Skip to main content
SpringerLink
Log in

Unusual behaviour in grey woolly monkeys (Lagothrix cana): Females breastfeeding adult males

  • Short Communication
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Weaning varies between primate species, usually occurring long before adulthood. Here we report adult female woolly monkeys, Lagothrix cana, breastfeeding adult males. From March to June 2013, a study was conducted on a group of 18 grey woolly monkeys, L. cana, living in an ex situ conservation area. During the observation period, five breastfeeding events between adults were observed. The events involved two adult females and two adult males. Although our findings generally correlate with current literature on allonursing, the nursee far exceeded the expected age. Thus, we propose three hypotheses that may explain the occurrence of this adult nursing behaviour: (1) extended maternal care, (2) opportunistic foraging and (3) forming of alliances. The most likely explanation for our observations is that the female woolly monkeys use breastfeeding to move up or maintain the hierarchy, through alliances with top-ranking males. This study adds to our understanding of a little-studied, endangered primate, as well as the costs and benefits of breastfeeding behaviour.

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

References

  • Altmann, J., 1974. Observational study of behavior: sampling methods. Behavior 48, 227–267.

    Article  Google Scholar 

  • Baldovino, M.C., Di Bitetti, M.S., 2008. Allonursing intufted capuchin monkeys (Cebus nigritus): milk or pacifier? Folia Primatol. 79, 79–92.

    Article  Google Scholar 

  • Barlett, A., 2005. Maternal sexuality and breastfeeding. Sex Educ. 5, 67–77.

    Article  Google Scholar 

  • Bergstrom, M.L., Fedigan, L.M., 2010. Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability. Behaviour 147, 899–931.

    Article  Google Scholar 

  • Boubli, J.P., Di Fiore, A., Rylands, A.B., Wallace, R.B., 2008. IUCN Red List of Threatened Species. Version 2012.2, Retrieved 18.03.13. Lagothrix cana: https://doi.org/www.iucnredlist.org

  • Buss, D.H., 1971. Isolation and partial characterization of lysozyme from baboon milk. Biochim. Biophys. Acta 236, 587–592.

    Article  CAS  Google Scholar 

  • Charnov, E.L., 1976. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–136.

    Article  CAS  Google Scholar 

  • Clutton-Brock, T.H., Albon, S.D., Guiness, F.E., 1984. Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308, 358–360.

    Article  Google Scholar 

  • Coe, C.L., Lubach, G., Ershler, W.B., 1989. Immunological consequences of maternal separation in infant primates. New Dir. Child Adolesc. Dev. 45, 65–91.

    Article  Google Scholar 

  • Feng, X., Wang, L., Yang, S., Qin, D., Wang, J., Li, C., Lv, L., Ma, Y., Hu, X., 2012. Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys. PNAS, https://doi.org/10.1073/pnas.1010943108.

    Article  CAS  Google Scholar 

  • Gittleman, J.L., Thompson, S.D., 1988. Energy allocation in mammalian reproduction. Am. Zool. 28, 863–875.

    Article  Google Scholar 

  • Heiduck, S., 1997. Food choice in masked titi monkeys (Callicebus per-sonatus melanochir): selectivity or opportunism? Int. J. Primatol. 18, 487–502.

    Google Scholar 

  • Hennessy, M.B., O’Leary, S.K., Hawke, J.L., Wilson, S.E., 2002. Social influences on cortisol and behavioral responses of preweaning, periadolescent, and adult guinea pigs. Physiol. Behav. 76, 305–314.

    Article  CAS  Google Scholar 

  • Hosey, G.R., 2005. How does the zoo environment affect the behavior of captive primates? Appl. Anim. Behav. Sci. 90, 107–129.

    Article  Google Scholar 

  • Hrdy, S.B., 2010. Estimating the Prevalence of Shared Care and Cooperative Breeding in the Order Primates, an Appendix to Mothers and Others: The Evolutionary Origins of Mutual Understanding. Harvard University Press, Cambridge.

    Google Scholar 

  • Iwagana, S., Ferrari, S.F., 2002. Geographic distribution and abundance of woolly (Lagothrix cana) and spider (Ateles chamek) monkeys in southwestern Brazilian Amazonia. Am. J. Primatol. 56, 57–64.

    Article  Google Scholar 

  • Jovanic, T., Maestripieri, D., 2010. Effects of early traumatic experience on vocal expression of emotion in young female rhesus macaques. Dev. Psychobiol. 52, 794–801.

    Article  Google Scholar 

  • Kennedy, G.E., 2005. From the ape’s dilemma to the weanling’s dilemma: early weaning and its evolutionary context. J. Hum. Evol. 48, 123–145.

    Article  CAS  Google Scholar 

  • Klinowska, M., 1991. Dolphins, Porpoises and Whales of the World. The IUCN Red Data Book. IUCN, Gland Switzerland and Cambridge, UK.

    Google Scholar 

  • Kumashiro, M., Ishibashi, H., Uchiyama, Y., Itakura, S., Murata, A., Iriki, A., 2003. Natural imitation induced by joint attention in Japanese monkeys. Int. J. Psychol. 50, 81–99.

    Google Scholar 

  • Laudenslager, M.L., Reite, M., Harbeck, R.J., 1982. Suppressed immune response in infant monkeys associated with maternal separation. Behav. Neural. Biol. 36, 40–48.

    Article  CAS  Google Scholar 

  • Lee, P.C., Moss, C.J., 1986. Early maternal investment in male and female African elephant calves. Behav. Ecol. Sociobiol. 18, 353–361.

    Article  Google Scholar 

  • Lee, P.C., 1997. The meanings of weaning: growth, lactation, and life history. Evol. Anthropol. 5, 87–96.

    Article  Google Scholar 

  • Leung, E.S., Vergara, V., Barrett-Lennard, L.G., 2010. Allonursing in captive belugas (Delphinapterus leucas). Zoo. Biol. 29, 633–637.

    Article  Google Scholar 

  • Moro-Rios, R.J., Miranda, J.M., Passos, C.F., 2009. Relaçõessociais, emigraçãoe fissão de um grupo de Alouatta guariba clamittans em um remanescente de floresta ombrófila mista. Neotrop. Primates 16, 57–60.

    Article  Google Scholar 

  • McClellen, H.L., Miller, S.J., Hartmann, P.E., 2008. Evolution of lactation: nutrition v. protection with special reference to five mammalian species. Nutr. Res. Rev. 21, 97–116.

    Google Scholar 

  • McKenna, J.J., 1979. The evolution of allomothering behavior among colobine monkeys: function and opportunism in evolution. Am. Anthropol. Assoc. 81, 818–840.

    Article  Google Scholar 

  • Nishimura, A., 1994. Social interaction patterns of woolly monkeys (Lagothrix lagothricha): a comparison among the Atelines. Sci. Eng. Rev. Doshisha Univ. 35, 91–110.

    Google Scholar 

  • Peres, C.A., 1991. Humboldt’s woolly monkeys decimated by hunting in Amazonia. Oryx 25, 89–95.

    Article  Google Scholar 

  • Peres, C., 1994. Diet and feeding ecology of gray woolly monkeys (Lagothrix lagothricha cana) in central Amazonia: comparisons with other Atelines. Int. J. Primatol. 15, 333–372.

    Article  Google Scholar 

  • Perry, S., 2011. Social traditions and social learning in capuchin monkeys (Cebus). Phil. Trans. 366, 988–996.

    Article  Google Scholar 

  • Ramirez, M., 1988. The woolly monkeys, genus Lagothrix. In: Coimbra-Filho, A.F., Mittermeier, R.A. (Eds.), Ecology and Behaviour of Neotropical Primates. WWF, Washington, DC, pp. 539–575.

    Google Scholar 

  • Ren, B., Li, D., Garber, P.A., Li, M., 2012. Evidence of allomaternal nursing across one-male units in the Yunnan Snub-Nosed Monkey (Rhinopithecus bieti). PLoS ONE 7, e30041.

    Article  CAS  Google Scholar 

  • Roulin, A., 2002. Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Anim. Behav. 63, 201–208.

    Article  Google Scholar 

  • Stanley, C.R., Shultz, S., 2012. Mummy’s boys: sex differential maternal-offspring bonds in semi-feral horses. Behaviour 149, 251–274.

    Article  Google Scholar 

  • Stone, S., Bakwin, H., 1948. Breast-feeding. J. Pediatr. 33, 660–667.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Bárbara Cartagena-Matos & Mariana Cravo-Mota

  2. Biology Institute, Federal University of Bahia, Rua Barão de Jeremoabo, 147, Campus de Ondina, CEP 40170-290, Salvador, Bahia, Brazil

    Hilton Ferreira Japyassú

  3. School of Biological Sciences, University of Bristol, Woodland Road, BS8 1UG, Bristol, UK

    Bruna Martins Bezerra

  4. Department of Zoology, Federal University of Pernambuco, Avenida Prof. Moraes Rego, 1235, Cidade Universitária, CEP 50670-901, Recife, PE, Brazil

    Bruna Martins Bezerra

Authors
  1. Bárbara Cartagena-Matos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hilton Ferreira Japyassú
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariana Cravo-Mota
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruna Martins Bezerra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bárbara Cartagena-Matos.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cartagena-Matos, B., Japyassú, H.F., Cravo-Mota, M. et al. Unusual behaviour in grey woolly monkeys (Lagothrix cana): Females breastfeeding adult males. Mamm Biol 80, 59–62 (2015). https://doi.org/10.1016/j.mambio.2014.08.005

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2014.08.005

Keywords

Search

Navigation