Skip to main content
Log in

Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies

  • Published:
Primates Aims and scope Submit manuscript

Abstract

There is wide interest in the effects of reproductive biology, mating partner preference, and rank on mating success (MS) and reproductive success (RS) in primates. In particular, theory stresses importance on the mechanisms for attaining RS. Most theory hedges on competitive ability and priority of access to resources, whether they be food or estrous females. However, the majority of data used in favor of such hypotheses come from relatively short-term studies. We review these hypotheses based on long-term data from provisioned and unprovisioned populations of Japanese macaques. Neither MS nor RS were consistently attained by high-ranking males and females. For males, female choice and mating partner preference is seen to over-ride most male-male competitive behaviors likely to affect MS and RS through priority of access to estrous females. Long-term mating patterns driven largely by female partner preferences, results in decreasing MS and RS for older higher-ranking males. The long-term trend for females to prefer less familiar or novel partners results in higher MS and RS for younger, middle-ranking males. The effects of this vary according to troop size and the duration of male tenure. For females, no consistent trend was recognized for rank related RS in either provisioned or unprovisioned troops. Non-reproductive mating may provide differential benefit to high-ranking females for access to limited food resources in some habitats but overall the relationship was inconclusive. Distribution and defendability of food resource, rather than provisioning per se may be more important.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altmann, S. A. 1962. A field study of the sociobiology of rhesus monkeys (Macaca mulatta).Ann. New York Acad. Sci. 102: 338–435.

    Article  CAS  Google Scholar 

  • Berard, J. 1999. A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta).Primates, 40: 159–175.

    Google Scholar 

  • Berard, J. D.;Nurnberg, P.;Epplen, J. T.;Schmidtke, J. 1994. Alternative reproductive tactics and reproductive success in male rhesus macaques.Behaviour, 129: 177–201.

    Google Scholar 

  • Bercovitch, F. B. 1992. Re-examining the relationship between rank and reproduction in male primates.Anim. Behav., 44: 1168–1170.

    Article  Google Scholar 

  • Bercovitch, F. B. 1997. Reproductive strategies of rhesus macaques.Primates, 38: 247–263.

    Article  Google Scholar 

  • Bercovitch, F. B.;Berard, J. D. 1993. Life history costs and consequences of rapid reproductive maturation in female rhesus macaques.Behav. Ecol. Sociobiol., 32: 103–109.

    Article  Google Scholar 

  • Carpenter, C. R. 1942. Sexual behaviour of free-ranging rhesus monkeys,Macaca mulatta, 1: Specimens, procedures, and behavioural characteristics of estrus.J. Comp. Psychol., 33: 113–142.

    Article  Google Scholar 

  • Chapais, B. 1983. Reproductive activity in relation to male dominance at the likelihood of ovulation in rhesus monkeys.Behav. Ecol. Sociobiol., 12: 215–228.

    Article  Google Scholar 

  • Chapais, B. 1986. Why do adult male and female rhesus monkeys affiliate during the birth season? In:The Cayo Santiago Macaques,Rawlins,R. G.;Kessler,M. J., (eds.), State Univ. New York Press, Albany, pp. 173–200.

    Google Scholar 

  • Chapais, B.;Mignault, C. 1991. Homosexual incest avoidance among females in captive Japanese macaques.Amer. J. Primatol., 23: 171–183.

    Article  Google Scholar 

  • Cheney, D. L.;Seyfarth, R. M.;Andelman, S. J.;Lee, P. C. 1988. Reproductive success in vervet monkeys. In:Reproductive Success,Clutton-Brock,T. H. (ed.), Univ. of Chicago Press, Chicago, pp. 384–402.

    Google Scholar 

  • Cowlishaw, G.;Dunbar, R. I. M. 1991. Dominance rank and mating success in male primates.Anim. Behav., 41: 1045–1056.

    Article  Google Scholar 

  • Dewsbury, D. A. 1982. Ejaculate cost and mate choice.Amer. Naturalist, 119: 601–610.

    Article  Google Scholar 

  • Enomoto, T. 1974. The sexual behavior of Japanese monkeys.J. Human Evol., 3: 351–372.

    Article  Google Scholar 

  • Enomoto, T. 1978. On social preference in sexual behavior of Japanese monkeys (Macaca fuscata).J. Human Evol., 7: 283–293.

    Article  Google Scholar 

  • Fedigan, L. M. 1983. Dominance and reproductive success in primates.Yrbk. Phys. Anthropol., 26: 91–129.

    Google Scholar 

  • Fedigan, L. M.;Fedigan, L.;Gouzoules, S.;Gouzoules, H.;Koyama, N. 1986. Lifetime reproductive success in female Japanese macaques.Folia Primatol., 47: 143–157.

    PubMed  CAS  Google Scholar 

  • Fedigan, L. M.;Gouzoules, H. 1978. The consort relationship in a troop of Japanese monkeys. In:Recent Advances in Primatology,Chivers,D. J.;Herbert,J. (eds), Academic Press, New York, pp. 493–495.

    Google Scholar 

  • Fredrickson, W. T.;Sackett, G. P. 1984. Kin preference in primates (Macaca nemestrina): relatedness or familiarity?J. Comp. Psychol., 98: 29–34.

    Article  Google Scholar 

  • Hanby, J. P.;Brown, C. E. 1974. The development of sociosexual behaviours in Japanese macaques,Macaca fuscata.Behaviour, 49: 152–196.

    PubMed  CAS  Google Scholar 

  • Harcourt, A. H. 1987. Dominance and fertility among female primates.J. Zool. Lond., 213: 471–487.

    Google Scholar 

  • Hasegawa, T. 1992. Mesu ni totte no rankon, (The evolution of female promiscuity: chimpanzees and Japanese macaques). In:Doubutsu-shakai niokeru Kyodo to Kogeki (Aggression and Cooperation among Animal Societies),Ito,Y. (ed.), Tokaidaigaku-shuppankai, Tokyo, pp. 223–250. (in Japanese)

    Google Scholar 

  • Hill, D. A. 1991. The patterns of affiliative relationships involving non-natal males in a troop of wild Japanese macaques (Macaca fuscata yakui) in Yakushima In:Primatology Today,Ehara,A.;Kimura,T.;Takenaka,O.;Iwamoto,M. (eds.), Elsevier, Amsterdam, pp. 211–214.

    Google Scholar 

  • Hrdy, S. B. 1981.The Woman That Never Evolved. Harvard Univ. Press, Cambridge, Massachusetts.

    Google Scholar 

  • Hrdy, S. B.;Whiten, P. L. 1987. Patterning of sexual activity. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. Chicago Press, Chicago, pp. 370–384.

    Google Scholar 

  • Huffman, M. A. 1987. Consort intrusion and female mate choice in Japanese macaquesEthology, 75: 221–234.

    Article  Google Scholar 

  • Huffman, M. A. 1991a. History of the Arashiyama Japanese macaques in Kyoto, Japan. In:The Monkeys of Arashiyama: Thirty-five Years of Research in Japan and the West,Fedigan,L. M.;Asquith,P. J. (eds.), State Univ. New York Press, Albany, pp. 21–53.

    Google Scholar 

  • Huffman, M. A. 1991b. Mate selection and partner preferences in female Japanese macaques. In:The Monkeys of Arashiyama: Thirty-five Years of Research in Japan and the West,Fedigan,L. M.;Asquith,P. J. (eds.), State Univ. New York Press, Albany, pp. 101–122.

    Google Scholar 

  • Huffman, M. A. 1992. Influences of female partner preference on potential reproductive outcome in Japanese macaques.Folia Primatol., 59: 77–88.

    Article  PubMed  CAS  Google Scholar 

  • Inoue, M. 1995. Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates.Human Evol., 10: 53–62.

    Article  Google Scholar 

  • Inoue, M.;Mitsunaga, F.;Nozaki, M.;Ohsawa, H.;Takenaka, A.;Sugiyama, Y.;Shimizu, K.;Takenaka, O. 1993. Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating.Primates, 34: 503–511.

    Article  Google Scholar 

  • Itani, J. 1972. A preliminary essay on the relationship between social organization and incest avoidance in nonhuman primates. In:Primate Socialization,Poirier,F. E. (ed.), Random House, New York, pp. 165–171.

    Google Scholar 

  • Itani, J. 1985. The evolution of primate social structures.Man, 20: 593–611.

    Article  Google Scholar 

  • Itoigawa, N.;Tanaka, T.;Ukai, N.;Fujii, H.;Kurokawa, T.;Koyama, T.;Ando, A.;Watanabe, Y.;Imakawa, S. 1992. Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama.Primates, 33: 49–68.

    Article  Google Scholar 

  • Kawai, M.;Azuma, S.;Yoshiba, K. 1967. Ecological studies of reproduction in Japanese monkeys (Macaca fuscata), I: Problems of the birth season.Primates, 8: 35–74.

    Article  Google Scholar 

  • Koyama, N.;Takahata, Y.;Huffman, M. A.;Norikoshi, K.;Suzuki, H. 1992. Reproductive parameters of female Japanese macaques thirty years data from the Arashiyama troops, Japan.Priamtes, 33: 33–47.

    Article  Google Scholar 

  • Kuester, J.;Paul, A.;Arnemann, J. 1994. Kinship, familiarity and mating avoidance in Barbary macaques,Macaca sylvanus.Anim. Behav., 48: 1183–1194.

    Article  Google Scholar 

  • Manson, J. P. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques.Anim. Behav., 44: 405–416.

    Article  Google Scholar 

  • Manson, J. P. 1995. Do female rhesus macaques choose novel males?Amer. J. Primatol., 37: 285–296.

    Article  Google Scholar 

  • McMillan, C. A. 1989. Male age, dominance and mating success among rhesus macaques.Amer. J. Phys. Anthropol., 80: 83–89.

    Article  CAS  Google Scholar 

  • Mitsunaga, F.;Nozaki, M.;Inoue, M.;Takenaka, O.;Sakura, O.;Sugiyama, Y.;Ohsawa, H. 1992. Steroid hormones and sexual behavior of female Japanese monkeys in an enclosed group. In:Topics in Primatology, Vol. 2.Itoigawa, N.;Sugiyama, Y.;Sackett, G. P.;Thompson, R. K. P. (eds.), Univ. of Tokyo Press Tokyo, pp. 23–34.

    Google Scholar 

  • Moore, J.;Ali, R. 1984. Are dispersal and inbreeding avoidance related?Anim. Behav., 32: 94–112.

    Article  Google Scholar 

  • Nigi, H.;Hayama, S.;Torii, R. 1990. Copulatory behavior unaccompanied by ovulation in the Japanese monkey (Macaca fuscata).Primates, 31: 243–250.

    Article  Google Scholar 

  • van Noordwijk, M. A.;van Schaik, C. P. 1999. The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaquesMacaca fascicularis.Primates, 40: 105–130.

    Google Scholar 

  • Nozaki, M. 1991. Mechanisms controlling seasonal breeding in Japanese monkeys.Primate Res., 7: 103–125. (in Japanese with English abstract)

    Article  Google Scholar 

  • Oi, T. 1996. Sexual behaviour and mating system of the wild pig-tailed macaque in West Sumatra. In:Evolution and Ecology of Macaque Societies,Fa,J. E.;Lindburg,D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 342–368.

    Google Scholar 

  • Okayasu, N. 1989a. Part 1: Prolonged and simultaneous estrus. In: Estrus and female mate choice during troop takeover in a wild Japanese macaque troop on Yakushima Island. Ph.D. diss., Kyoto Univ., Kyoto.

    Google Scholar 

  • Okayasu, N. 1989b. Part 2: Promiscuous mating and partner preference. In: Estrus and female mate choice during troop takeover in a wild Japanese macaque troop on Yakushima Island. Ph.D. diss., Kyoto Univ., Kyoto.

    Google Scholar 

  • Packer, C. 1979. Male dominance and reproductive activity inPapio anubis.Anim. behav., 27: 37–45.

    Article  PubMed  Google Scholar 

  • Paul, A.;Kuester, J. 1996. Differential reproduction in male and female Barbary macaques. In:Evolution and Ecology of Macaque Societies,Fa,J. E.;Lindburg,D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 293–317.

    Google Scholar 

  • Perloe, S. I. 1992. Male mating competition, female choice and dominance in a free ranging group of Japanese macaques.Primates, 33: 289–304.

    Article  Google Scholar 

  • van Schaik, C. P. 1983. Why are diurnal primates living in groups?Behaviour, 87: 120–144.

    Google Scholar 

  • van Schaik, C. P.;van Noordwijk, M. A.;de Boer, R. J.;den Tonkelaar, I. 1983. The effect of group size on time budges and social behaviour in wild long-tailed macaques (Macaca fascicularis).Behav. Evol. Sociobiol., 13: 173–181.

    Article  Google Scholar 

  • Silk, J. A. 1983. Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities.Amer. Naturalist, 121: 56–66.

    Article  Google Scholar 

  • Small, M. F. 1988. Female primate sexual behavior and conception.Cur. Anthropol., 29: 81–100.

    Article  Google Scholar 

  • Small, M. F. 1989. Female choice in nonhuman primates.Yrbk. Phys. Anthropol., 32: 103–127.

    Article  Google Scholar 

  • Smuts, B. B. 1983a. Dynamics of ‘special relationships’ between adult male and female olive baboons. In:Priamte Social RelationshipsHinde, R. A. (ed.), Blackwell, Oxford, pp. 112–116.

    Google Scholar 

  • Smuts, B. B. 1983b. ‘Special relationships’ between adult male and female olive baboons: selective advantages. In:Primate Social Relationships,Hinde,R. A. (ed.), Blackwell, Oxford, pp. 262–266.

    Google Scholar 

  • Soltis, J.;Mitsunaga, F.;Shimizu, K.;Nozaki, M.;Yanagihara, Y.;Domingo-Roura, Z.;Takenaka, O. 1997. Sexual selection in Japanese macaques, II: Female mate choice and male-male competition.Anim. Behav., 54: 737–746.

    Article  PubMed  Google Scholar 

  • Sprague, D. S. 1989. Male inter-troop movement during the mating season among the Japanese macaques of Yakushima Island, Japan. Ph.D. diss., Yale Univ., New Haven.

    Google Scholar 

  • Sprague, D. S. 1992. Life history and male inter-troop mobility among Japanese macaques (Macaca fuscata).Int. J. Priamtol., 13: 437–454.

    Article  Google Scholar 

  • Sprague, D. S. 1998. Age, dominance rank, natal status, and tenure among male macaquesAmer. J. Phys. Anthropol., 105: 511–521.

    Article  CAS  Google Scholar 

  • Stephenson, G. R. 1975. Social structure of mating activity in Japanese macaques. In:Proceedings from the Symposia of the Fifth Congress of the International Primatological Society, Nagoya, Japan, August 1974,Kondo,S.;Kawai,M.;Ehara,A.;Kawamura,S. (eds.), Japan Science Press, Tokyo, pp. 63–115.

    Google Scholar 

  • Sugiyama, Y.;Ohsawa, H. 1982. Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding.Folia Primatol., 39: 238–263.

    Article  PubMed  CAS  Google Scholar 

  • Takahata, Y. 1980. The reproductive biology of a free-ranging troop of Japanese monkeys.Primates, 21: 303–329.

    Article  Google Scholar 

  • Takahata, Y. 1982. The socio-sexual behavior of Japanese monkeys.Z. Tierpsychol., 59: 89–104.

    PubMed  CAS  Google Scholar 

  • Takahata, Y.;Suzuki, S.;Agetsuma, N.;Okayasu, N.;Sugiura, H.;Takahashi, H.;Yamagiwa, J.;Izawa, K.;Furuichi, T.;Hill, D. A.;Maruhashi, T.;Saito, C.;Sato, S.;Sprague, D. S. 1998a. Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report.Primates, 39: 339–349.

    Google Scholar 

  • Takahata, Y.;Suzuki, S.;Okayasu, N.;Sugiura, H.;Takahashi, H.;Yamagiwa, J.;Izawa, K.;Agetsuma, N.;Hill, D. A.;Saito, C.;Sato, S.;Tanaka, T.;Sprague, D. S. 1998b. Does troop size of wild Japanese macaques influece birth rate and infant mortality in the absence of predators?Primates, 39: 245–251.

    Google Scholar 

  • Tokuda, K. 1961–62. A study on the sexual behavior in the Japanese monkey troop.Primates, 3(2): 1–40.

    Article  Google Scholar 

  • Trivers, R. L.;Willard, D. E. 1973. Natural selection of parental ability to vary the sex ratio of offspring.Science, 179: 90–92.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe, K.;Mori, A.;Kawai, M. 1992. Characteristic features of the reproduction of Koshima monkeys,Macaca fuscata fuscata: a summary of 34 years of observation.Primates, 33: 1–32.

    Article  CAS  Google Scholar 

  • Westermarck, E. 1889.The History of Human Marriage. Allerton Press, New York.

    Google Scholar 

  • Wolf, W. P. 1995.Sexual Attraction and Childhood Association: A Chinese Brief forEdward Westermarck. Stanford Univ. Press, Stanford.

    Google Scholar 

  • Wolfe, L. D. 1984. Female rank and reproductive success among Arashiyama B Japanese macaques (Macaca fuscata).Int. J. Primatol., 5: 133–143.

    Google Scholar 

  • Wolfe, L. D. 1986. Sexual strategies of female Japanese macaques (Macaca fuscata).Human Evol., 1: 267–275

    Article  Google Scholar 

  • Wrangham, R. W. 1980. An ecological model of female-bonded primate groups.Behaviour, 75: 262–300.

    Google Scholar 

  • Zuckerman, S. 1932.The Social Life of Monkeys and Apes. Kegan Paul, London.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

About this article

Cite this article

Takahata, Y., Huffman, M.A., Suzuki, S. et al. Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies. Primates 40, 143–158 (1999). https://doi.org/10.1007/BF02557707

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02557707

Key Words

Navigation