International Journal of Primatology

, Volume 35, Issue 2, pp 476–490 | Cite as

Maternal Investment and Infant Survival in Gray-Cheeked Mangabeys (Lophocebus albigena)

  • Małgorzata E. Arlet
  • Lynne A. Isbell
  • Freerk Molleman
  • Ants Kaasik
  • Rebecca L. Chancellor
  • Colin A. Chapman
  • Raivo Mänd
  • James R. Carey


Differences among females in infant survival can contribute substantially to variance in fitness. Infant survival is a product of external risk factors and investment by kin, especially the mother, and is thus closely tied with the evolution of behavior and life history. Here we present a 9-yr study (2004–2012) of infant survival and sex ratio relative to age and dominance ranks of mothers and the presence of immigrant males in a free-ranging population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We consider immigrant males because they are known to increase infant mortality in several other species. We found that infants of older mothers had higher survival than those of younger mothers but that high rank did not confer a significant benefit on infant survival. Female infants had higher survival than male infants. Young, low-ranking females had more male infants than young, high-ranking females, which had slightly more daughters, but this difference declined as females aged because low-ranking females had more daughters as they aged. With limited data, we found a significant relationship between the presence of male immigrants and infant mortality (falls and unexplained disappearances) to 18 mo. Our results suggest that infant survival in gray-cheeked mangabeys is most precarious when mothers must allocate energy to their own growth as well as to their infants, that sons of young mothers are at greatest risk, and that immigrant males can negatively affect infant survival.


Fitness Kibale National Park Life history Primates Reproductive strategies 



We thank the Uganda Wildlife Authority, Uganda National Council for Science and Technology, and personnel at the Makerere University Biological Field Station in Kanyawara for permission to work in Kibale National Park. The study complied with all current laws of Uganda. We thank all the field assistants who worked with us during these years for their invaluable help: Kaseregenyu Richard, Katusabe Swaibu, Irumba Peter, Sabiti Richard, Akora Charles, and Koojo John. We thank Richard Wrangham and field assistants of Kibale Chimpanzee Project who informed us on chimpanzee predation on mangabeys. Thanks also to Linda-Liisa Veromann for help in entering behavioral data. This research was supported by the Leakey Foundation and the University of California, Davis, Department of Anthropology (to R. L. Chancellor), by NIH/NIA grants PO1 A6022500 and PO1 A608761 (to J. R. Carey), by the European Union through the European Social Fund (Mobilitas postdoctoral grant MJD56, to M. E. Arlet). R. Mänd and F. Molleman were supported by the Estonian Ministry of Education and Science (targeted financing projects number 0180004s09 and 0180122s08 and ESF 9215,7406, 7699, 7522, 8413, and GD6019), and the European Regional Development Fund (Center of Excellence FIBIR). Finally, we appreciate the diligent efforts of Joanna Setchell and two anonymous reviewers to improve this manuscript.


  1. Altmann, J. (1980). Baboon mothers and infants. Cambridge: Harvard University Press.Google Scholar
  2. Altmann, J., & Alberts, S. C. (2005). Growth rates in a wild primate population: Ecological influences and maternal effects. Behavioral Ecology and Sociobiology, 57, 490–501.CrossRefGoogle Scholar
  3. Arlet, M. E., Molleman, F., & Chapman, C. A. (2008). Mating tactics in male grey-cheeked mangabeys (Lophocebus albigena). Ethology, 114, 841–852.Google Scholar
  4. Arlet, M. E., Grote, M. N., Isbell, L. A., Molleman, F., & Carey, J. R. (2009). Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena). Hormones and Behavior, 55, 210–216.PubMedCrossRefGoogle Scholar
  5. Arlet, M. E., Kaasik, A., Molleman, F., Isbell, L. A., Carey, J. R., & Mänd, R. (2011). Social factors increase fecal testosterone levels in wild male gray-cheeked mangabeys (Lophocebus albigena). Hormones and Behavior, 59, 605–611.PubMedCrossRefGoogle Scholar
  6. Barton, R. A. (1993). Sociospatial mechanisms of feeding competition in female olive baboons, Papio anubis. Animal Behaviour, 46, 791–802.CrossRefGoogle Scholar
  7. Bates, D., Maechler, M., & Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes. R package version 0.999375–41/r1341. Retrieved from
  8. Bercovitch, F. B. (2002). Sex-biased parental investment in primates. International Journal of Primatology, 23, 905–921.CrossRefGoogle Scholar
  9. Bercovitch, F. B., & Berard, J. D. (1993). Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behavioral Ecology and Sociobiology, 32, 103–109.CrossRefGoogle Scholar
  10. Bercovitch, F. B., Lebron, M. R., Martinez, H. S., & Kessler, M. J. (1998). Primigravidity, body weight, and costs of rearing first offspring in rhesus macaques. American Journal of Primatology, 46, 135–144.PubMedCrossRefGoogle Scholar
  11. Bercovitch, F. B., Widdig, A., & Nürnberg, P. (2000). Maternal investment in rhesus macaques (Macaca mulatta): Reproductive costs and consequences of raising sons. Behavioral Ecology and Sociobiology, 48, 1–11.CrossRefGoogle Scholar
  12. Blomquist, G. E., Sade, D. S., & Berard, J. S. (2011). Rank-related fitness differences and their demographic pathways in semi-free-ranging rhesus macaques (Macaca mulatta). International Journal of Primatology, 32, 193–208.CrossRefGoogle Scholar
  13. Brown, G. R., & Silk, J. B. (2002). Reconsidering the null hypothesis: Is maternal rank associated with birth sex ratios in primate groups? Proceedings of the National Academy of Sciences of the USA, 99, 11252–11255.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Chancellor, R. L., & Isbell, L. A. (2009a). Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology and Sociobiology, 63, 1447–1458.PubMedCentralPubMedCrossRefGoogle Scholar
  15. Chancellor, R. L., & Isbell, L. A. (2009b). Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology, 20, 78–86.CrossRefGoogle Scholar
  16. Chapman, C. A., Chapman, L. J., Jacob, A. L., Rothman, J. M., Omeja, P., Reyna-Hurtado, R., Hartter, J., & Lawes, M. J. (2010). Tropical tree community shifts: Implications for wildlife conservation. Biological Conservation, 143, 366–374.CrossRefGoogle Scholar
  17. Charnov, E. L. (1993). Life history invariants: Some explorations of symmetry in evolutionary ecology. Oxford: Oxford University Press.Google Scholar
  18. Cheney, D. L., Seyfarth, R. M., Andelman, S. J., & Lee, P. C. (1988). Reproductive success in vervet monkeys. In T. H. Clutton-Brock (Ed.), Reproductive success (pp. 384–402). Chicago: University of Chicago Press.Google Scholar
  19. Cheney, D. L., & Wrangham, R. W. (1987). Predation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 227–239). Chicago: University of Chicago Press.Google Scholar
  20. Clutton-Brock, T. H. (1984). Reproductive effort and terminal investment in iteroparous animals. American Naturalist, 123, 212–229.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Deputte, B. L. (1991). Reproductive parameters of captive grey-cheeked mangabeys. Folia Primatologica, 57, 57–69.CrossRefGoogle Scholar
  23. Descamps, S., Boutin, S., Berteaux, D., & Gaillard, J. (2008). Age-specific variation in survival, reproductive success and offspring quality in red squirrels: Evidence of senescence. Oikos, 117, 1406–1416.CrossRefGoogle Scholar
  24. Drevenstedt, G. L., Crimmins, E. M., Vasunilashorn, S., & Finch, C. E. (2008). The rise and fall of excess male mortality. Proceedings of the National Academy of Sciences of the USA, 105, 5016–5021.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Fairbanks, L. A. (1990). Reciprocal benefits of allomothering for female vervet monkeys. Animal Behaviour, 40, 553–562.CrossRefGoogle Scholar
  26. French, J. A., Pissinatti, A., & Coimbra-Filho, A. F. (1996). Reproduction in captive lion tamarins (Leontopithecus): Seasonality, infant survival, and sex ratios. American Journal of Primatology, 39, 17–33.CrossRefGoogle Scholar
  27. Garcia, C., Lee, P. C., & Rosetta, L. (2006). Dominance and reproductive rates in captive female olive baboons, Papio anubis. American Journal of Physical Anthropology, 131, 64–72.PubMedCrossRefGoogle Scholar
  28. Heesen, M., Roghan, S., Ostner, J., & Schülke, O. (2013). Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behavioral Ecology and Sociobiology, 67, 1053–1066.CrossRefGoogle Scholar
  29. Hinde, K. (2007). First-time mothers bias milk composition in favor of sons. Current Biology, 17, R958–R959.PubMedCrossRefGoogle Scholar
  30. Hinde, K. (2009). Richer milk for sons but more milk for daughters: Sex-biased investment during lactation varies with maternal life history in rhesus macaques. American Journal of Human Biology, 21, 512–519.PubMedCrossRefGoogle Scholar
  31. Hinde, K., & Capitanio, J. P. (2010). Lactational programming? Mother’s milk energy predicts infant behavior and temperament and rhesus macaques (Macaca mulatta). American Journal of Primatology, 72, 522–529.PubMedCentralPubMedGoogle Scholar
  32. Isbell, L. A. (2012). Re-evaluating the ecological constraints model with red colobus monkeys (Procolobus rufomitratus tephrosceles). Behaviour, 149, 493–529.CrossRefGoogle Scholar
  33. Isbell, L. A., & Young, T. P. (1993). Human presence reduces predation in a free-ranging vervet monkey population in Kenya. Animal Behaviour, 45, 1233–1235.CrossRefGoogle Scholar
  34. Isbell, L. A., Young, T. P., Jaffe, K. E., Carlson, A. A., & Chancellor, R. L. (2009). Demography and life histories of sympatric patas monkeys (Erythrocebus patas) and vervets (Cercopithecus aethiops) in Laikipia, Kenya. International Journal of Primatology, 30, 103–124.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Kleindorfer, S., & Wasser, S. K. (2004). Infant handling and mortality in yellow baboons. Behavioral Ecology and Sociobiology, 56, 328–337.CrossRefGoogle Scholar
  36. Koenig, A. (2000). Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behavioral Ecology and Sociobiology, 48, 93–109.CrossRefGoogle Scholar
  37. Nishida, T., Corp, N., Hamai, M., Hasegawa, T., Hiraiwa-Hasegawa, M., Hosaka, K., Hunt, K. D., Itho, N., Kawanaka, K., Matsumoto-Oda, A., Mitani, J. C., Nakamura, M., Norikoshi, K., Sakamaki, T., Turner, L., Uehara, S., & Zamma, K. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology, 59, 99–121.PubMedCrossRefGoogle Scholar
  38. Olupot, W., & Waser, P. M. (2001). Correlates of intergroup transfer in male grey-cheeked mangabeys. International Journal of Primatology, 19, 169–187.CrossRefGoogle Scholar
  39. Olupot, W., & Waser, P. M. (2013). Lophocebus albigena Grey-cheeked mangabey. In T. M. Butynski, J. S. Kingdon, & J. Kalina (Eds.), The mammals of Africa (Primates, Vol. II, pp. 206–209). London: Bloomsbury Publishing.Google Scholar
  40. Ostner, J., Borries, C., Schülke, O., & Koenig, A. (2005). Sex allocation in a colobine monkey. Ethology, 111, 924–939.CrossRefGoogle Scholar
  41. Packer, C., Collins, D. A., Sindwimwo, A., & Goodall, J. (1995). Reproductive constraints on aggressive competition in female baboons. Nature, 373, 60–63.PubMedCrossRefGoogle Scholar
  42. 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
  43. Pusey, A. E. (2012). Magnitude and sources of variation in female reproductive performance. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 143–166). Chicago: University of Chicago Press.Google Scholar
  44. Pusey, A., Williams, J., & Goodall, J. (1997). The influence of dominance rank on the reproductive success of female chimpanzees. Science, 227, 828–831.CrossRefGoogle Scholar
  45. R Development Core Team. (2011). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from Scholar
  46. Robbins, A. W., Robbins, M. M., & Fawcett, K. (2007). Maternal investment of the Virunga mountain gorillas. Ethology, 113, 235–245.CrossRefGoogle Scholar
  47. Schino, G., & Troisi, A. (2005). Neonatal abandonment in Japanese macaques. American Journal of Physical Anthropology, 126, 447–452.PubMedCrossRefGoogle Scholar
  48. Setchell, J. M., Lee, P. C., Wickings, E. J., & Dixson, A. F. (2001). Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). American Journal of Physical Anthropology, 115, 349–360.PubMedCrossRefGoogle Scholar
  49. Setchell, J. M., Lee, P. C., Wickings, E. J., & Dixson, A. F. (2002). Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). International Journal of Primatology, 23, 51–68.CrossRefGoogle Scholar
  50. Silk, J. B. (1983). Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. American Naturalist, 121, 56–66.CrossRefGoogle Scholar
  51. Silk, J. B., & Brown, G. R. (2004). Sex ratios in primate groups. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 253–265). Cambridge University Press.Google Scholar
  52. Silk, J. B., & Brown, G. R. (2008). Local resource competition and local resource enhancement shape primate birth sex ratios. Proceedings of the Royal Society of London B: Biological Sciences, 275, 1761–1765.CrossRefGoogle Scholar
  53. Silk, J. B., Clark-Wheatley, C. B., Rodman, P. S., & Samuels, A. (1981). Differential reproductive success and facultative adjustment of sex ratios among female bonnet macaques (Macaca radiata). Animal Behaviour, 29, 1106–1120.CrossRefGoogle Scholar
  54. Strum, S. C., & Western, J. D. (1982). Variation in fecundity with age and environment in olive baboons (Papio anubis). American Journal of Primatology, 3, 61–76.CrossRefGoogle Scholar
  55. Therneau, T. (2011). Survival: Survival analysis, including penalised likelihood. Original Splus->R port by Thomas Lumley. R package version 2.36–10.Google Scholar
  56. Trivers, R. L., & Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90–92.PubMedCrossRefGoogle Scholar
  57. Valtonen, A., Molleman, F., Chapman, C. A., Carey, J. R., Ayres, M. P., & Roininen, H. (2013). Tropical phenology: Bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage. Ecosphere, 4, 1–28.CrossRefGoogle Scholar
  58. Veeroja, R., Kirk, A., Tilgar, V., Säde, S., Kreitsberg, M., & Tõnisson, J. (2010). Conception date affects litter type and foetal sex ratio in female moose in Estonia. Journal of Animal Ecology, 79, 169–175.PubMedCrossRefGoogle Scholar
  59. Waser, P. M. (1974). Intergroup interaction in a forest monkey: The mangabey Cercocebus albigena. Dissertation. New York: The Rockefeller University.Google Scholar
  60. Wasser, S. K., Norton, G. W., Kleindorfer, S., & Rhine, R. J. (2004). Population trend alters the effects of maternal dominance rank on lifetime reproductive success in yellow baboons (Papio cynocephalus). Behavioral Ecology and Sociobiology, 56, 338–345.CrossRefGoogle Scholar
  61. Whitten, P. L. (1983). Diet and dominance among female vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 5, 139–159.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Małgorzata E. Arlet
    • 1
    • 2
  • Lynne A. Isbell
    • 3
  • Freerk Molleman
    • 4
  • Ants Kaasik
    • 1
  • Rebecca L. Chancellor
    • 5
  • Colin A. Chapman
    • 6
    • 7
  • Raivo Mänd
    • 1
  • James R. Carey
    • 8
  1. 1.Department of Zoology, Institute of Ecology and Earth SciencesUniversity of TartuTartuEstonia
  2. 2.Animal and Human Ethology Research UnitUniversity of Rennes 1RennesFrance
  3. 3.Department of Anthropology and Animal Behavior Graduate GroupUniversity of California DavisDavisUSA
  4. 4.Ecosystems, Biodiversity and Evolution Research UnitUniversity of Rennes 1RennesFrance
  5. 5.Departments of Anthropology, Sociobiology and PsychologyWest Chester University of PennsylvaniaWest ChesterUSA
  6. 6.Department of Anthropology and McGill School of EnvironmentMcGill UniversityMontrealCanada
  7. 7.Wildlife Conservation SocietyBronxUSA
  8. 8.Department of EntomologyUniversity of California DavisDavisUSA

Personalised recommendations