Chemical Ecology in Aquatic Systems This page intentionally left blank Chemical Ecology in Aquatic Systems EDITED BY C hrister B rönmark Lund University, Sweden and Lars-Anders Hansson Lund University , Sweden 1 1 Great Clarendon Street, Oxford ox2 6dp Oxford University Press is a department of the University of Oxford. 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Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Library of Congress Control Number: 2011945452 Typeset by SPI Publisher Services, Pondicherry, India Printed and bound by CPI Group (UK) Ltd, Croydon, CR0 4YY ISBN 978–0–19–958309–6 (Hbk.) 978–0–19–958310–2 (Pbk.) 1 3 5 7 9 10 8 6 4 2 Contents List of contributors xii Chemical ecology in aquatic systems—an introduction xiv Christer Brönmark and Lars-Anders Hansson 1 Aquatic odour dispersal fi elds: opportunities and limits of detection, communication, and navigation 1 Jelle Atema 1.1 Odour dispersal: where are the molecules? 3 1.1.1 A question of scale 3 1.1.2 Odour plumes 4 1.1.3 Near-source coincidence 7 1.1.4 Boundary layers 7 1.2 Signal detection: accessing odour 8 1.2.1 Detection threshold 8 1.2.2 Signal-to-noise ratios 8 1.2.3 Intermittency: a patch in space is a pulse in time 8 1.2.4 Aquatic noses 11 1.3 Odour information currents 12 1.4 Navigation in odour fi elds 13 1.4.1 Odour-fl ow coincidence would signal the close proximity of the source 14 1.5 Conclusion 15 References 16 2 Information conveyed by chemical cues 19 Eric von Elert 2.1 Habitat and food fi nding 19 2.2 Induced defences in primary producers and bacteria 23 2.3 Induced defences in animal prey 25 2.3.1 Morphological changes 25 2.3.2 Life history and behavioural changes 26 2.4 Alarm cues in invertebrates 27 2.5 Alarm cues in vertebrates 28 2.6 Pheromones and quorum sensing 29 2.7 Dispersal and settlement cues 32 vi CONTENTS 2.8 Pheromones 32 2.9 Conclusions 33 References 34 3 Pheromones mediating sex and dominance in aquatic animals 39 Thomas Breithaupt and Jörg D. Hardege 3.1 What is a pheromone? 39 3.2 Production, transmission, and reception 40 3.3 Sex pheromones in fi sh—spying males and the evolution of chemical communication 41 3.3.1 The time course of reproductive behaviour in cyprinid fi sh 42 3.3.2 Exceptions from hormonal pheromone communication systems 44 3.4 Sex pheromones in crustaceans—indicators of female receptivity and triggers of mate guarding 45 3.5 Pheromones mediating dominance interactions 47 3.6 Pheromones mediating spawning without courtship—A renicola marina 48 3.7 Pheromones mediating broadcast spawning 49 3.8 Future perspectives and applications of pheromone research 51 References 53 4 Chemical signals and kin biased behaviour 57 Gabriele Gerlach and Cornelia Hinz 4.1 Living with relatives 57 4.1.1 Kin selection 57 4.1.2 Kin recognition 58 4.1.3 Evidence for kin recognition and kin associations in the aquatic environment 58 4.2 Chemical components involved in kin recognition 64 4.2.1 The role of MHC-molecules in the immune system 64 4.2.2 Infl uence of MHC-genotype on social interactions 64 4.2.3 MHC and social interactions in amphibians and fi sh 65 4.3 Concluding remarks 66 References 66 5 The use of chemical cues in habitat recognition and settlement 72 Gabriele Gerlach and Jelle Atema 5.1 Olfactory driven choice of settlement habitat in invertebrates 73 5.2 Habitat recognition in coral reef fi sh 75 5.2.1 Imprinting 78 5.2.2 Climate change and pollution impair habitat recognition 78 5.3 Concluding remarks 79 References 79 6 Migration and navigation 82 Ole B. Stabell 6.1 Introduction 82 6.2 Bottom-dwelling animals 82 6.2.1 Invertebrate homing to specifi c sites after foraging 82 6.2.2 Trail making and trail detection in benthic invertebrates 84 6.2.3 Mechanisms of chemosensory trail detection in molluscs 85 CONTENTS vii 6.3 Free-swimming animals 85 6.3.1 Stationary behaviour and site fi delity 86 6.3.2 Substrate marking by fi sh 86 6.3.3 Feeding migration and homing for reproduction 88 6.3.4 Homing theories 89 6.3.5 Chemical cues involved in site marking and site detection 90 6.3.6 Long distance homing and navigation 91 6.4 Concluding remarks 92 References 93 7 Death from downstream: chemosensory navigation and predator–prey processes 96 Marc Weissburg 7.1 Plumes—a very brief review 96 7.2 Navigational strategies 99 7.3 Ecological consequences 103 7.4 Chemosensory guidance at different scales 106 7.5 Concluding remarks 107 References 108 8 The taste of predation and the defences of prey 111 Linda Weiss , Christian Laforsch , and Ralph Tollrian 8.1 Predation drives evolution of prey 111 8.1.1 Modes of predator detection 111 8.1.2 Chemical cues as indicators of general and acute predation threat 113 8.1.3 Predator-induced defences 114 8.1.4 Multi-predator environments 115 8.2 D aphnia as a model organism for studies of the ecology and evolution of phenotypic plasticity 116 8.2.1 Inducible defences in D aphnia 116 8.2.2 Mechanisms of kairomone perception and information processing in D aphnia 118 8.2.3 Receptors and integration of chemical cues 119 8.2.4 Neuronal signalling 120 8.2.5 Cellular components 121 8.2.6 Developmental time frames 122 8.3 Synopsis and future directions 123 References 123 9 The evolution of alarm substances and disturbance cues in aquatic animals 127 Douglas P. Chivers , Grant E. Brown , and Maud C.O. Ferrari 9.1 Alarm substances 127 9.1.1 The taxonomic distribution of alarm substances 127 9.1.2 The conservation of alarm substances 128 9.2 The chemistry of alarm substances 129 9.3 The ecology of alarm substances 130 9.4 The evolution of alarm substances 132 9.4.1 Predation-centred hypotheses 133 9.4.2 Immune system-centred hypotheses for the evolution of alarm substances 134 9.4.3 Multiple selection pressures? 135 viii CONTENTS 9.5 Disturbance cues 135 9.5.1 The taxonomic distribution of disturbance cues 135 9.5.2 The chemistry of disturbance cues 136 9.5.3 Evolution of disturbance signals 136 9.6 Next steps 136 References 137 10 Scaling up infochemicals: ecological consequences of chemosensory assessment of predation risk 140 Andrew M. Turner and Scott D. Peacor 10.1 From trait response to community level effects: an overview of the process 141 10.2 Population-level processes 142 10.2.1 Predator effect on prey growth rate through induced changes in foraging 142 10.2.2 Predator effect on within-population variation in growth and size 144 10.2.3 Predator effect on prey life history 144 10.2.4 Demographic consequences of trait shifts 144 10.3 Community- and ecosystem-level effects of infochemicals in aquatic systems 145 10.3.1 Trophic cascades 146 10.3.2 Interspecifi c competition 146 10.3.3 Effects of multiple predators: facilitation and inhibition 147 10.3.4 Linked trait modifi cations 147 10.3.5 Nutrient translocation 148 10.3.6 Ecological effi ciency across productivity gradients 149 10.3.7 Theoretical implications 149 10.4 Scaling up the effects of infochemicals 150 10.4.1 Does sensory mode affect species’ interactions? 150 10.4.2 Predator diet 151 10.4.3 Predator identity 151 10.4.4 Chemical cues as an experimental tool 152 10.4.5 Environmental constraints on sensory perception 152 10.5 Conclusion 154 References 154 11 Neuroecology of predator–prey interactions 158 Charles D. Derby and Richard K. Zimmer 11.1 Natural histories and trophic ecologies of spiny lobsters and blue crabs 159 11.2 Chemical attraction mediating search for live, intact prey 161 11.3 Chemical attraction mediating search for a ‘free lunch’—fresh carrion 162 11.4 Chemical stimulation and suppression of feeding 163 11.5 Chemical defences and their effect on ingestion 165 11.6 Neural mechanisms underlying the detection and recognition of feeding stimulants and deterrents 167 11.7 Conclusions and future directions 168 References 169 CONTENTS ix 12 Why is the jack of all trades a master of none? Studying the evolution of inducible defences in aquatic systems 172 Ulrich K. Steiner and Josh R. Auld 12.1 Extrinsic factors and the evolution of inducible defences 174 12.1.1 Environmental fl uctuation 174 12.1.2 Environmental cues 175 12.1.3 Evolutionary arms race: inducible defences and inducible offences 177 12.2 Internal factors and the evolution of inducible defences 177 12.2.1 Reversibility and time lag of induced defence 177 12.2.2 Benefi ts and costs of induced defence 178 12.2.3 Adaptive and passive induced defence 178 12.2.4 Multiple benefi ts and antagonistic induced defence 179 12.2.5 Cost of plasticity and evolutionary time limits 179 12.3 Genetic variation in and genetic basis of induced defences 180 12.4 Conclusions 181 References 181 13 How to explore the sometimes unusual chemistry of aquatic defence chemicals 184 Geo rg Pohnert 13.1 The role of primary metabolites in chemical defence 185 13.1.1 Natural product symbiosis 186 13.2 General chemical properties and biosynthesis of bioactive metabolites 188 13.2.1 Structure elucidation 189 13.2.2 Determination of ecologically relevant concentrations and localization of defence metabolites 190 13.3 Conclusions 192 References 193 14 Allelochemical interactions among aquatic primary producers 196 Elisabeth M. Gross , Catherine Legrand , Karin Rengefors , and Urban Tillmann 14.1 The quagmires of allelopathy—what defi nes allelopathic interactions? 196 14.2 Out and gone—what is an effi cient way to distribute allelochemicals? 197 14.3 Exploitative versus interference competition 199 14.4 Evolution of allelopathy 200 14.4.1 Benefi ts and costs of bioactivity against primary producers 200 14.4.2 Does allelopathy benefi t single cells or the many individuals in a genetically diverse population? 202 14.4.3 Coevolution of donor and target—an arms race? 203 14.5 Are aquatic systems different from terrestrial habitats? 204 14.6 Will disentangling the molecular mechanisms solve the riddles of allelopathy? 205 14.7 Conclusions 207 References 207 15 Chemical defences against herbivores 210 Henrik Pavia , Finn Baumgartner , Gunnar Cervin , Swantje Enge , Julia Kubanek , Göran M. Nylund , Erik Selander , J. Robin Svensson , and Gunilla B. Toth 15.1 Theories of chemical defences 212 15.2 Cost of chemical defence 215
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