Behavioral Ecology and Sociobiology

, Volume 69, Issue 2, pp 303–312 | Cite as

The costs of parental and mating effort for male baboons

  • Dorothy L. Cheney
  • Catherine Crockford
  • Anne L. Engh
  • Roman M. Wittig
  • Robert M. Seyfarth
Original Paper

Abstract

Sexual selection theory predicts that males in polygynous species of mammals will invest more reproductive effort in mate competition than parental investment. A corollary to this prediction is that males will mount a stress response when their access to mates is threatened. Indeed, numerous studies have shown that males exhibit elevated stress hormones, or glucocorticoids (GCs), when their access to females, or a proxy to this access like dominance rank, is challenged. In contrast, the relationship between stress hormones and paternal effort is less obvious. We report results from a study of wild male chacma baboons indicating that males experienced elevated GC levels during periods of social instability following the immigration of a dominant male. These effects were strongest in males whose mating opportunities were at greatest risk: high-ranking males and males engaged in sexual consortships. Males involved in friendships with lactating females, a form of paternal investment, also experienced high GC levels during these periods of instability. There was a tendency for males with lactating female friends to reduce their time spent in consortships during unstable periods, when the risk of infanticide was high. Thus, even in a highly polygynous mammal, males may have to balance paternal effort with mating effort. Males who invest entirely in mating effort risk losing the infants they have sired to infanticide. Males who invest in paternal care may enhance their offspring’s survival, but at the cost of elevated GC levels, the risk of injury, and the loss of mating opportunities.

Keywords

Male baboons Parental and mating effort Paternal care Sexual selection 

Notes

Acknowledgments

We thank the Office of the President of the Republic of Botswana and the Botswana Department of Wildlife and National Parks for permission to conduct research in the Moremi Reserve. We are grateful to R. Hoffmeier, K. Seyfarth, E. Wikberg, M. Mokopi, and A. Mokopi for assistance with data collection. We thank J. Beehner for comments and R. Mundry for advice on statistics. Research was supported by the National Science Foundation, the National Institutes of Health, the Leakey Foundation, the National Geographic Society, and the University of Pennsylvania.

Ethical standards

This project complied with regulations in the Republic of Botswana (Department of Wildlife and National Parks) and in the USA (University of Pennsylvania, Animal Care and Use Committee, Protocol no.19001).

References

  1. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196CrossRefGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:229–267CrossRefGoogle Scholar
  3. Bales KL, Kramer KM, Lewis-Reese AD, Carter CS (2006) Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol Behav 87:424–429PubMedCrossRefGoogle Scholar
  4. Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A (2002) Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav 42:85–96PubMedCrossRefGoogle Scholar
  5. Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2005) The effect of new alpha males on female stress in free-ranging baboons. Anim Behav 69:1211–1221CrossRefGoogle Scholar
  6. Beehner JC, Gesquiere L, Seyfarth RM, Cheney DL, Alberts SC, Altmann J (2009) Testosterone related to age and life-history stages in male baboons and geladas. Horm Behav 56:472–480PubMedCentralPubMedCrossRefGoogle Scholar
  7. Beehner JC, Whitten PL (2004) Modifications of a field method for faecal steroid analysis in baboons. Physiol Behav 82:269–277PubMedCrossRefGoogle Scholar
  8. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL (2005) Correlates of stress in free-ranging male chacma baboons. Anim Behav 70:703–713CrossRefGoogle Scholar
  9. Buchan J, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181PubMedCrossRefGoogle Scholar
  10. Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103CrossRefGoogle Scholar
  11. Carlson AA, Manser MB, Young AJ, Russell AJ, Jordan NR, McNeilly AS, Clutton-Brock T (2006) Cortisol levels are positively associated with pup-feeding rates in male meerkats. Proc R Soc Lond B 273:571–577CrossRefGoogle Scholar
  12. Cavanaugh J, French JA (2013) Post-partum variation in the expression of paternal care is unrelated to urinary steroid metabolites in marmoset fathers. Horm Behav 63:551–558PubMedCentralPubMedCrossRefGoogle Scholar
  13. 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
  14. Clarke PMR, Henzi SP, Barrett L (2009) Sexual conflict in chacma baboons (Papio hamadryas ursinus): absent males select for proactive females. Anim Behav 77:1217–1225CrossRefGoogle Scholar
  15. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  16. Crockford C, Wittig RM, Whitten PL, Seyfarth RM, Cheney DL (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53:254–265PubMedCrossRefGoogle Scholar
  17. Deschner T, Kratzsch J, Hohmann G (2008) Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Horm Behav 54:620–626PubMedCrossRefGoogle Scholar
  18. Engh AE, Beehner JC, Bergman TJ, Whitten PL, Hoffmeier RR, Seyfarth RM, Cheney DL (2006) Female hierarchy instability, male immigration, and infanticide increase glucocorticoid levels in female chacma baboons. Anim Behav 71:1227–1237CrossRefGoogle Scholar
  19. Fischer J, Kitchen DM, Seyfarth RM, Cheney DL (2004) Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion. Behav Ecol Sociobiol 56:140–148CrossRefGoogle Scholar
  20. Gesquiere LR, Learn NH, Simao CM, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: rank and stress in wild male baboons. Science 333:357–360PubMedCentralPubMedCrossRefGoogle Scholar
  21. Girard-Buttoz C, Heistermann M, Rahmi E, Marzec A, Agil M, Fauzan PA, Engelhardt A (2014a) Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): physiological stress and aggression. Horm Behav 66:637–648PubMedCrossRefGoogle Scholar
  22. Girard-Buttoz C, Heistermann M, Rahmi E, Marzec A, Agil M, Fauzan PA, Engelhardt A (2014b) Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis). Behav Ecol Sociobiol 68:583–595PubMedCentralPubMedCrossRefGoogle Scholar
  23. Goymann W, Wingfield JC (2004) Allostatic load, social status, and stress hormones—the costs of social status matter. Anim Behav 67:591–602CrossRefGoogle Scholar
  24. Henkel S, Heistermann M, Fischer J (2010) Infants as costly social tools in male Barbary macaque networks. Anim Behav 79:1199–1206CrossRefGoogle Scholar
  25. Higham JP, Heistermann M, Maestripieri D (2013) The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67:19–30PubMedCentralPubMedCrossRefGoogle Scholar
  26. Huchard E, Alvergne A, Fejan D, Knapp LA, Cowlishaw G (2010) More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons. Behav Ecol Sociobiol 64:769–781CrossRefGoogle Scholar
  27. Kitchen DM, Cheney DL, Seyfarth RM (2005) Contextual factors mediating contests between male chacma baboons in Botswana: the effect of food, friends, females. Int J Primatol 26:105–125CrossRefGoogle Scholar
  28. Kitchen DM, Seyfarth RM, Fischer J, Cheney DL (2003) Loud calls as an indicator of dominance in male baboons, Papio cynocephalus ursinus. Behav Ecol Sociobiol 53:374–384Google Scholar
  29. Maynard Smith J (1977) Parental investment: a prospective analysis. Anim Behav 25:1–9CrossRefGoogle Scholar
  30. Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol 63:1471–1482PubMedCentralPubMedCrossRefGoogle Scholar
  31. Moscovice LR, DiFiore A, Crockford C, Kitchen DW, Wittig R, Seyfarth RM, Cheney DL (2010) Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. Anim Behav 79:1007–1015CrossRefGoogle Scholar
  32. Muller MN, Wrangham RW (2004) Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 55:332–340CrossRefGoogle Scholar
  33. Nguyen N, Van Horn RC, Alberts SC, Altmann J (2009) “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol 63:1331–1344PubMedCentralPubMedCrossRefGoogle Scholar
  34. Nunes S, Fite JE, Patera KJ, French JA (2001) Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm Behav 39:70–78PubMedCrossRefGoogle Scholar
  35. Onyango PO, Gesquiere LR, Altmann J, Alberts SC (2013) Testosterone positively associated with both male mating effort and paternal behavior in savanna baboons (Papio cynocephalus). Horm Behav 63:430–436PubMedCentralPubMedCrossRefGoogle Scholar
  36. Ostner J, Heistermann M, Schulke O (2008) Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 54:613–619PubMedCrossRefGoogle Scholar
  37. Palombit RA, Cheney D, Seyfarth R, Rendall D, Silk J, Johnson S, Fischer J (2000) Male infanticide and defense of infants in chacma baboons. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 123–152CrossRefGoogle Scholar
  38. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of “friendships” to female baboons: experimental and observational evidence. Anim Behav 54:599–614PubMedCrossRefGoogle Scholar
  39. Queller D (1997) Why do females care more than males? Proc R Soc Lond B 264:1555–1557CrossRefGoogle Scholar
  40. Sapolsky RM (1992) Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 17:701–709PubMedCrossRefGoogle Scholar
  41. Sapolsky RM (2004) Why zebras don’t get ulcers, 3rd edn. WH Freeman, New YorkGoogle Scholar
  42. Setchell JM, Smite TE, Wickings J, Knapp LA (2010) Stress, social behaviour, and secondary sexual traits in a male primate. Horm Behav 58:720–728PubMedCrossRefGoogle Scholar
  43. Seyfarth RM (1978) Social relationships among adult male and female baboons: II behaviour throughout the female reproductive cycle. Behaviour 64:227–247CrossRefGoogle Scholar
  44. Smuts BB (1985) Sex and friendship in baboons. Aldine, New YorkGoogle Scholar
  45. Surbeck M, Deschner T, Weltring A, Hohmann G (2012) Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Horm Behav 62:27–35PubMedCrossRefGoogle Scholar
  46. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  47. Wasser S, Hunt K, Brown J, Cooper K, Crockett C, Bechert U, Millspaugh J, Larson S, Monfort S (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120:260–275PubMedCrossRefGoogle Scholar
  48. Weingrill T (2000) Infanticide and the value of male–female relationships in mountain chacma baboons. Behaviour 137:337–359CrossRefGoogle Scholar
  49. Weingrill T, Lycett JE, Henzi SP (2000) Consortship and mating success in chacma baboons (Papio cynocephalus ursinus). Ethology 106:1033–1044CrossRefGoogle Scholar
  50. Werren JH, Gross MR, Shine R (1980) Paternity and the evolution of male parental care. J Theor Biol 82:619–631PubMedCrossRefGoogle Scholar
  51. Wittig RM, Crockford C, Lehmann J, Whitten PL, Seyfarth RM, Cheney DL (2008) Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54:170–177PubMedCentralPubMedCrossRefGoogle Scholar
  52. Wynne-Edwards KE, Timonin ME (2007) Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 52:114–121PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Dorothy L. Cheney
    • 1
  • Catherine Crockford
    • 2
  • Anne L. Engh
    • 3
  • Roman M. Wittig
    • 2
  • Robert M. Seyfarth
    • 4
  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  3. 3.Department of BiologyKalamazoo CollegeKalamazooUSA
  4. 4.Deparment of PsychologyUniversity of PennsylvaniaPhiladelphiaUSA

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