Inside the Fish Brain: Cognition, Learning and Consciousness

  • Anders FernöEmail author
  • Ole Folkedal
  • Jonatan Nilsson
  • Tore S. Kristiansen
Part of the Animal Welfare book series (AWNS, volume 20)


Detecting and interpreting information about resources and dangers and behaving flexibly and effectively are essential for survival and welfare. Fish, as well as other organisms, access their surroundings through their sensory systems. They must also have a cognitive system capable of integrating and interpreting the sensory input in relation to earlier experiences, and eventually act according to this input. Learning ability and memory enable fish to detect regularities and associations and construct mental images, categories and concepts. In this way, they can adapt their behaviour to the dynamic environment and predict the near future and the consequences of their behaviour. Numerous studies have shown that many fish species have evolved good cognitive abilities, and can construct internal maps, cope with complex social relationships and retain memories for long periods. Some fish can even innovate and use tools. However, the enormous diversity within the piscine world demands that we view learning, cognition and welfare from an ecological perspective. The cognitive capacity of individual species depends on the environmental and social complexity they encounter, and also differs between populations, coping styles and sexes. It is reasonable to believe that fish are conscious and have emotions and feelings, although their subjective experiences must be very different from ours and also vary between species. Their cognitive capacity and the behavioural flexibility that enables them to cope with aquaculture environments and procedures are essential for the welfare of farmed fish.


Memory Intelligence Categorising Emotions Ecological perspective Aquaculture Domestication Welfare 



We are grateful to Dr. Ruud van den Bos who provided very useful suggestions based on an earlier version of this chapter.


  1. Agrillo C, Miletto Petrazzini ME, Bisazza A (2017) Numerical abilities in fish: a methodological review. Behav Process 141:161–171Google Scholar
  2. Arlinghaus R, Laskowski KL, Alós J, Klefoth T, Monk CT, Nakayama S, Schröder A (2017) Passive gear-induced timidity syndrome in wild fish populations and its potential ecological and managerial implications. Fish Fish 18:360–373Google Scholar
  3. Ashley PJ, Ringrose S, Edwards KL, Wallington E, McCrohan CR, Sneddon LU (2009) Effect of noxious stimulation upon antipredator responses and dominance status in rainbow trout. Anim Behav 77:403–410Google Scholar
  4. Bannier F, Tebbich S, Taborsky B (2017) Early experience affects learning performance and neophobia in a cooperatively breeding cichlid. Ethology 123:712–723Google Scholar
  5. Barrett LF (2009) The future of psychology: Connecting mind to brain. Perspect Psychol Sci 4:326–339PubMedPubMedCentralGoogle Scholar
  6. Barrett LF (2017) How emotions are made: The secret life of the brain. Houghton Mifflin Harcourt Publishing Company, New YorkGoogle Scholar
  7. Barrett LF, Simmons WK (2015) Interoceptive predictions in the brain. Nat Rev Neurosci 16:419–429PubMedPubMedCentralGoogle Scholar
  8. Bassett L, Buchanan-Smith HM (2007) Effects of predictability on the welfare of captive animals. Appl Anim Behav Sci 102:223–245Google Scholar
  9. Bateson P, Laland KN (2013) Tinbergen’s four questions: an appreciation and an update. Trends Ecol Evol 28:712–718PubMedGoogle Scholar
  10. Bateson M, Mather M (2007) Performance on a categorization task suggests that removal of environmental enrichment induces “pessimism” in captive European starlings. Anim Welf 16:33–36Google Scholar
  11. Bekoff M, Sherman PW (2004) Reflections on animal selves. Trends Ecol Evol 19:176–180PubMedGoogle Scholar
  12. Berridge KC, Winkielman P (2003) What is an unconscious emotion? (The case for unconscious “liking”). Cognit Emot 17:181–211Google Scholar
  13. Beukema JJ (1970) Angling experiments with carp: decreased catchability through one trial learning. Netherlands J Zool 20:81–92Google Scholar
  14. Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proc Natl Acad Sci 105:2919–2922PubMedGoogle Scholar
  15. Bitterman ME (1975) The comparative analysis of learning. Science 188:699–709PubMedGoogle Scholar
  16. Boakes RA (1977) Performance on learning to associate a stimulus with positive reinforcement. In: Operant-Pavlovian interactions. Erlbaum, Hillsdale, NJ, pp 67–97Google Scholar
  17. Braithwaite VA, Salvanes AGV (2005) Environmental variability in early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations. Proc R Soc Lond Ser B 272:1107–1113Google Scholar
  18. Braithwaite VA, Huntingford F, van den Bos R (2013) Variation in emotion and cognition among fishes. J Agric Environ Ethics 26:7–23Google Scholar
  19. Bratland S, Stien L, Braithwaite VA, Juell J-E, Folkedal O, Nilsson J, Oppedal F, Fosseidengen JE, Kristiansen TS (2010) From fright to anticipation: using aversive light stimuli to investigate reward conditioning in large groups of Atlantic salmon (Salmo salar). Aquacult Int 18:991–1001Google Scholar
  20. Broglio C, Gomez A, Duran E, Ocana FM, Jimenez-Moya F, Rodriguez F, Salas C (2005) Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Res Bull 66:277–281PubMedGoogle Scholar
  21. Brown C (2001) Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Anim Cogn 4:109–113Google Scholar
  22. Brown C (2012) Tool use in fishes. Fish Fish 13:105–115Google Scholar
  23. Brown C (2015) Fish intelligence, sentience and ethics. Anim Cogn 18:1–17Google Scholar
  24. Brown C, Braithwaite VA (2005) Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcope. Behav Ecol 16:482–487Google Scholar
  25. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288Google Scholar
  26. Brown C, Laland K, Krause J (2011) Fish cognition and behavior, 2nd edn. Wiley-Blackwell, OxfordGoogle Scholar
  27. Bshary R (2006) Machiavellian intelligence in fishes. In: Fish cognition and behavior. Blackwell, Oxford, pp 223–242Google Scholar
  28. Bshary R (2011) Machiavellian intelligence in fishes. In: Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 277–297Google Scholar
  29. Bshary R, Hohner A, Ait-el-Djoudi K, Fricke H (2006) Interspecific communicative and coordinated hunting between groupers and giant moray eels in the red sea. PLoS Biol 4:2393–2398Google Scholar
  30. Bshary R, Gingins S, Vail AL (2014) Social cognition in fishes. Trends Cogn Sci 18:465–471PubMedGoogle Scholar
  31. Bull HO (1928) Studies on conditioned responses in fishes. J Mar Biol Assoc U K 15:485–533Google Scholar
  32. Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922Google Scholar
  33. Butler J (1736) The analogy of religion, natural and revealed, to the constitution and course of nature. J.J. & P. Knapton, LondonGoogle Scholar
  34. Cabanac M (1992) Pleasure: the common currency. J Theor Biol 155:173–200PubMedGoogle Scholar
  35. Carpenter RE, Summers CH (2009) Learning strategies during fear conditioning. Neurobiol Learn Mem 91:415–423PubMedPubMedCentralGoogle Scholar
  36. Castanheira MF, Conceicão LEC, Millot S, Rey S, Bégout M-L, Damsgård B, Kristiansen T, Höglund E, Øverli Ø, Martins CIM (2017) Coping styles in farmed fish: consequences for aquaculture. Rev Aquacult 9:23–41Google Scholar
  37. Cerqueira M, Millot S, Castanheira MF, Félix AS, Silva T, Oliveira GA, Oliveira CC, Martins CIM, Oliveira RF (2017) Cognitive appraisal of environmental stimuli induces emotion-like states in fish. Sci Rep 7, article number 13181Google Scholar
  38. Chandroo KP, Duncan IJH, Moccia RD (2004) Can fish suffer? Perspectives on sentience, pain, fear and stress. Appl Anim Behav Sci 86:225–250Google Scholar
  39. Clark A (2013) Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behav Brain Sci 36:1–73Google Scholar
  40. Clark A (2016) Surfing uncertainty: prediction, action, and the embodied mind. Oxford University Press, New YorkGoogle Scholar
  41. Clark RE, Squire LR (1998) Classical conditioning and brain systems: a key role for awareness. Science 280:77–81PubMedGoogle Scholar
  42. Clark RE, Squire LR (1999) Human eyeblink classical conditioning: Effects of manipulating awareness of the stimulus contingencies. Psychol Sci 10:14–18Google Scholar
  43. Coble DW, Farabee GB, Anderson RO (1985) Comparative learning ability of selected fishes. Can J Fish Aquat Sci 42:791–796Google Scholar
  44. Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435PubMedGoogle Scholar
  45. Coolen I, van Bergen Y, Day RL, Laland KN (2003) Species difference in adaptive use of public information in sticklebacks. Proc R Soc Lond Ser B 270:2413–2419Google Scholar
  46. Coppens CM, de Boer SF, Koolhaas JM (2010) Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc B Biol Sci 365:4021–4028Google Scholar
  47. Corten A (2002) The role of “conservatism” in herring migrations. Rev Fish Biol Fish 11:339–361Google Scholar
  48. Couzin ID (2007) Collective minds. Nature 445:715PubMedGoogle Scholar
  49. Croy MI, Hughes RN (1991) The role of learning and memory in the feeding behaviour of the fifteen-spined stickleback, Spinachia spinachia L. Anim Behav 41:149–159Google Scholar
  50. Dall SRX (2010) Managing risk: the perils of uncertainty. In: Evolutionary behavioral ecology. Oxford University Press, New York, pp 194–206Google Scholar
  51. Damasio A, Carvalho GB (2013) The nature of feelings: evolutionary and neurobiological origins. Nat Rev Neurosci 14:143–152PubMedGoogle Scholar
  52. Dawkins MS (1998) Evolution and animal welfare. Q Rev Biol 73:305–328PubMedGoogle Scholar
  53. Dawkins MS (2003) Behaviour as a tool in the assessment of animal welfare. Zoology 106:383–387PubMedGoogle Scholar
  54. Dawkins MS (2004) Using behaviour to assess animal welfare. Anim Welf 13:3–7Google Scholar
  55. Dawkins MS (2008) The science of animal suffering. Ethology 114:937–945Google Scholar
  56. Dawkins MS (2017) Animal welfare with and without consciousness. J Zool 301:1–10Google Scholar
  57. De Luca G, Mariani P, MacKenzie BR, Marsili M (2014) Fishing out collective memory of migratory schools. J R Soc Interface 11:20140043PubMedPubMedCentralGoogle Scholar
  58. Dugatkin LA, Alfieri MS (2003) Boldness, behavioral inhibition and learning. Ethol Ecol Evol 15:43–49Google Scholar
  59. Dugatkin LA, Godin J-GJ (1992) Reversal of female mate choice by copying in the guppy Poecilia reticulata. Philos Trans R Soc B Biol Sci 249:179–184Google Scholar
  60. Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50PubMedGoogle Scholar
  61. Eckroth JR, Aas-Hansen Ø, Sneddon LU, Bichão H, Døving KB (2014) Physiological and behavioural responses to noxious stimuli in the Atlantic cod (Gadus morhua). PLoS One 9:e100150PubMedPubMedCentralGoogle Scholar
  62. Fabbro F, Aglioti SM, Bergamasco M, Clarici A, Panksepp J (2015) Evolutionary aspects of self- and world consciousness in vertebrates. Front Hum Neurosci 9, article number157Google Scholar
  63. Fernö A (1993) Advances in understanding of basic behaviour - consequences for fish capture. ICES Mar Sci Symp 196:5–11Google Scholar
  64. Fernö A, Huse I (1983) The effect of experience on the behaviour of cod (Gadus morhua L.) towards a baited hook. Fish Res 2:19–28Google Scholar
  65. Fernö A, Järvi T (1998) Domestication genetically alters the anti-predator behaviour of anadromous brown trout (Salmo trutta) - a dummy predator experiment. Nord J Freshw Res 74:95–100Google Scholar
  66. Fernö A, Pitcher TJ, Melle V, Nøttestad L, Mackinson S, Hollingworth C, Misund OA (1998) The challenge of the herring in the Norwegian Sea: making optimal collective spatial decisions. Sarsia 83:149–167Google Scholar
  67. Fernö A, Huse G, Jakobsen PJ, Kristiansen TS, Nilsson J (2011) Fish behaviour, learning, aquaculture and fisheries. In: Fish Cogn Behav, 2nd edn. Wiley-Blackwell, Oxford, pp 359–404Google Scholar
  68. Fleming IA, Einum S (1997) Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication. ICES J Mar Sci 54:1051–1063Google Scholar
  69. Fleming IA, Agustsson T, Finstad B, Johnsson JI, Björnsson BT (2002) Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 59:1323–1330Google Scholar
  70. Folkedal O, Stien LH, Torgersen T, Oppedal F, Olsen RE, Fosseidengen JE, Braithwaite VA, Kristiansen TS (2012) Food anticipatory behaviour as an indicator of stress response and recovery in Atlantic salmon post-smolt after exposure to acute temperature fluctuation. Physiol Behav 105:350–356PubMedGoogle Scholar
  71. Folkedal O, Fernö A, Nederlof MAJ, Fosseidengen JE, Cerqueira M, Olsen RE, Nilsson J (2018) Habituation and conditioning in gilthead sea bream (Sparus aurata): Effects of aversive stimuli, reward and social hierarchies. Aquac Res 49:335–340Google Scholar
  72. Frank SA (2002) Immunology and evolution of infectious disease. Princetown University Press, Princetown and OxfordGoogle Scholar
  73. Fuss T, Schluessel V (2015) Something worth remembering: Visual discrimination in sharks. Anim Cogn 18:463–471PubMedGoogle Scholar
  74. Gabagambi PN (2008) Learning ability in juvenile Atlantic cod (Gadus morhua L.): different CS-US relationships and reward value. Master of Science Thesis, University of BergenGoogle Scholar
  75. Galhardo L, Vital J, Oliveira RF (2011) The role of predictability in the stress response of a cichlid fish. Physiol Behav 102:367–372PubMedGoogle Scholar
  76. Garcia J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124Google Scholar
  77. Gibson RN (2005) The behaviour of flatfishes. In: Flatfishes: biology and exploitation. Blackwell, Oxford, pp 213–239Google Scholar
  78. Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Lond Ser B 265:913–918Google Scholar
  79. Griffin DR (1998) From cognition to consciousness. Anim Cogn 1:3–16Google Scholar
  80. Grissom N, Bhatnagar S (2009) Habituation to repeated stress: get used to it. Neurobiol Learn Mem 92:215–224PubMedGoogle Scholar
  81. Grosenick L, Clement TS, Fernald RD (2007) Fish can infer social rank by observation alone. Nature 445:429–432PubMedGoogle Scholar
  82. Hearst E, Jenkins HM (1974) Sign-tracking: the stimulus-reinforcer relation and directed actions. Monograph of the Psychonomic Society, Austin, TXGoogle Scholar
  83. Helfman GS, Schultz ET (1984) Social tradition of behavioural traditions in a coral reef fish. Anim Behav 32:379–384Google Scholar
  84. Huneman P, Martens J (2017) The behavioural ecology of irrational behaviours. Hist Philos Life Sci 39, article number 23Google Scholar
  85. Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142Google Scholar
  86. Huntingford FA, Adams CE (2005) Behavioural syndromes in farmed fish: implications for production welfare. Behaviour 142:1207–1221Google Scholar
  87. Huntingford FA, Wright PJ (1992) Inherited population differences in avoidance conditioning in three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 122:264–273Google Scholar
  88. Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandoe P, Turnbull JF (2006) Current issues in fish welfare. J Fish Biol 68:332–372Google Scholar
  89. Huse G, Railsback S, Fernö A (2002) Modelling changes in migration pattern of herring: collective behaviour and numerical domination. J Fish Biol 60:571–582Google Scholar
  90. Huse G, Fernö A, Holst J (2010) Establishment of novel wintering areas in herring co-occurs with peaks in the ‘first time/repeat spawner’ ratio. Mar Ecol Prog Ser 409:189–198Google Scholar
  91. Ibrahim AA, Huntingford FA (1992) Experience of natural prey and feeding efficiency in 3-spined sticklebacks (Gasterosteus aculeatus L.). J Fish Biol 41:619–625Google Scholar
  92. Ingraham E, Anderson ND, Hurd PL, Hamilton TJ (2016) Twelve-day reinforcement-based memory retention in African cichlids (Labidochromis caeruleus). Front Behav Neurosci 10:157PubMedPubMedCentralGoogle Scholar
  93. Ioannou CC (2017) Swarm intelligence in fish? The difficulty in demonstrating distributed and self-organised collective intelligence in (some) animal groups. Behav Process 141:141–151Google Scholar
  94. Johnsson JI, Brockmark S, Näslund J (2014) Environmental effects on behavioural development consequences for fitness of captive-reared fishes in the wild. J Fish Biol 85:1946–1971PubMedGoogle Scholar
  95. Jones A, Brown C, Gardener S (2011) Tool use in the spotted tuskfish, Choerodon schoenleinii. Coral Reefs 30:865Google Scholar
  96. Kelley JL (2008) Assessment of predation risk by prey fishes. In: Fish behaviour. Science Publishers, Enfield, NH, pp 269–301Google Scholar
  97. Kendal JR, Rendall L, Pike TW, Laland KN (2009) Nine-spined sticklebacks deploy a hill-climbing social learning strategy. Behav Ecol 20:238–244Google Scholar
  98. Key B (2016) Why fish do not feel pain. Anim Sentience 1(1)Google Scholar
  99. Kittilsen S (2013) Functional aspects of emotions in fish. Behav Process 100:153–159Google Scholar
  100. Kittilsen S, Ellis T, Schjolden J, Braastad BO, Øverli Ø (2009) Determining stress-responsiveness in family groups of Atlantic salmon (Salmo salar) using non-invasive measures. Aquaculture 298:146–152Google Scholar
  101. Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935PubMedGoogle Scholar
  102. Korte SM, Koolhaas JM, Wingfield JC, McEwen BS (2005) The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev 29:3–38PubMedGoogle Scholar
  103. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351PubMedPubMedCentralGoogle Scholar
  104. Kotrschal K, van Staaden MJ, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fish 8:373–408Google Scholar
  105. Kraemer PJ, Golding JM (1997) Adaptive forgetting in animals. Psychon Bull Rev 4:480–491Google Scholar
  106. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  107. Kristiansen TS, Svåsand T (1992) Comparative analysis of stomach contents of cultured and wild cod, Gadus morhua L. Aquacult Fish Manag 23:661–668Google Scholar
  108. Kuba MJ, Byrne RA, Burghardt GM (2010) A new method for studying problem solving and tool use in stingrays (Potamotrygon castexi). Anim Cogn 13:507–513PubMedGoogle Scholar
  109. Kuzawa CW, Chugani HT, Grossman LI, Lipovich L, Muzik O, Hof PR, Wildman DE, Sherwood CC, Leonard WR, Lange N (2014) Metabolic costs and evolutionary implications of human brain development. Proc Natl Acad Sci 111:13010–13015PubMedGoogle Scholar
  110. Laland KN, Williams K (1998) Social transmission of maladaptive information in the guppy. Behav Ecol 9:493–499Google Scholar
  111. Laland KN, Atton N, Webster MM (2011) From fish to fashion: experimental and theoretical insights into the evolution of culture. Philos Trans R Soc Lond B Biol Sci 366:958–968PubMedPubMedCentralGoogle Scholar
  112. Langer EJ, Roth J (1975) Heads I win, tails its chance – illusion of control as a function of sequence of outcomes in a purely chance task. J Pers Soc Psychol 32:951–955Google Scholar
  113. LeDoux J (1996) The emotional brain. The mysterious underpinnings of emotional life. Simon & Schuster, New YorkGoogle Scholar
  114. LeDoux J (2012) Rethinking the emotional brain. Neuron 73:653–676PubMedPubMedCentralGoogle Scholar
  115. Leduc AOHC, Roh E, Breau C, Brown GE (2007) Learned recognition of a novel odour by wild juvenile Atlantic salmon, Salmo salar, under fully natural conditions. Anim Behav 73:471–477Google Scholar
  116. Lieberman DA (1990) Learning, behaviour and cognition, 3rd edn. Wadsworth, Belmont, CAGoogle Scholar
  117. Little EE (1977) Conditioned aversion to amino acid flavors in the catfish, Ictalurus punctatus. Physiol Behav 19:743–747PubMedGoogle Scholar
  118. Lorenzen K, Beveridge M, Mangel M (2012) Cultured fish: integrative biology and management of domestication and interactions with wild fish. Biol Rev 87:639–660PubMedGoogle Scholar
  119. Lucon-Xiccato T, Bisazza A (2016) Male and female guppies differ in speed but not in accuracy in visual discrimination learning. Anim Cogn 19:733–744PubMedGoogle Scholar
  120. Macdonald JI, Logemann K, Krainski ET, Sigurdsson T, Beale CM, Huse G, Hjøxllo SS, Marteinsdóttir G (2018) Can collective memories shape fish distributions? a test, linking space-time occurrence models and population demographics. Ecography 41:938–957Google Scholar
  121. MacKay B (1974) Conditioned food aversion produced by toxicosis in Atlantic cod. Behav Biol 12:347–355PubMedGoogle Scholar
  122. Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253Google Scholar
  123. Madaro A, Fernö A, Kristiansen TS, Olsen RE, Gorissen M, Flik G, Nilsson J (2016) Effect of predictability on the stress response to chasing in Atlantic salmon (Salmo salar L.) parr. Physiol Behav 153:1–6PubMedGoogle Scholar
  124. Mamuneas D, Spence AJ, Manica A, King AJ (2015) Bolder stickleback fish make faster decisions, but they are not less accurate. Behav Ecol 26:91–96Google Scholar
  125. Manteifel YB, Karelina MA (1996) Conditioned food aversion in the goldfish, Carassius auratus. Comp Biochem Physiol 115A:31–35Google Scholar
  126. Manuel R, Gorissen M, Roca CP, Zethof J, van de Vis H, Flik G, van den Bos R (2014) Inhibitory avoidance learning in zebrafish (Danio rerio): effects of shock intensity and unraveling differences in task performance. Zebrafish 11:341–352PubMedPubMedCentralGoogle Scholar
  127. Marchetti MP, Nevitt GA (2003) Effects of hatchery rearing on brain structures of rainbow trout, Oncorhynchus mykiss. Environ Biol Fish 66:9–14Google Scholar
  128. Martins CIM, Silva PIM, Conceição LEC, Costas B, Höglund E, Øverli Ø, Schrama JW (2011) Linking fearfulness and coping styles in fish. PLoS One 6:e28084PubMedPubMedCentralGoogle Scholar
  129. Martins CI, Galhardo L, Noble C, Damsgard B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau JC, Carter T, Planellas SR, Kristiansen T (2012) Behavioural indicators of welfare in farmed fish. Fish Physiol Biochem 38:17–41PubMedGoogle Scholar
  130. Mas-Muñoz J, Komen H, Schneider O, Visch SW, Schrama JW (2011) Feeding behaviour, swimming activity and boldness explain variation in feed intake and growth of sole (Solea solea) reared in captivity. PLoS One 6:e21393PubMedPubMedCentralGoogle Scholar
  131. Mason GJ (2010) Species differences in responses to captivity: stress, welfare and the comparative method. Trends Ecol Evol 25:713–721PubMedGoogle Scholar
  132. Mayer I, Meager JJ, Skjæraasen JE, Rodewald P, Sverdrup G, Fernö A (2011) Domestication causes rapid changes in heart and brain morphology in Atlantic cod (Gadus morhua). Environ Biol Fish 92:181–186Google Scholar
  133. McEwen BS, Gianaros PJ (2011) Stress- and allostasis-induced brain plasticity. Annu Rev Med 62:431–445PubMedPubMedCentralGoogle Scholar
  134. McKean KA, Lazzaro BP (2011) The costs of immunity and the evolution of immunological defense mechanisms. In: Mechanisms of life history evolution. Oxford University Press, Oxford, pp 299–310Google Scholar
  135. McNamara JM, Trimmer PC, Houston AI (2012) It is optimal to be optimistic about survival. Biol Lett 8:516–519PubMedPubMedCentralGoogle Scholar
  136. Meager JJ, Rodewald P, Domenici P, Fernö A, Järvi T, Skjæraasen JE, Sverdrup GK (2011) Behavioural responses of hatchery-reared and wild cod (Gadus morhua L.) to mechano-acoustic stimuli. J Fish Biol 78:1437–1450PubMedGoogle Scholar
  137. Meager JJ, Fernö A, Skaeraasen JE, Järvi T, Rodewald P, Sverdrup G, Winberg S, Mayer I (2012) Multidimensionality of behavioural phenotypes in Atlantic cod, Gadus morhua. Physiol Behav 106:462–470PubMedGoogle Scholar
  138. Meager JJ, Fernö A, Skjæraasen JE (2018) The behavioural diversity of Atlantic cod: insights into variability within and between individuals. Rev Fish Biol Fish 28:153–176Google Scholar
  139. Mesoudi A, Chang L, Dall SRX, Thornton A (2016) The evolution of individual and cultural variation in social learning. Trends Ecol Evol 31:215–225PubMedGoogle Scholar
  140. Metzinger T (2003) Being no one. the self-model theory of subjectivity. The MIT Press, CambridgeGoogle Scholar
  141. Milinski M, Kulling D, Kettler R (1990) Tit for tat: stickleback, Gasterosteus aculeatus, trusting a cooperative partner. Behav Ecol 1:7–11Google Scholar
  142. Miller N, Garnier S, Hartnett AT, Couzin ID (2013) Both information and social cohesion determine collective decisions in animal groups. Proc Natl Acad Sci 110:5263–5268PubMedGoogle Scholar
  143. Millot S, Nilsson J, Fosseidengen JE, Bégout M-L, Fernö A, Braithwaite VA, Kristiansen TS (2013) Innovative behaviour in fish: Atlantic cod can learn to use an external tag to manipulate a self-feeder. Anim Cogn 17:779–785PubMedGoogle Scholar
  144. Murren CJ, Auld JR, Callahan H, Ghalambor CK, Handelsman CA, Heskel MA, Kingsolver JG, Maclean HJ, Mase J, Maughan H, Pfennig DW, Relyea RA, Seiter S, Snell-Rood E, Steiner UK, Schlichting CD (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115:293–301PubMedPubMedCentralGoogle Scholar
  145. Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates. Springer, HeidelbergGoogle Scholar
  146. Nilsson J, Torgersen T (2010) Exploration and learning of demand-feeding in Atlantic cod (Gadus morhua). Aquaculture 306:384–387Google Scholar
  147. Nilsson J, Kristiansen TS, Fosseidengen JE, Fernö A, van den Bos R (2008a) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222PubMedGoogle Scholar
  148. Nilsson J, Kristiansen TS, Fosseidengen JE, Fernö A, van den Bos R (2008b) Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim Cogn 11:651–659PubMedGoogle Scholar
  149. Nilsson J, Kristiansen TS, Fosseidengen JE, Stien LH, Fernö A, van den Bos R (2010) Learning and anticipatory behaviour in a “sit-and-wait” predator: The Atlantic halibut. Behav Process 83:257–266Google Scholar
  150. Nilsson J, Stien LH, Fosseidengen JE, Olsen RE, Kristiansen TS (2012) From fright to anticipation: Reward conditioning versus habituation to a moving dip net in farmed Atlantic cod (Gadus morhua). Appl Anim Behav Sci 138:118–124Google Scholar
  151. Nødtvedt M, Fernö A, Gjøsæter J, Steingrund P (1999) Anti-predator behaviour of hatchery-reared and wild juvenile Atlantic cod (Gadus morhua L.) and the effect of predator training. In: Stock enhancement and sea ranching. Fishing News Books, Blackwell Publishing Ltd, Oxford, pp 350–362Google Scholar
  152. Odling-Smee L, Braithwaite VA (2003) The role of learning in fish orientation. Fish Fish 4:235–246Google Scholar
  153. Odling-Smee LC, Boughman JW, Braithwaite VA (2008) Sympatric species of threespine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62:1935–1945Google Scholar
  154. Odling-Smee L, Simpson SD, Braithwaite VA (2011) The role of learning in fish orientation. In: Fish cognition and behavior, 2nd edn. Wiley-Blackwell, Oxford, pp 166–185Google Scholar
  155. Oppedal F, Dempster T, Stien LH (2011) Environmental drivers of Atlantic salmon behaviour in sea-cages: a review. Aquaculture 311:1–18Google Scholar
  156. Overmier JB, Hollis KL (1990) Fish in the think tank: learning, memory and integrated behavior. In: Neurobiology of comparative cognition. Lawrence Erlbaum Associates, Hillsdale, pp 204–236Google Scholar
  157. Özbilgin H, Glass CW (2004) Role of learning in mesh penetration behaviour of haddock (Melanogrammus aeglefinus). ICES J Mar Sci 61:1190–1194Google Scholar
  158. Panksepp J (1994) Evolution constructed the potential for subjective experience within the neurodynamics of the mammalian brain. In: The nature of emotion: fundamental questions. Oxford University Press, New York, pp 396–399Google Scholar
  159. Panksepp J (2005) Affective consciousness: core emotional feelings in animals and humans. Conscious Cogn 14:30–80PubMedGoogle Scholar
  160. Panksepp J, Lane RD, Solmes M, Smith R (2017) Reconciling cognitive and affective neuroscience perspectives on the brain basis of emotional experience. Neorosci Biobehav Rev 76:187–215Google Scholar
  161. Paul ES, Harding EJ, Mendl M (2005) Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev 29:469–491PubMedGoogle Scholar
  162. Petitgas P, Secor DH, McQuinn I, Huse G, Lo N (2010) Stock collapses and their recovery: mechanisms that establish and maintain life-cycle closure in space and time. ICES J Mar Sci 67:1841–1848Google Scholar
  163. Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SCP, Shumway CA, Hofmann HA (2007) Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav Evol 70:21–39PubMedGoogle Scholar
  164. Portavella M, Torres B, Salas C (2004) Avoidance response in goldfish: Emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335–2342PubMedPubMedCentralGoogle Scholar
  165. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wum C-F, Thompson RF (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92:135–138PubMedGoogle Scholar
  166. Rescorla RA (1966) Predictability and number of pairings in Pavlovian fear conditioning. Psychon Sci 4:383–384Google Scholar
  167. Rodriguez F, Duran E, Vargas JP, Torres B, Salas C (1994) Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes. Anim Learn Behav 22:409–420Google Scholar
  168. Rose JD (2002) The neurobehavioral nature of fishes and the question of awareness and pain. Rev Fish Sci 10:1–38Google Scholar
  169. Rose JD, Arlinghaus R, Cooke SJ, Diggles BK, Sawynok W, Stevens ED, Wynne CDL (2014) Can fish really feel pain? Fish Fish 15:97–133Google Scholar
  170. Rozin P, Kalat J (1972) Learning as a situation-specific adaption. In: Biological boundaries of learning. Appelton, New York, pp 66–97Google Scholar
  171. Ruiz-Gomez ML, Huntingford FA, Øverli Ø, Thörnqvist P-O, Höglund E (2011) Response to environmental change in rainbow trout selected for divergent stress coping styles. Physiol Behav 102:317–322Google Scholar
  172. Salas C, Broglio C, Durán E, Gómez A, Ocaña FM, Jiménez-Moya F, Rodríguez F (2006) Neuropsychology of learning and memory in teleost fish. Zebrafish 3:157–171PubMedGoogle Scholar
  173. Salvanes AGV, Moberg O, Ebbesson LOE, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc Lond Ser B 280:1–7Google Scholar
  174. Salwiczek LH, Pretot L, Demarta L, Proctor D, Essler J, Pinto AI, Wismer S, Stoinski T, Brosnan SF, Bshary R (2012) Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orangutans in a complex foraging task derived from cleaner – client reef fish cooperation. PLoS One 7:e49068PubMedPubMedCentralGoogle Scholar
  175. Schlag KH (1998) Why imitate and if so, how? A boundedly rational approach to multi-armed bandits. J Econ Theory 78:130–156Google Scholar
  176. Scholtz AT, Horrall RM, Cooper JC, Hasler AD (1976) Imprinting to chemical cues: the basis for home stream selection in salmon. Science 192:1247–1249Google Scholar
  177. Schreck CB, Jonsson L, Feist G, Reno P (1995) Conditioning improves performance of juvenile Chinook salmon, Oncorhynchus tshawytscha, to transportation stress. Aquaculture 135:99–110Google Scholar
  178. Schuster S, Wöhl S, Griebsch M, Klostermeier I (2006) Animal cognition: How archer fish learn to down rapidly moving targets. Curr Biol 16:378–383PubMedGoogle Scholar
  179. Seth AK (2013) Interoceptive inference, emotion, and the embodied self. Trends Cogn Sci 17:565–573PubMedGoogle Scholar
  180. Sevenster P (1973) Incompatibility of response and reward. In: Constraints on learning. Academic Press, London, pp 265–283Google Scholar
  181. Sheenaja KK, Thomas KJ (2011) Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792). Mar Freshw Behav Physiol 44:349–358Google Scholar
  182. Shettleworth SJ (2010) Cognition, Evolution and Behaviour, 2nd edn. University Press, OxfordGoogle Scholar
  183. Sih A, Del Giudice M (2012) Linking behavioral syndromes and cognition: a behavioral ecology perspective. Philos Trans R Soc B Biol Sci 367:2762–2772Google Scholar
  184. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Q Rev Biol 19:372–378Google Scholar
  185. Sinclair ELE, Noronha de Souza CR, Ward AJW, Seebacher F (2014) Exercise changes behaviour. Funct Ecol 28:652–659Google Scholar
  186. Smithdeal M (2016) Belief in free will as an adaptive, ungrounded belief. Philos Psychol 29:1241–1252Google Scholar
  187. Sneddon L (2003) The bold and the shy: individual differences in rainbow trout. J Fish Biol 62:971–975Google Scholar
  188. Sneddon LU (2011) Pain perception in fish: evidence and implications for the use of fish. J Conscious Stud 18:209–229Google Scholar
  189. Sneddon LU (2015) Pain in aquatic animals. J Exp Biol 218:967–976PubMedGoogle Scholar
  190. Snell-Rood EC (2012) Selective processes in development: Implications for the costs and benefits of phenotypic plasticity. Integr Comp Biol 52:31–42PubMedGoogle Scholar
  191. Solberg MF, Skaala Ø, Nilsen F, Glover KA (2013a) Does domestication cause changes in growth reaction norms? A study of farmed, wild and hybrid Atlantic salmon families exposed to environmental stress. PLoS One 8:e54469PubMedPubMedCentralGoogle Scholar
  192. Solberg MF, Zhang Z, Nilsen F, Glover KA (2013b) Growth reaction norms of domesticated, wild and hybrid Atlantic salmon families in response to differing social and physical environments. BMC Evol Biol 13:234PubMedPubMedCentralGoogle Scholar
  193. Spruijt BM, van den Bos R, Pijlman TA (2001) A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Appl Anim Behav Sci 72:145–171PubMedGoogle Scholar
  194. Steingrund P, Fernö A (1997) Feeding behaviour of reared and wild cod and the effect of learning: two strategies of feeding on the two-spotted goby. J Fish Biol 51:334–348Google Scholar
  195. Sumpter DJT, Krause J, James R, Couzin I (2008) Consensus decision making by fish. Curr Biol 18:1773–1777PubMedGoogle Scholar
  196. Tinbergen N (1963) On aims and methods of ethology. Zeitschrift für Tierpsychologi 20:410–433Google Scholar
  197. Toates F (2004) Cognition, motivation, emotion and action: a dynamic and vulnerable interdependence. Appl Anim Behav Sci 86:173–204Google Scholar
  198. Torgersen T, Bracke MBM, Kristiansen TS (2011) Reply to Diggles et al. (2011): ecology and welfare of aquatic animals in wild capture fisheries. Rev Fish Biol Fish 21:767–769Google Scholar
  199. Vail AL, Manica A, Bshary R (2013) Referential gestures in fish collaborative hunting. Nat Commun 4, article number 1765Google Scholar
  200. van den Bos R, Flik G (2015) Editorial: decision-making under stress: the importance of cortico-limbic circuits. Front Behav Neurosci 9:203PubMedPubMedCentralGoogle Scholar
  201. van den Bos R, Meijer M, van Renselaar J, van der Harst J, Spruijt B (2003) Anticipation is differently expressed in rats (Rattus norvegicus) and domestic cats (Felis silvestris catus) in the same Pavlovian conditioning paradigm. Behav Brain Res 141:83–89PubMedGoogle Scholar
  202. van den Bos R, Jolles JW, Homberg JR (2013) Social modulation of decision-making: a cross-species review. Front Hum Neurosci 7:301PubMedPubMedCentralGoogle Scholar
  203. van Staaden M, Huber R, Kaufman L, Liem K (1995) Brain evolution in cichlids of the African Great Lakes: brain and body size, general patterns and evolutionary trends. Zoology 98:165–178Google Scholar
  204. Venkatraman A, Edlow BL, Immordino-Yang MH (2017) The brainstem in emotion: A review. Front Neuroanat 11:15PubMedPubMedCentralGoogle Scholar
  205. Vindas MA, Madaro A, Fraser TWK, Höglund E, Olsen RE, Øverli Ø, Kristiansen TS (2016) Coping with a changing environment: the effects of early life stress. R Soc Open Sci 3:160382PubMedPubMedCentralGoogle Scholar
  206. von Uexküll J (1921) Umwelt und Innenwelt der Tiere, 2nd edn. Springer, BerlinGoogle Scholar
  207. Ward AJW, Herbert-Read JE, Sumpter DJT, Krause J (2011) Fast and accurate decisions through collective vigilance in fish shoals. Proc Natl Acad Sci USA 108:2312–2315PubMedGoogle Scholar
  208. Ward AJW, Krause J, Sumpter DJT (2012) Quorum decision-making in foraging fish shoals. PLoS One 7:e32411PubMedPubMedCentralGoogle Scholar
  209. Weary DM, Droege P, Braithwaite VA (2017) Chapter two - behavioral evidence of felt emotions: Approaches, inferences, and refinements. Adv Study Behav 49:27–48Google Scholar
  210. Weinstein ND (1980) Unrealistic optimism about future life events. J Pers Soc Psychol 39:806–820Google Scholar
  211. White GE, Brown C (2015) Cue choice and spatial learning ability are affected by habitat complexity in intertidal gobies. Behav Ecol 26:178–184Google Scholar
  212. White SL, Wagner T, Gowan C, Braithwaite VA (2017) Can personality predict individual differences in brook trout spatial learning ability? Behav Process 141:220–228Google Scholar
  213. Wingfield JC (2003) Control of behavioural strategies for capricious environments. Anim Behav 66:807–815Google Scholar
  214. Wisenden BD, Harter KR (2001) Motion, not shape, facilitates association of predation risk with novel objects by fathead minnows. Ethology 107:357–364Google Scholar
  215. Yoshida M, Hirano R (2010) Effects of local anesthesia of the cerebellum on classical fear conditioning in goldfish. Behav Brain Funct 6, article number 20Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Anders Fernö
    • 1
    Email author
  • Ole Folkedal
    • 2
  • Jonatan Nilsson
    • 2
  • Tore S. Kristiansen
    • 2
  1. 1.Department of BiologyUniversity of BergenBergenNorway
  2. 2.Institute of Marine ResearchBergenNorway

Personalised recommendations