The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Abstract

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.

This is a preview of subscription content, access via your institution.

References

  1. Altmann, J. 1980.Baboon Mothers and Infants. Harvard Univ. Press, Cambridge, Massachusetts.

    Google Scholar 

  2. Bakeman, R.;Gottman, J. M. 1986.Observing Interaction: An Introduction to Sequential Analysis. Cambridge Univ. Press, Cambridge.

    Google Scholar 

  3. Berman, C. M. 1980. Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs.Anim. Behav., 28: 860–873.

    Article  Google Scholar 

  4. Berman, C. M. 1984. Variation in mother-infant relationships: traditional and non-traditional factors. In:Female Primates: Studies by Women Primatologists,Small,M. F. (ed.), Alan Liss, New York, pp. 17–36.

    Google Scholar 

  5. Berman, C. M.;Rasmussen, K. L. R.;Suomi, S. J. 1997. Group size, infant development and social networks in free-ranging rhesus monkeys.Anim. Behav., 53: 405–421.

    Article  Google Scholar 

  6. Brown, G. R.;Dixson, A. F. 1999. Investigation of the role of postnatal testosterone in the expression of sex differences in behaviour in infant rhesus macaques (Macaca mulatta).Horm. Behav., 35: 186–194.

    PubMed  Article  CAS  Google Scholar 

  7. Cheney, D. L. 1978. The play partners of immature baboons.Anim. Behav., 26: 1038–1050.

    Article  Google Scholar 

  8. de Jonge, G.;Dienske, H.;van Luxemburg, E.;Ribbens, L. 1981. How rhesus monkey infants budget their time between mothers and peers.Anim. Behav., 29: 598–609.

    Article  Google Scholar 

  9. Dixson, A. F. 1977. Observations on the displays, menstrual cycles and sexual behaviour of the ‘black ape’ of Celebes (Macaca nigra).J. Zool. Lond., 182: 63–84.

    Article  Google Scholar 

  10. Fairbanks, L. A. 1988. Vervet monkey grandmothers: effects on mother-infant relationships.Behaviour, 104: 176–188.

    Google Scholar 

  11. Fedigan, L. 1972. Social and solitary play in a colony of vervet monkeys (Cercopithecus aethiops).Primates, 13: 347–364.

    Article  Google Scholar 

  12. Gard, G. C.;Meier, G. W. 1977. Social and contextual factors of play behaviour in sub-adult rhesus monkeys.Primates, 18: 367–377.

    Article  Google Scholar 

  13. Goldfoot, D. A.;Wallen, K. 1978. Development of gender role behaviors in heterosexual and isosexual groups of infant rhesus monkeys. In:Recent Advances in Primatology, Vol. 1: Behavior,Chivers,D. J.;Herbert,J. (eds.), Academic Press, London, pp. 155–159.

    Google Scholar 

  14. Goy, R. W.;McEwen, B. S. 1980.Sexual Differentiation of the Brain MIT Press, Cambridge, Massachusetts.

    Google Scholar 

  15. Hanby, J. P.;Brown, C. E. 1974. The development of sociosexual behaviors in Japanese macaques (Macaca fuscata).Behaviour, 49: 151–196.

    Google Scholar 

  16. Hauser, M. D.;Fairbanks, L. A. 1988. Mother-offspring conflict in vervet monkeys: variation in response to ecological conditions.Anim. Behav., 36: 802–813.

    Article  Google Scholar 

  17. Hinde, R. A.;Rowell, T. E.;Spencer-Booth, Y. 1964. Behaviour of socially living rhesus monkeys in their first six months.Proc. Zool. Soc. Lond., 143: 609–649.

    Google Scholar 

  18. Hinde, R. A.;Spencer-Booth, Y. 1967. The behaviour of socially living rhesus monkeys in their first two and a half years.Anim. Behav., 15: 169–196.

    PubMed  Article  CAS  Google Scholar 

  19. Hooley, J. M.;Simpson M. J. A. 1981. A comparison of primiparous and multiparous mother-infant dyads inMacaca mulatta Primates, 22: 379–392.

    Article  Google Scholar 

  20. Hooley, J. M.;Simpson, M. J. A. 1983. Influence of siblings on the infant's relationship with the mother and others. In:Primate Social Relationships: An Integrated Approach,Hinde,R. A. (ed.)., Blackwell Scientific Publ., Oxford, pp. 139–141.

    Google Scholar 

  21. Jensen, G. D.;Bobbitt, R. A.;Gordon, B. N. 1968. Sex differences in the development of independence of infant monkeys.Behaviour, 30: 1–14.

    PubMed  CAS  Google Scholar 

  22. Lee, P. C. 1984a. Early infant development and maternal care in free-ranging vervet monkeys.Primates, 25: 36–47.

    Article  Google Scholar 

  23. Lee, P. C. 1984b. Ecological constraints on the social development of vervet monkeys.Behaviour, 91: 245–262.

    Google Scholar 

  24. Maestripieri, D. 1998. Social and demographic influences on mothering style in pigtail macaques.Ethology, 104: 379–385.

    Article  Google Scholar 

  25. Martin, P.;Bateson, P. 1986.Measuring Behaviour: An Introductory Guide. Cambridge Univ. Press, Cambridge.

    Google Scholar 

  26. Mitchell, G. 1979.Behavioural Sex Differences in Nonhuman Primates. Van Nostrand Reinhold, New York.

    Google Scholar 

  27. Mitchell, G.;Brandt, E. M. 1970. Behavioral differences related to experience of mother and sex of infant in the rhesus monkey.Develop. Psychol., 3: 149.

    Article  Google Scholar 

  28. Mitchel, G.;Stevens, C. W. 1968. Primiparous and multiparous monkey mothers in a mildly stressful social situation: first three months.Develop. Psychobiol., 1: 280–286.

    Article  Google Scholar 

  29. Nakamichi, M. 1989. Sex differences in social development during the first four years in a free-ranging group of Japanese monkeys.Macaca fuscata. Anim. Behav., 38: 737–748.

    Article  Google Scholar 

  30. Nakamichi, M.;Cho, F.;Minami, T. 1990. Mother-infant interactions of wild-born, individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life.Primates, 31: 213–224.

    Article  Google Scholar 

  31. Nakamichi, M.;Minami, T.;Cho, F. 1996. Comparison between wild-born mother-female infant interactions and laboratory-born mother-female infant interactions during the first 14 weeks after birth in individually caged cynomolgus macaques.Primates, 37: 155–166.

    Article  Google Scholar 

  32. Nevison, C. M.;Brown, G. R.;Dixson, A. F. 1997. Effects of altering testosterone in early infancy on social behaviour in captive yearling rhesus monkeys.Phsiol. Behav., 62: 1397–1403.

    Article  CAS  Google Scholar 

  33. Nicolson, N. A. 1987. Infants, mothers, and other females. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 330–342.

    Google Scholar 

  34. Owens, N. W. 1973. The development of behaviour in free-living baboons,Papio anubis Unpubl. Ph.D. thesis, Univ. of Cambridge, Cambridge.

    Google Scholar 

  35. Owens, N. W. 1975. Social play behaviour in free-living baboons,Papio anubis.Anim. Behav., 23: 387–408.

    Article  Google Scholar 

  36. Rosenblum, L. A.;Nadler R. D. 1971. The ontogeny of sexual behavior in male bonnet macaques. In:Influence of Hormones on the Nervous System,Ford,D. H. (ed.), Karger, Basel, pp. 126–139.

    Google Scholar 

  37. Rowell, T. E.;Chism, J. 1986. The ontogeny of sex differences in the behavior of patas monkeys.Int. J. Primatol., 7: 83–107.

    Google Scholar 

  38. Schino, G.;D'Amato, F. R.;Troisi, A. 1995. Mother-infant relationships in Japanese macaques: sources of inter-individual variation.Anim. Behav., 49: 151–158.

    Article  Google Scholar 

  39. Seay, B. 1966. Maternal behavior in primiparous and multiparous rhesus monkeys.Folia Primatol., 4: 146–168.

    PubMed  CAS  Article  Google Scholar 

  40. Siegel, S.;Castellan, N. J. 1988.Nonparametric Stastistics for the Behavioural Sciences. McGraw-Hill, London.

    Google Scholar 

  41. Simpson, M. J. A. 1983. Effect of the sex of an infant on the mother-infant relationship and the mother's subsequent reproduction. In:Primate Social Relationships: An Integrated Approach,Hinde,R. A. (ed.), Blackwell, Oxford, pp. 53–57.

    Google Scholar 

  42. Simpson, M. J. A.;Gore, M. A.;Janus, M.;Rayment, F. D. G. 1989. Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year.Primates, 30: 493–509.

    Article  Google Scholar 

  43. Symons, D. 1978.Play and Aggression: A Study of Rhesus Monkeys. Columbia Univ. Press, New York.

    Google Scholar 

  44. Tanaka, I. 1989. Variability in the development of mother-infant relationships among free-ranging Japanese macaques.Primates, 30: 477–491.

    Article  Google Scholar 

  45. Tartabini, A.;Dienske, H. 1979. Social play and rank order in rhesus monkeys (Macaca mulatta).Behav. Process., 4: 375–383.

    Article  Google Scholar 

  46. Wallen, K. 1996. Nature needs nurture: the interaction of hormonal and social influences on the development of behavioral sex differences in rhesus monkeys.Horm. Behav., 30: 364–378.

    PubMed  Article  CAS  Google Scholar 

  47. Wallen, K.;Maestripieri, D.;Mann, D. R. 1995. Effects of neonatal testicular suppression with a GnRH antagonist on social behavior in group-living juvenile rhesus monkeys.Horm. Behav., 29: 322–337.

    PubMed  Article  CAS  Google Scholar 

  48. Wasser, L. M.;Wasser, S. K. 1995. Environmental variation and developmental rate among free ranging yellow baboons (Papio cynocephalus).Amer. J. Primatol., 35: 15–30.

    Article  Google Scholar 

  49. Zar, J. H. 1974.Biostastistical Analysis. Prentice-Hall, New Jersey.

    Google Scholar 

Download references

Author information

Affiliations

Authors

About this article

Cite this article

Brown, G.R., Dixson, A.F. The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta). Primates 41, 63–77 (2000). https://doi.org/10.1007/BF02557462

Download citation

Key Words

  • Sex differences
  • Infant development
  • Rhesus macaques