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Mothering Style and Infant Behavioral Development in Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) in China

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Abstract

Considerable variation in mothering styles is found among primate species, which may be directly related to species-typical differences in social structure, dominance style, patterns of infant development, and rates of intragroup aggression. We predicted that, as egalitarian Asian colobines, mothers of Yunnan snub-nosed monkeys (Rhinopithecus bieti) would adopt a mothering style characterized by low restrictiveness and low rejection. We followed six mother–infant dyads in a provisioned group of Rhinopithecus bieti inhabiting the Baimaxueshan National Nature Reserve, Yunnan, China, and collected 717.2 h of observational data on maternal care and infant development. In the first month after birth, infants were completely dependent on their mothers for nutrition and movement. They began to locomote clumsily during their second month of life. Mothers restricted the movements of their infants only during their first 2 mo of life. Maternal rejection occurred infrequently and never exceeded a mean of two events per hour for a given infant over any 1-mo period. Most rejections were mild, and did not result in a cessation of nursing. Infants were not weaned when they were 12 mo old. Our study offers support for the contention that females of Rhinopithecus bieti adopt a relaxed mothering style in caring for offspring during their first year of life.

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References

  • Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 69, 227–267.

    Article  Google Scholar 

  • Altmann, J. (1980). Baboon mothers and infants. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Bardi, M., Shimizu, K., Fujita, S., Borgognini-Tarli, S., & Huffman, M. A. (2001). Hormonal correlates of maternal style in captive macaques (Macaca fuscata and M. mulatta). International Journal of Primatology, 22, 647–662.

    Article  Google Scholar 

  • Bercovitch, F. B. (2002). Sex-biased parental investment in primates. International Journal of Primatology, 23, 905–921.

    Article  Google Scholar 

  • Berman, C. M. (1980). Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Animal Behaviour, 28, 860–873.

    Article  Google Scholar 

  • Cameron, E. Z. (1998). Is suckling behaviour a useful predictor of milk intake? A review. Animal Behaviour, 56, 521–532.

    Article  PubMed  Google Scholar 

  • Cameron, E. Z., Stafford, K. J., Linklater, W. L., & Veltman, C. J. (1999). Suckling behaviour does not measure milk intake in horses, Equus caballus. Animal Behaviour, 57, 673–678.

    Article  PubMed  Google Scholar 

  • Cui, L., Sheng, A., He, S., & Xiao, W. (2006). Birth seasonality and interbirth interval of captive Rhinopithecus bieti. American Journal of Primatology, 68, 457–463.

    Article  PubMed  Google Scholar 

  • de Waal, F. B. M., & Luttrell, L. M. (1989). Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptail macaques. American Journal of Primatology, 19, 83–109.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1991). Functional significance of social grooming in primates. Folia Primatology, 57, 121–131.

    Article  Google Scholar 

  • Dunbar, R. I. M., & Dunbar, P. (1988). Maternal time budgets of gelada baboons. Animal Behaviour, 36, 970–980.

    Article  Google Scholar 

  • Fairbanks, L. A., & McGuire, M. T. (1987). Mother-infant relationships in vervet monkeys: response to new adult males. International Journal of Primatology, 8, 351–366.

    Article  Google Scholar 

  • Forster, S., & Cords, M. (2002). Development of mother-infant relationships and infant behavior in wild blue monkeys (Cercopithecus mitis stuhlmanni). In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaption in African monkeys (pp. 245–272). New York: Kluwer Academic.

    Google Scholar 

  • Grueter, C. C. (2004). Conflict and postconflict behaviour in captive black-and-white snub-nosed monkeys (Rhinopithecus bieti). Primates, 45, 197–200.

    Google Scholar 

  • Grueter, C. C., Li, D., Ren, B., Wei, F., Xiang, Z., & van Schaik, C. P. (2009). Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. American Journal of Physical Anthropology, 140, 700–715.

    Article  PubMed  Google Scholar 

  • Grueter, C. C., Li, D., & Ren, B. (2013). Insights into the social system of Yunnan snub-nosed monkeys. In C. L. Tan, C. C. Grueter, & B. W. Wright (Eds.), Odd-nosed monkeys: Recent advances in the study of the forgotten colobines. New York: Springer.

    Google Scholar 

  • Hinde, R. A., and Simpson, M. J. A. (1975). Qualities of mother-infant relationships in monkeys.In (CIBA Symposium 33) "Parent-Infant Interaction" pp. 39-67. Elsevier, Amsterdam.

  • Hinde, R. A., & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour, 15, 169–196.

    Article  PubMed  CAS  Google Scholar 

  • Hinde, R. A., Rowell, T. E., & Spencer-Booth, Y. (1964). Behaviour of socially living rhesus monkeys in their first six months. Proceedings of the Zoological Society of London, 143, 609–649.

    Article  Google Scholar 

  • Hrdy, S. B. (1999). Mother nature: A history of mothers infants, and natural selection. New York: Pantheon Books.

    Google Scholar 

  • Huang, Z., Cui, L., Scott, M. B., Wang, S., & Xiao, W. (2012). Seasonality of reproduction of wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan, China. Primates, 53, 237–245.

    Article  PubMed  Google Scholar 

  • Kappeler, P. M., Pereira, M. E., & van Schaik, C. P. (2003). Primate life histories and socioecology. In P. M. Kappeler & M. E. Pereira (Eds.), Primate life histories and socioecology (pp. 1–20). Chicago: University of Chicago Press.

    Google Scholar 

  • Keverne, E. B., Martensz, N. D., & Tuite, B. (1989). Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology, 14, 155–161.

    Article  PubMed  CAS  Google Scholar 

  • Kirkpatrick, R. C. (1996). Ecology and behavior of the Yunnan snub-nosed langur (Rhinopithecus bieti, Colobinae). Ph.D. dissertation, University of California, Davis.

  • Kirkpatrick, R. C. (2007). The Asian colobines: Diversity among leaf-eating monkeys. In C. J. Campbell, A. Fuentes, C. K. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 186–200). Oxford: Oxford University Press.

    Google Scholar 

  • Kirkpatrick, R. C., Long, Y., Zhong, T., & Xiao, L. (1998). Social organization and range use in the Yunnan snub-nosed monkey Rhinopithecus bieti. International Journal of Primatology, 19, 13–51.

    Article  Google Scholar 

  • Kirkpatrick, R. C., Zou, R., Dierenfeld, E. S., & Zhou, H. (2001). Digestion of selected foods by Yunnan snub-nosed monkey Rhinopithecus bieti (Colobinae). American Journal of Physical Anthropology, 114, 156–162.

    Article  PubMed  CAS  Google Scholar 

  • Lee, P. C. (1996). The meaning of weaning: Growth, lactation, and life history. Evolutionary Anthropology, 5, 87–96.

    Article  Google Scholar 

  • Li, Y., Li, B., & Tan, C. L. (2005). Behavioral development within one-year-old individuals of Sichuan snub-nosed monkeys Rhinopithecus roxellana in the Qinling Mountains. Acta Zoologica Sinica, 51, 953–960.

    Google Scholar 

  • Li, D., Grueter, C. C., Ren, B., Long, Y., Li, M., Peng, Z., & Wei, F. (2008). Ranging of Rhinopithecus bieti in the Samage Forest, China. II. Use of land cover types and altitudes. International Journal of Primatology, 29, 1147–1173.

    Article  Google Scholar 

  • Li, D., Ren, B., Grueter, C. C., Li, B., & Li, M. (2010). Noctural sleeping habits of the Yunnan snub-nosed monkey in Xiangguqing, China. American Journal of Primatology, 72, 1092–1099.

    Article  PubMed  Google Scholar 

  • Li, Y., Guo, S., Ji, W., He, G., Wang, X., & Li, B. (2011). Social play behavior in infant Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Qinling Mountains, China. American Journal of Primatology, 73, 845–851.

    Article  PubMed  Google Scholar 

  • Long, Y., Kirkpartrick, C. R., Zhong, T., & Xiao, L. (1994). Report on the distribution, population, and ecology of the Yunnan snub-nosed monkeys (Rhinopithecus bieti). Primates, 35, 241–250.

    Article  Google Scholar 

  • Maestripieri, D. (1993a). Maternal anxiety in rhesus macaques (Macaca mulatta). I. Measurement of anxiety and identification of anxiety-eliciting situations. Ethology, 95, 19–31.

    Article  Google Scholar 

  • Maestripieri, D. (1993b). Maternal anxiety in rhesus macaques (Macaca mulatta). II. Emotional bases of individual differences in mothering style. Ethology, 95, 32–42.

    Article  Google Scholar 

  • Maestripieri, D. (1994a). Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides). I. Development of the mother-infant relationship in the first three months. Behaviour, 131, 75–96.

    Article  Google Scholar 

  • Maestripieri, D. (1994b). Social structure, infant handling, and mothering styles in group-living old world monkeys. International Journal of Primatology, 15, 531–553.

    Article  Google Scholar 

  • Martin, P., & Bateson, P. (1993). Measuring behaviour: An introductory guide. Cambridge, U.K.: Cambridge University Press.

    Book  Google Scholar 

  • Mithchell, G. (1979). Behavioral sex differences in nonhuman primates. New York: Van Nostrand Reinhold.

    Google Scholar 

  • Moore, J. (1992). Dispersal, nepotism, and primate social behavior. International Journal of Primatology, 13, 361–378.

    Article  Google Scholar 

  • Newton, P. N., & Dunbar, R. I. M. (1994). Colobine monkey society. In G. Davies & J. Oates (Eds.), Colobine monkeys: Their ecology, behaviour, and evolution (pp. 311–346). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Nicolson, N. A. (1987). Infants, mothers, and other females. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhasaker (Eds.), Primate societies (pp. 330–342). Chicago: University of Chicago Press.

    Google Scholar 

  • Poirier, E. E. (1968). The Nilgiri langur (Presbytis johnii) mother-infant dyad. Primates, 9, 45–68.

    Article  Google Scholar 

  • Ren, B., Li, D., He, X., Qiu, J., & Li, M. (2011). Female resistance to invading males increases infanticide in langurs. PLoS One, 6, 1–4.

    Article  Google Scholar 

  • Ross, C. (1998). Primate life histories. Evolution Anthropology, 6, 54–63.

    Article  Google Scholar 

  • Simpson, M. J. A., & Howe, S. (1980). The interpretation of individual differences in rhesus monkey infants. Behaviour, 72, 127–155.

    Article  Google Scholar 

  • Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291–309.

    Article  Google Scholar 

  • Struhsaker, T. T., & Leland, L. (1987). Colobines: infanticide by adult males. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 83–97). Chicago: University of Chicago Press.

    Google Scholar 

  • Su, Y., Ren, R., Qi, H., Liang, B., & Bao, W. (1992). Development of social relationship of infant golden monkeys in breeding group: a case study. Acta Psychologica Sinica, 24, 66–72.

    Google Scholar 

  • Sugiyama, Y. (1965). Behavioral development and social structure in two troops of Hanuman langurs (Presbytis entellus). Primates, 6, 213–247.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Thierry, B. (1990). Feedback loop between kinship and dominance: the macaque model. Journal of Theoretical Biology, 145, 511–521.

    Article  PubMed  CAS  Google Scholar 

  • Trivers, R. L. (1974). Parent-offspring conflict. American Zoologist, 14, 249–264.

    Google Scholar 

  • Xiang, Z., & 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.

    Article  PubMed  Google Scholar 

  • Xiang, Z., & Sayers, K. (2009). Reports on seasonality of mating and birth events in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Xiaochangdu, Tibet. Primates, 50, 50–55.

    Article  PubMed  Google Scholar 

  • Yeager, C. P., & Kool, K. (2000). The behavioral ecology of Asian colobines. In P. F. Whitehead & C. J. Jolly (Eds.), Old world monkeys (pp. 496–521). Cambridge, U.K.: Cambridge University Press.

    Chapter  Google Scholar 

  • Zhang, Y. (2012). Female-female relationships of Yunnan snub-nosed monkeys (Rhinopithecus bieti) within one-male units. Master’s thesis. Beijing: University of Chinese Academy of Sciences.

  • Zhao, Q., Tan, C. L., & Pan, W. (2008). Weaning age, infant care, and behavioral development in Trachypithecus leucocephalus. International Journal of Primatology, 29, 583–591.

    Article  Google Scholar 

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Acknowledgments

This study was supported by Project of Public Benefit (201104073), the Natural Science Foundation of China (No. 30970442), and the State Forestry Administration of China. We thank the Baimaxueshan National Nature Reserve for work permits. Special thanks are due to Prof. Paul Garber (University of Illinois), Dr. Cyril Grueter (University of Western Australia), and two anonymous reviewers for their valuable comments and English revision for the manuscript. We are very grateful to our field assistants for data collection.

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Authors and Affiliations

  1. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China

    Tengfei Li, Baoping Ren, Dayong Li, Pingfen Zhu & Ming Li

  2. Graduate School of the University of Chinese Academy of Sciences, Beijing, 100049, China

    Tengfei Li & Pingfen Zhu

  3. College of Life Sciences, China West Normal University, Nanchong, Sichuan, 637002, China

    Dayong Li

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  1. Tengfei Li
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Correspondence to Ming Li.

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Li, T., Ren, B., Li, D. et al. Mothering Style and Infant Behavioral Development in Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti) in China. Int J Primatol 34, 681–695 (2013). https://doi.org/10.1007/s10764-013-9687-7

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