Abstract
Eyes play an important role in communication amongst humans and animals. However, relatively little is known about specific differences in eye morphology amongst primates and how these features might be associated with social structure and direction of gaze. We present a detailed study of gazing and eye morphology—exposed sclera and surrounding features—in orangutans. We measured gazing in rehabilitating orangutans in two contexts: interspecific viewing of the experimenter (with video camera) and intraspecific gazing (between subjects). Our findings show that direct staring is avoided and social looking is limited to certain age/social categories: juveniles engage in more looking at other orangutans than do adults or infants. While orangutans use eye movements in social communication, they avoid the more prolonged mutual gaze that is characteristic of humans, and also apparent in chimpanzees and gorillas. Detailed frame-by-frame analysis of videotapes from field and zoo studies of orangutans revealed that they pay visual attention to both human observers and conspecifics by glancing sideways, with the head turned at an angle away from the subject being observed. Mutual gaze was extremely rare, and we have observed only two incidences of gaze following. Orangutans in captivity appear to use a more restricted pattern of gazes compared to free-living, rehabilitating ones, possibly suggesting the presence of a pathological condition (such as depression) in the captive subjects. Our findings have implications for further investigations of social communication and cognition in orangutans.
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REFERENCES
Andrew, R. J. (1963). The origin and evolution of the calls and facial expressions of the primates. Behaviour 20: 1–109.
Andrew, R. J. (1964). The displays of the primates. In Buettner-Janusch, J. (ed.), Evolutionary and Genetic Biology of the Primates, Vol. 2, Academic Press, New York.
Argyle, M. (1971). The Psychology of Interpersonal Behaviour, Penguin, Harmondsworth.
Argyle, M., and Cook, M. (1976). Gaze and Mutual Gaze, Cambridge University Press, Cambridge.
Bard, K. A. (1990). “Social tool use” by free-ranging orang-utans:APiagetian and development perspective on the manipulation of an animate object. In Parker, S. T., and Gibson, K. R. (eds.), ”Language” and Intelligence in Monkeys and Apes: Comparative Developmental Perspectives, Cambridge University Press, Cambridge, pp. 356–378.
Blest, A.D. (1957). The function of eyespot patterns in the lepidoptera. Behaviour 11: 209–256.
Bolwig, N. (1964). Facial expression in primates with remarks on a parallel development in certain primates. Behaviour 22: 167–192.
Brésard, B., and Lacour, M.-C. (1982). Recherches préliminaires sur les communications visuelles au cours développement chez un jeune orang-outang. Mammalia 46: 121–123.
Call, J., and Tomasello, M. (1994). Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J. Comp. Psychol. 108(4): 307–317.
Chance, M. R. A., and Jolly, C. J. (1970). Social Groups of Monkeys, Apes and Man, Jonathan Cape, London.
Chevalier-Skolnikoff, S. (1982). A cognitive analysis of facial behavior in Old World monkeys, apes and human beings. In Snowdon, C. T., Brown, C. H., & Petersen, M. R. (eds.), Primate Communication, Cambridge University Press, New York, pp. 303–368.
deWaal, F. (1982). Chimpanzee Politics: Power and Sex Among Apes, Jonathan Cape, London.
deWaal, F. (1989). Peacemaking Among Primates, Harvard University Press, Cambridge, MA.
de Waal, F., and Yoshihara, D. (1983). Reconciliation and redirected affection in rhesus monkeys. Behaviour 85: 224–241.
Deijen, J. B., Orlebeke, J. F., and Rijsdijk, F. V. (1993). Effect of depression on psychomotor skill, eye movements and recognition memory. J. Affect. Disord. 29(1): 33–40.
Delgado, R., and van Schaik, C. P. (2000). The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands. Evol. Anthropol. 9: 201–218.
Diebold, A. R. (1968). Anthropological perspectives: Anthropology and the comparative psychology of communicative behavior. In Sebeok, T. A. (ed.), Animal Communication, Indiana University Press, Bloomington, IN.
Flechtner, K. M., Steinacher, B., Sauer, R., and Mackert, A. (1997). Smooth pursuit eye movements in schizophrenia and affective disorders. Psychol. Med. 27(6): 1411–1419.
Galdikas, B. M. F. (1984). Adult female sociality among wild orangutans at Tanjung Puting Reserve. In Small, M. (ed.), Female Primates: Studies by Women Primatologist, Alan R. Liss, New York.
Galdikas, B. M. F. (1985a). Adult male sociality and reproductive tactics among orangutans at Tanjung-Puting Borneo Indonesia. Folia Primatol. 45(1): 9–24.
Galdikas, B. M. F. (1985b). Subadult male orangutan sociality and reproductive behavior at Tanjung Putting. Am. J. Primatol. 8(2): 87–100.
Galdikas, B. M., and Insley, S. J. (1988). The fast call of the adult male orangutan. J. Mammal. 69(2): 371–375.
Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behaviour, The Belknap Press, Cambridge, MA.
Goodenough, J., McGuire, B., and Wallace, R. (1993). Perspectives on Animal Behavior,Wiley, New York.
Gó mez, J. C. (1996). Ostensive behavior in great apes: The role of eye contact. In Russon, A. E., Bard, K. A., and Parker, S. T. (eds.), Reaching into Thought. The Minds of the Great Apes, Cambridge University Press, Cambridge.
Gó mez, J.C., and Teixidor, P. (eds.). (1992). Theory of mind in an orangutan:Anonverbal test of false-belief appreciation? In Abstracts. XIVth Congress of the International Primatological Society, International Primatological Society, Strasbourg, France.
Gregory, R., and Hopkins, P. (1974). Pupils of a talking parrot. Nature 252: 637–638.
Hauser, M. D. (1993). Right hemisphere dominance for the production of facial expression in monkeys. Science 261: 475–477.
Hess, E. H. (1965). Attitude and pupil size. Sci Am. (April) 212: 46–54.
Hinchcliffe, M., Lancashire, M., and Robers, F. J. (1970). Eye-contact and depression: A preliminary report. Br. J. Psychiatry 117: 571–572.
Hinde, R. A., and Rowell, T. E. (1962). Communication by posture and facial expression in the rhesus monkey. Proc. Zool. Soc. Lond. 138: 1–21.
Hindmarch, I. (1973). Eyes, eye-spots and pupil dilation in nonverbal communication. In Cranach, M.V., and Vine, I. (eds.), Social Communication and Movement, Academic Press, London.
Hook-Costigan, M., and Rogers, L. J. (1998). Lateralized use of the mouth in production of vocalization by marmosets. Neuropsychologia 36: 1265–1273.
Hutt, C., and Ounsted, C. (1966). The biological significance of gaze aversion with particular reference to the syndrome of infantile autism. Behav. Sci. 11: 346–356.
Ishizuka, K., Kashiwakura, M., and Oiji, A. (1998). Eye movements in patients with schizophrenia: Visual stimuli, semantic content and psychiatric symptoms. Acta Psychiatr. Scand. 97(5): 364–373.
Kano, T. (1980). Social behavior of wild pygmy chimpanzees (Pan paniscus) of Wamba: A preliminary Report. J. Hum. Evol. 9: 243–260.
Kaplan, G., & Rogers, L. J. (1994). Orang-Utans in Borneo, University of New England Press, Armidale.
Kaplan, G., and Rogers, L. J. (1996). Eye-gaze avoidance and learning in orang-utans. In Abstracts. International Society for Comparative Psychology Conference, Concordia University, Montreal.
Kaplan, G., and Rogers, L. J. (2000). The Orang-Utans, Perseus, New York.
Kobayashi, H., and Koshima, S. (1997). Unique morphology of the human eye. Nature 387: 767–768.
Kojima, T., Matsushima, E., Ando, K., Ando, H., Sakurada, M., Ohta, K., Moriya, H., and Shimazono, Y. (1992). Exploratory eye movements and neuropsychological tests in schizophrenic patients. Schizophr. Bull. 18(1): 85–94.
LeCompte, W. F., and Rosenfeld, H. M. (1971). Effects of minimal eye contact in the instruction period on impressions of the experimenter. J. Exp. Soc. Psychol. 7: 211–220.
MacKinnon, J. (1974). In Search of the Red Ape,William Collins, London.
Malaspina, D., Amador, X. F., Coleman, E. A., Mayr, T. L., Friedman, J. H., and Sackeim, H. A. (1994). Smooth pursuit eye movement abnormality in severe major depression. Effects of ECT and clinical recovery. J. Neuropsychiatry Clin. Neurosci. 6(1): 36–42.
Marler, P. (1968). Aggregation and dispersal: Two functions in primate communication. In Jay, P. C. (ed.), Primates: Studies in Adaptation and Variability, Holt, Rinehart and Winston, New York.
Matsushima, E., Kojima, T., Ohta, K., Obayashi, S., Nakajima, K., Kakuma, T., Ando, H., Ando, K., and Toru, M. (1998). Exploratory eye movement dysfunctions in patients with schizophrenia-possibility as a discriminator for schizophrenia. J. Psychiatr. Res. 32(5): 289–295.
Miles, H. L. (1990). The cognitive foundations for reference in a signing orangutan. In Parker, S. T., and Gibson, K. R. (eds.), ”Language” and Intelligence in Monkeys and Apes: Comparative Developmental Perspectives, Cambridge University Press, Cambridge, UK, pp. 511–539.
Miller, R. E. (1971). Experimental studies of communication in the monkey. In Rosenblum, L. A. (ed.), Primate Behavior: Developments in Field and Laboratory Research, Vol. II, Academic Press, New York.
Mitani, J. C. (1985). Sexual selection and adult male orangutan pongo-pygmaeus long calls. Anim. Behav. 33: 272–283.
Mitani, J. C., Grether, G. F., Rodman, P. S., and Priatna, D. (1991). Associations among wild orang-utans: Sociality, passive aggressions or chance? Anim. Behav. 42: 33–46.
Mitchell, G. (1972). Looking behavior in the rhesus monkey. J. Phenomenol. Psychol. 3: 53–67.
Napier, J. R., and Napier, P.H. (1985). The Natural History of Primates, MIT Press, Cambridge, MA.
Normile, D. (1998). Habitat seen playing larger role in shaping behavior. Science 279: 1454–1455.
Oppenheimer, J.R. (1977). Communication in new world monkeys. In Sebeok, T. A. (ed.), How Animals Communicate, Indiana University Press, Bloomington, IN, pp. 851–889.
Povinelli, D. J. (1998). Animal Self-Awareness: A Debate. Can Animals Empathize? Maybe Not. Sci. Am. http://www.sciam.com/1998/1198intelligence/1198povinelli.html, 1- 8.
Redican, W. K. (1975). Facial Expressions in Nonhuman Primates. In Rosenblum, L. A. (ed.), Primate Behavior. Developments in Field and Laboratory Research,Vol. 4, Academic Press, New York, pp. 103–194.
Riemer, M. D. (1949). The averted gaze. Psychiatr. Q. 23: 108–115.
Rijksen, H.D. (1978). A Field Study of Sumatran Orangutans (Pongo pygmaeus abelli): Ecology, Behaviour and Conservation, Veenman & Zonen, Wageningen, The Netherlands.
Rijksen, H.D., and Meijaard, E. (1999). OurVanishing Relative. The Status of Wild Orang-Utans at the Close of the Twentieth Century, Kluwer, Dordrecht, The Netherlands.
Rogers, L. J. (1998). Minds of Their Own. Thinking and Awareness in Animals, Westview Publishers, Colorado.
Rogers, L. J., and Kaplan, G. (1996). Hand preferences and other lateral biases in rehabilitant orang-utans (Pongo pygmaeus pygmaeus). Anim. Behav. 51: 13–25.
Rogers, L. J., and Kaplan, G. (2000). Songs, Roars and Rituals. Communication in Birds, Mammals and other Animals, Harvard University Press, Cambridge, UK.
Sackeim, H. A., Gur, R. C., and Saucy, M. L. (1978). Emotions are expressed more intensely on the left side of the face. Science 202: 434–436.
Schaller, G. B. (1963). The Mountain Gorilla: Ecology and Behavior, University of Chicago Press, Chicago.
Shapiro, G., and Galdikas, B.M. F. (1995).Attentiveness in orangutans within the sign learning context. In Nadler, R. D., Galdikas, B. F. M., Sheeran, L. K., and Rosen, N. (eds.), The Neglected Ape, Plenum Press, New York.
Sweeny, J. A., Strojwas, M. H., Mann, J. J., and Thase, M. E. (1998). Prefrontal and cerebellar abnormalities in major depression: Evidence from oculomotor studies. Biol. Psychiatry 43(8): 584–594.
Sweeny, J. A., Luna, B., Haas, G. L., Keshavan, M. S., Mann, J. J., and Thase, M. E. (1999). Pursuit tracking impairments in schizophrenia and mood disorders: Step-ramp studies with unmedicated patients. Biol. Psychiatry 46(5): 671–680.
Sugardjito, J., te Boekhorst, I. J. A., and van Hoof, J. A. R. A.M. (1987). Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. Int. J. Primatol. 8(1): 17–41.
Tinbergen, N. (1959). Comparative studies of the behaviour of gulls (Laridae): A progress report. Behaviour 15: 1–70.
Utami, S. S., Wich, S. A., Sterck, E. H. M., and van Hooff, J.A.R.A.M. (1997). Food competition between wild orang-utans in large fig trees. Int. J. Primatol. 18: 909–927.
Van Hooff, J. A. R. A. M. (1972). A comparative approach to the phylogeny of laughter and smiling. In Hinde, R. A. (ed.), Non-Verbal Communication, Cambridge University Press, Cambridge, pp. 209–241.
Van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates 40(1): 69–86.
Wada, J. A. (1961). Modification of cortically induced responses in brain stem of shift of attention in monkeys. Science 133: 40–42.
Whiten, A., and Byrne, R. W. (1988). Tactical deception in primates. Behav. Brain Sci. 11: 233–273.
Winkler, L. A. (1989). Morphology and relationships of the orangutan fatty cheek pads. Am. J. Primatol. 17(4): 305- 320.
Yamagiwa, J. (1992). Functional Analysis of Social Staring Behavior in an All-male Group of Mountain Gorillas. Primates 33(4): 523–544.
Young, G., and Décarie, T. G. (1977). An ethology-based catalogue of facial/vocal behaviour in infancy. Anim. Behav. 25: 95–107.
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Kaplan, G., Rogers, L.J. Patterns of Gazing in Orangutans (Pongo pygmaeus). International Journal of Primatology 23, 501–526 (2002). https://doi.org/10.1023/A:1014913532057
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DOI: https://doi.org/10.1023/A:1014913532057