Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness?

Abstract

Elaborate cognitive skills arose independently in different taxonomic groups. Self-recognition is conventionally identified by the understanding that one’s own mirror reflection does not represent another individual but oneself, which has never been proven in any elasmobranch species to date. Manta rays have a high encephalization quotient, similar to those species that have passed the mirror self-recognition test, and possess the largest brain of all fish species. In this study, mirror exposure experiments were conducted on two captive giant manta rays to document their response to their mirror image. The manta rays did not show signs of social interaction with their mirror image. However, frequent unusual and repetitive movements in front of the mirror suggested contingency checking; in addition, unusual self-directed behaviors could be identified when the manta rays were exposed to the mirror. The present study shows evidence for behavioral responses to a mirror that are prerequisite of self-awareness and which has been used to confirm self-recognition in apes.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Amsterdam B (1972) Mirror image reactions before age two. Dev Psychobiol 5:297–305

    CAS  Article  PubMed  Google Scholar 

  2. Anderson JR (1986) Mirror-mediated finding of hidden food by monkeys (Macaca tonkeana and M. fasicularis). J Comp Psychol 100:237–242

    Article  Google Scholar 

  3. Ari C (2009) On the brain of cartilaginous fishes: cerebralization, astroglial architecture and blood-brain barrier composition. Lambert, Saarbrücken

    Google Scholar 

  4. Ari C (2011) Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives. Open Anat 3:1–13

    Article  Google Scholar 

  5. Ari C (2014) Rapid coloration changes of manta rays (Mobulidae). Biol J Linn Soc 113:180–193

    Article  Google Scholar 

  6. Ari C, Correia JP (2008) Role of sensory cues on the food searching behaviour of a captive Manta birostris (Myliobatiformes, Mobulidae). Zoo Biol 27(4):294–304

    Article  PubMed  Google Scholar 

  7. Balzarini V, Taborsky M, Wanner S, Koch F, Frommen J (2014) Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish. Behav Ecol Sociobiol 68:871–878

  8. Bekoff M, Sherman PW (2004) Reflections on animal selves. Trends Ecol Evol 19:176–180

    Article  PubMed  Google Scholar 

  9. Broglio C, Gómez A, Durán E, Salas C, Rodríguez F (2011) Brain and cognition in teleost fish. In: Brown C, Krause J, Laland K (eds) Fish cognition and behavior. Wiley, Oxford, pp 325–358

    Google Scholar 

  10. Brown C (2014) Fish intelligence, sentience and ethics. Anim Cogn 18:1

    Article  PubMed  Google Scholar 

  11. Chandroo KP, Yue S, Moccia RD (2004) An evaluation of current perspectives on consciousness and pain in fishes. Fish Fisheries 5:281–295

    Article  Google Scholar 

  12. Dawkins MS (2001) Who needs consciousness? Anim Welfare 10(Suppl1):19–29

    Google Scholar 

  13. de Veer M, van den Bos R (1999) A critical review of methodology and interpretation of mirror self-recognition research in non-human primates. Anim Behav 58:459–568

    Article  PubMed  Google Scholar 

  14. Delfour F, Marten K (2001) Mirror image processing in three marine mammal species: Killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus). Behav Process 53:181–190

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  16. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744–747

    Article  PubMed  PubMed Central  Google Scholar 

  17. Gallup GG (1970) Chimpanzees: self-recognition. Science 167:86–87

    Article  Google Scholar 

  18. Heyes CM (1994) Reflections on self-recognition in primates. Anim Behav 47:909–919

    Article  Google Scholar 

  19. Heyes CM (1998) Theory of mind in nonhuman primates. Behav Brain Sci 21:101–114

    CAS  PubMed  Google Scholar 

  20. Itakura S (1987) Mirror guided behavior in Japanese monkeys (Macaca fuscata fuscata). Primates 28:149–161

    Article  Google Scholar 

  21. Lethmate J, Ducker G (1973) Untersuchungen zum Selbsterkennen im Spiegel bei Orangutans und einigen anderen Affenarten. Z Tierpsychol 33:248–269

    CAS  Article  PubMed  Google Scholar 

  22. Marino L, Reiss D, Gallup G (1994) Mirror self-recognition in bottlenose dolphins: Implications for comparative investigations of highly dissimilar species. In: Parker S, Boccia M, Mitchell R (eds) Self-awareness in animals and humans: Developmental perspectives. Cambridge University Press, New York, pp 273–290

    Google Scholar 

  23. Miles HL (1994) Me Chantek: The development of self-awareness in a signing orangutan. In: Parker S, Boccia M, Mitchell R (eds) Self-awareness in animals and humans: Developmental perspectives. Cambridge University Press, New York, pp 254–272

    Google Scholar 

  24. Panksepp J (2005) Affective consciousness: core emotional feelings in animals and humans. Conscious Cogn 14:30–80

    Article  PubMed  Google Scholar 

  25. Patterson F, Cohn R (1994) Self-recognition and self-awareness in the lowland gorilla. In: Parker S, Boccia M, Mitchell R (eds) Self-awareness in animals and humans: Developmental perspectives. Cambridge University Press, New York, pp 273–290

    Google Scholar 

  26. Pepperberg IM, Garcia SE, Jackson EC, Marconi S (1995) Mirror use by African Grey parrots (Psittacus erithacus). J Comp Psychol 109:182–195

    Article  Google Scholar 

  27. Platek SM, Levin SL (2004) Monkeys, mirrors, mark tests, and minds. Trends Ecol Evol 19:406–407

    Article  PubMed  Google Scholar 

  28. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 103:17053–17057

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Povinelli DJ, Rulf AB, Landau K, Bierschwale DT (1993) Self-recognition in chimpanzees. J Comp Psychol 107:347–372

    CAS  Article  PubMed  Google Scholar 

  30. Povinelli DJ, Gallup GG, Eddy TJ, Bierschwale DT, Engstrom MC, Perilloux HK, Toxopeus IB (1997) Chimpanzees recognize themselves in mirrors. Anim Behav 53:1083–1088

    Article  Google Scholar 

  31. Prior H, Schwarz A, Güntürkün O (2008) Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition. PLoS Biol 6(8):e202. doi:10.1371/journal.pbio.0060202

    Article  PubMed  PubMed Central  Google Scholar 

  32. Reiss D (2012) The dolphin in the mirror: exploring dolphin minds and saving dolphin lives. Houghton Mifflin Harcourt, New York

  33. Reiss D, Marino L (2001) Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc Natl Acad Sci 98:5937–5942

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Sarko D, Marino L, Reiss D (2002) A bottlenose dolphin’s (Tursiops truncatus) responses to Its mirror image: further analysis. Int J Comp Psychol 15(1):69–76

    Google Scholar 

  35. Shettleworth SJ (2010) Cognition, evolution, and behaviour, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  36. Suddendorf T, Butler DL (2013) The nature of visual self-recognition. Trends Cogn Sci 17:121–127

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

    Article  PubMed  Google Scholar 

  38. Verbeek P, Iwamoto T, Murakami N (2007) Differences in aggression between wild-type and domesticated fighting fish are context dependent. Anim Behav 73:75–83

    Article  Google Scholar 

  39. Walraven V, van Elsacker L, Verheyen R (1995) Reactions of a group of pygmy chimpanzees (Pan paniscus) to their mirror images–evidence of self-recognition. Primates 36:145–150

    Article  Google Scholar 

  40. Whiten A, Byrne RW (1997) Machiavellian intelligence II: extensions and evaluations. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

This study was funded by the Save Our Seas Foundation. We are very grateful to Michelle Liu, Dave Wert and the staff of the Aquarium for the possibility and logistical support to conduct this research at the Atlantis Aquarium, Bahamas. The Divers Alert Network Europe and Dr. Huntington Potter provided essential support. The observations during this study were in compliance with all ethical standards and were approved by the Kerzner Marine Foundation and the Atlantis Aquarium, Bahamas. We thank three anonymous reviewers for their thoughtful comments on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Csilla Ari.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Movie 1: Manta ray is swimming through the OA in control conditions without the mirror. (WMV 3509 kb)

Movie 2: Manta ray is swimming through the OA in control conditions after the mirror has been removed. (WMV 2666 kb)

Movie 3: Manta rays perform repetitive turning, circling in front of the mirror. This behavior was performed for 6 min continously during this session. (WMV 4081 kb)

Movie 4: Manta ray rolls cephalic fin and slows down when passing in front of the mirror (9–13 s). (WMV 4840 kb)

Movie 5: Manta ray rolls cephalic fin in front of the mirror (1–3 s). Bubble blowing behavior is presented front of the mirror while displaying the ventral side and staying visually oriented (22–24 s). (WMV 4832 kb)

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ari, C., D’Agostino, D.P. Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness?. J Ethol 34, 167–174 (2016). https://doi.org/10.1007/s10164-016-0462-z

Download citation

Keywords

  • Self-recognition
  • Mirror test
  • Comparative cognition
  • Mobulidae
  • Cognition