Animal Cognition

, Volume 21, Issue 1, pp 127–136 | Cite as

A social cichlid fish failed to pass the mark test

  • Takashi HottaEmail author
  • Shiho Komiyama
  • Masanori Kohda
Original Paper


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.


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



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:

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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.

Data availability

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

Supplementary material

10071_2017_1146_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 24 kb)


  1. Ari C (2011) Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives. Open Anat 3:1–13. CrossRefGoogle 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. CrossRefGoogle Scholar
  3. ASAB/ABS (2014) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 99:I–IXGoogle 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. CrossRefGoogle 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. CrossRefGoogle Scholar
  6. Beckoff M, Sherman PW (2004) Reflections on animal selves. Trends Ecol Evol 19:176–180. CrossRefGoogle Scholar
  7. Brown C, Laland K, Krause J (2011) Fish cognition and behaviour. Wiley, OxfordCrossRefGoogle Scholar
  8. Bshary R, Gingins S, Vail AL (2014) Social cognition in fishes. Trends Cogn Sci 18(9):465–471CrossRefPubMedGoogle Scholar
  9. Byrne RW (1995) The thinking ape: evolutionary origins of intelligence. Oxford University Press, OxfordCrossRefGoogle 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. CrossRefGoogle Scholar
  11. Clary D, Kelly DM (2016) Graded mirror self-recognition by Clark’s nutcrackers. Sci Rep 6:36459. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cohen J (1988) Statistical power analysis for the behavioural sciences. Lawrence Earlbaum Associates, HillsideGoogle 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. CrossRefPubMedGoogle 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. CrossRefGoogle Scholar
  15. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744–747. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Devue C, Brédart S (2011) The neural correlates of visual self-recognition. Conscious Cognit 20:40–51. CrossRefGoogle Scholar
  17. Frederick JL (1997) Evaluation of fluorescent elastomer injection as a method for marking small fish. Bull Marine Sci 69:399–408Google 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. CrossRefPubMedGoogle Scholar
  19. Gallup GG (1970) Chimpanzees: self-recognition. Science 167:86–87. CrossRefGoogle 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. CrossRefPubMedGoogle Scholar
  21. Gallup GG (1998) Self-awareness and the evolution of social intelligence. Behav Process 42:239–247. CrossRefGoogle Scholar
  22. Gallup GG, McClure MK, Hill SD, Bundy RA (1971) Capacity of self-recognition in differentially reared chimpanzees. Psychol Rec 21:69–74CrossRefGoogle 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. CrossRefPubMedGoogle 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. CrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle 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. CrossRefPubMedGoogle Scholar
  27. Jerison HJ, Jerison I (1988) The evolutionary biology of intelligence. Nato ASI series in ecology. Springer, New YorkCrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle 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. CrossRefGoogle 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. CrossRefGoogle Scholar
  31. Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246. CrossRefPubMedGoogle Scholar
  32. Lucon-Xiccato T, Bisazza A (2017) Individual differences in cognition among teleost fishes. Behav Process 141:184–195. CrossRefGoogle 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. CrossRefPubMedGoogle 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. CrossRefGoogle 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. CrossRefGoogle 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. CrossRefGoogle Scholar
  37. Oliveira RF, La C, Canario AVM (2005) Behavioural endocrinology: no hormonal response in tied fights. Nature 437:207–208. CrossRefPubMedGoogle Scholar
  38. Parker ST, Mitchell RW, Boccia ML (1994) Self-awareness in animals and humans: developmental perspectives. Cambridge University Press, New YorkCrossRefGoogle 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. CrossRefPubMedGoogle Scholar
  40. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 103:17053–17057. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Premack D, Woodruff G (1978) Does the chimpanzee have a theory of mind? Behav Brain Sci 1:515–526. CrossRefGoogle 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. CrossRefPubMedGoogle 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. CrossRefPubMedPubMedCentralGoogle 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 84:753–760CrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle 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. CrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle 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 15:69–76Google Scholar
  49. Shillito DJ, Gallup GG, Beck B (1999) Factors affecting mirror behaviour in western lowland gorillas, Gorilla gorilla. Anim Behav 57:999–1004. CrossRefPubMedGoogle 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. CrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle 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. CrossRefGoogle Scholar
  53. Suarez SD, Gordon G, Gallup GG (1981) Self-recognition in chimpanzees and orangutans, but not gorillas. J Hum Evol 11:239–244. Google Scholar
  54. Suddendorf T, Butler DL (2013) The nature of visual self-recognition. Trends Cognit Sci 17:121–127. CrossRefGoogle Scholar
  55. Thunken T, Waltschyk N, Bakker TCM, Kullmann H (2009) Olfactory self-recognition in a cichlid fish. Anim Cogn 12:717–724. CrossRefPubMedGoogle 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. CrossRefGoogle 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. CrossRefGoogle 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. CrossRefGoogle Scholar
  59. Wong M, Balshine S (2010) Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue. Biol Lett. PubMedCentralGoogle Scholar
  60. Yang H (2005) On the uniqueness of self-face recognition. Psychol Sci 28:1517–1519Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Laboratory of Animal Sociology, Department of Biology and Geosciences, Graduate School of SciencesOsaka City UniversitySumiyoshi, OsakaJapan

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