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Female Reproductive Parameters in Wild Geladas (Theropithecus gelada)

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Abstract

Accurate data on reproductive parameters are essential for evaluating the adaptive and mechanistic bases of variation within and between species. Here, we combine fecal ovarian hormone analysis with measurements of sex skin swellings and reproductive behavior to describe female reproduction in geladas living in the Simien Mountains National Park, Ethiopia. We collected 10 years of reproductive data from 197 females across 36 units, with hormone data from a subset of these females (60 females from 16 units). First, we use these data to calculate age at maturation, age at first birth, interbirth interval, menstrual cycle length, gestation length, and duration of postpartum amenorrhea. Second, we present composite profiles of ovarian hormones, i.e., estrogens, progestogens, and sex skin measures across reproductive stages. Third, we examine whether ovarian hormones, sex skin phenotypes, and/or reproductive behaviors reliably reflect fertility or pregnancy in female geladas. The reproductive parameters calculated from our data were similar to those in previous studies on geladas and within the range of those for closely-related baboon species. We were able to reliably identify fertility and pregnancy using fecal estrogens only. The tumescent sex skin phenotypes and reproductive behaviors associated with fertility were also observed across all reproductive stages. We suggest that their presence outside of fertility may be a by-product of the flexibility needed for one or more female counterstrategies to infanticide.

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References

  • Altmann, J., Altmann, S. A., Hausfater, G., & McCuskey, S. A. (1977). Life history of yellow baboons: Physical development, reproductive parameters, and infant mortality. Primates, 18(2), 315–330.

    Article  Google Scholar 

  • Altmann, S. A. (1973). The pregnancy sign in savannah baboons. The Journal of Zoo Animal Medicine, 4(2), 8–12.

    Article  Google Scholar 

  • Altmann, S. A., & Altmann, J. (1970). Baboon ecology: African field research. Chicago: University of Chicago Press.

    Google Scholar 

  • Alvarez, F. (1973). Periodic changes in the bare skin areas of Theropithecus gelada. Primates, 14, 195–199.

    Article  Google Scholar 

  • Barrett, L., Henzi, S. P., & Lycett, J. E. (2006). Whose life is it anyway? Maternal investment, developmental trajectories, and life history strategies in baboons. In L. Swedell & S. R. Leigh (Eds.), Reproduction and fitness in baboons: Behavioral, life history, and life history perspectives (pp. 199–224). Developments in Primatology: Progress and Prospects. New York: Springer Science + Business Media.

  • Beach, F. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior, 7(1), 105–138.

    Article  CAS  PubMed  Google Scholar 

  • Beehner, J. C., & Bergman, T. J. (2008). Infant mortality following male takeovers in wild geladas. American Journal of Primatology, 70, 1–8.

    Article  Google Scholar 

  • Beehner, J. C., & McCann, C. (2008). Seasonal and altitudinal effects on glucocorticoid metabolites in a wild primate (Theropithecus gelada). Physiology & Behavior, 95(3), 508–514.

    Article  CAS  Google Scholar 

  • Beehner, J. C., Nguyen, N., Wango, E. O., Alberts, S. C., & Altmann, J. (2006). The endocrinology of pregnancy and fetal loss in wild baboons. Hormones and Behavior, 49, 688–699.

    Article  CAS  PubMed  Google Scholar 

  • Bentley-Condit, V. K., & Smith, E. O. (1997). Female reproductive parameters of Tana River yellow baboons. International Journal of Primatology, 18(4), 581–596.

    Article  Google Scholar 

  • Bercovitch, F. B., & Strum, S. C. (1993). Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behavioral Ecology and Sociobiology, 33, 313–318.

    Article  Google Scholar 

  • Borries, C., Gordon, A. D., & Koenig, A. (2013). Beware of primate life history data: a plea for data standards and a repository. PLoS ONE, 8(6), e67200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borries, C., Koenig, A., & Winkler, P. (2001). Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behavioral Ecology and Sociobiology, 50, 391–402.

    Article  Google Scholar 

  • Borries, C., Lu, A., Ossi-Lupo, K., Larney, E., & Koenig, A. (2011). Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. American Journal of Physical Anthropology, 144, 286–299.

    Article  PubMed  Google Scholar 

  • Brown, J. L. (1997). Faecal steroid analysis for monitoring ovarian and testicular function in diverse mild carnivore, primate and ungulate species. International Journal of Mammalian Biology, 62, 27–31.

    Google Scholar 

  • Cheney, D. L., Seyfarth, R. M., Fischer, J., Beehner, J., Bergman, T., et al. (2004). Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. International Journal of Primatology, 25, 401–428.

    Article  Google Scholar 

  • Czaja, J. A., Robinson, J. A., Eisele, S. G., Scheffler, G., & Goy, R. W. (1977). Relationship between sexual skin colour of female rhesus monkeys and midcycle plasma levels of oestradiol and progesterone. Journal of Reproduction and Fertility, 49, 147–150.

    Article  CAS  PubMed  Google Scholar 

  • Doran-Sheeny, D. M., Fernandez, D., & Borries, C. (2009). The strategic use of sex in wild female western gorillas. American Journal of Primatology, 71(12), 1011–1020.

    Article  Google Scholar 

  • Dubac, C., Brent, L. J. N., Accamando, A. K., Gerald, M. S., Maclarnon, A., et al. (2009). Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. International Journal of Primatology, 30, 777–789.

    Article  Google Scholar 

  • Dunbar, R. I., & Dunbar, P. (1974). The reproductive cycle of the gelada baboon. Animal Behaviour, 22(1), 203–210.

    Article  CAS  PubMed  Google Scholar 

  • Dunbar, R. I. M. (1977). Age-dependent changes in sexual skin colour and associated phenomena of female gelada baboons. Journal of Human Evolution, 6, 667–672.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1980). Demographic and life history variables of a population of gelada baboons (Theropithecus gelada). The Journal of Animal Ecology, 49(2), 485–506.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon social strategies. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Dunbar, R. I. M., & Dunbar, P. (1975). Social dynamics of gelada baboons. In H. Kuhn, W. P. Luckett, C. R. Noback, A. H. Schultz, D. Starck, & F. S. Szalay (Eds.), Contributions to primatology (pp. 1-157). Basel: S. Karger.

  • Engelhardt, A., Hodges, J. K., & Heistermann, M. (2007). Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance. Hormones and Behavior, 51, 3–10.

    Article  PubMed  Google Scholar 

  • Gesquiere, L. R., Wango, E. O., Alberts, S. C., & Altmann, J. (2007). Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Hormones and Behavior, 51, 114–125.

    Article  CAS  PubMed  Google Scholar 

  • Godfrey, L. R., Samonds, K. E., Jungers, W. L., Sutherland, M. R., & Irwin, M. T. (2004). Ontogenetic correlates of diet in Malagasy lemurs. American Journal of Physical Anthropology, 123, 250–276.

    Article  CAS  PubMed  Google Scholar 

  • Hausfater, G. (1975). Dominance and reproduction in baboons (Papio cynocephalus): A quantitative analysis. Contributions to primatology, Vol. 7. New York: S. Karger.

  • Higham, J. P., Heistermann, M., Ross, C., Semple, S., & MacLarnon, A. M. (2008a). The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates, 49, 295–299.

    Article  PubMed  Google Scholar 

  • Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M., & Semple, S. (2008b). Baboon sexual swellings: information content of size and color. Hormones and Behavior, 53, 452–462.

    Article  PubMed  Google Scholar 

  • Higham, J. P., Warren, Y., Adanu, J., Umaru, B. N., Maclarnon, A. M., et al. (2009). Living on the edge: life-history of olive baboons at Gashaka–Gumti National Park, Nigeria. American Journal of Primatology, 71, 293–304.

    Article  PubMed  Google Scholar 

  • Hill, R. A., Lycett, J. E., & Dunbar, R. I. M. (2000). Ecological and social determinants of birth intervals in baboons. Behavioral Ecology, 11(5), 560–564.

    Article  Google Scholar 

  • Hrdy, S. B. (1979). Infanticide among animals: a review, classification, and examination of the implications for reproductive strategies of females. Ethology and Sociobiology, 1, 13–40.

    Article  Google Scholar 

  • Hunter, C. P. (2001). Ecological determinants of gelada ranging patterns (Theropithecus gelada). Ph.D. thesis, University of Liverpool.

  • Kawai, M., Dunbar, R. I. M., Oshawa, H., & Mori, U. (1983). Social organization of gelada baboons: social units and definitions. Primates, 24, 13–24.

    Article  Google Scholar 

  • Kummer, H. (1968). Social organisation of hamadryas baboons: A field study. Basel and Chicago: S. Karger and University of Chicago Press.

  • le Roux, A., Beehner, J. C., & Bergman, T. J. (2011). Female philopatry and dominance patterns in wild geladas. American Journal of Primatology, 73, 422–430.

    Article  PubMed  Google Scholar 

  • Lu, A., Beehner, J. C., Czekala, N. M., Koenig, A., Larney, E., & Borries, C. (2011). Phytochemicals and reproductive function in wild female Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). Hormones and Behavior, 59, 28–36.

    Article  CAS  PubMed  Google Scholar 

  • Lu, A., Borries, C., Czekala, N. M., & Beehner, J. C. (2010). Reproductive characteristics of wild female Phayre’s leaf monkeys. American Journal of Primatology, 72(12), 1073–1081.

    Article  PubMed  Google Scholar 

  • Martin, R. D. (2007). The evolution of human reproduction: a primatological perspective. Yearbook of Physical Anthropology, 50, 59–84.

    Article  Google Scholar 

  • Matthews, L. H. (1956). The sexual skin of the gelada baboon (Theropithecus gelada). Transactions of the Zoological Society of London, 28(7), 543–552.

    Article  Google Scholar 

  • McCann, C. M. (1995). Social factors affecting reproductive success in female gelada baboons (Theropithecus gelada). Ph.D. thesis, The City University of New York.

  • Mori, U., & Dunbar, R. I. M. (1985). Changes in the reproductive condition of female gelada baboons following the takeover of one-male units. Zeitschrift für Tierpsychologie, 67, 215–224.

    Article  Google Scholar 

  • R Core Team (2013). R: A language and environment for statistical computing. R. Foundation for Statistical Computing, Vienna, Austria. www.R-project.org/.

  • Rhine, R. J., Norton, G. W., & Wasser, S. K. (2000). Lifetime reproductive success, longevity, and reproductive life history of female yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. American Journal of Primatology, 51(4), 229–241.

    Article  CAS  PubMed  Google Scholar 

  • Rigaill, L., MacIntosh, A. J. J., Higham, J. P., Winters, S., Shimizu, K., et al. (2015). Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PLoS ONE, 10(8), e0135127.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roberts, E. K., Lu, A., Bergman, T. J., & Beehner, J. C. (2012). A Bruce effect in wild geladas. Science, 335, 1222–1225.

    Article  CAS  PubMed  Google Scholar 

  • Rowell, T. E. (1972). Female reproduction cycles and social behaviour in primates. Advances in the Study of Behaviour, 4, 69–105.

    Article  Google Scholar 

  • Sigg, H., Stolba, A., Abegglen, J. J., & Dasser, V. (1982). Life history of hamadryas baboons: physical development, infant mortality, reproductive parameters and family relationships. Primates, 23(4), 473–487.

    Article  Google Scholar 

  • Smuts, B. B., & Nicholson, N. (1989). Dominance rank and reproduction in female baboons. American Journal of Primatology, 19, 229–246.

    Article  Google Scholar 

  • Snyder-Mackler, N., Beehner, J. C., & Bergman, T. J. (2012). Defining higher levels in a gelada multilevel society. International Journal of Primatology, 33(5), 1054–1068.

    Article  Google Scholar 

  • Stavisky, R. C., Russell, E., Stallings, J., Smith, E. O., Worthman, C., & Whitten, P. L. (1995). Fecal steroid analysis of ovarian cycles in free-ranging baboons. American Journal of Primatology, 36, 285–297.

    Article  CAS  Google Scholar 

  • Swedell, L. (2005). Strategies of sex and survival in hamadryas baboons: Through a female lens. Upper Saddle River, NJ: Pearson Prentice Hall.

    Google Scholar 

  • Takahata, Y., Suzuki, S., Agetsuma, N., Okayasu, N., Sugiura, H., et al. (1998). Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report. Primates, 39, 339.

    Article  Google Scholar 

  • Whitten, P. L., Brockman, D. K., & Stavisky, R. C. (1998). Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yearbook of Physical Anthropology, 41, 1–23.

    Article  Google Scholar 

  • Yan, C., & Jiang, Z. (2006). Does estradiol modulate sexual solicitations in female Rhinopithecus roxellana? International Journal of Primatology, 27(4), 1171–1186.

    Article  Google Scholar 

  • Zhao, Q., Borries, C., & Pan, W. (2011). Male takeover, infanticide, and female countertactics in white-headed leaf monkeys (Trachypithecus leucocephalus). Behavioral Ecology and Sociobiology, 65, 1535–1547.

    Article  Google Scholar 

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Acknowledgments

We extend our thanks to the Ethiopian Wildlife Conservation Authority and the wardens and staff of the Simien Mountains National Park for permission to conduct this research, and to the participants of the University of Michigan Gelada Research project for their tireless help in the field. We also thank Dr. Toni Ziegler at the Wisconsin National Primate Research Center and Teera Parr for their expert help on laboratory analyses. This work was supported by the Wildlife Conservation Society (SSF Gr# 67250), the National Geographic Society (Gr# 8100-06; 8989-11), the Leakey Foundation (multiple grants), the National Science Foundation (Gr# BCS-0715179, Gr# BCS-0824592, IOS-1255974), and the University of Michigan. We thank James Higham, Joanna Setchell, and two anonymous reviewers for their constructive comments.

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Correspondence to Eila K. Roberts.

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Roberts, E.K., Lu, A., Bergman, T.J. et al. Female Reproductive Parameters in Wild Geladas (Theropithecus gelada). Int J Primatol 38, 1–20 (2017). https://doi.org/10.1007/s10764-016-9939-4

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  • DOI: https://doi.org/10.1007/s10764-016-9939-4

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