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Does a cichlid fish process face holistically? Evidence of the face inversion effect

  • Kento KawasakaEmail author
  • Takashi Hotta
  • Masanori Kohda
Original Paper

Abstract

Faces are the most important body part for differentiating among human individuals by humans. Humans read the face as a whole, rather than looking at its parts, which makes it more difficult to recognise inverted faces than upright. Some other mammals also identify each other based on the upright face and take longer to recognise inverted faces. This effect is called the face inversion effect and is considered as evidence for face-specific perception. This ability has rarely been observed in animals other than mammals, but it was recently reported that some fish species could distinguish among individuals based on the face. For example, the cichlid fish Neolamprologus pulcher rapidly recognises familiar conspecifics by faces rather than other body parts. Here, we examined the face inversion effect in N. pulcher, by showing photographs of conspecific fish faces and objects in both upright and inverted orientations. Subjects gazed at novel faces longer than familiar faces in upright presentation, whereas they did not show such a tendency for inverted faces. Although the object discrimination was difficult, we did not observe the difference between upright and inverted object photographs. Our results indicate that fish exhibits the inversion effect for faces. These findings suggest that N. pulcher may process their conspecifics’ face holistically, like humans.

Keywords

Cichlid fish Face inversion effect Face perception Holistic processing Visual paired comparison 

Notes

Acknowledgements

We thank the members of the Laboratory of Animal Sociology, Osaka City University, for their general assistance and fruitful discussion.

Author contributions.

KK, TH, and MK conceived and designed the experiments. KK performed the experiments and analysed the data. KK, TH, and MK contributed reagents/materials/analysis tools. KK, TH, and MK wrote this paper.

Funding

This study was financially supported by Japan Society for the Promotion of Science (JSPS) Grants-in-aid of Scientific Research (KAKENHI) (Nos. 26540070, 26118511, 16H05773, and 17K18712) to MK and (No. H16J09486) to TH.

Compliance with ethical standards

Conflict of interest

Authors KK, TH, and MK declare that they have no conflict of interest.

Ethics statement

Our experiment did not kill study fish. Fish were fed sufficient food once per day and kept in good aquarium conditions. Diseased or injured individuals were removed from the experimental aquarium, treated with medication, and used only after recovery. Our experiments were conducted in compliance with the Guidelines for Animal Welfare of the Japan Ethological Society, and the Animal Care and Use Committee of Osaka City University. No permits from Japanese government were needed for experiments involving N. pulcher.

References

  1. Agrillo C, Miletto Petrazzini ME, Dadda M (2013) Illusory patterns are fishy for fish, too. Front Neural Circuits 7:137CrossRefGoogle Scholar
  2. Balshine S, Leach B, Neat F, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134–140CrossRefGoogle Scholar
  3. Balzarini V, Taborsky M, Villa F, Frommen JG (2016) Computer animations of color markings reveal the function of visual threat signals in Neolamprologus pulcher. Curr Zool 63(1):45–54CrossRefGoogle Scholar
  4. Brecht KF, Wagner L, Ostojic L, Clayton NS, Nieder A (2017) Comparing the face inversion effect in crows and humans. J Comp Psychol A 203(12):1017–1027Google Scholar
  5. Brown SD, Dooling RJ (1992) Perception of conspecific faces by budgerigars (Melopsittacus undulatus): I. Natural faces. J Comp Psychol 106:203–216CrossRefGoogle Scholar
  6. Brown SD, Dooling RJ (1993) Perception of conspecific faces by budgerigars (Melopsittacus undulatus): II. Synthetic faces. J Comp Psychol 107:48–60CrossRefGoogle Scholar
  7. Bruce V, Young A (1998) In the eye of the beholder: the science of face perception. Oxford University Press, OxfordGoogle Scholar
  8. Bshary R, Brown C (2014) Fish cognition. Curr Biol 24(19):R947–R950CrossRefGoogle Scholar
  9. Burke D, Sulikowski D (2013) The evolution of holistic processing of faces. Front Psychol 4.  https://doi.org/10.3389/fpsyg.2013.00011
  10. Gothard KM, Erickson CA, Amaral DG (2004) How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim Cogn 7(1):25–36CrossRefGoogle Scholar
  11. Helfman G, Collete BB, Facey DE, Bowen BW (2009) The diversity of fish: biology, evolution and ecology. Wiley, HobokenGoogle Scholar
  12. Hotta T, Takeyama T, Jordan LA, Kohda M (2014) Duration of memory of dominance relationships in a group living cichlid. Naturwissenschaften 101(9):745–751CrossRefGoogle Scholar
  13. Hotta T, Satoh S, Kosaka N, Kohda M (2017) Face recognition in the Tanganyikan cichlid Julidochromis transcriptus. Anim Behav 127:1–5CrossRefGoogle Scholar
  14. Hotta T, Kawasaka K, Satoh S, Kohda M (2018) Fish focus primarily on the faces of other fish. Sci Rep (unpublished) Google Scholar
  15. Kanwisher N, Yovel G (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4211–4302CrossRefGoogle Scholar
  16. Kendrick KM, Atkins K, Hinton MR, Heavens P, Keverne B (1996) Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behav Processes 38:19–35CrossRefGoogle Scholar
  17. Kohda M, Jordan LA, Hotta T, Kosaka N, Karino K, Tanaka H, Taniyama M, Tomohiro T (2015) Facial recognition in a group-living cichlid. PLoS One 10.  https://doi.org/10.1371/journal.pone.0142552
  18. O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social decision-making network. Science 336(6085):1154–1157CrossRefGoogle Scholar
  19. Parr LA (2011) The evolution of face processing in primates. Philos Trans R Soc Lond B Biol Sci 366:1764–1777CrossRefGoogle Scholar
  20. Parr LA, Winslow JT, Hopkins WD (1999) Is the inversion effect in rhesus monkeys face-specific? Anim Cogn 2:123–129CrossRefGoogle Scholar
  21. Parr LA, Winslow JT, Hopkins WD, de Waal FB (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:47–60CrossRefGoogle Scholar
  22. Peterson MA, Rhodes G (2003) Perception of faces, objects, and scences analystic and holistic processes. Oxford University Press, OxfordGoogle Scholar
  23. Phelps MT, Roberts WA (1994) Memory for pictures of upright and inverted primate faces in humans (Homo sapiens), Squirrel monkeys (Saimiri sciureus), and pigeons (Columba livia). J Comp Psychol 108:114–125CrossRefGoogle Scholar
  24. Racca A, Amadei E, Ligout S, Guo K, Meints K, Mills D (2010) Discrimination of human and dog faces and inversion responses in domestic dogs (Canis familiaris). Anim Cogn 13:525–533CrossRefGoogle Scholar
  25. Rosenfeld SA, Van Hoesen GW (1979) Face recognition in the rhesus monkey. Neuropsychologia 17(5):503–509CrossRefGoogle Scholar
  26. Satoh S, Tanaka H, Kohda M (2016) Facial recognition in a discus fish (Cichlidae): Experimental approach using digital models. PLoS One 11.  https://doi.org/10.1371/journal.pone.0154543
  27. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252CrossRefGoogle Scholar
  28. Tanaka JW (2001) The entry point of face recognition: evidence for face expertise. J Exp Psychol 130(3):534–543CrossRefGoogle Scholar
  29. Tanaka JW, Farah MJ (2003) The holistic representation of faces. In: Peterson MA, Rhodes G (eds) Perception of faces, objects, and scenes: analytic and holistic processes. Oxford University Press, OxfordGoogle Scholar
  30. Tate AJ, Fischer H, Leigh AE, Kendrick KM (2006) Behavioural and neurophysiological evidence for face identity and face emotion processing in animals. Philos Trans R Soc Lond B Biol Sci 361:2155–2172CrossRefGoogle Scholar
  31. Turati C, Sangrigoli S, Ruely J, Schonen S (2004) Evidence of the face inversion effect in 4-month-old. Infancy 6:275–297CrossRefGoogle Scholar
  32. Valentine T (1988) Upside-down faces: a review of the effect of inversion upon face recognition. Br J Psychol 79:471–491CrossRefGoogle Scholar
  33. Wang MY, Takeuchi H (2017) Individual recognition and the ‘face inversion effect’ in medaka fish (Oryzias latipes). eLife.  https://doi.org/10.7554/eLife.24728.001 Google Scholar
  34. Yin RK (1969) Looking at upside-down faces. J Exp Psychol 81:141–145CrossRefGoogle Scholar
  35. Yovel G, Kanwisher N (2004) Face perception: domain specific, not process specific. Neuron 44:889–898Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Animal Sociology, Department of Biology and Geosciences, Graduate School of ScienceOsaka City UniversityOsakaJapan
  2. 2.Department of Psychology, Graduate School of LettersKyoto UniversityKyotoJapan

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