Fish Cognition and Behavior

Culum Brown is at the Department of Biological Sciences, Macquarie University, Sydney, Australia. Kevin Laland is at the Centre for Social Learning and Cognitive Evolution, School of Biology, University of St Andrews, UK. Jens Krause is at the Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, and also at Humboldt University, both in Berlin, Germany.

• Preface and Acknowledgements xvSeries Foreword xviList of Contributors xix1 Fish Cognition and Behaviour 1Brown, Laland and Krause1.1 Introduction 11.2 Contents of this book 3References 92 Learning of Foraging Skills by Fish 10Warburton and Hughes2.1 Introduction 102.2 Some factors affecting the learning process 122.2.1 Reinforcement 122.2.2 Drive 122.2.3 Stimulus attractiveness 122.2.4 Exploration and sampling 142.2.5 Attention and simple association 142.2.6 Cognition 152.2.7 Memory systems and skill transfer 182.3 Patch use and probability matching 192.4 Performance 212.5 Tracking environmental variation 232.6 Competition 262.7 Learning and fish feeding: some applications 272.8 Conclusions 27Acknowledgements 28References 293 Learned Defences and Counterdefences in Predator–Prey Interactions 36Kelley and Magurran3.1 Introduction 363.2 The predator–prey sequence 383.2.1 Encounter 393.2.1.1 Avoiding dangerous habitats 393.2.1.2 Changing activity patterns 403.2.2 Detection 413.2.2.1 Crypsis 423.2.2.2 Sensory perception 423.2.3 Recognition 433.2.3.1 Associative learning 433.2.3.2 Learning specificity 443.2.3.3 Search images 453.2.3.4 Aposematism and mimicry 463.2.4 Approach 473.2.4.1 Pursuit deterrence 473.2.4.2 Gaining information about the predator 473.2.4.3 Social learning 473.2.4.4 Habituation 493.2.5 Evasion 493.2.5.1 Reactive distance and escape speed and trajectory 503.2.5.2 Survival benefits/capture success 503.3 Summary and discussion 51Acknowledgements 52References 534 Learning about Danger: Chemical Alarm Cues and Threat-Sensitive Assessment of Predation Risk by Fishes 59Brown, Ferrari and Chivers4.1 Introduction 594.2 Chemosensory cues as sources of information 604.2.1 Learning, innate responses and neophobia 604.2.2 Learned predator recognition through conditioning with alarm cues 624.3 Variable predation risk and flexible learning 624.3.1 Assessing risk in time 644.3.2 Sensory complementation and threat-sensitive learning 654.4 Generalisation of risk 664.4.1 Generalising of predator cues 664.4.2 Generalisation of non-predator cues 674.5 Predator recognition continuum hypothesis 684.5.1 Ecological selection for innate versus learned recognition of predators 694.5.2 Ecological selection for generalised learning 694.6 Retention: the forgotten component of learning 704.7 Conservation, management and learning 724.7.1 Conditioning predator recognition skills 724.7.2 Anthropogenic constraints 734.7.3 Field-based studies 734.8 Conclusions 74Acknowledgements 74References 745 Learning and Mate Choice 81Witte and Nöbel5.1 Introduction 815.2 Sexual imprinting 825.2.1 Does sexual imprinting promote sympatric speciation in fishes? 825.3 Learning after reaching maturity 835.4 Eavesdropping 845.4.1 Eavesdropping and mate choice 845.4.2 Benefits of eavesdropping 845.4.3 The audience effect 855.5 Mate-choice copying 875.5.1 Mate-choice copying – first experimental evidence and consequence 885.5.2 Mate-choice copying – evidence from the wild 895.5.3 Mate-choice copying when living in sympatry or allopatry 915.5.4 Mate-choice copying – the role of the early environment 925.5.5 Quality of the model fish 935.6 Social mate preferences overriding genetic preferences 945.6.1 Indications from guppies 945.6.2 Indications from sailfin mollies 955.7 Cultural evolution through mate-choice copying 965.8 Does mate-choice copying support the evolution of a novel male trait? 965.8.1 Theoretical approaches 975.8.2 Experimental approaches 985.9 Is mate-choice copying an adaptive mate-choice strategy? 995.9.1 Benefits of mate-choice copying 995.9.2 Costs of mate-choice copying 1005.10 Outlook 1015.11 Conclusions 102References 1026 Aggressive Behaviour in Fish: Integrating Information about Contest Costs 108Hsu, Earley and Wolf6.1 Introduction 1086.2 Information about resource value 1106.3 Information about contest costs 1106.3.1 Assessing fighting ability 1116.3.2 Information from past contests 1136.3.2.1 Winner and loser effects 1136.3.2.2 Individual recognition 1176.3.2.3 Social eavesdropping 1176.3.3 Integrating different types of cost-related information 1186.4 Physiological mechanisms 1196.5 Conclusions and future directions 126Acknowledgements 128References 1287 Personality Traits and Behaviour 135Budaev and Brown7.1 Introduction 1357.2 Observation and description of personality 1377.2.1 Current terminology 1377.2.1.1 Shyness–boldness 1387.2.1.2 Coping styles 1407.2.1.3 Behavioural syndromes 1407.2.2 Objectivity 1407.2.3 Labelling personality traits; construct validity 1427.2.4 Objective and subjective measurements of personality 1427.2.5 Modern terminology and statistical approaches 1457.3 Proximate causation 1467.4 Ontogeny and experience 1497.5 Is personality adaptive? 1507.5.1 Frequency- and density-dependent selection 1507.5.2 State-dependent models 1517.6 Evolution 1537.7 Wider implications 1557.7.1 Fish production and reproduction 1557.7.2 Personality and population dynamics 1557.8 Conclusions 156Acknowledgements 157References 1578 The Role of Learning in Fish Orientation 166Odling-Smee, Simpson and Braithwaite8.1 Introduction 1668.2 Why keep track of location? 1668.3 The use of learning and memory in orientation 1678.4 Learning about landmarks 1688.5 Compass orientation 1718.6 Water movements 1728.7 Inertial guidance and internal ‘clocks’ 1738.8 Social cues 1748.9 How flexible is orientation behaviour? 1748.9.1 When to learn? 1748.9.2 What to learn? 1758.9.3 Spatial learning capacity 1768.10 Salmon homing – a case study 1778.11 Conclusion 179Acknowledgements 179References 1809 Social Recognition of Conspecifics 186Griffiths and Ward9.1 Introduction 1869.2 Recognition of familiars 1869.2.1 Laboratory studies of familiarity 1879.2.2 Mechanisms of familiarity recognition 1879.2.3 Functions of associating with familiar fish 1919.2.4 Familiarity in free-ranging fishes 1949.2.5 Determinants of familiarity 1959.3 Familiarity or kin recognition? 1969.3.1 Kin recognition theory 1969.3.2 Evidence for kin recognition from laboratory studies 2009.3.3 Advantages of kin discrimination 2019.3.4 Kin association in the wild 2019.3.5 Explaining the discrepancies between laboratory and field 2039.3.6 Kin avoidance 2059.4 Conclusion 206References 20710 Social Organisation and Information Transfer in Schooling Fish 217Ioannou, Couzin, James, Croft and Krause10.1 Introduction 21710.2 Collective motion 21810.3 Emergent collective motion in the absence of external stimuli 21910.4 Response to internal state and external stimuli: Information processing within schools 22010.4.1 Collective response to predators 22010.4.2 Mechanisms and feedback in information transfer 22210.4.3 Information transfer during group foraging and migration 22510.5 Informational status, leadership and collective decision-making in fish schools 22510.6 The structure of fish schools and populations 22710.7 Social networks and individual identities 22910.8 Community structure in social networks 23210.9 Conclusions and future directions 233Acknowledgements 234References 23411 Social Learning in Fishes 240Brown and Laland11.1 Introduction 24011.2 Antipredator behaviour 24111.3 Migration and orientation 24411.4 Foraging 24711.5 Mate choice 24811.6 Aggression 24911.7 Trade-offs in reliance on social and asocial sources of information 25011.8 Concluding remarks 252Acknowledgements 252References 25212 Cooperation and Cognition in Fishes 258Alfieri and Dugatkin12.1 Introduction 25812.2 Why study cooperation in fishes? 25912.3 Cooperation and its categories 26112.3.1 Category 1 – kin selection 26112.3.1.1 Cognition and kin selection 26112.3.1.2 Example of kin selected cooperation: Cooperative breeding 26212.3.1.3 Example of kin selected cooperation: Conditional territory defence 26212.3.2 Category 2 – reciprocity 26312.3.2.1 Cognition and reciprocity 26412.3.2.2 Example of reciprocity: Egg trading 26512.3.2.3 Example of reciprocity: Predator inspection 26612.3.2.4 Example of reciprocity: Interspecific cleaning behaviour 26712.3.3 Category 3 – by-product mutualism 26812.3.3.1 Cognition and by-product mutualism 26812.3.3.2 Example of by-product mutualism: Cooperative foraging 26912.3.4 Category 4 – trait group selection 27012.3.4.1 Cognition and trait group selection 27012.3.4.2 Example of trait group selected cooperation: Predator inspection 27012.4 Conclusion 271Acknowledgements 272References 27213 Machiavellian Intelligence in Fishes 277Bshary13.1 Introduction 27713.2 Evidence for functional aspects of Machiavellian intelligence 27913.2.1 Information gathering about relationships between other group members 27913.2.2 Predator inspection 28013.2.3 Group-living cichlids 28113.2.4 Machiavellian intelligence in cleaning mutualisms 28313.2.4.1 Categorisation and individual recognition of clients 28313.2.4.2 Building up relationships between cleaners and resident clients 28413.2.4.3 Use of tactile stimulation by cleaners to manipulate client decisions and reconcile after conflicts 28413.2.4.4 Audience effects in response to image scoring and tactical deception 28513.2.4.5 Punishment by males during pair inspections 28513.3 Evidence for cognitive mechanisms in fishes 28613.3.1 What cognitive abilities might cleaners need to deal with their clients? 28613.3.2 Other cognitive mechanisms 28713.4 Discussion 28813.4.1 Future avenues I: How Machiavellian is fish behaviour? 28913.4.2 Future avenues II: Relating Machiavellian-type behaviour to brain size evolution 29013.4.3 Extending the Machiavellian intelligence hypothesis to general social intelligence 291Acknowledgements 291References 29114 Lateralization of Cognitive Functions in Fish 298Bisazza and Brown14.1 Introduction 29814.2 Lateralized functions in fish 30014.2.1 Antipredator behavior 30014.2.1.1 Predator inspection 30114.2.1.2 Predator evasion 30214.2.1.3 Fast escape response 30314.2.2 Mating behavior 30414.2.3 Aggression 30414.2.4 Shoaling and social recognition 30414.2.5 Foraging behavior 30614.2.6 Exploration and response to novelty 30614.2.7 Homing and spatial abilities 30714.2.8 Communication 30714.3 Individual differences in lateralization 30814.3.1 Hereditary basis of lateralization 30814.3.2 Sex differences in lateralization 30914.3.3 Environmental factors influencing development of lateralization 31014.3.4 Lateralization and personality 31114.4 Ecological consequences of lateralization of cognitive functions 31214.4.1 Selective advantages of cerebral lateralization 31214.4.2 Costs of cerebral lateralization 31414.4.3 Maintenance of intraspecific variability in the degree of lateralization 31614.4.4 Evolutionary significance of population biases in laterality 31614.5 Summary and future research 317Acknowledgements 318References 31915 Brain and Cognition in Teleost Fish 325Broglio, Gómez, Durán, Salas and Rodríguez15.1 Introduction 32515.2 Classical conditioning 32715.2.1 Delay motor classical conditioning and teleost fish cerebellum 32815.2.2 Role of the teleost cerebellum and telencephalic pallium in trace motor classical conditioning 33015.3 Emotional learning 33115.3.1 Role of the medial pallium in avoidance conditioning and taste aversion learning 33215.3.2 Teleost cerebellum and fear conditioning 33415.4 Spatial cognition 33615.4.1 Allocentric spatial memory representations in teleost fishes 33715.4.2 Role of the teleost telencephalon in egocentric and allocentric spatial navigation 34015.4.3 Map-like memories and hippocampal pallium in teleost fishes 34515.4.4 Neural mechanisms for egocentric spatial orientation 34715.5 Concluding remarks 349Acknowledgements 350References 35016 Fish Behaviour, Learning, Aquaculture and Fisheries 359Fernö, Huse, Jakobsen, Kristiansen and Nilsson16.1 Fish learning skills in the human world 35916.2 Fisheries 36216.2.1 Spatial dynamics 36216.2.1.1 Learning skills and movement 36216.2.1.2 Social learning of migration pattern 36316.2.1.3 Implications of learning for fisheries management 36616.2.2 Fish capture 36716.2.2.1 Natural variations in spatial distribution and behaviour 36916.2.2.2 Avoidance and attraction before fishing 36916.2.2.3 Before physical contact with the gear 36916.2.2.4 After physical contact with the gear 37116.2.2.5 Behaviour after escaping the gear and long-term consequences 37216.2.3 Abundance estimation 37416.3 Aquaculture 37516.3.1 Ontogeny 37516.3.2 Habituation, conditioning and anticipation 37616.3.3 Pavlovian learning – delay and trace conditioning 37816.3.4 Potential use of reward conditioning in aquaculture 37916.3.5 Operant learning 38216.3.6 Individual decisions and collective behaviour 38316.4 Stock enhancement and sea-ranching 38416.5 Escapees from aquaculture 38816.6 Capture-based aquaculture 38916.7 Conclusions and perspectives 389Acknowledgements 391References 39117 Cognition and Welfare 405Sneddon17.1 Introduction 40517.1.1 Fish welfare 40617.1.2 Preference and avoidance testing 40717.1.3 Behavioural flexibility and intraspecific variation 40817.2 What is welfare? 40817.2.1 Sentience and consciousness 40917.2.2 Cognition and welfare 41017.3 What fishes want 41017.3.1 Preference tests 41117.3.1.1 Physical habitat 41117.3.1.2 Breeding 41317.3.1.3 Diet 41317.3.1.4 Social interactions 41417.4 What fishes do not want 41617.5 Pain and fear in fish 41717.6 Personality in fish 42017.7 Wider implications for the use of fish 42017.7.1 Aquaculture 42117.7.2 Fisheries 42517.7.3 Recreational fishing 42517.7.4 Research 42617.7.5 Companion fish 42717.8 Conclusion 427Acknowledgements 429References 429Species List 435Index 443

“With the inclusion of new aspects and the update of the content of the first edition this book is a must for all researchers in the field of fish behaviour and interaction.”  (Bulletin of Fish Biology, 1 October 2011)“Summing Up: Recommended.  Upper-division undergraduates through professionals.”  (Choice, 1 March 2012)