Behavioral Ecology and Sociobiology

, Volume 68, Issue 7, pp 1183–1193 | Cite as

Costs of reproduction in a long-lived female primate: injury risk and wound healing

  • Elizabeth A. Archie
  • Jeanne Altmann
  • Susan C. Alberts
Original Paper


Reproduction is a notoriously costly phase of life, exposing individuals to injury, infectious disease, and energetic trade-offs. The strength of these costs should be influenced by life history strategies, and in long-lived species, females may be selected to mitigate costs of reproduction because life span is such an important component of their reproductive success. Here, we report evidence for two costs of reproduction that may influence survival in wild female baboons—injury risk and delayed wound healing. Based on 29 years of observations in the Amboseli ecosystem, Kenya, we found that wild female baboons experienced the highest risk of injury on days when they were most likely to be ovulating. In addition, lactating females healed from wounds more slowly than pregnant or cycling females, indicating a possible trade-off between lactation and immune function. We also found variation in injury risk and wound healing with dominance rank and age: Older and low-status females were more likely to be injured than younger or high-status females, and older females exhibited slower healing than younger females. Our results support the idea that wild nonhuman primates experience energetic and immune costs of reproduction and they help illuminate life history trade-offs in long-lived species.


Aging Social status Ecoimmunology Lactation Reproductive effort 



We gratefully acknowledge the support of the National Science Foundation for the majority of the data represented here, most recently through IOS 1053461, IBN 9985910, IBN 0322613, IBN 0322781, BCS 0323553, BCS 0323596, DEB 0846286, DEB 0846286, DEB 0846532, and IOS 0919200. We are also grateful to the National Institute of Aging (R01AG034513-01 and P01AG031719) and the Princeton Center for the Demography of Aging (P30AG024361). We also thank the Chicago Zoological Society, the L.S.B. Leakey Foundation, the Max Planck Institute for Demography, and the National Geographic Society. We thank the Office of the President of the Republic of Kenya, the Kenya Wildlife Service, its Amboseli staff and Wardens, the members of the Amboseli-Longido pastoralist communities, and the Institute for Primate Research in Nairobi for their cooperation and assistance. We are also grateful to the Amboseli Baboon Project long-term field team (R.S. Mututua, S. Sayialel, and J.K. Warutere) and to V. Somen and T. Wango for their assistance in Nairobi. Several people contributed to long-term data collection, especially the late G. Hausfater, who established the protocol for this data set, and N. Learn, L. Opkala, and K. Pinc, who prepared the database for analyses.

Data accessibility

Data sets on observations of injuries and rates of wound healing will be deposited in Dryad (

Ethical standards

All protocols were noninvasive and adhered to the laws and guidelines of Kenya (Kenya Research Permit numbers NCST RRI/12/1/SS011/1543 to EAA, NCST 5/002/R/777 to SCA, and NCST 5/002/R/776 to JA). All protocols were approved by the Animal Care and Use Committees at the University of Notre Dame (13-030), Duke University (A0840903), and Princeton University (1689).

Supplementary material

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  1. Alberts SC, Altmann J (2012) The Amboseli Baboon Research Project: themes of continuity and change. In: Kappeler P, Watts DP (eds) Long-term field studies of primates. Springer Verlag, New York, pp 261–287CrossRefGoogle Scholar
  2. Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277CrossRefGoogle Scholar
  3. Allison PD (2010) Survival analysis using SAS. SAS Institute, Cary, NCGoogle Scholar
  4. Altmann SA (1973) The pregnancy sign in savannah baboons. J Zoo Anim Med 4:8–12CrossRefGoogle Scholar
  5. Altmann J (1980) Baboon Mothers and Infants. Harvard University Press, Cambridge, MAGoogle Scholar
  6. Altmann J (1983) Costs of reproduction in baboons. In: Aspey WP, Lustick SI (eds) Behavioral energetics: the cost of survival in vertebrates. Ohio State University Press, Columbus, pp 67–88Google Scholar
  7. Altmann J, Alberts SC (2003) Intraspecific variability in fertility and offspring survival in a nonhuman primate: behavioral control of ecological and social sources. In: Wachter KW, Bulatao RA (eds) Offspring: the biodemography of fertility and family behavior. National Academy Press, Washington, DC, pp 140–169Google Scholar
  8. Altmann J, Samuels A (1992) Costs of maternal care: infant-carrying in baboons. Behav Ecol Sociobiol 29:391–398CrossRefGoogle Scholar
  9. Altmann J, Altmann SA, Hausfater G (1978) Primate infant's effects on mother's future reproduction. Science 201:1028–1030PubMedCrossRefGoogle Scholar
  10. Altmann J, Lynch JW, Nguyen N, Alberts SC, Gesquiere LR (2004) Life-history correlates of steroid concentraions in wild peripartum baboons. Am J Primatol 64:95–106PubMedCrossRefGoogle Scholar
  11. Altmann J, Gesquiere L, Galbany J, Onyango PO, Alberts SC (2010) Life history context of reproductive aging in a wild primate model. Ann NY Acad Sci 1204:127–38PubMedCentralPubMedCrossRefGoogle Scholar
  12. Archie EA (2013) Wound healing in the wild: stress, sociality, and energetic costs affect wound healing in natural populations. Parasitol Immunol 35:374–385Google Scholar
  13. Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. Proc Natl Acad Sci U S A 109:9017–9022PubMedCentralPubMedCrossRefGoogle Scholar
  14. Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524CrossRefGoogle Scholar
  15. Ashcroft GS, Mills SJ, Ashworth JJ (2002) Ageing and wound healing. Biogerontology 3:337–45PubMedCrossRefGoogle Scholar
  16. Barton RA (1993) Sociospatial mechanisms of feeding competition in female olive baboons, Papio anubis. Anim Behav 46:791–802CrossRefGoogle Scholar
  17. Beehner JC, Nguyen N, Wango EO, Alberts SC, Altmann J (2006) The endocrinology of pregnancy and fetal loss in wild baboons. Horm Behav 49:688–699PubMedCrossRefGoogle Scholar
  18. Bercovitch FB (1987) Female weight and reproductive condition in a population of olive baboons (Papio anubis). Am J Primatol 12:189–195CrossRefGoogle Scholar
  19. Bonenfant C, Gaillard J, Coulson T, Festa-Bianchet M, Loison A, Garel M, Loe LE, Blanchard P, Pettorelli N, Owen-Smith N, du Toit JT, Duncan P (2009) Empirical evidence of density dependence in populations of large herbivores. Adv Ecol Res 41:313–357CrossRefGoogle Scholar
  20. Bowen WD, Iverson SJ, Boness DJ, Oftedal OT (2001) Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Funct Ecol 15:325–334CrossRefGoogle Scholar
  21. Bulger JB, Hamilton WJ (1987) Rank and density correlates of inclusive fitness measures in a natural chacma baboon (Papio ursinus) troop. Int J Primatol 8:635–650CrossRefGoogle Scholar
  22. Charpentier MJE, Tung J, Altmann J, Alberts SC (2008) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17:2026–2040PubMedCrossRefGoogle Scholar
  23. Cheney DL, Seyfarth RM, Fischer J, Beehner J, Bergman T, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2004) Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int J Primatol 25:401–428CrossRefGoogle Scholar
  24. Cheney DL, Silk JB, Seyfarth RM (2012) Evidence for intrasexual selection in wild female baboons. Anim Behav 84:21–27CrossRefGoogle Scholar
  25. Chilvers BL, Robertson BC, Wilkinson IS, Duignan PJ, Gemmell NJ (2005) Male harassment of female New Zealand sea lions, Phocarctos hookeri: mortality, injury, and harassment avoidance. Can J Zool 83:642–648CrossRefGoogle Scholar
  26. Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262PubMedCrossRefGoogle Scholar
  27. Cohen BJ, Cutler RG, Roth GS (1987) Accelerated wound repair in old deer mice (Peromyscus maniculatus) and white-footed mice (Peromyscus leucopus). J Gerontol 42:302–307PubMedCrossRefGoogle Scholar
  28. Cox RM, Calsbeek R (2010) Severe costs of reproduction persist in anolis lizards despite the evolution of a single-egg clutch. Evolution 64:1321–1330PubMedCrossRefGoogle Scholar
  29. de Groot J, Boersma WJA, Scholten JW, Koolhaas JM (2002) Social stress in male mice impairs long-term antiviral immunity selectively in wounded subjects. Physiol Behav 75:277–285PubMedCrossRefGoogle Scholar
  30. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710–730PubMedCrossRefGoogle Scholar
  31. Dufour DL, Sauther ML (2002) Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am J Hum Biol 14:584–602PubMedCrossRefGoogle Scholar
  32. Emmerson E, Hardman MJ (2012) The role of estrogen deficiency in skin ageing and wound healing. Biogerontology 13:3–20PubMedCrossRefGoogle Scholar
  33. Festa-Bianchet M (1989) Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). J Anim Ecol 58:785–795CrossRefGoogle Scholar
  34. French SS, Moore MC (2008) Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. Gen Comp Endocrinol 155:148–156PubMedCrossRefGoogle Scholar
  35. French SS, DeNardo DF, Moore MC (2007a) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170:79–89PubMedCrossRefGoogle Scholar
  36. French SS, Johnston GIH, Moore MC (2007b) Immune activity suppresses reproduction in food-limited female tree lizards Urosaurus ornatus. Funct Ecol 21:1115–1122CrossRefGoogle Scholar
  37. French SS, Moore MC, Demas GE (2009) Ecological immunology: the organism in context. Integr Comp Biol 49:246–253PubMedCrossRefGoogle Scholar
  38. French SS, Dearing MD, Demas GE (2011) Leptin as a physiological mediator of energetic trade-offs in ecoimmunology: implications for disease. Integr Comp Biol 51:505–513PubMedCrossRefGoogle Scholar
  39. Gesquiere LR, Wango EO, Alberts SC, Altmann J (2007) Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51:114–125PubMedCrossRefGoogle Scholar
  40. Gesquiere LR, Khan M, Shek L, Wango TL, Wango EO, Alberts SC, Altmann J (2008) Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 54:410–416PubMedCentralPubMedCrossRefGoogle Scholar
  41. Gesquiere LR, Onyango PO, Alberts SC, Altmann J (2010) Endocrinology of year-round reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 144:169–176PubMedCentralPubMedCrossRefGoogle Scholar
  42. Gesquiere L, Learn NH, Simao MCM, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: energetic and psychological stress in wild male primates. Science 333:357–360PubMedCentralPubMedCrossRefGoogle Scholar
  43. Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875Google Scholar
  44. Glasper ER, DeVries AC (2005) Social structure influences effects of pair-housing on wound healing. Brain Behav Immun 19:61–68PubMedCrossRefGoogle Scholar
  45. Glass GE, Childs JE, Korch GW, LeDuc JW (1988) Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101:459–72PubMedCentralPubMedCrossRefGoogle Scholar
  46. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662–5PubMedCrossRefGoogle Scholar
  47. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnstrom A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans Roy Soc B 346:323–331CrossRefGoogle Scholar
  48. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  49. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc Lond B 272:1039–1046CrossRefGoogle Scholar
  50. Hart BL (2011) Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Philos Trans Roy Soc B366:3406–3417CrossRefGoogle Scholar
  51. Hart BL, Powell KL (1990) Antibacterial properties of saliva: role in maternal periparturient grooming and in licking wounds. Physiol Behav 48:383–386PubMedCrossRefGoogle Scholar
  52. Hausfater G (1975) Dominance and reproduction in baboons: a quantitative analysis. S. Karger, BaselGoogle Scholar
  53. Houdijk JGM (2008) Influence of periparturient nutritional demand on resistance to parasites in livestock. Parasitol Immunol 30:113–121CrossRefGoogle Scholar
  54. Huchard E, Cowlishaw G (2011) Female-female aggression around mating: an extra cost of sociality in a multimale primate society. Behav Ecol 22:1003–1011CrossRefGoogle Scholar
  55. Jones LA, Houdijk JGM, Sakkas P, Bruce AD, Mitchell M, Knox DP, Kyriazakis I (2011) Dissecting the impact of protein versus energy host nutrition on the expression of immunity to gastrointestinal parasites during lactation. Int J Parasitol 41:711–719PubMedCrossRefGoogle Scholar
  56. Kiecolt-Glaser JK, Marucha PT, Malarkey WB, Mercado AM, Glaser R (1995) Slowing of wound healing by psychological stress. Lancet 346:1194–1196PubMedCrossRefGoogle Scholar
  57. Konig B, Riester J, Markl H (1988) Maternal care in house mice (Mus musculus): II. The energy cost of lactation as a function of litter size. J Zool 216:195–210CrossRefGoogle Scholar
  58. MacCormick HA, MacNulty DR, Bosacker AL, Lehman C, Collins DA, Packer C (2012) Male and female aggression: lessons from sex, rank, age, and injury in olive baboons. Behav Ecol 24:683–691Google Scholar
  59. Martin P (1997) Wound healing–aiming for perfect skin regeneration. Science 276:75–81PubMedCrossRefGoogle Scholar
  60. Martin LB, Glasper ER, Nelson RJ, DeVries AC (2006a) Prolonged separation delays wound healing in monogamous California mice, Peromyscus californicus, but not in polygynous white-footed mice, P. leucopus. Physiol Behav 87:837–841PubMedCrossRefGoogle Scholar
  61. Martin LB, Weil ZM, Kuhlman JR, Nelson RJ (2006b) Trade-offs within the immune systems of female white-footed mice, Peromyscus leucopus. Funct Ecol 20:630–636CrossRefGoogle Scholar
  62. Martin LB, Weil ZM, Nelson RJ (2007) Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516–2528PubMedCrossRefGoogle Scholar
  63. Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans Roy Soc B 363:321–39CrossRefGoogle Scholar
  64. Marucha PT, Kiecolt-Glaser JK, Favagehi M (1998) Mucosal wound healing is impaired by examination stress. Psychosom Med 60:362–365PubMedGoogle Scholar
  65. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018PubMedCrossRefGoogle Scholar
  66. Muruthi P, Altmann J, Altmann S (1991) Resource base, parity and reproductive condition affect females' feeding time and nutrient intake within and between groups of a baboon population. Oecologia 87:467–472CrossRefGoogle Scholar
  67. Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298CrossRefGoogle Scholar
  68. Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Philos Trans Roy Soc B 364:61–69CrossRefGoogle Scholar
  69. Nussey DH, Watt K, Pilkington JG, Zamoyska R, McNeilly TN (2012) Age-related variation in immunity in a wild mammal population. Aging Cell 11:178–80PubMedCentralPubMedCrossRefGoogle Scholar
  70. Nussey DH, Froy H, Lemaitre JF, Gaillard JM, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–25PubMedCrossRefGoogle Scholar
  71. Ots I, Horak P (1996) Great tits Parus major trade health for reproduction. Proc R Soc Lond B 263:1443–1447CrossRefGoogle Scholar
  72. Padgett DA, Marucha PT, Sheridan JF (1998) Restraint stress slows cutaneous wound healing in mice. Brain Behav Immun 12:64–73PubMedCrossRefGoogle Scholar
  73. Post DG, Hausfater G, Mccuskey SA (1980) Feeding behavior of yellow baboons (Papio cynocephalus): relationship to age, gender and dominance Rank. Folia Primatol 34:170–195PubMedCrossRefGoogle Scholar
  74. Roberts SB, Cole TJ, Coward WA (1985) Lactational performance in relation to energy-intake in the baboon. Am J Clin Nutr 41:1270–1276PubMedGoogle Scholar
  75. Rojas IG, Padgett DA, Sheridan JF, Marucha PT (2002) Stress-induced susceptibility to bacterial infection during cutaneous wound healing. Brain Behav Immunol 16:74–84CrossRefGoogle Scholar
  76. Rolff J (2002) Bateman's principle and immunity. Proc R Soc Lond B 269:867–72CrossRefGoogle Scholar
  77. Rosetta L, Lee PC, Garcia C (2011) Energetics during reproduction: a doubly labeled water study of lactating baboons. Am J Phys Anthropol 144:661–668PubMedCrossRefGoogle Scholar
  78. Routley CE, Ashcroft GS (2009) Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen 17:42–50PubMedCrossRefGoogle Scholar
  79. Sakkas P, Houdijk JGM, Jones LA, Knox DP, Kyriazakis I (2011) Dietary protein and energy supplies differentially affect resistance to parasites in lactating mammals. Br J Nutr 106:1207–1215PubMedCrossRefGoogle Scholar
  80. Seno H, Miyoshi H, Brown SL, Geske MJ, Colonna M, Stappenbeck TS (2009) Efficient colonic mucosal wound repair requires Trem2 signaling. Proc Natl Acad Sci U S A 106:256–261PubMedCentralPubMedCrossRefGoogle Scholar
  81. Seyfarth RM (1976) Social relationships among adult female baboons. Anim Behav 24:917–938CrossRefGoogle Scholar
  82. Shaikh AA, Celaya CL, Gomez I, Shaikh SA (1982) Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23:444–452CrossRefGoogle Scholar
  83. Silk JB (1986) Eating for two: behavioral and environmental correlates of gestation length among free-ranging baboons (Papio cynocephalus). Int J Primatol 7:583–602CrossRefGoogle Scholar
  84. Silk JB (1987) Activities and feeding behavior of free-ranging pregnant baboons. Int J Primatol 8:593–613CrossRefGoogle Scholar
  85. Silk JB, Rendall D, Cheney DL, Seyfarth RM (2003) Natal attraction in adult female baboons (Papio cynocephalus ursinus) in the Moremi Reserve, Botswana. Ethology 109:627–644CrossRefGoogle Scholar
  86. Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738–46PubMedCrossRefGoogle Scholar
  87. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  88. Stockley P, Bro-Jorgensen J (2011) Female competition and its evolutionary consequences in mammals. Biol Rev 86:341–366PubMedCrossRefGoogle Scholar
  89. Van Horn RC, Buchan JC, Altmann J, Alberts SC (2007) Divided destinies: group choice of female savannah baboons during social group fission. Behav Ecol Sociobiol 61:1823–1837CrossRefGoogle Scholar
  90. Wasser SK, Starling AK (1988) Proximate and ultimate causes of reproductive suppression among female yellow baboons at Mikumi National Park, Tanzania. Am J Primatol 16:97–121CrossRefGoogle Scholar
  91. Wildt DE, Doyle LL, Stone SC, Harrison RM (1977) Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle. Primates 18:261–270CrossRefGoogle Scholar
  92. Williams GC (1966) Natural selection, the costs of reproduction and a refinement of Lack’s principle. Am Nat 100:687–690CrossRefGoogle Scholar
  93. Wilson BS (1992) Tail injuries increase the risk of mortality in free-living lizards (Uta stansburiana). Oecologia 92:145–152CrossRefGoogle Scholar
  94. Wynn TA (2004) Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 4:583–594PubMedCentralPubMedCrossRefGoogle Scholar
  95. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023PubMedCrossRefGoogle Scholar
  96. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Elizabeth A. Archie
    • 1
    • 2
  • Jeanne Altmann
    • 2
    • 3
    • 4
  • Susan C. Alberts
    • 5
    • 2
  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Institute of Primate Research, National Museums of KenyaNairobiKenya
  3. 3.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA
  4. 4.Department of Veterinary Anatomy and PhysiologyUniversity of NairobiNairobiKenya
  5. 5.Department of BiologyDuke UniversityDurhamUSA

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