Animal Cognition

, Volume 20, Issue 4, pp 677–688 | Cite as

Sneaking a peek: pigeons use peripheral vision (not mirrors) to find hidden food

  • Emre Ünver
  • Alexis Garland
  • Sepideh Tabrik
  • Onur Güntürkün
Original Paper

Abstract

A small number of species are capable of recognizing themselves in the mirror when tested with the mark-and-mirror test. This ability is often seen as evidence of self-recognition and possibly even self-awareness. Strangely, a number of species, for example monkeys, pigs and dogs, are unable to pass the mark test but can locate rewarding objects by using the reflective properties of a mirror. Thus, these species seem to understand how a visual reflection functions but cannot apply it to their own image. We tested this discrepancy in pigeons—a species that does not spontaneously pass the mark test. Indeed, we discovered that pigeons can successfully find a hidden food reward using only the reflection, suggesting that pigeons can also use and potentially understand the reflective properties of mirrors, even in the absence of self-recognition. However, tested under monocular conditions, the pigeons approached and attempted to walk through the mirror rather than approach the physical food, displaying similar behavior to patients with mirror agnosia. These findings clearly show that pigeons do not use the reflection of mirrors to locate reward, but actually see the food peripherally with their near-panoramic vision. A re-evaluation of our current understanding of mirror-mediated behavior might be necessary—especially taking more fully into account species differences in visual field. This study suggests that use of reflections in a mirrored surface as a tool may be less widespread than currently thought.

Keywords

Bird Mirror-self-recognition Visual system 

Notes

Acknowledgements

All procedures were in compliance with the National Institutes for the Care and Use of Laboratory Animals and were approved by the National Committee of North Rhine-Westphalia, Germany. The study was supported by the Deutsche Forschungsgemeinschaft through Gu227/16-1 and through SFB 874. We thank Sebastian Ocklenburg and Erhan Genç for statistical advice and support.

References

  1. Anderson JR (1986) Mirror-mediated finding of hidden food by monkeys (Macaca tonkeana and Macaca fascicularis). J Comp Psychol 100:237–242CrossRefGoogle Scholar
  2. Anderson JR, Gallup GG (2011) Which primates recognize themselves in mirrors? PLoS Biol. doi:10.1371/journal.pbio.1001024 Google Scholar
  3. Anderson JR, Gallup GG (2015) Mirror self-recognition: a review and critique of attempts to promote and engineer self-recognition in primates. Primates 56:317–326CrossRefPubMedGoogle Scholar
  4. Anderson JR, Roeder JJ (1989) Responses of capuchin monkeys (Cebus apella) to different conditions of mirror-image stimulation. Primates 30:581–587CrossRefGoogle Scholar
  5. Bard KA, Todd BK, Bernier C, Love J, Leavens DA (2006) Self-awareness in human and chimpanzee infants: what is measured and what is meant by the mark and mirror test? Infancy 9(2):185–213CrossRefGoogle Scholar
  6. Broom DM, Sena H, Moynihan KL (2009) Pigs learn what a mirror image represents and use it to obtain information. Anim Behav 78:1037–1041CrossRefGoogle Scholar
  7. Calhoun S, Thompson RL (1988) Long-term retention of self-recognition by chimpanzees. Am J Primatol 15:361–365CrossRefGoogle Scholar
  8. Chang L, Fang Q, Zhang S, Poo M, Gong N (2015) Mirror-induced self-directed behaviors in rhesus monkeys after visual-somatosensory training. Curr Biol 25:212–217CrossRefPubMedGoogle Scholar
  9. Clary D, Kelly DM (2016) Graded mirror self-recognition by Clark’s nutcrackers. Sci Rep 6:36459CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dawkins MS (2002) What are birds looking at? Head movements and eye use in chickens. Anim Behav 63:991–998CrossRefGoogle Scholar
  11. Epstein R, Lanza RP, Skinner BF (1981) ‘‘Self-awareness’’ in the pigeon. Science 212:695–696CrossRefPubMedGoogle Scholar
  12. Gallup GG (1970) Chimpanzees: self-recognition. Science 167:86–87CrossRefGoogle Scholar
  13. Gallup GG, Suarez SD (1991) Social responding to mirrors in rhesus monkeys: effects of temporary mirror removal. J Comp Psychol 105:376–379CrossRefPubMedGoogle Scholar
  14. Gallup GG, Wallnau LB, Suarez SD (1980) Failure to find self-recognition in mother-infant and infant-infant rhesus monkey pairs. Folia Primatol 33:210–219CrossRefPubMedGoogle Scholar
  15. Gallup GG, Anderson JR, Shillito DJ (2002) The mirror test. In: Bekoff M, Allen C, Burghardt GM (eds) The cognitive animal. Empirical and theoretical perspectives on animal cognition. MIT, Cambridge, pp 325–333Google Scholar
  16. Gelhard BS, Wohlman SH, Thompson RKR (1982). Self-recognition in the pigeon: a second look. Paper presented at the Northeast Regional Meeting of the Animal Behavior SocietyGoogle Scholar
  17. Gieling ET, Mijdam E, van der Staay FJ, Nordquist RE (2014) Lack of mirror use by pigs to locate food. Appl Anim Behav Sci 154:22–29CrossRefGoogle Scholar
  18. Goodale MA (1983) Visually guided pecking in the pigeon (Columba livia). Brain Behav Evol 22:22–41CrossRefPubMedGoogle Scholar
  19. Güntürkün O, Bugnyar T (2016) Cognition without neocortex. Trends Cogn Sci 20:291–303CrossRefPubMedGoogle Scholar
  20. Hauser MD, Miller CT, Liu K, Gupta R (2001) Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration. Am J Primatol 53:131–137CrossRefPubMedGoogle Scholar
  21. Heschl A, Burkart J (2006) A new mark test for mirror self-recognition in non-human primates. Primates 47:187–198CrossRefPubMedGoogle Scholar
  22. Heschl A, Fuchsbichler C (2009) Siamangs (Hylobates syndactylus) recognize their mirror image. Int J Comp Psychol 22:221–233Google Scholar
  23. Howell TJ, Bennett PC (2011) Can dogs (Canis familiaris) use a mirror to solve a problem? J Vet Behav 6:306–312CrossRefGoogle Scholar
  24. Howell TJ, Toukhsati S, Conduit R, Bennett P (2013) Do dogs use a mirror to find hidden food? J Vet Behav 6:425–430CrossRefGoogle Scholar
  25. Hyatt CW (1998) Responses of gibbons (Hylobates lar) to heir mirror images. Am J Primatol 45:307–311CrossRefPubMedGoogle Scholar
  26. Inoue-Nakamura N (1997) Mirror self-recognition in nonhuman primates: a phylogenetic approach. Jpn Psychol Res 39:266–275CrossRefGoogle Scholar
  27. Itakura S (1987) Mirror-guided behavior in Japanese macaques (Macaca fuscata fuscata). Primates 28:149–161CrossRefGoogle Scholar
  28. Jahnke HJ (1984) Binocular visual field differences among various breeds of pigeons. Bird Behav 5:96–102Google Scholar
  29. Jiménez OL, Stoppa K, Güntürkün O, Troje NF (2009) Vision during head-bobbing: Are pigeons capable of shape discrimination during the thrust phase? Exp Brain Res 199:313–321CrossRefGoogle Scholar
  30. Ledbetter DH, Basen JA (1982) Failure to demonstrate self-recognition in gorillas. Am J Primatol 2:307–310CrossRefGoogle Scholar
  31. Macellini S, Ferrari PF, Bonini L, Fogassi L, Paukner A (2010) A modified mark test for own-body recognition in pig tailed macaques (Macaca nemestrina). Anim Cogn 13(4):631–639CrossRefPubMedPubMedCentralGoogle Scholar
  32. Medina FS, Taylor AH, Hunt GR, Gray RD (2011) New Caledonian crows’ response to mirrors. Anim Behav 82:981–993CrossRefGoogle Scholar
  33. Menzel EW Jr, Savage-Rumbaugh ES, Lawson J (1985) Chimpanzee (Pan troglodytes) spatial problem solving with the use of mirror and televised equivalent of mirrors. J Comp Psychol 99:211–217CrossRefPubMedGoogle Scholar
  34. Nicholson IS, Gould JE (1995) Mirror mediated object discrimination and self-directed behavior in a female gorilla. Primates 36(4):515–521CrossRefGoogle Scholar
  35. Pepperberg IM, Garcia SE, Jackson EC, Marconi S (1995) Mirror use by African grey parrots (Psittacus erithacus). J Comp Psychol 109(2):182–195CrossRefGoogle Scholar
  36. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. PNAS 103:17053–17057CrossRefPubMedPubMedCentralGoogle Scholar
  37. Plotnik JM, de Waal F, Moore D, Reiss D (2010) Self-recognition in the Asian elephant and future directions for cognitive research with elephants in zoological settings. Zoo Biol 29(2):179–191CrossRefPubMedGoogle Scholar
  38. Posada S, Colell M (2007) Another gorilla (Gorilla gorilla gorilla) recognizes himself in a mirror. Am J Primatol 69(5):576–583CrossRefPubMedGoogle Scholar
  39. Povinelli D (1989) Failure to find self-recognition in Asian elephants (Elephans maximus) in contrast to their use of mirror cues to discover hidden food. J Comp Psychol 103:122–131CrossRefGoogle Scholar
  40. Povinelli DJ, Rulf AR, Landau KR, Bierschwale DT (1993) Self-recognition in chimpanzees (Pan troglodytes): distribution, ontogeny, and patterns of emergence. J Comp Psychol 107:347–372CrossRefPubMedGoogle Scholar
  41. Povinelli DJ, Gallup GG Jr, Eddy TJ, Bierschwale DT, Engstrom MC, Perilloux HK, Toxopeus IB (1997) Chimpanzees recognize themselves in mirrors. Anim Behav 53:1083–1088CrossRefGoogle Scholar
  42. Prior H, Schwarz A, Güntürkün O (2008) Mirror-induced behaviour in the magpie (Pica pica): evidence of self-recognition. PLoS Biol 6(8):e202. doi:10.1371/journal.pbio.0060202 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rajala AZ, Reininger KR, Lancaster KM, Populin LC (2010) Rhesus monkeys (Macaca mulatta) do recognize themselves in the mirror: implications for the evolution of self-recognition. PLoS ONE. doi:10.1371/journal.pone.0012865 Google Scholar
  44. Ramachandran V, Altschuler E, Hillyer S (1997) Mirror agnosia. Proc R Soc Lond B Biol Sci 264(1382):645–647CrossRefGoogle Scholar
  45. Reiss D, Marino L (2001) Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. PNAS 98(10):5937–5942CrossRefPubMedPubMedCentralGoogle Scholar
  46. Roma PG, Silberberg A, Huntsberry ME, Christensen CJ, Ruggier AM, Suomi SJ (2007) Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks. Am J Primatol 69:989–1000CrossRefPubMedGoogle Scholar
  47. Shillito DJ, Gallup GG, Beck BB (1999) Factors affecting mirror behavior in western lowland gorillas, Gorilla gorilla. Anim Behav 57:999–1004CrossRefPubMedGoogle Scholar
  48. 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):e86193CrossRefPubMedPubMedCentralGoogle Scholar
  49. Suarez SD, Gallup GG (1981) Self-recognition in chimpanzees and orangutans, but not gorillas. J Hum Evol 10(2):175–188CrossRefGoogle Scholar
  50. Suarez SD, Gallup GG (1986) Social responding to mirrors in rhesus macaques (Macaca mulatta): effects of changing mirror location. Am J Primatol 11:239–244CrossRefGoogle Scholar
  51. Suddendorf T, Collie-Baker E (2009) The evolution of primate visual self-recognition: evidence of absence in lesser apes. Proc R Soc B 276:1671–1677CrossRefPubMedPubMedCentralGoogle Scholar
  52. Thompson RKR, Contie C (1986) Further reflections on mirror usage by pigeons. Paper presented at the annual meeting of the Psychonomic Society, New OrleansGoogle Scholar
  53. Thompson RKR, Contie CL (1994) Further reflections on mirror-usage by pigeons: lessons from Winnie the Pooh and Pinocchio too. In: Parker S, Boccia M, Mitchell R (eds) Self-awareness in animals and humans. Cambridge University Press, New York, pp 392–409CrossRefGoogle Scholar
  54. Troje NF, Frost BJ (2000) Head-bobbing in pigeons: how stable is the hold phase? J Exp Biol 203:935–940PubMedGoogle Scholar
  55. Uchino E, Watanabe S (2014) Self-recognition in pigeons revisited. J Exp Anal Behav 102:327–334CrossRefPubMedGoogle Scholar
  56. Wallman J, Letelier J-C (1993) Eye movements, head movements, and gaze stabilization in birds. In: Zeigler HP, Bischof H-J (eds) Vision, brain, and behaviour in birds. MIT Press, Cambridge, pp 245–263Google Scholar
  57. Wilkie DM, Saksida LM (1994) The spatial distribution of pigeons' target detection. Behav Brain Res 60:137–140CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Emre Ünver
    • 1
  • Alexis Garland
    • 1
  • Sepideh Tabrik
    • 1
  • Onur Güntürkün
    • 1
    • 2
  1. 1.Faculty of Psychology, BiopsychologyRuhr University BochumBochumGermany
  2. 2.Wallenberg Research Centre at Stellenbosch UniversityStellenbosch Institute for Advanced Study (STIAS)StellenboschSouth Africa

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