International Journal of Primatology

, Volume 37, Issue 2, pp 175–184 | Cite as

Male Infanticide in the Golden Snub-Nosed Monkey (Rhinopithecus roxellana), a Seasonally Breeding Primate

  • Hui Yao
  • Huiliang Yu
  • Banghe Yang
  • Wangji Yang
  • Haiqing Xu
  • Cyril C. Grueter
  • Ming Li
  • Zuofu Xiang
Article

Abstract

In nonhuman primates, infanticide by adult males can occur when the leader male is ousted from a one-male, multifemale group, or when male dominance rank changes within a multimale, multifemale group. According to the sexual selection hypothesis, this behavior may be adaptive if perpetrators increase their reproductive success by killing unrelated, unweaned infants, thus shortening the interbirth interval of the mother, and then siring her next infant. Under an alternative hypothesis, infanticide is a byproduct of aggressive male–male competition and these predictions do not hold. Direct observations of the context surrounding infanticide in free-ranging primate populations that allow a test of these predictions are rare. Here, we document four cases of male infanticide and report paternity data for a group of golden snub-nosed monkeys (Rhinopithecus roxellana) at Shennongjia, China. Three cases of infanticide by new leader males supported the predictions of the sexual selection hypothesis, while another provides partial support for the sexual selection hypothesis, but can also be explained via a nonadaptive hypothesis. In this latter case, a male from an all-male group killed an infant during an aggressive episode that appeared to be accidental, as it took place 7 mo before a male takeover happened, and the perpetrator did not obtain any reproductive advantage. We conclude that most male infanticide events in golden snub-nosed monkeys are consistent with the adaptive selection sexual hypothesis.

Keywords

Male infanticide Rhinopithecus roxellana Sexual selection hypothesis 

References

  1. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–267.CrossRefPubMedGoogle Scholar
  2. Bartlett, T. Q., Sussman, R. W., & Cheverud, J. M. (1993). Infant killing in primates: a review of observed cases with specific reference to the sexual selection hypothesis. American Anthropologist, 95, 958–990.CrossRefGoogle Scholar
  3. Bellemain, E., Swenson, J. E., & Taberlet, P. (2006). Mating strategies in relation to sexually selected infanticide in a non-social carnivore: the Brown Bear. Ethology, 112, 238–246.CrossRefGoogle Scholar
  4. Borries, C. (1997). Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal). Behavioral Ecology and Sociobiology, 41, 139–150.CrossRefGoogle Scholar
  5. Borries, C., Launhardt, K., Epplen, C., Epplen, J. T., & Winkler, P. (1999). DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys. Proceedings of the Royal Society of London B: Biological Sciences, 266, 901–904.CrossRefGoogle Scholar
  6. Bronson, F. H. (1989). Mammalian reproductive biology. Chicago: University of Chicago Press.Google Scholar
  7. Cords, M., & Fuller, J. L. (2010). Infanticide in Cercopithecus mitis stuhlmanni in the Kakamega Forest, Kenya: variation in the occurrence of an adaptive behavior. International Journal of Primatology, 31, 409–431.CrossRefGoogle Scholar
  8. Grueter, C. C. (2013). The biology of snub-nosed monkeys, douc langurs, proboscis monkeys and simakobu. Hauppauge: Nova.Google Scholar
  9. Guo, S., Ji, W., Li, M., Chang, H., & Li, B. (2010). The mating system of the Sichuan snub-nosed monkey (Rhinopithecus roxellana). American Journal of Primatology, 72, 25–32.CrossRefPubMedGoogle Scholar
  10. Hrdy, S. B. (1974). Male-male competition and infanticide among the langurs (Prebytis entellus) of Abu, Rajasthan. Folia Primatologica, 22, 19–58.CrossRefGoogle Scholar
  11. Hrdy, S. B. (1979). Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology, 1, 13–40.CrossRefGoogle Scholar
  12. Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16, 1099–1106.CrossRefPubMedGoogle Scholar
  13. Lukas, D., & Huchard, E. (2014). The evolution of infanticide by males in mammalian societies. Science, 346(6211), 841–844.CrossRefPubMedGoogle Scholar
  14. Palombit, R. A. (2012). Infanticide: Male strategies and female counterstrategies. In J. C. Mitani, J. P. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), Evolution of primate societies (pp. 432–468). Chicago: University of Chicago Press.Google Scholar
  15. Qi, H. J., Liang, B., Bao, W. Y., Jia, Y. C., Hama, N., Czekala, N. M., & Harvey, N. C. (1995).The hormone change in the urine of female snub-nosed monkeys. ActaTheriologica Sinica, 15(2), 106–112.Google Scholar
  16. Qi, X. G., Li, B. G., Garber, P. A., Ji, W., & Watanabe, K. (2009). Social dynamics of the golden snub-nosed monkey (Rhinopithecusroxellana): female transfer and one-male unit succession. American Journal of Primatology, 71, 670–679.CrossRefPubMedGoogle Scholar
  17. Ren, B., Li, D., He, X., Qiu, J., & Li, M. (2011). Female resistance to invading males increases infanticide in Langurs. PLoS ONE, 6(4), e18971.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Soltis, J., Thomsen, R., Matsubayashi, K., & Takenaka, O. (2000). Infanticide by resident males and female counter-strategies in wild Japanese macaques (Macacafuscata). Behavioral Ecology and Sociobiology, 48, 195–202.CrossRefGoogle Scholar
  19. Sussman, R. W., Cheverud, J. M., & Bartlett, T. Q. (1995). Infant killing as an evolutionary strategy: reality or myth? Evolutionary Anthropology, 3, 149–151.CrossRefGoogle Scholar
  20. van Schaik, C. P. (2000). Vulnerability to infanticide by males: Patterns among mammals. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 61–71). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  21. Wright, P. C. (1995). Demography and life history of free-ranging Propithecus diadema edwardsii in Ranomafana National Park, Madagascar. International Journal of Primatology, 16, 835–854.CrossRefGoogle Scholar
  22. Xiang, Z. F., & Grueter, C. C. (2007). First direct evidence of infanticide and cannibalism in wild snub-nosed monkeys (Rhinopithecus bieti). American Journal of Primatology, 69, 249–254.CrossRefPubMedGoogle Scholar
  23. Xiang, Z. F., Yang, B. H., Yu, Y., Yao, H., Grueter, C. C., Garber, P. A., & Li, M. (2014). Males collectively defend their one-male units against bachelor males in a multi-level primate society. American Journal of Primatology, 76, 609–617.CrossRefPubMedGoogle Scholar
  24. Yan, C. E., Jiang, Z. G., Li, C. W., Zen, Y., Tan, N. N., & Xia, S. Z. (2003). Monitoring the menstrual cycle and pregnancy in the Sichuan golden monkey (Rhinopithecus roxellana) by measuring urinary estradiol and progesterone. Acta Zoologica Sinica, 49, 693–697.Google Scholar
  25. Yang, B., Ren, B., Xiang, Z., Yang, J., Yao, H., Garber, P. A., & Li, M. (2014). Major histocompatibility complex and mate choice in the polygynous primate: the Sichuan snub-nosed monkey (Rhinopithecus roxellana). Integrative Zoology. doi:10.1111/1749-4877.12084.Google Scholar
  26. Yao, H., Liu, X., Standford, C., & Li, Y. (2011). Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China. American Journal of Primatology, 73, 1280–1288.CrossRefPubMedGoogle Scholar
  27. Yu, Y., Xiang, Z. F., Yao, H., Grueter, C. C., & Li, M. (2013). Female snub-nosed monkeys exchange grooming for sex and infant handling. PLoS ONE, 8(9), e74822.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Zhang, S. Y., Liang, B., & Wang, L. X. (1999). Infanticide within captive groups of Sichuan golden snub-nosed monkeys (Rhinopithecus roxellana). Folia Primatologica, 70, 274–276.CrossRefGoogle Scholar
  29. Zhao, D., Li, B., Li, Y., & Wada, K. (2005). Extra-unit sexual behaviour among wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatologica, 76, 172–176.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Hui Yao
    • 1
    • 2
  • Huiliang Yu
    • 2
  • Banghe Yang
    • 3
  • Wangji Yang
    • 2
  • Haiqing Xu
    • 2
  • Cyril C. Grueter
    • 4
  • Ming Li
    • 3
  • Zuofu Xiang
    • 1
  1. 1.College of Life Science and TechnologyCentral South University of Forestry & TechnologyChangshaChina
  2. 2.Key Lab of Conservation Biology for Shennongjia Golden Monkey, Hubei ProvinceShennongjia Forest DistrictChina
  3. 3.Key Lab of Animal Ecology and Conservation Biology, Institute of ZoologyChinese Academy of SciencesBeijingChina
  4. 4.School of Anatomy, Physiology, and Human BiologyThe University of Western AustraliaCrawleyAustralia

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