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Direct Stacked Investment Is a Flexible Reproductive Strategy for Female Colobus vellerosus

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Abstract

Most primates produce one offspring at a time but can overlap investment in consecutive offspring (stacked investment) depending on ecological and/or social conditions. “Direct stacked investment” occurs when a female conceives and gestates a new offspring while a previous infant is still suckling. We investigate direct stacked investment in Colobus vellerosus by determining if there is a period of overlap between nipple contact with a female’s first infant and gestation of her subsequent infant. We then investigate the effect of male group-membership and stability on stacked investment to test the hypothesis that stacking investment is a female strategy to avoid infanticide. We collected scan data to record when an infant was in nipple contact from 16 females in four groups of C. vellerosus, from May 2012 to May 2013 at Boabeng-Fiema Monkey Sanctuary in Ghana. We studied three group types, stable multimale, multifemale; unstable multimale, multifemale; and stable unimale, multifemale. Eight of our study females directly stacked investment. The frequency of direct stacked investment varied significantly among the group types. Stacked investment was due to earlier conception rather than delayed weaning, with females in stable multimale groups conceiving a subsequent infant earlier than those in unstable multimale groups. The timing of conception did not differ between stable unimale groups and either unstable or stable multimale groups. There was no difference in time to last nipple contact among group types. These results do not support the predictions of the infanticide avoidance hypothesis, but a larger sample size would help to test the hypothesis more comprehensively. Delayed conception by females in unstable groups may be infanticide avoidance, however, if it allows time for females to spread paternity certainty among males. Alternatively, females in unstable groups may be under stress or experience reduced feeding time due to frequent male–male agonistic interactions, both of which can suppress female ovulation. This study contributes to a growing body of research that explores flexibility in infant investment strategies, particularly in relation to external factors such as male group membership and stability.

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References

  • Abbott, D., Keverene, E., Moore, G., & Yodyingyuad, U. (1986). Social suppression of reproduction in subordinate talapoin monkeys, Miopithecus talapoin. In J. G. Else & P. C. Lee (Eds.), Primate ontogeny, cognition and social behavior (pp. 329–341). Cambridge: Cambridge University Press.

    Google Scholar 

  • Adams, M. R., Kaplan, J. R., & Koritnik, D. R. (1985). Psychological influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiology & Behavior, 35, 935–940.

    CAS  Google Scholar 

  • Alberts, S. C., Sapolsky, R. M., & Altmann, J. (1992). Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a Natural Primate Group. Hormones and Behavior, 26, 167–178.

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Altmann, J., & Samuels, A. (1992). Costs of maternal care: Infant-carrying in baboons. Behavioral Ecology and Sociobiology, 29, 391–398.

    Google Scholar 

  • Altmann, J., Altmann, S. A., & Hausfater, G. (1978). Primate infant’s effects on mother’s future reproduction. Science, 201, 1028–1029.

    CAS  PubMed  Google Scholar 

  • Badescu, I., Katzenberg, M. A., Watts, D. P., & Sellen, D. W. (2016). A novel fecal stable isotope approach to determine the timing of age-related feeding transitions in wild infant chimpanzees. American Journal of Physical Anthropology, 162(2), 228–299. https://doi.org/10.1002/ajpa.2311.

    Article  Google Scholar 

  • Beehner, J., & Lu, A. (2013). Reproductive suppression in female primates: A review. Evolutionary Anthropology, 22, 226–238.

    PubMed  Google Scholar 

  • Beehner, J. C., Bergman, T. J., Cheney, D. L., Seyfarth, R. M., & Whitten, P. L. (2005). The effect of new alpha males on female stress in free-ranging baboons. Animal Behaviour, 69, 1211–1221.

    Google Scholar 

  • Berghänel, A., Schülke, O., & Ostner, J. (2015). Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off. Science Advances, 1(7), e1500451.

    PubMed  PubMed Central  Google Scholar 

  • von Borell, E., Dobson, H., & Prunier, A. (2007). Stress, behaviour and reproductive performance in female cattle and pigs. Hormones and Behavior, 52, 130–138.

    Google Scholar 

  • Borries, C., & Koenig, A. (2000). Infanticide in Hanuman langurs: Social organization, male migration, and weaning age. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 99–122). Cambridge: Cambridge University Press.

    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.

    Google Scholar 

  • Borries, C., Lu, A., Ossi-Lupo, K., Larney, E., & Koenig, A. (2014). The meaning of weaning in Wild Phayre’s Leaf monkeys: Last nipple contact, survival, and independence. American Journal of Physical Anthropology, 154(2), 291–301. https://doi.org/10.1002/ajpa.22511.

    Article  PubMed  Google Scholar 

  • Boyce, M. S. (1988). Evolution of life histories: Theory and patterns from mammals. In M. S. Boyce (Ed.), Evolution of life histories of mammals: Theory and pattern (pp. 3–30). New Haven, CT: Yale University Press.

    Google Scholar 

  • Bulger, J., & Hamilton, W. J. (1987). Rank and density correlates of inclusive fitness measures in a natural chacma baboon (Papio ursinus) troop. International Journal of Primatology, 8, 635–650.

    Google Scholar 

  • Busse, C., & Hamilton, W. J. (1981). Infant carrying by male chacma baboons. Science, 212, 1281–1283.

    CAS  PubMed  Google Scholar 

  • Cameron, J. L. (1997). Stress and behaviorally induced reproductive dysfunction in primates. Seminars in Reproductive Endocrinology, 15, 37–45.

    CAS  PubMed  Google Scholar 

  • Carnegie, S. D., Fedigan, L. M., & Ziegler, T. E. (2011). Social and environmental factors affecting fecal glucocorticoids in wild, female white-faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 861–869.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke, P., Pradhan, G., van Schaik, C., Muller, M.N., & Wrangham, R.W. (2009). Intersexual conflict in primates: infanticide, paternity allocation, and the role of coercion. In M.N. Muller & R.W. Wrangham (Eds.), Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females (pp 42–77). Cambridge: Harvard University Press.

  • Collins, D. A., Busse, C. D., & Goodall, J. (1984). Infanticide in two populations of savanna baboons. In G. Hausfater & S. B. Hrdy (Eds.), Infanticide: Comparative and evolutionary perspectives (pp. 193–216). New York: Aldine.

    Google Scholar 

  • Crotty, A. M. (2016). Influences on lactation length and the timing of weaning events in Colobus vellerosus. Master’s Thesis, University of Calgary.

  • Dobson, H., Fergani, C., Routly, J. E., & Smith, R. F. (2012). Effects of stress on reproduction in ewes. Animal Reproduction Science, 130, 135–140.

    CAS  PubMed  Google Scholar 

  • Ellison, P. T. (1990). Human ovarian function and reproductive ecology: New hypotheses. American Anthropologist, 92, 933–952.

    Google Scholar 

  • Ellison, P. T. (2001). On fertile ground: A natural history of human reproduction. Cambridge: Harvard University Press.

    Google Scholar 

  • Emery Thompson, M., Muller, M. N., & Wrangham, R. W. (2014). Male chimpanzees compromise the foraging success of their mates in Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 68, 1973–1983. https://doi.org/10.1007/s00265-014-1803-y.

    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.

    Google Scholar 

  • Gibson, D., & Chu, E. (1992). Management and behavior of Francois langur (Presbytic francoisi francoisi) at the Zoological Society of San Diego. International Zoo Yearbook, 31, 184–191.

    Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Belknap Press.

    Google Scholar 

  • Harcourt, A. H. (1987). Dominance and fertility among female primates. Journal of Zoology, 213, 471–487.

    Google Scholar 

  • Hausfater, G., & Hrdy, S. B. (1984). Infanticide: Comparative and evolutionary perspectives. New York: Aldine.

    Google Scholar 

  • Hrdy, S. B. (1974). Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatologica, 22(1), 19–58.

  • 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(1), 13–40.

  • Hrdy, S. B. (2000). Foreword. In C. P. van Schaik & C. H. Jansen (Eds.), Infanticide by males and its implications (pp. xi–xiv). Cambridge: Cambridge University Press.

    Google Scholar 

  • Kalantaridou, S. N., Makrigiannakis, A., Zoumakis, E., & Chrousos, G. P. (2004). Stress and the female reproductive system. Journal of Reproductive Immunology, 62, 61–68.

    CAS  PubMed  Google Scholar 

  • Lee, P. C. (1987). Nutrition, fertility and maternal investment in primates. Journal of Zoology, 217, 449–442.

    Google Scholar 

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

    Google Scholar 

  • Leland, L., Struhsaker, T. T., & Butynski, T. M. (1984). Infanticide by adult male primate species of the Kibale forest, Uganda: A test of hypotheses. In G. Hausfater & S. B. Hrdy (Eds.), Infanticide: Comparative and evolutionary perspectives (pp. 151–172). New York: Aldine.

    Google Scholar 

  • Mas-Rivera, A., & Bercovitch, F. B. (2008). Postpartum recuperation in primiparous Rhesus macaques and development of their infants. American Journal of Primatology, 70, 1047–1054.

    PubMed  Google Scholar 

  • McNeilly, A. S. (2001). Lactational control of reproduction. Reproduction, Fertility and Development, 13, 583–590.

    CAS  Google Scholar 

  • McNeilly, A. S., Abbot, D. H., Lunn, S. F., Chambers, P. C., & Hearn, J. P. (1981). Plasma prolactin concentrations during the ovarian cycle and lactation and their relationship to return of fertility post partum in the common marmoset. Journal of Reproduction and Fertility, 62, 253–260.

    Google Scholar 

  • Newton, P. N. (1988). The variable social organization of Hanuman langurs (Presbytis entellus), infanticide, and the monopolization of females. International Journal of Primatology, 9, 199–232.

    Google Scholar 

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

    Google Scholar 

  • Nicolson, N. (1982). Weaning and the development of independence in olive baboons. Doctoral dissertation, Harvard University.

  • van Noordwijk, M. A. (2012). From maternal investment to lifetime maternal care. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 321–342). Chicago: University of Chicago Press.

    Google Scholar 

  • van Noordwijk, M. A., Willems, E. P., Utami Atmoko, S. S., Kuzawa, C. W., & van Schaik, C. P. (2013). Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii). Behavioral Ecology and Sociobiology, 67, 805–814.

    Google Scholar 

  • Palombit, R. A. (2015). Infanticide as sexual conflict: Coevolution of male strategies and female counterstrategies. Cold Spring Harbor Perspectives in Biology, 7(6). https://doi.org/10.1101/cshperspect.a017640.

  • Palombit, R. A. (2012). Infanticide: Male strategies and female counterstrategies. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 432–468). Chicago: University of Chicago Press.

    Google Scholar 

  • Palombit, R. A., Cheney, D. L., Fischer, J., Johnson, S., Rendall, D., Seyfarth, R. M., & Silk, J. B. (2000). Male infanticide and defense of infants in chacma baboons. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 123–152). Cambridge: Cambridge University Press.

    Google Scholar 

  • Pereira, M. (1983). Abortion following the immigration of an adult male baboon (Papio cynocephalus). American Journal of Primatology, 4, 93–98.

    PubMed  Google Scholar 

  • Pusey, A. E. (1983). Mother-offspring relationships in chimpanzees after weaning. Animal Behaviour, 31, 363–377.

    Google Scholar 

  • Recabarren, M. P., Vergara, M., Martinez, M. C., Gordon, K., & Seron-Ferre, M. (2000). Impact of lactation upon fertility in the New World primate capuchin monkey (Cebus apella). Journal of Medical Primatology, 29, 350–360.

    CAS  PubMed  Google Scholar 

  • Reitsema, L. J. (2012). Introducing fecal stable isotope analysis in primate weaning studies. American Journal of Primatology, 74, 926–939.

    CAS  PubMed  Google Scholar 

  • Rowell, T. E. (1966). Forest living baboons in Uganda. Journal of Zoology, 149, 344–364.

    Google Scholar 

  • Saj, T. L., Teichroeb, J. A., & Sicotte, P. (2005). The population status of the ursine colobus (Colobus vellerosus) at Boabeng-Fiema, Ghana. In J. D. Paterson & J. Wallis (Eds.), Special topics in primatology, Commensalism and conflict: The human primate interface (Vol. 4, pp. 350–375). Norman, OK: American Society of Primatologists.

    Google Scholar 

  • Sapolsky, R. M. (1993). Endocrinology alfresco: Psychoendocrine studies of wild baboons. Recent Progress in Hormone Research, 48, 437–468.

    CAS  PubMed  Google Scholar 

  • Sapolsky, R. M. (2002). Endocrinology of the stress-response. In J. B. Becker, S. M. Breedlove, D. Crews, & M. M. McCarthy (Eds.), Behavioral endocrinology (pp. 410–450). Cambridge: MIT Press.

    Google Scholar 

  • van Schaik, C. P. (2000). Infanticide by male primates: The sexual selection hypothesis revisited. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 27–60). Cambridge: Cambridge University Press.

    Google Scholar 

  • van Schaik, C. R., Pradhan, G. R., & van Noordwijk, M. A. (2004). Mating conflict in primates: infanticide, sexual harassment and female sexuality. In P. Kappeler & C. R. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 131–150). Cambridge: Cambridge University Press.

    Google Scholar 

  • Short, R. V. (1976). Lactation: The central control of reproduction. In K. Elliot & D. W. Fitzsimons (Eds.), Ciba Foundation Symposium 45: Breast feeding and the mother (pp. 73–81). Amsterdam: Elsevier.

    Google Scholar 

  • Sicotte, P., Teichroeb, J. A., Vayro, J. V., Fox, S. A., Bădescu, I., & Wikberg, E. C. (2015). The influence of male takeovers on female dispersal in Colobus vellerosus. American Journal of Primatology, 79(7). https://doi.org/10.1002/ajp.22436.

  • Symington, M. M. (1987). Sex ratio and maternal rank in wild spider monkeys: When daughters disperse. Behavioral Ecology and Sociobiology, 20, 421–425.

    Google Scholar 

  • Tanaka, I. (1992). Three phases of lactation in free-ranging Japanese macaques. Animal Behaviour, 44, 129–139.

    CAS  Google Scholar 

  • Tarara, E. B. (1987). Infanticide in a chacma baboon troop. Primates, 28, 267–270.

    Google Scholar 

  • Teichroeb, J. A., & Sicotte, P. (2008). Infanticide in ursine colobus monkeys (Colobus vellerosus): New cases and a test of the existing hypotheses. Behavior, 145, 727–755.

    Google Scholar 

  • Teichroeb, J. A., Wikberg, E. C., & Sicotte, P. (2009). Female dispersal patterns in six groups of ursine colobus (Colobus vellerosus): Infanticide avoidance is important. Behavior, 146, 551–582.

    Google Scholar 

  • Teichroeb, J. A., Wikberg, E. C., & Sicotte, P. (2011). Dispersal in male ursine colobus monkeys (Colobus vellerosus): Influence of age, rank and contact with other groups on dispersal decisions. Behavior, 148, 765–793.

    Google Scholar 

  • Teichroeb, J. A., Wikberg, E. C., Badescu, I., Macdonald, L. J., & Sicotte, P. (2012). Infanticide risk and male quality influence optimal group composition for Colobus vellerosus. Behavioral Ecology, 23(6), 1348–1359.

    Google Scholar 

  • Therneau, T. (2015). Mixed effects Cox models. CRAN repository.

    Google Scholar 

  • Therneau, T. M., & Grambsch, P. M. (2000). The cox model. In Modeling survival data: extending the cox model. Springer, New York, NY: Statistics for Biology and Health. https://doi.org/10.1007/978-1-4757-3294-8_3.

    Chapter  Google Scholar 

  • Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man, 1871-1971 (pp. 136–179). Aldine: Chicago, IL.

    Google Scholar 

  • Varley, M. A., & Stedman, R. (1994). Stress and reproduction. In J. Wiseman, M. A. Varley, & B. Kemp (Eds.), Perspectives in Pig Science, Easter School Series, volume 59, Proceedings of Nottingham University Easter School in Agricultural Science (pp. 277–296). Loughborough, Leicestershire: Nottingham University Press.

  • Vayro, J. (2017). Social and hormonal correlates of life history characteristics and mating patterns in female Colobus vellerosus. Doctoral Dissertation: University of Calgary.

    Google Scholar 

  • Vayro, J. V., Fedigan, L. M., Ziegler, T. E., Crotty, A., Ataman, R., et al (2016). Hormonal correlates of life history characteristics in wild female Colobus vellerosus. Primates, 57, 509–519. https://doi.org/10.1007/s10329-016-0551-1.

    Article  CAS  PubMed  Google Scholar 

  • Wade, G. N., & Schneider, J. E. (1992). Metabolic fuels and reproduction in female mammals. Neuroscience and Biobehavioral Reviews, 16, 235–272.

    CAS  PubMed  Google Scholar 

  • Wasser, S. K., & Starling, A. K. (1988). Proximate and ultimate causes of reproductive suppression among female yellow baboons at Mikumi National Park, Tanzania. American Journal of Primatology, 16, 97–121.

    PubMed  Google Scholar 

  • Williams, R. F. (1986). The interbirth interval in primates: Effects of pregnancy and nursing. In K. Benirschke (Ed.), Primates: The road to self-sustaining populations. New York: Springer-Verlag.

    Google Scholar 

  • Wilson, M. E. (1992). Primiparous rhesus monkey mothers are more sensitive to the nursing-induced inhibition of LH and ovarian steroid secretion. Journal of Endocrinology, 134(3), 493–503. https://doi.org/10.1677/joe.0.1340493.

    Article  CAS  Google Scholar 

  • Wong, S. N. P., & Sicotte, P. (2006). Population size and density of Colobus vellerosus at the Boabeng-Fiema Monkey Sanctuary and surrounding forest fragments in Ghana. American Journal of Primatology, 68, 465–476.

    PubMed  Google Scholar 

  • Xiao, E., & Ferin, M. (1997). Stress-related disturbances of the menstrual cycle. Annals of Medicine, 29, 215–219. https://doi.org/10.3109/07853899708999339.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

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Acknowledgments

We thank the Ghana Wildlife Division and the management committee of the Boabeng–Fiema Monkey Sanctuary for permission to conduct this research. Robert Koranteng and Charles Kodom provided research assistance. This study was funded by Natural Sciences and Engineering Research Council of Canada, Grant Number: RGPIN/203059-2012 and the University of Calgary. We thank two anonymous reviewers and the journal editor for their comments on an earlier version of this article.

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JV conceived and designed the study, conducted fieldwork, analyzed the data, and wrote the manuscript. TZ contributed to the hormonal analysis and provided editorial advice. LF contributed to the study design and provided editorial advice. AC conducted fieldwork and contributed to the data set. SF conducted fieldwork, contributed to the data set, and provided editorial advice. PS conceived and designed the study and provided editorial advice.

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Correspondence to J. V. Vayro.

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Vayro, J.V., Ziegler, T.E., Fedigan, L.M. et al. Direct Stacked Investment Is a Flexible Reproductive Strategy for Female Colobus vellerosus. Int J Primatol 42, 1–15 (2021). https://doi.org/10.1007/s10764-020-00183-2

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