Aquaculture and Behavior HHuunnttiinnggffoorrdd__ffffiirrss..iinndddd ii 1111//99//22001111 1122::2200::3366 PPMM Aquaculture and Behavior Edited by Felicity Huntingford Emeritus Professor of Functional Ecology, College of Medicine, Veterinary Medicine and Life Sciences, University of Glasgow, UK Malcolm Jobling Professor of Aquaculture, BFE, University of Tromsø, Norway Sunil Kadri Director of OptoSwim Technologies, Europharma Scotland & AQ1 Systems and Honorary Research Fellow, University of Glasgow, UK A John Wiley & Sons, Ltd., Publication HHuunnttiinnggffoorrdd__ffffiirrss..iinndddd iiiiii 1111//99//22001111 1122::2200::3366 PPMM This edition first published 2012 © 2012 by Blackwell Publishing Ltd. Blackwell Publishing was acquired by John Wiley & Sons in February 2007. Blackwell’s publishing program has been merged with Wiley’s global Scientific, Technical and Medical business to form Wiley-Blackwell. Registered Office John Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK Editorial Offices 9600 Garsington Road, Oxford, OX4 2DQ, UK The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK 2121 State Avenue, Ames, Iowa 50014-8300, USA For details of our global editorial offices, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell. The right of the authors to be identified as the authors of this work has been asserted in accordance with the UK Copyright, Designs and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. Library of Congress Cataloging-in-Publication Data Aquaculture and behavior / edited by Felicity Huntingford, Malcolm Jobling, Sunil Kadri. p. cm. Includes bibliographical references and index. ISBN-13: 978-1-4051-3089-9 (pbk. : alk. paper) ISBN-10: 1-4051-3089-X 1. Fishes–Behavior. 2. Shellfish–Behavior. 3. Aquaculture. I. Huntingford, Felicity. II. Jobling, Malcolm. III. Kadri, Sunil. QL639.3.A68 2012 639.801′5915–dc23 2011024818 A catalogue record for this book is available from the British Library. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. Set in 9.5/12pt Times by SPi Publisher Services, Pondicherry, India 1 2012 HHuunnttiinnggffoorrdd__ffffiirrss..iinndddd iivv 1111//99//22001111 1122::2200::3366 PPMM Contents Contributors xiii Preface xiv Foreword by V.O. Crampton xvi 1 Introduction: Aquaculture and Behaviour 1 Felicity Huntingford, Sunil Kadri and Malcolm Jobling 1.1 Why behaviour and aquaculture? 1 1.2 About aquaculture 2 1.2.1 What aquaculture is 2 1.2.2 Why finfish are cultured 2 1.2.3 Which finfish are cultured 3 1.2.4 Kinds of culture systems 5 1.3 Introducing the spotlight species 7 1.3.1 Fish farmed for the table 7 1.3.2 Fish farmed for supplementation programmes or conservation 10 1.3.3 Fish farmed as ornamentals and for research 11 1.4 About behaviour 14 1.4.1 What behaviour is and why biologists are interested in it 14 1.4.2 Some basic behavioural biology 14 1.4.3 How complex is fish behaviour? 19 1.5 Fish welfare 20 1.5.1 Definitions of welfare 20 1.5.2 Identifying and measuring welfare 20 1.5.3 Talking a common welfare language 24 1.6 Domestication, captive rearing and behaviour 24 1.6.1 Domestication and captive rearing 24 1.6.2 Selective breeding 25 1.6.3 Are cultured fish domesticated animals? 25 1.6.4 Behavioural responses to domestication and selective breeding 26 1.6.5 Captive rearing and fish behaviour 26 1.7 Criteria for effective and sustainable fish culture 27 1.7.1 Production criteria 27 1.7.2 Environmental criteria 27 1.7.3 Welfare criteria 29 1.7.4 Behaviour and effective, sustainable aquaculture 31 1.8 Structure and content of this book 32 v HHuunnttiinnggffoorrdd__ffttoocc..iinndddd vv 1111//99//22001111 1122::2200::1111 PPMM vi Contents 2 Fish in Aquaculture Environments 36 Malcolm Jobling 2.1 Introduction 36 2.1.1 Fish and their behaviour 37 2.2 Locomotion and swimming ability 37 2.2.1 Body form 37 2.2.2 Swimming muscles 39 2.3 Sensing environmental stimuli 39 2.3.1 Sensory cues in the aquatic environment 39 2.3.2 Vision 39 2.3.3 Mechanosensory systems 42 2.3.4 Thermoreception 44 2.3.5 Electroreception 44 2.3.6 Chemoreception 45 2.4 Internal communication systems 47 2.4.1 Role of the neural and endocrine systems 47 2.4.2 The nervous system 47 2.4.3 The endocrine system 49 2.4.4 Cross-talk between the nervous and endocrine system 51 2.5 Coping with adverse conditions 52 2.5.1 Unpredictable environments 52 2.5.2 The stress response 53 2.6 Contrasts in life history patterns and reproductive biology 55 2.6.1 Reproductive options 55 2.6.2 Rates of development 56 2.6.3 Developmental contrasts in farmed species 57 2.7 Life history programming 58 2.7.1 Genotype–environmental interactions 58 2.7.2 Maternal contributions 58 2.7.3 Environmental factors and the development of motor systems in fish 60 2.7.4 Long-term consequences of early developmental events 60 2.8 Synopsis 61 3 Tools for Studying the Behaviour of Farmed Fish 65 Marie Laure Bégout, Sunil Kadri, Felicity Huntingford and Børge Damsgård 3.1 Introduction 65 3.2 Describing and measuring behaviour 66 3.3 What we need to know about the behaviour of farmed fish 67 3.4 Indirect reconstruction of the behaviour of cultured fish 67 3.4.1 Reconstructing fish diets 67 3.4.2 Reconstructing interactions with predators and rivals 68 3.4.3 Indirect assessment of stress 69 3.5 Methods of marking and tagging fish 69 3.5.1 External marks and tags 69 3.5.2 Internal tags 70 3.5.3 Internal tags that are visible externally 71 3.6 Direct behavioural observation via video monitoring 71 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd vvii 1111//99//22001111 1122::2200::1111 PPMM Contents vii 3.6.1 Video technology 71 3.6.2 Limitations 71 3.6.3 Preparation before sampling 72 3.6.4 Sampling 72 3.6.5 Analysis 72 3.6.6 An example of the use of video analysis to study the behaviour of PIT tagged fish 73 3.7 Direct behavioural monitoring using electronic tags 74 3.7.1 Electronic tagging 74 3.7.2 Types of electronic tag 75 3.7.3 Scanning stations 76 3.7.4 Examples of the use of electronic tags to study the behaviour of farmed fish 77 3.8 Direct behavioural monitoring using echo integration 77 3.8.1 Echo integration 78 3.8.2 Examples of the use of echo integration to monitor the behaviour of farmed fish 78 3.9 Measuring feeding behaviour in farmed fish 78 3.9.1 X-ray detection of feed intake 78 3.9.2 Self-feeding systems for controlling and monitoring feed delivery 78 3.9.3 Examples of the use of self-feeding on-demand systems to monitor feeding in farmed fish 80 3.9.4 Feedback systems for controlling and monitoring feed delivery 81 3.9.5 Examples of the use of interactive feedback systems to monitor feeding in farmed fish 82 3.10 Synopsis 82 4 Movement and Orientation 87 Felicity Huntingford, William Hunter and Victoria Braithwaite 4.1 Introduction 87 4.1.1 Space use in wild fish 88 4.2 Mechanisms 89 4.2.1 Spatially informative cues in the aquatic environment 89 4.2.2 How fish use spatial information 91 4.2.3 Effects of hormones on migration 92 4.2.4 Summary of the causes of space use and orientation in fish 93 4.3 Development 93 4.3.1 Ontogenetic changes in movement patterns 93 4.3.2 Inherited differences in space use 94 4.3.3 Effects of experience on space use and migration 95 4.3.4 Summary of the development of space use and orientation in fish 96 4.4 Functions 96 4.4.1 Benefits of adopting particular space use patterns 96 4.4.2 The costs of adopting particular space use patterns 97 4.4.3 Integrating costs and benefits 98 4.4.4 Summary of the functions of space use in fish 100 4.5 Implications for aquaculture 100 4.5.1 How fish use space in culture system 100 4.5.2 Problems during production arising from the ways in which fish use space 101 4.5.3 Space use problems when cultivating fish for purposes other than food 106 4.5.4 Solving problems in aquaculture arising from the biology of space use in fishes 107 4.5.5 Improving the effectiveness of general husbandry practices 109 4.6 Synopsis 112 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd vviiii 1111//99//22001111 1122::2200::1122 PPMM viii Contents 5 Feeding Biology and Foraging 121 Malcolm Jobling, Anders Alanärä, Sunil Kadri and Felicity Huntingford 5.1 Introduction to the feeding biology of fishes 121 5.2 Foraging strategies of wild fish 122 5.2.1 What fish eat 122 5.2.2 How fish acquire food 123 5.2.3 Variability in foraging within species 123 5.3 Mechanisms 124 5.3.1 The sensory cues that fish use to locate food 124 5.3.2 The structures that fish use to gather food 126 5.3.3 Mechanisms for capture and ingestion of food 128 5.3.4 Summary of foraging mechanisms in fish 128 5.4 Development 129 5.4.1 Ontogeny of foraging 129 5.4.2 Inherited differences in foraging methods 130 5.4.3 Experience and foraging methods 131 5.4.4 Summary of the development of foraging patterns in fish 132 5.5 Functions 132 5.5.1 Benefits 132 5.5.2 Costs 132 5.5.3 Trading costs against benefits 133 5.5.4 Summary of functional aspects of foraging strategy 134 5.6 Implications for aquaculture 134 5.6.1 How cultured fish are fed 134 5.6.2 Problems during production arising from natural foraging patterns 137 5.6.3 Effects of domestication and captive rearing 139 5.6.4 Solving problems arising from the natural feeding biology of cultured fish 140 5.6.5 Mitigating the effects of domestication and captive rearing 143 5.7 Synopsis 143 6 Nutrition and Diet Choice 150 David Raubenheimer, Steve Simpson, Javier Sánchez-Vázquez, Felicity Huntingford, Sunil Kadri and Malcolm Jobling 6.1 Introduction to what fish eat 150 6.1.1 What fish need from the foods they eat 151 6.1.2 What fish choose to eat 152 6.2 Mechanisms 152 6.2.1 Mechanisms for selective foraging 152 6.2.2 Sensory inputs to diet choice 153 6.2.3 Post-ingestive signals and diet choice 155 6.2.4 Modulation of diet choice 156 6.2.5 Overview of the mechanisms controlling diet choice in fish 156 6.3 Development 157 6.3.1 Ontogeny of diet choice 157 6.3.2 Inherited differences in diet choice 159 6.3.3 Experience and diet choice 160 6.3.4 Summary of the development of diet choice 161 6.4 Functions 161 6.4.1 The behavioural ecology of energy-based diet choice 161 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd vviiiiii 1111//99//22001111 1122::2200::1122 PPMM Contents ix 6.4.2 The nutritional ecology of diet choice 163 6.4.3 Summary of functional approaches to diet choice 166 6.5 Implications for aquaculture 166 6.5.1 The kinds of diet that cultured fish receive 166 6.5.2 Problems arising from the nutritional needs of cultured fish 169 6.5.3 Problems arising from natural dietary choices in cultured fish 169 6.5.4 Problems arising from domestication and captive rearing 171 6.5.5 Solutions to nutritional and behavioural problems relating to diet choice in cultured fish 171 6.5.6 Using nutritional ecology to solve problems in aquaculture 174 6.6 Synopsis 176 7 Appetite and Feed Intake 183 Malcolm Jobling, Anders Alanärä, Chris Noble, Javier Sánchez-Vázquez, Sunil Kadri and Felicity Huntingford 7.1 Introduction 183 7.1.1 Irregular changes in appetite 184 7.1.2 Regular changes in appetite: feeding rhythms 185 7.1.3 Feeding in relation to life history events 187 7.1.4 Feeding by diseased fish 188 7.2 Mechanisms 189 7.2.1 Mechanisms underlying meal-based changes in appetite 189 7.2.2 Mechanisms that control circadian rhythms 192 7.2.3 Mechanisms underlying circannual changes in appetite 194 7.2.4 Mechanisms underlying appetite changes in relation to life history events 194 7.2.5 Summary of the mechanisms underlying appetite changes in fish 195 7.3 Development 195 7.3.1 Ontogeny of appetite patterns 196 7.3.2 Genetic effects on appetite 197 7.3.3 Effects of experience on appetite 197 7.3.4 Summary of the development of appetite patterns 198 7.4 Functions 198 7.4.1 Costs and benefits of feeding at a particular rate 198 7.4.2 Costs and benefits of feeding at a particular time 199 7.4.3 Summary of the costs and benefits of appetite patterns 200 7.5 Implications for aquaculture 200 7.5.1 Patterns of feed delivery in fish culture 200 7.5.2 Problems for fish culture arising from natural appetite variation in fish 202 7.5.3 The effects of under-feeding 202 7.5.4 The effects of over-feeding 204 7.5.5 Failure to match feed delivery to natural appetite patterns 204 7.5.6 Solutions to problems for fish culture arising from natural appetite variation in fish 206 7.5.7 Domestication and captive rearing 208 7.6 Synopsis 209 8 Avoiding Predators 220 Felicity Huntingford, Susan Coyle and William Hunter 8.1 Introduction 220 8.1.1 How fish avoid being eaten by predators 220 8.1.2 Individual variation in risk taking 223 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd iixx 1111//99//22001111 1122::2200::1122 PPMM x Contents 8.2 Mechanisms 224 8.2.1 External stimuli 224 8.2.2 The internal dynamics of fish schools 224 8.2.3 Some internal factors that control and mediate antipredator behaviour 224 8.2.4 Summary of the mechanisms that control predator avoidance in fish 225 8.3 Development 225 8.3.1 The ontogeny of predator avoidance 226 8.3.2 Genetic influences on antipredator behaviour in fish 227 8.3.3 Environmental effects 228 8.3.4 Summary of the development of predator avoidance 229 8.4 Functions 229 8.4.1 Benefits of antipredator behaviour 229 8.4.2 Costs of antipredator behaviour 230 8.4.3 Integrating costs and benefits 231 8.4.4 Summary of the functions of antipredator behaviour 231 8.5 Implications for aquaculture 232 8.5.1 The incidence of antipredator behaviour in culture systems 232 8.5.2 Adverse effects of antipredator behaviour in culture systems 233 8.5.3 Effects of domestication and captive rearing 234 8.5.4 Solutions to the problems arising from antipredator behaviour in fish culture 236 8.5.5 Using predators and antipredator behaviour in fish culture 237 8.5.6 Mitigating the effects of domestication and captive rearing 238 8.6 Synopsis 240 9 Fighting and Aggression 248 Børge Damsgård and Felicity Huntingford 9.1 Introduction 248 9.1.1 What aggression is 248 9.1.2 Aggression in the lives of fish 249 9.1.3 Territoriality and dominance 249 9.1.4 Individual variation in aggressiveness 250 9.2 Mechanisms 251 9.2.1 Stimuli from potential opponents 251 9.2.2 Effects of environmental factors 252 9.2.3 Internal factors 252 9.2.4 Effects of aggression on the neuroendocrine system 254 9.2.5 Summary of the mechanisms of aggression in fish 255 9.3 Development 256 9.3.1 Ontogeny of aggression 256 9.3.2 Genes and aggression 257 9.3.3 Environmental effects 258 9.3.4 Summary of the development of aggression 260 9.4 Functions 260 9.4.1 Benefits of winning fights 260 9.4.2 Costs of fighting 260 9.4.3 Integrating benefits and costs 261 9.4.4 Summary of the functions of aggression 263 9.5 Implications for aquaculture 263 9.5.1 The incidence of aggression in culture systems 264 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd xx 1111//99//22001111 1122::2200::1122 PPMM Contents xi 9.5.2 Problematic consequences of aggression in aquaculture 265 9.5.3 Effects of domestication and captive rearing on aggressive behaviour in cultured fish 268 9.5.4 Solutions: controlling aggression during fish culture 270 9.5.5 Solutions: mitigating the effects of domestication and captive rearing 277 9.6 Synopsis 277 10 Reproductive Behaviour 286 Ian A. Fleming and Felicity Huntingford 10.1 Introduction 286 10.1.1 The reproductive biology of wild fish 287 10.1.2 The reproductive behaviour of wild fish 288 10.2 Mechanisms 291 10.2.1 The control of maturation in fish 291 10.2.2 The control of reproductive behaviour: external stimuli 292 10.2.3 The control of reproductive behaviour: neuroendocrine processes 293 10.2.4 Summary of the mechanisms that control the reproductive behaviour of fish 294 10.3 Development 295 10.3.1 Ontogenetic process 295 10.3.2 Genetic effects 295 10.3.3 Environmental effects 296 10.3.4 Summary of the development of reproductive behaviour in fish 297 10.4 Functions 297 10.4.1 Natural selection, sexual selection and reproduction 297 10.4.2 Differential selection on males and females 297 10.4.3 Functional aspects of the timing of life history events 298 10.4.4 Functional aspects of courtship 299 10.4.5 Functional aspects of parental care 301 10.4.6 Summary of the functions of reproductive behaviour in fish 301 10.5 Implications for aquaculture 302 10.5.1 Management of reproduction in cultured fish 302 10.5.2 Problems in production arising from the behavioural biology of fish reproduction 305 10.5.3 Problems arising from domestication and captive rearing 308 10.6 Solutions 310 10.6.1 Research into the natural breeding behaviour of cultured and candidate species 311 10.6.2 Providing the right physical environment for spawning 311 10.6.3 Providing the right social environment for spawning 311 10.6.4 Avoiding domestication 313 10.6.5 Mitigating the effects of captive rearing 313 10.7 Synopsis 314 11 Conclusions: Aquaculture and Behaviour 322 Felicity Huntingford, Malcolm Jobling and Sunil Kadri 11.1 The relevance of behaviour in current aquaculture systems 322 11.1.1 Aquaculture and its aims 322 11.1.2 The behaviour of fish in nature and in culture 323 11.1.3 Problems in fish culture arising from the natural behaviour of fish 323 11.1.4 Behavioural solutions to behavioural problems 325 11.1.5 Behavioural solutions to non-behavioural problems 326 11.1.6 A disclaimer 327 HHuunnttiinnggffoorrdd__ffttoocc..iinndddd xxii 1111//99//22001111 1122::2200::1122 PPMM