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A social cichlid fish failed to pass the mark test

Abstract

Since the pioneering work in chimpanzees, mirror self-recognition (MSR), the ability to recognise oneself in a mirror, has been reported in great apes, Asian elephants, dolphins, and some social birds using the mark test, in which animals that possess MSR touch an imperceptible mark on their own bodies only when a mirror is present. However, giant pandas, which are solitary, failed to pass the mark test, suggesting that MSR evolved solely in highly social animals. In contrast to the increasing evidence of MSR in mammals and birds, little is known about MSR in fish. A Tanganyikan cichlid, Neolamprologus pulcher, is a good candidate for study because these fish live in highly social groups and recognise conspecifics about as rapidly as primates. We examined their responses to a mirror image and tested whether N. pulcher could pass the mark test. When the mirror was first exposed, they stayed in front of the mirror and exhibited aggressive behaviour towards the mirror image. These social behaviours suggested that the focal fish perceived the mirror image as an unfamiliar conspecific. The social responses decreased over the following days, as has generally been the case in animals with MSR. After mark injection, we found no increase in scraping behaviour or prolonged observation of the marked side. These results show a lack of contingency checking and mark-directed behaviours, meaning that N. pulcher failed to pass the mark test and did not recognise their self-image in the mirror.

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References

  1. Ari C (2011) Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives. Open Anat 3:1–13. https://doi.org/10.2174/1877609401103010001

    Article  Google Scholar 

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

    Article  Google Scholar 

  3. ASAB/ABS (2014) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 99:I–IX

    Google Scholar 

  4. Balzarini V, Taborsky M, Wanner S, Koch F, Frommen JG (2014) Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish. Behav Ecol Sociobiol 68:871–878. https://doi.org/10.1007/s00265-014-1698-7

    Article  Google Scholar 

  5. Bashine-Earn S, Neat FC, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behaviour in a cooperatively breeding fish. Behav Ecol 9:432–438. https://doi.org/10.1093/beheco/9.5.432

    Article  Google Scholar 

  6. Beckoff M, Sherman PW (2004) Reflections on animal selves. Trends Ecol Evol 19:176–180. https://doi.org/10.1016/j.tree.2003.12.010

    Article  Google Scholar 

  7. Brown C, Laland K, Krause J (2011) Fish cognition and behaviour. Wiley, Oxford

    Book  Google Scholar 

  8. Bshary R, Gingins S, Vail AL (2014) Social cognition in fishes. Trends Cogn Sci 18(9):465–471

    Article  PubMed  Google Scholar 

  9. Byrne RW (1995) The thinking ape: evolutionary origins of intelligence. Oxford University Press, Oxford

    Book  Google Scholar 

  10. Cattelan S, Lucon-Xiccato T, Pilastro A, Griggio M (2017) Is the mirror test a valid measure of fish sociability? Anim Behav 127:109–116. https://doi.org/10.1016/j.anbehav.2017.03.009

    Article  Google Scholar 

  11. Clary D, Kelly DM (2016) Graded mirror self-recognition by Clark’s nutcrackers. Sci Rep 6:36459. https://doi.org/10.1038/srep36459

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Cohen J (1988) Statistical power analysis for the behavioural sciences. Lawrence Earlbaum Associates, Hillside

    Google Scholar 

  13. de Veer MW, van den Bos R (1999) A critical review of methodology and interpretation of mirror self-recognition research in nonhuman primates. Anim Behav 58:459–468. https://doi.org/10.1006/anbe.1999.1166

    Article  PubMed  Google Scholar 

  14. Delfour F, Marten K (2001) Mirror image processing in three mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus). Behav Process 53:181–190. https://doi.org/10.1016/S0376-6357(01)00134-6

    CAS  Article  Google Scholar 

  15. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744–747. https://doi.org/10.1098/rsbl.2010.0247

    Article  PubMed  PubMed Central  Google Scholar 

  16. Devue C, Brédart S (2011) The neural correlates of visual self-recognition. Conscious Cognit 20:40–51. https://doi.org/10.1016/j.concog.2010.09.007

    Article  Google Scholar 

  17. Frederick JL (1997) Evaluation of fluorescent elastomer injection as a method for marking small fish. Bull Marine Sci 69:399–408

    Google Scholar 

  18. Furtbauer I, King AJ, Heistermann M (2015) Visible implant elastomer (VIE) tagging and simulated predation risk elicit similar physiological stress response in three-spined stickleback Gasterosteus aculeatus. J Fish Biol 86:1644–1649. https://doi.org/10.1111/jfb.12662

    CAS  Article  PubMed  Google Scholar 

  19. Gallup GG (1970) Chimpanzees: self-recognition. Science 167:86–87. https://doi.org/10.1093/oxfordhb/9780199548019.003.0004

    Article  Google Scholar 

  20. Gallup GG (1977) Absence of self-recognition in a monkey (Macaca fascicularis) following prolonged exposure to a mirror. Dev Psychobiol 10:281–284. https://doi.org/10.1002/dev.420100312

    Article  PubMed  Google Scholar 

  21. Gallup GG (1998) Self-awareness and the evolution of social intelligence. Behav Process 42:239–247. https://doi.org/10.1016/S0376-6357(97)00079-X

    Article  Google Scholar 

  22. Gallup GG, McClure MK, Hill SD, Bundy RA (1971) Capacity of self-recognition in differentially reared chimpanzees. Psychol Rec 21:69–74

    Article  Google Scholar 

  23. Gatto E, Lucon-Xiccato T, Savasci BB, Dadda M, Bisazza A (2017) Experimental setting affects the performance of guppies in a numerical discrimination task. Anim Cogn 20:187–198. https://doi.org/10.1007/s10071-016-1037-7

    Article  PubMed  Google Scholar 

  24. Gonzalez-Voyer A, Winberg S, Kolm N (2009) Social fishes and single mothers: brain evolution in African cichlids. Proc R Soc B Biol Sci 276:161–167. https://doi.org/10.1098/rspb.2008.0979

    Article  Google Scholar 

  25. Groenewoud F, Frommen JG, Josi D, Tanaka H, Jungwirth A, Taborsky M (2016) Predation risk drives social complexity in cooperative breeders. Proc Natl Acad Sci USA 113:4104–4109. https://doi.org/10.1073/pnas.1524178113

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Horowitz A (2017) Smelling themselves: dogs investigate their own odours longer when modified in an “olfactory mirror” test. Behav Processes 143:17–24. https://doi.org/10.1016/j.beproc.2017.08.001

    Article  PubMed  Google Scholar 

  27. Jerison HJ, Jerison I (1988) The evolutionary biology of intelligence. Nato ASI series in ecology. Springer, New York

    Book  Google Scholar 

  28. Kohda M, Jordan LA, Hotta T, Kosaka N, Karino K, Tanaka H, Taniyama M, Takeyama T (2015) Facial recognition in a group-living cichlid. PLoS ONE 10:e0142552. https://doi.org/10.1371/journal.pone.0142552

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kroeger RHH, Bowmaker JK, Wagner HJ (1999) Morphological changes in the retina of Aequidens pulcher (Cichlidae) after rearing in monochromatic light. Vision Res 39:2411–2448. https://doi.org/10.1016/S0042-6989(98)00256-9

    Article  Google Scholar 

  30. Kusayama T, Ikeda Y, Irie N, Chin H, Tsubokawa T, Takeno J, Sakai M (2012) Reminiscences about mirror self-recognition. Jpn J Anim Psychol 62:111–124. https://doi.org/10.2502/janip.62.1.9

    Article  Google Scholar 

  31. Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246. https://doi.org/10.1159/000076784

    Article  PubMed  Google Scholar 

  32. Lucon-Xiccato T, Bisazza A (2017) Individual differences in cognition among teleost fishes. Behav Process 141:184–195. https://doi.org/10.1016/j.beproc.2017.01.015

    Article  Google Scholar 

  33. Ma X, Jin Y, Luo B, Zhang G, Wei R, Liu D (2015) Giant pandas failed to show mirror self-recognition. Anim Cogn 18:713–721. https://doi.org/10.1007/s10071-015-0838-4

    Article  PubMed  Google Scholar 

  34. Mitchell RW (1997) A comparison of the self-awareness and kinesthetic–visual matching theories of self-recognition: autistic children and others. Ann New York Acad Sci 818:39–62. https://doi.org/10.1111/j.1749-6632.1997.tb48245.x

    Article  Google Scholar 

  35. Moretz JA, Martins EP, Robinson BD (2006) The effects of early and adult social environment on zebrafish (Danio rerio) behaviour. Environ Biol Fishes 80:91–101. https://doi.org/10.1007/s10641-006-9122-4

    Article  Google Scholar 

  36. Mousavi SM, Nasab EM, Yavari V, Ghatrami ER, Jalali MR (2012) Effects of two anaesthetic regimes, MS-222 and eugenol, on plasma biochemical profile in Barbus sharpeyi. Comp Clin Pathol 21:859–863. https://doi.org/10.1007/s00580-011-1189-4

    CAS  Article  Google Scholar 

  37. Oliveira RF, La C, Canario AVM (2005) Behavioural endocrinology: no hormonal response in tied fights. Nature 437:207–208. https://doi.org/10.1038/437207a

    CAS  Article  PubMed  Google Scholar 

  38. Parker ST, Mitchell RW, Boccia ML (1994) Self-awareness in animals and humans: developmental perspectives. Cambridge University Press, New York

    Book  Google Scholar 

  39. Parry JWL, Carleton KL, Spady T, Carboo A, Hunt DM, Bowmaker JK (2005) Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in Lake Malawi Cichlids. Curr Biol 15:1734–1739. https://doi.org/10.1016/j.cub.2005.08.010

    CAS  Article  PubMed  Google Scholar 

  40. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 103:17053–17057. https://doi.org/10.1073/pnas.0608062103

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Premack D, Woodruff G (1978) Does the chimpanzee have a theory of mind? Behav Brain Sci 1:515–526. https://doi.org/10.1017/S0140525X00076512

    Article  Google Scholar 

  42. Pretot L, Bshary R, Brosnan SF (2016) Comparing species decisions in a dichotomous choice task: adjusting task parameters improves performance in monkeys. Anim Cogn 19:819–834. https://doi.org/10.1007/s10071-016-0981-6

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  44. Reddon AR, O’Conner CM, Marsh-Rollo SE, Bakshine S (2012) Effects of isolation on social response in a cooperatively breeding fish. Anim Behav 84:753–760

    Article  Google Scholar 

  45. Reiss D, Marino L (2001) Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc Natl Acad Sci USA 98:5937–5942. https://doi.org/10.1037/pnas.101086398

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Riebli T, Taborsky M, Chervet N, Apolloni N, Zurcher Y, Heg D (2012) Behavioural type, status and social context affect behaviour and resource allocation in cooperatively breeding cichlids. Anim Behav 84:925–936. https://doi.org/10.1016/j.anbehav.2012.07.017

    Article  Google Scholar 

  47. 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 orang-utans in a complex foraging task derived from cleaner-client reef cooperation. PLoS ONE 7:e49068. https://doi.org/10.1371/journal.pone.0049068

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  49. Shillito DJ, Gallup GG, Beck B (1999) Factors affecting mirror behaviour in western lowland gorillas, Gorilla gorilla. Anim Behav 57:999–1004. https://doi.org/10.1006/anbe.1998.1062

    CAS  Article  PubMed  Google Scholar 

  50. Sogawa S, Ota K, Kohda M (2016) A dear enemy relationship in a territorial cichlid: evidence for the threat-level hypothesis. Behaviour 153:387–400. https://doi.org/10.1163/1568539X-00003351

    Article  Google Scholar 

  51. Soler M, Perez-Contreras T, Peralta-Sanchez JM (2014) Mirror-mark tests performed on jackdaws reveal potential methodological problems in the use of stickers in avian mark-test studies. PLoS ONE 9(1):e86193. https://doi.org/10.1371/journal.pone.0086193

    Article  PubMed  PubMed Central  Google Scholar 

  52. Stewart JD, Stevens GMW, Marshall GJ, Abernathy K (2017) Are mantas self aware or simply social? A response to Ari and D’Agostino 2016. J Ethol 35:145–147. https://doi.org/10.1007/s10164-016-0491-7

    Article  Google Scholar 

  53. Suarez SD, Gordon G, Gallup GG (1981) Self-recognition in chimpanzees and orangutans, but not gorillas. J Hum Evol 11:239–244. https://doi.org/10.1016/S0047-2484(81)80016-4

    Google Scholar 

  54. Suddendorf T, Butler DL (2013) The nature of visual self-recognition. Trends Cognit Sci 17:121–127. https://doi.org/10.1016/j.tics.2013.01.004

    Article  Google Scholar 

  55. Thunken T, Waltschyk N, Bakker TCM, Kullmann H (2009) Olfactory self-recognition in a cichlid fish. Anim Cogn 12:717–724. https://doi.org/10.1007/s10071-009-0231-2

    Article  PubMed  Google Scholar 

  56. Vollestad LA, Quinn TP (2003) Trade-off between growth rate and aggression in juvenile coho salmon, Oncorhynchus kisutch. Anim Behav 66:561–568. https://doi.org/10.1006/anbe.2003.2237

    Article  Google Scholar 

  57. Walraven 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. https://doi.org/10.1007/BF02381922

    Article  Google Scholar 

  58. Weber RA, Peleteiro JB, Garcia Martin LO, Aldegunde M (2009) The efficacy of 2-phenoxyethanol, metomidate, clove oil and MS-222 as anaesthetic agents in the Senegalese sole (Solea senegalensis Kaup 1858). Aquaculture 288:147–150. https://doi.org/10.1016/j.aquaculture.2008.11.024

    CAS  Article  Google Scholar 

  59. Wong M, Balshine S (2010) Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue. Biol Lett. https://doi.org/10.1098/rsbl.2010.0639

    PubMed Central  Google Scholar 

  60. Yang H (2005) On the uniqueness of self-face recognition. Psychol Sci 28:1517–1519

    Google Scholar 

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Acknowledgements

We thank the members of the Laboratory of Animal Sociology, Osaka City University, for their fruitful discussion regarding this work. This study was financially supported by KAKENHI (Nos. 16H05773 and 17K18712) to MK and (No. H16J09486) to TH from JSPS. The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, see: http://www.textcheck.com/certificate/index/R1wM76.

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Correspondence to Takashi Hotta.

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The authors declare that they have no conflict of interest.

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All experiments adhered to the Association for the Study of Animal Behaviours Guidelines for the Use of Animals in Research (ASAB/ABS 2014) and were conducted in compliance with the Regulations on Animal Experiments of Osaka City University and the Japan Ethological Society. No permits from the Japanese government were needed for experiments involving N. pulcher.

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The raw data for each individual fish have been made available in supplementary material to this publication.

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Hotta, T., Komiyama, S. & Kohda, M. A social cichlid fish failed to pass the mark test. Anim Cogn 21, 127–136 (2018). https://doi.org/10.1007/s10071-017-1146-y

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Keywords

  • Contingency checking behaviour
  • Mark test
  • Mirror self-recognition
  • Neolamprologus pulcher
  • Scraping behaviour