Seasonal Patterns of Infant Mortality in Wild Sanje Mangabeys, Cercocebus sanjei

  • Gráinne M. McCabeEmail author
  • David Fernández
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Infant mortality is a fundamental factor influencing population growth. This study examines the distribution of infant mortality in relation to seasonality for the endangered Sanje mangabey, Cercocebus sanjei, endemic to the Udzungwa Mountains, Tanzania. Data were collected over 40 continuous months (August 2008 to November 2011). Censuses conducted during monthly group follows recorded 35 live births, plus 6 births just prior to the start of the study data (23 females, 16 males and 2 of undetermined sex). The survival probability for these infants combined was 60.2% (27 survived and 14 died before 1 year of age). Mean annual infant mortality (39.8 ± 4.1%) was at the higher end of results reported for other wild cercopithecines. All infant deaths occurred within the dry season (June to October), although most (64%, 9 of 14) were highly clustered within the early dry season (June to August), a period coinciding with an initial drop in fruit production and a peak in tick infestation among adult females. Six of the 14 infants that died were conceived in the previous dry season and born in the wet season; our previous work has demonstrated that this is considered ‘out-of-phase’ with optimal conceptive timing for the species. Previous studies in this species have demonstrated that timing conception with peak food abundance can influence infant survival. We also suggest that tick-borne disease, prevalent in the region, should be further studied as it could be a factor impacting infant mortality and may be interacting with decreasing nutritional intake during the early dry season.


Infant survivorship Disease Ectoparasites Seasonality 



We would like to thank the Udzungwa Ecological Monitoring Centre and the Conservation Resource Center for providing logistical support for this project. Permission to carry out research has been granted by the Udzungwa Mountains National Park, Tanzania National Parks, Tanzanian Wildlife Research Institute and Tanzanian Commission for Science and Technology. Valuable assistance was also provided by the wardens and staff of the Udzungwa Mountains National Park, as well as the Sanje Mangabey Project field assistants. Funding for this study was provided by the National Science Foundation Doctoral Dissertation Improvement Grant (DF and GMM), Leakey Foundation (DF and GMM), Primate Conservation, Inc. (GMM), Margot Marsh Biodiversity Foundation (DF), Conservation International Primate Action Fund (GMM) and IDEA Wild, as well as the University of Texas at San Antonio (UTSA) International Education Fund and Department of Anthropology Doctoral Research Grant (GMM) and Stony Brook University (SBU) Dean’s Fellowship for Professional Development (DF). This study was approved by the IACUC regulations committee for both UTSA and SBU.


  1. Agostinelli C, Lund U (2013) R package ‘circular’: circular statisticsGoogle Scholar
  2. Altmann J, Alberts S (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409CrossRefGoogle Scholar
  3. Altmann J, Altmann S, Hausfater G, McCuskey S (1977) Life history of yellow baboons: physical development, reproductive parameters and infant mortality. Primates 18:315–330CrossRefGoogle Scholar
  4. Altmann J, Hausfater G, Altmann S (1985) Demography of Amboseli baboons, 1963–1983. Am J Primatol 8:113–125CrossRefGoogle Scholar
  5. Arlet M, Isbell L, Molleman F, Kaasik A, Chancellor R, Chapman C, Mänd R, Carey J (2014) Maternal investment and infant survival in gray-cheeked mangabeys (Lophocebus albigena). Int J Primatol 35:476–490CrossRefGoogle Scholar
  6. Beehner J, Bergman T (2008) Infant mortality following male takeovers in wild geladas. Am J Primatol 70:1152–1159CrossRefGoogle Scholar
  7. Beisel W (1996) Nutrition and immune function: overview. J Nutr 126(suppl_10):2611–2615CrossRefGoogle Scholar
  8. Bentley-Condit V, Smith E (1997) Female reproductive parameters of Tana River yellow baboons. Int J Primatol 18:581–596CrossRefGoogle Scholar
  9. Bercovitch F (1991) Social stratification, social strategies, and reproductive success in primates. Ethol Sociobiol 12:315–333CrossRefGoogle Scholar
  10. Brain C, Bohrmann R (1992) Tick infestation of baboons (Papio ursinus) in the Namib Desert. J Wildl Dis 28:188–191CrossRefGoogle Scholar
  11. Carrai V, Borgognini-Tarli S, Huffman M, Bardi M (2003) Increase in tannin consumption by sifaka (Propithecus verreauxi verreauxi) females during the birth season: a case for self-medication in prosimians? Primates 44:61–66PubMedGoogle Scholar
  12. Chapman C, Gillespie T, Goldberg T (2005) Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evol Anthropol 14:134–144CrossRefGoogle Scholar
  13. Chapman C, Speirs M, Gillespie T, Holland T, Austad K (2006) Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. Am J Primatol 68:397–409CrossRefGoogle Scholar
  14. Cheney D, Seyfarth R, Fischer J, Beehner J, Bergman T, Johnson S, Kitchen D, Palombit R, Rendall D, Silk J (2004) Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int J Primatol 25:401–428CrossRefGoogle Scholar
  15. Dinesen L (2001) Conservation priorities for the forests of the Udzungwa Mountains, Tanzania, based on primates, duikers and birds. Biol Conserv 99:223–236CrossRefGoogle Scholar
  16. Ehardt C, Jones T, Butynski T (2005) Protective status, ecology and strategies for improving conservation of Cercocebus sanjei in the Udzungwa Mountains, Tanzania. Int J Primatol 26:557–583CrossRefGoogle Scholar
  17. Fedigan L (1983) Dominance and reproductive success in primates. Am J Phys Anthropol 26(S1):91–129CrossRefGoogle Scholar
  18. Fernández D (2017) Consequences of a male takeover on mating skew in wild Sanje mangabeys. Am J Primatol 79:e22532CrossRefGoogle Scholar
  19. Fernández D, Ehardt C, McCabe G (2018) Monitoring the Sanje mangabey population in Tanzania while engaging the local community. In: Behie AM, Teichroeb JA, Malone N (eds) Primate research and conservation in the Anthropocene. Cambridge University Press, Cambridge (in press)Google Scholar
  20. Gogarten JF, Brown LM, Chapman CA, Cords M, Doran-Sheehy D, Fedigan LM, Grine FE, Perry S, Pusey AE, Sterck EH, Wich SA (2012) Seasonal mortality patterns in non-human primates: implications for variation in selection pressures across environments. Evolution 66:3252–3266CrossRefGoogle Scholar
  21. Gulland F (1992) The role of nematode parasites in Soay sheep (Ovis aries) mortality during a population crash. Parasitology 105:493–503CrossRefGoogle Scholar
  22. Higham J, Warren Y, Adanu J, Umaru B, MacLarnon A, Sommer V, Ross C (2009) Living on the edge: life-history of olive baboons at Gashaka-Gumti National Park, Nigeria. Am J Primatol 71:293–304CrossRefGoogle Scholar
  23. Homewood K, Rodgers W (1981) A previously undescribed mangabey from southern Tanzania. Int J Primatol 2:47–55CrossRefGoogle Scholar
  24. Houdijk J, Jessop N, Kyriazakis I (2001) Nutrient partitioning between reproductive and immune functions in animals. Proc Nutr Soc 60:515–525CrossRefGoogle Scholar
  25. Hsu M, Lin J, Agoramoorthy G (2006) Effects of group size on birth rate, infant mortality and social interactions in Formosan macaques at Mt longevity, Taiwan. Ethol Ecol Evol 18:3–17CrossRefGoogle Scholar
  26. Hull M, Glazener C, Kelly N, Conway D, Foster P, Hinton R, Coulson C, Lambert P, Watt E, Desai K (1985) Population study of causes, treatment, and outcome of infertility. Br Med J (Clin Res Ed) 291:1693–1697CrossRefGoogle Scholar
  27. Isbell L, Young T, Jaffe K, Carlson A, Chancellor R (2009) Demography and life histories of sympatric patas monkeys, Erythrocebus patas, and vervets, Cercopithecus aethiops, in Laikipia, Kenya. Int J Primatol 30:103–124CrossRefGoogle Scholar
  28. Jensenius M, Fournier P, Raoult D (2004) Rickettsioses and the international traveler. Clin Infect Dis 39:1493–1499CrossRefGoogle Scholar
  29. Jones T, Laurent S, Mselewa F, Mtui A (2006) Sanje mangabey Cercocebus sanei kills an African crowned eagle Stephanoaetus coronatus. Folia Primatologica, 77:359–363.Google Scholar
  30. Kalter S, Kuntz R, Myers B, Eugster A, Rodriguez A, Benke M, Kalter G (1968) The collection of biomedical specimens from baboons (Papio sp.) Kenya, 1966. Primates 9:123–139CrossRefGoogle Scholar
  31. Kuntz R, Myers B (1967) Parasites of the Kenya baboon: arthropods, blood protozoa and helminths (Kenya, 1966). Primates 8:75–82CrossRefGoogle Scholar
  32. Lacy RC, Clark TW (1990) Population viability assessment of eastern barred bandicoot. In: Clark TW, Seebeck JH (eds) The management and conservation of small populations. Chicago Zoological Society, Brookfield, pp 131–146Google Scholar
  33. Lee P (1987) Nutrition, fertility, and maternal investment in primates. J Zool 213:409–422CrossRefGoogle Scholar
  34. Lee P, Majluf P, Gordon I (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool 225:99–114CrossRefGoogle Scholar
  35. Lovett JC (1996) Elevational and latitudinal changes in tree associations and diversity in the Eastern Arc Mountains of Tanzania. J Trop Ecol 12:629–650Google Scholar
  36. Maina A, Jiang J, Omulo S, Cutler S, Ade F, Ogola E, Feikin D, Njenga M, Cleaveland S, Mpoke S, Ng'ang'a Z (2014) High prevalence of Rickettsia africae variants in Amblyomma variegatum ticks from domestic mammals in rural western Kenya: implications for human health. Vector Borne Zoonotic Dis 14:693–702CrossRefGoogle Scholar
  37. McCabe G, Emery Thompson M (2013) Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: relationship between the capital breeding strategy and infant survival. Behaviour 150:1399–1429CrossRefGoogle Scholar
  38. McCabe G, Fernández D, Ehardt C (2013) Ecology of reproduction in Sanje mangabeys (Cercocebus sanjei): dietary strategies and energetic condition during a high fruit period. Am J Primatol 75:1196–1208PubMedGoogle Scholar
  39. McCabe G, Fernández D, Butynski T, Struhsaker T, Rovero F (2018) Cercocebus sanjei The IUCN Red List of Threatened Species 2016 (in press)Google Scholar
  40. Miller J, Ahn S, Monsanto S, Khalaj K, Koti M, Tayade C (2017) Implications of immune dysfunction on endometriosis associated infertility. Oncotarget 8:7138–7147PubMedGoogle Scholar
  41. Milton K (1980) The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New YorkGoogle Scholar
  42. Mittermeier R, Robles Gil P, Hoffmann M, Pilgrim J, Brooks T, Mittermeier C, Lamoreux J, da Fonseca G (2004) Hotspots revisited. CEMEX, MexicoGoogle Scholar
  43. Nunn C, Altizer S (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  44. Parola P (2006) Rickettsioses in sub-Saharan Africa. Ann N Y Acad Sci 1078:42–47CrossRefGoogle Scholar
  45. Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831CrossRefGoogle Scholar
  46. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  47. Rasmussen K, Thenen S, Hayes K (1980) Effect of folic acid supplementation on pregnancy in the squirrel monkey (Saimiri sciureus). J Med Primatol 9:169–184CrossRefGoogle Scholar
  48. Rosso P (1990) Nutrition and metabolism in pregnancy. Oxford University Press, New YorkGoogle Scholar
  49. Rovero F, Marshall A, Jones T, Perkin A (2009) The primates of the Udzungwa Mountains: diversity, ecology and conservation. J Anthropol Sci 87:93–126PubMedGoogle Scholar
  50. Sigg H, Stolba A, Abegglen J, Dasser V (1982) Life history of hamadryas baboons: physical development, infant mortality, reproductive parameters and family relationships. Primates 23:473–487CrossRefGoogle Scholar
  51. Smuts B, Nicolson N (1989) Reproduction in wild female olive baboons. Am J Primatol 19:229–246CrossRefGoogle Scholar
  52. Struhsaker T, Marshall A, Detwiler K, Siex K, Ehardt C, Lisbjerg D, Butynski T (2004) Demographic variation among Udzungwa red colobus in relation to gross ecological and sociological parameters. Int J Primatol 25:615–658CrossRefGoogle Scholar
  53. Sugiyama Y, Ohsawa H (1982) Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding. Folia Primatol 39:238–263CrossRefGoogle Scholar
  54. Swedell L, Leedom L, Saunders J, Pines M (2014) Sexual conflict in a polygynous primate: costs and benefits of a male-imposed mating system. Behav Ecol Sociobiol 68:263–273CrossRefGoogle Scholar
  55. Therneau T (2015) A package for survival analysis in S. R package version 2.38Google Scholar
  56. Ullrey D, Allen M, Ausman L, Conklin-Brittain N, Edwards M, Erwin J, Holick M, Hopkins D, Lewis S, Lonnerdal B, Rudel L (2003) Nutritional requirements of non-human primates, 2nd edn. National Research Council: Committee on Animal Nutrition. The National Academies Press, Washington, D.CGoogle Scholar
  57. van den Broek N, Letsky E (2000) Etiology of anemia in pregnancy in South Malawi. Am J Clin Nutr 72:247–256CrossRefGoogle Scholar
  58. van Noordwijk M, van Schaik C (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Field Conservation and ScienceBristol Zoological SocietyBristolUK
  2. 2.Department of Applied SciencesUniversity of the West of EnglandBristolUK

Personalised recommendations