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Climate Change and Small Pelagic Fish

This book details the effects of climate variability on small Dave Checkley is a biological oceanographer with expertise
pelagic fish and their ecosystems and fisheries. These fish (for in the ecology of marine zooplankton and fish and fisheries
example, anchovy, sardine, sprat, and herring) comprise about oceanography. He is a Professor at the Scripps Institution of
one-quarter of the global fish catch and are particularly abundant Oceanography, University of California, San Diego. He has been
in coastal upwelling regions off the west coasts of the Americas a NATO Postdoctoral Fellow at DAFS in Aberdeen, Scotland, a
and Africa, off Japan, and in the NE Atlantic. Their stocks fluc- member of the faculties of the University of Alaska, the University
tuate greatly over the time scale of decades, with large ecological of Texas, and North Carolina State University, and a Tech Awards
and economic effects. This book describes the nature and cause Laureate of the Tech Museum, San José, California. He led the
of these fluctuations, and their effects. It outlines results from development of CUFES, SOLOPC, and REFLICS. He is the
paleo-oceanographic studies, showing that fluctuations similar co-chair of Small Pelagic Fish and Climate Change (SPACC) and
to those at present have also occurred over the past two millen- Editor-in-Chief of Fisheries Oceanography.
nia. The potential effects of future climate change, both natural Jürgen Alheit is a fisheries biologist. His main interest is the
and anthropogenic, on stocks and fisheries, are considered. It con- impact of climate variability on marine ecosystems. While work-
cludes by recommending the continued international study and ing at the Intergovernmental Oceanographic Commission at
assessment of small pelagic fish in order to best inform manage- UNESCO in Paris, he was responsible for the Ocean Sciences in
ment and policy under a changing climate. Relation to Living Resources Programme of IOC and FAO, which
No other book addresses climate change effects on fish in such focused on small pelagics. He is the co-founder and former co-
an extensive manner. The book is also distinctive in being the chair of SPACC, chair of the GLOBEC Focus 1 Working group
product of a collaboration of academic and fisheries scientists on Retrospective Analysis, and chair of the German GLOBEC
from each of the regions with major stocks of small pelagic fish. It Project. He serves on the Scientific Steering Committee of the
is written for research scientists, academics, and policy makers in GLOBEC International Programme.
fisheries, oceanography, and climate change.
Yoshioki Oozeki is the Chief Scientist of the Fish Ecology
Section, National Research Institute of Fisheries Science,
Fisheries Research Agency, Japan, and Professor of Marine
Life Science at the Tokyo University of Marine Science and
Technology. He is a fisheries biologist with expertise in the larval
biology and ecology of small pelagic fish, and has led the egg and
larval survey project in waters around Japan for 12 years. He has
also investigated larva physiology, database management, stock
assessment, sampling gear technology, and variation of fish in
relation to climate. He received the Uda Award from the Japanese
Society of Fisheries Oceanography in 2007.
Claude Roy is a physical oceanographer with expertise in fish-
eries oceanography and upwelling systems dynamics. As a sci-
entist of the French Research Institute for Development (IRD),
he spent extended periods of time in countries bordering upwell-
ing systems during which he contributed to the implementation
of several regional “climate and fisheries” research and training
projects. He has been involved in SPACC since the late 1990s and
served as its co-chair from 2003 to 2008.
Climate Change
and Small Pelagic
Fish
edi t ed by

DAv I D M. CH E Ck L EY, Jr.

Scripps Institution of Oceanography, University of California, San
Diego, USA

J ü RGE N A LH EI T
Baltic Sea Research Institute, Warnemünde, Germany

YOSH IOk I O Oz Ek I
National Research Institute of Fisheries Science, Kanagawa, Japan

C LAU DE ROY
L’Institut de Recherche pour le Développement (IRD), Plouzané, France
ca m br i d ge u n i v e r s i t y p r e s s
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo, Delhi
Cambridge University Press
The Edinburgh Building, Cambridge CB2 8RU, Uk

Published in the United States of America by Cambridge University Press, New York

www.cambridge.org
Information on this title: www.cambridge.org/9780521884822

© Cambridge University Press, 2009

This publication is in copyright. Subject to statutory exception

and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.

First published 2009

Printed in the United kingdom at the University Press, Cambridge

A catalog record for this publication is available from the British Library

Library of Congress Cataloging in Publication data

Checkley, David.
Climate change and small pelagic fish / David M. Checkley, Jürgen Alheit, Yoshioki Oozeki.
p. cm.
Includes bibliographical references and index.
ISBN 978-0-521-88482-2 (hardback)
1. Pelagic fishes–Effect of temperature on. 2. Pelagic fishes–Behavior–Climatic factors. 3. Fisheries–Climatic factors.
4. Pelagic fishes–Population viability analysis. 5. Climatic changes. I. Alheit, J. (Jürgen) II. Oozeki, Yoshioki. III. Title.
QL638.C64C44 2009
597.1722–dc22 2009007318

ISBN 978-0-521-88482-2 hardback

Cambridge University Press has no responsibility for the persistence or

accuracy of URLs for external or third-party internet websites referred to
in this publication, and does not guarantee that any content on such
websites is, or will remain, accurate or appropriate.
To Reuben Lasker
 Contents

Acknowledgments page viii 9 Current trends in the assessment and

List of abbreviations ix management of stocks 191
List of contributors xi Manuel Barange, Miguel Bernal, Maria Cristina Cergole,
Foreword by Jorge Csirke, Michael Glantz, Luis A. Cubillos, Georgi M. Daskalov, Carryn L. de Moor
and James Hurrell xv (formerly Cunningham), José A.A. De Oliveira, Mark
Preface xix Dickey-Collas, Dave J. Gaughan, Kevin Hill, Larry D.
Jacobson, Fritz W. Köster, Jacques Massé, Miguel Ñiquen,
Hiroshi Nishida, Yoshioki Oozeki, Isabel Palomera, Suzana
1 History of international co-operation in
A. Saccardo, Alberto Santojanni, Rodolfo Serra, Stylianos
research 1 Somarakis, Yorgos Stratoudakis, Andres Uriarte, Carl D.
Jürgen Alheit and Andrew Bakun van der Lingen, and Akihiko Yatsu

2 A short scientific history of the fisheries 6 10 Global production and economics 256
Alec D. MacCall Samuel F. Herrick, Jr., Jerrold G. Norton, Rognvaldur
Hannesson, U. Rashid Sumaila, Mahfuzuddin Ahmed,
3 Habitats 12 and Julio Pena-Torres
David M. Checkley, Jr., Patricia Ayon, Tim R.
Baumgartner, Miguel Bernal, Janet C. Coetzee, 11 Human dimensions of the fisheries under
Robert Emmett, Renato Guevara-Carrasco, Larry
global change 275
Hutchings, Leire Ibaibarriaga, Hideaki Nakata, Yoshioki
Rosemary E. Ommer, Astrid C. Jarre, R. Ian Perry,
Oozeki, Benjamin Planque, Jake Schweigert, Yorgos
Manuel Barange, Kevern Cochrane, and Coleen Moloney
Stratoudakis, and Carl D. van der Lingen

12 Mechanisms of low-frequency fluctuations in

4 Variability from scales in marine sediments
sardine and anchovy populations 285
and other historical records 45
Alec D. MacCall
David B. Field, Tim R. Baumgartner, Vicente Ferreira,
Dimitri Gutierrez, Hector Lozano-Montes, Renato
Salvatteci, and Andy Soutar 13 Research challenges in the twenty-first
century 300
Andrew Bakun
5 Decadal-scale variability in populations 64
Jürgen Alheit, Claude Roy, and Souad Kifani
14 Conjectures on future climate effects on
6 Biophysical models 88 marine ecosystems dominated by small
Christophe Lett, Kenneth A. Rose, and Bernard pelagic fish 312
A. Megrey Pierre Fréon, Francisco Werner, and Francisco P.
Chavez
7 Trophic dynamics 112
Carl D. van der Lingen, Arnaud Bertrand, Antonio 15 Synthesis and perspective 344
Bode, Richard Brodeur, Luis Cubillos, Pepe Espinoza, David M. Checkley, Jr., Andrew Bakun,
Kevin Friedland, Susana Garrido, Xabier Irigoien, Todd Manuel Barange, Leonardo R. Castro, Pierre
Miller, Christian Möllmann, Ruben Rodriguez-Sanchez, Fréon, Renato Guevara-Carrasco, Samuel F. Herrick,
Hiroshige Tanaka, and Axel Temming Jr., Alec D. MacCall, Rosemary Ommer, Yoshioki
Oozeki, Claude Roy, Lynne Shannon, and Carl D. van
der Lingen
8 Impacts of fishing and climate change
explored using trophic models 158
Lynne Shannon, Marta Coll, Sergio Neira, Philippe Cury, Index 352
and Jean-Paul Roux
Acknowledgments

We thank the International Project Office of the Global

Ocean Ecosystems Dynamics Program (GLOBEC) for
its support during the production of this book and, in
particular, Manuel Barange. The Institute of Research
and Development (IRD) of France and the University of
California, San Diego contributed financial support.
SPACC acknowledges the support it received from
GLOBEC and its sponsors, in particular the International
Geosphere-Biosphere Programme (IGBP), the International
Oceanographic Commission of UNESCO (IOC), and the
Scientific Committee on Oceanic Research (SCOR) sup-
ported by NSF grant No. UCE-0608600.

Dave Checkley
Jurgen Alheit
Yoshi Oozeki, and
Claude Roy
 Abbreviations

AAIW Antarctic Intermediate Water EwE EcoPath with EcoSim

ABC Allowable Biological Catch FAO Food and Agriculture Organization
AC Azores Current FiB Fishing-in-Balance
ACMRR Advisory Committee of Experts on Marine FL Fork Length
Resources Research GAM Generalized Additive Model
AEP Annual Egg Production GCM Global Ocean Circulation Models
ALP Aleutian Low Pressure GFCM General Fisheries Council for the
AMCI Assessment Model Combining Information Mediterranean
AMO Atlantic Multidecadal Oscillation GL Gulf of Lions
ASAP Age-Structured Assessment Program GLM General Linear Model
BP Before Present GLOBEC Global Ocean Ecosystem Dynamics
BAC Biological Action Centers GOOS Global Ocean Observing System
BC Benguela Current HAMSOM Hamburg Shelf Ocean Model
BITS Baltic International Trawl Survey HC Humboldt Current
BMSY Biomass of Maximal Sustainable Yield HCE Humboldt Current Ecosystem
CACom California Commercial Fish Landing Records HCR Harvest Control Rule
CalCOFI California Cooperative Oceanic Fisheries HSI Habitat Suitability Index
Investigations IBM Individual-Based Model
CanCE Canary Current Ecosystem IBTS International Bottom Trawl Survey of the
CANSAR Catch-at-Age Analysis for Sardine North Sea
CC California Current ICA Integrated Catch-at-Age
CC Climate Change (Chapter 14) ICLARM International Center for Living Aquatic
CCAMLR Commission for the Conservation of Antarctic Resources Management
Marine Living Resources IFOP Instituto de Fomento Pesquero
CCE California Current Ecosystem IGBP International Geosphere Biosphere Programme
CCO Central California Offshore subpopulation of IGP Intraguild Predation
sardine IMARPE Instituto del Mar del Perú
CCSR Center for Climate System Research IMECOCAL Investigaciones Mexicanas de la Corriente de
CCW Cold Coastal Water California
CEOS Climate and Eastern Ocean Systems IOC Intergovernmental Oceanographic Commission
CHRS Constant Harvest Rate Strategy IPCC Intergovernmental Panel on Climate Change
CPR Continuous Plankton Recorder IRD Institute for Research and Development
CPUE Catch per Unit Effort IREP International Recruitment Project
CS Catalan Sea ISPR Instantaneous Surplus Production Rate
CSA Catch-Survey Analysis ITQ Individual Transferable Quota
CUFES Continuous Underway Fish Egg Sampler IUCN International Union for the Conservation of
Cv Coefficient of variation Nature and Natural Resources
DEPM Daily Egg Production Method kC kuroshio Extension
DFR Daily Fecundity Reduction kCE kuroshio Current Ecosystem
DIN Dissolved Inorganic Nitrogen kESA kuroshio Extension South Area
EAF Ecosystem Approach to Fisheries kO kuroshio–Oyashio
EBUS Eastern Boundary Upwelling Systems kOTz kuroshio–Oyashio Transition zone
EEz Exclusive Economic zone LME Large Marine Ecosystem
ENSO El Niño Southern Oscillation MIN Minimum Number of Individuals
EOF Empirical Orthogonal Function MLD Mixed Layer Depth
ERS European Remote-Sensing Satellite MLE Maximum Likelihood Estimator
ESSW Equatorial Subsurface Water MSC Marine Stewardship Council
EU European Union MSvPA Multispecies virtual Population Analysis
EURO-SARP European Sardine–Anchovy Recruitment MSY Maximum Sustained Yield
Program MTI Mixed Trophic Impact
x List of abbreviations

NA Northeast Atlantic SARDYN Sardine Dynamics and Stock Structure in the

NAC North Atlantic Current Northeast Atlantic
NACW North Atlantic Central Water SARP Sardine–Anchovy Recruitment Program
NAO North Atlantic Oscillation SATW Sub-Antarctic Temperate Water
NEA Northeast Atlantic SAW Sub-Antarctic Water
NEMURO North Pacific Ecosystem Model for Understanding SBB Santa Barbara Basin
Regional Oceanography SCOR Scientific Committee on Oceanic Research
NIES National Institute for Environmental Studies SDR Scale Deposition Rate
NISP Number of Identified Specimens SECC Southern Extension of the Cromwell Current
NMFS National Marine Fisheries Service SEW Surface Equatorial Water
NOAA National Oceanographic and Atmospheric SL Standard Length
Administration SLP Sea Level Pressure
NPz Nutrient–Phytoplankton–zooplankton SPACC Small Pelagic Fish and Climate Change
OMP Operational Management Procedure SPF Small Pelagic Fish
ORSTOM Office de la Recherche Scientifique et Technique SSB Spawning Stock Biomass
Outre Mer SSB/R Spawning Stock Biomass/Recruit
OSLR Ocean Science in Relation to Living Resources SSS Sea Surface Salinity
Programme SST Sea Surface Temperature
P/B Production/Biomass SSW Subtropical Surface Water
P2P Prey-to-Predator STECF Scientific, Technical and Economic Committee for
PC Peru Current Fisheries (EU)
PCC Peru Coastal Current STSW Subtropical Surface Water
PDO Pacific Decadal Oscillation SURBA Survey Based
POM Princeton Ocean Model TAB Total Allowable Bycatch
PROCOPA Peruvian–German Cooperative Program for TAC Total Allowable Catch
Fisheries Investigations TL Trophic Level
REX Recruitment Experiment TNA Tropical North Atlantic Index
ROMS Regional Ocean Model System vMS vessel Monitoring System
RPS Recruit Per Spawner vPA virtual Population Analysis
RQ Respiratory Quotient WA Western Australia (but also Washington state)
RSHR Regime-Specific Harvest Rate WCRP World Climate Research Program
SACW South Atlantic Central Water WSSD World Summit for Sustainable Development
SAfE South Africa Experiment XSA Extended Survival Analysis
 Contributors

Mahfuzuddin Ahmed Kevern Cochrane

The WorldFish Center, Jalan Batu Maung, Batu Maung, 11960 FAO, via delle Terme di Caracalla, 00100 Roma, Italy
Bayan Lepas, Penang, Malaysia
Janet C. Coetzee
Jürgen Alheit Marine and Coastal Management, Private Bag X2, Rogge Bay
Baltic Sea Research Institute, Seestr. 15, 18119 Warnemünde, 8012, South Africa
Germany
Marta Coll
Patricia Ayon Dalhousie University, Department of Biology, 1355 Oxford
Instituto del Mar del Perú, Apartado 22 Callao, Perú Street, Halifax, Nova Scotia, Canada, B3H4J1 and Institute
of Marine Science (CMIMA-CSIC), Passeig Marítim de la
Andrew Bakun
Barceloneta, 37–49, 08002, Barcelona, Spain
Pew Institute for Ocean Science, Rosenstiel School of Marine
and Atmospheric Science, University of Miami, Miami, Florida, Luis A. Cubillos
33149–1098, USA Instituto Español de Oceanografía, Centro Oceanográfico de A
Coruña, Spain
Manuel Barange
Plymouth Marine Laboratory, Prospect Place, Plymouth Carryn L. de Moor (formerly Cunningham)
PL1 3DH, Uk MARAM (Marine Resource Assessment and
Management), Department of Mathematics and Applied
Tim R. Baumgartner
Mathematics, University of Cape Town, Rondebosch 7701,
Centro de Investigación Científica y de Educación Superior de
South Africa
Ensenada, km 107 Carretera Tijuana-Ensenada, Ensenada, Baja
California, C.P. 22860, Mexico Philippe Cury
Centre de Recherche Halieutique Méditerranéenne
Miguel Bernal
et Tropicale, IRD – IFREMER & Université
Instituto Español de Oceanografía, C/ República Saharaui, s/n,
Montpellier II Avenue Jean Monnet, BP 171 34203 Sète,
11510 Puerto Real
Cedex, France
Arnaud Bertrand
Georgi M. Daskalov
Institut de Recherche pour le Développement, CRH, Avenue Jean
CEFAS, Pakefield Road, Lowestoft, Suffolk
Monnet, Sète, France c/o Instituto del Mar del Perú, Lima, Perú
NR33 0HT, Uk
Antonio Bode
José A. A. De Oliveira
Instituto Español de Oceanografía, Centro Oceanográfico de A
CEFAS, Pakefield Road, Lowestoft, Suffolk
Coruña, Spain
NR33 0HT, Uk
Richard Brodeur
Mark Dickey-Collas
Northwest Fisheries Science Center, NOAA, Newport,Oregon, USA
IMARES, PO Box 68, 1970 AB Ijmuiden,
Leonardo R. Castro The Netherlands
Laboratorio de Oceanografía Pesquera y Ecología Larval,
Robert Emmett
Departamento de Oceanografía, Universidad de Concepción, PO
NOAA Fisheries, 2030 South Marine Science Drive, Newport,
Box 160-C, Concepción, Chile
Oregon, 97391, USA
Maria Cristina Cergole
Pepe Espinoza
Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Instituto del Mar del Perú, Lima, Perú
Renováveis (IBAMA), Alameda Tietê 637, CEP 01417–020, São
Paulo, SP, Brasil Vicente Ferreira
Centro de Investigación Científica y de Educación Superior de
Francisco P. Chavez
Ensenada, km 107 Carretera Tijuana-Ensenada, Ensenada, Baja
Monterey Bay Aquarium Research Institute, 7700 Sandholdt
California, C.P. 22860, Mexico
Road, Moss Landing, California, 95039 USA
David B. Field
David M. Checkley, Jr.
Monterey Bay Aquarium Research Institute, Moss
Scripps Institution of Oceanography, University of California,
Landing, CA & University of California, Santa Cruz, Santa
San Diego, La Jolla, California 92093–0218, USA
Cruz, California, USA
xii List of contributors

Pierre Fréon Hector Lozano-Montes

ECO-UP Unit, Centre de Recherche Halieutique, IRD, BP 171, CSIRO Marine and Atmospheric Research, Underwood Avenue,
34203 Sète, Cedex, France Floreat, WA, Australia, 6014
Kevin Friedland Alec D. MacCall
National Marine Fisheries Service, Narragansett , Rhode Island, National Marine Fisheries Service, Southwest Fisheries Science
USA Center, 110 Shaffer Rd., Santa Cruz, California, 95060, USA
Susana Garrido Jacques Massé
Instituto Nacional de Investigação Agráia e das Pescas, Lisboa, IFREMER, Rue de l’Ile d’Yeu, B.P. 21105, 44311 Nantes,
Portugal France
Daniel J. Gaughan Bernard A. Megrey
WA Fisheries and Marine Research Laboratory, National Oceanic and Atmospheric Administration, National
Department of Fisheries, PO Box 20, North Beach Marine Fisheries Service, Alaska Fisheries Science Center,
WA 6920, Australia Seattle, Washington, 98115, USA
Renato Guevara-Carrasco Todd Miller
Instituto del Mar del Perú, Apartado 22 Callao, Perú Center for Marine Environmental Studies, Ehime University,
Ehime, Japan
Dimitri Gutierrez
Instituto del Mar del Perú, Callao, Perú Christian Möllmann
Institute for Hydrobiology and Fisheries Science, University of
Rognvaldur Hannesson Hamburg, Hamburg, Germany
Norwegian School of Economics and Business Administration,
Helleveien 30, NO-5045, Bergen, Norway Coleen Moloney
zoology Department and Marine Research Institute, University
Samuel F. Herrick Jr. of Cape Town, Rondebosch 7701, South Africa
NOAA, NMFS, Southwest Fisheries Science Center, 8604 La
Jolla Shores Drive, La Jolla, California, 92037, USA Hideaki Nakata
Faculty of Fisheries, Nagasaki University, 1–14 Bunkyo-cho,
Kevin Hill Nagasaki, 852–8521, Japan
NOAA-NMFS, Southwest Fisheries Science Center, 8604 La
Jolla Shores Drive, La Jolla, California, 92037, USA Sergio Neira
Marine Biology Research Centre, University of Cape Town,
Larry Hutching Rondebosch 7702 Cape Town, South Africa
Marine and Coastal Management, Private Bag X2, Rogge Bay
8012, South Africa Miguel Ñiquen
IMARPE, Esquina Gamarra y General valle S/N, Chucuito,
Leire Ibaibarriaga Callao, Perú
AzTI-Tecnalia, Marine Research Unit, Herrera kaia Portualdea
z/g, 20110 Pasaia, Spain Hiroshi Nishida
National Research Institute of Fisheries Science, Fuku-ura 2–12,
Xabier Irigoien kanazawa-ku, Yokohama, 236–8648, Japan
Arantza eta Elikaigintzarako Institutu Teknologikoa, Pasaia,
Spain Jerrold G. Norton
NOAA, NMFS, Southwest Fisheries Science Center, 1352
Larry Jacobson Lighthouse Avenue, Pacific Grove, California, 93950, USA
NOAA-NMFS, Northeast Fisheries Science Center, 166 Water
Street, Woods Hole, Massachusetts, 02543–1026, USA Rosemary E. Ommer
University of victoria, CEOR, victoria, British Columbia,
Astrid C. Jarre v8W 2Y2, Canada
Danish Institute for Fisheries Research, The North Sea Centre,
P.O. Box 101, 9850 Hirtshals, Denmark Yoshioki Oozeki
National Research Institute of Fisheries Science, Fisheries
Souad Kifani Research Agency, 2–12–4 Fuku-ura, kanazawa, Yokohama,
Institut National de Recherche Halieutique, Casablanca, kanagawa, 236–8648, Japan
Morocco
Isabel Palomera
Fritz W. Köster Institut de Ciencias del Mar (CSIC), Passeig Marítim de la
Danish Institute for Fisheries Research, Jaegersborgvej 64–66, Barceloneta 37–49, 08003 Barcelona, Spain
Lyngby Dk-2800, Denmark
Julio Pena-Torres
Christophe Lett Universidad Alberto Hurtado, Erasmo Escala 1835, Santiago, Chile
Institut de Recherche pour le Développement, UR ECO-UP,
University of Cape Town, Oceanography Department, R. Ian Perry
Rondebosch, 7701, South Africa Fisheries and Oceans Canada, Pacific Biological Station,
Nanaimo, British Columbia, v9T 6N7, Canada
List of contributors xiii

Benjamin Planque Stylianos Somarakis

Institute of Marine Research – Tromsø, Postboks 6404, 9294 University of Patras, Department of Biology, 26500 Patra,
Tromsø, Norway Greece
Ruben Rodriguez-Sanchez Andy Soutar
Centro Interdisciplinario de Ciencias Marinas, La Paz, Drumlins Farm, Massena, New York, USA
Mexico
Yorgos Stratoudakis
Kenneth A. Rose Instituto Nacional de Investigaçäo Agrária e das Pescas (INIAP/
Department of Oceanography and Coastal Sciences, Louisiana IPIMAR), Avenida de Brasilia s/n, 1449–006 Lisboa, Portugal
State University, Baton Rouge, Louisiana, 70803, USA
U. Rashid Sumaila
Jean-Paul Roux Fisheries Economics Research Unit, Fisheries Centre,
Ministry of Fisheries and Marine Resources, Lüderitz, University of British Columbia, vancouver, British Columbia,
Namibia v6T 1z4, Canada
Claude Roy Hiroshige Tanaka
L’Institut de Recherche pour le Développement (IRD), Plouzané, Seikai National Research Institute, Fisheries Research Agency,
France Nagasaki, Japan
Suzana A. Saccardo Axel Temming
CNR-ISMAR, Largo Fiera della Pesca, 60125 Ancona, Italy Institute for Hydrobiology and Fisheries Science, University of
Hamburg, Hamburg, Germany
Renato Salvatteci
Centro de Investigación Científica y de Educación Superior de Andres Uriarte
Ensenada, km 107 Carretera Tijuana-Ensenada, Ensenada, Baja AzTI, Herrera kaia Portualde z/g, 20110 Pasaia (Guipuzkoa),
California, C.P. 22860, Mexico Basque country, Spain
Alberto Santojanni Carl D. van der Lingen
CNR-ISMAR, Largo Fiera della Pesca, 60125 Ancona, Italy Marine and Coastal Management, Private Bag X2, Rogge Bay
8012, South Africa
Jake Schweigert
Fisheries & Oceans Canada, Pacific Biological Station, 3190 Francisco Werner
Hammond Bay Road, Nanaimo, British Columbia, v9T 6N7, Marine Sciences Department, University of North Carolina,
Canada Chapel Hill, North Carolina, 27599–3300, USA

Rodolfo Serra Akihiko Yatsu

Instituto de Fomento Pesquero, Blanco 839, valparaiso, Hokkaido National Fisheries Research Institute, katsurakoi 116,
Chile kushiro 085–0802, Japan

Lynne Shannon
Marine Research (MA-RE) Institute, University of Cape Town,
Private Bag X3, Rondebosch 7702, Cape Town, South Africa
 Foreword

The effects of large-scale, environmentally driven changes current state of knowledge and future research prospects
on the distribution and abundance of fish populations have of small pelagics–climate interactions, their fisheries and
been a major source of concern for fishery scientists and related ecosystems.
managers for decades, particularly those dealing with the Science is an iterative learning process where current
assessment and management of small pelagic fisheries. researchers build on challenge as well as modify the find-
While much still needs to be investigated and elucidated, ings of their predecessors. To make progress in science,
significant progress has been made in describing and one needs to look at and analyze the past. The historical
understanding the primary aspects of observed large-scale perspective provided in Chapters 1 and 2 fulfills this pur-
changes in small pelagic fish production and the most likely pose by including a brief but thorough review of the main
causal mechanisms, climate–fish abundance interactions, international research initiatives, working hypotheses,
patterns of change, species interactions, and many other mathematical models, research results and findings, and
important issues. A newer and additional difficulty is that meetings and events where these were publicized and dis-
global climate change is altering the structure and function- cussed, some of which are now considered major bench-
ing of marine ecosystems, which in turn affects availability marks in the development of our current understanding
of ecological resources and benefits, changes the magnitude of the variability of small pelagic fish populations. These
of some feedbacks between ecosystems and the climate sys- two chapters highlight the progress made in the last three
tem, and will affect economic systems that depend on mar- decades towards understanding the effects of climate on
ine ecosystems. Newer questions and uncertainties have the life history and population dynamics of small pelag-
to be faced. For instance, will there be an increase in vari- ics and on the use of this knowledge for, first, challenging
ability from season to season and year to year? Predictions traditional fisheries management approaches typical of the
of such changes in the future are likely to be less reliable 1950s, 1960s and 1970s where the aim was maximizing
than they may have been in the past, given that the past will long-term production under steady-state assumptions, and,
become less useful as a guide to the future. second, moving towards fully recognizing the importance
There is, therefore, a pressing need to assess progress of climate-induced fluctuations and changes in these fish
made in knowledge development and emerging challenges populations and the various spatial and temporal scales
regarding the variability of and changes in marine eco- on which they vary. Reference is also made to more recent
systems, including the dynamics of populations of small efforts towards trying to elucidate the role of small pelagics
pelagic fish, which collectively occupy a central role in the in regulating the ecosystems and to the steps being taken
food web. This book makes an important and timely contri- to move towards a fisheries management that takes more
bution to this overall need. It covers the major trends, find- into account the ecosystem as a whole, in line with the prin-
ings and results of various international research efforts ciples of the Ecosystem Approach to Fisheries (EAF) pro-
aimed at improving our understanding of climate-induced moted by the FAO.1
changes in the production and abundance of small pelagic The habitat characteristics of the main marine systems
fish populations, as well as progress made in assessing the hosting particularly large populations of small pelagic
predictability of future changes. fish are described and discussed in Chapter 3. This chap-
The book builds mostly on the results achieved through ter highlights both the uniqueness and similarities of these
the collaborative research work undertaken under the aus- habitats, as well as the possible effects of future climate
pices of the Small Pelagic Fish and Climate Change regional change on them. The natural variability of small pelagics
programme (SPACC) of the Global Ocean Ecosystem is well covered in Chapter 4, while Chapter 5 describes
Dynamics international project (GLOBEC). Indeed, this decadal-scale fluctuations of small pelagics. Analyses of
publication represents one of the major achievements of scales in marine sediments, archeological remains and his-
SPACC/GLOBEC. Over the subsequent 15 chapters, a torical records confirm that small pelagics did vary con-
well-selected group of international experts has summa- siderably prior to the development of current industrial
rized working hypotheses, results and findings in their
own fields of expertise. The end result is a successful and
comprehensive technical summary and assessment of the 1
Food and Agriculture Organization.
xvi Foreword

fishing, but also show important differences in the variabil- gic fisheries were allowed to rebuild, which is in agreement
ity patterns of small pelagic populations during the nine- with circumstantial evidence for some systems.
teenth and the twentieth centuries, with some extremes in The assessment and management of small pelagic fish-
variability occurring on shorter time scales under intensive eries, including the social and economic dimensions, are
fishing. This suggests that ecosystem paradigms based on well examined in Chapters 9, 10 and 11. The assessment
industrial catch records and modern observations may only and management approaches, methods, models, harvest-
capture a small part of the range of intrinsic variability of ing strategies, and controls and regulatory measures used
small pelagics, thus limiting our understanding of the pos- in selected major small pelagic fisheries are analyzed in
sible responses to climate change. Nevertheless, observa- Chapter 9. The point is made that the speed of response and
tions of catch records and other usually higher-resolution the flexibility of management that these highly variable
twentieth and twenty-first century records confirm that fisheries demand can only be provided though properly
populations of small pelagics are characterized by large tailored scientific assessment and management programs,
and relatively long-lasting changes in their abundance while noting that improved management of fisheries and
and in other population parameters, which are often asso- related ecosystems is essential in adapting to the impacts
ciated with regime shifts in the dynamics of their marine of climate change in fisheries. Chapter 10 examines a full
ecosystems. There is also growing evidence that these eco- range of economic benefits small pelagics can provide,
system shifts could be associated with large-scale changes including their direct commercial value as well as their
in subsurface processes and basin-scale circulation in the value as prey of predators of higher commercial value and
oceans. for recreational and non-commercial predators, including
Chapters 6, 7 and 8 cover the several biophysical and international and domestic considerations when looking
trophic dynamics models that have been developed and/or at different management and conservation options. Social
are applied to small pelagics to synthesize current under- and economic aspects are further dealt with in Chapter 11,
standing, test hypotheses and examine potential conse- where important issues such as social and economic power,
quences of changes in environmental conditions and species institutional frameworks, resource access rights, equity,
interactions. Chapter 6 provides a thorough overview of property rights, differences in temporal and spatial scales,
models that include the physical environment and the popu- market globalization, ethics, technology, and interactive
lation dynamics of either early life stages of fish or juveniles political agendas between developed and developing coun-
and adults. While referring to the various models, their tries are examined and discussed.
input requirements, computing challenges and forecasting Future challenges and ways forward are summarized and
capabilities, the point is made that much effort is still neces- highlighted in the last four chapters. Chapter 12 examines
sary to get to the stage of having usable “physics-to-fish full potential mechanisms for the low-frequency variability in
life-cycle models” capable of addressing the long-term con- sardine and anchovy populations discussed in other sec-
sequences of climate change on fish and fisheries. Chapter 7 tions. A working theory is proposed in which sardine prod-
provides an updated review of the trophic dynamics of small uctivity is linked to low-frequency variability in boundary
pelagics, using seven selected regional case studies and current flows, with weaker flow periods being favorable
information on feeding-apparatus morphology, diet compos- for extended sardine reproductive success and stronger
ition, foraging behavior, and other observations used for the flow periods restricting reproduction success to coastal
parameterization of bioenergetic and other trophic dynamic areas. On the other hand, anchovies are always restricted
models. In discussing the interactions and disparities in the to coastal waters and are more influenced by upwelling
trophic dynamics of coexisting small pelagic species, and and coastal productivity (which tend to be correlated with
between anchovy and sardine in particular, it is suggested boundary current fluctuations), giving rise to a tendency of
that the observed abundance alternations between the two sardine and anchovy alternations. A number of unresolved
could be trophically mediated. The use of trophic models issues key for improved management and understanding of
to examine the trophic dynamic role of small pelagics in small pelagics and their related ecosystems are examined in
five selected marine ecosystems is described in Chapter 8, Chapter 13. In particular, this chapter explores further the
where it is reported that the models analyzed show how a wasp-waist concept, according to which a dominant highly
decrease in small pelagic fish abundance will have detri- variable small pelagic fish population, largely responding to
mental effects on both higher and lower trophic levels of its own internal dynamics, may significantly drive the oper-
the food web and that, for instance, trophic model simula- ation of its entire ecosystem. Several types of non-linear
tions consistently suggest that gelatinous zooplankton may feedback mechanisms, breakout thresholds, distributional
increase when small pelagic fish stocks decline. Conversely, dynamics, density dependent growth, niche replacement
a decrease in jellyfish abundance may be expected if pela- and mechanisms of species alternations are discussed,
Foreword xvii

in support of proposals, worth noting, for research in the global climate change requires even more precautionary
years to come. Chapter 14 points out that there is already and adaptive approaches on behalf of all stakeholders.
evidence of sensitivity of small pelagic species and related
ecosystems to climate change and of decreased resilience Jorge Csirke (FAO)
of natural ecosystems caused by overexploitation. Possible Michael H. Glantz (NCAR )2
1

scenarios of climate and ecosystem change are then dis- James Hurrell (NCAR)
cussed to identify significant gaps in the knowledge of proc-
esses and interactions between changes in climate and other Addresses and Affiliations:
ecosystem stressors. Lastly, the book concludes with a thor- Jorge Csirke
ough synthesis in Chapter 15 of SPACC, its reasons to exist Director
and its major work and findings. Much of it is distilled from Fisheries and Aquaculture Management Division
the ideas and findings reported in the first fourteen chap- Fisheries and Aquaculture Department
ters while emphasizing that, for instance, observations from Food and Agriculture Organization of the United Nations
both paleontological and historical records are consistent (FAO)
with a conceptual model in which populations fluctuate viale delle Terme di Caracalla
due to extrinsic rather than intrinsic factors, which in turn 00153 Rome, Italy
is consistent with the observed out-of-phase variations of
sardines and anchovies. Also emphasized is that humans Michael H. Glantz 3 2

must be considered an important part of the ecosystem Director

and that overexploitation decreases resilience of systems to Center for Capacity Building (CCB)
climate change as well as to more “ normal” climate con- National Center for Atmospheric Research
ditions, while reference is made to the wasp-waist concept Box 3000
and the pivotal role small pelagics play in the ecosystems Boulder, Colorado 80307
in which they are found. Main gaps in current knowledge USA
and understanding of small pelagic fish dynamics are fur-
ther discussed, concluding that: the synthetic approach so James Hurrell
far focused on small pelagics in highly productive upwell- Senior Scientist
ing regions shall be extended to multiple systems at a global National Center for Atmospheric Research
scale, including, for example, western boundary currents; Climate and Global Division
future research work be undertaken under the aegis of an PO Box 3000
international program like SPACC, using the comparative Boulder, Colorado 80307-3000, USA
approach and involving scientists from a broad spectrum of
disciplines, including climate, fisheries, oceanography, and 2
National Center for Atmospheric Research.
the social sciences; and that a periodic international assess- 3
Address as of January 1, 2009:
ment of the state of science and climate effects on small Michael H. Glantz, Director
pelagic fish be undertaken, as in other fields of science. A Consortium for Capacity Building
Institute for Arctic and Alpine Research
key point brought out by the book as a whole is the import- University of Colorado
ance of a more ecosystem-oriented approach to research and Boulder, Colorado 80309–0450
fisheries management. Regarding the latter, one may stress that USA.
 Preface

Small pelagic fish include anchovy, sardine, herring, and will form a basis and hence point of departure for future
sprat. They comprise approximately one-quarter of the research.
world’s fish catch. The abundance and catch of the small The book consists of 15 chapters. Each, save the first,
pelagic fish fluctuate greatly on the scale of decades, nota- contains a summary and boxes, the latter connecting the
bly anchovy and sardine off Peru, Japan, Southern Africa, chapters to the overarching theme of climate change and
and California. Climate varies on the same scale. How small pelagic fish. Chapters 1 and 2 provide a historical
does climate affect small pelagic fish? Can our understand- context. Chapter 3 describes habitats of the major stocks.
ing of this relationship be used to inform management and Chapters 4 and 5 concern past variability of small pelagic
policy? fish, inferred from sediments and historical records.
Small pelagic fish occupy a key position in marine Chapters 6, 8, and 12 address models, and Chapter 7 trophic
ecosystems. They respond to change from below (climate, dynamics. Chapters 9, 10, and 11 concern the fisheries for
bottom-up) and above (fishing, top-down). In turn, variation small, pelagic fish, stock-by-stock and globally, and the
of stocks of small pelagic fish affect their prey (plankton) human dimensions of climate change and small pelagic
and predators (e.g. fish, marine birds and mammals, and fish. Chapters 13 and 14 address the future. Chapter 15 pro-
human). Capture fisheries are now maximal and, as the vides a synthesis and recommendations.
human population increases, aquaculture will thus con- This book would not have been possible without the long-
tinue to grow, exacerbating the demand for small pelagic term support of GLOBEC and its contributing members.
fish as food for cultured fish. The complex ecosystem and L’Institut de Recherche pour le Développement (IRD) of
economic roles of small pelagic fish necessitate a holistic France provided partial support for a workshop on and pro-
view of their dynamics. duction of the book. Finally, we express our appreciation
The Small Pelagic Fish and Climate Change (SPACC) to John Hunter who, with Jürgen Alheit, founded SPACC
program is a part of Global Ocean Ecosystem Dynamics and was its former co-chair, leading it with good nature,
(GLOBEC). SPACC was formed to understand and predict wisdom, and the insight of a fisheries scientist.
climate-induced changes in the production of small pelagic
fish. It is unusual in being composed of scientists from David M. Checkley, Jr.
both academia and management. This book, a product of Jürgen Alheit
SPACC, presents the status of our understanding in 2008. It Yoshioki Oozeki
has 82 authors from 22 countries in Africa, Asia, Australia, Claude Roy
Europe, and North and South America. Our hope is that it
 1 History of international
co-operation in research
Jürgen Alheit and Andrew Bakun

Over the last 25 years, since about 1980, international the formation of a “Group of Four” experts (Bakun et al.,
co-operation in research on small pelagic schooling fish 1982) to advise on program formulation. FAO and SCOR3
with pelagic eggs, such as anchovy, sardine, sprat, and were asked in the resolution to develop a comprehensive
sardinella focused, first on processes determining recruit- scientific program for OSLR. SCOR and the ACMRR4
ment variability and, then, since the mid 1990s, on the of FAO responded to the IOC request forming Working
impact of climate variability on ecosystems dominated by Group 67 on “Oceanography, Marine Ecology and Living
small pelagics. Recruitment research was carried out to a Resources.” This group was formed with the aim to develop
large extent under the umbrella of the Sardine–Anchovy– a proposal for an international recruitment experiment to
Recruitment Program (SARP) within the Ocean Science investigate the relationships between environmental vari-
in Relation to Living Resources Program (OSLR) run ability and fluctuations of living resources (Barber et al.,
jointly by IOC1 and FAO2 and the Climate and Eastern 1982). The same year, coincidentally, the “Fish Ecology
Ocean Systems project (CEOS) conducted by a variety of III Conference” in the USA developed a conceptual frame-
research institutions. work for REX, a “recruitment experiment” (Rothschild and
Lack of scientific understanding of the mechanisms Rooth, 1982). In the meantime, a “Workshop on the Effects
regulating recruitment was widely recognized in the 1980s of Environmental variation on Survival of Larval Pelagic
(and still is) as the key unsolved scientific problem cur- Fishes” (IOC, 1981) was organized in Lima as a contribu-
rently hindering effective management of small pelagic fish tion to OSLR by FAO and the Peruvian–German technical
populations. Their collapses such as the Californian sar- aid project PROCOPA5 (Pauly and Tsukayama, 1987) was
dine or the Peruvian anchovy have had enormous negative established at the Peruvian fisheries institute, IMARPE.6
economic and social effects on fishing nations which might These efforts finally converged in a joint “Ocean Science in
have been avoided had there been the opportunity to pre- Relation to Living Resources” (OSLR) program, which was
dict recruitment. Consequently, several international and co-sponsored by IOC and FAO, the main focus of which
national initiatives were started in the 1980s to understand was to be the processes governing recruitment to fish popu-
the relationship between environmental processes and fish lations (IOC, 1983).
recruitment. At this point, Reuben Lasker’s “stable ocean The DEPM is a fisheries-independent method to esti-
hypothesis” (Lasker, 1975, 1978) had suddenly caught the mate the spawning biomass of small pelagics, includ-
attention of the fisheries scientific community, and provided ing the associated statistical precision of the estimated
a major conceptual basis for motivating and planning the value. It was developed at the Southwest Fisheries Science
early activity. Simultaneously, two new technologies, the Center in La Jolla under the leadership of Reuben Lasker
“Daily Egg Production Method” (DEPM) (Lasker, 1985) (Lasker, 1985). The breakthrough for its development was
and a technique for daily age and growth estimates based the finding of Hunter and Goldberg (1980) that the age of
on measuring and counting daily marks laid down on lar- postovulatory follicles can be used to estimate the daily
val fish otoliths (Methot, 1983), were under development in proportion of spawning females. After its first applica-
Lasker’s laboratory. By increasing the temporal resolution tion to the Californian anchovy in 1980, it was success-
of demographic studies on fish larvae, these appeared to fully carried out for the Peruvian anchovy (Santander
offer promising new ways to seek improved understanding et al., 1984) and is now widely used in South America,
of fish recruitment variability. South Africa and Europe (Alheit, 1993; Stratoudakis et
At its 11th Assembly in 1979, the IOC passed resolution al., 2006). The application of this method for spawn-
XI-17 to promote development of plans for major oceano- ing biomass estimates requires extensive knowledge of
graphic studies of the physical–ecological interactions of reproductive parameters such as batch fecundity, spawn-
importance to fishery resource-related problems, including ing frequency and daily egg mortality and, consequently,

Climate Change and Small Pelagic Fish, eds. Dave Checkley, Jürgen Alheit, Yoshioki Oozeki, and Claude Roy. Published by Cambridge University
Press. © Cambridge University Press 2009.
2 J. Alheit and A. Bakun

as a by-product, has furthered international co-operation coupled with a comprehensive physical and biological
in recruitment research. oceanographic sampling program designed to determine
The Lima Workshop in 1980 (IOC, 1981) brought variations in conditions related to larval starvation (Lasker,
together an international group of recruitment researchers 1981), predation (Lasker, 1981), advection, physiological
with scientists working on reproduction and recruitment of stress, and other factors leading to mortalities of early life
the Peruvian anchovy and allowed comparisons of recruit- stages. Later in the season, surviving juveniles were to be
ment processes between small pelagics in the Humboldt sampled and their birthdate frequencies determined using
and California currents. Important outcomes of this meet- daily otolith growth rings (Methot, 1983). These frequen-
ing were the first quantitative estimate of egg cannibalism cies, when compared with the observed larval production
(MacCall, 1980) and the first sketch of the “Basin Model,” rates corresponding to the various birthdates, provide an
an attempt to explain population dynamics of small pelag- index of variation in survival rate of early life stages. This
ics based on an “optimal free distribution” interrelationship is compared to variations in environmental processes to
between geography, movement, and growth dynamics at identify the mechanisms that best explain the observations.
the population level (MacCall, 1990). It also produced an The SARP concept therefore, while basically an empirical
early comprehensive review (Bakun and Parrish, 1981) of field approach, offered a major departure from previous
empirical and conceptual frameworks for applying available empirical approaches to study the recruitment problem in
environmental data to inferring the primary causative fac- its ability to address higher frequency “within-year” vari-
tors in recruitment variability, including the suggestion for ability. Whereas previous empirical attempts have been
the formulation that became known as “Lasker windows” defeated by the necessity to combine shorter scale varia-
(Peterman and Bradford, 1987; Pauly, 1989). tions, having various causes, into single annual composites,
A most authoritative account on the ecology of marine SARP offered the possibility of resolving different causes
fish larvae with a focus on anchovy and sardine was pub- and effects on the time scales on which they actually act to
lished in 1981 by four eminent fish larval researchers from determine net reproductive success.
the Southwest Fisheries Center in La Jolla: R. Lasker, J.R. Accordingly, a number of regional field-going SARP
Hunter, H.G. Moser and P.E. Smith (Lasker, 1981). It contains components (direct investigations) were initiated to test
a thorough discussion of the role of larval starvation and pre- the several recruitment hypotheses (starvation, preda-
dation on fish larvae for recruitment and was a pacemaker for tion, advection) (Bakun et al., 1991): a US SARP in the
the Sardine–Anchovy Recruitment Program, SARP. California Current on anchovy, an Iberian SARP on
The 12th Assembly of IOC in 1982 adopted the OSLR anchovy and sardine in a joint Spanish–Portuguese–US
concept as a long-term program. It promoted coordinated project (López-Jamar and Garcia, 1992), a SW Atlantic
regional research projects to elucidate factors determin- SARP on anchovy and sardine in a co-operation by Brazil,
ing recruitment to fish populations with the International Uruguay, Argentina, Germany, and Sweden (Alheit et
Recruitment Project (IREP) as the initial main focus al., 1991) and a EURO-SARP7 project on anchovy, sar-
of OSLR. The Assembly established a Guiding Group dine, and sprat in European waters run by scientists from
of Experts for the OSLR Program and initiated the Germany, Spain, Portugal, and the Uk (Alheit and Bakun,
“Workshop on the IREP Component of the IOC Program 1991; valenzuela et al., 1991). A major aspect of SARP’s
on Ocean Science in Relation to Living Resources” in scientific rationale was the application of the comparative
Halifax, Canada, in 1983 (IOC, 1983). This workshop, method of science, whereby the multiple expressions of
under the chairmanship of R. Beverton, recommended (i) the problem afforded by various species groups inhabiting
direct investigations of the early life history, particularly different regional ecosystems were considered as “proxy
SARP, including, inter alia, the otolith ring method, the replicates” of similar processes, gaining additional explan-
DEPM and relevant oceanographic measurements (IREP atory power (degrees of freedom), to sort out the complex
Minimum Plan) and (ii) indirect (inferential) approaches interacting mechanisms involved in recruitment variabil-
by making available the wealth of long-term time series, ity. The comparative scientific method (Bakun, 1996) is
including relevant information, normally peripheral to the particularly appropriate to problem areas where experi-
marine field, such as climatic and meteorological data that mental controls are unavailable. This is one of the reasons
could help to elucidate the physical and biological coupling why a coordinated international scientific SARP effort
controlling recruitment at different scales. was thought to offer large potential benefits. Whereas all
At its first meeting in Paris in 1984, the Guiding Group these SARP initiatives provided a wealth of new important
of Experts for OSLR recommended SARP as the pilot information on the life history of small pelagics, it has to be
program for IREP. The basic SARP concept involved admitted that no breakthrough was made in understanding
repeated surveys of larval production during the extended and predicting recruitment. The main constraint was that
spawning season of small pelagic fish. These surveys were no regional initiative had sufficient funding to carry out the
History of international co-operation in research 3

complete SARP program. On the other hand, the increase in processes and ecosystem responses, and (3) to resolve under-
temporal resolution for the study of larval demography was lying global-scale trends that in each individual regional sys-
insufficient by itself to explain differential larval mortality tem may be obscured by local interannual and interdecadal
without a comparable increase in resolution in the observa- variability. Major ideas emanating from the CEOS project
tion of the potentially causally related oceanographic vari- are (i) the “Ocean Triad Concept” of Bakun (1996) which
ables. A serious blow was delivered to the SARP initiative suggests that an optimal combination of three physical proc-
when the most promising US SARP project was stopped esses (enrichment, concentration, retention) provides an
suddenly by federal budget restrictions. optimal situation for successful fish recruitment and (ii) the
Progress was made using inferential methods as sug- “Optimal Environmental Window” hypothesis (Cury and
gested by the Guiding Group of Experts. Scientists from Roy, 1989), which is a dome-shaped response curve of popu-
the Peruvian–German aid project PROCOPA teamed up in lation growth to increasing intensity of wind stress-associ-
1981 with an international group to rescue, assemble, and ated mixing and transport. The CEOS project paved the way
analyze on a monthly basis long-term time series from the for SPACC, as it started to look not only at recruitment, but
period 1953–1982 of all measured variables likely to have also at climatic effects on the dynamics of small pelagics.
affected the Peruvian anchovy and its ecosystem. This SARP had established itself in the international science
resulted in an extremely rich data archive captured in two community so much that it opened access to national fund-
books (Pauly and Tsukayama, 1987; Pauly et al., 1989), ing to carry out recruitment research. Although the large
which have served as an important source in later studies on international funding hoped for in the mid 1980s never
the impact of climate variability on the Humboldt Current materialized, several SARP projects were established suc-
and its small pelagic fish resources (e.g. Alheit and Bernal, cessfully using national funding. However, due to its com-
1993; Alheit and Niquen, 2004). plexity the recruitment problem could not be solved by
A meeting which proved to be a milestone in small SARP. It became clear in the early 1990s that (i) recruitment
pelagics research was the “Expert Consultation to Examine studies must be conducted from an ecosystem point of view
Changes in Abundance and Species Composition of Neritic and that (ii) climatic effects play a major role in population
Fish Resources” organized by G. Sharp and J. Csirke of FAO fluctuations of small pelagics leading to so-called regimes
in 1983 in San José, Costa Rica (FAO, 1983). This meeting (Lluch-Belda et al., 1992).
gathered most of the information on ecology and fisheries of Consequently, SARP and CEOS researchers widened
the large stocks of small pelagics relevant then for SARP and the scope of their investigations accordingly and jointly
later for Small Pelagic Fish and Climate Change, SPACC, created in 1994 the SPACC (Small Pelagic Fishes and
a regional project of the GLOBEC8 program, particularly Climate Change) project which became one of the four
from developing countries, and still serves as a rich source core projects of GLOBEC of the IGBP (International
of information. A key paper which was an enormous stimu- Geosphere Bioshere) Program. Science (Hunter and
lus for climate variability research within SPACC even 20 Alheit, 1995) and Implementation (Hunter and Alheit,
years thereafter was given by T. kawasaki (1983) on syn- 1997) plans of SPACC were developed at three inter-
chronous large-scale fluctuations of the three sardine stocks national meetings in La Paz, Mexico (1994), Swakopmund,
in the Pacific. Namibia (1995), and Mexico City (1996). SPACC’s
The CEOS project (Durand et al., 1998) was an interna- objective is to clarify the effect of climate variability on
tional collaborative study of potential effects of global cli- the population dynamics of pelagic fish by comparing the
mate change on the living resources of the highly productive ecosystems that support such populations (Hunter and
eastern ocean upwelling ecosystems and on the ecological Alheit, 1995). The goals are (i) to describe the charac-
and economic issues directly associated with such effects. teristics and variability of the physical environment and
CEOS involved a variety of research institutions, notably of zooplankton population dynamics and their impact on
NOAA/NMFS,9 ORSTOM,10 and ICLARM,11 and was small pelagic fish populations in each key ecosystem and
devoted to a study of the potential effects of global change (ii) to improve understanding of the nature and causes of
on the resources of upwelling systems through identifica- long-term changes in these ecosystems. SPACC uses two
tion of global and local effects impacting on these systems. general approaches to meet these goals:
A major focus of the study was the clupeoid fishes (such
as anchovy and sardine). The main objectives were: (1) to (1) Retrospective studies, wherein ecosystem histories are
assemble, summarize, and analyze the data record of the reconstructed by means of fishery data and zooplank-
four decades since 1960 regarding the four eastern bound- ton and other time series and paleoecological data. This
ary upwelling ecosystems and other upwelling areas, (2) initiative was started in 1994 when SPACC researchers
to apply the comparative method to identify key physical analyzed long-term data from ecosystems rich in small
4 J. Alheit and A. Bakun

pelagics, together with SCOR Working Group 98 on Bakun, A. (1996). Patterns in the Ocean: Ocean Processes and
“World-wide Large-Scale Fluctuations of Sardine and Marine Population Dynamics. University of California,
Anchovy Populations” (Schwartzlose et al., 1999). La Jolla: California Sea Grant College System, 323 pp.
(2) Process studies in which cause-and-effect linkages Bakun, A. and Parrish, R. H. (1981). Environmental inputs to
fishery population models for eastern boundary current
between zooplankton, fish population dynamics and
regions. In Workshop on the Effects of Environmental
ocean forcing are inferred from comparisons of stand-
Variation on Survival of Larval Pelagic Fishes, Lima, 20
ard measurements made in different ecosystems. April – 5 May 1980, Sharp, G. D., ed. Intergovernmental
The long-range goal is to develop predictive scenarios Oceanographic Commission, Unesco, Paris, Workshop
for the fate of small pelagic fish populations. Results of the Rep. 28, p. 67–104.
Bakun, A., Beyer, J., Pauly, D., Pope, J. G., and Sharp, G. D.
SPACC project are presented in the following chapters.
(1982). Ocean sciences in relation to living resources. Can.
J. Fish. Aquat. Sci. 39: 1059–1070.
Acknowledgments Bakun, A., Alheit, J., and kullenberg, G. (1991). The Sardine-
Anchovy Recruitment Project (SARP): rationale, design
The authors wish to thank Patricio Bernal (IOC) and Jorge and development. ICES C.M. 1991/L: 43.
Csirke (FAO) for reviewing the manuscript and many valu- Barber, R. T., Csirke, J., Jones, R., Lasker, R., Parrish, R., and
able suggestions. Tomczak., M. (1982). Report of SCOR/ACMRR Working
Group 67, Oceanography, Marine Ecology and Living
Resources. SCOR/WG-67, 21pp.
Cury, P. and Roy, C. (1989). Optimal environmental window and
Not e s pelagic fish recruitment success in upwelling areas. Can. J.
1 Intergovernmental Oceanographic Commission. Fish. Aquat. Sci. 46: 670–680.
2 Food and Agriculture Organization. Durand, M.-H., Cury, P., Mendelssohn, R., Roy, C., Bakun, A.,
3 Scientific Committee on Oceanic Research. and Pauly, D. (eds.) 1998. Global Versus Local Changes in
4 Advisory Committee of Experts on Marine Resources Upwelling Systems. Paris: ORSTOM editions, 594 pp.
Research. FAO (1983). Proceedings of the Expert Consultation to Examine
5 Peruvian–German Cooperative Program for Fisheries Changes in Abundance and Species Composition of Neritic
Investigations. Fish Resources. FAO Fish. Rep. 291, 1224 pp.
6 Instituto del Mar del Perú. Hunter, J. R. and Alheit, J. (1995). International GLOBEC Small
7 European Sardine–Anchovy Recruitment Program. Pelagic Fishes and Climate Change Program. GLOBEC
8 Global Ocean Ecosystem Dynamics. Report No. 8, 72 pp.
9 US National Oceanic and Atmospheric Administration/ Hunter, J. R. and Alheit, J. (1997). International GLOBEC
National Marine Fisheries Service. Small Pelagic Fishes and Climate Change Program.
10 Office de la Recherche Scientifique et Technique Outre Mer. Implementation Plan. GLOBEC Report No. 11, 36 pp.
11 International Center for Living Aquatic Resources Hunter, J. R. and Goldberg, S. R. (1980). Spawning incidence and
Management. batch fecundity in northern anchovy, Engraulis mordax.
Fish. Bull. (US) 77: 641–652.
IOC (1981). Workshop on the Effects of Environmental Variation
R e f e r enc e s on Survival of Larval Pelagic Fishes, Lima, 20 April–
Alheit, J. (1993). Use of the daily egg production method for esti- 5 May 1980. G. D. Sharp (ed.). Intergovernmental
mating biomass of clupeoid fishes: a review and evaluation. Oceanographic Commission, Unesco, Paris, Workshop
Bull. Mar. Sci. 53: 750–767. Rep. 28, 323 pp.
Alheit, J. and Bakun, A. (1991). Reproductive success of sprat IOC (1983). Workshop on the IREP Component of the IOC
(S. sprattus) in German Bight during 1987. ICES C.M. Programme on Ocean Science in relation to Living
1991/L:44. Resources (OSLR). Intergovernmental Oceanographic
Alheit, J. and Bernal, P. (1993). Effects of physical and biologi- Commission, Unesco, Paris, Workshop Rep. 33, 17 pp.
cal changes on the biomass yield of the Humboldt Current kawasaki, T. (1983). Why do some pelagic fishes have wide
ecosystem. In k. Sherman, L. M. Alexander, and B. D. Gold fluctuations in their numbers? – Biological basis of fluc-
(eds.), Large Marine Ecosystems – Stress, Mitigation and tuations from the viewpoint of evolutionary ecology.
Sustainability, pp. 53–68. Washington, DC: American In Proceedings of the Expert Consultation to Examine
Association for the Advancement of Science, 376 pp. Changes in Abundance and Species Composition of
Alheit, J. and Niquen, M. (2004). Regime shifts in the Humboldt Neritic Fish Resources, Sharp, G. and Csirke, J., eds. FAO
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Alheit, J., Ciechomski, J., Djurfeldt, L. et al. (1991). SARP Lasker, R. (1975). Field criteria for survival of anchovy lar-
studies on the Southwest Atlantic anchovy, Engraulis vae: the relation between inshore chlorophyll maximum
anchoita, off Argentina, Urugay and Brazil. ICES layers and successful first feeding. Fish. Bull. (US) 73:
C.M./L: 46, 32 pp. 453–462.
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Lasker, R. (1978). The relation between oceanographic condi- Pauly, D. (1989). An eponym for Reuben Lasker. Fish. Bull. (US)
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identification of factors contributing to recruitment Pauly, D. and Tsukayama, I. (eds.) (1987). The Peruvian ancho-
failure. Rapp. P.-v. Réun. Cons. Int. Explor. Mer. 173: veta and its upwelling ecosystem: Three decades of
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Ecology and Relation to Fisheries. Seattle: University of The Peruvian upwelling ecosystem: Dynamics and inter-
Washington Press, 131 pp. actions. ICLARM Conference Proceedings 18, 438 pp.
Lasker, R. (ed.) (1985). An egg production method for estimat- Peterman, R. M. and Bradford, M. J. (1987). Wind speed and mor-
ing spawning biomass of pelagic fish: application to the tality rate of a marine fish, the northern anchovy (Engraulis
northern anchovy (Engraulis mordax). NOAA Techn. mordax). Science 235: 354–356.
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Lluch-Belda, D., Schwartzlose, R. A., Serra, R. et al. (1992). Foundation for REX, A Recruitment Experiment. University
Sardine and anchovy regime fluctuations of abundance in of Miami Tech. Rep. 82008; Miami, Florida, USA, 389 pp.
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Oceanogr. 1: 339–347. biomasa de la población desovante de anchoveta peruana,
López-Jamar, E. and Garcia, A. (1992). Foreword. Boletín Engraulis ringens, en 1981 por aplicacion del “Método
Instituto Espanol de Oceanografía 8: 3–4. de Producción de Huevos”. Boletin Instituto del Mar del
MacCall, A. D. (1980). The consequences of cannibalism in the stock- Perú-Callao 8: 208–250.
recruitment relationship of planktivorous pelagic fishes such Schwartzlose, R. A., Alheit, J., Bakun, A. et al. (1999). Worldwide
as Engraulis. In Workshop on the Effects of Environmental large-scale fluctuations of sardine and anchovy popula-
Variation on the Survival of Larval Pelagic Fishes, G. tions. S. Afr. J. Mar. Sci. 21: 289–347.
Sharp, ed. Intergovernmental Oceanographic Commission, Stratoudakis, Y., Bernal, M., Ganias, k., and Uriarte, A. (2006).
Unesco, Paris, Workshop Report 28, pp. 201–220. The daily egg production method: recent advances, current
MacCall, A. D. (1990). Dynamic Geography of Marine Fish applications and future challenges. Fish Fish. 7: 35–57.
Populations. Seattle: University of Washington Press, 153 pp. valenzuela, G. J., Alheit, J., Coombs, S., and knust, R. (1991).
Methot, R. D. (1983). Seasonal variation in survival of larval Spawning patterns of sprat and survival chances of sprat
anchovy, Engraulis mordax, estimated from the age distri- larvae in relation to frontal systems in the German Bight.
bution of juveniles. Fish. Bull. (US) 81: 741–750. ICES C.M. 1991/L:45.
 2 A short scientific history of the
fisheries
Alec D. MacCall

CON T E N T S Introduction
Summary This history of small pelagic fisheries focuses specifically
Introduction on the development of a scientific understanding of their
The classical period dynamics, especially regarding their problematic fluctua-
The doubt period tions in abundance. Fréon et al. (2005) describe several dis-
A new millennium tinct historical periods in the study of pelagic fish stocks, a
Acknowledgments system that is adopted for this review. During the pre-1900
References “mother nature period”, oceanic fish stocks tended to be
regarded as inexhaustible, and little attention was given to
the patterns and dynamics of their fluctuations. Fréon et al.
do not give a name to the first half of the twentieth century,
Summary but it could be called the “developmental period.” They
describe the period 1900–1950 as being a time of indus-
This chapter briefly summarizes the history of scientific
trial development, the beginnings of scientific studies, and
understanding of the fluctuations of small pelagic fishes
growing awareness of environmental influences. The third
and fisheries. The classical quantitative models underlying
quarter of the twentieth century, which could be called
modern fishery analysis and management were developed
“the classical period” saw the development of the classical
in the 1950s and 1960s. Although California and Japan
models of fish population dynamics, and is where this brief
had previously experienced collapses of major fisheries for
review begins.
small pelagics in the 1940s and 1950s, it was the collapse
The fourth quarter of the twentieth century was aptly
of the “scientifically managed” Peruvian anchoveta fish- termed “the doubt period” by Fréon et al. (2005). Whereas
ery in the early 1970s that drew worldwide attention to the the mathematical models developed during the preced-
problem of collapsing small pelagic fisheries. The inability ing period had engendered a confidence that good science
of the anchoveta to regain its former levels of productiv- would lead to high and sustainable yields, a growing world-
ity cast doubt on the classical equilibrium fishery models.
wide list of fishery collapses (Mullon et al., 2005) steadily
In the late twentieth century, substantial progress was made eroded that confidence. Because ideas and events after 1980
toward understanding the environmental influences on are extensively covered by several other chapters, recent
these fishes. Some of the major environmental influences developments are treated more briefly in this chapter.
(which often may not be specifically identified) fluctuate at
interdecadal time scales, giving rise to prolonged periods of
high and low fish productivity, abrupt transitions including
The classical period
collapses, global teleconnections and phase relationships.
These so-called “regimes” have recently become a major By the mid twentieth century, there was a widespread
topic of research in fishery science. Despite scientific pro- perception that fisheries for small pelagics tend to be more
gress in understanding many facets of these fisheries and prone to collapse than are those for other types of marine
their fluctuations, there still is no accepted theory of the fishes. Large fisheries for sardines off Japan (Sardinops
fishery–oceanographic dynamics of small pelagic fishes melanosticta) and California (S. sagax caerulea) collapsed
that links their commonly shared properties and that pro- during the 1940s. After a long decline, the Hokkaido her-
vides the predictive capability needed for ecosystem-based ring (Clupea harengus pallasi) fishery finally collapsed in
management. the mid 1950s, shortly followed by a much more sudden

Climate Change and Small Pelagic Fish, eds. Dave Checkley, Jürgen Alheit, Yoshioki Oozeki, and Claude Roy. Published by Cambridge University
Press. © Cambridge University Press 2009.
A short scientific history of the fisheries 7

collapse of Norwegian herring (C. harengus harengus). In following years saw no substantial recovery of the ancho-
the mid 1960s yet another sardine (S. sagax ocellata) fish- veta resource, despite major reductions in fishing pressure.
ery collapsed, this time off South Africa. All of these stocks The problem could no longer be associated simply with the
appeared to withstand intense exploitation for an extended El Niño of 1972. Something had mysteriously changed in
length of time, but suddenly failed to exhibit the vigorous the ecosystem. In the early 1970s, sardines (S. sagax sagax)
productivity that characterized their pre-collapse fisher- unexpectedly appeared in abundances sufficient to support
ies. There was intense debate (e.g. Clark and Marr, 1955) an alternative fishery (see below).
whether these collapses were due to the effects of fishing, or Through the 1970s the conventional viewpoint was
whether they were unavoidable consequences of environ- strongly based on equilibrium fishing assumptions: If fish-
mental fluctuations. ing pressure could be reduced sufficiently, it should be pos-
Development of now-classical quantitative theories of sible to rehabilitate these collapsed fisheries. In view of a
fishery dynamics during the 1950s and 1960s provided con- sustained increase in abundance of California’s anchovies
vincing evidence that marine fish stocks can be depleted (E. mordax) in the 1950s following the decline of the sardine,
by intense fishing even in the absence of environmental simple ecological competition models allowed the equilib-
perturbations. The monumental treatise by Beverton and rium fishing view to be extended to a multispecies equiva-
Holt (1957) was especially influential, as it demonstrated lent whereby competition from anchovies was thought to be
the analytical power and insights that could be gained the reason for low sardine productivity. In California, fish-
from rigorous mathematical modeling of fish populations. ery managers were being urged to “intentionally overfish”
Quantitative fishery scientists developed nearly all of the anchovies to assist recovery of the sardine resource (Sette,
elements of modern fishery analysis between the mid 1950s 1969; McEvoy, 1986). A nearly identical rise in anchovies
and mid 1960s. Some landmark contributions during this (E. capensis) off South Africa during the 1960s generated
period include Ricker’s (1954) examination of the stock- similar claims of dynamics driven by inter-species compe-
recruitment relationship, Schaefer’s (1954) development tition (Stander and Le Roux, 1968). Immediately following
of the stock production model, and development of virtual the anchoveta collapse in South America, sardine abun-
Population Analysis (vPA) independently by Murphy dance increased rapidly in the 1970s, leading to widespread
(1965) and by John Gulland (1965). One of the first mod- acceptance of some form of sardine–anchovy alternation,
ern stock assessments based on vPA was Murphy’s (1966) usually described as “species replacement.” Indeed, the
analysis of the California sardine fishery. South American fishery on sardines was quickly develop-
In contrast to the problem of “growth overfishing” seen ing toward levels rivaling those of the previous anchoveta
in the North Sea where individual fish were being harvested fishery. Sardines formerly had been relatively scarce in
at too small a size, other ecosystems faced the problem Peru and Chile, but coincident with the 1970s’ increase in
of “recruitment overfishing” whereby intense fisheries apparent abundance, their range also expanded nearly 1000
remove individuals faster than they could be generated by km southward to Talcahuano, Chile, where they had never
the parental reproduction (e.g. Cushing, 1973). The notable before been seen (Serra, 1983).
small pelagic fishery collapses cited above were generally A decade after the Peruvian anchoveta collapse, Gulland
considered to be examples of recruitment overfishing. (1983) still viewed the problem in equilibrium terms, although
A Peruvian fishery for anchoveta (Engraulis ringens) recognition of the increasing abundance of Peruvian sardines
developed rapidly during the late 1950s and early 1960s, extended his concern to interactions in a multispecies system.
accelerated by the transfer of existing equipment and Gulland (1983, p. 1019) observed that these pelagic species
expertise from the collapsed sardine industry in California have been especially susceptible to collapse as the result of
(Radovich, 1981; Ueber and MacCall, 1992). The Peruvian recruitment overfishing, but also that the collapse of one spe-
fishery, which quickly became the largest in the world, cies frequently coincided with the rise of another. Notably,
was also notable as being managed “scientifically” under he says “The collapses have too often followed a period of
advice from the United Nations Food and Agriculture very heavy fishing to be due solely to chance or environmen-
Organization (FAO) and a panel of the world’s leading fish- tal effects, and also the rise of a competing species has now
ery scientists using the newly developed kit of mathemati- occurred too often to be based on chance alone …”
cal tools. It came as a shock to both the scientific world and
the global economy when the anchoveta fishery collapsed in
The doubt period
1972. As had been prophesied by Paulik (1971), the collapse
appeared to be the result of intense fishing on a resource Fréon et al. (2005) insightfully called the last quarter of the
made vulnerable by the El Niño conditions in 1972 that twentieth century “the doubt period.” Ushered in by the catas-
concentrated the fish in the nearshore region. The initial trophic collapse of the Peruvian anchoveta fishery, which
sense of shock slowly evolved into a sense of numbness, as had been the largest fishery in the world, this period saw a
8 A. D. MacCall

growing worldwide list of fishery collapses. It seemed that

small pelagic fish were especially prone to collapse. However, 30

it should be noted that in hindsight, Mullon et al. (2005)

25
recently found that collapses of small pelagics were no more

Number of publications
frequent than in other fisheries. More disturbing than the col- 20
lapses themselves was the frequent lack of recovery relative
to the former productivity of those fisheries. Both “the clas- 15

sical period” and “the doubt period” produced significant

10
advances in understanding many of the underlying patterns
and mechanisms of pelagic fish fluctuations, but remarkably 5
little progress was made toward integrating those compo-
nents into a complete theory of small pelagic fish dynamics 0
that had useful predictive power. By the end of the twentieth

1965

1968

1971

1974

1977

1980

1983

1986

1989

1992

1995

1998

2001

2004

2007
century it was apparent that small pelagic fish fluctuations
Year
presented a scientific puzzle that was far more difficult than
anyone had imagined (e.g. Chavez et al., 2003). Fig. 2.1. Number of publications containing the keyword “regime”
In contrast to the classical equilibrium fishery models, an together with “climate” and “fish” or “fisheries” in the Aquatic
alternative, non-equilibrium view was beginning to emerge Sciences and Fisheries Abstracts database. Recent years are
during the 1970s. Soutar and Isaacs (1969, 1974) developed incomplete.
a remarkable time series of prehistoric sardine and anchovy
abundances based on fish scales preserved in laminated
anerobic sediments found in a nearshore basin in southern Box 2.1. The origin of the “regime” concept
California. The 2000-year paleosedimentary record indi-
At the 1973 Symposium of the California Cooperative
cated that unfished sardine abundances have always been
Oceanic Fisheries Investigations (CalCOFI), John Isaacs
highly variable off California, with some virtual disappear-
(1976) formalized his concern that sardine–anchovy
ances (however, at the coarse resolution of ca. 0.5 million
systems may be far less predictable than our simplistic
tons) even in the absence of fishing. It was not possible to
models would suggest. Not only was this was the first
explain those prehistoric fluctuations in terms of equilib-
use of the term “regime” in its modern fishery meaning
rium models, and the new paleosedimentary evidence was
but the explanation of what he meant by the term was
eagerly taken to absolve the fishery of responsibility for the
extraordinarily clear:
disappearance of the resource: “Nor can the virtual absence
“ … there are probably a great number of possible
of the sardine from the waters off Alta California be consid-
regimes and abrupt discontinuities connecting them,
ered an unnatural circumstance” (Soutar and Isaacs 1974),
flip–flops from one regime to another … Sardines, for
Another of Soutar and Isaacs’ surprising findings was that
example, are either here or not here… There are internal,
there was no indication of anchovy–sardine alternations of
interactive episodes locked into persistence, and one
abundance in the paleosedimentary time series, despite sci-
is entirely fooled if one takes one of these short inter-
entific consensus that the two species were competitors (e.g.
vals of a decade or so and decides there is some sort of
Sette, 1969). Probably due to the strong circumstantial pat-
simple probability associated with it … organisms must
tern of anchovy–sardine alternations recently experienced
respond to more than just fluctuations around some opti-
in fisheries off California, South Africa and South America,
mum condition …. Fluctuations of populations must be
the lack of paleosedimentary evidence for sardine–anchovy
related to these very large alternations of conditions.”
alternation received little attention.
The pattern of sardine fluctuations implied by the paleosed-
imentary record could not be reconciled with the conventional
equilibrium view of an approximately constant “reference” An early development in the field of dynamical systems
state of the resource corresponding to an unfished condition that gained popularity in the 1970s was “catastrophe the-
(i.e. carrying capacity, in ecological terms). Isaacs (1976), ory” (Thom, 1993), which provided a useful explanation
expressed this concern clearly, and coined the term “regime” to of the dynamics of fishery collapses. A number of studies
describe the tendency of ecosystems to fall into prolonged states had shown that searching behavior by fishermen, espe-
and patterns that would suddenly change to a new and different cially for surface-schooling fishes, could result in a ten-
pattern (Box 2.1). The terms “regime” and “regime shift” have dency for catch-per-unit-effort (CPUE) to be insensitive
become common key words in recent climate-related fisheries to declines in underlying fish abundance (Paloheimo
and oceanographic publications (Fig. 2.1). and Dickie, 1964; Pope and Garrod, 1975; MacCall,
A short scientific history of the fisheries 9

1
Box 2.2. Catastrophe theory and fishery collapse
The classical Schaefer model assumes that abundance 0.8

Relative abundance
(as measured by catch-per-unit-effort, CPUE) declines
linearly as fishing effort increases (Fig. 2.2, thin lines). 0.6
However, experience has shown that the fishing mortal-
ity rate generated per fishing effort may increase rapidly 0.4
when abundance is low. Thus at low abundances, fisher-
men are able to locate and catch the few remaining fish, 0.2
so that a small amount of fishing effort can catch a very
large fraction of the population. Although the under- 0
lying relationship between abundance and fishing mor- 0 0.2 0.4 0.6 0.8 1
tality rate may still be described by a Schaefer model, Fishing rate
the relationship between apparent abundance (CPUE)
and nominal fishing effort (e.g., vessel–days) is severely 0.3
distorted (Fig. 2.2, thick lines). There is now a stable
upper equilibrium, and an unstable lower equilibrium.

Sustainable yield
As nominal fishing effort increases, the relationship 0.2
initially behaves like a Schaefer model, but at some
intermediate fishing rate sustainability is no longer pos-
sible, resulting in sudden collapse. Rebuilding requires 0.1
severely reducing fishing effort to where it falls on the
left side of the equilibrium line (Fig. 2, upper), where
abundance can increase. The associated rebuilding
0
catch is very low.
0 0.2 0.4 0.6 0.8 1

Fishing rate
Fig. 2.2. Effect of a population-dependent catchability coefficient
1976; Ulltang, 1976). Equivalently, a unit of nominal fish-
on fishery production curves. Thin line: CPUE is proportional
ing effort, such as a vessel–day, could generate an ever- to true abundance. Thick line: CPUE varies as the square root of
increasing fishing mortality rate as stock size becomes abundance, which is typical in fisheries for small pelagic fish.
small. The role of this mechanism in fishery collapses
and its critical importance in management of fisher-
ies for small pelagics was recognized at a 1978 ICES long last there were signs of improvement in sardines off
Symposium (Ulltang, 1980). The phenomenon has more California. The Peruvian anchoveta remained at a low
recently found to be widespread also in demersal fisheries level. In California the anchovy population reached peak
(Harley, 2002), and is largely due to the effectiveness of abundances earlier in the decade, but decades too late to
modern fish-finding technology. Fox (1974, also reported be explained by competitive release due to lack of sardines
by Gulland, 1977) incorporated this non-linearity in a (Methot, 1989). A large number of herring stocks in the
production model, and obtained a model akin to a “fold North Atlantic were in various stages of collapse, with
catastrophe” that helped explain fishery collapses and unprecedented fishing bans being imposed on some of
quantified the extreme reductions in fishing pressure them (Jakobsson, 1980; Schumacher, 1980). Fluctuations
needed to rebuild stocks even under equilibrium bio- of small pelagics had become a serious problem in world
logical dynamics (Box 2.2). fisheries. The mechanisms were more puzzling than ever.
By the end of the 1970s, fisheries on small pelagics The good news, especially from the Japanese sardine
were showing alarming fluctuations around the world. (kondo, 1980), was that small pelagic fishery collapses
Following the 1960s’ collapse of the southern Benguela might not be permanent.
fishery for sardines, a large fishery developed on the north- The optimism that the puzzle would soon be solved
ern Benguela sardine stock off Walvis Bay, but that too generated a flurry of workshops and symposia in the 1980s.
collapsed shortly afterward. Anchovies were becoming At a workshop in Lima, Peru, Bakun and Parrish (1980)
the dominant small pelagic fish in both subregions of the presented an outline of the essential elements of fishery–
Benguela system. By the late 1970s, large sardine fisher- oceanography associated with small pelagic fishes, and
ies had developed in South America and Japan, while at greatly expanded that treatment in a presentation to a 1983
10 A. D. MacCall

FAO Expert Consultation in San Jose, Costa Rica (Parrish to management. An open question is whether this can be
et al., 1983). Fréon (1983) produced one of the first regime- done without a predictive theory of the dynamics of small
like environmentally driven pelagic fish population mod- pelagic fishes on which to base management decisions.
els. Also at this meeting, an apparent worldwide synchrony Notwithstanding the repeated disappointments of the past
of sardine fluctuations was captured vividly by kawasaki few decades, the science of fisheries–oceanography again
(1983). Although the synchrony now appears less clear seems to be close to achieving this breakthrough.
than kawasaki portrayed it, in 1983 the strength and con-
trast of the worldwide pattern suggested that the under-
Acknowledgments
lying mechanism should be easily discovered. Shortly
afterward, Pauly and Tsukayama edited a comprehensive I thank Rob Crawford and Pierre Fréon for their useful
analysis of the Peruvian ecosystem, and in his concluding reviews of the manuscript. Pierre Fréon suggested reference
chapter, Pauly (1987) clearly departed from the classical to the historical periods described in Fréon et al. (2005),
equilibrium paradigm in favor of a regime-like model of which I found very useful in structuring this review.
ecosystem behavior. Combined with the oceanographic
mechanisms elucidated by Parrish, Bakun, and others, it
appeared that all of the pieces of the puzzle were now in R e f e r enc e s
Bakun, A. and Parrish. R. (1980). Environmental inputs to fishery
hand. A breakthrough seemed to be imminent, generating population models for eastern boundary current regions.
major pelagic fish symposia in Capetown, South Africa, In Workshop on the Effects of Environmental Variation
and vigo, Spain in 1986 and in Sendai, Japan in 1989. on the Survival of Larval Pelagic Fishes. IOC Workshop
Lluch-Belda et al. (1989) captured the essence of “the Rep. 28, IOC/UNESCO, Paris, pp. 67–104.
regime problem” as being fundamentally different from Beverton, R. J. H. and Holt, S. J. (1957). On the dynamics of
“the recruitment problem” that had dominated fishery exploited fish populations. HM Stationary Off., London,
science for decades. Yet the answer remained elusive. Fish. Invest., Ser. 2, vol. 19, 533 pp.
There was growing awareness that environmental shifts Chavez, F. P., Ryan, J. Lluch-Cota, S. E., and Ñiquen M. C. (2003).
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uctivity in such places as South Africa, Peru and Japan. The in the Pacific Ocean. Science 299: 217–221.
Clark, F. N. and Marr, J. C. (1955). Population dynamics of the
“new” sardine fisheries off Japan and Peru–Chile collapsed
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by the early 1990s, while South Africa experienced a long- Rep., 1 July 1953 to 31 March 1955: 11–48.
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management policy was adopted for sardines in the US portion stock. J. Fish. Res. Board Can. 30: 1965–1976.
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(1995) use of sea surface temperature as a proxy for the admit- 142–156. In Workshop on Population Dynamics of Tuna.
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from the viewpoint of evolutionary ecology. pp. 1065–1080. Ricker, W. E. (1954). Stock and recruitment. J. Fish. Res. Board,
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Neritic Fish Resources. San Jose, Costa Rica, 18–29 April lations important to the management of the commercial
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kondo, k. (1980). The recovery of the Japanese sardine – The bio- 2: 245–285.
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Mer, Rapp. P.-v. Reuns. 177: 332–354. tistics. Cons. Int. Explor. Mer, Rapp. P.-v. Reuns.
Lluch-Belda, D., Crawford, R. J. M., kawasaki, T. et al. (1989). 177: 8–22.
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the regime problem. S. Afr. J. Mar. Sci. 8: 195–205. large-scale fluctuations of sardine and anchovy popula-
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caerulea, purse seine fishery. Calif. Coop. Oceanic Fish. along the Chilean coast, pp. 255–284. In Proceedings of the
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Methot, R. D. (1989). Synthetic estimates of historical abundance Sette, O. E. (1969). A perspective of a multi-species fishery. Calif.
and mortality for northern anchovy. Amer. Fish. Soc. Coop. Oceanic Fish. Invest. Rep. 13: 81–87.
Symp. 6: 66–82. Soutar, A. and Isaacs, J. D. (1969). History of fish popula-
Mullon, C., Fréon, P., and Cury, P. (2005). The dynamics of col- tions inferred from fish scales in anaerobic sediments
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1983. FAO Fish. Rep. 291. California sardine empire. pp. 31–48. In Glantz, M. H.
Paulik, G. J. (1971). Anchovies, birds, and fishermen in the Peru ed., Climate Variability, Climate Change and Fisheries.
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(eds.) 1981, pp 35–79. Resource Management and Ulltang, Ø. (1976). Catch per unit effort in the Norwegian
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 3 Habitats
David M. Checkley, Jr., Patricia Ayon, Tim R. Baumgartner,
Miguel Bernal, Janet C. Coetzee, Robert Emmett, Renato
Guevara-Carrasco, Larry Hutchings, Leire Ibaibarriaga,
Hideaki Nakata, Yoshioki Oozeki, Benjamin Planque, Jake
Schweigert, Yorgos Stratoudakis, and Carl D. van
der Lingen

CON T E N T S Introduction
Summary Small, pelagic fish, especially anchovy and sardine, abound
Introduction in many, productive regions of the world ocean. Their habi-
Regional descriptions tats include areas with coastal and oceanic upwelling and
Synthesis freshwater influence and can be characterized by both geog-
Future climate change raphy (properties of the coast and bottom) and hydrography
Conclusions (properties of the water). The effects of climate change, be it
Acknowledgments of natural or anthropogenic origin, on populations of small,
Notes pelagic fish, are mediated by their habitats. Our objectives
References in this chapter are to describe the habitats of the major
stocks of small, pelagic fish and comment on the possible
effects of climate change on these habitats and, in turn, on
the populations. Finally, we present future challenges.
Small Pelagic Fish and Climate Change (SPACC) is a
Summary
program of International Global Ecosystem Dynamics
The habitats of populations of small, pelagic fish, espe- (GLOBEC) that uses the comparative approach (cf. Mayr,
cially anchovy and sardine, in the Benguela, California, 1982) to assess the impact of climate variation and change
Humboldt, and kuroshio-Oyashio current systems, and in on ecosystems in which small pelagic fish, particularly
the NE Atlantic, are described and discussed in regard to anchovy and sardine, play an important role. The regions
future climate change. These stocks have been the primary on which SPACC is focused (Fig. 3.1) include, in the
concern of the Small Pelagic Fish and Climate Change Pacific, the California Current (Canada, US, and Mexico),
(SPACC) program of International GLOBEC. Each of the Humboldt Current (Peru, Chile), and the kuroshio-
these regions and stocks has a unique set of climate and Oyashio Region (Japan), and, in the Atlantic, the Benguela
ocean conditions and their variability. However, they also Current (South Africa, Namibia), the Canary Current
share common characteristics. Spawning and development (Morocco, Western Sahara, Mauritania, and Senegal), and
occurs within broad ranges of temperature (12–26 °C) and the European Atlantic (Portugal, Spain, and France). Other
salinity (<30–36) and in regions of high plankton produc- regions, including the Mediterranean and Baltic Seas, the
tion, associated with either upwelling or freshwater. Often, Gulf of California, waters off Australia, korea, Taiwan,
sardine are more oceanic and anchovy more coastal, often and China, and certain open ocean regions (e.g. the western
associated with wind-driven upwelling and rivers. Sardine tropical Pacific), contain significant populations of small,
tend to make longer migrations between spawning and pelagic fish but have not been a focus of SPACC. Stocks
feeding regions than do anchovy. The habitat of most pop- of some of these other regions are treated elsewhere in this
ulations of small, pelagic fish expands when the popula- volume, but not in this chapter.
tion size is large and contracts when it is small, often into Anchovy (Engraulis) and sardine (or pilchard: Sardinops,
refugia. Climate change may affect populations of small, Sardina, and Sardinella) are the genera that have been
pelagic fish by causing poleward shifts in distribution due studied most within SPACC. Other genera receiving atten-
to warming, some of which have already occurred. Other tion have been jack, or horse, mackerel (Trachurus), true
potential effects are due to changes in winds, hydrology, mackerel (Scomber), sprat (Sprattus), herring (Clupea), and
currents, stratification, acidification, and phenology. round herring (Etrumeus). Interactions, or replacements,

Climate Change and Small Pelagic Fish, eds. Dave Checkley, Jürgen Alheit, Yoshioki Oozeki, and Claude Roy. Published by Cambridge University
Press. © Cambridge University Press 2009.
Habitats 13

75º N

60º N

45º N Northeast
Atlantic
Kuroshio California
Oyashio Current
30º N

15º N

0º

15º S
Humboldt
Current Benguela
30º S Current

45º S

105º E 120º E 135º E 150º E 165º E 180º 165º W 150º W 135º W 120º W 105º W 90º W 75º W 60º W 45º W 30º W 15º W 0º 15º E 30º E 45º E 60º E 75º E

Fig. 3.1. World map showing SPACC regions treated in this chapter.

among these taxa and anchovy and sardine are of particu- 11% of global landings (http://www.fao.org). In general,
lar interest. Genetic studies of anchovy and sardine (Grant these fish inhabit regions of high productivity, often due
and Bowen, 1998; Lecomte et al., 2004) indicate six major to nutrients supplied by wind-driven upwelling but also in
regions of speciation of these taxa: the California Current, fresh water, and low diversity, including plankton and fish.
Humboldt Current, kuroshio–Oyashio, Australia, Benguela This, combined with their planktivory, hence feeding low
Current, and the European Atlantic. These regions are, in in the food web, results in productive, single-species popu-
general, synonymous with those of SPACC, with the excep- lations ideal for exploitation. While these, like all exploited
tion of Australia. These studies show “shallow” evolution- populations, are susceptible to, and have experienced, over-
ary relationships, indicating recent expansion into current exploitation, they may be resilient, due to their fast growth
habitats. This, in turn, indicates that habitats of each taxon and young age of reproduction and thus high productivity.
may share common characteristics. Further, this may allow Climate change effects on fish populations will be under-
generalities in regard to the effects of climate change on stood only if they are distinguishable from other effects,
these taxa. especially fishing and density dependent processes. To this
Anchovy and sardine often differ from one another end, in this chapter we focus on the habitat of fish, as feasi-
in regard to their individual characteristics and habitats ble, during all stages of development: egg, larva, juvenile,
(Barange et al., 2005; cf. van der Lingen et al., 2005a). In and adult feeding and spawning. Because our informa-
general, anchovy feed on larger particles, have a smaller tion is from diverse sources worldwide, it is not uniform.
body (length, weight), and migrate less than sardine. Our goal is to assess differences and similarities using this
Anchovy are also more often associated with regions of information. We are also particularly interested in compar-
coastal upwelling or freshwater influence, while sardine ing anchovy and sardine and the roles of geography and
occur further offshore. hydrography in their responses to climate change. Here,
SPACC is unusual among research programs in that all of geography means location in Earth coordinates, e.g. lati-
the populations it studies have been and/or are exploited. In tude and longitude, and bottom depth. Hydrography refers
2004, 25% of world fish landings were small, pelagic fish, to currents and water properties, e.g. temperature, salin-
including the Peruvian achoveta (Engraulis ringens), which ity, and contained plankton. variability in the distribution,
supports the world’s largest single-species fishery, itself abundance, and size of populations of pelagic fish may be
14 D. M. Checkley, P. Ayon, T. Baumgartner et al.

better explained by hydrography than geography. Often, Northern anchovy (Engraulis mordax)
though not always, the size of populations of these taxa in The range of Engraulis mordax extends from vancouver
a region vary out of phase (Schwartzlose et al., 1999). The Island, Canada to Baja California, Mexico (Fig. 3.2b). The
cause of their variation remains unknown but may involve northern anchovy consists of one genetic stock (Smith,
both the environment, hence habitat-, and density-dependent 2005; Lecomte et al., 2004). However, it has two distinct
processes (Lluch-Belda et al., 1992; Schwartzlose et al., spawning areas (Richardson, 1981), and its range expands
1999; Jacobson et al., 2001; this volume, Chapters 5 and 12). and contracts with increases and decreases in the size of
In this chapter, we first describe the habitats for the the population (MacCall, 1990; this volume, Chapter 5).
major SPACC regions and stocks. We then synthesize these Spawning generally occurs in areas with wind-driven,
regional descriptions, highlighting similarities and dif- coastal upwelling or river runoff, with peak spawning
ferences. Finally, we briefly address the effects of past and in January–March off southern and central California
future climate change on small, pelagic fish, as mediated by (Lasker and Smith, 1977; Moser et al., 1993, 2001) and
habitat. June–August off Oregon/Washington (Richardson, 1981;
Emmett et al., 1997). Waters with anchovy spawning are
presently, in general, cold (12–16 °C), of high salinity
Regional descriptions
(33.5–33.7) (Checkley et al., 2000), although off the north-
California Current (CC) west coast, spawning appears to be related to the Columbia
The northern anchovy (Engraulis mordax) and Pacific sar- River plume (Richardson, 1981; Emmett et al., 1997), and
dine (Sardinops sagax) are the two dominant species of these areas often have abundant nutrients, resulting in abun-
small, pelagic fish off the West Coast of North America. dant diatoms and copepods, including Calanus pacificus.
Both exhibit large, multi-decadal variations in popula- During El Niño, e.g. in 1983, spawning can occur along
tion size, both in and out of phase, inferred from histori- much of the NW coast. In general, these are regions with
cal scientific and fisheries data (Schwartzlose et al., 1999; both enhanced nutrient supply and water-column stability
this volume, Chapter 9) and paleo-oceanographic studies (cf. Lasker, 1975).
(Soutar and Isaacs, 1974; Baumgartner et al., 1992; this Juveniles and adult northern anchovy are abundant
volume, Chapter 4). Data are both fisheries dependent (e.g. off California, Oregon, and Washington in spring but
landings data during periods of high and moderate popula- decline in abundance during the summer, perhaps due to
tion size) and fisheries independent (e.g. ichthyoplankton predation. Consistent with variation of its northern limit,
and adult acoustic-trawl surveys, largely independent of the abundance of the northern anchovy off Oregon and
population size). Washington exhibits significant interannual fluctuations,
and has increased notably in recent years in Puget Sound,
Physical characteristics Washington. Regular sampling off the Columbia River
The west coast of North America (Fig. 3.2a), from vancouver since 1998 (every 2 weeks at 12 stations at night; Emmett et
Island, Canada, to Baja California, Mexico, is influenced al., 2006) shows large interannual fluctuations, with peak
by the California Current, wind-driven upwelling, and, abundance in April and May and lagging ocean productiv-
to a lesser extent, runoff (Hickey, 1979, 1998; Lynn and ity (Peterson and Schwing, 2003) by several years.
Simpson, 1987, 1990). The California Current originates off
British Columbia and flows south past the US west coast to Pacific sardine (Sardinops sagax)
Baja California. It is of lower salinity (<ca. 33.2) than water Pacific sardine is presently more abundant than the northern
of the oceanic N. Pacific to the west and coastal upwelling anchovy and, consistent with past fluctuations, has a large
and the Davidson Current to the east. The latter is a pole- range, extending from Canada to Baja California (Fig. 3.2c)
ward-flowing current that is strongest and extends furthest (Parrish et al., 1989). The Pacific sardine consists of three
north, beyond Point Conception, in winter; it is subsurface subpopulations (Gulf of California, not further considered;
in summer. In spring, NW winds induce upwelling, contrib- Baja California Sur Inshore, BCSI; and Central California
uting to the geostrophically balanced California Current. Offshore, CCO; Smith 2005), although these have not been
Water upwelled is from the California Undercurrent and found to be genetically distinct (Smith, 2005, and references
typically cool (<15 °C) and high in salinity (> 33.2). Open- therein). During peak population size, the CCO subpopula-
ocean upwelling forced by wind-stress curl (Chelton et al., tion is the largest and adults occur from Baja California to
1982, Pickett and Schwing, 2006), in addition to wind-in- Canada. During low population size, the range of the Pacific
duced, coastal upwelling, has recently received attention in sardine contracts and the BCSI subpopulation dominates,
regard to sardine habitat (Rykaczewski and Checkley, 2008). with the inshore waters off Baja California perhaps being
A nearshore, equator-ward jet can develop in spring, particu- a refuge (Mais, 1974). Spawning and early development
larly off Washington and Oregon. of the CCO population occurs primarily in relatively low
Habitats 15

(a)
Vancouver
Island
British Columbia
Canada
Juan de Fuca Strait

Washington
Puget Sound
Columbia River

Oregon

United States
3

San Francisco
California
Monterey Bay
Latitude

Point Conception

San Diego

Mexico

Fig. 3.2. California Current

region. (a) Circulation.
Punta (b) Distribution of northern
Eugenia anchovy (Engraulis mordax).
Baja (c) Distribution of Pacific
California sardine (Sardinops sagax). Note
that these distributions are the
maximal ranges. As discussed
in the text, these distributions
. become smaller at lower
population size. (See also this
volume, Chapter 5)

Longitude

salinity water at the inshore edge of the California Current during El Niño (e.g., Lynn, 2003). Juvenile and adult Pacific
off southern and central California and off Baja California sardine occur off California, Oregon, Washington, and
(Parrish et al., 1989; Checkley et al., 2000). Spawning has Canada, indicating a northward migration from spawning
been noted off Oregon and Washington from 1994–1998 to juvenile nursery to adult feeding areas. Significant varia-
(R. Emmett, unpublished data). Offshore eddies have been tion in sardine production on the decadal scale is explained
hypothesized to be important regions of retention and by variation in open-ocean upwelling forced by wind-stress
growth of sardine larvae and juveniles (Logerwell and curl (Rykaczewski and Checkley, 2008).
Smith, 2001). Significant interannual variation occurs in Sardine migrate annually from spawning grounds off
the geographic extent of spawning, extending further off- southern California northward to the Pacific Northwest
shore during La Niña and being compressed shoreward and Canada and occasionally into southeast Alaska. It is
16 D. M. Checkley, P. Ayon, T. Baumgartner et al.

(b)

50

45

40

35

30

Spawning

Juveniles and adults

25

Fig. 3.2 (cont.)

–130 –128 –126 –124 –122 –120 –118 –116 –114 –112 –110 –108

generally believed that the northward migration is to spawn of migration may be limited by the rate of northward
and feed, as coastal upwelling in this area results in a ready progression of the local spring and the associated 12 °C iso-
source of phytoplankton and zooplankton for sardine. therm (Emmett et al., 2005; D. Ware, Aquatic Ecosystem
Analysis of stomach contents of sardine in Canadian waters Associates, Nanaimo, BC, Canada, unpublished data).
indicates an affinity for phytoplankton, primarily diatoms, During its annual spring and summer northward expan-
but there is a definite prevalence of copepods and the eggs sion, the adult sardine population appears to remain rela-
and later stages of euphausiids in most years (Emmett et al., tively offshore but once it reaches the area of the Columbia
2005; McFarlane et al., 2005). River and the mouth of Juan de Fuca Strait there is a ten-
The mechanism underlying the annual northward dency to move inshore. Sardine generally arrive off the
movement of sardine is not well understood but the rate coast of southwest vancouver Island by late June and are
Habitats 17

(c)

50

45

40

35

30

Spawning

Juveniles and adults

25

Fig. 3.2 (cont.)

–130 –128 –126 –124 –122 –120 –118 –116 –114 –112 –110 –108

frequently found in substantial quantities in the inlets of the Canadian waters are occasionally conducive to sardine
west coast of vancouver Island shortly thereafter, possibly spawning but in general are too cold. During the warm
due to the elevated sea surface temperatures and high phyto- years associated with intense El Niños, such as in 1997 and
plankton concentrations. McFarlane et al. (2005) found 1998, limited spawning occurred off vancouver Island but
that the northern limit of sardines in Canadian waters was the fate of the eggs and any resulting progeny is unknown.
broadly related to the sea surface temperature off the west Although the habitat for sardine becomes unfavorable
coast of vancouver Island and northward into Hecate Strait in the winter and the bulk of the adult sardine population
(53–54° N) during the months of June through August. By migrates southward again, both juvenile and adult sardine
October, as sea temperatures begin to cool, sardine begin frequently over-winter in inlets of the west coast of British
to move southward again, although 0-age sardine do not Columbia, at times (e.g. 2005) mixing with schools of
appear to migrate but stay in coastal waters. Pacific herring (Clupea pallasi).
18 D. M. Checkley, P. Ayon, T. Baumgartner et al.

Generalizations (> 25 °C, < 33.8) (zuta and Guillén, 1970; Guillén, 1983).
Analyses of both recent and past (1950–2000) spawning Northern upwelling is supplied by waters of the SECC
of the northern anchovy and Pacific sardine from Baja between 4 and 8ºS, central upwelling by the PCC, and
California to central California allow the following general- southern upwelling by the Sub-Antarctic Temperate Water,
izations. Anchovy tends to spawn in regions of wind-driven SATW (< 15 °C, < 34.7) (Morón, 2000).
coastal upwelling and river runoff, while sardine spawn in A recent analysis of time series of salinity to 60 nm off-
more oceanic water, perhaps upwelled due to wind-stress shore and by latitude (O. Morón, personal communication)
curl and Ekman pumping (Rykaczewski and Checkley, showed a preponderance of the CCW from 1960 to the start
2008). Both taxa spawn in the upper water column (Curtis of the 1970s; strong influence of SSW from the early 1970s
et al., 2007 and references therein). This results in anchovy to mid 1980s; and since, dominance of CCW. These find-
and sardine spawning in water of different characteristics ings have important implications for anchovy and sardine
and at different times. Anchovy spawn primarily January– dynamics. The oxygen minimum layer is a boundary for
March in 12–16 °C, high salinity (> 33.2) water, or in lower the vertical distribution of organisms. During El Niño, the
salinity water near river plumes. Sardine spawn primarily central coast shelf, normally hypoxic or anoxic, becomes
April–June in water 12–14 °C off California (Checkley oxygenated, due to the strong development of the SECC. A
et al., 2000; Moser et al., 2001) and 14–16 °C in May–July significant increase of macrobenthos biomass and displace-
off Oregon/Washington (Emmett et al., 2005), during ment of coastal and demersal species toward the edge of the
periods of large population size, and of lower salinity. shelf have been reported (Tarazona, 1990).
Exceptions include spawning during El Niño, when coast- Upwelling of the Equatorial Undercurrent occurs in the
ally upwelled water is not of high salinity and anchovy Galapagos. This may serve as a refuge for small, pelagic fish
spawn in lower salinity water (Checkley et al., 2000), and in of the HC during periods of low population size (M. Niquen,
periods of low sardine abundance, when this species spawns unpublished data).
later in the year (summer) and in 14–21°C, high salinity water,
primarily in inshore waters off Baja California. At any one Anchoveta (Engraulis ringens)
time, particularly during a period of low abundance of a spe- Anchoveta is widely distributed along the coast of South
cies, not all habitat that appears suitable is used for spawning America between 04º30 S and 42º30 S (Fig. 3.3b). Off
(cf. Smith, 1990; Reiss et al., 2008). Importantly, the CC the Peruvian coast, two population units are recognized:
system does not exhibit a single, normal state but, rather, the north-central stock, from northern limit to 15º S, and
variability is the norm, with conditions apparently favoring the southern stock, from 15º S to the southern limit of the
anchovy, sardine, or both at any given time, as indicated in Peruvian maritime domain (IMARPE, 1973; Pauly and
the paleo-oceanographic record (this volume, Chapter 4). Tsukayama, 1987; Csirke, 1996). Anchoveta is associated
with the CCW and sea surface temperatures of 14–22 °C,
Humboldt Current (HC) salinities of 34.9–35.1, and occurs in the upper 70 m. Under
Physical characteristics average conditions, its concentration is high near the coast
The Humboldt Current system extends along Chile, Peru, and in austral spring and summer and low, extending 100 nm
Ecuador, including the Galapagos Islands (Fig. 3.3a). The offshore, in autumn and winter. During warming events
ecosystem is characterized by intense coastal upwelling and El Niño, anchoveta is concentrated near the coast and
and high productivity that vary between years, particularly migrates southward.
with ENSO,1 and multi-decadally for the whole Pacific The northern and central areas (04º30–14º S) contain the
basin (Chavez et al., 2003) and for the coastal zone (Purca, main spawning ground. The highest egg concentration is
2005). found in the upper 30 m (Santander and de Castillo, 1973).
The main surface current flows northward and has two The spawning area is related to the influence of the CCW
branches: the Peru Current (PC) and the Peruvian Coastal with salinities between 34.9 and 35.0.
Current (PCC). Between these the Peru–Chile Undercurrent Three levels of carrying capacity for anchoveta have been
flows southward carrying equatorial waters below 100 m proposed (Csirke et al., 1996): the highest in the 1960s until
and extending 250 km offshore (zuta and Guillén, 1970; the collapse in 1972, the lowest from 1973 to 1983, and an
Morón, 2000). In addition, the Southern Extension of the intermediate level from 1984 to 1994, updated to 2001 by
Cromwell Current (SECC) flows near the coast below 50 m Ayón et al. (2004). During the 1990s, anchoveta had five
to 300 m, with high oxygen content. years (1992–96) of high abundance similar to those of the
Four types of surface water masses exist: Cold Coastal 1960s, but since then has remained at an ‘‘intermediate’’
Water CCW (14–18 ºC and 34.9–35.0), Surface Subtropical level.
Water SSW (18–27 °C, 35.1–35.7), Surface Equatorial Water Different factors affect spawning and recruitment.
SEW (> 20 °C, 33.8–34.8), and Surface Tropical Water El Niño is the most striking of these, impacting the
Habitats 19

(a) Galapagos
7
Islands
0
9
Ecuador
Guayaquil

–5
Paita
5
Pimentel
10

8 Peru
–10

Lima
1
–15

Ilo

6 2
–20
Latitude

–25

–30 –
1
–

Chile
–35

Concepcion Fig. 3.3. Humboldt Current region. (a) Circulation.

(b) Distribution of anchovy (Engraulis ringens).
(c) Distribution of sardine (Sardinops sagax). Note
–40 that these distributions are the maximal ranges. As
3 discussed in the text, these distributions become
smaller at lower population size. (See also Alheit et al.,
4
2008).
–90 –85 –80 –75 –70
Longitude

spawning process and eventually changing the main peak phytoplankton, with flagellates as the main item of the diet.
from winter–spring to summer and by lowering its inten- As larvae grow, their preference changes to zooplankton
sity (Santander and zuzunaga, 1984). Long-term changes (Muck, 1989). Studies of stomach contents of postlarval
have also been observed in the extension of spawning areas (juvenile and adult) anchoveta collected during 1953–1982
with increasing abundance. However, after the 1997–98 El show variation with latitude and distance from the coast.
Niño, the areas widened and the center of the distribution In the north-central region near the coast, it feeds more on
shifted northward compared with the 1960s. Another fac- phytoplankton but, further offshore, more on zooplankton.
tor is the effect of the fishery on spawning biomass and/or In the southern region it feeds more on zooplankton, and
recruits. this also occurs at a higher temperature (Pauly et al., 1989),
The feeding and food environment of the anchoveta has probably because of warming associated with a change of
been studied for decades. Anchovy larvae feed mainly on water mass. This spatial strategy can help to explain the
20 D. M. Checkley, P. Ayon, T. Baumgartner et al.

(b)

–5

–10

–15

–20

–25

–30

–35

Spawning

–40
Juveniles and adults

Fig. 3.3 (cont.)

–90 –85 –80 –75 –70

observed long-term variability of zooplankton volumes. In Pauly et al., 1987); demersal species like hake, though
the 1960s, zooplankton volumes were high but diminished mainly during warm periods (Sánchez et al., 1985; Muck,
with decreasing anchoveta abundance. By the end of the 1989); seabirds like cormorants, boobies and pelicans
1980s, both started to recover, but this was more marked in (Jahncke and Goya, 1998); and sea mammals (Muck and
anchoveta than in zooplankton (Ayón et al., 2004). Recent Fuentes, 1987). When sardine was abundant it preyed on
analysis suggests that, after the 1980s, anchoveta has the first life stages of anchoveta. Adult anchoveta canni-
been feeding more on zooplankton (P. Espinoza, Instituto balize their own eggs, especially when the population is
del Mar del Perú, personal communication), which could large (Santander, 1987). Pauly and Soriano (1989) consid-
explain why zooplankton abundance has not recovered to ered that during warm periods, anchoveta eggs and larvae
the levels observed in the 1960s. have a higher mortality rate because of the increase of
Anchoveta is the prey of higher trophic level species like predation by zooplankton and taxa of other trophic levels,
mackerel and jack mackerel (Muck and Sánchez, 1987; including anchoveta.
 Habitats 21

(c)

–5

–10

–15

–20

–25

–30

–35

Spawning

–40
Juveniles and adults

Fig. 3.3 (cont.)

–90 –85 –80 –75 –70

Sardine (Sardinops sagax) The increase of the sardine population started after the
Sardine has a wide distribution in the SE Pacific, includ- decline of anchoveta in the start of the 1970s. The period of
ing off Peru in SSW with temperatures of 19–22 °C high abundance coincided with the period of major influ-
and salinities of 35.0–35.3 (Santander and de Castillo, ence of SSW in the first 60 nm offshore, probably favoring
1981) (Fig. 3.3c). In general, the adult distribution is far good recruitment. By the start of the 1990s, sardine entered
offshore of the intense upwelling zone, although juveniles into a new period of low abundance (Csirke et al., 1996)
are distributed in the same areas as anchoveta. This species that coincided with less SSW near the coast.
extends its area of distribution during warm periods and El The spawning area of sardine varies greatly with dis-
Niño, as in 1982–83, when it occurred near the coast in high tance from the coast and with latitude. Between 1966
densities and in the southern region, because of the south- and 1971, spawning was poor and restricted to the north-
ward advection of SSW. Sardine occur as far south as 42° S ern areas. It expanded southward after the anchoveta
off Chile (Parrish et al., 1989). decline. Major spawning concentrations occurred in SSW
22 D. M. Checkley, P. Ayon, T. Baumgartner et al.

(Santander and Flores, 1983) near the coast after migrat- west coast, and coastal upwelling, particularly on the west
ing from the equatorial zone (Santander and zuzunaga, coast (Fig. 3.4a). The Agulhas turns eastward at the south-
1984; Arntz and Fahrbach, 1996). After the 1997–98 El ern tip of Africa, forming the Agulhas Retroflection and
Niño, sardine spawning diminished drastically and has Agulhas Return Current. The Benguela Current extends
been sparse and restricted to areas off Pimentel (P. Ayón, from the SW tip of Africa (34° S) to the Angola–Benguela
unpublished data). Front, near 16° S. The Benguela Current has a well-defined
mean flow confined mostly near the continent, and a more
Jack mackerel (Trachurus murphyi) and mackerel
variable, transient flow on its western side. The latter is
(Scomber japonicus)
dominated by large eddies, while the former includes the
Jack mackerel (Trachurus murphyi) and mackerel (Scomber
Benguela Jet off Cape Town. Upwelling is notable in iso-
japonicus, also called chub mackerel) are transboundary
lated locations off the south and west coasts, particularly
species widely distributed off Peru and Chile (Serra, 1983;
adjacent to Cape Town, south of the Orange River, between
Arcos et al., 2001 and references therein). Both species are
Luderitz and Walvis Bay, and the north coast of Namibia.
frequently caught in the same areas and associated with
Persistent, intense upwelling off Luderitz (27°S), and its
SSW (Tsukayama, 1982; Santander and zuzunaga, 1984),
associated cold temperatures and offshore transport, pre-
although other authors (Santander and Flores, 1983) con-
clude spawning by small, pelagic fish and thus form a nat-
sider that mackerel is also associated with the SEW and
ural, biogeographic boundary between the northern and
jack mackerel was probably related to the SECC with high
southern Benguela subsystems.
oxygen content. Before the 1990s, the major concentrations
off Peru were found north of 11° S, and mainly north of
Anchovy (Engraulis encrasicolus) and sardine
7° S, between depths of 50 and 150 m. However, after those
(Sardinops sagax)
years, their concentrations were restricted south of 14° S.
Small pelagic fish have been relatively well studied in
Mackerel has been reported off Chile at 45° S, but with a
the southern Benguela off South Africa. The anchovy
typical southern boundary of 25° S, while jack mackerel
(Engraulis encrasicolus) and sardine (Sardinops sagax)
has been observed at 52° S, with a large fishery at 35–38° S,
habitat in southern Africa extends from Baia dos Tigres in
off Talcuhuano (Serra, 1983).
southern Angola (14° S, 10° E), down the west coast to Cape
The main spawning area of jack mackerel off Peru is
Town, across the Agulhas Bank, and to the Natal Bight just
the frontal zone of 14–18° S (Santander and Flores, 1983),
north of Durban, a distance of approximately 5000 km, with
where upwelling CCW and SSW meet 100–150 nm off-
a notable gap in the central Benguela region in the vicinity
shore, with surface temperatures higher that 18°C and
of the Luderitz upwelling cell (Fig. 3.4b). Boundaries at the
oxygen content higher than 5 ml l−1. In this area, larvae
northern and eastern margins occur when temperatures rise
are displaced offshore by the Ekman transport. Spawning
above 22–24 °C, at the Angola–Benguela Frontal region
has also been observed in other places off the Peruvian
and on the east coast, in both cases where the continental
coast but with low concentrations of eggs. Jack mackerel
shelf narrows and warm water approaches close inshore.
occurs off Chile between the Peru border and 25° S and off
The fish habitat is restricted to the continental shelf
Talcuhuano (Serra, 1983). Spawning occurs January–May.
and only extends a short distance beyond it in a few loca-
Jack mackerel is known to migrate to spawn extensively in
tions with strong advection, such as the southern tip of the
oceanic waters off Chile, as far west as New zealand, and
Agulhas Bank. There are no known extensions into the
return to the coastal nursery and adult feeding areas, where
warm, oligotrophic ocean interior. The strong Agulhas
the fishery occurs (Arcos et al., 2001).
Current on the east coast, the jet current on the west coast,
Mackerel spawn between August and March with a
and low phytoplankton concentrations offshore on both
peak in the austral summer and, under average conditions,
coasts largely limit the habitat to the continental shelf.
off the north-central region of Peru. During El Niño,
Few epipelagic fish occur in the vicinity of the powerful
spawning increases and higher concentrations of eggs
upwelling cell at Luderitz, where cold water, high turbu-
and larvae occur (Santander and Flores, 1983), probably
lence, and offshore transport prevail.
associated with SSW. Mackerel spawn off Chile prima-
Elsewhere, the cool water coincides with enriched phyto-
rily near the border with Peru and, less so, off Talcahuano
plankton concentrations (Demarcq et al., 2007). This
(Serra, 1983).
extends far offshore near the Angola–Benguela Front, asso-
Benguela Current (BC) ciated with strong offshore displacement. The width of the
Physical characteristics zone of enriched plankton decreases at Luderitz, then wid-
The waters off southern Africa are dominated by the ens on the South African west coast as far as 33° S before
southward-flowing Agulhas Current on the east and south narrowing again. While surface concentrations of chl a
coasts, the northward flowing Benguela Current on the decline on the Agulhas Bank, there are extensions offshore
Habitats 23

(a) –16

5
Angola
–18 1. Benguela Current
4 2. Agulhas Current
3. South Atlantic Current
–20 4. Coastal Current
Namibia 5. Angola–Benguela Front
6. Benguela Jet
–22 7. Agulhas Bank
Walvis Bay
–24 1

–26
Latitude

Lüderitz
–28 South
Natal Bight
4
–30 Africa Durban

Hondeklip Bay
–32
St Helena Bay
Port Elizabeth Fig. 3.4. Benguela Current
–34 6 Cape Town region. (a) Circulation.
(b) Distribution of anchovy
2
–36 7 (Engraulis encrasicolus).
3 (c) Distribution of sardine
–38 (Sardinops sagax).
10 15 20 25 30
Longitude

associated with a subsurface ridge at 22° E and at 26° E, to the west of Cape Agulhas to predominantly to the east
where the Agulhas Current diverges from the coastline. occurred in 1996 and has persisted since (van der Lingen et
A narrow belt of cool, phytoplankton-rich water extends al., 2002; Roy et al., 2007). Sardine eggs occur around the
up the east coast in winter, with a spawning microhabitat, South African coast from Hondeklip Bay (32° S) to Durban,
consisting of a wider shelf and upwelling in the Natal Bight principally during summer off the west and/or south coasts
(Lutjeharms et al., 2000) in the extreme east. The east coast but also in winter off the east coast during the annual migra-
is the location of the famous “Sardine Run,” which occurs tion known as the sardine run (Connell, 2001) (Fig. 3.4c).
in June–July each year and comprises about 3%–13% of the Both the west and the south coasts have been the dominant
total biomass in the southern Benguela region. site of summer spawning by sardine during different peri-
Mesozooplankton concentrations are moderate to high ods, with a recent shift from the west coast over the period
throughout the Benguela upwelling system and peak on 1994–2000 to the south coast (to the east of Cape Agulhas)
the west coast near St Helena Bay (33° S) and just down- from 2001 onwards (van der Lingen et al., 2005b). Winter
stream (NW) from the Luderitz upwelling cell at 23–25° S spawning off the central Agulhas Bank may be linked to
(Hutchings et al., 1991) with declining levels in warmer a phytoplankton surface maximum in the austral autumn
water of the boundary zones. Pelagic fish therefore migrate (March to June) (Demarcq et al., 2007).
against food gradients to spawn in locations upstream of Spawning habitat for both species has been character-
the main nursery grounds. These costly migrations may ized in terms of a variety of environmental variables, both
account for the poor fish yield relative to primary produc- physical (e.g. SST, salinity, water depth, mixed layer depth
tivity in the Benguela relative to the Humboldt Current sys- and current speed) and biological (e.g., phytoplankton and
tem (Hutchings, 1992; Ware, 1992). zooplankton biomass and production) using co-inertia analy-
Anchovy eggs are found in spring and early summer pre- sis, single parameter quotient (SPQ) analysis, and temper-
dominantly over the Agulhas Bank between Cape Point and ature–salinity plots (Twatwa et al., 2005; van der Lingen,
Port Elizabeth (Fig. 3.4b), although they are reported from 2005). Those studies indicate that anchovy egg habitat is
the east coast as far north as Durban and also off the west characterized by a narrower range for many environmental
coast during years of anomalously warm water (van der variables than is sardine egg habitat, and that anchovy eggs
Lingen and Huggett, 2003). An eastward shift in anchovy are found in waters of 17–21 °C and sardine at 15–21 °C,
egg (and spawner) distributions from being predominantly with other variables being roughly similar for both species.
24 D. M. Checkley, P. Ayon, T. Baumgartner et al.

(b) –16

–18

–20

–22

–24

–26

–28

–30

–32

–34

–36

–38 Fig. 3.4 (cont.)

10 15 20 25 30

(c) –16

–18

–20

–22

–24

–26

–28

–30

–32

–34

–36

–38 Fig. 3.4 (cont.)

10 15 20 25 30
Habitats 25

Anchovy spawning was significantly related to tempera- inshore along the entire west coast, reaching a maximum
ture, salinity, phytoplankton and zooplankton biomass, but from February to May each year, but it does not appear to
not to current speed, wind speed, mixed-layer depth, and geographically restrict the habitat of pelagic fish, as they
zooplankton production. Sardine spawning was signifi- occupy the well-oxygenated and productive upper mixed
cantly related to water depth and zooplankton biomass, but layer and the pycnocline.
not to other variables. The recent shift eastwards in spawn- The geographic characterization of adult distribution in
ing habitat of sardine was accompanied by an upward shift the southern Benguela was most recently performed also by
in spawning temperature to 22–24 °C in November (sum- Barange et al. (1999). Anchovy are found over the Agulhas
mer). Minimum surface temperature thresholds for spawn- Bank off the south coast whereas adult sardine have been
ing of 13–14 °C characterize the west coast between 22° S found off both the south and west coasts during different
and 33° S, which, combined with strong offshore advection periods. There has been a noticeable eastward shift in dis-
of buoyant eggs, preclude this area as a spawning habitat. tributions of anchovy and particularly sardine over the past
However, the broad shelf on the west coast of South Africa decade (van der Lingen et al., 2005b; Fairweather et al.,
is a suitable nursery area for juveniles of both species, indi- 2006; Roy et al., 2007; Coetzee et al., 2008).
cating tolerance to both warm and cool waters at different Much less is documented on the life history stages of
life stages. pelagic fish off Namibia. There have, until recently, been
Eggs and resultant larvae of both species spawned on the few studies of the early life history stages of pelagic fish in
South African south coast are transported to the west coast the northern region (e.g. Stenevik et al., 2001). Despite the
nursery area by a shelf-edge jet current (van der Lingen massive decline in biomass of both species compared to his-
and Huggett, 2003). Anchovy larva size increases pro- torical population sizes (Griffiths et al., 2004), both sardine
gressively both alongshore (equatorward) and cross-shelf, and anchovy still spawn in localized areas in similar habi-
indicating transport at the shelf edge and shoreward move- tats, although within a much smaller range and with much
ment of larvae as they grow. The shoreward movement of lower densities than previously observed. Spawning of both
pre-recruits to the nearshore habitat against the predom- species occurs in summer and autumn towards the Angola–
inant offshore Ekman drift appears to be via active trans- Benguela frontal area at 15–20° S at 19–21 °C, and older
port through swimming and/or passive transport in surface sardine further southwards on the central Namibian shelf
waters during a relaxation of upwelling (Parada et al., at 20–23° S and during austral spring in cooler upwelled
2008), as both active and passive transport are required water of 14–17 °C. Juveniles of both species occur close
to move young fish shorewards in sufficient numbers to inshore in the central–northern Namibian shelf (18–22° S).
account for observed recruitment. Active directed swim- Low dissolved oxygen concentration influences the distri-
ming by a 20 mm larva at one body length s21 for 12 hours butions of anchovy and sardine eggs and larvae (kreiner
day21 would require 105 days to swim the 180 km from off- et al., 2009), and may impact their recruitment success
shore of the continental shelf to the nearshore region (van (Ekau and verheye, 2005). A combination of a decaying
der Lingen et al., 2006). A decline in upwelling-favorable algal blooms and accumulated oxygen debt can result in
wind stress in the austral autumn (March–May) may facili- hydrogen sulfide eruptions which result in mass mortalities,
tate this movement, and whilst vertical migration of larvae although pelagic fish are less affected than rock lobster or
to below the Ekman layer should minimize offshore trans- inshore species such as mullet (Bakun and Weeks, 2004).
port during strong southerly winds in summer months, the The collapse of the Namibian sardine population, together
modelling studies of Parada et al. (2008) did not support with the eastward shift of southern Benguela sardine to the
this hypothesis. Single-parameter quotient analysis for Agulhas Bank, has meant that there is a dearth of sardine
pre-recruits and early juveniles of 20–40 mm SL (van der in the entire cool-water upwelling regime of the Benguela
Lingen, unpublished data) indicates that sardine are found system from Cape Point to Cape Frio, despite high phyto-
in warmer waters than are anchovy, offshore on the west plankton and zooplankton levels and productivity.
coast and on the Agulhas Bank. Population changes are dramatic in the Benguela sys-
The juvenile habitat was most recently described by tem, with contrasting trends in the northern and south-
Barange et al. (1999). Recruits of both species are found ern populations (this volume, Chapter 9). In the southern
primarily off the west and southwest coasts, although some Benguela, peak annual catches of sardine (400 000 tonnes)
south coast recruitment of sardine has been observed, but occurred in 1961–2, with a vPA2-estimated biomass of
generally much less than that observed off the west coast 2 million tonnes (Butterworth, 1983). As sardine declined,
(Coetzee et al., 2008). Juveniles migrate, against a food emphasis shifted to anchovy and catch levels were main-
gradient, to the south coast, where they metamorphose and, tained at 300 000–400 000 tonnes for the next 30 years,
at the end of their first (anchovy) or second (sardine) year, but dominated by anchovy. Sardine recovered in the period
spawn. Low oxygen occurs in a bottom mixed layer close 1984–2003, peaking at approximately 4 million tonnes
26 D. M. Checkley, P. Ayon, T. Baumgartner et al.

biomass. Anchovy fluctuated through the 1990s, but good to below 1000 m with a profound impact to slope dynamics
recruitment in 2000 and 2001 led to record high popula- and regional circulation. The dominant offshore sources
tion levels of both species. In the northern Benguela, sar- of water in the NA are two eastward flowing basin-scale
dine dominated the catches, peaking at 1.3 million tonnes, currents, both transporting North Atlantic Central Water
from a vPA-estimated population biomass of 6–7 million (NACW, 8–18 °C, 35.2–36.7): the North Atlantic Current
tonnes (Butterworth, 1983). A steep decline saw a shift to (NAC) at the north of Iberia (48–53° N), with a branch flow-
target anchovy and juvenile horse mackerel and a midwater ing into the Bay of Biscay, and the Azores Current (AC) at
fishery for horse mackerel developed. Fishing effort was the south of Iberia (34–35° N), with its northerly edge affect-
directed at anchovy, perceived to be a direct competitor of ing coastal circulation off western Iberia and its southerly
sardine, but after a few years anchovy biomass and catches component feeding the Canary Current. Some exchange
decreased to low levels and horse mackerel became the between the two (NAC and AC) is enabled by the broad,
dominant planktivore in the northern Benguela. Sardine slow, generally southward-flowing Portugal Current. Cape
started improving in the early 1990s, but a combination Blanc (21° N), on northwest Africa, has NACW to the north
of a huge low oxygen event in 1994, a Benguela Niño in and South Atlantic Central Water (8–18 °C, 34.7–36.3) to
1995, and sustained warming in the northern Benguela the south (Sverdrup et al., 1960). These features are major
has continued to suppress sardine biomass in the northern contributors to a complex and variable circulation system
Benguela, in stark contrast to the southern Benguela (Boyer onto which are superimposed multi-scale seasonal varia-
and Hampton, 2001; Boyer et al., 2001). There was some tions in atmospheric forcing, heating, and input of buoyancy
speculation that sardine moved into the southern Benguela through river discharges (e.g. Hernandez-Leon et al., 2007
following poor environmental conditions in the north, but and references therein; Relvas et al., 2007).
no fish were detected at intermediate localities during the Given that sardine and anchovy in the NA are almost
past decade. Ironically, some fish were caught in southern exclusively constrained within the continental shelf (with
Angola in Namibian purse seines in 1994 and 1995, indicat- the bulk of both species in the Iberian Peninsula being
ing a portion of the stock was still present in the northern found at the inner shelf and only juvenile anchovy in the
portion of the Angola–Benguela frontal region, despite the Bay of Biscay having a clearly oceanic phase), shelf area
warm water. Most of the fish were shifted southwards sev- and coastal circulation are important physical character-
eral degrees of latitude, making them more available to the istics of their habitat. Shelf width is generally narrow off
purse-seine fleet based at Walvis Bay (Boyer et al., 2001). the Iberian Peninsula but becomes progressively wider at
Speculation about the role of large carnivorous jellyfish in the French coast. Off western Iberia, the Iberian Poleward
predation of fish eggs and larvae continues, but no histor- Current (IPC), subsurface and density driven, is a domi-
ical time series of jellyfish abundance exists. Alternatively, nant feature of mesoscale circulation outside the summer
predation by horse mackerel on sardine eggs and larvae and upwelling season, flowing northwards along the shelf edge
enhanced mortality of adult sardine from other predators, with warmer, less saline and oligotrophic water (Peliz
such as seals, may be keeping sardine repressed, when it is et al., 2005). Outside the season of upwelling, the IPC has
limited in its range, in addition to the warm water effects of been shown to interact with the Ekman layer, enriched by
diminished plankton on the nursery grounds. Fishing pres- river runoff off northern Portugal, creating a barrier to off-
sure has been severely limited in Namibia, yet despite these shore advection of eggs and larvae (Santos et al., 2004).
low levels of effort, fishing mortality may still be a signifi- During the upwelling season (April–September), the sur-
cant part of the total mortality of sardine, which has still face signature of the IPC is lost but there are recent indica-
not recovered. tions that it may persist as a subsurface poleward current
(Relvas et al., 2007). Off northern Spain, the shelf is nar-
Northeast Atlantic (NA) row and circulation controlled by local features, such as
Physical characteristics small river plumes, local wind-induced upwelling, and
The Northeast Atlantic (European Atlantic and Canary capes, bays, and deep canyons. The main hydrographic
Current) is a more complex oceanographic region than feature on the shelf is the variable extension of the IPC
other major eastern boundary systems, mainly due to the off northern Spain, creating fronts parallel to the coast,
greater irregularity of the European and northwest African reducing cross-shelf fluxes, and fronts perpendicular to the
coastline and bathymetry (Fig. 3.5a). The largely meridi- coast as the IPC advances eastwards off the north Iberian
onal orientation of the coast is interrupted by significant coast (González-Quirós et al., 2004; Llope et al., 2006).
zonal stretches in the Bay of Biscay and the Gulf of Cadiz. Off France, the shelf hydrography is predominantly under
Also, the Straits of Gibraltar form a salient topographic fea- the influence of river runoff from the Loire and Gironde
ture where dense Mediterranean water enters from a shal- but also from the Adour, which flows in front of the Cap
low sill (ca. 300 m) in the Gulf of Cadiz and rapidly sinks Breton Canyon, an important area for anchovy and sardine
Habitats 27

(a)
Ireland
52 England
1. North Atlantic current
2. Portugal current
50 3. Iberian Poleward current English Channel
4. Azores current
5. Mediterranean outflow

48 Brittany

Loire River

1 France
46 Bay of Biscay
Gironde River

44
Adour River
Latitude

Galicia Cantabria

42
Minho River
2 Douro River
3
40 Spain
Portugal

n
nea Fig. 3.5. Northeast Atlantic region.
38 rra
Guadalquivir River d ite ea (a) Circulation. (b) Distribution of
M e S anchovy (Engraulis encrasicolus).
(c) Distribution of sardine (Sardina
Gibraltar Straits
36 pilchardus). Note that these
Gulf of 5
distributions are the maximal
Cadiz
Algeria ranges. As discussed in the text,
4 Morocco these distributions become smaller
34 at lower population size.
–10 –5 0
Longitude

spawning. Wind-driven upwelling partially controls pri- anchovy and sardine in the Bay of Biscay (koutsikopoulos
mary production and offshore transport along the coast and Le Cann, 1996).
north of the Adour river in spring. The IPC, which flows
in winter along the northern coast of Spain, turns counter- Bay of Biscay anchovy (Engraulis encrasicolus)
clockwise in the south-western part of the Bay of Biscay The main spawning areas of the Bay of Biscay anchovy
and flows northward (Pingree and Le Cann, 1990). At the are the Gironde and Adour river plumes, the smaller but
shelf break, large amplitude internal waves can result in abundant Cantabrian river plumes, shelf edge fronts,
the vertical pumping of sub-pycnocline water, which can and oceanic eddies (Fig. 3.5b) (Motos et al., 1996, 2004;
reach the surface. These colder and productive waters can ICES 2004; Sagarminaga et al., 2004; Bellier et al., 2007;
be directly observed via satellite, for they generate fron- Ibaibarriaga et al., 2007). All these are recurrent features
tal structures at the surface (Bardey et al., 1999). Off the where the potential for high biological production exists
shelf, hydrography is characterized by intense mesoscale (valencia et al., 2004). Spawning starts at low rates in the
activity, with cyclonic and anticyclonic eddies (Pingree southeast corner of the Bay of Biscay and extends to most of
and Le Cann, 1992; van Aken, 2002). This ensemble of the southeast Bay of Biscay, with two consistent centers: the
oceanic features results in a mosaic of potential habitats for coastal region in front of the Gironde estuary and the shelf,
28 D. M. Checkley, P. Ayon, T. Baumgartner et al.

(b)

52

50

48

46

44

42

Spawning

40

Juveniles and adults

38

36

34 Fig. 3.5 (cont.)

–10 –5 0

shelf break and oceanic regions in the southernmost Bay. surface waters, and extends to August with a peak in May
In June, the coastal and oceanic spawning regions appear and June, when the maximum rate of warming and the
well separated. During the summer, spawning is scattered onset of stratification occur (Motos et al., 1996).
all along the shelf and close to the shelf break in northern Irigoien et al. (2005) characterized the environmental
areas. Moreover, some authors have suggested that coastal and hydrographic conditions of the realized spawning habi-
and oceanic regions are used by different components of tat of anchovy using single quotient analysis and bivariate
the anchovy population. One-year-old anchovy spawn in plots. The main variables used for those analyses were sea
coastal areas, whereas two- or more year old individuals are surface temperature (SST) and sea surface salinity (SSS).
in oceanic areas close to or beyond the shelf (Massé, 1996; Anchovy eggs are present in warm waters (15–19 °C) with
Motos et al., 1996; Uriarte et al., 1996; vaz and Petitgas, low salinity (< 35). Instead of considering the absolute val-
2002). Macroscopic maturity studies conducted by Lucio ues of SST and SSS, the anomalies of SST and SSS indi-
and Uriarte (1990) showed that smallest anchovy reach cate a preference for a combination of both variables with
maturity slightly later than bigger individuals, consistent respect to the average situation: either warmer waters with
with younger fish spawning in coastal areas and slightly lower salinities or colder water with higher salinities. These
later than older fish at the shelf break and oceanic areas. two situations may represent the two main spawning sites:
The spawning season of the Bay of Biscay anchovy pop- the Gironde river plume in the north and the shelf break
ulation begins in mid March, triggered by the warming of and oceanic regions in the south, respectively. Ibaibarriaga
Habitats 29

(c)

52

50

48

46

44

42 Spawning

Juveniles and/or adults

40

Seasonal movement

38 Ontogenetic movement

36

34 Fig. 3.5 (cont.)

–10 –5 0

et al. (2005) use generalized additive models (GAMs), distribution changes depending on the overall level of the
including a bivariate smoothing of SST and SSS, to model population. In years with high adult abundances, eggs cover
the realized egg production in space. Planque et al. (2007) most of the sampling area, going well beyond the habitat
go a step further and uses GAMs on presence/absence of predicted from hydrological conditions, whereas in years
CUFES (Continuous Underway Fish Egg Sampler; Checkley with low adult abundance eggs are found in discrete aggre-
et al., 1997) egg abundance to predict the anchovy poten- gations restricted to the more favorable sites. Uriarte et al.
tial spawning habitat as a function of environmental vari- (1996) and Somarakis et al. (2004) show a linear relation-
ables derived from hydrological model simulations. The ship between the positive area and the total spawning bio-
best predictor was bottom temperature, followed by surface mass for anchovy. Similar relationships have been observed
temperature and mixed-layer depth. Surface and bottom for anchovy and sardine in the CC (Reiss et al., 2008).
salinity were not significant. Even if potential habitat can After spawning, anchovy larvae first appear in April and
be characterized in terms of environmental and hydro- are generally present until August. In June, young larvae are
graphic variables, its relationship to realized and suc- found in the middle French shelf, whereas older larvae are
cessful habitats will depend on additional factors, such as found in the southeastern area, on the Cantabrian shelf, and
the population abundance, and the age structure and the in oceanic waters. This age gradient could be due to advec-
environmental and hydrographic conditions after spawn- tion, due to NE winds, preferential areas, or their combination
ing. For instance, it is well known that the anchovy spatial (Cotano et al., 2008; Irigoien et al., 2008).
30 D. M. Checkley, P. Ayon, T. Baumgartner et al.

Larvae metamorphose into juveniles at approximately project SARDYN (SARdine DYNamics and stock struc-
30–40 days of age and these can be found from July to ture in the northeast Atlantic, http://ipimar-iniap.ipimar.pt/
November. Until 1998, information on the distribution of sardyn) show the existence of five genetically distinct units:
juvenile anchovy was obtained only from the fishermen the first three are related to isolated islands (Azores and
that use them as live bait for tuna fishing in summer and Madeira) and the Mediterranean Sea, while the entire sar-
early autumn. However, since the pilot surveys conducted dine distribution area along the Atlantic coast can only be
in 1998 and 1999 (Uriarte et al., 2001), regular autumn separated in two genetically distinct units (kasapidis et al.,
surveys targeting anchovy juveniles have taken place 2004), with the limit somewhere around the Bay of Agadir,
(ICES, 2005). Early juveniles are found mainly offshore, Morocco (30.3° N, 9.6° W). Within European waters, where
beyond the Cantabrian and French shelves, whereas older more data on sardine population dynamics and habitat occu-
juveniles are found on the shelf and near the Gironde. The pation are available, the species is mainly found around the
lack of a significant difference in larva growth between Iberian Peninsula and the Armorican (NW France) shelf
areas (Cotano et al., 2008; Irigoien et al., 2008) is consist- and up to Brittany and the western English Channel.
ent with the hypothesis of Uriarte et al. (2001) that larvae The population dynamics and habitat of the NA sardine
are advected off the shelf and juveniles return to coastal are complex. A gradient in some genetic and biological
zones to overwinter. Data from the commercial fishery characteristics along this wide area (Laurent et al., 2006;
(Uriarte et al., 1996 and references therein) support the idea Silva et al., 2006; Stratoudakis et al., 2007) suggests a
that in October and November juveniles can be found all limited degree of mixing between distant units, although
along the Cantabrian and French coasts. In addition, the specific oceanographic features that could act as barriers
hydrological conditions of the Bay of Biscay in autumn are to sardine gene flow or specific permanent oceanographic
characterized by downwelling, high turbulence and vertical regimes that could lead to different coastal habitats have
mixing which, when combined with the eastern drift, may not been identified (Peliz et al., 2005; Santos et al., 2005;
facilitate homing during migration of the juveniles. The Mason et al., 2006). Oceanographic conditions along the
juveniles moving towards the coast for the winter would NA coast form a mosaic of small and mesoscale hetero-
comprise the new recruits to the population that would geneous habitats, but with similar large-scale properties,
spawn the next spring. and create a wide distribution of suitable habitats for sar-
Anchovy occur elsewhere than the Bay of Biscay in the dine in terms of temperature (Coombs et al., 2006), food
NA. There are populations in the Gulf of Cádiz. Along availability (Smyth et al., 2005), and potential spawning
the Spanish Cantabrian coast, to Galicia and Portugal, are grounds (Stratoudakis et al., 2004; Bernal et al., 2007;
areas where anchovy appear irregularly. In recent years, an Planque et al., 2007).
increase of anchovy, together with other species with more Sardine distribution along the NA coast is nearly contin-
southern affinities, like sardine and red mullet (Mullus sur- uous from the Strait of Gibraltar to the English Channel
meletus), has been detected in survey trawling in the North (Fig. 3.5c). However, life history characteristics (such as
Sea (Beare et al., 2004a,b). Anchovy has been present in longevity, maximum age, length at maturity, growth, dura-
the North Sea up to the east coast of Scotland and the Baltic tion of spawning, and recruitment strength) differ between
in the past (Calderwood, 1892; Cunningham, 1890, 1895, regions. The spatial distribution of young and old individu-
1896), with spawning and supporting fisheries on the Dutch als is different, with old fish being observed more offshore
coast (Cunningham, 1896). The recently detected increase over the continental shelf and young fish more inshore.
(Beare et al., 2004a,b) is associated with the regional Spatial fidelity of young fish to recruitment hotspots has
increase in sea temperatures hypothesized to be associated been observed off northern Portugal and in the Gulf of
with climate change. Cadiz at depths < 30 m during the summer months, while,
for adult populations, pronounced local variations have been
European Atlantic sardine (Sardina pilchardus) reported. In both cases, the physical and/or biological con-
Sardine is widely and continuously distributed along the ditions which could promote recruitment hotspots or vari-
eastern Atlantic shelf from Mauritania to the English ability in the adult population distribution are still unclear
Channel (Parrish et al., 1989), with occasional occurrences (ICES, 2006). Spawning habitats also show some perma-
along Senegal in the south (Fréon et al., 1979) and off the nent features, with spawning confined to the shelf and to
coast of Scotland in the north (Beare et al., 2004a) (Fig. 3.5c). temperatures of 12–17 °C, but with variation along the time
Sardine is also found in all oceanic eastern Atlantic islands, series that is not clearly related to environmental variables
including the Azores, Madeira and the Canary Islands, as or to the stock size (Bernal et al., 2007). Bathymetric con-
well as within most of the Mediterranean coastal habitat, straints and some unknown environmental variables allow
with the exception of the southwest corner. Within this the separation of the spawning habitat into four geographic
broad distribution, recent results from the European Union nuclei, located in south Iberia, west Iberia, the Cantabrian
Exploring the Variety of Random
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