Abstract
In many species the face mediates social communication, conveying meaningful information to other individuals. The face is thus a highly important visual stimulus, and many factors are involved in recognizing individuals from facial information. Capuchin monkeys are excellent subjects for studying facial recognition from a comparative perspective because of their intelligence and their highly social nature. Furthermore, they show polymorphic color vision, with groups containing both dichromatic and trichromatic individuals, which provides an opportunity to examine potential effects of color on facial recognition. In this chapter, I describe experimental research on the relationships between color vision and detection of face color modulations in capuchin monkeys. Using face images of familiar individuals, the color of either the left eye, the right eye, or the nose was shifted in a red or blue direction. Face orientation (upright and inverted) and face identity were also manipulated. Trichromatic monkeys showed no greater sensitivity to face color modulation, but face parts, orientation, and identity all affect their accuracy and reaction times in the detection task. These results indicate that facial stimuli appear equally salient to dichromatic and trichromatic individuals, and that social factors such as dominance and kinship affect face processing in capuchin monkeys.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adachi I, Chou DP, Hampton RR (2009) Thatcher effect in monkeys demonstrates conservation of face perception across Primates. Curr Biol 19(15):1270–1273. https://doi.org/10.1016/j.cub.2009.05.067
Anderson JR, Kuroshima H, Paukner A, Fujita K (2009) Capuchin monkeys (Cebus apella) respond to video images of themselves. Anim Cogn 12(1):55–62. https://doi.org/10.1007/s10071-008-0170-3
Bognar Z, Iotchev IB, Kubinyi E (2018) Sex, skull length, breed, and age predict how dogs look at faces of humans and conspecifics. Anim Cogn 21(4):447–456. https://doi.org/10.1007/s10071-018-1180-4
Calcutt SE, Rubin TL, Pokorny JJ, de Waal FBM (2017) Discrimination of emotional facial expressions by tufted capuchin monkeys (Sapajus apella). J Comp Psychol 131(1):40–49. https://doi.org/10.1037/com0000055
Chang L, Tsao DY (2017) The code for facial identity in the primate brain. Cell 169(6):1013–1028. https://doi.org/10.1016/j.cell.2017.05.011
Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate colour vision. Biol Lett 2(2):217–221
Corso J, Bowler M, Heymann EW, Roos C, Mundy NI (2016) Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus). Proc R Soc B Biol Sci 283(1856):20160067. https://doi.org/10.1098/rspb.2016.0067
Dubuc C, Allen WL, Maestripieri D, Higham JP (2014) Is male rhesus macaque red color ornamentation attractive to females? Behav Ecol Sociobiol 68(7):1215–1224
Dubuc C, Brent LJ, Accamando AK, Gerald MS, Mac Larnon A, Semple S, Heistermann M, Engelhardt A (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. Int J Primatol 30(6):777–789
Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, Cambridge, UK
Griffin JW (2020) Quantifying the face inversion effect in nonhuman primates: a phylogenetic meta-analysis. Anim Cogn 23(2):237–249. https://doi.org/10.1007/s10071-019-01340-8
Guo K, Meints K, Hall C, Hall S, Mills D (2009) Left gaze bias in humans, rhesus monkeys and domestic dogs. Anim Cogn 12(3):409–418. https://doi.org/10.1007/s10071-008-0199-3
Hattori Y, Kuroshima H, Fujita K (2007) I know you are not looking at me: capuchin monkeys’ (Cebus apella) sensitivity to human attentional states. Anim Cogn 10(2):141–148. https://doi.org/10.1007/s10071-006-0049-0
Heesy CP, Ross CF (2001) Evolution of activity patterns and chromatic vision in primates: Morphometrics, genetics and cladistics. J Hum Evol 40(2):111–149
Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 21(4):739–746. https://doi.org/10.1093/beheco/arq047
Higham JP, Hughes KD, Brent LJ, Dubuc C, Engelhardt A, Heistermann M, Maestriperi D, Santos LR, Stevens M (2011) Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques. Proc R Soc B 278(1723):3452–3458
Hiramatsu C, Tsutsui T, Matsumoto Y, Aureli F, Fedigan LM, Kawamura S (2005) Color vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica. Am J Primatol 67(4):447–461. https://doi.org/10.1002/ajp.20199
Hiramatsu C, Fujita K (2015) Visual categorization of surface qualities of materials by capuchin monkeys and humans. Vis Res 115:71–82. https://doi.org/10.1016/j.visres.2015.07.006
Hiramatsu C, Melin AD, Allen WL, Dubuc C, Higham JP (2017) Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals. Proc R Soc B Biol Sci 284(1856):20162458. https://doi.org/10.1098/rspb.2016.2458
Hung C-C, Yen CC, Ciuchta JL, Papoti D, Bock NA, Leopold DA, Silva AC (2015) Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset. J Neurosci 35(3):1160–1172. https://doi.org/10.1523/JNEUROSCI.2659-14.2015
Jacobs GH (1996) Primate photopigments and primate color vision. Proc Natl Acad Sci 93(2):577–581
Jacobs GH (2007) New World monkeys and color. Int J Primatol 28(4):729–759
Jacobs GH, Neitz J, Neitz M (1993) Genetic basis of polymorphism in the color vision of platyrrhine monkeys. Vis Res 33(3):269–274. https://doi.org/10.1016/0042-6989(93)90083-9
Kanwisher N, Yovel G (2006) The fusiform face area: a cortical region specialized for the perception of faces. Phil Trans R Soc B 361(1476):2109–2128. https://doi.org/10.1098/rstb.2006.1934
Kawaguchi Y, Kuroshima H, Fujita K (2019) Age categorization of conspecific and Heterospecific faces in capuchin monkeys (Sapajus apella). J Comp Psychol 133(4):502–511. https://doi.org/10.1037/com0000185
Kendrick KM, da Costa AP, Leigh AE, Hinton MR, Peirce JW (2001) Sheep don’t forget a face. Nature 414(6860):165–166. https://doi.org/10.1038/35102669
Kingdom FAA, Prins N (2010) Psychophysics: a practical introduction. Elsevier Academic Press, Cambridge, MA, p 279
Kohda M, Jordan LA, Hotta T, Kosaka N, Karino K, Tanaka H, Taniyama M, Takeyama T (2015) Facial recognition in a group-living cichlid fish. PLoS One 10(11):e0142552. https://doi.org/10.1371/journal.pone.0142552
Kuroshima H, Fujita K, Fuyuki A, Masuda T (2002) Understanding of the relationship between seeing and knowing by tufted capuchin monkeys (Cebus apella). Anim Cogn 5(1):41–48. https://doi.org/10.1007/s10071-001-0123-6
Lonsdorf EV, Engelbert LM, Howard LH (2019) A competitive drive? Same-sex attentional preferences in capuchins. Am J Primatol 81(6):e22998. https://doi.org/10.1002/ajp.22998
Matsuno T, Fujita K (2018) Body inversion effect in monkeys. PLoS One 13(10):e0204353. https://doi.org/10.1371/journal.pone.0204353
Maurer D, Grand RL, Mondloch CJ (2002) The many faces of configural processing. Trends Cogn Sci 6(6):255–260. https://doi.org/10.1016/S1364-6613(02)01903-4
Megreya AM, Havard C (2011) Left face matching bias: right hemisphere dominance or scanning habits? Laterality 16(1):75–92. https://doi.org/10.1080/13576500903213755
Mollon JD (1989) “Tho’she kneel’d in that place where they grew…” the uses and origins of primate colour vision. J Exp Biol 146(1):21–38
Morimoto Y, Fujita K (2012) Capuchin monkeys (Cebus apella) use conspecifics’ emotional expressions to evaluate emotional valence of objects. Anim Cogn 15(3):341–347. https://doi.org/10.1007/s10071-011-0458-6
Nakata R, Osada Y (2012) The Thatcher illusion in squirrel monkeys (Saimiri sciureus). Anim Cogn 15(4):517–523. https://doi.org/10.1007/s10071-012-0479-9
Neiworth JJ, Hassett JM, Sylvester CJ (2007) Face processing in humans and new world monkeys: the influence of experiential and ecological factors. Anim Cogn 10(2):125–134. https://doi.org/10.1007/s10071-006-0045-4
Paukner A, Wooddell LJ, Lefevre CE, Lonsdorf E, Lonsdorf E (2017) Do capuchin monkeys (Sapajus apella) prefer symmetrical face shapes? J Comp Psychol 131(1):73–77. https://doi.org/10.1037/com0000052
Regan BC, Julliot C, Simmen B, Viénot F, Charles–Dominique, P., and Mollon, J. D. (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc London Ser B Biol Sci 356(1407):229–283
Saito A, Kawamura S, Mikami A, Ueno Y, Hiramatsu C, Koida K, Fujita K, Kuroshima H, Hasegawa T (2005) Demonstration of a genotype-phenotype correlation in the polymorphic color vision of a non-callitrichine new world monkey, capuchin (Cebus apella). Am J Primatol 67(4):471–485. https://doi.org/10.1002/ajp.20201
Sheehan MJ, Tibbetts EA (2011) Specialized face learning is associated with individual recognition in paper wasps. Science 334(6060):1272–1275. https://doi.org/10.1126/science.1211334
Stephen ID, Smith MJL, Stirrat MR, Perrett DI (2009) Facial skin coloration affects perceived health of human faces. Int J Primatol 30(6):845–857
Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203(13):1963–1986
Takagi S, Arahori M, Chijiiwa H, Saito A, Kuroshima H, Fujita K (2019) Cats match voice and face: cross-modal representation of humans in cats (Felis catus). Anim Cogn 22(5):901–906. https://doi.org/10.1007/s10071-019-01265-2
Takimoto A, Fujita K (2011) I acknowledge your help: capuchin monkeys’ sensitivity to others’ labor. Anim Cogn 14(5):715–725. https://doi.org/10.1007/s10071-011-0406-5
Talbot CF, Leverett KL, Brosnan SF (2016) Capuchins recognize familiar faces. Anim Behav 122:37–45. https://doi.org/10.1016/j.anbehav.2016.09.017
Thorstenson CA, Pazda AD, Young SG, Elliot AJ (2019) Face color facilitates the disambiguation of confusing emotion expressions: toward a social functional account of face color in emotion communication. Emotion 19(5):799–807. https://doi.org/10.1037/emo0000485
Tomonaga M (2007) Visual search for orientation of faces by a chimpanzee (Pan troglodytes): face-specific upright superiority and the role of facial configural properties. Primates 48(1):1–12. https://doi.org/10.1007/s10329-006-0011-4
Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci 105(49):19514–19519. https://doi.org/10.1073/pnas.0809662105
Zangenehpour S, Chaudhuri A (2005) Patchy organization and asymmetric distribution of the neural correlates of face processing in monkey inferotemporal cortex. Curr Biol 15(11):993–1005. https://doi.org/10.1016/j.cub.2005.04.031
Acknowledgements
My sincere and deep gratitude goes to Professor Kazuo Fujita and his enthusiasm for exploring the animal mind. I was always encouraged by his expert advice, and his kindness continues to help people and animals. I am grateful to Dr. Takaaki Kaneko, who gave valuable suggestions for our study. I am also grateful to Professor James Anderson for his kind editing of the manuscript and to Dr. Annika Paukner for helpful suggestions for improving this chapter. This research was supported by a Grant-in-Aid for JSPS Fellows (No. 10 J04395) to C. Hiramatsu and JSPS Grants-in-Aide for Scientific Research Nos. 20220004 and 25240020 to K. Fujita.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Hiramatsu, C. (2021). Factors Affecting Facial Recognition in Capuchin Monkeys. In: Anderson, J.R., Kuroshima, H. (eds) Comparative Cognition. Springer, Singapore. https://doi.org/10.1007/978-981-16-2028-7_5
Download citation
DOI: https://doi.org/10.1007/978-981-16-2028-7_5
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-2027-0
Online ISBN: 978-981-16-2028-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)