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P o l l i n at i o n a n d F l o r a l E c o l o g y
This page intentionally left blank
P o l l i n at i o n a n d F l o r a l E c o l o g y

Pat Willmer

Princeton University Press

Princeton and Oxford
Copyright © 2011 by Princeton University Press
Published by Princeton University Press, 41 William Street,
Princeton, New Jersey 08540
In the United Kingdom: Princeton University Press, 6 Oxford Street,
Woodstock, Oxfordshire OX20 1TW
press.princeton.edu
Jacket photograph: The bee Eucera longicornis foraging on the sweet pea
Lathyrus. (c) Andrej Gogala

All Rights Reserved

Library of Congress Cataloging-in-Publication Data

Willmer, Pat, 1953-
Pollination and floral ecology / Pat Willmer.
    p. cm.
Includes bibliographical references.
ISBN 978-0-691-12861-0 (cloth : alk. paper) 1. Pollination. 2. Polli-
nation by insects. 3. Pollination by animals. 4. Plant ecology. I. Title.
QK926.W55 2011
571.8'642—dc22 2010049061

British Library Cataloging-in-Publication Data is available

This book has been composed in Times

Printed on acid-free paper ∞

Printed in the United States of America

10 9 8 7 6 5 4 3 2 1
 Contents

Preface vii
Acknowledgments ix

Part I Ess e nt i als of F low er D e si gn an d F unct i on

Chapter 1 Why Pollination Is Interesting 3

Chapter 2 Floral Design and Function 11
Chapter 3 Pollination, Mating, and Reproduction in Plants 55
Chapter 4 Evolution of Flowers, Pollination, and Plant Diversity 88

Part II F loral Ad ve rt i s e m ents an d F loral Re war d s

Chapter 5 Advertisements 1: Visual Signals and Floral Color 105

Chapter 6 Advertisements 2: Olfactory Signals 134
Chapter 7 Rewards 1: The Biology of Pollen 154
Chapter 8 Rewards 2: The Biology of Nectar 190
Chapter 9 Other Floral Rewards 221
Chapter 10 Rewards and Costs: The Environmental Economics of Pollination 234

Part III Poll i nat i on S yn d rom e s?

Chapter 11 Types of Flower Visitors: Syndromes, Constancy, and Effectiveness 261

Chapter 12 Generalist Flowers and Generalist Visitors 288
Chapter 13 Pollination by Flies 304
Chapter 14 Pollination by Butterflies and Moths 322
Chapter 15 Pollination by Birds 337
Chapter 16 Pollination by Bats 356
Chapter 17 Pollination by Nonflying Vertebrates and Other Oddities 370
Chapter 18 Pollination by Bees 378
Chapter 19 Wind and Water: Abiotic Pollination 418
Chapter 20 Syndromes and Webs: Specialists and Generalists 434
vi • Contents

Part I V F loral Ecology

Chapter 21 The Timing and Patterning of Flowering 483

Chapter 22 Living with Other Flowers: Competition and Pollination Ecology 503
Chapter 23 Cheating by Flowers: Cheating the Visitors and Cheating Other Flowers 524
Chapter 24 Flower Visitors as Cheats and the Plants’ Responses 542
Chapter 25 The Interactions of Pollination and Herbivory 554
Chapter 26 Pollination Using Florivores: From Brood Site Mutualism to
 Active Pollination 565
Chapter 27 Pollination in Different Habitats 575
Chapter 28 The Pollination of Crops 605
Chapter 29 The Global Pollination Crisis 620

Appendix 639
Glossary 643
References 663
Subject Index 751
Index of Animal Genera 768
Index of Plant Genera 771
 P r ef a c e

When I first became interested in pollination biology ers in the field: Jones and Little (1983) began the trend
around thirty years ago, there was essentially just one with Handbook of Experimental Pollination Ecology,
book to consult for core information, the classic by while Lloyd and Barrett (1996) produced Floral Biol-
Faegri and van der Pijl, The Principles of Pollination ogy: Studies on Floral Evolution in Animal Pollinated
Ecology, which has been the inspiration to genera- Systems, opening up a broader and more ecological
tions, its last edition appearing in 1979 but still struc- and evolutionary perspective on the whole subject.
tured around the 1966 original. But twenty years on I Then two collected contributions came along in 2006,
became frustrated that there had been no single vol- picking up the themes that had been emerging in the
ume since that date which covered the field. This is preceding decade: Waser and Ollerton in Plant-Polli-
particularly extraordinary given that the subject itself nator Interactions: From Specialization to General-
has expanded and blossomed prodigiously, both in its ization, and Harder and Barrett in Ecology and Evolu-
own right and as a testing ground for wider theories, as tion of Flowers. These have been seen as especially
well as having assumed greater importance in both sci- important in expounding new approaches and expos-
entific circles and as a wider public concern. ing older assumptions to a more critical analysis. The
It has not been all quiet on the publishing front debates about generalization and specialization, and
since the 1970s of course. There have been excellent the usefulness of the syndrome concept or of alterna-
books with more of a natural history approach (M. tive modeling approaches, have been particularly
Proctor et al. 1996; Buchmann and Nabhan 1996) and thought-provoking, so that anyone starting out as a re-
botanical books concentrating on floral structures searcher in pollination ecology will find much to en-
(Barth 1985; Endress 1994) or on floral development gage them from the authors represented in those two
(Glover 2007). Over the same period many extremely books.
useful edited volumes have also appeared, each with Those readers, however, would not get the back-
chapters contributed by experts updating readers on ground information, the core material of pollination
particular themes, such as nectar and nectaries (Bent- and floral biology. A beginner would still have to ex-
ley and Elias 1983; Nicolson et al. 2007), anthers and plore very widely across the mass of scientific jour-
pollen (D’Arcy and Keating 1996; Dafni et al. 2000), nals, hoping to light upon a reasonably up-to-date re-
and floral scents (Dudareva and Pichersky 2006). Sev- view article. And in the last decade the primary
eral books have compiled useful reviews on practical literature has undergone an extraordinary explosion in
techniques (Dafni 1992; Kearns and Inouye 1993; volume, almost more than in any other field, partly be-
Dafni et al. 2005) or on applied aspects of crop polli- cause of the practical and applied environmental prob-
nation (Free 1993), while Chittka and Thomson (2001) lems now seen to be emerging with pollination ser-
took a fresh approach by assembling chapters on as- vices, and partly because around twenty-five years ago
pects of pollinator cognition and learning. interest began to spread much more widely beyond the
But perhaps most important have been a select few European and North American temperate pollination
edited volumes with broader pollination coverage and systems, with expertise emerging especially in the
sometimes a more eclectic assemblage of contribu- New and Old World Tropics, in southern Africa and
tions. Here the editors have been very much the lead- Australia, and in Japan and China.
viii • Preface

For all these reasons, it seemed to me timely to at- those highly respected authors whose work I draw
tempt a book that would cover the subject more thor- heavily on. Some, seeing pollination biology as pio-
oughly, providing chapters on every key topic, and neering a new era where ecological modelers have
serve both as an introduction for anyone coming into more to tell us than old-style field workers, might
the field as advanced undergraduate or postgraduate find my approach too traditional. But at least those
and as a source book for professionals. Begun half coming in to the field hereafter may gain a better un-
way through the decade, it has inevitably burgeoned derstanding of the foundations on which models can
beyond the original intentions as the expanding litera- be built and so will better see where the key issues
ture burst around my ears, to the distress of my pub- may lie.
lishers. But the resulting book will, I hope, achieve at
least part of its aims and will not too greatly annoy Pat Willmer, November 2009
 A c k n o w l e d g me n t s

It is a pleasure to begin by thanking the many genera- Peter Gibbs, Aubrey Manning, Gidi Ne’eman, Sue Ni-
tions of students and postgraduates who have let me colson, Samy Zalat, Theodora Petanidou, Chris
know when I taught them in ways that inspired their O’Toole, and Rob Raguso.
interest and when I merely confused them. From Several of these colleagues have read and com-
them, I realized where the real fascinations of pollina- mented wisely on outlines, drafts, or chapters for me,
tion lay and where my own interests were too biased and to them I owe enormous gratitude and an apology
or quirky for a wider audience—I have tried, not al- where I have insufficiently taken on their criticisms;
ways successfully, to play down those quirks. Many the misconceptions or infelicities that remain are en-
former postgraduates and postdocs, now running re- tirely my fault. Particular thanks to Clive Nuttman on
search groups of their own and blossoming into major color and scent issues, Peter Gibbs on incompatibility
players in the world pollination and mutualism de- and on general issues of specialization and syndromes,
bates, have been especially important to me, and I Francis Gilbert (especially for updating my dipteran
thank them all for discussions, arguments, and the taxonomy), and Jonathan Pattrick for taking a broad
chance to read and learn from their own works; in par- beginner’s view of the book and being even more per-
ticular I must pay tribute to Graham Stone (GS) and snickety about semicolons than I am!
Simon Potts (SP), and more recently to Clive Nutt- I am deeply grateful to many who have allowed me
man (CN), Betsy Vulliamy, Gavin Ballantyne (GB), to use their photographs, which usually put my own
Caroline King, and Jonathan Pattrick, and to those efforts to shame. All are acknowledged by initials in
whose names are followed by initials for use of their the plates, and all of course retain their copyrights in
photos. the photos reproduced here. Susie Whiten (SW), Ali-
On a wider front, I confess to being a very poor son Fernie (AF), Ian Johnston (IJ), and Sandy Edwards
networker, so that I know the pollination biologists of (SE) were generous with their own photographs from
the world far less well on a personal level than I should, the UK and abroad. Special thanks to Steve Johnson
which is my loss. My communications with them have (SJ), Dino Martens (DM), Karen Sarkisyan (KS), and
nevertheless been wonderfully invigorating, and I Andrej Gogala (AG) for supplying superb photographs
thank so many of them for their generosity in exchang- of the more difficult animal visitors. I also owe a mas-
ing ideas. In particular, I have benefitted at various sive debt of gratitude to my illustrators, especially
times from conversations about bees or pollination or Dawn Toshack for most of the pictures of flowers and
wider mutualisms, whether prolonged or brief (and visitors and their detailed structures, and Caroline
some so brief they will scarcely remember me!), with King for reproducing most of the graphical figures
Jane Memmott, Steve Johnson, Judith Bronstein, Sally from other published works, as well as to Dimitri Kar-
Corbet, Florian Schiestl, Dick Southwood, Naomi etnikov for advice on figures in general. I must also
Pierce, Amots Dafni, Nigel Raine, Ingrid Williams, thank others at Princeton University Press who have
Cathy Kennedy, Francis Gilbert, Dino Martens, John patiently supported my efforts to complete this work;
Free, Jette Knudsen, James Cresswell, Steve Bullock, for the initial enthusiasm of Robert Kirk especially,
James Cook, Peter Yeo, Scott Armbruster, Mo Stanton, and the subsequent diligence of Stefani Wexler, Beth
Spencer Barrett, Dini Eisikowitch, Barbara Gemmill, Clevenger, Gail Schmitt, and Jennifer Slater, as well as
x • Acknowledgments

the anonymous reviewers who offered comments at an process, especially Clare and Iain and Morven, San-
early stage. dra who was so often a rock at work, Peter and Elisa-
Finally a thank-you to many colleagues and friends beth, and neighbor Pam; all of these have been
who have helped to keep me sane through this whole invaluable.
 Pa r t I

E s s e n t i a l s o f F l o we r
De s i g n a n d F u n c t i o n
This page intentionally left blank
 Chapter 1

W h y P o l l i n at i o n I s I n t e r e s t i n g

Outline ary trajectory of the plant. But the plant itself is im-
mobile, so that incoming pollen has to be borne on
1. Which Animals Visit Flowers? some motile carrier, sometimes wind or water but
2. Why Do Animals Visit Flowers? much more commonly on a visiting animal. To quote
3. How Do Flowers Encourage Animal Visitors? one source (Rothrock 1867), “among plants, the nup-
4. What Makes a Visitor into a Good Pollinator? tials cannot be celebrated without the intervention of
5. Costs, Benefits, and Conflicts in Animal a third party to act as a marriage priest”! A pictorial
Pollination overview of the stages is shown in figure 1.1, covering
6. Why Is Pollination Worth Studying? the processes of pollination that are the focus of this
book.
A flower also serves to protect the pollen as it ger-
minates and as the male nucleus locates the egg and
then to protect the ovules as they are fertilized and be-
The flowering plants (angiosperms) account for about gin their development into mature seeds. However,
one in six of all described species on earth and provide these later events (germination of the pollen and fer-
the most obvious visual feature of life on this planet. tilization of the ovule) are technically not part of pol-
In the terrestrial environment, their interactions with lination, and they are covered here only as needed to
other living organisms are dominant factors in com- understand the characteristics and effects of pollen
munity structure and function; they underpin all nutri- transfer.
ent and energy cycles by providing food for a vast Since flowers bring about and control plant repro-
range of animal herbivores, and the majority of them duction, they are central to much of what goes on in
use animal pollinators to achieve reproduction. Most the terrestrial world, and pollination is a key mutual-
of the routine “work” of a plant is carried out by roots ism between two kingdoms of organisms, perhaps the
and leaves, but it is the flowers that take on the crucial most basic type of exchange of sex for food; the plant
role of reproduction. gains reproductive success, and the animal—usually—
A flower is usually hermaphrodite, with both male gains a food reward as it visits the plant. But the visitor
and female roles. Hence it is essentially a structure does not “want” to be a good pollinator and has to be
that produces and dispenses the male gametophytes manipulated by the plant to move on and to carry pol-
(pollen), organizes the receipt of incoming pollen len to another plant. In practice, only about 1% of all
from another plant onto its own receptive surfaces on pollen successfully reaches a stigma (Harder 2000).
the stigma, and then appropriately guides the pollen’s Nevertheless, pollination by animals (biotic polli-
genetic material to the female ovules. The flower also nation) is both more common (Renner 1998) and usu-
protects the delicate male and female tissues (stamens ally more effective than alternative modes of abiotic
and pistils) and has a role in controlling the balance pollen movements using wind or water, and animal
between inbreeding and outbreeding, hence influenc- pollination is usually also associated with more rapid
ing the genetic structure and ultimately the evolution- speciation of plants (Dodd et al. 1999; K. Kay et al.
4 • Chapter 1

pollen grain

pollen

anther

pollen
stigma grain
stigma

pollen
conducting grains
tissue
style
anther Figure 1.1 The central processes of pollination in a
pollen typical angiosperm flower, with the route taken by
tube pollen from anther to stigma (followed by pollen tube
filament
growth into the style) in an animal-pollinated species.
ovary (Modified from Barth 1985.)

2006). Discussion of animal pollination therefore rably reveals the actions, both historical and contem-
dominates this book, and around 90% of all flowering porary, of the selective agents (mainly, but not solely,
plants are animal pollinated (Linder 1998; Renner the pollinators) that we know have shaped them. These
1998). Furthermore, plants are, of course, the founda- factors make floral biology an ideal resource for un-
tion of all food chains on the planet, and their efficient derstanding biological adaptation at all levels, in con-
pollination by animals to generate further generations trast with many other systems, where there are multi-
is vital to ensure food supplies for animals. Natural ple and often uncertain selective agents.
ecosystems therefore depend on pollinator diversity to In this first chapter, some of these central themes
maintain overall biodiversity. That dependence natu- are introduced to set the scene for more specialist
rally extends to humans and their agricultural systems chapters; it should be apparent from the outset that
too; about one-third of all the food we eat relies di- while each chapter might stand alone for some pur-
rectly on animal pollination of our food crops (and the poses, it cannot be taken in isolation from this whole
carnivorous proportion of our diet has some further in- picture.
direct dependence on animal pollination of forage
crops). Pollination and factors that contribute to the
maintenance of pollination services are vital compo- 1. Which Animals Visit Flowers?
nents to take into account in terms of the future health
of the planet and the food security and sustainability of At least 130,000 species of animal, and probably up to
the human populations it supports. 300,000, are regular flower visitors and potential pol-
Beyond its practical significance, the flower-animal linators (Buchmann and Nabhan 1996; Kearns et al.
mutualism has been a focus of attention for naturalists 1998). There are at least 25,000 species of bees in this
and ecologists for at least two hundred years and pro- total, all of them obligate flower visitors and often the
vides almost ideal arenas for understanding some of most important pollinators in a given habitat.
the fundamental aspects of biology, from evolution There are currently about 260,000 species of angio-
and ecology to behavior and reproduction. It is per- sperms (P. Soltis and Soltis 2004; former higher esti-
haps more amenable than any other area to providing mates were confounded by many duplicated namings),
insights into the balance and interaction of ecological and it has been traditional to link particular kinds of
and evolutionary effects (Mitchell et al. 2009). Flow- flowers to particular groups of pollinators. About 500
ers are complex structures, and their complexity admi- genera contain species that are bird pollinated, about
 Why Pollination Is Interesting • 5

250 genera contain bat-pollinated species, and about 3. How Do Flowers Encourage
875 genera predominantly use abiotic pollination; the Animal Visitors?
remainder contain mostly insect-pollinated species,
with a very small number of oddities using other kinds Many plant attributes contribute to attraction of visi-
of animals (Renner and Ricklefs 1995). tors: J. Thomson (1983) usefully groups these as plant
The patterns of animal flower visitors differ region- presentation. Some of these attributes are readily ap-
ally. In central Europe, flower visitors over a hundred parent to visitors, and these may be features of indi-
years ago were recorded as 47% hymenopterans vidual flowers (e.g., color, shape, scent, reward avail-
(mainly bees), 26% flies, 15% beetles, and 10% but- ability, or time of flowering) or features of whole plants
terflies and moths; only 2% were insects outside these or groups of plants (e.g., flower density, flower num-
four orders (Knuth 1898). But in tropical Central ber, flower height, or spatial pattern). The more readily
America, the frequencies would be very different, with apparent plant presentation traits can be divided into
bird and bat pollination entering the picture and fewer attractants (advertising signals), dealt with mainly in
fly visitors, while in high-latitude habitats the verte- chapters 5 and 6, which discuss visual and olfactory
brate pollinators are absent and flies tend to be more signals, and rewards (usually foodstuffs), dealt with in
dominant. Some of these patterns will be discussed in chapters 7–9. Aspects of the timing and spacing of
chapter 27. flowers, and how these might be affected by competi-
tion between different flowering plants, are given more
in-depth treatments in chapters 21 and 22.
2. Why Do Animals Visit Flowers? Other floral attributes are more cryptic to the visitor
and may only determine the reproductive success of
The majority of flower visitors go there simply for the plant in the longer term; these might include pollen
food, feeding on sugary nectar and sometimes also on amounts, ovule numbers, the genetic structure of the
the pollen itself. Chapters 7 and 8 will therefore deal in plant population, the presence and type of incompat-
detail with these commodities, and chapter 9 will cov- ibility system, etc.
er a few more unusual foodstuffs and rewards that can It is generally in the plant’s interest to support and
be gathered from flowers; chapter 10 will take an eco- even improve its visitors’ efficiency, encouraging them
nomic view of all these food-related interactions, in to go to more flowers of the same species (so ensuring
terms of costs and benefits to each participant. Major that only conspecific pollen is taken and received) and
themes in other chapters include the ways that flower to go to flowers with fresh pollen available and/or with
feeders can improve their efficiency: learning recogni- receptive stigmas for pollen to be deposited upon.
tion cues to select between flowers intra- and interspe- Many flowers therefore add signals of status to their
cifically, learning handling procedures, learning to repertoire, via color change, odor change, or even
avoid emptied flowers, and avoiding some of the haz- shape change. Visitors are thereby directed away from
ards of competing with other visitors. flowers that are too young or too old or already polli-
Flowers are also sometimes visited just as a conve- nated. Instead they will tend to concentrate their ef-
nient habitat, often simply because they offer an equa- forts on those (fewer) flowers per plant that are most in
ble sheltered microclimate for a small animal to rest need of visitation, thus also being encouraged to move
in, a place that is somewhat protected against bad around between separate plants more often and to en-
weather, predators, or parasitoids. Or flowers may of- sure outcrossing rather than selfing. Reasons for fa-
fer a reliable meeting site for mates or hosts or prey, or voring breeding by outcrossing (i.e., with other plants)
for females an oviposition site providing shelter for are covered more fully in chapter 3.
eggs and larvae. More rarely they are used as a warm-
ing-up site by insects in cold climates, usually because
the flowers trap some incoming solar radiation, which 4. What Makes a Visitor into
enhances their own ovule development, but occasion- a Good Pollinator?
ally because a few flowers can achieve some metabolic
thermogenesis that warms their own tissues (chapter 9 In many ways this is the crucial theme running through
will provide more details on this topic). this book. It relates to what is probably the major
6 • Chapter 1

current debate in pollination ecology, that is, to what Physical Factors

extent pollination it is a generalist process and to what
extent it is a specialist one. Pollination has in the past Any animal that is to be an effective pollinator must
nearly always been categorized in terms of syndromes, have the ability to passively pick up pollen as its body
with particular groups of flowers recognized as hav- moves past the anthers of a flower that it visits and
ing particular sets of characteristics (of color and carry that pollen to another flower. Normally this will
scent, shape, timing, reward, etc.) that suit them to be be aided by the animal being a good physical fit in
visited by particular kinds of animals; and it is im- terms of size and shape, so that in alighting on the
plicit in this approach that these suites have often been flower surface, or when inserting its tongue or beak of
arrived at and selected for by convergent evolution in appropriate length, some specific part of its body
plant families that are unrelated. Thus most authors touches the anther. Additionally pollen pickup and car-
have used terms such as ornithophily to describe the riage will be aided if the animal has appropriate sur-
bird pollination syndrome, or psychophily for the face structures; pollen adheres well to feathers, fur,
butterfly pollination syndrome. Flower characteristics and hairy or scaly surfaces in insects but does not get
would be listed that fit each syndrome, and an unfa- transported well on shiny or waxy surfaces (and may
miliar flower’s probable pollinators could therefore be even be damaged by certain surface secretions). Hence
predicted. Flowers in each category were seen as hav- a small shiny beetle taking some nectar by crawling
ing a degree of specialization that suited them to their into the lower surface of a large tubular corolla where
particular visitors, with some syndromes being more the anthers are in the corolla roof may well be a regu-
specialized than others. Nearly all earlier works on lar visitor to that flower but is unlikely to be an effec-
pollination were organized around this theme of syn- tive mover of its pollen; in effect, it is acting as a
dromes, and it served as a useful structure for under- “cheat” as far as the flower is concerned and may be
standing animal-flower interactions for nearly two termed an illegitimate visitor.
centuries. Without knowing this background it would
be nearly impossible to follow the current debates that
are a major focus for pollination ecologists, and it Behavioral Factors
would also be very difficult to structure the informa-
tion on flower attractants and flower rewards in chap- Different animals land on and forage at flowers in very
ters 5–9. This book thus retains a syndrome-based ap- different fashions. There are many aspects of behavior
proach throughout its early chapters and explicitly that will affect whether a given animal is going to be a
considers the evidence in support of a syndrome ap- good pollinator. Pollinators will seldom have a com-
proach in chapter 11; then it unashamedly covers each plete perception of all the aspects of plant presentation
of the syndromes in turn in chapters 12–19, providing mentioned above, but they will respond to at least
all the core materials on which later criticisms might some of them in ways that are useful to the plant:
be based.
The criticisms and debates focus around the reality 1. Their choices of places and times to visit, and ex-
of syndromes and how far they have been overplayed actly which flowers to visit, will be critical. Visits
in the previous literature, perhaps blinkering or bias- occurring before dehiscence (the splitting of the
ing our perceptions. Many authors now regard flower anthers to reveal the pollen) or after pollen deple-
pollination as a much more generalized phenomenon, tion are normally of no value to the flower in ful-
where most flowers get many different kinds of visi- filling its male role, and visits before or after the
tors and have not been and are not being heavily se- stigma is receptive to incoming pollen are of no
lected to specialize for the needs of one particular value to the flower in its female role.
“best” visitor. This approach is specifically addressed 2. Their handling of the flowers affect their pollen
in chapter 20. It will be a major argument there that the pickup and deposition characteristics; ideally they
issue has been clouded by an as yet insufficient dis- should receive pollen at a specific site on their
tinction between flower visitors and pollinators. So bodies, and one that is also a good site for subse-
what does make a visitor into a good pollinator? quent deposition of that pollen onto a stigma.
 Why Pollination Is Interesting • 7

3. Their handling time per flower affects how many late their body temperature and water balance more
flowers are visited in a given time. precisely; they generate heat internally through their
4. Their speed and directionality of movement be- own metabolism (endothermy) and regulate their own
tween plants affect pollen dispersal. body fluids with efficient skin exchanges, respiratory
5. They should not be too efficient at grooming off controls, and excretory organs. They can in principle
the pollen, or indeed at eating it. forage at almost any time and in any habitat, though
6. Their flower constancy, that is, the likelihood that they may still conserve their own energy by picking
they will move to another flower of the same spe- more equable sites.
cies, is perhaps most critical. If they innately or by The distinction does not lie exactly between the
learning prefer a particular flower phenotype, vulnerable invertebrates and the highly regulated birds
their high constancy will usually ensure that they and mammals, however. It is now clear that a rather
move neatly and sequentially among conspecific small proportion of insects can also show endothermy,
flowers, not wasting pollen by depositing it in the at least some of the time when they need to warm up in
wrong species. Constancy to a flower (considered the absence of solar inputs (chapter 10); this applies
in detail in chapter 11) gives economies to the vis- especially to most bees, a few hoverflies, some large
itor also; it may minimize travel distances, han- moths, and some beetles, occurring more sporadically
dling times, and learning effort and maximize pol- in other groups. It is perhaps no coincidence that endo-
len packing. thermic abilities in insects are most common in the
flower-visiting groups, which have access to ready
Behavioral factors such as these are often the key to
fuel supplies in the form of nectar but which may also
being a good pollinator and of course are affected by
need to compete for that nectar in the cool of early
the animals’ abilities to learn as they become more ex-
mornings or at dusk.
perienced as foragers. The ability to form a search im-
age or to respond consistently to other cues, associat-
Given the list of factors that can turn a visitor into a
ing particular signals with the presence of food, hones
good pollinator, two obvious points should emerge:
their foraging ability and can cement their relation-
ships with particular flowers. Hence later chapters of
1. A great many of the animals that go to flowers for
this book, in considering particular groups of animals
a short drink of nectar may be rather poor at pollinat-
that visit flowers, include careful consideration of their
ing that flower. Those with a poor physical fit, those
sensory and learning capacities.
that cheat, and those with little or no flower constancy
are likely to be especially ineffective.
Physiological Factors
2. Of all the visitors, bees are likely to be especially
Animals have differing physiological strategies and good as pollinators. They rely solely on flowers for
constraints, and these too can affect their energetic food, both as adults and as larvae, and so must visit
needs and thence their flower-visiting patterns, as will more flowers than any other animals. Their sizes, hairy
be discussed in chapter 10. Most animals (including surfaces, and variably long tongues, their excellent
nearly all invertebrates, and therefore many of the in- learning abilities, communication systems and floral
sect flower visitors) lack elaborate internal physiologi- constancy, and their endothermic capacities all equip
cal regulatory systems, and their thermal balance and them to visit flowers efficiently (from their own per-
water balance are strongly influenced by environmen- spective) and effectively (from the plant’s point of
tal conditions. They cannot function if they are too hot view). Although they are sometimes described as pol-
or too cold or are short of water, and must forage in len wasters (because they, or rather their offspring
times and places that provide suitable microclimates, back at the nest, eat so much of the pollen that they
using the sun’s radiation to warm up by basking, or pick up), they are by far the most important pollinators
shady places to cool down again, and seeking (usually) in most ecosystems, and they do achieve high pollen
sites that are relatively humid. However, birds and bats export from visited flowers (Harder and Wilson 1997);
are physiologically more sophisticated and can regu- plants have adapted over evolutionary time to make
8 • Chapter 1

best use of them by providing more than enough pol- offset the additional costs of animal exploiters: those
len to cater for their needs and ensure that sufficient visitors who take rewards without pollinating (thereby
pollen still commonly reaches other flowers. cheating, chapter 24) and the flower eaters (florivores)
or foliage herbivores also attracted by the pollination
cues (chapters 25 and 26). For the animals, there may
5. Costs, Benefits, and Conflicts in be costs linked to carrying the pollen they have inad-
Animal Pollination vertently picked up (sometimes it is very unwieldy and
can interfere with their wings or legs or sense organs),
Plants with hermaphrodite flowers benefit greatly be- which may favor animals trying to cheat, and there
cause a single animal visit can allow both pickup of may be costs also from the potential risks of predation
pollen and its deposition on a stigma, fulfilling both or parasitism at flowers, since enemies can use them as
the male and female functions of that flower at the a place to find prey or hosts reliably (chapter 24).
same time. Animals benefit greatly by finding easily There are also costs arising from the tendencies of the
acquired foods, both sugary (nectar) and often also plants to cheat (chapter 23) by offering no real reward
proteinaceous (pollen). Pollination by animals may and sometimes by trapping the animal.
therefore be a mutualism, of benefit to both partici-
pants, but it is not altruistic; for the animals, pollina-
tion of the flowers they forage at is almost always just 6. Why Is Pollination Worth Studying?
an irrelevant by-product. In fact the plant and animal
have a conflict of interest, often with adaptation and Pollination ecology can provide almost unparalleled
counteradaptation going on from both sides through insights into evolution, ecology, animal learning, and
evolutionary time to try and get a bigger share of the foraging behavior (fig. 1.2). It is perhaps the best of all
benefits. So the situations that we see now are the end areas to see and understand some basic biological pro-
products of the long and sometimes quite duplicitous cesses and patterns; studies that deal exclusively with
associations of flowers with animals. pollination biology have often had major impacts on
The plant ideally wants a visitor that is cheap to general ecological and evolutionary theory.
feed, alighting only briefly, moving on rapidly to an- Pollination interactions often show us evolution by
other plant, and being faithful to its chosen plant spe- natural selection in action almost before our eyes and
cies; so ideally, the forager should be chronically un- provide some very clear-cut examples of adaptive ra-
derfed and continuously on the move. But (again diation and, perhaps, of plant speciation. They are
ideally) the animal would prefer to be as well fed and particularly useful for studying coadaptations (co-
lazy as possible, getting as much food as it can from evolution), because such interaction often involve rel-
one flower with minimum energy expenditure, being atively few organisms interacting with relatively high
relatively sedentary, and then moving on to any other interdependence and incorporating the most funda-
nearby flower with copious nectar, whatever its spe- mental of phenomena (reproduction for the plant, food
cies (although we already noted that some degree of supply for the animal). There are selection pressures
fidelity may improve its foraging efficiency). on each side of the partnership, offering hopes that ef-
Hence, although there are obvious benefits to both fects at the basic level of male and female gene flow
partners, there are potentially clear costs as well. The can be quantified, sometimes (in crop pollination espe-
plant has to invest in attractants (its carbon and nitro- cially) on a time scale that can be detected within one
gen resources are used to make flamboyant petals, pig- scientist’s period of study.
ments, and chemical scents), as well as mere rewards. In terms of ecology, the study of pollination sheds
If the plant reduces its rewards too far, the animal may light on how different organisms interact and affect
not get enough food and will give up on that species. each other, especially the competitive effects of plants
The plant generally also has to compete with other upon each other, and on the various levels of interac-
plant species for pollination, to obtain a share of the tions of plants with pollinators, including resource al-
“good” pollinators, so it cannot afford to skimp on its location, competition, exploitation, and simply cheat-
offerings too much if it is growing within a reasonably ing. In the last two decades there has been an increasing
diverse plant community. Many plants also have to stress on community-level interactions in pollination
 Why Pollination Is Interesting • 9

Environmental factors

Energy balance/ Animal

economics Physiology

Ecology
Thermal Water Sensory
balance needs systems
FLOWER

POLLINATOR POLLINATION

Plant
Biochemistry
Rewards
Nectar Behavior
Pollen Evolution
Selection
Foraging
Learning Genetics
Searching
Advertisements Choosing Memory ST/LT
Colors
Handling Constancy
Odors
Shape/size Optimising

Figure 1.2 Key interactions of major biological topics and themes promoting interest in the study of pollination.

biology, now seen as an especially useful (because ment offering different proportions of alternative prey
highly quantifiable) arena for more general work on as potential food items of differing value (also taking
community structures (J. Thomson 1983); so this book into account factors such as conspicuousness and dif-
inevitably considers the community ecology of polli- ferent variances). The theory predicts that a range of
nation, especially in later chapters. outcomes from complete specialization on one kind of
Pollination biology also gives exceptional insight prey item to complete generalization on all possible
into the ecology of reproductive strategies and the items is to be expected, even from the same animal, as
complexities of sex and reproduction. Flowers usually the prey parameters are varied. Substituting “flower”
are hermaphrodites, but they have many ways of orga- for “prey item” (and with the immense advantage of
nizing their sex life sequentially or spatially to maxi- very easily quantified caloric rewards from nectar), it
mize their reproductive output and fitness. This book is not unexpected that pollinators similarly turn out to
contains rather little coverage of plant reproductive show almost the full range of possible foraging behav-
strategies beyond the basics, because the field has now iors. Furthermore, they have proved ideal subjects with
become dominated by theory and modeling, and the which to develop foraging models that can take into
topic has also been extensively and recently reviewed account different constraints on the foraging animals,
in other works (e.g., Harder and Barrett 2006). whether from different physiological limits or from
In the realm of animal behavior some key influ- different cognitive skills. Learning ability is especially
ences can be especially easily measured and manipu- needed where resources are of intermediate predict-
lated with flower visitors, and it is no accident that ability (Stephens 1993): that is, too unpredictable over
much of the key work on visual discrimination, learn- one or a few generations for fixed behavior patterns to
ing behaviors, and above all optimal foraging has be favored, but not so greatly unpredictable that an in-
used pollinators, especially bees. Optimal diet theory dividual cannot track the changes. This exactly applies
can model how animals should behave in an environ- to floral resources, so that we should expect flower
10 • Chapter 1

visitors from any taxon to be good learners. Fortunate- the models are sometimes hampered by reliance on in-
ly this is also readily tested with real or model flowers adequate records, and understanding, of flower-visitor
where just one trait at a time can be varied or associa- behaviors, and one of the most important issues for the
tions of traits compared; again, social bees are ideal immediate future is ensuring that the new generation of
animals to work with, reliably emerging from their pollination ecologists understand the core subject ma-
nests and traveling straight to the flowers provided, terial of floral biology and can measure and categorize
then displaying clear choices between alternative pollination as distinct from mere visitation to feed into
flowers. their models. We are in need of many and better quan-
titative studies of the effectiveness of visitors (for ex-
For all these reasons, and with the added concern over ample, the average number of conspecific outcrossing
human-induced effects on pollinator services in rela- pollen grains deposited on a stigma at an appropriate
tion to biodiversity and to crops, interest in pollination time by a given visitor in a single visit; chapter 11).
ecology has burgeoned in the last ten to fifteen years, Then we can properly understand plant and pollinator
and the subject is attracting strong interest beyond the communities and pollination networks, and the effects
traditional academic centers of the developed world, of potential extinctions of flower visitors/pollinators on
giving us valuable insights into more varied habitats in the communities of which they are a part. This book
Asia, Africa, and South America and into a greater di- therefore hopes to provide in a single source a useful
versity of interactions. Increasingly these systems are reference for all the aspects of floral biology and polli-
being modeled, and our preconceptions (of these and of nation interactions that need to be considered to give a
other kinds of mutualisms) are being challenged. But real appreciation of these fascinating mutualisms.
Another random document with
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 Paksu Wiers saapui hengästyneenä. Hän rikkoi juhlallisuuden
puhumalla ääneen nahkuri Svendsen'ille, joka seurasi häntä
ylöspäin kauheasti hämillään. Muutoinkin juhlallisuus tuli häirittyä
tuon tuostakin: niin esim. rouva Beer'in tullessa liinatukkaisten
kaksoistensa kera, jotka olivat ensimmäisellä valmistavalla luokalla,
huusi toinen ääneen ja selvästi, että "tuon laatikon päälle minä
tahtoisin mennä istumaan", — osoittaen puhujalavaa.

Sisään tulivat kaikki, suuret ja pienet, sali täyttyi, siinäkös

kuiskailtiin ja sohistiin…

Nyt rehtori Holst nousi puhujalavalle. Kello oli täsmälleen

puoliyksitoista, niinkuin kutsuntakorteissa oli sanottu.

Salissa vallitsi kuolon hiljaisuus. Vahtimestari Ibenfeldt puuhaili,

käyden varpaillaan ja puhuen kuiskaamalla, hakien paikkaa
muutamille myöhästyneille.

Rehtori seisoi vaiti hetken aikaa, tapansa mukaan hiukan heiluen

ja suurilla silmillään tarkastaen yleisöä. Kun myöhästelijät ja
vahtimestari Ibenfeldt olivat rauhoittuneet ja täydellinen hiljaisuus
vallitsi, yskäsi hän ja alkoi.

Rehtori Holst ei pitänyt koskaan pitkiä puheita. Lyhyesti, levollisesti

ja järkähtämättömällä totisuudella hän puhui koululle tavallisuuden
mukaan ja siirtyi sitten ylioppilaskokelaisiin, joille hän puhui
"elämään astumisesta" ja antoi varoituksia. Ja asianomaiset
seisoivat päät kumarassa nyppien silkkitupsujaan.

Sitten siirryttiin Luokka luokalta alaspäin.

 Rehtori mainitsi aina parilla sanalla luokan edistyksestä ja
ahkeruudesta yleensä, ja sitten luettiin todistukset; yksitellen tulivat
pojat numerojärjestyksen mukaan puhujalavan eteen ja seisoivat
siinä, kunnes arvosana edistyksessä, ahkeruudessa ja käytöksessä
oli luettu; näin julistettiin tuomio enemmän tai vähemmän syntiselle.

Kuudes keskiluokka, joka oli suorittanut keskikoulun kurssin sai

osakseen erityisen, tavanmukaisen huomautuksen.

Mikko Tiukkatuulen vatsaa kouristi.

— Viides keskiluokka! luki rehtori.

Hetken hiljaisuus. Mikko Tiukkatuuli painui koukkuun, vatsaa niin

kivisti, — vielä oli hetki hengityksen aikaa, ensin yleinen lausunto,
sitten Simo ja Antti ja…

Hän putkahti: Rehtori mainitsi hänen nimensä, lausumatta

sanaakaan luokasta yleensä…

Hän ei heti voinut tointua. Mieleen välähti: ehkä rehtori aikoo —

koko kansan läsnä ollessa — pitää hänelle rangaistuspuheen
kaikesta tämän vuoden huonoudesta…

— No, Mikko! huusi rehtori Holst uudestaan katsellen alas

penkkeihin.
Ruununvouti nousi ylös nojatuolistaan ja tuijotti ankarana Mikko
Tiukkatuulen paikkaa kohti.

Notkuvin polvin, pelosta kalpeana Mikko Tiukkatuuli melkein

horjuen astui keskikäytävää pitkin. Rehtori odotti, todistus kädessä.
Hän katsahti Mikko Tiukkatuuleen, joka oli pysähtynyt hänen
eteensä, Sitten rehtori luki:
 — Edistys hyvin kiitettävä 1,45. Muutetaan 6:een keskiluokkaan
ensimmäisenä oppilaana.

Rehtori kurkotti todistusta alaspäin. Mikko Tiukkatuuli ei ottanut

sitä.

— No, so! sanoi rehtori, — saat ottaa todistuksesi! Paperi rasahti

Mikko Tiukkatuulen kourassa. Hän unohti kumartaa muiden tapaan,
seisoi vaan ja tuijotti rehtoriin.

Mutta rehtori jatkoi levollisesti:

— — Simo Selmer!

Pois kääntyessään kohtasi hän Simo Selmerin happaman

naaman, — ja samassa hän vilaukselta näki herra Selmerin
ensimmäisellä penkillä.

Silloin vasta Mikko Tiukkatuuli tajusi, että hänestä oli tullut numero
yksi —!

Koko poikaa loisti riemusta saapuessaan äidin luo, jolla oli

ilokyyneleet silmissä.
 *** END OF THE PROJECT GUTENBERG EBOOK MIKKO
TIUKKATUULI ***

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