Volume 34 Issue 3
May  2013
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Shuang WANG, Jin-Hua LI, Dong-Po XIA, Yong ZHU, Bing-Hua SUN, Xi WANG, Lei ZHU. Male-to-female agonistic support for copulation in Tibetan macaques (Macaca thibetana) at Huangshan, China. Zoological Research, 2013, 34(3): 139-144. doi: 10.11813/j.issn.0254-5853.2013.3.0139
Citation: Shuang WANG, Jin-Hua LI, Dong-Po XIA, Yong ZHU, Bing-Hua SUN, Xi WANG, Lei ZHU. Male-to-female agonistic support for copulation in Tibetan macaques (Macaca thibetana) at Huangshan, China. Zoological Research, 2013, 34(3): 139-144. doi: 10.11813/j.issn.0254-5853.2013.3.0139

Male-to-female agonistic support for copulation in Tibetan macaques (Macaca thibetana) at Huangshan, China

doi: 10.11813/j.issn.0254-5853.2013.3.0139
  • Received Date: 2013-01-13
  • Rev Recd Date: 2013-04-20
  • Publish Date: 2013-06-08
  • Biological market theory predicts that animals exchange the same commodities, or interchange different ones, to their mutual benefit. Using focal and behavioral sampling methods and continuous recording techniques, we studied Tibetan macaques (Macaca thibetana) in two study groups (YA1 and YA2) at Huangshan, China to see whether adults interchanged male-to-female agonistic support for copulation. Overall, male-to-female agonistic support was significantly correlated with copulation behaviors when data from both study groups were combined. For YA1, copulations in post-agonistic support observation (PO) was greater, but not significantly so, than random observation (RO) in the breeding season, and copulation in PO was significantly greater than RO in the non-breeding season. For YA2 copulations in PO were significantly greater than RO in both breeding and non-breeding seasons. These results suggest that a male who extends post-agonistic support to a female is significantly more likely to copulate with her. Our study provides evidence for the existence of a biological market involving interchanged social behaviors. Our study also illuminates the reproductive strategies of male competition and female choice in this species.
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  • [1]
    Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour, 49(3): 227-267.
    Barrett L, Henzi SP. 2001. The utility of grooming in baboon trops. In: Noe R, van Hooff Jaram, Hammerstein P. Economics in Nature. Cambridge: Cambridge University Press, 119-145.
    Berman CM, Ionica CS, Li JH. 2004. Dominance style among Macaca thibetana on Mt. Huangshan, China. International Journal of Primatology, 25(6): 1283-1312.
    Chen R, Li JH, Zhu Y, Xia DP. 2008. Seasonal changes in aggressive behavior and fecal testosterone level in male Tibetan macaques Macaca thibitana at Huangshan, China. Acta Zoologica Sinica, 54(3): 393-398. [陈燃, 李进华, 朱勇, 夏东坡. 2008. 雄性黄山短尾猴攻击行为和粪便睾酮水平季节性变化. 动物学报, 54(3): 393-398.]
    Darwin C. 1871. The Descent of Man and Selection in Relation to Sex. New York: Modern Library.
    de Vries H. 1993. The rowwise correlation between two proximity matrices and the partial rowwise correlation. Psychometrika, 58(1): 53-69.
    de Waal FBM. 1984. Sex differences in the formation of coalitions among chimpanzees. Ethology and Sociobiology, 5(4): 239-255.
    Duffy KG, Wrangham RW, Silk JB. 2007. Male chimpanzees exchange political support for mating opportunities. Current Biology, 17(5): 586-587.
    Gomes CM, Boesch C, Allen C. 2009. Wild chimpanzees exchange meat for sex on a long-term basis. PloS ONE, 4(4): e5116.
    Gumert MD. 2007a. Payment for sex in a macaque mating market. Animal Behaviour, 74(6): 1655-1667.
    Gumert MD. 2007b. Grooming and infant handling interchange in Macaca fascicularis: the relationship between infant supply and grooming payment. International Journal of Primatology, 28(5): 1059-1074.
    Hemelrijk CK. 1990. Models of, and tests for, reciprocity, unidirectionality and other social interaction patterns at a group level. Animal Behaviour, 39(6): 1013-1029.
    Hemelrijk CK. 1994. Support for being groomed in long-tailed macaques, Macaca fascicularis. Animal Behaviour, 48(2): 479-481.
    Hemelrijk CK, Steinhauser J. 2007. Cooperation, coalition, and alliances. In: Henk W, Tattersall I. Handbook of Paleoanthropology, Part II. Berlin Heidelberg: Springer, 1321-1346.
    Koyama NF, Caws C, Aureli F. 2006. Interchange of grooming and agonistic support in chimpanzees. International Journal of Primatology, 27(5): 1293-1309.
    Li JH. 1999. The Tibetan Macaque Society: A Field Study. Hefei: Anhui University Press. [李进华. 1999. 野生短尾猴的社会. 合肥: 安徽大学出版社.]
    Li JH. 2000. Recognition of rank relationship by Tibetan Monkeys. Journal of Anhui University: Natural Science, 24(3): 116-120. [李进华. 2000. 短尾猴对顺位关系的认知. 安徽大学学报: 自然科学版, 24(3): 116-120.]
    Li JH, Wang QS, Han DM. 1996. Fission in a free-ranging Tibetan macaque group at Huangshan Mountain, China. Chinese Science Bulletin, 41: 1377-1381.
    Li JH, Yin HB, Wang QS. 2005. Seasonality of reproduction and sexual activity in female Tibetan macaques (Macaca thibetana) at Huangshan, China. Acta Zoologica Sinica, 51(3): 365-375.
    Li JH, Yin HB, Zhou LZ. 2007. Non-reproductive copulation behavior among Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates, 48(1): 64-72.
    McNamara JM, Barta Z, Fromhage L, Houston AI. 2008. The coevolution of choosiness and cooperation. Nature, 451(7175): 189-192.
    Mitani JC, Watts DP. 2001. Why do chimpanzees hunt and share meat? Animal Behaviour, 61(5): 915-924.
    Noë R, Sluijter AA. 1990. Reproductive tactics of male savanna baboons. Behaviour, 113(1): 117-170.
    Noë R, Hammerstein P. 1994. Biological market: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology, 35(1): 1-11.
    Noë R, Hammerstein P. 1995. Biological markets. Trends in Ecology & Evolution, 10(8): 336-339.
    Noë R, van Hooff JARAM, Hammerstein P. 2001. Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets. Cambridge: Cambridge University Press.
    Pastor-Nieto R. 2001. Grooming, kinship, and co-feeding in captive spider
    monkeys (Ateles geoffroyi). Zoo Biology, 20(4): 293-303.
    Pereira ME. 1989. Agonistic interactions of juvenile savanna baboons: II. Agonistic support and rank acquisition. Ethology, 80(1-4): 152-171.
    Perloe SI. 1992. Male mating competition, female choice and dominance in a free ranging group of Japanese macaques. Primates, 33(3): 289-304.
    Robbins MM. 1999. Male mating patterns in wild multimale mountain gorilla groups. Animal Behaviour, 57(5): 1013-1020.
    Schino G. 2007. Grooming and agonistic support: A meta-analysis of primate reciprocal altruism. Behavioral Ecology, 18(1): 115-120.
    Schino G, di Sorrentino EP, Tiddi B. 2007. Grooming and coalitions in Japanese macaques (Macaca fuscata): partner choice and the time frame of reciprocation. Journal of Comparative Psychology, 121(2): 181-188.
    Schino G, di Giuseppe F, Visalberghi E. 2009. Grooming, rank, and agonistic support in tufted capuchin monkeys. American Journal of Primatology, 71(2): 101-105.
    Seyfarth RM, Cheney DL. 1984. Grooming, alliances and reciprocal altruism in vervet monkeys. Nature, 308(5959): 541-542.
    Silk JB. 1992. The Patterning of intervention among male Bonnet Macaques: reciprocity, revenge, and loyalty. Current Anthropology, 33(3): 318-325.
    Smuts B. 1985. Sex and Friendship in Baboons. Cambridge: Cambridge University Press.
    Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y, Domingo-Roura X, Takenaka O. 1997. Sexual selection in Japanese macaques II: female mate choice and male-male competition. Animal Behaviour, 54(3): 737-746.
    Sterck EHM, Watts DP, van Schaik CP. 1997. The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41(5): 291-309.
    Trivers RL. 1971. The evolution of reciprocal altruism. The Quarterly Review of Biology, 46(1): 35-57.
    van Noordwijk MA. 1985. Sexual behaviour of Sumatran long-tailed macaques (Macaca fascicularis). Zeitschrift für Tierpsychologie, 70(4): 277-296.
    Ventura R, Majolo B, Koyama NF, Hardie S, Schino G. 2006. Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. American Journal of Primatology, 68(12): 1138-1149.
    Widdig A, Streich WJ, Tembrock G. 2000. Coalition formation among male Barbary macaques (Macaca sylvanus). American Journal of Primatology, 50(1): 37-51.
    Wrangham RW. 1980. An ecological model of female-bonded primate groups. Behaviour, 75(3): 262-299.
    Xia DP, Li JH, Garber PA, Sun LX, Zhu Y, Sun BH. 2012. Grooming reciprocity in female Tibetan macaques. American Journal of Primatology, 74(6):569-579.
    Xiong CP, Wang QS. 1991. Comparison of male sexual behaviors between Tibetan and Japanese macaques. Acta Theriologica Sinica, 11(1): 13-22. [熊成培, 王岐山. 1991. 短尾猴和日本猴雄性性行为的比较研究. 兽类学报, 11(1): 13-22.]
    Zhang M, Li JH, Zhu Y, Wang X, Wang S. 2010. Male mate choice in Tibetan macaques Macaca thibetana at Mt. Huangshan, China. Current Zoology, 56(2): 213-221.
    Zhu Y, Li JH, Xia DP, Chen R, Sun BH. 2008. Inbreeding avoidance by female Tibetan macaques Macaca thibetana at Huangshan, China. Acta Zoologica Sinica, 54(2): 183-190. [朱勇, 李进华, 夏东坡, 陈燃, 孙丙华. 2008. 雌性黄山短尾猴回避近亲交配. 动物学报, 54(2): 183-190.]
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