Behavioral Ecology and Sociobiology

, Volume 70, Issue 11, pp 1921–1930 | Cite as

Testing socially mediated estrous synchrony or asynchrony in wild baboons

  • Yasuo Ihara
  • D. Anthony Collins
  • Ryo Oda
  • Akiko Matsumoto-Oda
Original Article


Social structure of animal groups is affected by the spatial and temporal distribution of females. In particular, the extent to which fertile periods of females are temporally overlapped has been deemed as a crucial factor to determine the structure of social groups in primate species. Dominant males are less able to monopolize fertile females when there are more females being in estrous simultaneously. This provides a potential opportunity for females to manipulate their defensibility by dominant males by modifying the level of estrous overlap. Previous studies that have attempted to detect socially mediated synchrony or asynchrony of estrous cycles have produced mixed results, some of which have been questioned on methodological grounds. Here, we address this issue using an exceptionally large dataset of daily reproductive states in four troops of wild anubis baboons (Papio anubis) over 14 to 24 years (77 troop-years). We compare observed levels of estrous synchrony with null distributions obtained by a randomization procedure under the assumption that estrous cycles are mutually independent among females in the same troop. We do not find any evidence supporting synchrony or asynchrony of estrous cycles. Based on our result and those of previous studies in other species of baboons, we conclude that socially mediated synchrony or asynchrony is unlikely to play a significant role in structuring social groups in baboons. In addition, our analysis points out that care should be taken when applying randomization procedures to a dataset with missing observations.

Significance statement

Females in some animal species have been suggested to synchronize or desynchronize their estrus cycles. This phenomenon may have a significant impact on the structure of animal societies because when there are more females simultaneously in estrus, even a dominant male is less able to defend them from other males. Previous attempts to detect non-random estrous cycles in primates have produced mixed results, and some of them have been criticized on the methodological grounds. We investigate whether wild female anubis baboons exhibit non-random estrous cycles using a larger dataset than previous studies. For a statistical analysis, we use a randomization procedure, taking a biasing effect of missing observations into consideration. Consistent with earlier studies on other species of baboons, our analysis does not find any evidence supporting estrous synchrony or asynchrony in anubis baboons.


Estrous synchrony index Female defensibility Female-female competition Ovarian cycle Papio anubis 



We thank Craig Packer, Anne E. Pusey, and the Jane Goodall Institute for permitting the use of their long-term data. We are grateful to the Tanzanian agencies of TANAPA, TAWIRI, and COSTECH for allowing research to be conducted in Gombe National Park. We thank Eiiti Kasuya for critical comments on an earlier draft and help during the process of making copies of the original datasheets stored at the University of Minnesota. Finally, we thank the Gombe Stream Research Centre staff for their work of collecting daily observational data. We also thank two anonymous reviewers for constructive comments. This work was supported by Japan Society for the Promotion of Science KAKENHI Grant Numbers 19570230, 23405016 (to AM-O).

Compliance with ethical standards


This study was funded by Japan Society for the Promotion of Science KAKENHI Grant Numbers 19,570,230, 23,405,016 (to AM-O).

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.


  1. Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï Forest. Am J Phys Anthropol 130:103–115CrossRefPubMedGoogle Scholar
  2. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181CrossRefPubMedGoogle Scholar
  3. Carnes LM, Nunn CL, Lewis RJ (2011) Effects of the distribution of female primates on the number of males. PLoS One 6:e19853CrossRefPubMedPubMedCentralGoogle Scholar
  4. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008) Paternal effects on offspring fitness in a multimale primate society. P Natl Acad Sci USA 105:1988–1992CrossRefGoogle Scholar
  5. Clarke PMR, Henzi SP, Barrett L (2012) Estrous synchrony in a nonseasonal breeder: adaptive strategy or population process? Behav Ecol 23:573–581CrossRefGoogle Scholar
  6. Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A (2011) Testing the priority-of-access model in a seasonally breeding primate species. Behav Ecol Sociobiol 65:1615–1627CrossRefPubMedPubMedCentralGoogle Scholar
  7. Dunbar RIM, Sharman M (1983) Female competition for access to males affects birth rate in baboons. Behav Ecol Sociobiol 13:157–159CrossRefGoogle Scholar
  8. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  9. French JA, Stribley JA (1987) Synchronization of ovarian cycles within and between social groups in golden lion tamarins (Leontopithecus rosalia). Am J Primatol 12:469–478CrossRefGoogle Scholar
  10. Fürtbauer I, Mundry R, Heistermann M, Schülke O, Ostner J (2011) You mate, I mate: macaque females synchronize sex not cycles. PLoS One 6:e26144CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gogarten JF, Koenig A (2013) Reproductive seasonality is a poor predictor of receptive synchrony and male reproductive skew among nonhuman primates. Behav Ecol Sociobiol 67:123–134CrossRefGoogle Scholar
  12. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for reproductive strategies of females. Ethol Sociobiol 1:13–40CrossRefGoogle Scholar
  13. Huchard E, Alvergne A, Féjan D, Knapp LA, Cowlishaw G, Raymond M (2010) More than friends? Behavioral and genetic aspects of heterosexual associations in wild chacma baboons. Behav Ecol Sociobiol 64:769–781CrossRefGoogle Scholar
  14. Johnstone RA (2000) Models of reproductive skew: a review and synthesis. Ethology 106:5–26CrossRefGoogle Scholar
  15. Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete model. Behav Ecol Sociobiol 60:695–706CrossRefGoogle Scholar
  16. Lehmann J, Fickenscher G, Boesch C (2006) Kin based investment in wild chimpanzees. Behaviour 143:931–955CrossRefGoogle Scholar
  17. Lemasson A, Palombit RA, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035CrossRefGoogle Scholar
  18. Lindenfors P, Fröberg L, Nunn CL (2004) Females drive primate social evolution. Proc R Soc Lond B 271:S101–S103CrossRefGoogle Scholar
  19. Matsumoto-Oda A, Ihara Y (2011) Estrous asynchrony causes low birth rates in wild female chimpanzees. Am J Primatol 73:180–188CrossRefPubMedGoogle Scholar
  20. Matsumoto-Oda A, Kasuya E (2005) Proximity and estrous synchrony in Mahale chimpanzees. Am J Primatol 66:159–166CrossRefPubMedGoogle Scholar
  21. Matsumoto-Oda A, Hamai M, Hayaki H, Hosaka K, Hunt KD, Kasuya E, Kawanaka K, Mitani JC, Takasaki H, Takahata Y (2007) Estrus cycle asynchrony in wild female chimpanzees, Pan troglodytes schweinfurthii. Behav Ecol Sociobiol 61:611–618CrossRefGoogle Scholar
  22. McClintock MK (1971) Menstrual synchrony and suppression. Nature 229:244–245CrossRefPubMedGoogle Scholar
  23. Mitani JC, Gros-Louis J, Manson JH (1996) Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38:315–332CrossRefGoogle Scholar
  24. Monfort SL, Bush M, Wildt DE (1996) Natural and induced ovarian synchrony in golden lion tamarins (Leontopithecus rosalia). Biol Reprod 55:875–882CrossRefPubMedGoogle Scholar
  25. Moscovice LR, Di Fiore A, Crockford C, Kitchen DM, 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
  26. 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 63:1331–1344CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nishida T, Corp N, Hamai M, et al. (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99–121CrossRefPubMedGoogle Scholar
  28. Nunn CL (1999a) The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13CrossRefGoogle Scholar
  29. Nunn CL (1999b) The evolution of exaggerated sexual swelling in primates and the graded-signal hypothesis. Anim Behav 58:229–246CrossRefPubMedGoogle Scholar
  30. Ostner J, Nunn CL, Schülke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150–1158CrossRefPubMedPubMedCentralGoogle Scholar
  31. Packer C, Collins DA, Sindimwo A, Goodall J (1995) Reproductive constraints on aggressive competition in female baboons. Nature 373:60–63CrossRefPubMedGoogle Scholar
  32. Palombit RA (2012) Infanticide: male strategies and female counterstrategies. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp. 432–468Google Scholar
  33. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614CrossRefPubMedGoogle Scholar
  34. Paul A (1996) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol 68:344–349CrossRefGoogle Scholar
  35. Pereira ME (1991) Asynchrony within estrous synchrony among ringtailed lemurs (primates: Lemuridae). Physiol Behav 49:47–52CrossRefPubMedGoogle Scholar
  36. Port M, Kappeler PM (2010) The utility of reproductive skew models in the study of male primates, a critical evaluation. Evol Anthropol 19:46–56CrossRefGoogle Scholar
  37. Rhine RJ, Norton GW, Wasser SK (2000) Lifetime reproductive success, longevity, and reproductive life history of female yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. Am J Primatol 51:229–241CrossRefPubMedGoogle Scholar
  38. Ridley M (1986) The number of males in a primate group. Anim Behav 34:1848–1858CrossRefGoogle Scholar
  39. Schank JC (2001) Measurement and cycle variability: reexamining the case for ovarian-cycle synchrony in primates. Behav Process 56:131–146CrossRefGoogle Scholar
  40. Setchell JM, Kendal J, Tyniec P (2011) Do non-human primates synchronise their menstrual cycles? A test in mandrills. Psychoneuroendocrino 36:51–59CrossRefGoogle Scholar
  41. Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. W. H. Freeman and Company, New YorkGoogle Scholar
  42. Stanford CB (2002) Avoiding predators: expectations and evidence in primate antipredator behavior. Int J Primatol 23:741–757CrossRefGoogle Scholar
  43. Tobler R, Pledger S, Linklater W (2010) No evidence for ovarian synchrony or asynchrony in hamadryas baboons. Anim Behav 80:829–837CrossRefGoogle Scholar
  44. van Schaik CP, Hörstermann M (1994) Predation risk and the number of adult males in a primate group: a comparative test. Behav Ecol Sociobiol 35:261–272CrossRefGoogle Scholar
  45. Wallis J (1985) Synchrony of estrous swelling in captive group-living chimpanzees (Pan troglodytes). Int J Primatol 6:335–350CrossRefGoogle Scholar
  46. Yang Z, Schank JC (2006) Women do not synchronize their menstrual cycles. Hum Nat 17:433–447CrossRefPubMedGoogle Scholar
  47. Zinner D, Schwibbe MH, Kaumanns W (1994) Cycle synchrony and probability of conception in female hamadryas baboons Papio hamadryas. Behav Ecol Sociobiol 35:175–183CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Yasuo Ihara
    • 1
  • D. Anthony Collins
    • 2
  • Ryo Oda
    • 3
  • Akiko Matsumoto-Oda
    • 4
  1. 1.Department of Biological Sciencesthe University of TokyoTokyoJapan
  2. 2.The Jane Goodall Institute, Gombe Stream Research CentreKigomaTanzania
  3. 3.Graduate School of EngineeringNagoya Institute of TechnologyNagoyaJapan
  4. 4.Graduate School of Tourism SciencesUniversity of the RyukyusOkinawaJapan

Personalised recommendations