although they certainly play a role in the establishment of the
aggressors. Detailed mechanisms on elicitation and development of the induced
defences are almost completely unknown. Effects of these defence systems on
insects and fungi have been poorly investigated, especially for the European species.
The role of tree genetic factors merits development by focusing on the utilization of
resistance predictors at juvenile stages of the trees. Possible counter-adaptations by
beetles and fungi should also be studied. Research in relation to environmental
factors is particularly needed in relation to global change (Lieutier, chapter 9).
Considerable gaps exist both in Europe and North America regarding the effects of
these factors on the mechanisms involved in tree defence systems, be they attacks on
trees by other organisms (defoliators, pathogens), water or nutrient stress, fire,
pollution, or others. Very little information is available either regarding the relations
between silviculture (thinning, tree biodiversity, etc) and tree resistance, although
this represents a considerable component of modern forestry. Characterizing the
physiological state of the stands in relation to their susceptibility is also a necessity
prior to building risk prediction models. Almost nothing is known regarding
defence systems to bark beetle attacks in deciduous trees.
Considerable progress has been made in the knowledge of fungi from the
Ophiostomataceae family associated with barkk beetles. However, the meaning of the
association is still a matter of discussion, especially regarding the role of the fungi
and the spore load carried by the beetles in exhausting tree defences, the relations
between their pathogenicity and beetle aggressiveness, and their role in the tree
killing process (Lieutier, chapter 9; Kirisits, chapter 10). Relatively few associations
have already been studied and research is needed in a large array of models if we
want to clarify the debate (Kirisits, chapter 10). Moreover, certainly a large number
of Ophiostoma species are still to be discovered and further surveys will improve the
knowledge on taxonomy, ecology and biogeography of these organisms. In this
task, as for the bark beetles themselves, the use of molecular markers will help
considerably. The species composition of the fungal flora associated with a given
bark beetle species varies considerably between localities, even over short distances,
and the factors driving these variations are still poorly known (Kirisits, chapter 10).
As in North America, research on parasitoids and predators of European bark
beetles has been concentrated on a few beetle species, leaving the natural enemy
complex of others almost completely unknown (Kenis et al., chapter 11). This is a
regrettable gap because most natural enemies are not host- or prey-specific and
knowledge on enemies of secondary beetles would help in understanding the natural
control of the economically important species. Moreover, research has been more
focused on parasitoids, whereas predators have been largely under-investigated,

although they also have large potential for natural regulation of beetle populations
(Kenis et al., chapter 11). The available information differs largely between species
in the same group. The role of natural enemies in bark beetle population dynamics
needs to be better assessed. Except for the D. micans / R. grandis relationships, few
attempts to use the natural enemies have been made in the field. Classical biological
control must be considered, owing to the possibility of introductions of exotic bark
beetle species to Europe. However, because presently all European bark beetle pests
are indigenous, biological control by favouring indigenous natural enemies seems
most promising. Taxonomy and identification studies for natural parasitoids and
predators are also an important field that needs to be developed, since identification
is a crucial step in any biological control program (Kenis et al., chapter 11). Many
species of pathogens have been described, but very little is known on their impacts
on populations and effects on the hosts (Wegensteiner, chapter 12). This
information is needed, in relation to the period of the year, host generation or
environmental factors. Many pathogens (viruses, fungi, microsporidia) seem
promising for the biological control of bark beetles, but methods for artificially
contaminating beetles must be investigated, as well as infectivity of the pathogens
for the non-target organisms, before envisaging practical control aspects.
2. WEEVILS
Among the twenty-two species of Curculionidae which are listed in this volume as
bark and wood boring weevils of living trees in Europe, only three genera are likely
to be considered pests of trees and only one species is genuinely a persistent
problem in forestry. Species of the genus Pissodes are capable of killing trees
although their role as primary or secondary pests requires further clarification.
Species of Otiorrhynchus can seriously damage seedling crops, but such reports are
rare and localised in Europe. Nevertheless, further investigation of Otiorrhynchus
articus and O. nodosus would seem prudent since current understanding rests largely
on the better known surrogate, O. sulcatus.
Hylobius abietis is arguably the single most economically important forest
weevil pest in Europe, hence much of the existing literature and a significant part of
this volume is devoted to it. How far has this research effort informed current forest
management? The goal of successfully replacing the use of insecticides for seedling
protection in all plantation forests and at no additional cost may seem a long way
off. However, much progress has been made in suggesting measures which may
improve seedling survival, as several chapters emphasise (Långström and Day,
chapter 19; Day et al. chapter 14; Schlyter, chapter 15; Wainhouse, chapter 16;
Kenis et al., chapter 18). It is clearly already possible to achieve adequate seedling
protection by combining silvicultural methods with physical barriers, but hitherto,
the relatively high cost has not encouraged the universal implementation of this
approach. Changes to the unit cost and effectiveness of physical barriers seems now
to give cause for optimism. A new type of barrier consisting of a flexible coating
containing mineral particles and applied to the lower part of the seedling stem can
provide good protection at low cost through mass use and machine production (G.
Nordlander, pers. comm.). With rational aapplication, low cost per plant and long-
lasting protection, this approach could be successful.
The investigation of silvicultural management of pine weevil damage has paid
dividends in recent years. The Swedish research effort, for example, has
demonstrated through carefully designed field experiments to what extent seedling
conifers can be protected, att what cost, and the mechanisms for this protection from
an ecological perspective. Continued experimentation on weevil behaviour,
physiology and performance are vital to understanding the processes which will
eventually underpin an effective and flexible pest management system.
Important aspects of the biology of all BAWBILT weevils still require
investigation. As well as Hylobius, adults of Pissodes spp. have been poorly studied,
especially in the field. Very little is known about the chemical relationships between
Pissodes species and their hosts. This has proved an important area of knowledge
supporting the management of Pissodes pests in N America and should also be
given attention in Europe (Day et al., chapter 14). Should a sex pheromone be
identified for Hylobius, it would be a useful route for testing a low-volatile
compound for behavioural modification (Schlyter, chapter 15).
The plant-insect interface will continue to be a priority target of research.
Dispersal and reproduction of Hylobius are both dependent on adult feeding, which
in turn must be selective in order to acquire sufficient nitrogen. To some extent, the
main bark defensive system – resin – mediates the pattern of feeding (Wainhouse,
chapter 16). Bark feeding therefore has two important outcomes – one is the amount
of short-term seedling mortality it generates and the other is the longer-term effect
of adult nutrition on subsequent population growth (and the probability of exporting
future weevil problems to other sites).
The relationships between consumption of bark, reproduction, and the
development and resorption of flight muscles and migration are poorly understood.
How does bark feeding relate to seedling damage and are there conditions at a site
that mitigate feeding? Where do weevils occur in the forest environment and where
do they feed? These are rather obvious but, as yet, unanswered questions. The
ecology of larval and maturation feeding needs to be better understood so the
outcomes of reproductive success and damage to seedlings can be modelled.
Seedling conifers seem very vulnerable to attack by pine weevils, but even small
degrees of resistance may play a part in the future integrated management of this
pest. The underlying mechanisms of resistance to feeding need further exploration;
existing research indicates a role for both induced resistance and tolerance but field
and laboratory investigations are needed to show how plant phenotype influences
resistance expression (Wainhouse chapter 16). The effect of seedling size on the
damage sustained from weevil attack is one of a number of phenotypic
characteristics that are only partially understood (Wainhouse, chapter 16; Långström
and Day, chapter 19). The structure and activity of antifeedants deserve more
attention; adult feeding decisions are partly based on contact chemoreception , and
may be redirected (Schlyter, chapter 15).
Conditions in the conifer stump which affect the number of weevils emerging
from a site, have received some attention, butt not enough. It is here that most of the
weevil life cycle is played out yet we know little about the range of factors which
determine the performance of weevils in this environment. Field experiments are
needed to verify the possibility of high larval mortality in the early stage of root-
stump colonisation (Wainhouse, chapter 16).
Populations of Hylobius abietis are highly damaging to forest trees, but they are
also elusive and difficult to track in time and space. Our knowledge of their
population dynamics is still rudimentary, yet this knowledge is essential to
predicting the potential impact of management and to fully understanding the
relationship between silviculture and the impact of weevils on transplanted
seedlings. As we have implied, larval development will require more intensive study
and overall levels of larval mortality (including that attributable to natural enemies)
must be investigated more holistically. Eventually, such knowledge will contribute
to the estimation of site-related adult production and the subsequent risks to
neighbouring and more distant sites.
Existing data and new experimental data should be harnessed to generate useful,
thermally-dependent developmental models for larvae and adults so that the
presence of weevils on a clear cut can be described by thermal data. Such models
will require a stochastic approach, so that the ranges of temperature that might be
dependent on larval position in the soil or site structural factors, can be readily
incorporated and can help predict the outcome in terms of weevil phenology or
performance. Risk rating systems should be based upon better, spatially-explicit
population models which can express the results of new research on, for example,
the population consequences of insect-plant interactions, the effect of thermal
environment on insect development, or the influence of silvicultural interventions.
Work will continue on finding new and improved tools for suppressing weevil
populations or limiting their access to forestt seedlings. Many of these tools have
commercial potential. Some, like natural enemies, could be sustainable solutions.
The role of parasitoids and other natural enemies in regulating populations of their
weevil hosts is unclear (Kenis et al., chapter 18). While the overall impact of
parasitoids on populations of Pissodes is likely to be considerable and on Hylobius
or Otiorrhynchus, much less (Kenis et al., chapter 18), there is scope for integrating
small gains in host population reduction with other
t control strategies. In particular,
design and implementation of strategies for enhancing parasitoid impact through
silvicultural management should be a priority. On the subject of the use of biocides,
there is further potential for the formulation of commercially competitive nematode
products for application against Hylobius.
In conclusion, the literature on BAWBILT weevils, particularly Hylobius, is
considerable but only in recent years has the pace of research accelerated in order
meet the demands of forest protection and forest environmental policy. This research
has created a platform in several novel and promising areas. It is from these that
further research results will need to emerge in order to successfully tackle one of the
major challenges to Europe’s forest industry.
3. BUPRESTIDAE AND CERAMBYCIDAE

The two beetle families Buprestidae and Cerambycidae offer interesting contrasts in
their biologies and, particularly, their pest statuses within the overall BAWBILT
group of organisms. Although there are pest representatives in both families, either
in their own rights or as vectors of damaging organisms (e.g. cerambycids in the
genus Monochamus are vectors of the highly destructive pinewood nematode,
Bursaphelenchus xylophilus), the majority of representatives are scarce and, often,
of biodiversity significance.
Among the pest representatives in the Buprestidae, most attention has been paid
in central and southern parts of Europe where they can be quite destructive and have
been linked to climate change. With the exception of the genus Phaenops, all are
pests of broadleaved trees. In relation to future studies of this group an important
consideration should be the interface between pest status and biodiversity status.
There is clearly a fine balance between these two extremes and there is too little
information on the environmental and population dynamics characteristics that
determines the final status of a given species. In addition, interaction with other
groups of BAWBILT organisms, especially the Scolytidae, requires attention. The
fact that some buprestids have moved internationally and are causing significant
damage in new regions of the world (e.g. Agrilus planipennis is killing ash trees in
north America after its introduction from China) is also a subject for future research.
Cerambycidae are ubiquitous components off natural and managed forests and are
generally at relatively low levels, especially when there is relatively little weakened
or freshly killed material present. In this sense they tend to be regarded as “technical
pests” causing damage to the final wood product rather than killing trees in their
own right. However, the switch to attacking living trees, albeit usually when they are
weakened, is a characteristic that requires further study both in their native ranges
and when they have established in new locations, e.g. Tetropium fuscum in Nova
Scotia. Other species, exemplified by Phorocantha semipunctata and Anoplophora
glabripennis have caused significant damage to living trees as they have moved
around the world in international trade and have established in new locations. More
studies are needed of the nature of the interactions that lead to successful
establishment in a given area and, particularly, to the factors that lead to tree damage
and mortality.
Although both families of beetle are regarded as being associated with stressed
trees, the question of climate change and increased availability of exotic tree hosts
may change this perception over time. Research into the future effects of differing
climatic conditions, compounded with local site characteristics should be studied at
a European scale, especially since the range of climatic and environmental
conditions in this area is already quite large.
4. NON-COLEOPTERAN BAWBILT ORGANISMS

In comparison with bark beetles and pine weevils, the species treated under part 4
are clearly less important as pests on living trees. They seldom cause tree mortality
and the growth losses resulting from attacks by some of the species are mostly
modest and transient. The horntails constitute one exception to this statement, as
they - outside of Europe - have become serious pests in pine plantations in the
southern hemisphere. The main damage caused by this diverse group of ”other”
BAWBILT-organisms is related to the wood formation of the growing trees where
they may inflict severe and lasting disturbances that eventually will affect the quality
of the end product, the harvestable timber. Thus, their damage is in fact comparable
to that caused by “true” timber pests i.e. insects that degrade the timber quality after
the trees have been felled. As for most timber
m pests, there are few, if any, control
options available against current attacks by any of these other BAWBILT
organisms. The main emphasis in research and practical forest protection should
hence be on preventing damage from occurring rather than controlling ongoing
attacks. Understanding the population dynamics of the pest species in question as
well as the host resistance mechanisms are crucial for any forest protection strategy
and especially those based mainly on damage prevention.
As has been shown in part 4, the general biology of these BAWBILT pests is
fairly well known but their population dynamics are still poorly understood. In most
of these species, population regulation seems to be more of the bottom-up-type. i.e.
host factors may be more important than natural enemies in the population dynamics
of these, and probably most of the species described in this book.
Typically, most BAWBILT species live in an intimate relationship with their
host plants, as most of the life cycle is spent inside the living plants, mainly in the
phloem but sometimes also in the xylem of the stem, branches, shoots or buds. Thus,
the pest-host interaction becomes central in the understanding of the population
dynamics of the BAWBILT pests. Although considerable knowledge has been
gathered in recent decades about host defence strategies and systems, much remains
to be discovered regarding the genetic, physiological and chemical basis for host
resistance. Considering the powerful study tools that are becoming available via
biotechnological research, it seems reasonable to assume that, given the research
opportunities, we could elucidate much of the physiological and chemical properties
relating to pest resistance in different host species, and that this could open up new
avenues for selection or breeding of more resistant varieties, or even immunity to
pests via genetic engineering.
On the other hand, processes involved in host and mate finding of the pest
species, offer tools for monitoring and disturbing pest populations. Sexual
pheromones have been identified for most of the lepidopteran species included here,
and probably exist for all of them. The host finding and selection processes are still
poorly understood in all these species, but deserve more attention.
At least in some of these species ((Aradus, Dioryctria and Phytobia), cultural
practice and stand composition seem to play important roles in damage occurrence.
Mixed stands seem to suffer less damage, but the reasons for this are still unknown,
although mixed stands are thought to support more natural enemies which in turn
may stabilize pest populations. Site quality and stand treatment may play different
roles for different pests, as the occurrence of Aradus-damage clearly decreases with
increasing soil fertility, whereas the pattern is rather the opposite in Dioryctria.
These examples show that there is a potential for preventive measures incorporating
novel forest management schemes promoting biological control and increased tree
vigour against BAWBILT pests.
5. RESEARCH PRIORITIES AT THE EUROPEAN LEVEL

Research prospects that we consider essential in the BAWBILT domain in relation
to the present needs of society, and that should be developed in a cooperative
approach at the European level, can be grouped into two main areas. The first
concerns the further development of the most essential and promising fields which
have been identified by consideration of accumulated research, including the need to
fill important and fundamental gaps that impede our understanding of the
mechanisms of population dynamics. The second is concerned with new situations,
particularly in the socio-economic sphere, that characterize the beginning of the 21st
century.
5.1. Promising fields to be developed and fundamental

f gaps to be filled, arising from
previous research
5.1.1. Better understanding population dynamics of European BAWBILT
A good knowledge of its population dynamics will always be the key to open the
door on damage risk evaluation and control methods of a pest. In none of the
European BAWBILT species, is this knowledge sufficient. Factors appearing to
play a key-role have been studied more thoroughly, such as tree resistance for most
bark beetle pest species. However, rarely is one factor alone a sufficient explanation
for observed insect population dynamics. Other factors suspected of playing at least
an important secondary role have been largely underestimated for all BAWBILT.
This is especially the case for natural enemies and diseases, which would be worthy
of a joint research effort in order to take into account a wide range of natural
situations. Similarly, the quality of both the host and the insect merits rapid and
joint consideration by the community of European BAWBILT scientists. The
nutritional quality of the host has almost never been considered in North America
and research on this factor in Europe has just begun on H. abietis (Wainhouse,
chapter 16), although certain aspects of the tree constitutive defences may be
considered in this direction (Lieutier, chapter 9). Research on qualitative variations
in beetle populations, especially by comparing endemic and epidemic populations,
should give very useful information on the role of insect quality in population
dynamics. This approach has started recently on bark beetles in both North America
((D. rufipennis) and Europe ((I. typographus) and has concerned the morphometry,
the behaviour, the genetics and the associatedd fungi of the beetles (Wallin and Raffa,
2004; Sallé, 2004).
There are thus several parameters that deserve to be considered for a better
understanding of population dynamics of European BAWBILT organisms. In such
a situation, a holistic approach at a European scale, taking into account several
factors which possibly interfere with population dynamics, is recommended. We
suggest that one BAWBILT model be chosen for which all these factors will be
studied simultaneously and at a wide scale. Considering the accumulated
knowledge, the available methodologies, and the economic interest, I. typographus
and T. piniperda seem the best candidates.
In relation to beetle population dynamics, a reliable and accurate method of

rapidly estimating the beetle population level is urgently needed. Owing to the
diversity of the natural situations, it can only result from a European cooperative
program. Looking for indicators related to qualitative characteristics of the
populations such as those cited above, might be a promising research track.
5.1.2. To define pan-European policies and develop control methods (genetic

selection, silviculture, IPM).
Damaging BAWBILT pest organisms ignore boundaries, and damage often extends
over areas spanning several different countries at the same time or consecutively.
There is a crucial need for building common control procedures and defining pan-
European policies. A first step towards this objective has been met within the
BAWBILT EU project through a tentative approach to estimating damage on a
common basis and to synthesize control methods (Grégoire and Evans, chapter 4).
Future exchanges of information and integration of experiences from various
European countries, parallel to improvements in knowledge of pest population
dynamics, are needed to go further and to develop procedures of wide applicability.
It is also essential, probably as the next step, to improve quantification of the cost
and effectiveness of pest management. Intensive cooperation with socio-economists
is evidently needed.
Regarding control itself, very few field assays have been made and only in some
localities. In particular, IPM approaches on Hylobius control that have been
developed in Sweden and UK should be extended to other parts of Europe
(Långström and Day, chapter 19). Tree resistance offers several promising
perspectives for applications in both genetic selection and silviculture (Lieutier,
chapter 9). Chemical indicators of Norway spruce and Scots pine resistance to bark
beetles should be thoroughly studied and the findings extended to several conifer
species with research emphasis on their applicability at the juvenile stage of the tree.
Resistance is known to be expressed both genetically and environmentally, the latter
bring modifiable through silvicultural manipulation. The potential for research here
justifies the development of cooperative projects aimed at defining the possibilities
of manipulating tree resistance through silviculture. Basic research is, however
needed in the field of the relationships between tree resistance and environmental
factors (Lieutier, chapter 9 and see 5.2.1).
5.1.3 Filling gaps regarding BAWBILT species of secondary economic importance

and species of broadleaves trees
The number of published papers on the different European BAWBILT species is
related directly to the economic importance of the organisms. This situation is
particularly evident for bark beetles for which one fifth of the research papers deals
with I. typographus and half with 6 species only (Sauvard, chapter 7). It is even
more striking for weevils where a very large majority of research papers is devoted
to H. abietis (Day et al., chapter 14). This seems logical because there is a crucial
need to control dangerous species, and the consequent higher likelihood of obtaining
funding to study these species. The consequences, however, are that only the
biology of these dangerous species is known in detail. Detailed information on less

damaging species is often dramatically missing, although it would be very useful for
comparisons and generalization, and would certainly also lead to a better
understanding of the reasons for the aggressiveness of the dangerous species. There
is therefore a wide and regrettable gap in our knowledge of secondary BAWBILT
organisms, and this situation is the same everywhere in the world. Similarly, the
role of BAWBILT organisms in deciduous stands has attracted little attention, due to
their much lower pest status than in conifer stands. It is especially true that
resistance mechanisms in these trees are completely unknown with regard to attacks
by BAWBILT organisms.
5.2. New fields to explore in relation to the emergence of a new social context
5.2.1 The environmental dimension and global change
Placing BAWBILT research in the context of global change is essential, since
relations between environment and society are global priorities at the beginning of
the 21stt century. In all fields considered in the different chapters of this synthesis,
several aspects still need to be studied to understand BAWBILT basic biology, their
relations with other organisms, and their population dynamics. However, almost all
chapters have also emphasized that information regarding the effects of
environmental factors represent a large gap. This gap is regrettable in the present
context. The environmental dimension should be taken into account while
improving knowledge on various topics, and all fields that have been presented
should be re-considered under the scope of environmental changes. Present models
of BAWBILT population dynamics, although taking some account of climatic
conditions, do not generally consider a changing environment, particularly in
prediction of future impacts and risks to forests. Taking into consideration this new
dimension at a large geographic scale should lead to more dynamic models.
However, a consideration of the environmental dimension in BAWBILT research
supposes new basic research on the insects, their associated organisms, their natural
enemies, their host trees, and the relations between these different biological
components.
5.2.2. Forest sustainability, wood production, biodiversity and conservation

The assurance that wood production is compatible with the social functions of
forests and the preservation of biodiversity in a sustainable forest environment is
also one of the priorities of the 21stt century. BAWBILT research is particularly
concerned with this aspect. BAWBILT comprises comprise many insects that
impede wood production or social functions of the forest (the “classical pests”). In
this way, they can compromise forest sustainability and biodiversity, especially in
forests that have been actively managed for a long time, which includes the major
part of the European forest estates. Studies dealing with relations between
outbreaks, damage, and forest sustainability should be initiated. The temporal and
spatial scales considered in such studies certainly represent an important factor to
consider, which justifies a pan-European project over several years. Biodiversity
aspects are also another dimension where BAWBILT organisms are considered as
pests. There is already experimental evidence that plant (especially tree)
biodiversity can affect damage by BAWBILT organisms. However, there is a large
field of research that still remains unexplored. On the other hand, some species that
are pests in one region of Europe can be a significant factor in forest sustainability
or an important component of biodiversity and conservation in another region.
Moreover, even in a similar location, classical pests have relationships with
biodiversity as they open the succession leading to wood decomposition. In
addition, an insect is a pest only when it reaches a certain population level. During
its endemic phases, it can even play an important role in maintaining biodiversity.
Even though they are often mentioned in the literature, the relations between these
different situations have been rarely studied thoroughly.
5.2.3. Emerging pest problems

Another challenge for European forest research is the emergence of new pest
problems, for which BAWBILT organisms are frequently responsible. Such
problems can result from the rapid expansion of markets between continents, leading
to accidentally introduced insects or to voluntarily introduced hosts. New pest
problems can also emerge from climatic changes that modify the geographic
distributions of the BAWBILT organisms and their associates. In the latter case, the
problem overlaps that of climatic change presented above. Pests can be insects
themselves, such as Phoracantha species that have followed their Eucalyptus hosts
in Southern Europe, or the recently introduced species of Anoplophora that have
established on many indigenous hardwood tree species in Central and southern
Europe. Pests can also be other organisms that are vectored by BAWBILT
organisms. In this situation, the BAWBILT vector can be introduced while carrying
the pest, or can be an indigenous insect collecting an introduced pest, such as for the
pinewood nematode Bursaphelenchus xylophilus recently introduced in Southern
Portugal, probably with its original vector but which adapted to the local vector
Monochamus galloprovincialis. All present or potential emerging pest problems
must be considered very seriously when they represent high threats for European
forests. Research on the BAWBILT pests that have recently been introduced in
Europe is urgently needed. Preventative studies should also be developed for alien
species likely to being introduced to determine the possible routes of introduction
and extension, the possibilities for their establishment, the risks of damage, and the
available control methods. In all cases, research must be conducted at the level of
the whole of Europe, in collaboration with the countries of origin.
6. REFERENCES
Sallé, A. 2004. Caractéristiques génétiques, morphométriques et flore fongique associée à Ips
typographus (Coleoptera : Scolytinae), application à l'estimation des niveaux de population du
ravageur. Thèse Université d’Orléans: Physiologie et biologie des organismes.
Wallin, K.F. & Raffa, K.F. 2004. Feedback between individual host selection behavior and population
dynamics in an eruptive herbivore. Ecological Monographs, 74, 1001-16.
Index of scientific names
Abies ..... 18, 119, 137, 148, 152, 154, 156, 157, Agrilus viridis ...5, 449, 451, 454, 455, 475, 476,
202, 250, 325, 326, 332, 339, 416, 461, 462 492, 493, 494
Abies alba (Abies pectinata) ...18, 148, 202, 325, Ailanthus ......................................................... 519
326, 332, 339 Aleochara ........................................................ 245
Abies amabilis ................................................ 156 Aleochara sparsa ............................................ 245
Abies concolorr ........18, 119, 152, 154, 159, 169 Allantonema ................................................... 400
Abies grandis ....... 149, 154, 155, 156, 157, 159, Allantonema miribile ..................................... 400
160, 166, 169, 339 Allodorus ........................................396, 398, 403
Abies lasiocarpa ............................................... 18 Allodorus lepidus ...................................396, 398
Abies magnifica ............................................. 119 Allonyx ........................................................... 242
Abies nobilis ............................................. 18, 339 Allonyx quadrimaculatus ............................... 242
Abies nordmanniana ........................18, 326, 339 Alnus ........................................ 18, 250, 325, 539
Abies sibirica ............................................ 18, 157 Ambrosiella ..184, 192, 194, 195, 197, 198, 199,
Absyrtus .......................................................... 487 200, 204, 205, 206, 210, 211, 212, 213, 214,
Absyrtus vicinator .......................................... 487 222
Acanthocinus .......................................... 461, 483 Ambrosiella brunneaa ...................................... 194
Acanthocinus aedilis ...................................... 461 Ambrosiella ferruginea 194, 195, 198, 199, 213,
Acanthocinus griseus ..................................... 483 214
Acanthospora .................................................. 305 Ambrosiella gnathotrichi
t ............................... 194
Acanthospora crypturgi ................................. 305 Ambrosiella hartigii .............. 194, 198, 199, 213
Acer ......... 18, 118, 461, 462, 463, 517, 519, 522 Ambrosiella ips ......................................194, 206
Acer negundo ................................................. 463 Ambrosiella macrospora 194, 197, 198, 205, 222
Acer pseudoplatanus ................................ 18, 356 Ambrosiella sulcati a ........................................ 194
Acinetobacter ................................................. 297 Ambrosiella sulfurea ............. 194, 198, 199, 213
Acinetobacter calcoacetius ............................ 297 Ambrosiella tingens ...... 195, 206, 210, 212, 222
Acrocormus
m .................................................... 254 Ambrosiella xylebori ..................................... 194
Acrocormus semifasciatus ............................. 254 Ambrosiozyma ............................................... 199
Aerobacter ...................................................... 296 Ambrosiozyma monospora ........................... 199
Aerobacter scolyti .......................................... 296 Amylostereum m ........................................ 536, 537
Aesculus .......................................................... 121 Amylostereum areolatum ......................536, 537
Aesculus .................................................... 18, 517 Amylostereum chailletii .........................536, 537
Aesculus octandraa .......................................... 121 Amylostereum laevigatum m ............................ 536
Aggelma ......................................................... 491 Ancistrocerusr .................................................. 516
Aggelma agrili ................................................ 491 Ancistrocerus gazella ..................................... 516
Aggelma spiracularis ..................................... 491 Ancistrocerus ichneumonideus ..................... 516
Agrilocida .......................................254, 491, 493 Angophora ...................................................... 462
Agrilocida ferrierei .........................254, 491, 493 Anisandrus dispar: see Xyleborus dispar
Agrilus ..5, 21, 22, 23, 25, 38, 42, 45, 49, 54, 58, Anoplophora ...3, 5, 12, 459, 460, 461, 476, 486,
448, 449, 450, 451, 454, 455, 457, 475, 490, 488, 495
491, 492, 493, 494, 495 Anoplophora chinensis ..... 5, 462, 476, 486, 488
Agrilus angustulus ... 5, 451, 454, 455, 475, 476, Anoplophora glabripennis 5, 459, 460, 461, 462,
490, 491, 492, 493 470, 476, 486, 488
Agrilus anxius ................................................ 450 Anoplophora macularia ................................. 462
Agrilus ater ..................................................... 451 Anthaxiaa .......................................................... 493
Agrilus biguttatus ... 5, 21, 22, 25, 38, 42, 45, 49, Anthonomus .......................... 319, 321, 325, 358
54, 58, 448, 449, 454, 455, 457, 475, 490, Anthonomus grandis .... 154, 155, 156, 157, 159,
491, 492, 493 160, 166, 169, 339, 358
Agrilus bilineatus ........................................... 450 Anthonomus rectirostris ................................ 321
Agrilus elongatus ........................................... 451 Apanteles ........................................511, 523, 528
Agrilus planipennis ........................................ 495 Apanteles evonymellae .................................. 528
Agrilus populneus (Agrilus suvorovi) ...... 5, 23, Apanteles lacteipennis ................................... 523
449, 451, 457, 475, 490, 491, 492, 493 Apanteles laevigatus ...................................... 523
Agrilus sinuatus .............................................. 451 Apanteles lineipes .......................................... 511
Agrilus sulcicollis ..................................451, 455 Apechthis ........................................................ 487
Apechthis capulifera ...................................... 487
553
554 INDEX OF SCIENTIFIC NAMES
Apeliomaa ........................................................ 491 Baryscapus hylesini .......................255, 491, 493

Apelioma pteromalinum m ................................ 491 Bathyplectes ................................................... 490
Aprostocetus ........................................... 249, 488 Bdellaa .............................................................. 506
Aprostocetus hedqvisti ................................... 249 Bdella longicornis .......................................... 506
Aradus ... 5, 23, 25, 502, 503, 504, 505, 506, 507 Beauveria ......294, 298, 299, 300, 301, 302, 399,
Aradus cinnamomeus .. 5, 23, 25, 502, 503, 504, 411, 463, 468, 520, 529
505, 506, 507 Beauveria bassiana ....... 294, 298, 300, 301, 302,
Arhopalus .......................... 5, 461, 475, 476, 479 303, 304, 399, 411, 463, 468, 520, 529
Arhopalus rusticus ............ 5, 461, 475, 476, 477 Beauveria brongniartii .. 302, 303, 400, 411, 463
Arhopalus tristis ............................................. 461 Beauveria caledonica .............................299, 300
Arion ............................................................... 359 Beddingia ................................................537, 538
Armillaria .......156, 384, 385, 386, 409, 468, 482 Beddingia siricidicola ............................537, 538
Armillaria mellea ...........................156, 384, 482 Betula ..... 18, 117, 118, 119, 213, 450, 531, 539,
Aromiaa ............................................................ 461 540
Aromia moschata ........................................... 461 Betula pendula ................. 18, 117, 119, 356, 540
Ascogasterr .............................................. 489, 490 Betula pubescens ...................................... 18, 540
Ascogaster varipes .................................489, 490 Billaea ....................480, 481, 482, 484, 485, 488
Aspergillus ...................................................... 523 Billaea adelphaa ...............................480, 485, 488
Aspergillus parasiticu
a s ................................... 523 Billaea irrorataa ........................................ 484, 488
Aspilota ................................................... 396, 397 Billaea triangulifera f ........................480, 481, 482
Atanycolus ....477, 478, 480, 481, 482, 488, 489, Bitoma .....................................................238, 242
490, 492, 493, 494 Bitoma crenata ................................................ 242
Atanycolus denigrator ....................480, 482, 488 Blacus .............................................................. 246
Atanycolus genalis 477, 478, 480, 481, 482, 489, Blacus humilis ................................................ 246
490 Blastesthia ...............................................510, 511
Atanycolus initiator ........................477, 481, 489 Blastesthia turionana
u a ...................................... 510
Atanycolus ivanowi .......................480, 490, 492 Blastesthia turionell
u a ...................................... 511
Atanycolus neesii ...........................480, 488, 490 Borrelinavirus ................................................. 520
Atanycolus sculpturatus ................................. 490 Borrelinavirus cossi ........................................ 520
Athous ..................................................... 477, 482 Brachistes ........................................................ 403
Athous subfuscus
f ........................................... 482 Brachyopaa ....................................................... 399
Atractodes ....................................................... 405 Brachytemnus .................................319, 321, 324
Atractogaster ..........................................490, 492 Brachytemnus porcatus ..........................321, 324
Atractogaster semisculptus .................... 490, 492 Bracon .. 246, 252, 396, 397, 398, 405, 407, 410,
Aulogymnus ................................................... 255 436, 488, 489, 490, 511
Aulogymnus bivestigatus .............................. 255 Bracon brachycerus r ................................ 396, 398
Aulonium ................................................ 238, 242 Bracon caudatus ............................................. 252
Aulonium ruficorne ........................................ 242 Bracon discoideus .......................................... 488
Aulonium trisulcum ....................................... 242 Bracon hylobii ......246, 396, 397, 398, 405, 407,
Aureobasidium m ....................................... 383, 385 436
Aureobasidium pullulans ....................... 383, 385 Bracon immutator .......................................... 410
Avetianella .............................................. 466, 486 Bracon instabilis ............................................. 246
Avetianella longoi .................................. 466, 486 Bracon maculiger ........................................... 489
Bacillus ..........112, 292, 293, 296, 297, 520, 524 Bracon osculator ............................................. 246
Bacillus alvei .................................................. 297 Bracon palpebrator .........................246, 252, 405
Bacillus cereus ........................................ 112, 297 Bracon praetermissus .............................405, 407
Bacillus coagulans ......................................... 296 Bracon ratzeburgii .......................................... 252
Bacillus megaterium m ...................................... 297 Bracon stabilis ................................246, 252, 511
Bacillus pumilus ............................................. 296 Bracon tenuicornis ......................................... 252
Bacillus subtilis .............................................. 296 Bracon variator ............................................... 490
Bacillus thuringiensis ... 292, 293, 294, 297, 520, Broscus ........................................................... 410
524 Bruchophagus ................................................. 256
Baculovirus ..................................................... 295 Bruchophagus maurus ................................... 256
Baranisobas .................................................... 405 Bupalus ........................................................... 156
Baranisobas ridibundus .................................. 405 Bupalus piniaria ............................................. 156
Baryscapus ............................. 255, 491, 493, 494 Bursaphelenchus ............................................ 467
Baryscapus agrilorum ....................491, 493, 494 Bursaphelenchus xylophilus ..................467, 471
INDEX OF SCIENTIFIC NAMES 555
Calathus .......................................................... 359 Ceratocystis autographa a ........ 203, 204, 212, 213
Callibracon ..................................................... 466 Ceratocystis clavigera (Ophiostoma clavigerum)
Callibracon limbatus ...................................... 466 ..................................................................... 159
Callidium ................................................ 461, 462 Ceratocystis coerulescensr ......................205, 210
Callidium violaceum ...................................... 461 Ceratocystis fagacearum ................184, 189, 191
Calodromius ........................................... 238, 242 Ceratocystis fimbriata .................................... 191
Calodromius spilotus ..................................... 242 Ceratocystis laricicola .. 192, 193, 194, 200, 206,
Calosota .........245, 251, 406, 408, 483, 491, 494 225, 226
Calosota acron ................................................ 483 Ceratocystis leucocarpa .........................202, 209
Calosota aestivalis .245, 251, 406, 408, 491, 494 Ceratocystis polonica ... 140, 146, 153, 155, 160,
Calosota anguinalis ........................................ 483 161, 169, 188, 192, 193, 194, 200, 202, 204,
Calosota vernalis ............................406, 491, 494 206, 207, 210, 211, 215, 216, 217, 220, 225,
Calymmochilus .............................................. 255 226
Calymmochilus russoi ................................... 255 Ceratocystis rufipenni .................................... 200
Calyptus .......................................................... 403 Cerceris ...................................................410, 489
Camponotus .................................................... 503 Cerceris bupresticidaa ...................................... 489
Campoplex ...................................................... 511 Cerocephala ....................................240, 251, 254
Campoplex submarginatus ............................ 511 Cerocephala cornigera ................................... 254
Candidaa ........................................................... 185 Cerocephala eccoptogastri .............240, 251, 254
Candida diddensii ........................................... 185 Chalara ............................................................ 189
Canningia ................................................ 306, 308 Charmon ......................................................... 511
Canningia spinidentis ..................................... 308 Charmon extensor .......................................... 511
Canningia tomici ............................................ 308 Cheiropachus ................. 240, 244, 245, 248, 254
Carabus ........................................................... 410 Cheiropachus obscuripes ............................... 254
Carpinus ............................................18, 462, 539 Cheiropachus quadrum . 240, 244, 245, 248, 254
Carya ......................................................... 18, 105 Choristoneura ................................................. 156
Carya ovata .......................................18, 105, 121 Choristoneura pinus ...............................156, 157
Castanea ............................................18, 451, 517 Chrysobothris ................................................. 451
Cedrus ..................................................... 137, 461 Chrysobothris affinis ...................................... 451
Centistes .................................................. 241, 252 Chrysoperla ..................................................... 248
Centistes cuspitatus ........................................ 241 Chrysoperla carnea ......................................... 248
Cephalonomia ........................................ 251, 257 Chytridiopsis ..................................306, 307, 308
Cephalonomia cursorr ..................................... 257 Chytridiopsis typographi ...............306, 307, 308
Cephalonomia hypobori y ........................ 251, 257 Cleonymus ...................................................... 254
Cerambyx 5, 458, 461, 470, 475, 476, 485, 487, Cleonymus obscurus ...................................... 254
488, 495 Clistopyga ....................................................... 479
Cerambyx cerdo ...458, 461, 475, 485, 486, 487, Clistopyga sauberi .......................................... 479
488 Cloacaa ............................................................. 296
Cerambyx scopolii ......................................... 461 Cloaca cloacae ................................................ 296
Cerambyx velutinus (Cerambyx welensii) ...... 5, Clubiona .......................................................... 506
461, 470, 475, 485, 486, 495 Clubiona subsultans ....................................... 506
Cerasus ............................................................ 325 Coccotrypes ...................................................... 59
Cerasus avium ................................................ 325 Coccotrypes carpophagus ................................ 59
Cerasus padus ................................................. 325 Coelichneumon .............................................. 487
Cerasus vulgaris ............................................. 325 Coelichneumon impressor ............................. 487
Ceratocystiopsis ...182, 186, 188, 190, 197, 202, Coeloides ......240, 242, 244, 245, 246, 252, 254,
203, 204, 205, 206, 207, 209, 210, 211, 212, 402, 403, 404, 406, 407, 408, 480, 489, 490
383, 385 Coeloides abdominalis . 242, 246, 252, 404, 407,
Ceratocystiopsis alba ............ 202, 203, 204, 207 490
Ceratocystiopsis falcata ................................. 209 Coeloides bostrichorum .................240, 244, 245
Ceratocystiopsis minima ....................... 202, 205 Coeloides filiformis ...............................245, 252
Ceratocystiopsis minuta 202, 203, 204, 205, 206, Coeloides forsteri ...........................404, 407, 480
207, 209, 210, 211, 212, 214, 215, 383, 385 Coeloides melanostigma ........................404, 489
Ceratocystis ....97, 140, 146, 182, 183, 184, 186, Coeloides melanotus ...................................... 252
187, 188, 189, 190, 191, 192, 193, 194, 197, Coeloides scolyticida ............ 246, 252, 254, 490
199, 200, 202, 203, 204, 205, 206, 207, 209, Coeloides sordidator .... 242, 246, 252, 404, 408,
210, 211, 212, 213, 214, 217, 224, 226 489, 490
Coeloides stigmaticus .................................... 404 Crypturgus ....................... 47, 201, 202, 299, 305
Coeloides subconcolorr ................................... 252 Crypturgus cinereus ...............................201, 202
Coeloides ungularis ........................................ 252 Crypturgus pusillus ............... 201, 202, 299, 305
Coeloides vancouverensis ............................. 244 Cryptus ............................................489, 490, 532
Coleocentrus ........................................... 405, 479 Cryptus maculipennis ............................489, 490
Coleocentrus caligatus ........................... 405, 479 Cryptus pseudonymus .................................... 532
Conidiobolus .................................................. 300 Cupressus ....................................18, 74, 250, 462
Conidiobolus coronatus ................................. 300 Curculio .........318, 319, 320, 321, 322, 323, 416
Copidosoma .................................................... 523 Daldiniaa ........................................................... 537
Copidosoma truncatellum m .............................. 523 Daldinia concentrica ...................................... 537
Cordyceps ....................................................... 302 Dendrocopos .......................... 241, 250, 485, 523
Cordyceps militaris ........................................ 302 Dendrocopos major ............... 241, 250, 485, 523
Coroebus .....................................5, 451, 452, 453 Dendrocopos minor ................................485, 523
Coroebus florentinus (Coraebus florentinus) ...5, Dendroctonus 3, 6, 20, 22, 25, 37, 41, 45, 49, 50,
451, 452, 453, 475, 489, 490, 491, 492 51, 54, 58, 63, 65, 89, 90, 91, 96, 98, 104,
Coroebus undatus (Coraebus undatus) .... 5, 452, 107, 108, 114, 122, 136, 145, 148, 161, 183,
453, 454, 475, 476, 489 186, 197, 203, 239, 243, 244, 246, 259, 260,
Corticeus ................................................. 238, 245 241, 242, 252, 253, 254, 255, 256, 295, 297,
Corticeus fraxini .....................................238, 245 301, 306, 307, 405
Corticeus linearis ............................................ 245 Dendroctonus adjunctud s .................................. 51
Corticeus longulus ......................................... 245 Dendroctonus armandi ................................... 295
Corticeus pini ................................................. 245 Dendroctonus brevicomis .... 91, 94, 97, 98, 101,
Corticeus suberis ............................................ 245 105, 106, 111, 112, 114, 122, 51, 158, 162,
Corticeus unicolor .......................................... 246 169
Corylus ...................................................... 18, 539 Dendroctonus frontalis ....... 51, 93, 97, 111, 114,
Corynebacterium ............................................ 296 117, 148, 149, 155, 158, 159, 160, 161, 169,
Cosmophorus ..................................241, 242, 247 197, 222, 223, 252, 254, 295, 298, 307
Cosmophorus cembrae .................................. 247 Dendroctonus micans ... 6, 20, 22, 25, 37, 41, 45,
Cosmophorus klugi ........................................ 247 49, 50, 54, 58, 63, 65, 66, 68, 71, 73, 77, 82,
Cosmophorus regius ...................................... 247 107, 136, 137, 140, 143, 148, 149, 150, 151,
Cossus ......8, 22, 24, 37, 41, 44, 48, 53, 58, 502, 169, 170, 183, 201, 203, 239, 246, 247, 248,
504, 517, 518, 520, 524, 533 249, 250, 260, 242, 253, 254, 255, 256, 297,
Cossus cossus ...8, 22, 24, 37, 41, 44, 48, 53, 58, 405
502, 504, 517, 518, 519, 520, 521, 524, 533 Dendroctonus ponderosae 3, 6, 51, 92, 105, 111,
Crataegus ........................................................ 539 114, 120, 145, 148, 156, 160, 162, 169, 170,
Cratocentrus
r .................................................... 492 222, 252, 254, 301
Cratocentrus fastuosus ................................... 492 Dendroctonus pseudotsugae .. 51, 102, 103, 111,
Cremnodes ...................................................... 543 113, 148, 156, 169, 244, 306
Cremnodes atricapillus .................................. 543 Dendroctonus punctatus ........................148, 150
Cronartium .............................................. 340, 385 Dendroctonus rufipennis ..........3, 6, 51, 113, 200
Cronartium flaccidum m .................................... 385 Dendroctonus simplex ................................... 113
Cryphalus 6, 22, 65, 66, 201, 202, 241, 246, 468 Dendroctonus terebrans 148, 150, 160, 169, 388,
Cryphalus abietis ....................................201, 202 405, 406, 479, 487
Cryphalus fulvus ............................................ 468 Dendroctonus valens ..... 148, 150, 253, 388, 389
Cryphalus piceae .... 6, 65, 66, 22, 241, 246, 247, Dendrolaelaps ................................................. 249
248, 249, 250 Dendrolaelaps apophyseosimilis ................... 249
Cryptococcus .......................................... 185, 503 Dendrolimus ...........................................157, 467
Cryptococcus fagisugaa ................................... 503 Dendrolimus sibiricus .................................... 467
Cryptolestes .................................................... 243 Dendrolimus superans ................................... 157
Cryptolestes fractipennis ............................... 243 Dendrosoter ..240, 242, 244, 245, 247, 251, 252,
Cryptolestes spartii ......................................... 243 254
Cryptorhynchus 6, 20, 22, 24, 37, 41, 45, 49, 54, Dendrosoter chaenopachoides ....................... 254
58, 319, 321, 324, 410, 416, 419, 485, 533 Dendrosoter ferrugineus ................................ 252
Cryptorhynchus lapathi 6, 20, 22, 24, 37, 41, 45, Dendrosoter flaviventris ................................ 247
49, 54, 58, 397, 410, 419, 485, 533 Dendrosoter hartigi ........................................ 247
Cryptoxilos ............................................. 241, 247 Dendrosoter middendorffii .. 240, 242, 243, 244,
Cryptoxilos cracoviensis ................................ 241 245
Dendrosoter protuberans ..... 240, 244, 247, 251, Dothichiza populea ........................................ 527
252, 254 Drapetis ........................................................... 247
Dendrosotinus ................................................ 247 Drapetisca ....................................................... 506
Deuteroxorides ...................... 479, 487, 490, 493 Drapetisca socialis .......................................... 506
Deuteroxorides elevator ........ 479, 487, 490, 493 Dromius ..................................................238, 242
Diadegmaa ........................................................ 523 Dromius quadrimaculatus .............................. 242
Diadegma terebrans ..... 150, 160, 169, 388, 405, Dryocoetes .....298, 299, 304, 305, 306, 307, 308
406, 479, 487, 523 Dryocoetes ....................... 51, 107, 114, 201, 203
Dicaelotus
t ....................................................... 519 Dryocoetes autographus ..... 201, 203, 298, 299,
Dicaelotus pussilator ...................................... 519 304, 305, 306, 307, 308
Dichrostigma: see Raphidia Dryocoetes confusus ........................................ 51
Digamasellus .................................................. 241 Dryocopus .......................................241, 250, 481
Dimeris ........................................................... 490 Dryocopus martius .........................241, 250, 481
Dinotiscus .............................. 242, 245, 248, 254 Eblisia .....................................................238, 242
Dinotiscus aponius .................................248, 254 Eblisia minorr .......................................... 238, 242
Dinotiscus colon .............................242, 248, 254 Echthrus .......................................................... 487
Dinotiscus eupterus ............... 242, 245, 248, 254 Echthrus reluctatorr ......................................... 487
Dioryctria ................... 8, 406, 502, 503, 504, 514 Ecphylus ........................ 242, 243, 247, 253, 254
Dioryctria abietella .........................504, 514, 515 Ecphylus caudatus ................. 243, 247, 484, 488
Dioryctria mutatella ............................... 406, 503 Ecphylus eccoptogastri .................................. 253
Dioryctria schuetzeella .................................. 514 Ecphylus hylesini ...................................247, 253
Dioryctria simpliciellaa ................................... 514 Ecphylus silesiacus ............... 243, 247, 253, 254
Dioryctria splendidella (Dioryctria sylvestrella) Elachertus ....................................................... 523
................................ 8, 502, 504, 514, 515, 516 Elachertus nigritulus ...................................... 523
Diplogaster ..................................................... 400 Elasmus ........................................................... 523
Diprion ............................................................ 156 Elasmus albipennis ......................................... 523
Diprion pini ....................................156, 157, 167 Elasmus ciopkaloi .......................................... 523
Dirhabdilaimus ............................................... 400 Elasmus schmidti ........................................... 523
Dirhabdilaimus leuckarti ............................... 400 Elaterr ............................................................... 477
Dirhicnus ........................................................ 410 Endamoeba ..................................................... 305
Dolichogenidea .............................................. 523 Endocronartium r .............................................. 514
Dolichogenidea laevigata .............................. 523 Endocronartium strobi ................................... 514
Dolichomitus 239, 245, 248, 396, 397, 402, 405, Entedon 239, 242, 243, 250, 251, 255, 252, 254,
407, 410, 476, 478, 479, 481, 482, 484, 485, 491
486, 487, 490, 492 Entedon armigerae ......................................... 255
Dolichomitus aciculatus ................................ 479 Entedon ergias ......239, 242, 243, 251, 252, 254,
Dolichomitus agnocendus ............................. 487 491
Dolichomitus cognatorr .................................. 487 Entedon methion ............................................ 250
Dolichomitus t dux ........................................... 479 Entedon pinetorum ......................................... 250
Dolichomitus imperator ........ 479, 486, 487, 490 Enterobacter .................................................... 296
Dolichomitus mesocentrus ............476, 479, 487 Enterobacter aerogenes .................................. 296
Dolichomitus messor ............................. 484, 485 Enterobacter agglomerans ............................. 296
Dolichomitus populneus ................479, 484, 487 Enterobacter cloacae ...................................... 296
Dolichomitus sericeus ............................ 479, 481 Entomocorticium ....................................186, 223
Dolichomitus terebrans 150, 160, 169, 239, 245, Entomopoxvirus .............................295, 296, 520
248, 388, 402, 405, 406, 407, 479, 487 Entomopoxvirus cossi .................................... 520
Dolichomitus tuberculatus ... 396, 397, 410, 478, Ephialtes ......................................................... 487
479, 486, 487 Ephialtes manifestatorr .................................... 487
Dolichopus ...................................................... 246 Epuraea ...................................................238, 243
Doryctes 247, 253, 480, 481, 482, 489, 491, 494 Epuraea angustula .......................................... 243
Doryctes leucogaster ............. 247, 480, 481, 491 Epuraea laeviuscula ....................................... 243
Doryctes mutillator ....... 480, 481, 482, 489, 491 Epuraea marseuli ............................................ 243
Doryctes pomarius .................................247, 253 Epuraea pygmaea ........................................... 243
Doryctes rex ................................................... 253 Epuraea rufomarginat a a ................................... 243
Doryctes striatellus ......................................... 247 Epuraea silacea ............................................... 243
Doryctes undulatus ................ 253, 480, 491, 494 Epuraea thoracica ........................................... 243
Dothichiza ....................................................... 526 Epuraea unicolor ............................................ 243
Ergates ............................................................ 461 Foersteria puber .............................................. 490

Ergates faber
a ................................................... 461 Fomes: see Heterobasidion
Eriborus ........................................................... 528 Forficula ..........................................246, 482, 483
Eriborus terebrans .......................................... 528 Forficula auricularia .......................246, 482, 483
Erwinia ............................................................ 297 Formica ........................................................... 410
Erwinia rhapontici
a .......................................... 297 Fraxinus ...........18, 209, 250, 333, 521, 522, 531
Erwinia rubrifaciens
f ....................................... 297 Fraxinus exelsiorr ............................................ 333
Escherichia ..................................................... 296 Fraxinus pennsylvanica ................................. 522
Escherichia klebsiellaeformis ........................ 296 Freraea ....................................................492, 494
Eubadizon ....................................................... 403 Freraea gagateaa ....................................... 492, 494
Eubazus ..........238, 341, 402, 403, 404, 408, 412 Fringilla ........................................................... 249
Eubazus abieticola .........................403, 404, 408 Fringilla coelebs ............................................. 249
Eubazus robustus t .................................... 403, 408 Fusarium .........................................111, 194, 524
Eubazus semirugosus ............ 238, 403, 404, 408 Fusarium circinatum m ...................................... 111
Eucalyptus .........11, 18, 460, 462, 464, 465, 486 Glischrochilus .........................................238, 243
Eucalyptus globulus ....................................... 465 Glischrochilus hortensis ................................. 244
Eucorystes .......................................490, 491, 494 Glischrochilus quadripunctatus t ..................... 243
Eucorystes aciculatus t ............ 490, 491, 492, 494 Gloeocystidium .............................................. 185
Euderus ..................255, 484, 488, 491, 493, 523 Gloeocystidium ipidophilum ......................... 185
Euderus agrili ......................................... 491, 493 Glyptaa .............................................................. 510
Euderus albitarsis ...........................255, 484, 488 Glypta resinanae ............................................. 510
Euderus caudatus .................................... 484, 488 Gnathotrichus ...6, 21, 23, 25, 38, 42, 46, 49, 50,
Eulimneria ...................................................... 511 51, 54, 59, 89, 196, 198, 203, 299
Eulimneria rufifemur u ..................................... 511 Gnathotrichus materiarius . 6, 21, 23, 25, 38, 42,
Eupelmus ...............242, 245, 250, 256, 406, 408 46, 49, 50, 54, 59, 196, 198, 199, 203, 238,
Eupelmus aloysii ............................................ 256 299
Eupelmus annulatus
a ....................................... 256 Gnathotrichus retusus .................................... 113
Eupelmus urozonus ...... 242, 245, 250, 256, 406, Gnathotrichus sulcatus ............................. 51, 113
408 Graphium ......189, 192, 194, 200, 202, 203, 204,
Eurytoma ......240, 242, 245, 250, 251, 256, 406, 205, 206, 207, 209, 210, 211, 212, 213, 384,
408 385
Eurytoma abieticola ............................... 250, 403 Graphium adustum
d ......................................... 203
Eurytoma aloisfilippoi ................................... 256 Graphium canum ............................................ 384
Eurytoma annilai .................................... 406, 408 Graphium fimbriisporum ..... 200, 202, 203, 204,
Eurytoma arctica ............................245, 250, 256 205, 206, 207, 210, 211
Eurytoma blastophagi .................................... 250 Graphium laricis .............................192, 200, 206
Eurytoma crassinervis .................................... 250 Graphium penicillioides 194, 200, 201, 211, 213
Eurytoma morio .................... 242, 245, 250, 251 Graphium pseudormiticum .. 200, 202, 203, 204,
Eurytoma polygraphi ............ 240, 242, 250, 256 206, 207, 209, 210, 211, 213
Eurytoma rufipes ............................................ 250 Gregarina ........................................304, 305, 400
Eurytoma wachtli ................................... 406, 408 Gregarina hylastidis ....................................... 305
Eusandalum ........................... 256, 490, 491, 493 Gregarina hylobii ........................................... 400
Eusandalum elongatum ................................. 491 Gregarina piktyokteinidis .............................. 305
Eusandalum ibericum m .................................... 491 Gregarina pityogenidis ................................... 305
Eusandalum merceti ....................................... 256 Gregarina typographi .............................304, 305
Eusandalum walkeri ............................... 491, 493 Gymnophania .........................................492, 494
Evetria ......................................................... 8, 503 Gymnophania nigripennis .....................492, 494
Exeristes ..........................................405, 407, 511 Habritys ........................................................... 254
Exeristes roborator ......................................... 511 Habritys brevicornis ....................................... 254
Exeristes ruficollis .................................. 405, 407 Habrocytust ...................................................... 511
Exoteleia ......................................................... 511 Habrocytus semotus ....................................... 511
Exoteleia dodecellaa ........................................ 511 Hansenula ....................................................... 185
Fagus ...... 18, 118, 211, 213, 250, 356, 451, 452, Hansenula holstii ............................................ 185
454, 522 Hecabolus ...............................................251, 253
Fagus sylvatica .........................18, 118, 211, 213 Hecabolus sulcatus .................................251, 253
Flavobacterium ............................................... 296 Hederaa ............................................................. 531
Foersteria ........................................................ 490 Hedera helix .................................................... 531
Helcon .............................................480, 491, 523 407, 412, 415, 416, 417, 418, 419, 420, 421,
Helcon angustator .......................................... 480 422, 423, 424, 425, 427, 432, 436, 437, 438
Helcon claviventris ........................................ 491 Hylobius abietis .... 6, 20, 21, 24, 28, 34, 36, 40,
Helcon tardator ............................................... 480 44, 48, 53, 57, 322, 325, 331, 332, 333, 334,
Helconidea .............................................. 478, 480 335, 351, 352, 354, 355, 358, 365, 366, 367,
Helconidea dentatorr .............. 478, 480, 481, 482 373, 374, 375, 381, 382, 384, 395, 396, 397,
Helcostizus ..................................................... 479 398, 399, 400, 401, 402, 403, 407, 409, 412,
Helcostizus restaurator ................................... 479 415, 416, 419, 421, 423, 432, 435, 436, 437
Helicosporidium ............................................. 307 Hylobius assimilis ................. 332, 356, 384, 389
Helicosporidium parasiticu a m ........................ 307 Hylobius congener .........................332, 401, 437
Herpestomus ................................................... 519 Hylobius pales ......332, 351, 353, 356, 384, 389,
Herpestomus arridens r .................................... 520 399, 401
Heterobasidion (Fomes) ...... 185, 381, 384, 385, Hylobius piceus ..............................325, 331, 415
408, 418, 437 Hylobius pinastri ... 6, 21, 23, 26, 38, 42, 46, 50,
Heterobasidion annosum ..... 185, 381, 382, 383, 55, 59, 322, 331, 351, 354, 395, 415, 419,
384, 385, 386, 437 432
Heterorhabditis .............. 401, 402, 411, 488, 525 Hylobius pinicolaa ........................................... 382
Heterorhabditis downesi ................................ 402 Hylobius radicis ............ 332, 356, 384, 388, 389
Heterorhabditis megidis ................................. 411 Hylobius rhizophagus ....................384, 389, 399
Heterospilus incompletus .............................. 251 Hylobius transversovittatus t ........................... 331
Heterospilus sicanus ...................................... 247 Hylobius warreni ....................................332, 382
Heydenia ........................ 242, 248, 251, 254, 491 Hylobius xiaoi ................................................ 332
Heydenia pretiosa .......... 242, 243, 248, 251, 254 Hylurgopinus .................................................. 297
Heydenia pretiosaa ........................................... 491 Hylurgopinus rufipes ..................................... 297
Hirsutella ........................................................ 302 Hylurgops .....108, 195, 197, 198, 201, 204, 205,
Hirsutella thompsonii ..................................... 302 242, 298, 299, 302, 304, 305, 306, 307, 308,
Histerr ............................................................... 410 388
Hormonema .................................................... 201 Hylurgops glabratus ..... 201, 205, 305, 306, 307,
Hormonema dematoides ................................ 201 308
Horogenes ....................................................... 523 Hylurgops palliatus ..... 116, 117, 195, 197, 198,
Horogenes punctoriaa ...................................... 523 200, 201, 204, 242, 298, 299, 302, 304, 306,
Hyalorhinocladiella ........................186, 189, 194 307, 308
Hylastes .6, 21, 22, 25, 26, 38, 42, 46, 50, 54, 55, Hylurgops porosus ......................................... 388
59, 197, 198, 201, 203, 204, 238, 259, 260, Hylurgus ...............................................7, 23, 238
254, 298, 302, 305, 307, 333, 354, 355, 387, Hylurgus ligniperda .............................7, 23, 238
389 Hypoborus ...................................................... 243
Hylastes angustatu
a s .............................................6 Hypoborus ficus ............................................. 243
Hylastes ater .... 6, 21, 22, 25, 38, 42, 46, 50, 54, Hypothenemus .................................................. 89
59, 197, 198, 201, 203, 254, 298, 305 Ibaliaa ............................................................... 537
Hylastes attenuatus ..............................................6 Ichneumon ...................................................... 523
Hylastes brunneus ...............................................6 Ichneumon abeillei ......................................... 523
Hylastes cunicularius ... 6, 21, 22, 26, 38, 42, 46, Inocellia .......................................................... 482
50, 55, 59, 197, 198, 201, 204, 302, 305, 307 Inocellia crassicornis ...................................... 482
Hylastes nigrinus ............................................ 387 Iphiaulax ................478, 480, 484, 488, 491, 492
Hylastes opacus ................... 6, 89, 204, 298, 305 Iphiaulax impostor 478, 480, 484, 488, 491, 492
Hylesinus .......................................................... 23 Iphiaulax multiarticulatus ......................484, 488
Hylesinus ....6, 7, 23, 42, 47, 239, 252, 253, 254, Ipidiaa ............................................................... 244
255, 256, 257, 259, 299, 306 Ipidia binotata ................................................. 244
Hylesinus crenatus .......................6, 23, 239, 299 Iponemus ................................................241, 249
Hylesinus fraxini: see Leperisinus varius Iponemus gaebleri .......................................... 249
Hylesinus varius: see Leperisinus varius Ips .. 7, 20, 21, 22, 23, 24, 25, 26, 27, 30, 34, 36,
Hylobius ..3, 6, 12, 20, 21, 23, 24, 26, 28, 34, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48,
38, 40, 42, 44, 46, 48, 50, 53, 55, 57, 59, 319, 49, 50, 51, 53, 54, 55, 56, 57, 58, 59, 63, 65,
322, 325, 331, 332, 333, 334, 351, 352, 355, 66, 75, 81, 89, 90, 91, 93, 96, 98, 100, 102,
356, 359, 360, 365, 367, 374, 375, 381, 382, 104, 107, 114, 118, 137, 148, 156, 161, 169,
384, 386, 389, 395, 396, 399, 400, 401, 403, 183, 184, 186, 187, 191, 192, 194, 197, 198,
201, 205, 206, 207, 223, 225, 237, 238, 240,
241, 242, 243, 245, 246, 259, 260, 240, 242, Ischnoceros ............................ 479, 482, 485, 487
252, 255, 256, 295, 296, 297, 298, 299, 300, Ischnoceros caligatus t .....................479, 482, 487
302, 303, 304, 305, 306, 307, 308, 406 Ischnoceros rusticus ...............................485, 487
Ips acuminatus ..7, 20, 22, 24, 30, 34, 37, 40, 44, Itoplectis ......................................................... 515
48, 53, 56, 57, 58, 64, 71, 73, 77, 80, 81145, Itoplectis cristatae ........................................... 515
148, 151, 169, 184, 197, 198, 200, 201, 205, Jarra ................................................................. 466
215, 222, 238, 241, 242, 246, 247, 248, 249, Jarra phoracanthaa ........................................... 466
250, 260, 242, 299, 305, 306, 308 Juglans ..............................................18, 462, 523
Ips amitinus ....21, 22, 26, 39, 42, 46, 50, 55, 56, Juglans regia ............................................. 18, 523
59, 64, 76, 114, 117, 156, 193, 200, 201, 206, Juniperus ..................................................... 18, 74
215, 246, 247, 248, 249, 250, 298, 300, 305, Kalotermes .......................................................... 5
307, 308 Kalotermes flavicollis ........................................ 5
Ips avulsus ............................. 114, 117, 186, 223 Konowiaa .......................................................... 537
Ips calligraphus .......51, 114, 152, 223, 297, 298 Konowia betulae ............................................ 537
Ips cembrae 7, 21, 22, 26, 39, 42, 46, 50, 55, 56, Lachnellula ..................................................... 385
59, 113, 192, 200, 201, 206, 246, 247, 248, Lachnellula pini .............................................. 385
249, 250, 242 Laelius ............................................................. 257
Ips confusus ......................................51, 158, 169 Laelius elisae .................................................. 257
Ips curvidens ................................................... 296 Lamia .........................5, 461, 475, 485, 487, 488
Ips duplicatus ....7, 20, 22, 25, 38, 41, 45, 49, 54, Lamia textor ......5, 461, 475, 476, 485, 487, 488
56, 58, 114, 193, 200, 201, 206, 215, 246, Lampraa ............................................................ 452
298 Lampra rutilans .............................................. 452
Ips fallax ........................................................... 56 Laphria ................................... 246, 399, 477, 489
Ips grandicollis ........51, 105, 114, 117, 156, 223 Laphria flava ................................................... 246
Ips hauseri ......................................................... 51 Laphria gibbosa .............................................. 477
Ips japonicus ..................................................... 56 Laphria gilva ...........................................246, 489
Ips laricis ................................................. 305, 307 Larix ................................................................ 137
Ips lecontei ........................................................ 51 Larix . 18, 56, 192, 194, 200, 203, 204, 206, 213,
Ips mannsfeldi .................................................. 56 250, 459, 461, 462, 479
Ips paraconfusus ..... 51, 93, 94, 96, 97, 100, 104, Larix decidua ........................... 18, 203, 206, 213
105, 106, 111, 112, 113, 114, 119, 120, 121 Larix kaempferi ............... 18, 194, 204, 206, 213
Ips pini ....................... 51, 93, 109, 113, 114, 169 Lasioseius ....................................................... 249
Ips plastographus .............................................. 51 Lasioseius ometes .......................................... 249
Ips sexdentatus .7, 20, 22, 25, 38, 41, 45, 49, 54, Lasius .............................................................. 494
56, 58, 64, 66, 71, 73, 74, 75, 76, 83, 95, 102, Lasius niger .................................................... 494
137, 140, 143, 148, 151, 169, 197, 198, 200, Laspeyresia ..................................................... 504
201, 206, 223, 242, 246, 247, 248, 249, 250, Laspeyresia pactolana .................................... 504
260, 242, 305 Leiopus ...................................................459, 461
Ips shinanonensis ............................................ 56, Leiopus nebulosus ..................................459, 461
Ips subelongatus ................ 51, 56, 194, 297, 302 Leperisinus ...... 7, 201, 209, 238, 239, 241, 245,
Ips typographus ... 7, 20, 21, 23, 27, 28, 34, 36, 257, 252, 256
40, 43, 48, 50, 52, 53, 56, 57, 58, 59, 63, 65, Leperisinus varius (Leperisinus fraxini) .. 7, 201,
66, 67, 68, 69, 70, 73, 74, 75, 76, 77, 79, 81, 209, 238, 239, 241, 245, 257, 252, 256, 306
82, 92, 94, 95, 96, 98, 100, 101, 102, 103, Leptographium .....146, 156, 157, 160, 186, 189,
104, 105, 107, 111, 112, 113, 114, 115, 118, 191, 192, 194, 200, 203, 204, 205, 206, 207,
122, 137, 141, 145, 148, 150, 151, 156, 162, 209, 210, 211, 212, 213, 382, 383, 384, 385,
169, 183, 185, 187, 191, 193, 194, 200, 201, 386, 387, 388, 389, 390
202, 207, 215, 216, 217, 220, 222, 224, 225, Leptographium alethinum .....................183, 384
237, 238, 239, 240, 241, 242, 243, 244, 245, Leptographium euphyes ................................ 212
246, 259, 260, 240, 242, 251, 252, 255, 256, Leptographium guttulatum .. 203, 204, 205, 211,
295, 296, 297, 298, 299, 300, 301, 302, 303, 212
304, 305, 306, 307, 308, 406 Leptographium lundbergii ... 203, 204, 205, 206,
Isadelphus ....................................................... 490 207, 209, 210, 211, 212, 213, 385
Isadelphus gallicola ........................................ 490 Leptographium procerum .... 204, 212, 382, 384,
Isarthron castaneum: see Tetropium castaneum 385, 388, 389, 390
Isarthron gabrieli: see Tetropium gabrieli Leptographium serpens .................................. 203
Isarthron: see Tetropium Leptographium terebrantis .... 156, 384, 388, 389
Leptographium wageneri ..... 191, 382, 385, 387, Mattesiaa ........................................................... 306
388, 389 Mattesia schwenkei ........................................ 306
Leptographium wingfieldii .. 146, 149, 153, 157, Medetera ........................ 239, 246, 247, 251, 252
159, 160, 192, 193, 201, 204, 212, 220, 226, Medetera adjaniae
d .......................................... 246
383, 384 Medetera ambigua
m .......................................... 246
Leptographium yunnanense .......................... 160 Medetera dendrobaena ...........................239, 246
Leskiaa .............................................................. 532 Medetera dichroceraa ....................................... 246
Leskia aurea
u .................................................... 532 Medetera excellens ......................................... 246
Lestricus .......................................................... 248 Medetera impigra
m ........................................... 246
Lestricus secalis ............................................. 248 Medetera infumataa ......................................... 246
Liotryphon ...................................................... 487 Medetera melancholic
a a .................................. 246
Liotryphon crassisetus ................................... 487 Medetera nitida ............................................... 246
Liotryphon punctulatus .................................. 487 Medetera obscura ........................................... 246
Lissonota .........................................479, 511, 519 Medetera pinicolaa ........................................... 247
Lissonota buccator ......................................... 479 Medetera setiventris ....................................... 247
Lissonota dubia .............................................. 511 Medetera signaticornis ................................... 247
Lissonota setosa ............................................. 519 Medetera striata
t .............................................. 247
Litargus ........................................................... 243 Medetera thunebergi ...................................... 247
Litargus connexus .......................................... 243 Medetera vagans ............................................ 247
Lonchaea ........................ 239, 409, 483, 489, 494 Medophron ..................................................... 487
Lonchaea bruggeri
r ......................................... 247 Medophron afflictor ....................................... 487
Lonchaea chorea ............................................ 494 Megarhyssa ..................................................... 487
Lonchaea collini ..................................... 247, 489 Megarhyssa perlata ........................................ 487
Lonchaea corticis ........................................... 409 Megarhyssa superba ....................................... 487
Lonchaea fugax .............................................. 247 Megaselia ............................... 396, 398, 410, 523
Lonchaea helvetica ......................................... 247 Megaselia plurispinulosa .......................396, 398
Lonchaea laticornis ........................................ 247 Megaselia praecusta ....................................... 523
Lonchaea scutellaris ....................................... 247 Megaselia zeuzerae ........................................ 523
Lonchaea seitneri ........................................... 247 Melanconium .................................................. 537
Lonchaea zetterstedti .............................247, 483 Melanconium bicolor ..................................... 537
Lyctocoris ....................................................... 248 Melanophila ......5, 450, 452, 456, 457, 475, 490,
Lyctocoris campestris .................................... 248 491, 492
Lysitermus
m ...................................................... 247 Melanophila acuminataa .................................. 450
Lysitermus pallidus ........................................ 247 Melanophila picta .....5, 452, 457, 475, 476, 490,
Lythrum .......................................................... 331 491, 492
Lythrum salicaria ........................................... 331 Melanotus ....................................................... 477
Macrocentrus r .................................................. 515 Melia ............................................................... 463
Macrocentrus abdominali
a s ............................ 515 Melia azedarach ............................................. 463
Macrocentrus linearis ..................................... 515 Meniscus ......................................................... 532
Macrocentrus nitidus ...................................... 515 Meniscus setosus ............................................ 532
Macrocentrus resinellae ................................. 515 Menzbieria ...................................................... 306
Macrocentrus sylvestrellae ............................ 515 Menzbieria chalcographi ............................... 306
Macrocentrus watanabei ................................ 515 Mesopolobus ..................................241, 245, 249
Macromesus ................................................... 248 Mesopolobus typographi ...............241, 245, 249
Madizaa ............................................................ 247 Metacolus ...............242, 249, 251, 254, 405, 408
Madiza glabra ................................................. 247 Metacolus azureus .......................................... 249
Magdalis ........................ 319, 321, 322, 325, 403 Metacolus unifasciatus . 242, 249, 251, 254, 406,
Magdalis violaceus ......................................... 322 408
Malachius ....................................................... 483 Metamasius ..................................................... 358
Malachius bipustulatus .................................. 483 Metarhizium .................. 301, 303, 400, 411, 525
Malamoeba ..................................................... 304 Metarhizium anisopliae 301, 302, 303, 400, 411
Malamoeba locustae ...................................... 304 Meteorus ................................ 253, 477, 480, 511
Malus .............................................................. 539 Meteorus consimilis ....................................... 253
Mastrus ........................................................... 487 Meteorus corax .......................................477, 480
Mastrus rufobasalis ........................................ 487 Meteorus inctericus ........................................ 511
Matsucoccus ...........................................340, 503 Meteorus obfuscatu
f s ...................................... 253
Matsucoccus feydauti .................................... 340 Metoponcus .................................................... 245
Metoponcus brevicornis ................................ 245 Oberea linearis ................................................ 462

Metschnikowia ............................................... 300 Oberea oculata ................................................ 462
Metschnikowia typographiy ............................ 300 Obriumm ............................................................ 483
Micaria ............................................................ 506 Obrium brunneum
r .......................................... 483
Micaria subopaca ........................................... 506 Odinia ......................................................485, 523
Microdus ......................................................... 511 Odinia meijerei ............................................... 523
Microdus rufipes ............................................ 511 Odinia xanthocera
t a .......................................... 485
Microgaster ............................................. 491, 494 Odontocolon ...................................476, 479, 481
Microgaster globataa ....................................... 491 Odontocolon appendiculatum t ....................... 479
Moebiliaa .......................................................... 506 Odontocolon dentipes ............................476, 479
Moebilia penicillata ....................................... 506 Odontocolon quercinum m ................................ 479
Molorchus ....................................................... 462 Odontocolon spinipes ............................479, 481
Molorchus minor ............................................ 462 Olea ...................................................18, 250, 465
Monochamus ....5, 12, 21, 23, 26, 39, 42, 46, 50, Olea europaea ................................................. 465
55, 59, 458, 459, 460, 461, 462, 467, 468, Ontsira ....................248, 253, 480, 481, 488, 491
471, 475, 476, 477, 478, 479, 495 Ontsira antica ......................... 248, 480, 481, 491
Monochamus alternatus ................................. 468 Ontsira imperator .................. 248, 253, 480, 481
Monochamus galloprovincialis 5, 460, 462, 467, Ontsira longicaudis ................................488, 491
468, 471, 475, 477, 495 Oobius .............................................486, 488, 492
Monochamus sartor 5, 21, 23, 26, 39, 42, 46, 50, Oobius rudnevi .......................................486, 488
55, 59, 462, 467, 475, 477, 479 Oobius zahaikevitshi ...................................... 492
Monochamus sutor .... 5, 462, 467, 475, 477, 479 Oodera .....................................................491, 493
Monochamus urussovi ........................... 458, 467 Oodera formosa ......................................491, 493
Monolexis ....................................................... 253 Ophiostoma ....97, 111, 144, 146, 154, 157, 159,
Monolexis fuscicornis .................................... 253 169, 182, 183, 184, 186, 187, 188, 189, 190,
Mucor ...................................................... 300, 523 192, 194, 197, 199, 200, 201, 202, 203, 204,
Mucor hiemalis .......................................300, 523 205, 206, 207, 208, 209, 210, 211, 212, 213,
Nematopodius ................................................ 254 214, 215, 224, 382, 383, 384, 385, 386, 389
Nematopodius formosus ................................ 254 Ophiostoma ainoae ....... 202, 203, 204, 205, 206,
Nematus .......................................................... 503 207, 209, 210
Nematus ericssoni .......................................... 503 Ophiostoma ambrosiam a .................................... 213
Nemosoma ............................. 259, 249, 246, 255 Ophiostoma araucariae 202, 203, 207, 208, 209,
Nemosoma elongatum m .......... 259, 249, 246, 255 210
Neoaplectana .......................................... 437, 529 Ophiostoma bacillisporum m ............................ 213
Neoaplectana carpocapsae ..................... 437, 529 Ophiostoma bicolor ...... 192, 202, 204, 206, 208,
Neodiprion ...................................................... 156 209, 210, 211, 217, 221
Neoparasitylenchus ........................................ 409 Ophiostoma brunneo-ciliatum ......146, 154, 159,
Neoxorides .............248, 479, 480, 481, 487, 523 167, 192, 205, 206, 207, 215, 223, 226
Neoxorides collaris ............... 248, 479, 480, 482 Ophiostoma cainii .......................................... 208
Neoxorides nitens ...........................479, 487, 523 Ophiostoma canum ...... 192, 203, 205, 210, 211,
Nilea ................................................................ 519 212, 383, 385
Nilea lethifera ................................................. 519 Ophiostoma clavatum m ........... 205, 207, 209, 212
Nomuraea ....................................................... 302 Ophiostoma clavigerum: see Ceratocystis
Nomuraea rileyi .............................................. 302 clavigera
Nosema .................................. 306, 307, 308, 400 Ophiostoma cucullatum 203, 204, 205, 206, 208,
Nosema calcarati ............................................ 307 209, 210, 213
Nosema curvidentis ........................................ 307 Ophiostoma flexuosum ..........................205, 208
Nosema dendrocton
d i ...................................... 306 Ophiostoma floccosum 205, 208, 210, 211, 212,
Nosema dryocoetesi ....................................... 307 215
Nosema hylobii .............................................. 400 Ophiostoma fusiforme ................................... 206
Nosema scolyti ............................................... 307 Ophiostoma galeiformis ....... 203, 204, 212, 213
Nosema typographi ........................306, 307, 308 Ophiostoma grandicarpa ................................ 213
Nothorhina ...................................................... 489 Ophiostoma ips .....157, 159, 192, 203, 205, 207,
Nothorhina punctata ....................................... 489 209, 212, 215, 223, 383, 384, 385
Nudobius .........................................238, 245, 409 Ophiostoma japonicum 202, 203, 204, 207, 208,
Nudobius lentus ..............................238, 245, 409 209
Oberea ..................................................... 462, 484 Ophiostoma lunatum ...................................... 206
Ophiostoma minus 111, 192, 197, 201, 203, 205, Otiorrhynchus ovatus .............................323, 411
206, 207, 208, 209, 210, 211, 212, 215, 223, Otiorrhynchus scaberr ..................................... 356
383, 385 Otiorrhynchus singularis ... 6, 320, 323, 332, 419
Ophiostoma neglectum 202, 203, 204, 208, 210, Otiorrhynchus sulcatus ......................6, 411, 419
213 Ozopemon ......................................................... 47
Ophiostoma nigrocarpaa .................................. 111 Pachylobius ............................ 356, 382, 384, 389
Ophiostoma novo-ulmi . 184, 191, 201, 211, 221 Pachylobius picivorus ............................356, 389
Ophiostoma obscura .... 203, 207, 208, 209, 210, Paecilomyces ................. 298, 299, 300, 301, 302
511 Paecilomyces farinosus . 299, 300, 301, 302, 303
Ophiostoma olivaceum m .................................. 204 Paecilomyces fumoso-roseus ................299, 302
Ophiostoma penicillatum ..... 192, 202, 203, 204, Paecilomyces variotii ..................................... 299
205, 206, 208, 210, 211, 214, 221 Pales ................................................................ 488
Ophiostoma piceae ....... 192, 202, 203, 204, 205, Pales pumicata ................................................ 488
206, 208, 209, 210, 211, 212, 213, 214, 215, Palloptera usta: see Toxoneura usta
225, 383, 384, 385 Palloptera ustulataa .......................................... 248
Ophiostoma piceaperdum .... 192, 202, 203, 205, Palloptera: see Toxoneura
206, 207, 208, 209, 210, 211, 212, 214, 216, Palmarr ............................................................. 452
221 Palmar festiva ................................................. 452
Ophiostoma piliferum .. 204, 205, 206, 209, 212, Pandelleia ........................................................ 410
213, 214, 215, 383, 384 Paracarophenax ......................................241, 249
Ophiostoma pini ............................................. 383 Paracarophenax ipidarius ............................... 249
Ophiostoma pluriannulatum ..........209, 212, 383 Paranthrene .8, 20, 22, 25, 38, 41, 45, 49, 54, 58,
Ophiostoma quercus ..... 209, 211, 213, 215, 225 502, 504, 526, 528, 533, 534
Ophiostoma simplex ..............................203, 205 Paranthrene tabaniformis ... 8, 20, 22, 25, 38, 41,
Ophiostoma stenoceras 202, 203, 205, 209, 210, 45, 49, 54, 58, 502, 504, 505, 526, 528, 529,
211, 213, 383 530, 533
Ophiostoma tetropii ....................................... 209 Pareucorystes .................................................. 491
Ophiostoma torulosum ..................203, 213, 214 Pareucorystes varinervis ................................ 491
Ophiostoma ulmi ..169, 184, 191, 201, 211, 221, Paromalus ...............................................242, 477
223 Paromalus parallelepidus ............................... 477
Ophiostoma verrucosum m ................................ 213 Pasteurella ....................................................... 297
Ophiostoma wageneri .................................... 389 Pasteurella haemolytica ................................. 297
Ophryocystis ........................................... 306, 400 Paururus juvencus: see Sirex juvencus
Ophryocystis dendroctoni .............................. 306 Pediculoides ....................................406, 408, 523
Ophryocystis hylesini .................................... 306 Pediculoides ventricosus ................406, 408, 523
Ophryocystis hylobii ...................................... 400 Peridermium .......................... 382, 385, 386, 514
Orgilus ............................................................ 511 Peridermium pini ..249, 322, 323, 326, 332, 339,
Orgilus obscurator
u .......................................... 511 340, 341, 342, 382, 383, 385, 386, 387, 402,
Orthocentrus
r ................................................... 487 404, 405, 406, 409
Orthocentrus fulvipes ..................................... 487 Perilampus
m ...................................................... 523
Orthotomicus ..7, 23, 50, 56, 148, 201, 209, 246, Perilampus tristis ............................................ 523
242, 254, 299 Perilitus .................................. 248, 396, 410, 436
Orthotomicus erosus .... 7, 23, 56, 148, 246, 247, Perilitus areolaris ....................................396, 436
248, 249, 250, 242, 254 Perilitus rutilus ...............................248, 396, 436
Orthotomicus laricis .......................201, 209, 299 Perithous ......................................................... 479
Orthotomicus proximus .........................201, 209 Perithous divinator ......................................... 479
Orthotomicus robustus ..................................... 50 Perniphoraa .............................. 240, 242, 249, 254
Oryctes ............................................................ 296 Perniphora robustaa ................ 240, 242, 249, 254
Otiorrhynchus ...6, 318, 319, 320, 323, 332, 342, Perosis ............................................................. 410
343, 356, 395, 410, 411, 412, 416, 419, 433 Pesotum 186, 189, 192, 194, 200, 203, 204, 205,
Otiorrhynchus arcticus .... 6, 320, 323, 332, 342, 206, 207, 209, 210, 212, 213
343, 344, 411, 416 Petrova ............................................................ 503
Otiorrhynchus dubius ................................. 6, 411 Petrova resinella ............................................. 503
Otiorrhynchus ligustici .................................. 411 Phaenops .... 5, 20, 22, 24, 30, 32, 35, 37, 41, 44,
Otiorrhynchus niger ...............................320, 323 48, 53, 57, 450, 451, 452, 456, 475, 488, 490,
Otiorrhynchus nodosus .... 6, 320, 323, 332, 343, 491, 492
344, 410, 411, 416
Phaenops cyanea (Melanophila cyanea) ... 5, 20, Pichiaa ............................................................... 185

22, 24, 30, 32, 35, 37, 41, 44, 48, 53, 57, 450, Picoides ...................................................241, 250
451, 452, 456, 457, 475, 488, 490, 491, 492 Picoides syriacus ............................................ 250
Phaeostigma: see Raphidia Picoides tridactylus ................................241, 250
Phaonia ........................................................... 247 Picus ........................................................492, 523
Phaonia gobertii ............................................. 247 Picus viridis ............................................492, 523
Philodromus
m ................................................... 506 Pimplaa ............................................................. 511
Philodromus fuscomarginatus ....................... 506 Pimpla turionellae .......................................... 511
Phlebiopsis ..............................................418, 427 Pineus .............................................................. 503
Phlebiopsis gigantea ......................418, 427, 437 Pineus pini ...................................................... 503
Phloeonomus .................................................. 245 Pinus . 18, 56, 57, 59, 74, 91, 119, 120, 136, 137,
Phloeopora ...................................................... 245 138, 145, 152, 156, 169, 192, 202, 203, 204,
Phloeopora testaceaa ........................................ 245 205, 206, 209, 210, 211, 212, 243, 250, 324,
Phloeosinus .....................................7, 47, 74, 251 326, 333, 339, 354, 357, 374, 382, 386, 388,
Phloeosinus armatus ...........................................7 435, 452, 456, 461, 462, 465, 479, 492, 509,
Phloeosinus bicolor ...................................... 7, 74 511, 512, 514, 519, 538
Phloeosinus thujae ..............................................7 Pinus banksiana a ...................................... 156, 157
Phloeostiba ..................................................... 245 Pinus cembra ......................................18, 56, 206
Phloeostiba lapponicus
a .................................. 245 Pinus contorta .18, 105, 120, 138, 152, 153, 154,
Phloeotribus ..7, 23, 46, 110, 238, 240, 244, 252, 155, 159, 160, 169, 357, 358, 388, 435, 509
253, 254, 255, 256, 257, 252, 255, 256 Pinus echinataa .................................153, 155, 169
Phloeotribus scarabaeoides 7, 23, 110, 238, 240, Pinus elliottii ...........................................152, 169
244, 252, 253, 254, 255, 256, 257, 252, 255, Pinus halepensis ...............................18, 324, 456
256 Pinus lambertianar ........................................... 119
Phomopsis ...................................................... 121 Pinus nigra ...............18, 324, 509, 510, 511, 531
Phomopsis oblonga ........................................ 121 Pinus pinaster (Pinus maritima) .....18, 141, 169,
Phoracantha ....3, 5, 23, 460, 461, 462, 464, 486, 324, 386, 465, 514
495 Pinus ponderosa ....145, 153, 158, 161, 162, 169
Phoracantha recurva ....................................... 466 Pinus radiata ..152, 156, 161, 169, 509, 512, 538
Phoracantha semipunctata ......3, 5, 23, 460, 462, Pinus resinosa ........156, 157, 162, 386, 388, 509
464, 465, 466, 486, 495 Pinus strobus ............................ 18, 339, 382, 388
Phorocera ........................................................ 519 Pinus sylvestris ...18, 58, 91, 105, 119, 136, 141,
Phorocera assimilis ........................................ 519 156, 157, 160, 169, 202, 203, 204, 209, 210,
Photorhabdus
a .................................................. 401 333, 339, 354, 356, 357, 374, 456, 509, 511
Phymatodes .................................................... 462 Pinus taeda ....120, 138, 153, 154, 155, 160, 161,
Phymatodes testaceus .................................... 462 169
Phytobia ... 8, 502, 503, 504, 505, 539, 541, 542, Pinus uncinata (Pinus montana) .............. 56, 326
543 Pinus yunnanensis ........... 57, 145, 157, 160, 169
Phytobia betulae ...... 8, 502, 503, 504, 505, 539, Pissodes ..... 6, 20, 21, 22, 23, 25, 26, 38, 39, 41,
540, 541, 542, 543 42, 45, 46, 49, 50, 54, 55, 58, 59, 238, 245,
Phytobia cambii ..............................539, 542, 543 319, 322, 325, 332, 339, 340, 341, 342, 351,
Phytonomus .................................................... 396 357, 383, 384, 385, 386, 387, 389, 395, 398,
Phytophthora .................................................. 454 402, 403, 404, 405, 406, 407, 408, 409, 410,
Phytophthora cinnamomi .............................. 454 412, 415, 419, 489
Picea ..... 18, 56, 58, 73, 119, 136, 137, 154, 160, Pissodes approximatus ...........................385, 389
169, 185, 192, 194, 200, 202, 203, 204, 205, Pissodes castaneus (Pissodes notatus) . 6, 20, 22,
206, 207, 210, 211, 213, 216, 242, 250, 325, 25, 38, 41, 45, 49, 54, 58, 245, 322, 332, 339,
326, 333, 339, 357, 435, 461, 462, 479, 519 340, 341, 342, 385, 386, 402, 403, 404, 405,
Picea abies (Picea excelsa) 18, 56, 58, 119, 136, 406, 408, 409, 416, 419
160, 169, 185, 202, 203, 204, 205, 206, 207, Pissodes fasciatus a ................................... 385, 387
210, 211, 213, 216, 325, 326, 333, 339, 356 Pissodes gyllenhali .................................332, 402
Picea glauca ............................................ 154, 169 Pissodes harcyniae ...6, 322, 332, 340, 383, 402,
Picea glehnii ..................................................... 56 404, 405, 406, 416, 419
Picea jezoensis .................................................. 56 Pissodes nemorensis ......................339, 385, 389
Picea obovata .................................................. 169 Pissodes piceae ...6, 22, 322, 332, 339, 340, 341,
Picea orientalis ............................................... 242 342, 383, 385, 402, 403, 404, 405, 407, 409,
Picea sitchensis ..18, 50, 136, 160, 169, 357, 435 416, 419
Pissodes picivorus .......................................... 389 Platygerrhus ductilis ....................................... 254

Pissodes pini .... 6, 21, 22, 23, 26, 39, 42, 46, 50, Platygerrhus maculatus .................................. 254
55, 59, 249, 322, 323, 326, 332, 339, 340, Platypus ...........................................8, 42, 65, 182
341, 342, 383, 385, 386, 387, 402, 404, 405, Platypus cylindrus .......................................... 182
406, 409, 416, 419 Platypus cylindrus ........................................ 8, 42
Pissodes piniphilus . 6, 21, 22, 26, 39, 42, 46, 50, Platysoma ........................................238, 242, 243
55, 59, 323, 326, 332, 339, 340, 341, 342, Platysoma angustatu
a m ................................... 243
383, 385, 386, 387, 402, 404, 405, 406, 416, Platysoma elongatum m ..................................... 243
419 Platysoma lineare ........................................... 243
Pissodes scabricollis ...............................332, 402 Platystasius ..................................................... 486
Pissodes strobi ......339, 340, 357, 407, 409, 415, Platystasius transversus ................................. 486
433 Plegaderus .......................................238, 243, 477
Pissodes validirostris .... 332, 341, 402, 403, 404, Plegaderus discisus ........................................ 243
405, 406, 407 Plegaderus saucius ......................................... 477
Pityogenes ...7, 20, 22, 23, 24, 28, 29, 34, 37, 40, Plegaderus vulneratus .................................... 243
44, 48, 53, 57, 63, 65, 89, 90, 91, 93, 96, 98, Pleistophoraa ............................................ 306, 307
100, 107, 114, 118, 119, 124, 148, 162, 201, Pleistophora xyloteri ..............................249, 307
210, 241, 242, 243, 245, 246, 259, 260, 249, Plistophora ...................................................... 307
242, 299, 300, 301, 303, 304, 305, 306, 307, Plistophora scolyti ..................................249, 307
308 Podoschistus ...........................................479, 487
Pityogenes bidentatus t ........... 116, 119, 121, 305 Podoschistus scutellaris .........................479, 487
Pityogenes chalcographus ..7, 20, 22, 24, 28, 29, Poemenia ............................... 476, 479, 489, 490
34, 37, 40, 44, 48, 53, 57, 63, 70, 73, 77, 94, Poemenia hectica ............................................ 479
100, 109, 111, 114, 115, 118, 121, 124, 148, Poemenia notata .................... 476, 479, 489, 490
156, 162, 201, 210, 241, 242, 243, 245, 246, Pogonochaerus r ............................................... 462
247, 248, 249, 250, 260, 249, 242, 299, 300, Pogonochaerus fasciculatus ........................... 462
301, 302, 303, 304, 305, 306, 307, 308 Polygraphus 7, 21, 22, 26, 39, 43, 46, 50, 55, 59,
Pityogenes conjunctus 7, 23, 246, 247, 248, 249, 195, 201, 211, 246, 259, 242, 295, 298, 299,
250 303, 305, 308
Pityogenes quadridens
d ........................... 201, 210 Polygraphus poligraphus ......................................
Pityogenes trepanatus 7, 246, 247, 248, 249, 250 Polygraphus poligraphus ... 7, 21, 22, 26, 39, 43,
Pityokteines 7, 21, 22, 26, 39, 42, 46, 47, 50, 55, 46, 50, 55, 59, 195, 201, 211, 246, 247, 248,
59, 114, 148, 246, 305, 307, 308 249, 250, 242, 295, 298, 299, 303, 305, 308
Pityokteines curvidens . 7, 21, 22, 26, 39, 42, 46, Polystenus .......................................490, 491, 494
50, 55, 59, 114, 148, 246, 305, 307 Polystenus rugosus .........................490, 491, 494
Pityokteines spinidens 7, 22, 246, 247, 248, 249, Populus .. 18, 114, 117, 118, 120, 324, 451, 452,
250, 308 459, 461, 462, 470, 487, 492, 517, 522, 530,
Pityokteines vorontzovi ....................... 7, 22, 246 531, 532, 539
Pityophagus .................................................... 244 Populus albaa .................... 18, 324, 461, 470, 531
Pityophagus ferrugineus ................................ 244 Populus canadensis ....................................... 324,
Pityophthorus .....7, 22, 50, 65, 66, 89, 111, 306, Populus canescens .......................................... 531
307 Populus deltoides ...................................114, 120
Pityophthorus micrographus ........................... 50 Populus nigra ................... 18, 324, 509, 510, 531
Pityophthorus pityographus ....7, 22, 65, 66, 306, Populus tomentosa ......................................... 461
307 Populus tremula
m ............... 18, 117, 324, 470, 531
Placonotus ....................................................... 243 Populus virginianaa .......................................... 324
Placusa .................................................... 238, 245 Prinobius ......................................................... 462
Placusa adscita ................................................ 245 Prinobius scutellaris ....................................... 462
Placusa atrata
t .................................................. 245 Prionus ............................................................ 462
Placusa depressa ............................................. 245 Prionus coriarius ............................................. 462
Placusa tachyporoide
y s .................................... 245 Pristiphora ....................................................... 503
Plagionotus
t ..................................................... 462 Pristomerus .............................................511, 523
Plagionotus arcuatus ...................................... 462 Pristomerus orbitali
r s ...................................... 511
Plastanoxus ..................................................... 257 Pristomerus vulneratorr ................................... 523
Plastanoxus westwoodi .................................. 257 Proctolaelaps .................................................. 249
Platygerrhus ............................................ 249, 254 Proctolaelaps fiseri ......................................... 249
Platygerrhus affinis ........................................ 249
Proctolaelaps pini .249, 322, 323, 326, 332, 339, Rhagium ..................................................462, 483
340, 341, 342, 383, 386, 387, 402, 404, 405, Rhagium bifasciatum ..................................... 462
406, 409 Rhagium inquisitor .................................462, 483
Proctolaelaps xyloteri .................................... 249 Rhagium mordax ............................................ 462
Profeltiella ...................................................... 542 Rhaphitelus ............................ 240, 249, 251, 255
Profeltiella dizogymyzae ............................... 542 Rhaphitelus ladenbergii .........................249, 255
Prunus ...............................................18, 250, 539 Rhaphitelus maculatus ...........................251, 255
Pseudohylesinus ............................................. 156 Rhimphoctona ..... 479, 480, 481, 482, 487, 489,
Pseudomonas ..................................296, 297, 485 490
Pseudomonas alcaligenes .............................. 297 Rhimphoctona grandis .......... 260, 244, 253, 487
Pseudomonas caviae ...................................... 296 Rhimphoctona lucida .............................479, 482
Pseudomonas cepacia .................................... 297 Rhimphoctona megacephalus ................479, 489
Pseudomonas chlororaphys ........................... 296 Rhimphoctona obscuripes ............................. 479
Pseudomonas paucimobilis ........................... 297 Rhimphoctona pectoralis .......................479, 490
Pseudomonas septica ............................. 296, 485 Rhimphoctona teredo ..................................... 480
Pseudomonas syringae ................................... 297 Rhimphoctona xoridiformis ..................480, 482
Pseudopityophthorus t ........................................ 51 Rhinophora ..................................................... 488
Pseudopityophthorus minutissimus ................ 51 Rhinophora lepida .......................................... 488
Pseudopityophthorus pruinosus ...................... 51 Rhizophagus ...82, 259, 260, 244, 253, 254, 255,
Pseudotsuga ................. 8, 18, 119, 156, 169, 387 256
Pseudotsuga menziesii ...... 8, 119, 156, 169, 387 Rhizophagus bipustulatus ......................244, 254
Psychophagus ................................................. 249 Rhizophagus cribratus .................................... 244
Psychophagus omnivorusm .............................. 249 Rhizophagus depressus ..........................260, 244
Pteromalus .............................................. 249, 255 Rhizophagus dispar ........................260, 244, 254
Pteromalus abieticolaa ..................................... 249 Rhizophagus ferrugineus
r .......................244, 254
Pteromalus brunnicans
r ................................... 255 Rhizophagus grandis ..... 82, 260, 244, 253, 255,
Pteromalus puparum ...................................... 249 256
Pterostichus ..................................................... 359 Rhizophagus nitidulus ................................... 244
Pyemotes ................................................. 241, 249 Rhizophagus perforatus ................................. 244
Pyemotes dryas ............................................... 249 Rhizophagus puncticollis ............................... 244
Pyemotes herfsi .............................................. 249 Rhopalicus ....240, 242, 244, 245, 249, 251, 255,
Pyemotes scolyti ............................................ 249 254, 403, 405, 408, 491
Pygostolus .......................................397, 410, 436 Rhopalicus guttatus ....... 249, 403, 405, 408, 491
Pygostolus falcatus ......................................... 436 Rhopalicus quadratus .............................249, 251
Pyrrhidium ...................................................... 462 Rhopalicus tutela ..240, 242, 244, 245, 249, 255,
Pyrrhidium sanguineum
a m ................................. 462 254, 403, 405, 408
Pytho ....................................................... 238, 244 Rhoptrocentrusr ............................................... 253
Pytho depressus ...................................... 238, 244 Rhoptrocentrus piceus .................................... 253
Quadrastichus ......................................... 491, 494 Rhyacionia ..8, 20, 22, 24, 32, 35, 37, 41, 44, 48,
Quadrastichus misellus .................................. 491 53, 57, 502, 503, 504, 507, 508, 510, 511,
Quedius ........................................................... 245 512
Quedius laevigatus ......................................... 245 Rhyacionia buoliana .... 8, 20, 22, 24, 32, 35, 37,
Quedius plagiatus ........................................... 245 41, 44, 48, 53, 57, 502, 503, 504, 507, 508,
Quercus .. 18, 105, 118, 184, 211, 213, 250, 356, 509, 510, 511, 512
451, 452, 454, 461, 462, 487, 492, 517, 521, Rhyacionia duplana ........................................ 507
539 Rhyacionia piniana ......................................... 507
Quercus alba ................................................... 105 Rhyacionia pinicolana ...........................503, 507
Rabocerus ....................................................... 244 Rhyacionia pinivoranaa ................................... 507
Rabocerus foveolatus ..................................... 244 Rhynchophorus r .............................................. 358
Rabocerus gabrieli
a ......................................... 244 Rhyssa ............................ 478, 480, 482, 487, 537
Raphidia ..........................................482, 483, 506 Rhyssa amoena .......................................480, 487
Raphidia flavipes (Dichrostigma flavipes) ... 248 Rhyssa persuasoria .........................480, 482, 487
Raphidia notata (Phaeostigma notata) . 248, 479, Rickettsia ........................................................ 293
483 Rondania ......................................................... 410
Raphidia xanthostigma
t a .................................. 482 Ropalophorus ........................ 241, 242, 243, 248
Resinicium ...................................................... 437 Ropalophorus clavicornis ..... 241, 242, 243, 248
Resinicium bicolor ......................................... 437 Roptrocerus ............240, 242, 244, 245, 249, 255
Roptrocerus brevicornis .........................240, 249 120, 240, 244, 252, 253, 254, 255, 256, 257,
Roptrocerus mirus ................. 240, 244, 249, 255 254, 296, 298, 302, 307, 493
Roptrocerus xylophagorum . 240, 243, 244, 245, Scolytus pygmaeus ......................................... 307
249, 251 Scolytus quadrispinosus .......................... 94, 105
Saccharomyces ............................................... 185 Scolytus ratzeburgi .......................7, 23, 298, 301
Salix 18, 324, 451, 452, 459, 461, 462, 492, 517, Scolytus rugulosu
r s ......................................... 120
521, 531, 539 Scolytus scolytus .... 7, 20, 21, 24, 29, 34, 37, 40,
Salix caprea .............................................. 18, 324 42, 44, 48, 53, 57, 64, 65, 66, 67, 74, 201,
Salix fragilis .............................................. 18, 324 239, 252, 296, 297, 298, 301, 307
Salix purpurea ................................................ 324 Scolytus sulcifrons ............................................. 7
Salix triandra
a .................................................. 324 Scolytus triarmatus . 7, 21, 23, 27, 39, 43, 47, 50,
Salix viminalis ........................................324, 325 55, 60
Salpingus ................................................ 238, 244 Scolytus ventralis .105, 148, 149, 152, 156, 159,
Salpingus planirostris ..................................... 238 160, 169
Salticus ............................................................ 506 Semanotus ....................................................... 462
Salticus cingulatus .......................................... 506 Semanotus laurasi
a .......................................... 462
Saperda ...... 5, 21, 22, 26, 39, 43, 47, 50, 55, 60, Serratiaa ............................................................ 296
459, 460, 461, 462, 469, 470, 475, 476, 483, Serratia marcescens ........................................ 296
485, 487, 488, 494, 496, 503, 533 Sesia ... 8, 22, 502, 504, 505, 526, 528, 530, 531,
Saperda carcharias . 5, 21, 22, 26, 39, 43, 47, 50, 533
55, 60, 462, 469, 475, 483, 484, 485, 487, Sesia apiformis ...8, 22, 502, 504, 505, 526, 528,
488, 533 530, 531, 532
Saperda populnea ... 5, 21, 22, 26, 39, 43, 47, 50, Silvanus ........................................................... 245
55, 60, 460, 462, 469, 470, 475, 483, 484, Silvanus bidentatus ........................................ 245
485, 487, 488, 503 Silvanus unidentatus ...................................... 245
Scambus .................405, 406, 407, 510, 511, 515 Sirex ... 8, 21, 23, 27, 39, 43, 47, 51, 56, 60, 482,
Scambus brevicornis ..............................405, 511 502, 504, 505, 534, 535, 536, 537, 538
Scambus calobatus ......................................... 511 Sirex cyaneus ..............................8, 482, 502, 504
Scambus capitator .......................................... 515 Sirex juvencus (Paururus juvencus) .... 8, 21, 23,
Scambus sagax ...............................405, 407, 511 27, 39, 43, 47, 51, 56, 60, 502, 504, 505
Scambus sudeticus ................................. 405, 407 Sirex noctilio ................. 504, 505, 535, 537, 538
Schreineria ..............................................410, 523 Sitonaa .............................................................. 396
Schreineria zeuzerae ...................................... 523 Sorbus ...............................................18, 324, 539
Sclerodermus
m .................................................. 257 Sorbus aucuparia a ...................................... 18, 324
Sclerodermus brevicornis .............................. 257 Spathius 248, 253, 405, 408, 489, 491, 492, 493,
Sclerodermus domesticus .............................. 257 494
Scoloposcelis .......................................... 240, 248 Spathius brevicaudis ............. 248, 253, 491, 494
Scoloposcelis obscurellaa ................................ 248 Spathius curvicaudis ............. 253, 491, 492, 493
Scoloposcelis pulchella .......................... 240, 248 Spathius depressus ......................................... 491
Scolytoplatypus ................................................ 47 Spathius exarator ....................................248, 253
Scolytus 7, 20, 21, 22, 23, 24, 26, 27, 29, 34, 37, Spathius lignarius ........................................... 491
39, 40, 41, 42, 43, 44, 47, 48, 49, 50, 51, 53, Spathius melanophilae
a ...........................491, 492
55, 57, 60, 64, 65, 66, 89, 93, 104, 105, 108, Spathius phymatodis ...................................... 491
120, 148, 149, 184, 200, 201, 211, 221, 223, Spathius polonicus .................................491, 493
238, 239, 240, 242, 243, 244, 252, 253, 254, Spathius radjabii .....................................489, 491
255, 256, 257, 259, 242, 252, 254, 296, 297, Spathius radzayanus ...............................491, 494
298, 299, 301, 302, 307, 493 Spathius rubidus ....248, 405, 408, 491, 492, 493
Scolytus ensifer .............................................. 307 Sphaeriestes .................................................... 245
Scolytus intricatus .. 7, 21, 22, 26, 39, 43, 47, 50, Sphaeriestes castaneus ................................... 245
55, 60, 184, 201, 211, 299 Sphaerulariopsis ............................................. 409
Scolytus kirschii ............................................. 299 Spicaria ...................................................298, 520
Scolytus laevis ..7, 20, 22, 24, 34, 37, 41, 44, 48, Spicaria cossus ............................................... 520
53, 57, 298 Spicaria: see Paecilomyces
Scolytus morawitzi ........................................... 51 Sporothrix .......................................186, 189, 194
Scolytus multistriatus ... 7, 20, 22, 24, 29, 34, 37, Staphylococcus ............................................... 297
40, 44, 48, 49, 53, 57, 64, 67, 73, 74, 113, Staphylococcus lentus .................................... 297
Steinernema ...401, 409, 411, 468, 488, 521, 525
Steinernema carpocapsae ..... 401, 409, 411, 468, Thaumetopoea ................................................ 156
525 Thaumetopoea pityocampaa ........................... 156
Steinernema feltiae ................ 401, 411, 521, 525 Theocolax ....................................................... 255
Steinernema glaseri ........................................ 521 Theocolax formiciformis ............................... 255
Stempelliaa ............................................... 306, 307 Thielaviopsis ..........................................186, 188
Stempellia scolyti ........................................... 307 Thuja ...................................................18, 74, 462
Stenarellaa ................................................ 396, 519 Tilia ......... 19, 358, 452, 517, 519, 521, 523, 531
Stenarella gladiator ................................396, 519 Tolmerus ......................................................... 246
Stenomacrusr ................................................... 488 Tolmerus atricapillus ..................................... 246
Stenomacrus pusillatorr ................................... 488 Tolypocladium ............................................... 300
Stenomesius .................................................... 255 Tolypocladium cylindrosporum .................... 300
Stenomesius abbasi ........................................ 525 Tomicobia .....241, 242, 243, 245, 249, 396, 397,
Stenomesius rufescens ................................... 255 410, 436
Steremnius ......................................382, 385, 387 Tomicobia acuminati .............................241, 242
Steremnius carinatus .............................. 385, 387 Tomicobia pityophthori 241, 242, 243, 245, 249
Strophosoma .......................... 319, 320, 324, 356 Tomicobia seitneri ......... 241, 242, 243, 245, 249
Strophosoma capitata ..................................... 324 Tomicus ..7, 8, 20, 21, 22, 24, 25, 30, 31, 34, 37,
Strophosoma melanogramma ................ 324, 356 38, 41, 44, 45, 48, 49, 53, 54, 56, 57, 58, 59,
Symphya ......................................................... 543 63, 65, 67, 68, 70, 71, 73, 78, 89, 90, 91, 92,
Symphya hians ............................................... 543 93, 96, 98, 105, 106, 108, 137, 145, 148, 149,
Symphya ringens ............................................ 543 157, 169, 184, 192, 194, 201, 211, 212, 238,
Synanthedon .......................................8, 502, 524 246, 259, 260, 242, 252, 254, 303, 305, 308,
Synanthedon myopaeformis f ..............8, 502, 524 354, 386, 416, 503
Syngaster ........................................................ 466 Tomicus brevipilosus ....................................... 57
Syngaster lepidus ........................................... 466 Tomicus destruens (Blastophagus destruens) . 7,
Taphrorychus ......................... 200, 201, 211, 242 57, 63, 68, 69, 71, 250
Taphrorychus bicolor ............ 200, 201, 211, 242 Tomicus minor (Blastophagus minor) . 7, 20, 22,
Tarsonemus
m .................................................... 197 25, 38, 41, 45, 49, 54, 57, 58, 59, 64, 65, 66,
Tarsonemus krantzi ........................................ 197 68, 71, 98, 114, 156, 157, 184, 200, 201, 211,
Taxus ............................................................... 343 215, 222, 246, 247, 248, 249, 250, 260, 305,
Telenomus .............................................. 506, 528 386
Telenomus aradi ............................................. 506 Tomicus pilifer ................................................. 57
Telenomus phalaenarum ................................ 528 Tomicus piniperda (Blastophagus piniperda) 8,
Telosporidium ........................................ 304, 306 20, 21, 24, 30, 31, 34, 37, 41, 44, 48, 49, 53,
Telosporidium typographi ..................... 304, 306 57, 58, 59, 63, 65, 66, 68, 69, 70, 71, 72, 73,
Temelucha ...................................................... 511 74, 76, 78, 79, 80, 83, 90, 91, 92, 93, 94, 95,
Temelucha interruptor ................................... 511 96, 98, 105, 106, 108, 109, 110, 111, 115,
Tetrastichus .............................................491, 494 116, 117, 137, 140, 143, 145, 146, 148, 149,
Tetrastichus heeringi .............................. 491, 494 156, 157, 160, 161, 169, 192, 194, 201, 212,
Tetrastichus murciaa ........................................ 491 220, 238, 246, 247, 248, 249, 250, 259, 260,
Tetropium ...6, 21, 22, 27, 39, 43, 47, 51, 56, 60, 252, 254, 255, 298, 301, 303, 305, 308, 354,
459, 461, 462, 468, 469, 475, 476, 477, 478, 386, 416
479, 480, 481, 482, 483, 494 Tomicus puellus ............................................... 57
Tetropium castaneum (Isarthron castaneum) ...6, Tomoxia .......................................................... 494
22, 461, 462, 469, 475, 478, 481, 482, 6 Tomoxia biguttata t .......................................... 494
Tetropium fuscum .... 6, 462, 469, 475, 478, 481, Torneumaa ........................................................ 318
482, 483, 495 Torymus .......................................................... 256
Tetropium gabrieli (Isarthron gabrieli) 6, 21, 22, Torymus arundinis
r ......................................... 256
27, 39, 43, 47, 51, 56, 60, 459, 461, 462, 468, Torymus hylesini ............................................ 256
475, 478, 481, 482, 483 Townesia .................................................480, 488
Thanasimus ...259, 242, 251, 252, 254, 256, 409, Townesia tenuiventris ............................480, 488
482, 483, 489, 493, 494 Toxoneura ...............................................240, 248
Thanasimus femoralis .................................... 242 Toxoneura usta (Palloptera usta) ..240, 248, 482,
Thanasimus formicarius ...... 259, 251, 254, 256, 483
409, 482, 483, 489, 493, 494 Toxotus ........................................................... 462
Thanasimus rufipes ................................ 242, 489 Toxotus cursor
u ................................................ 462
Thanasimus undatulus ................................... 254 Trachodes ........................................319, 323, 326
Trachodes hispidus ........................................ 323 Virgichneumon ............................................... 488

Tremex .................................................... 534, 537 Virgichneumon monostagon ......................... 488
Tremex longicollis ......................................... 537 Xanthomonas .................................................. 297
Triarthria ......................................................... 488 Xanthomonas maltophilia .............................. 297
Triarthria setipennis ....................................... 488 Xenorhabdus
a ................................................... 401
Trichogramma ....................... 239, 256, 511, 512 Xeris ................................................................ 534
Trichogramma dendrolimi ............................. 512 Xiphydria ........................................................ 537
Trichogramma nerudai .................................. 512 Xiphydria ogasawarai .................................... 537
Trichogramma semblidis ....................... 239, 256 Xorides ...........248, 477, 480, 481, 488, 490, 494
Trichogramma telengai .......................... 511, 512 Xorides aterr ............................................ 480, 481
Trichomalus .................................................... 491 Xorides brachylabis a .......................480, 482, 483
Trichosporium .................................................. 97 Xorides depressus ..................................488, 490
Trichosporium symbioticum ......................... 157 Xorides ephialtoides ....................................... 480
Trichouropoda ................................................ 249 Xorides fuligator a .................................... 477, 480
Trichouropoda bipilis ..................................... 249 Xorides irrigator ....248, 480, 481, 482, 483, 490
Trigonoderus .......................................... 255, 492 Xorides praecatorius ............. 480, 481, 490, 494
Trigonoderus cyanescens .......................255, 492 Xorides propinquus ........................................ 480
Trogossitaa ....................................................... 468 Xyleborus ......8, 22, 47, 65, 74, 77, 89, 181, 196,
Trogossita japonica
a ........................................ 468 198, 199, 213, 252, 253, 254, 255, 256, 257,
Troxochrus ...................................................... 249 254
Troxochrus nasutus ........................................ 249 Xyleborus alni ................................................ 198
Trypodendron ...8, 20, 21, 22, 23, 25, 27, 38, 40, Xyleborus cryptographus ............................... 198
42, 43, 45, 46, 47, 49, 51, 54, 56, 58, 60, 63, Xyleborus dispar (Anisandrus dispar) . 8, 22, 65,
65, 74, 77, 89, 100, 104, 108, 238, 252, 253, 68, 74, 118, 181, 196, 198, 199, 213, 296
254, 255, 256, 257, 260, 242, 296, 299, 300, Xyleborus dryographus ..........................198, 213
302, 307 Xyleborus eurygraphus .................................. 198
Trypodendron domesticum (Xyloterus Xyleborus fornicatus ...................................... 254
domesticus) .8, 21, 22, 27, 40, 43, 47, 51, 56, Xyleborus monographus ....... 196, 198, 199, 213
60, 74, 116, 117, 196, 198, 199, 213, 252, Xyleborus saxeseni ........................196, 199, 213
253, 254, 255, 256, 257, 307 Xylocoris ................................................240, 248
Trypodendron lineatum (Xyloterus lineatus) ...8, Xylocoris cursitans .................................240, 248
20, 22, 25, 38, 42, 45, 49, 54, 58, 63, 74, 100, Xylophagus .............................................409, 489
103, 109, 114, 195, 196, 198, 199, 213, 247, Xylophagus cinctus ................................409, 489
248, 249, 250, 260, 242, 296, 299, 300, 302 Xylophrurus ............................................488, 490
Trypodendron signatum (Xyloterus signatus) ..8, Xylophrurus aaugustus ............................488, 490
23, 196, 198, 199, 214, 238 Xylophrurus lancifer
a r ...................................... 488
Ulmus ...........19, 29, 74, 120, 169, 211, 250, 517 Xylosandrus ...........................................................
Ulmus americana ........................................... 120 Xylosandrus ..............................8, 47, 50, 77, 238
Unikaryon .......................................306, 307, 308 Xylosandrus germanus (Xyleborus germanus) 8,
Unikaryon minutum ....................................... 307 50, 196, 198, 199, 213, 238
Unikaryon montanum m .................................... 308 Xylotachina ..................................................... 519
Unikaryon polygraphi .................................... 308 Xylotachina dilutaa .......................................... 519
Urocerus ......8, 21, 22, 27, 40, 43, 47, 51, 56, 60, Xyloterus domesticus: see Trypodendron
502, 504, 505, 534, 535, 536 domesticum
Urocerus aaugur ........................................... 8, 535 Xyloterus levae ............................................... 198
Urocerus gigas ..8, 21, 22, 27, 40, 43, 47, 51, 56, Xyloterus lineatus: see Trypodendron lineatum
60, 502, 504, 505, 536 Xyloterus signatus: see Trypodendron
Venturiaa .......................................................... 515 signatum
Venturia robusta ............................................. 515 Zabrachia ................................................248, 489
Verticilliumm .................... 299, 300, 301, 302, 520 Zabrachia minutissima ...........................248, 489
Verticillium lecanii 299, 300, 301, 302, 303, 520 Zabrachia tenella ............................................ 248
Vibrio .............................................................. 297 Zeiraphera ....................................................... 156
Vibrio alginolyticus ....................................... 297 Zeiraphera diniana .......................................... 156

Bark and Wood Boring Insects in Living Trees in Europe, A Synthesis

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Bark and Wood Boring Insects in Living Trees in Europe,

ISBN 978-1-4020-2240-1 (HB)

Printed on acid-free paper

First Edition 2004, Reprinted 2007

All Rights Reserved

The BAWBILT bases in Europe…………………................................…….1

Chapter 1 The BAWBILT context in Europe……………....................……3

Chapter 2 The directory of European experts…………......................……11

Chapter 3 The BAWBILT database……………………….........................15

Chapter 4 Damage and control of BAWBILT organisms, an overview…..19

Part 1, Bark Beetles.......................................................................................39

Chapter 5 Taxonomy and systematics off bark and ambrosia beetles……...41

Chapter 6 Genetic tools in Scolytid research…………………...................55

Chapter 7 General biology of bark beetles……………............…………...63

Chapter 8 Chemical ecology of bark beetles in a complex olfactory

Chapter 9 Host resistance to bark beetles and its variations….....……….135

Chapter 10 Fungal associates of European bark beetles with special

Chapter 11 Research on parasitoids and predators of Scolytidae,

Chapter 12 Pathogens in bark beetles……………………………….........291

Part 2, Bark Weevils....................................................................................315

Chapter 13 Taxonomy and systematics of bark weevils…………......…..317

Chapter 14 General biology and life cycles of bark weevils……………..331

Chapter 15 Semiochemicals in the life of bark feeding weevils………....351

Chapter 16 Hylobius abietis – Host utilisation and resistance………..….365

Chapter 17 Fungi associated with Hylobius abietis and other weevils…..381

Chapter 18 Parasitoids, predators, nematodes and pathogens

Chapter 19 Damage, control and management of weevil pests,

Part 3, Buprestids and Longhorns................................................................445

Chapter 20 Biology, ecology and economic importance of Buprestidae

Chapter 21 Natural enemies of Cerambycidae and Buprestidae infesting

Part 4, “Non-Coleopteran” BAWBILT organisms......................................499

Chapter 22 Non-Coleopteran insects…………………………………..…501

Research needs and priorities for Europe....................................................539

Chapter 23 General conclusions and research priorities for BAWBILT

Index of scientific names……………………………………….........……553

Ayres, Matthews P., Department of Biological Sciences, Hanover, USA. “Tree

List 2. BAWBILT experts who participated actively in the Action.

Lempérière, Guy, Université Joseph Fourrier, Grenoble

Nunes, Luisa, Escola Superior Agrária de Castelo Branco

THE BAWBILT CONTEXT IN EUROPE

WHAT ARE EUROPEAN BAWBILT?

Table 1. Recorded European BAWBILT species. Main synonyms are in brackets

Trypodendron domesticum ((Xyloterus domesticus)

OBJECTIVES AND RESULTS OF THE BAWBILT ACTION

pets, almost each country has its own strategy.

PARTICIPANTS AND ORGANIZATION OF THE RESEARCH WORK

organisms were approached through a questionnaire, including those not directly

This directory facilitated exchange of information and can continue to be used as a

MANAGEMENT OF THE BAWBILT ACTION

representative (the corresponding NTS) of each participating countryt and chaired by

THE DIRECTORY OF EUROPEAN EXPERTS

A. BATTISTI & M. FACCOLI

University of Padova, Agripolis, 35020 Legnaro PD, Italy

2. RESULTS AND DISCUSSION

Forest area (10^6 ha)

Figure 1. Distribution of experts involved in BAWBILT among 23 countries which showed an

Conifer and broadleaved tree genera

Conifer and broadleaved insect genera

Table 1. List of fields of interest in BAWBILT