Skip to main content
SpringerLink
Log in

Mating Tactics in Response to Costs Incurred by Mating with Multiple Males in Wild Female Japanese Macaques

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

We investigated the costs of mating with multiple males in terms of feeding time, traveling distances, sexual proceptivity, and male aggression, for wild female (Macaca fuscata yakui) on Yakushima Island, Japan. We analyzed all-day focal sampling data from 7 females during the mating season (Sept.-Nov. 1996). On days when estrous females copulated with multiple males, they decreased their feeding time to half that of anestrous days, traveled longer distances, showed more proceptive sexual behaviors and received more aggression from subordinate males than on days when they copulated with only the 1st-ranking male. On days when females copulated with only the 1st-ranking male, they showed no difference in feeding time with that of anestrous days, and expended less effort than the above mating pattern because of short traveling distances, diminished sexual proceptivity and a lower frequency of aggression received. The results suggest that the costs of estrous vary according to female sexual proceptivity and the number and social status of mating partners. Female Japanese macaques exhibit a mixed mating strategy over prolonged estrous periods, which may provide females with opportunities to maximize the benefits of copulating with multiple males and to minimize the costs of estrus by mating with only the 1st-ranking male. During an estrous cycle, females may be adjusting efforts for reproduction and survival; i.e., mating vs. feeding.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Albert, S. C., Altmann, J., and Wilson, M. L. (1996). Mate guarding constrains foraging activity of male baboons. Anim. Behav. 51: 1269-1277.

    Google Scholar 

  • Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour 49: 227-265.

    Google Scholar 

  • Arnqvist, G. (1989). Multiple mating in a water strider: Mutual benefits or intersexual conflict? Anim. Behav. 38: 749-756.

    Google Scholar 

  • Aujard, F., Heistermann, M., Thierry, B., and Hodges, J. K. (1998). Functional significance of behavioral morphological and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am. J. Primatol. 46: 285-309.

    Google Scholar 

  • Beach, F. A. (1976). Sexual attractivity proceptivity and receptivity in female mammals. Horm. and Behav. 7: 105-138.

    Google Scholar 

  • Bercovitch, F. B. (1983). Time budgets and consortships in olive baboons (Papio anubis).Folia Primatol. 41: 180-190.

    Google Scholar 

  • Bercovitch, F. B. (1987). Female weight and reproductive condition in a population of olive baboons (Papio anubis).Am. J. Primatol. 12: 189-195.

    Google Scholar 

  • Bercovitch, F. B., Lebron, M. R., Martinez, H. S., and Kessler, M. J. (1998). Primigravidity body weight and costs of rearing first offspring in rhesus macaques. Am. J. Primatol. 46: 135-144.

    Google Scholar 

  • Bielert, C., and Busse, C. (1983). Influences of ovarian hormones on the food intake and feeding of captive and wild female chacma baboons (Papio ursinus).Physiol. Behav. 30: 103-111.

    Google Scholar 

  • Brereton, A. R. (1992). Alternative reproductive tactics in stumptail macaques (Macaca arctoides).Folia Primatol. 59: 209-212.

    Google Scholar 

  • Brereton, A. R. (1994). Return-benefit spite hypothesis: An explanation for sexual interference in stumptail macaques (Macaca arctoides).Primates 35: 123-136.

    Google Scholar 

  • Bulger, J. B. (1993). Dominance rank and access to estrous females in male savanna baboons. Behaviour 127: 67-103.

    Google Scholar 

  • Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F., and Partridge, L. (1995). Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241-244.

    Google Scholar 

  • Czaja, J. A., and Goy, R. W. (1975). Ovarian hormones and food intake in female guinea pigs and rhesus monkeys. Horm. Behav. 6: 329-349.

    Google Scholar 

  • Daly, M. (1978). The cost of mating. Am. Nat. 112: 771-774.

    Google Scholar 

  • Dixson, A. F. (1997). Evolutionary perspectives on primate mating systems and behavior. Ann. N. Y. Acad. Sci. 807: 42-61.

    Google Scholar 

  • Dixson, A. F. (1998). Primate Sexuality, Oxford University Press, New York.

    Google Scholar 

  • Dwass, M. (1960). Some k-sample rank-order tests. In Olkin, I. (ed.), Contributions to Probability and Statistics Stanford University Press, California, pp. 198-202.

    Google Scholar 

  • Enomoto, T. (1974). The sexual behavior of Japanese monkeys. J. Hum. Evol. 3: 351-372.

    Google Scholar 

  • Enomoto, T. (1979). On the correlation between sexual behavior and ovarian hormone level during the menstrual cycle in captive Japanese monkeys. Primates 20: 563-570.

    Google Scholar 

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

    Google Scholar 

  • Furuichi, T. (1985). Inter-male associations in a wild Japanese macaque troop on Yakushima Island Japan. Primates 26: 219-237.

    Google Scholar 

  • Furuichi, T. (1987). Sexual swelling receptivity and grouping of wild pygmy chimpanzee females at Wamba Zaire. Primates 28: 309-318.

    Google Scholar 

  • Hasegawa, T. (1990). Sex differences in ranging patterns. In Nishida, T (ed.), The Chimpanzees of the Mahale Mountains, University of Tokyo Press, Tokyo, pp. 99-114.

    Google Scholar 

  • Hausfater, G. (1975). Dominance and Reproduction in Baboons (Papio cynocephalus): A Quantitative Analysis, S. Karger, Basel, Switzerland.

    Google Scholar 

  • Hogg, J. T. (1984). Mating in bighorn sheep: Multiple creative male strategies. Science 225: 526-528.

    Google Scholar 

  • Hrdy, S. B. (1977). Infanticide as a primate reproductive strategy. Am. Sci. 65: 40-49.

    Google Scholar 

  • Huffman, M. A. (1987). Consort intrusion and female male choice in Japanese macaques (Macaca fuscata).Ethology 75: 221-234.

    Google Scholar 

  • Huffman, M. A. (1991). Mate selection and partner preference in female Japanese macaques. In Fedigan, L. M., and Asquith, P. (eds.), The Monkeys of Arashiyama. Thirty-Five Years of Study in the East and West, State University of 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.

    Google Scholar 

  • Kurland, J. A. (1977). Kin selection in the Japanese monkey. In Szalay, E. S. (ed.), Contributions to Primatology, Vol. 12, S. Karger, New York, pp. 1-145.

    Google Scholar 

  • Manson, J. H. (1997). Primate consortships. Curr. Anthropol. 38: 353-374.

    Google Scholar 

  • Maruhashi, T. (1980). Feeding behavior and diet of the Japanese monkeys (Macaca fuscata yakui) on Yakushima Island Japan. Primates 21: 141-160.

    Google Scholar 

  • Maruhashi, T. (1982). An ecological study of troop fissions of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island Japan. Primates 23: 317-337.

    Google Scholar 

  • Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int. J. Primatol. 24: 1057-1075.

    Google Scholar 

  • Matsumoto-Oda, A., and Oda, R. (1998). Changes in the activity budget of cycling female chimpanzees. Am. J. Primatol. 46: 157-166.

    Google Scholar 

  • Milton, K. (1985). Mating patterns of wooly spider monkeys Brachyteles arachnoides: Implications for female choice. Behav. Ecol. Sociobiol. 17: 53-59.

    Google Scholar 

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

    Google Scholar 

  • Mori, A., Yamaguchi, N., Watanabe, K., Shimizu, K. (1997). Japanese macaques under poor nutritional conditions and food-enhanced perineal swelling in the Koshima troop. Int. J. Primatol. 18: 553-579.

    Google Scholar 

  • Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58: 229-246.

    Google Scholar 

  • Okayasu, N. (1992). Prolonged estrus in female Japanese macaques (Macaca fuscata yakui) and the social influence on estrus: With special reference to male intertroop movement. In Itoigawa, N., Sugiyama, Y., Sackett, G. P., and Thompson, R. K. R. (eds.), Topics in Primatology 2, University of Tokyo Press, Tokyo, pp. 163-178.

    Google Scholar 

  • Parker, G. A. (1984). Human sperm competition. In Smith, R. L. (ed.), Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, Orlando, Tokyo, pp. 601-659.

    Google Scholar 

  • Paul, A. (2002). Sexual selection and mate choice. Int. J. Primatol. 23: 877-904.

    Google Scholar 

  • Reynolds, J. D., and Gross, M. R. (1990). Costs and benefits of female mate choice: Is there a lek paradox? Am. Nat. 136: 230-243.

    Google Scholar 

  • Saayman, G. S. (1970). The menstrual cycle and sexual behavior in a troop of free ranging Chacma baboons (Papio ursinus).Folia. Primatol. 12: 81-110.

    Google Scholar 

  • Small, M. F. (1988). Female primate sexual behavior and conception: Are there really sperm to spare? Curr. Anthropol. 29: 81-100.

    Google Scholar 

  • Smuts, B. B. (1987). Sexual competition and mate choice. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 385-399.

    Google Scholar 

  • Smuts, B. B., and Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: Evidence and theoretical implications. Adv. Stud. Behav. 22: 1-63.

    Google Scholar 

  • Soltis, J. (1999). Measuring male–female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui).Primates 40: 453-467.

    Google Scholar 

  • Soltis, J. (2002). Do primate female gain nonprocreative benefits by mating with multiple males? Theoretical and empirical considerations. Evol. Anthropol. 11: 187-197.

    Google Scholar 

  • Soltis, J., and McElreath, R. (2001). Can females gain extra paternal investment by mating with multiple males? A game theoretic approach. Am. Nat. 158: 519-529.

    Google Scholar 

  • Soltis, J., Mitsunaga, F., Shimizu, K., Nozaki, M., Yanagihara, Y., Domingo-Roura, X., and Takenaka, O. (1997a). Sexual selection in Japanese macaques I: Female mate choice and male–male competition. Anim. Behav. 54: 725-736.

    Google Scholar 

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

    Google Scholar 

  • Sprague, D. S. (1998). Topographic effects on measures of monkey habitat-use in a mountainous study site in Japan. Am. J. Phys. Anthropol. 26: 207.

    Google Scholar 

  • Sprague, D. S., Suzuki, S., Takahashi, H., and Sato, S. (1998). Male life history in natural populations of Japanese macaques: Migration, dominance rank, and troop participation of males in two habitats. Primates 39: 351-363.

    Google Scholar 

  • Steel, R. D. G. (1960). A rank sum test for comparing all pairs of treatments. Technometrics 2: 197-207.

    Google Scholar 

  • Sugiyama, Y. (1965). On the social charge of hanuman langurs (Presbytis entellus) in their natural condition. Primates 6: 213-247.

    Google Scholar 

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

    Google Scholar 

  • Takahata, Y., Huffman, M. A., Suzuki, S., Koyama, N., and Yamagiwa, J. (1999). Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies. Primates 40: 143-158.

    Google Scholar 

  • Tardif, S. D., and Jaquish, C. E. (1994). The common marmoset as a model for nutritional impacts upon reproduction. Ann. N. Y. Acad. Sci. 709: 214-215.

    Google Scholar 

  • Taub, D. M. (1980). Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus).In Lindburg, D. G. (ed.), The Macaques: Studies in Ecology, Behavior and Evolution, Van Nostrand Reinhold, New York, pp. 287-344.

    Google Scholar 

  • Taylor, C. R., Schmidt-Nielsen, K., and Raab, J. L. (1970). Scaling of energetic cost of running to body size in mammals. Am. J. Physiol. 219: 1104-1107.

    Google Scholar 

  • Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii).Behav. Ecol. Sociobiol. 6: 29-38.

    Google Scholar 

  • van Noordwijk, M. A., and van Schaik, C. P. (2000). Reproductive patterns in eutherian mammals: Adaptations against infanticide? In Schaik, C. P., and Janson, C. H. (eds.), Infanticide by Males and its Consequences, Cambridge University Press, Cambridge, pp. 322-360.

    Google Scholar 

  • Wada, K., Moriya, K., Hara, K., and Ohsawa, W. (1975). On the body fat of Japanese monkeys inhabiting the Shiga Heights (in Japanese with English summary). Physiol. Ecol. Jpn. 16: 104-107.

    Google Scholar 

  • Walker, M. L., Gordon, T. P., and Wilson, M. E. (1983). Menstrual cycle characteristics of seasonally breeding rhesus monkeys. Biol. Reprod. 29: 841-848.

    Google Scholar 

  • Wrangham, R. W. (1979). Sex differences in chimpanzee dispersion. In Hamburg, D. A., and McCown, E. R. (eds.), The Great Apes, Benjamin/Cummings Publication, Menlo Park, CA, pp. 481-489.

    Google Scholar 

  • Yamagiwa, J. (1985). Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca fuscata yakui) Yakushima Island Japan. Primates 26: 105-120.

    Google Scholar 

  • Yamagiwa, J., and Hill, D. A. (1998). Intraspecific variation in the social organization of Japanese macaques: Past and present scope of field studies in natural habitats. Primates 39: 257-273.

    Google Scholar 

  • Yasui, Y. (1998). The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol. Evol. 13: 246-250.

    Google Scholar 

  • Yoshihiro, S., Ohtake, M., Matsubara, H., Zamma, K., Hanya, G., Tanimura, Y., Kubota, H., Kubo, R., Arakane, T., Hirata, T., Furukawa, M., Sato, A., and Takahata, Y. (1999). Vertical distribution of wild Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island Japan: Preliminary report. Primates 40: 409-415.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Human Evolution Studies, Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto, 606-8502, Japan

    Miki Matsubara

  2. Ecological Management Unit, Ecosystems Group, National Institute for Agro-Environmental Sciences, Japan

    David S. Sprague

Authors
  1. Miki Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David S. Sprague
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matsubara, M., Sprague, D.S. Mating Tactics in Response to Costs Incurred by Mating with Multiple Males in Wild Female Japanese Macaques. International Journal of Primatology 25, 901–917 (2004). https://doi.org/10.1023/B:IJOP.0000029128.00559.91

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:IJOP.0000029128.00559.91

Search

Navigation