Who would have thought that ‘Jaws’ also has brains? Cognitive functions in elasmobranchs

Abstract

Adaptation of brain structures, function and higher cognitive abilities most likely have contributed significantly to the evolutionary success of elasmobranchs, but these traits remain poorly studied when compared to other vertebrates, specifically mammals. While the pallium of non-mammalian vertebrates lacks the mammalian neocortical organization responsible for all cognitive abilities of mammals, several behavioural and neuroanatomical studies in recent years have clearly demonstrated that elasmobranchs, just like teleosts and other non-mammalian vertebrates, can nonetheless solve a multitude of cognitive tasks. Sharks and rays can learn and habituate, possess spatial memory; can orient according to different orientation strategies, remember spatial and discrimination tasks for extended periods of time, use tools; can imitate and learn from others, distinguish between conspecifics and heterospecifics, discriminate between either visual objects or electrical fields; can categorize visual objects and perceive illusory contours as well as bilateral symmetry. At least some neural correlates seem to be located in the telencephalon, with some pallial regions matching potentially homologous areas in other vertebrates where similar functions are being processed. Results of these studies indicate that the assessed cognitive abilities in elasmobranchs are as well developed as in teleosts or other vertebrates, aiding them in fundamental activities such as food retrieval, predator avoidance, mate choice and habitat selection.

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References

  1. Abellán A, Desfilis E, Medina L (2013) The olfactory amygdala in amniotes: an evo-devo approach. Anat Rec 296:1317–1332

    Google Scholar 

  2. Agrillo C, Petrazzini MEM, Dadda M (2013) Illusionary patterns are fishy for fish, too. Front Neural Circuits 7:137. doi:10.3389/fncir.2013.00137

    PubMed Central  PubMed  Google Scholar 

  3. Altbacker V, Csanyl V (1990) The role of eyespots in predator recognition and antipredatory behavior of the paradise fish, Macropodus-opercularis L. Ethology 85:51–57

    Google Scholar 

  4. Aronson LR (1951) Orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Am Mus Novit 1486:1–22

    Google Scholar 

  5. Aronson LR (1971) Further studies on orientation and jumping behaviour in the gobiid fish, Bathygobius Soporator. In: Adler HE (ed) Orientation: sensory bases. Ann NY Acad Sci 188:378–392

  6. Aronson LR, Aronson FR, Clark E (1967) Instrumental conditioning and light–dark discrimination in young nurse sharks. Bull Mar Sci 17:249–256

    Google Scholar 

  7. Atoji Y, Wild JM (2006) Anatomy of the avian hippocampal formation. Rev Neurosci 17:3–16

    PubMed  Google Scholar 

  8. Banner A (1972) Use of sound in predation by young lemon sharks, Negaprion brevirostris (Poey). Bull Mar Sci 22:251–283

    Google Scholar 

  9. Bauchot R, Platel R, Ridet JM (1976) Brain-body weight relationships in Selachii. Copeia 2:305–310

    Google Scholar 

  10. Berry JW (1968) Ecology, perceptual development and the Muller–Lyer illusion. Br J Psychol 59:205–210

    CAS  PubMed  Google Scholar 

  11. Beukema JJ (1970) Angling experiments with carp (Cyprinus carpio L.) II. Decreasing catchability through one-trial learning. Neth J Zool 20:81–92

    Google Scholar 

  12. Bindra D, Anchel H (1963) Immobility as an avoidance response, and its disruption by drugs. J Exp Anal Behav 6:213–218

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Brown C (2001) Familiarity with the test environment improves the escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Anim Cogn 4:109–113

    Google Scholar 

  14. Brown C (2012) Tool use in fishes. Fish Fish 13:105–115

    Google Scholar 

  15. Brown C, Laland K, Krause J (2011) Fish cognition and behavior, 2nd edn. Blackwell Publishing Ltd, Oxford

    Google Scholar 

  16. Bshary R (2006) Machiavellian intelligence in fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Blackwell Scientific, Oxford, pp 223–242

    Google Scholar 

  17. Bshary R, Wickler W, Fricke H (2002) Fish cognition: a primate’s eye view. Anim Cogn 5:1–23

    PubMed  Google Scholar 

  18. Burt de Perera T, Garcia M (2003) Amarillo fish (Girardinichthys multiradiatus) use visual landmarks to orient in space. Ethology 109:341–350

    Google Scholar 

  19. Burt de Perera T, Holbrook RI (2011) Three-dimensional spatial cognition: information in the vertical dimension overrides information from the horizontal. Anim Cogn 14:613–619

    PubMed  Google Scholar 

  20. Burt de Perera T, Holbrook RI (2012) Three-dimensional spatial representation in freely swimming fish. Cogn Proc 13:107–111

    Google Scholar 

  21. Butler AB, Reiner A, Karten HJ (2011) Evolution of the amniote pallium and the origins of mammalian neocortex. Ann N Y Acad Sci 1225:14–27

    PubMed Central  PubMed  Google Scholar 

  22. Chandroo K, Duncan IJ, Moccia R (2004) Can fish suffer? Perspectives on sentience, pain, fear and stress. Appl Anim Behav Sci 86:225–250

    Google Scholar 

  23. Chittka L, Skorupski P (2011) Information processing in miniature brains. Proc R Soc B 278:885–888

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Clark E (1959) Instrumental conditioning of lemon sharks. Science 130:217–218

    CAS  PubMed  Google Scholar 

  25. Clark E (1961) Visual discrimination in lemon sharks. Tenth Pac Sci Congr Honol 10:175–176

    Google Scholar 

  26. Clark E (1963) The maintenance of sharks in captivity, with a report on their instrumental conditioning. In: Gilbert PW (ed) Sharks and survival. DC Heath, Boston, pp 115–150

    Google Scholar 

  27. Collin SP (2012) The neuroecology of cartilaginous fishes: sensory strategies for survival. Brain Behav Evol 80:80–96

    PubMed  Google Scholar 

  28. Compagno LJV (1999) Systematics and body form. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. Johns Hopkins University Press, Baltimore, pp 1–42

    Google Scholar 

  29. Coolen I, Bergen YV, Day RL, Laland KN (2003) Species difference in adaptive use of public information in sticklebacks. Proc R Soc Lond B 270:2413–2419

    Google Scholar 

  30. Costa SS, Andrade R, Carneiro LA, Goncalves EJ, Kotrschal K, Oliveira RF (2011) Sex differences in the dorsolateral telencephalon correlate with home ranges in blenniid fish. Brain Behav Evol 77:55–64

    PubMed  Google Scholar 

  31. Coyer J (1995) Use of a rock as an anvil for breaking scallops by the yellowhead wrasse, Halichoeres garnoti (Labridae). Bull Mar Sci 57:548–549

    Google Scholar 

  32. 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 41:149–159

    Google Scholar 

  33. Csanyi V (1985) Ethological analysis of predator avoidance by the paradise fish (Macropodus-opercularis L). 1. Recognition and learning of predators. Behaviour 92:227–240

    Google Scholar 

  34. Csanyi V (1986) Ethological analysis of predator avoidance by the paradise fish (Macropodus-opercularis L). 2. Key stimuli in avoidance-learning. Anim Learn Behav 14:101–109

    Google Scholar 

  35. Cuthill IC, Kacelnik A, Krebs JR, Haccou P, Iwasa Y (1990) Starlings exploiting patches: the effect of recent experience on foraging decisions. Anim Behav 40:625–640

    Google Scholar 

  36. Darmaillacq AS, Dickel L, Rahmani N, Shashar N (2011) Do reef fish, Variola louti and Scarus niger, perform amodal completion? Evidence from a field study. J Comp Psychol 125:273

    PubMed  Google Scholar 

  37. Demski LS (2013) The pallium and mind/behavior relationships in teleost fishes. Brain Behav Evol 82:31–44

    PubMed  Google Scholar 

  38. Desjardins JK, Fernald RD (2011) What do fish make of mirror images? Biol Lett 6:744–747

    Google Scholar 

  39. Dicke U, Roth G (2007) Evolution of the amphibian nervous system. In: Kaas JH (ed) Evolution of nervous systems, vol 2. Academic Press, Oxford, pp 61–124

    Google Scholar 

  40. Dittman AH, Quinn TP (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91

    PubMed  Google Scholar 

  41. Douglas RH, Eva J, Guttridge N (1988) Size constancy in goldfish (Carassius auratus). Behav Brain Res 30:37–42

    CAS  PubMed  Google Scholar 

  42. Dugatkin LA (1992) Sexual selection and imitation: females copy the mate choice of others. Am Nat 139:1384–1389

    Google Scholar 

  43. Dugatkin LA, Wilson DS (1992) The prerequisites of strategic behavior in the bluegill sunfish. Anim Behav 44:223–230

    Google Scholar 

  44. Durán E, Ocana FM, Gómez A, Jiménez-Moya F, Broglio C, Rodríguez F (2008) Telencephalon ablation impairs goldfish allocentric spatial learning in a “hole-board” task. Acta Neurobiol Exp 68:519–525

    Google Scholar 

  45. Durán E, Ocana FM, Broglio C, Rodríguez F, Salas C (2010) Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a “hole-board” task. Behav Brain Res 214:480–487

    PubMed  Google Scholar 

  46. Ebbesson SOE (1972) New insights into the organization of the shark brain. Comp Biochem Physiol 42:121–129

    CAS  Google Scholar 

  47. Ebbesson SOE (1980) On the organization of the telencephalon in elasmobranchs. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 1–16

    Google Scholar 

  48. Ebbesson LOE, Braithwaite VA (2012) Environmental effects on fish neural plasticity and cognition. J Fish Biol 81:2151–2174

    CAS  PubMed  Google Scholar 

  49. Economakis AE, Lobel PS (1998) Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fish 51:129–139

    Google Scholar 

  50. Edren SMC, Gruber SH (2005) Homing ability of young lemon sharks, Negaprion brevirostris. Environ Biol Fish 72:267–281

    Google Scholar 

  51. Finger T (2008) Sorting food from stones: the vagal taste system in goldfish, Carassius auratus. J Comp Physiol A 194:135–143

    Google Scholar 

  52. Flood NC, Overmier JB, Savage GE (1976) Teleost telencephalon and learning: an interpretive review of data and hypotheses. Physiol Behav 16:783–798

    CAS  PubMed  Google Scholar 

  53. Font E, García-Verdugo JM, Desfilis E, Pérez-Cañellas M (1995) Neuron-glia interrelations during 3-acetylpyridine-induced degeneration and regeneration in the adult lizard brain. In: Vernadakis A, Roots B (eds) Neuron-glia interrelations during phylogeny: II. Plasticity and regeneration. Humana, Totowa, pp 275–302

    Google Scholar 

  54. Fricke H (1971) Fische als Feinde tropischer Seeigel. Mar Biol 9:328–338

    Google Scholar 

  55. Fricke H (1974) Ökoethologie des monogamen Anemonenfisches Amphiprion bicincthus. Z Tierpsychol 36:429–512

    CAS  PubMed  Google Scholar 

  56. Fukumori K, Okuda N, Yamaoka K, Yanagisawa Y (2009) Remarkable spatial memory in a migratory cardinal fish. Anim Cogn 13:385–389

    PubMed  Google Scholar 

  57. Fuss T, Bleckmann H, Schluessel V (2014a) Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus). J Comp Physiol A 200:37–52

    Google Scholar 

  58. Fuss T, Bleckmann H, Schluessel V (2014b) The shark Chiloscyllium griseum can orient using turn responses before and after partial telencephalon ablation. J Comp Physiol A 200:19–35

    Google Scholar 

  59. Fuss T, Bleckmann H, Schluessel V (2014c) Visual discrimination abilities in grey bamboo sharks (Chiloscyllium griseum). Zoology 117:104–111

    PubMed  Google Scholar 

  60. Fuss T, Bleckmann H, Schluessel V (2014d) The brain creates illusions not just for us: turns out sharks (Chiloscyllium griseum) can ‘see the magic’ as well. Front Neural Circuits 8:24. doi:10.3389/fncir.2014.00024

    PubMed Central  PubMed  Google Scholar 

  61. Gierszewski S, Bleckmann H, Schluessel V (2013) Cognitive abilities in Malawi cichlids (Pseudotropheus sp.): matching-to-sample and image/mirror-image discriminations. PLoS One 8:e57363

    CAS  PubMed Central  PubMed  Google Scholar 

  62. Giurfa M (2013) Cognition with few neurons: higher-order learning in insects. Trends Neurosci 36:285–294

    CAS  PubMed  Google Scholar 

  63. Goldman M, Shapiro S (1979) Matching-to-sample and oddity-from-sample in goldfish. J Exp Anal Behav 31:259–266

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Goldsmith M (1914) Les reactions physiologiques et psychiques des poisson. Bull Inst Gen Psychol 14:97–228

    Google Scholar 

  65. Graeber RC (1978) Behavioral studies correlated with central nervous system integration of vision in sharks. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates, and rays. Office of Naval Research, Arlington, pp 195–226

    Google Scholar 

  66. Graeber RC (1980) Telencephalic function in elasmobranchs, a behavioral perspective. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 17–39

    Google Scholar 

  67. Graeber RC, Ebbesson SO (1972) Visual discrimination learning in normal and tectal-ablated nurse sharks (Ginglymostoma cirratum). Comp Biochem Physiol 42:131–139

    CAS  Google Scholar 

  68. Graeber RC, Ebbesson SO, Jane JA (1973) Visual discrimination in sharks without optic tectum. Science 180:413–415

    CAS  PubMed  Google Scholar 

  69. Graeber RC, Schroeder DM, Jane JA, Ebbesson SOE (1978) Visual discrimination following partial telencephalic in nurse sharks (Ginglymostoma cirratum). J Comp Neurol 180:325–344

    CAS  PubMed  Google Scholar 

  70. Griffith SW, Magurran AE (1997) Familiarity in schooling fish: how long does it take to acquire? Anim Behav 53:945–949

  71. Griffith SW, Ward AJW (2006) Learned recognition of conspecifics. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Blackwell Publishing Ltd, Oxford, pp 139–165

    Google Scholar 

  72. Grill HJ, Norgren R (1978) Neurological tests and behavioral deficits in chronic thalamic and chronic decerebrate rats. Brain Res 142:299–312

    Google Scholar 

  73. Grosenick L, Clement TS, Fernald RS (2007) Fish can infer social rank by observation alone. Nature 445:429–432

    CAS  PubMed  Google Scholar 

  74. Gruber SH, Cohen JL (1978) Visual systems of the elasmobranchs: state of the art 1960-1975. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates, and rays. US Government Printing Office, Washington, pp 11–116

    Google Scholar 

  75. Gruber SH, Schneiderman N (1975) Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris). Behav Res Methods lnstrum 7:430–434

    Google Scholar 

  76. Guttridge TL, Brown C (2014) learning and memory in the Port Jackson shark, Heterodontus portusjacksoni. Anim Cogn 17:415–425

    PubMed  Google Scholar 

  77. Guttridge TL, Gruber SH, Gledhill KS, Croft DP, Sims DW, Krause J (2009a) Social preferences of juvenile lemon sharks Negaprion brevirostris. Anim Behav 78:543–548

    Google Scholar 

  78. Guttridge TL, Myrberg AM, Porcher IF, Sims DM, Krause J (2009b) The role of learning in shark behavior. Fish Fish 10:450–469

    Google Scholar 

  79. Guttridge TL, Gruber SH, DiBattista JD, Feldheim KA et al (2011) Assortative interactions and leadership in a wild population of juvenile lemon sharks. Mar Ecol Prog Ser 423:235–245

    Google Scholar 

  80. Guttridge TL, van Dijk S, Stamhuis EJ, Krause J, Gruber SH, Brown C (2013) Social learning in juvenile lemon sharks Negaprion brevirostris. Anim Cogn 16:55–64

    PubMed  Google Scholar 

  81. Heiligenberg W (1986) Jamming avoidance responses. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–649

    Google Scholar 

  82. Helfman GS, Schultz ET (1984) Social transmission of behavioral traditions in a coral-reef fish. Anim Behav 32:379–384

    Google Scholar 

  83. Herold C, Joshi I, Chehadi O, Hollmann M, Güntürkün O (2012) Plasticity in D1-like receptor expression is associated with different components of cognitive processes. PLoS One 7:e36484

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Herter K (1929) Dressurversuche an Fischen. Z vgl Physiol 10:688–711

    Google Scholar 

  85. Herter K (1930) Weitere Dressurversuche an Fische. Z vgl Physiol 11:730–748

    Google Scholar 

  86. Heupel MR, Simpfendorfer CA (2005) Quantitative analysis of aggregation behaviour in juvenile blacktip sharks. Mar Biol 147:1239–1249

    Google Scholar 

  87. Hofmann MH (2001) The role of the fish telencephalon in sensory information processing. In: Kapoor BG, Hara TJ (eds) Sensory biology of jawed fishes: new insights. Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, pp 255–274

  88. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 325–368

    Google Scholar 

  89. Hughes RN, Blight CM (2000) Two intertidal fish species use visual association learning to track the status of food patche in a radial maze. Anim Behav 59:613–621

    PubMed  Google Scholar 

  90. Jackson RL, Alexander J, Maier SF (1980) Learned helplessness, inactivity, and associative deficits: effects of inescapable shock on response choice escape learning. J Exp Psychol Anim Behav Proc 6:1–20

    CAS  Google Scholar 

  91. Jacoby DMP, Busawon DS, Sims DW (2010) Sex and social networking: the influence of male presence on social structure of female sharkgroups. Behav Ecol 21:808–818

    Google Scholar 

  92. Johnsson JI, Akerman A (1999) Watch and learn: preview of the fighting ability of opponents alters contest behaviour in rainbow trout. Anim Behav 56:771–776

    Google Scholar 

  93. Jones A, Brown C, Gardener S (2011) Tool use in the spotted tuskfish, Choerodon schoenleinii. Coral Reefs 30:865

    Google Scholar 

  94. Kaas JH (1987) The organization of the neocortex in mammals—implications for theories of brain function. Annu Rev Psychol 38:129–151

    CAS  PubMed  Google Scholar 

  95. Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science. McGraw-Hill, New York

    Google Scholar 

  96. Kanizsa G (1974) Contours without gradients or cognitive contours? G Ital Psicol 1:93–113

    Google Scholar 

  97. Karplus I, Algom D (1981) Visual cues for predator face recognition by reef fishes. J Comp Ethol 55:343–364

    Google Scholar 

  98. Karplus I, Goren M, Algom D (1982) A preliminary experimental-analysis of predator face recognition by Chromis-caeruleus (Pisces, Pomacentridae). J Comp Ethol 58:53–65

    Google Scholar 

  99. Karten HJ (2013) Neocortical evolution: neuronal circuits arise independently of lamination. Curr Biol 23:R12–R15

    CAS  PubMed  Google Scholar 

  100. Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark, Heterodontus francisci. J Acoust Soc Am 58:905–909

    CAS  PubMed  Google Scholar 

  101. Kendal JR, Rendell LR, Pike TW, Laland KN (2009) Nine-spined sticklebacks deploy a hill-climbing social learning strategy. Behav Ecol 20:238–244

    Google Scholar 

  102. Kimber JA, Sims DW, Bellamy PH, Gill AB (2011) The ability of a benthic elasmobranch to discriminate between biological and artificial electric fields. Mar Biol 158:1–8

    Google Scholar 

  103. Kimber JA, Sims DW, Bellamy PB, Gill AB (2014) Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Anim Cogn 17:55–65

    PubMed  Google Scholar 

  104. Kleerekoper H, Timms AM, Westlake GF, Davy FB, Malar T, Anderson VM (1970) An analysis of locomotor behaviour of goldfish (Carassius auratus). Anim Behav 18:317–330

    CAS  PubMed  Google Scholar 

  105. Kleerekoper H, Matis I, Gensler P, Maynard P (1974) Exploratory behaviour of goldfish Carassius auratus. Anim Behav 22:124–132

    Google Scholar 

  106. Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna Lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic-field. Mar Biol 117:1–22

    Google Scholar 

  107. Klimley AP, Nelson DR (1981) Schooling of the scalloped hammerhead shark, Sphyrna lewini, in the Gulf of California. Fish Bull 79:356–360

    Google Scholar 

  108. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351. doi:10.1371/journal.pbio.1000351

    PubMed Central  PubMed  Google Scholar 

  109. Kuba MJ, Byrne RA, Burghardt GM (2009) A new method for studying problem solving and tool use in stingrays (Potamotrygon castexi). Anim Cogn 13:507–513

    PubMed  Google Scholar 

  110. Laland KN, Williams K (1997) Shoaling generales social learning of foraging information in guppies. Anim Behav 53:1161–1169

    PubMed  Google Scholar 

  111. Lefebvre L (2013) Brains, innovations, tools and cultural transmission in birds, non-human primates, and fossil hominins. Front Hum Neurosci 7:245

    PubMed Central  PubMed  Google Scholar 

  112. Leung B, Forbes MR (1996) Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3:400–413

    Google Scholar 

  113. Lopez JC, Broglio C, Rodriguez F, Thinus-Blanc C, Salas C (2000) Reversal learning deficit in a spatial task but not in a cued one after telencephalic ablation in goldfish. Behav Brain Res 109:91–98

    CAS  PubMed  Google Scholar 

  114. López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (1999) Multiple spatial learning strategies in goldfish (Carassius auratus). Anim Cogn 2:109–120

    Google Scholar 

  115. Lucas JR, Brodin A, de Kort SR, Clayton NS (2004) Does hippocampal size correlate with the degree of caching specialisation? Proc R Soc Lond B 271:2423–2429

    Google Scholar 

  116. Malyukova IV, Rakich L, Kovachevich N (1983) Conditioned motor reactions in free-living elasmobranchs and bony fishes. Neurosci Behav Physiol 13:482–485

    CAS  PubMed  Google Scholar 

  117. Maren S, Holt WG (2004) Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. Behav Neurosci 118:97–110

    PubMed  Google Scholar 

  118. Martínez-García F, Novejarque A, Lanuza E (2009) The evolution of the amygdala in vertebrates. In: Kaas J (ed) Evolutionary neuroscience. Elsevier, Amsterdam, pp 407–458

    Google Scholar 

  119. Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201

    Google Scholar 

  120. Mazeroll AL, Montgomery WL (1995) Structure and organization of local migrations in brown surgeonfish (Acanthurus nigrofuscus). Ethology 99:89–106

    Google Scholar 

  121. Mazzi D, Künzler R, Bakker TCM (2003) Female preference for symmetry in computer-animated three-spined sticklebacks, Gasterosteus aculeatus. Behav Ecol Sociobiol 54:156–161

    Google Scholar 

  122. Mazzi D, Künzler R, Largiadèr CR, Bakker TCM (2004) Inbreeding affects female preference for symmetry in computer-animated sticklebacks. Behav Genet 34:417–424

    PubMed  Google Scholar 

  123. McManus MW, Johnson CS, Jeffries MM (1984) Training nurse sharks using operant conditioning. Naval Ocean systems Center Tech Rep No 977

  124. Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13:758–768

    CAS  PubMed  Google Scholar 

  125. Merry JW, Morris MR (2001) Preference for symmetry in swordtail fish. Anim Behav 61:477–479

    Google Scholar 

  126. Mervis CB, Rosch E (1981) Categorization of natural objects. Annu Rev Psychol 32:89–115

    Google Scholar 

  127. Meyer CG, Holland K, Papastamatiou YP (2005) Sharks can detect changes in the geomagnetic field. J R Soc Interface 2:129–130

    PubMed Central  PubMed  Google Scholar 

  128. Meyer CC, Papastamatiou YP, Holland KN (2010) A multiple instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii. Mar Biol 157:1857–1868

    Google Scholar 

  129. Milinski M, Pfluger D, Kulling D, Kettler R (1990a) Do sticklebacks cooperate repeatedly in reciprocal pairs. Behav Ecol Sociobiol 27:17–21

    Google Scholar 

  130. Milinski M, Kuelling D, Kettler R (1990b) Tit for Tat: sticklebacks (Gasterosteus aculeatus) “trusting” a cooperating partner. Behav Ecol 1:7–11

    Google Scholar 

  131. Moreno N, Gonzalez A (2007) Regionalization of the telencephalon in urodele amphibians and its bearing on the identification of the amygdaloid complex. Front Neuroanat 1:1–12

    PubMed Central  PubMed  Google Scholar 

  132. Morris MR, Casey K (1998) Female swordtail fish prefer symmetrical sexual signal. Anim Behav 55:33–39

    PubMed  Google Scholar 

  133. Mueller T, Wullimann MF (2009) An evolutionary interpretation of teleost forebrain anatomy. Brain Behav Evol 74:30–42

    PubMed  Google Scholar 

  134. Mueller T, Wullimann MF, Guo S (2008) Early teleostean basal ganglia development visualized by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression. J Comp Neurol 507:1245–1257

    CAS  PubMed  Google Scholar 

  135. Myrberg AA, Gruber AH (1974) Behavior of bonnethead shark, Sphyrna tiburo. Copeia 1974:358–374

    Google Scholar 

  136. Myrberg AA, Riggio RJ (1985) Acoustically mediated individual recognitions by a coral-reef fish (Pomacentrus-partitus). Anim Behav 33:411–416

    Google Scholar 

  137. Nams VO (2006) Detecting oriented movement of animals. Anim Behav 72:1197–1203

    Google Scholar 

  138. Nelson DR (1967) Hearing thresholds, frequency discriminations and acoustic orientation in the lemon shark, Negaprion brevirostris (Poey). Bull Mar Sci 17:741–768

    Google Scholar 

  139. Nieder A (2002) Seeing more than meets the eye: processing of illusory contours in animals. J Comp Physiol A 188:249–260

    CAS  Google Scholar 

  140. Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429

    Google Scholar 

  141. Northcutt R (1978) Brain organization in the cartilaginous fishes. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office of Naval Research, Arlington, pp 117–193

    Google Scholar 

  142. Northcutt RG (2011) Do teleost fish possess a homolog of mammalian isocortex? Brain Behav Evol 78:136–138

    PubMed  Google Scholar 

  143. O’Connell CP, Abel DC, Gruber SH et al (2011) Response of juvenile lemon sharks, Negaprion brevirostris, to a magnetic barrier simulating a beach net. Ocean Coast Manag 54:225–230

    Google Scholar 

  144. O’Gower AK (1995) Speculations on a spatial memory for the Port Jackson shark (Heterodontus portusjacksoni) (Meyer) (Heterodontidae). Mar Freshw Res 46:861–871

    Google Scholar 

  145. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford

    Google Scholar 

  146. Odling-Smee L, Braithwaite VA (2003a) The role of learning in fish orientation. Fish Fish 4:235–246

    Google Scholar 

  147. Odling-Smee L, Braithwaite VA (2003b) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65:701–707

    Google Scholar 

  148. Odling-Smee LC, Simpson SD, Braithwaite VA (2006) The role of learning in fish orientation. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Blackwell, Oxford, pp 166–185

    Google Scholar 

  149. Odling-Smee LC, Bouhman JW, Braithwaite VA (2008) Sympatic species of threespine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62:1935–1945

    Google Scholar 

  150. Papastamatiou YP, Cartamil DP, Lowe CG, Meyer CG, Wetherbee BM, Holland KN (2011) Scales of orientation, directed walks and movement path structure in sharks. J Anim Ecol 80:864–874

    PubMed  Google Scholar 

  151. Paśko K (2010) Tool-like behavior in the sixbar wrasse, Thalassoma hardwicke (Bennett, 1830). Zoo Biol 29:767–773

    PubMed  Google Scholar 

  152. Pike TT, Kendal JR, Rendell LE, Laland KN (2010) Learning by proportional observation in a species of fish. Behav Ecol 21:570–575

    Google Scholar 

  153. Pollen AA, Dobberfuhl AP, Scarce J, Igulu MM, Renn SCP, Shumway CA, Hofmann HA (2007) Environmental complexity and social organization sculpt the brain in Lake Tangayikan cichlid fish. Brain Behav Evol 70:21–39

    PubMed  Google Scholar 

  154. Portavella M, Vargas JP (2005) Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems. Eur J Neurosci 21:2800–2806

    PubMed  Google Scholar 

  155. Portavella M, Vargas JP, Torres B, Salas C (2002) The effects of telencephalic pallial lesions on spatial, temporal and emotional learning in goldfish. Brain Res Bull 57:397–399

    CAS  PubMed  Google Scholar 

  156. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JLR (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr 1. J Comp Neurol 424:409–438

    CAS  PubMed  Google Scholar 

  157. Puelles L, Harrison M, Paxinos G, Watson C (2013) A developmental ontology for the mammalian brain based on the prosomeric model. Trends Neurosci 36:570–578

    CAS  PubMed  Google Scholar 

  158. Rasmussen LEL, Schmidt MJ (1992) Are sharks chemically aware of crocodiles? In: Doty RL, Müller-Schwarze D (eds) Chemical signals in vertebrates IV. Plenum Press, New York, pp 335–342

    Google Scholar 

  159. Reese ES (1989) Orientation behavior of butterflyfishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps. Dev Environ Biol Fish 9:79–86

    Google Scholar 

  160. Reiner A (2004) Avian brain nomenclature consortium. Revised nomenclature for avian telencephalon some related brainstem nuclei. J Comp Neurol 473:377–414

    PubMed Central  PubMed  Google Scholar 

  161. Rensch B (1957) Ästhetische Faktoren bei Farb- und Formbevorzugungen von Affen. Z Tierpsychol 14:71–99

    Google Scholar 

  162. Rensch B (1958) Die Wirksamkeit ästhetischer Faktoren bei Wirbeltieren. Z Tierpsychol 15:447–461

    Google Scholar 

  163. 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 22:409–420

    Google Scholar 

  164. Rodriguez F, Broglio C, Durán E, Gómez Y, Salas C (2006) Neural mechanisms of learning in teleost fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Blackwell, Oxford, pp 243–277

    Google Scholar 

  165. Rodríguez I, Gumbert A, de Ibarra NH, Kunze J, Giurfa M (2004) Symmetry is in the eye of the beeholder: innate preference for bilateral symmetry in flower-naïve bumblebees. Naturwiss 91:374–377

    PubMed  Google Scholar 

  166. Rodriguez-Moldes I (2009) A developmental approach to forebrain organization in elasmobranchs: new perspectives on the regionalization of the telecephalon. Brain Behav Evol 74:20–29

    PubMed  Google Scholar 

  167. Roitblatt HL, Tham W, Golub L (1982) Performance of Betta splendens in a radial arm maze. Anim Learn Behav 10:108–114

    Google Scholar 

  168. Roth G, Grunwald S, Mühlenbrock-Lentner S (2004) Morphology and axonal projection pattern of neurons in the telencephalon of the fire-bellied toad Bombina orientalis. J Comp Neurol 478:35–61

    PubMed  Google Scholar 

  169. Saigusa T, Tero A, Nakagaki T, Kuramoto Y (2008) Amoebae anticipate periodic events. Phys Rev Lett 100:018101

  170. Salas C, Broglio C, Rodriguez F, Lopez JC, Portavella M, Torres B (1996a) Telencephalic ablation in goldfish impairs performance in a ‘spatial constancy’ problem but not in a cued one. Behav Brain Res 79:193–200

    CAS  PubMed  Google Scholar 

  171. Salas C, Rodriguez F, Vargas JP, Duran E, Torres B (1996b) Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. Behav Neurosci 110:965–980

    CAS  PubMed  Google Scholar 

  172. Salwiczek LH, Pretot L, Demarta L, Proctor D, Essler J, Pinto AL, Wismer S, Stoinski T, Brosnan SF, Bshary R (2012) Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner–clint reef fish cooperation. PLOS One 7:e49068

    CAS  PubMed Central  PubMed  Google Scholar 

  173. Sanders MJ, Wiltgen BJ, Fanselow MS (2003) The place of the hippocampus in fear conditioning. Eur J Pharmacol 463:217–223

    CAS  PubMed  Google Scholar 

  174. Schluessel V, Bleckmann H (2005) Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. J Comp Physiol A 191:695–706

    Google Scholar 

  175. Schluessel V, Bleckmann H (2012) Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zoology 115:346–353

    PubMed  Google Scholar 

  176. Schluessel V, Fricke G, Bleckmann H (2012) Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Anim Cogn 15:525–537

    CAS  PubMed  Google Scholar 

  177. Schluessel V, Kraniotakes H, Bleckmann H (2014a) Visual discrimination of rotated 3D objects in Malawi Cichlids (Pseudotropheus sp.): a first indication for form constancy in fishes. Anim Cogn 17:359–371

    CAS  PubMed  Google Scholar 

  178. Schluessel V, Beil O, Weber T, Bleckmann H (2014b) Symmetry perception in sharks (Chiloscyllium griseum) and cichlids (Pseudotropheus sp.). Anim Cogn. doi:10.1007/s10071-014-0751-2

    Google Scholar 

  179. Schlupp D, Ryan MJ (1997) Male sailfin mollies (Poecilia latipinna) copy the mate choice of other males. Behav Ecol 8:104–107

    Google Scholar 

  180. Schuster S, Rossel S, Schmidtmann A, Jäger I, Piralla J (2004) Archer fish learn to compensate for complex optical distortions to determine the absolute size of their aerial prey. Curr Biol 14:1565–1568

    CAS  PubMed  Google Scholar 

  181. Schuster S, Wöhl S, Griebsch M, Klostermeier I (2006) Animal cognition: how archer fish learn to down rapidly moving targets. Curr Biol 16:378–383

    CAS  PubMed  Google Scholar 

  182. Schwarze S, Bleckmann H, Schluessel V (2013) Avoidance conditioning in bamboo sharks (Chiloscyllium punctatum and C. griseum): behavioural and neuroanatomical aspects. J Comp Physiol A 199:843–856

    Google Scholar 

  183. Segall MH, Campbell LT, Herskovits MJ (1966) The influence of culture on visual perception. Bobbs-Merrill, Indianapolis

    Google Scholar 

  184. Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317

    CAS  PubMed  Google Scholar 

  185. Sherry DF, Jacobs LF, Gaulin SJC (1992) Spatial memory and adaptive specialisation of the hippocampus. Trends Neurosci 15:298–303

    CAS  PubMed  Google Scholar 

  186. Shettleworth SJ (2010) Clever animals and killjoy explanations in comparative psychology. Trends Cogn Sci 14:477–481

    PubMed  Google Scholar 

  187. Shumway CA (2008) Habitat complexity, brain, and behavior. Brain Behav Evol 72:123–134

    PubMed  Google Scholar 

  188. Siciliano AM, Kajiura SM, Long JH Jr, Porter ME (2013) Are you positive? Electric dipole polarity discrimination in the yellow stingray Urobatis jamaicensis. Biol Bull 225:85–91

    PubMed  Google Scholar 

  189. Siebeck UE, Litherland L, Wallis GM (2009) Shape learning and discrimination in reef fish. J Exp Biol 212:2113–2119

    CAS  PubMed  Google Scholar 

  190. Sims DW, Southall EJ, Richardson AJ, Reid PC, Metcalfe JD (2003) Seasonal movements and behaviour of basking sharks from archival tagging: no evidence of winter hibernation. Mar Ecol Prog Ser 248:187–196

    Google Scholar 

  191. Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Structure and functional correlations. Springer, Berlin

    Google Scholar 

  192. Sovrano VA, Bisazza A (2008) Recognition of partly occluded objects by fish. Cognition 11:161–166

    Google Scholar 

  193. Sovrano VA, Bisazza A (2009) Perception of subjective contours in fish. Perception 38:479–490

    Google Scholar 

  194. Sovrano VA, Bisazza A, Vallortigara G (2002) Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish. Cognition 85:B51–B59

    PubMed  Google Scholar 

  195. Sovrano VA, Bisazza A, Vallortigara G (2007) How fish do geometry in large and in small spaces. Cognition 10:47–54

    Google Scholar 

  196. Spaet JLY, Kessel ST, Gruber SH (2010) Learned hook avoidance of lemon sharks (Negaprion brevirostris) based on electroreception and shock treatment. Mar Biol Res 6:399–407

    Google Scholar 

  197. Spinozzi G (1996) Categorization in monkeys and chimpanzees. Behav Brain Res 74:17–24

    CAS  PubMed  Google Scholar 

  198. Squire L (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177

    PubMed  Google Scholar 

  199. Srinivasan MV (2010) Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol 55:267–284

    CAS  PubMed  Google Scholar 

  200. Striedter GF (1997) The telencephalon of tetrapods in evolution. Brain Behav Evol 49:179–213

    CAS  PubMed  Google Scholar 

  201. Suboski MD, Bain S, Carty AE, McQuoid LM, Seelen MI, Seifert M (1990) Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio). J Comp Psychol 104:101–112

    Google Scholar 

  202. Sundström LF, Gruber SH, Clermont SM, Correia JPS, de Marignac JRC, Morrissey JF, Lowrance CR, Thomassen L, Oliveira MT (2001) Review of elasmobranch behavioral studies using ultrasonic telemetry with special reference to the lemon shark, Negaprion brevirostris, around Bimini Islands, Bahamas. Environ Biol Fish 60:225–250

    Google Scholar 

  203. Tarrant RM (1964) Rate of extinction of a conditional response in juvenile sockeye salmon. Trans Am Fish Soc 93:399–401

    Google Scholar 

  204. Tester A, Kato S (1966) Visual target discrimination in blacktip sharks (Carcharhinus melanopterus) and grey sharks (C. menisorrah). Pac Sci 20:461–471

    Google Scholar 

  205. Teyke T (1989) Learning and remembering the environment in the blind cave fish Anoptichthys jordani. J Comp Physiol A 164:655–662

    Google Scholar 

  206. Thonhauser KE, Gutnick T, Byrne RA, Kral K, Burghardt GM, Kuba M (2013) Social learning in cartilaginous fish (stingrays Potamotrygon falkneri). Anim Cogn 16:927–932

    PubMed  Google Scholar 

  207. Thornton A, Clayton NS, Grodzinski U (2012) Animal minds: from computation to evolution. Philos Trans R Soc Lond B Biol Sci 367:2670–2676

    PubMed Central  PubMed  Google Scholar 

  208. Thünken T, Waitschyk N, Bakker TCM, Kullmann H (2009) Olfactory self-recognition in a cichlid fish. Anim Cogn 12:717–724

    PubMed  Google Scholar 

  209. Tigges M (1962) Muster- und Farbbevorzugung bei Fischen. Z Tierpsychol 20:129–142

    Google Scholar 

  210. Tricas TC, Sisneros JA (2004) Ecological functions and adaptations of the elasmobranch electrosense. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fish. Narosa Publishing house, pp 308–329

  211. Vargas JP, Lopez JC, Salas C, Thinus-Blanc C (2004) Encoding of geometric and featural spatial information by goldfish (Carassius auratus). J Comp Psychol 2:206–216

    Google Scholar 

  212. Vargas JP, López JC, Portavella M (2009) What are the functions of fish brain pallium? Brain Res Bull 79:436–440

    PubMed  Google Scholar 

  213. Vargas JP, Quintero E, López JC (2011) Influence of distal and proximal cues in encoding geometric information. Anim Cogn 14:351–358

    PubMed  Google Scholar 

  214. von der Emde G (1999) Active electrolocation of objects in weakly electric fish. J Exp Biol 202:1205–1215

    PubMed  Google Scholar 

  215. von der Emde G, Behr K, Bouton B, Engelmann J, Fetz S, Folde C (2010) 3-Dimensional scene perception during active electrolocation in a weakly electric pulse fish. Front Behav Neurosci 4:26

    PubMed Central  PubMed  Google Scholar 

  216. Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40:500–505

    Google Scholar 

  217. Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4:203–215

    Google Scholar 

  218. Ward AJW, Axford S, Krause J (2003) Cross-species familiarity in shoaling fish. Proc R Soc Lond B 270:1157–1161

    CAS  Google Scholar 

  219. Ware DM (1971) Predation by rainbow trout (Salmo gairdneri): the effect of experience. J Fish Res Board Can 28:1847–1852

    Google Scholar 

  220. Webster MM, Laland KN (2011) Reproductive state affects reliance on public information in sticklebacks. Proc R Soc B Biol Sci 278:619–627

    CAS  Google Scholar 

  221. White KG (2001) Forgetting functions. Anim Learn Behav 29:193–207

    Google Scholar 

  222. Wilkens LA, Hofmann MH, Wojtenek W (2002) The electric sense of the paddlefish: a passive system for the detection and capture of zooplankton prey. J Physiol 96:363–377

    Google Scholar 

  223. Wirtz P (1996) Werkzeuggebrauch bei Lippfischen. Aquarium Terrarium Z 1:4–5

    Google Scholar 

  224. Wood LS, Desjardins JK, Fernald R (2011) Effects of stress and motivation on performing in a spatial task. Neurobiol Learn Mem 95:277–285

    PubMed Central  PubMed  Google Scholar 

  225. Wright T, Jackson R (1964) Instrumental conditioning of young sharks. Copeia 1964:409–412

    Google Scholar 

  226. Wullimann MF (1997) The central nervous system. In: Evans DH (ed) Physiology of fishes. CRC Press, Boca Raton, pp 245–282

    Google Scholar 

  227. Wullimann MF, Mueller T (2004) Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143–162

    CAS  PubMed  Google Scholar 

  228. Wunder W (1934) Gattenwahlversuche bei Stichling und Bitterling. Dtsch Zool Ges 36:152–158

    Google Scholar 

  229. Wyzisk K (2005) Experimente zur Formen- und Größenwahrnehmung beim Goldfisch (Carassius auratus) unter Verwendung von Scheinkonturen und Größentäuschungen. PhD Thesis, Johannes Gutenberg Universität Mainz

  230. Wyzisk K, Neumeyer C (2007) Perception of illusory surfaces and contours in goldfish. Vis Neurosci 24:291–298

    PubMed  Google Scholar 

  231. Yopak KE (2012a) Neuroecology in cartilaginous fishes: the functional implications of brain scaling. J Fish Biol 80:1968–2023

    CAS  PubMed  Google Scholar 

  232. Yopak KE (2012b) The nervous system of cartilaginous fishes. Brain Behav Evol 80:77–79

    PubMed  Google Scholar 

  233. Yopak KE, Frank LR (2009) Brain size and brain organization of the whale shark, Rhincodon typus, using magnetic resonance imaging. Brain Behav Evol 74:121–142

    PubMed  Google Scholar 

  234. Yopak KE, Lisney TJ, Collin SP, Montgomery JC (2007) Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans. Brain Behav Evol 69:280–300

    PubMed  Google Scholar 

  235. Yue S, Moccia RD, Duncan IJH (2004) Investigating fear in domestic rainbow trout, (Oncorhynchus mykiss), using an avoidance learning task. Appl Anim Behav Sci 87:343–354

    Google Scholar 

  236. Zerbolio DJ, Royalty JL (1983) Matching and oddity conditional discrimination in the goldfish as avoidance responses: evidence for conceptual avoidance learning. Anim Learn Behav 11:341–348

    Google Scholar 

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Acknowledgments

I am grateful to H. Bleckmann and M. Mogdans for helpful suggestions on the manuscript.

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Schluessel, V. Who would have thought that ‘Jaws’ also has brains? Cognitive functions in elasmobranchs. Anim Cogn 18, 19–37 (2015). https://doi.org/10.1007/s10071-014-0762-z

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Keywords

  • Learning
  • Memory
  • Shark
  • Chondrichthyes
  • Rays