, Volume 47, Issue 1, pp 43–50 | Cite as

Environmental factors influencing the seasonality of estrus in chimpanzees

  • Dean P. AndersonEmail author
  • Erik. V. Nordheim
  • Christophe Boesch
Original Article


Although the energetics of the estrous cycle in primates is not well understood, evidence suggests that energy and nutrient acquisition influence ovulation and the timing of conception. Energy for estrus has to compete with energy allocated for cellular maintenance, thermoregulation, movement for food, and predation avoidance. While some chimpanzee (Pan troglodytes) populations do not have a seasonal birth period, evidence suggests that there is seasonality in the number of estrous females. Similarly, the onset of postpartum cycles has been reported to be seasonal. We used 33 months of data from the Taï National Park, Côte d’Ivoire, to examine how the number of estrous females in a given month was influenced by the abundance and distribution of food, diet, rainfall and temperature. In a second analysis, we examined if there was a seasonal effect on first estrous swellings in adolescent females and postpartum adult females. Results demonstrated that the number of females in estrous in a given month was positively related to food abundance and percent foraging time spent eating insects, and negatively related to mean rainfall in the two preceding months and the mean high temperature. The timing of first estrous swellings of postpartum females and prepartum young females was positively related to the food abundance, and negatively related to mean high temperature. These results showed that environmental conditions can seasonally limit the energetically demanding estrus cycle. The presence of estrous females increases gregariousness in chimpanzee communities, and this study identified environmental factors that affect estrus directly and hence social grouping indirectly.


Chimpanzee Environmental factors Estrus Pan troglodytes Social grouping 



D.P.A. thanks Juichi Yamagiwa for the invitation to participate in the symposium African Great Apes: Evolution, Diversity and Conservation. Funding for this research was provided by the Max Planck Society, the L.S.B. Leakey Foundation, the National Science Foundation, and U.S.A.I.D. – Program for Science and Technology (Timothy Moermond, P.I.). We are grateful to the Ministries of Eaux et Forêts and La Recherche Scientifique for granting permission to conduct this study. The Projet Autonome pour la Conservation du Parc National de Taï, the Centre Suisse pour la Recherche Scientifique en Côte d’Ivoire, and the Centre de Recherche Ecologique were valuable collaborators in this research. We thank all of the assistants of the Taï Chimpanzee Project, especially those involved with the behavioral and vegetation data collection; Néné Kpazahi Honora, Kohou Nohon Grégoire, Glebeo Pierre Polé, Bally Wabo Albert, Tahou Mompeho Jonas, and Dji Troh Camille. Ronald Noë kindly provided the climate data. Susanne Anderson assisted with data collection and management. Thomas Gordon provided computer assistance in the field. Téré Henri helped with the identification of plant species. Jakob and Marie Zinsstag provided logistic support in Abidjan. Helpful comments on the manuscript were provided by Janette Wallis Thomas J. Givnish, Monica G. Turner, Timothy C. Moermond, Karen B. Strier, and two anonymous reviewers for their comments on this manuscript.


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedGoogle Scholar
  2. Altmann J (1980) Baboon mothers and infants. Harvard University Press, CambridgeGoogle Scholar
  3. Anderson DP, Nordheim EV, Boesch C, Moermond TC (2002) Factors Influencing fission-fusion grouping in chimpanzees in the Taï Forest, Côte d’Ivoire. In: Boesch C, Hohmann G, Marchant LF (eds) Chimpanzee behavioural diversity. Cambridge University Press, CambridgeGoogle Scholar
  4. Anderson DP, Nordheim EV, Bi ZBG, Boesch C (2005) Deviations in tropical tree phenology patterns caused by climatic variables. Biotropica (in press).Google Scholar
  5. Bercovitch FB (1987) Female weight and reproductive condition in a population of olive baboons(Papio cynocephalus anubis). Am J Primatol 12:189–195CrossRefGoogle Scholar
  6. Boesch C, Boesch H (1983) Optimization of nut-cracking with natural hammers by wild chimpanzees. Behaviour 83:265–286Google Scholar
  7. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï Forest: behavioural ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  8. Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, ChicagoGoogle Scholar
  9. Butynski TM (1988) Guenon birth seasons and correlates with rainfall and food. In: Gautier-Hion A, Bourlière F, Gautier JP Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 284–322Google Scholar
  10. Chapman CA, Chapman LJ, Wrangham RW, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531Google Scholar
  11. Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70CrossRefGoogle Scholar
  12. Chapman CA, Wrangham RW, Chapman LJ, Kennard DK, Zanne AE (1999) Fruit and flower phenology at two sites in Kibale National Park, Uganda. J Trop Ecol 15:189–211CrossRefGoogle Scholar
  13. Coelho AM (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to eight years of age. Monogr Primatol 6:125–129Google Scholar
  14. Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536CrossRefGoogle Scholar
  15. Coley PD, Bryant JP, Chapin III FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899Google Scholar
  16. Conklin-Brittain N, Wrangham R, Hunt K (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. Int J Primatol 19:971–998Google Scholar
  17. Crockett CM, Rudran R (1987) Red howler monkey birth data I: Seasonal Variation. Am J Primatol 13:347–368CrossRefGoogle Scholar
  18. Deschner T, Meistermann M, Hodges K, Boesch C (2003) Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim Behav 66:551–560CrossRefGoogle Scholar
  19. Doran D (1997) Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. Int J Primatol 18:183–206CrossRefGoogle Scholar
  20. Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of Neotropical monkey. Am J Primatol 37:9–24CrossRefGoogle Scholar
  21. Foley WJ, McArthur C (1994) The effects and costs of allelochemicals for mammalian herbivores: an ecological perspective. In: Chivers DJ, Langer P (eds) The digestive system in mammals: food, form and function. Cambridge University Press, Cambridge, pp 370–391Google Scholar
  22. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289CrossRefGoogle Scholar
  23. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press, Cambridge, MassGoogle Scholar
  24. Graham CE (1982) Ovulation time: a factor in ape fertility assessment. Am J Primatol 1[Suppl]:51–55CrossRefGoogle Scholar
  25. Koenig A, Borries C, Chalise MK, Winkler P (1997) Ecology, nutrition and the timing of reproductive events in an Asian primate, the hanuman langur (Presbytis entellus). J Zool 43:215–235Google Scholar
  26. Lee PC, Bowman JE (1995) Influence of ecology and energetics on primate mothers and infants. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and non-human primates. Karger, Basel, pp 47–58Google Scholar
  27. Lindburg DG (1987) Seasonality of reproduction in primates. In: Mitchell G, Erwin J (eds) Comparative primate biology, vol 2B: behavior, cognition, and motivation. Liss, New York, pp 167–218Google Scholar
  28. Lindroth RL, Batzli GO, Avildsen SI (1986) Lespedeza phenolics and Penstemon alkaloids; effects on digestion efficiencies and growth of voles. J Chem Ecol 12:713–728CrossRefGoogle Scholar
  29. Martin P, Bateson P (1986) Measuring behavior: an introductory guide. Cambridge University Press, CambridgeGoogle Scholar
  30. Matsumoto-Oda A, Oda R (1998) Changes in the activity budget of cycling female chimpanzees. Am J Primatol 46:157–166CrossRefPubMedGoogle Scholar
  31. Matsumoto-Oda A, Hosaka K, Huffman MA, Kawanaka K (1998) Factors affecting party size in chimpanzees of the Mahale Mountains. Int J Primatol 19:999–1011CrossRefGoogle Scholar
  32. Melnick DJ, Pearl MC (1987) Cercopithecines in multimale groups: genetic diversity and population structure. In: Smuts BB, Cheney DC, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 121–134Google Scholar
  33. Murah KS, Sukumar R (1993) Leaf flushing phenology and herbivory in a tropical dry deciduous forest, southern India. Oecologia 94:114–119CrossRefGoogle Scholar
  34. Nadel ER (1983) Factors affecting the regulation of body temperature during exercise. J Therm Biol 8:165–169CrossRefGoogle Scholar
  35. Nadler RD, Graham CE, Gosselin RE, Collins DC (1985) Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycle of the chimpanzee (Pan troglodytes). Am J Primatol 9:273–284CrossRefGoogle Scholar
  36. Newton-Fisher N (1999) The diet of chimpanzees in the Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354CrossRefGoogle Scholar
  37. Nishida T (1990) The chimpanzees of the Mahale Mountains: sexual and life-history strategies. University of Tokyo Press, TokyoGoogle Scholar
  38. Patisaul HB, Whitten PL (1998) Dietary phytoestrogens. In: Naz RK (eds) Endocrine disruptors: effects on male and female reproductive systemss. CRC Press, Boca Raton, pp 89–123Google Scholar
  39. Prentice AM, Paul AA, Prentice A, Black AE, Cole TJ, Whitehead RG (1986) Cross-cultural difference in lactational perfomance. In: Hamosh M, Goldman AS (eds) Human lactation 2: maternal and environmental factors. Plenum Press, New York, pp 13–44Google Scholar
  40. Sokal RR, Oden NL (1978) Spatial autocorrelation in biology 1. Methodology. Biol J Linn Soc 10:199–228Google Scholar
  41. Stanford C, Wallis J, Mpongo E, Goodall J (1994) Hunting decisions in wild chimpanzees. Behaviour 131:1–18Google Scholar
  42. Strier KB (1991) Demography and conservation in an endangered primate, Brachyteles arachnoides. Conserv Biol 5:214–218CrossRefGoogle Scholar
  43. Strier KB, Ziegler TE (1994) Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides). Am J Primatol 32:31–40CrossRefGoogle Scholar
  44. Strier KB, Ziegler TE (1997) Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am J Primatol 42:299–310CrossRefPubMedGoogle Scholar
  45. Strier KB, Mendes SL, Santos RR (2001) Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 55:87–100CrossRefPubMedGoogle Scholar
  46. Sun C, Kaplin BA, Kristensen KA, Munyaligoga V, Mvukiyumwami J, Kajondo KK, Moermond TC (1996) Tree phenology in a tropical montane forest in Rwanda. Biotropica 28:668–681Google Scholar
  47. Takahashi H (2002) Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques. Am J Primatol 57:141–153CrossRefPubMedGoogle Scholar
  48. Thompson GE (1977) Physiological effects of cold exposure. Int Rev Physiol 15:29–69PubMedGoogle Scholar
  49. Tutin CEG, Fernandez M (1993) Relationships between minimum temperature and fruit production in some tropical forest trees in Gabon. J Trop Ecol 9:241–248Google Scholar
  50. Wallis J (1992) Socioenvironmental effects on timing of first postpartum cycles in chimpanzees. In: Nishida T, McGrew WC, Marler P, Pickford M, deWaal F (eds) Topics in primatology, human origins. University of Tokyo Press, Tokyo, pp 119–130Google Scholar
  51. Wallis J (1994) Socioenvironmental effects on first full anogenital swellings in adolescent female chimpanzees. In: Roeder JJ, Thierry B, Anderson JR, Herrenschmidt N (eds) Current primatology: social development, learning, and behavior. Université Louis Pasteur, Strasbourg, pp 25–32Google Scholar
  52. Wallis J (1995) Seasonal influence on reproduction in chimpanzees of Gombe National Park. Int J Primatol 16:435–451Google Scholar
  53. Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fert 109:297–307Google Scholar
  54. Wallis J (2002) Seasonality of reproductive behaviour in chimpanzees at Budongo and Gombe. In: Boesch C, Hohmann G, Marchant LF (eds) Chimpanzee behavioural diversity. Cambridge University Press, CambridgeGoogle Scholar
  55. Wallis J, Reynolds V (1999) Seasonal aspects of sociosexual behavior in two chimpanzee populations: A comparison of Gombe (Tanzania) and Budondo (Uganda). Am J Primatol 49:111(abstract)Google Scholar
  56. Whitten PL, Naftolin F (1991) Dietary estrogens: a biologically active background for estrogen action. In: Hochberg R, Naftolin F (eds) The new biology of steroid hormones. Raven Press, New York, pp 155–167Google Scholar
  57. Whitten PL, Lewis C, Russell E, Naftolin F (1995) Potential adverse effects of phytoestrogens. J Nutr 125[Suppl]:s771–776Google Scholar
  58. Whitten PL, Kudo S, Okubo KK (1997) Isoflavonoids. In: D’Mello J (eds) Handbook of plant and fungal toxicants. CRC Press, Boca Raton, pp 117–137Google Scholar
  59. Wrangham R, Conklin-Brittain N, Hunt K (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. I. Antifeedants. Int J Primatol 19:949–970CrossRefGoogle Scholar
  60. Young WC, Yerkes RM (1943) Factors influencing the reproductive cycle in the chimpanzee: the period of adolescent sterility and related problems. Endocrinology 3:121–154Google Scholar
  61. Ziegler T, Hodges K, Winkler P, Heistermann M (2000) Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus). Am J Primatol 51:119–134CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer-Verlag 2005

Authors and Affiliations

  • Dean P. Anderson
    • 1
    Email author
  • Erik. V. Nordheim
    • 2
  • Christophe Boesch
    • 3
  1. 1.Department of ZoologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of Forest Ecology and Management, and Department of StatisticsUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany

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