Skip to main content
Log in

Environmental factors influencing the seasonality of estrus in chimpanzees

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    PubMed  Google Scholar 

  • Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge

    Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • Anderson DP, Nordheim EV, Bi ZBG, Boesch C (2005) Deviations in tropical tree phenology patterns caused by climatic variables. Biotropica (in press).

  • Bercovitch FB (1987) Female weight and reproductive condition in a population of olive baboons(Papio cynocephalus anubis). Am J Primatol 12:189–195

    Article  Google Scholar 

  • Boesch C, Boesch H (1983) Optimization of nut-cracking with natural hammers by wild chimpanzees. Behaviour 83:265–286

    Google Scholar 

  • Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï Forest: behavioural ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago

    Google Scholar 

  • 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 284–322

    Google Scholar 

  • Chapman CA, Chapman LJ, Wrangham RW, Hunt K, Gebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531

    Google Scholar 

  • Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70

    Article  Google Scholar 

  • 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 15:189–211

    Article  Google Scholar 

  • Coelho AM (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to eight years of age. Monogr Primatol 6:125–129

    Google Scholar 

  • Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin III FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Google Scholar 

  • 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 19:971–998

    Google Scholar 

  • Crockett CM, Rudran R (1987) Red howler monkey birth data I: Seasonal Variation. Am J Primatol 13:347–368

    Article  Google Scholar 

  • 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 66:551–560

    Article  Google Scholar 

  • Doran D (1997) Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. Int J Primatol 18:183–206

    Article  Google Scholar 

  • Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of Neotropical monkey. Am J Primatol 37:9–24

    Article  Google Scholar 

  • 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 370–391

    Google Scholar 

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289

    Article  Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press, Cambridge, Mass

    Google Scholar 

  • Graham CE (1982) Ovulation time: a factor in ape fertility assessment. Am J Primatol 1[Suppl]:51–55

    Article  Google Scholar 

  • 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 43:215–235

    Google Scholar 

  • 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 47–58

    Google Scholar 

  • 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 167–218

  • Lindroth RL, Batzli GO, Avildsen SI (1986) Lespedeza phenolics and Penstemon alkaloids; effects on digestion efficiencies and growth of voles. J Chem Ecol 12:713–728

    Article  Google Scholar 

  • Martin P, Bateson P (1986) Measuring behavior: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Matsumoto-Oda A, Oda R (1998) Changes in the activity budget of cycling female chimpanzees. Am J Primatol 46:157–166

    Article  PubMed  Google Scholar 

  • Matsumoto-Oda A, Hosaka K, Huffman MA, Kawanaka K (1998) Factors affecting party size in chimpanzees of the Mahale Mountains. Int J Primatol 19:999–1011

    Article  Google Scholar 

  • 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 121–134

    Google Scholar 

  • Murah KS, Sukumar R (1993) Leaf flushing phenology and herbivory in a tropical dry deciduous forest, southern India. Oecologia 94:114–119

    Article  Google Scholar 

  • Nadel ER (1983) Factors affecting the regulation of body temperature during exercise. J Therm Biol 8:165–169

    Article  Google Scholar 

  • 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 9:273–284

    Article  Google Scholar 

  • Newton-Fisher N (1999) The diet of chimpanzees in the Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354

    Article  Google Scholar 

  • Nishida T (1990) The chimpanzees of the Mahale Mountains: sexual and life-history strategies. University of Tokyo Press, Tokyo

    Google Scholar 

  • 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 89–123

    Google Scholar 

  • 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 13–44

    Google Scholar 

  • Sokal RR, Oden NL (1978) Spatial autocorrelation in biology 1. Methodology. Biol J Linn Soc 10:199–228

    Google Scholar 

  • Stanford C, Wallis J, Mpongo E, Goodall J (1994) Hunting decisions in wild chimpanzees. Behaviour 131:1–18

    Google Scholar 

  • Strier KB (1991) Demography and conservation in an endangered primate, Brachyteles arachnoides. Conserv Biol 5:214–218

    Article  Google Scholar 

  • Strier KB, Ziegler TE (1994) Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides). Am J Primatol 32:31–40

    Article  Google Scholar 

  • Strier KB, Ziegler TE (1997) Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am J Primatol 42:299–310

    Article  PubMed  Google Scholar 

  • 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 55:87–100

    Article  PubMed  Google Scholar 

  • 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 28:668–681

    Google Scholar 

  • Takahashi H (2002) Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques. Am J Primatol 57:141–153

    Article  PubMed  Google Scholar 

  • Thompson GE (1977) Physiological effects of cold exposure. Int Rev Physiol 15:29–69

    PubMed  Google Scholar 

  • Tutin CEG, Fernandez M (1993) Relationships between minimum temperature and fruit production in some tropical forest trees in Gabon. J Trop Ecol 9:241–248

    Google Scholar 

  • 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 119–130

    Google Scholar 

  • 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 25–32

    Google Scholar 

  • Wallis J (1995) Seasonal influence on reproduction in chimpanzees of Gombe National Park. Int J Primatol 16:435–451

    Google Scholar 

  • Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fert 109:297–307

    Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • 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 

  • 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 155–167

    Google Scholar 

  • Whitten PL, Lewis C, Russell E, Naftolin F (1995) Potential adverse effects of phytoestrogens. J Nutr 125[Suppl]:s771–776

    Google Scholar 

  • Whitten PL, Kudo S, Okubo KK (1997) Isoflavonoids. In: D’Mello J (eds) Handbook of plant and fungal toxicants. CRC Press, Boca Raton, pp 117–137

    Google Scholar 

  • 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 19:949–970

    Article  Google Scholar 

  • Young WC, Yerkes RM (1943) Factors influencing the reproductive cycle in the chimpanzee: the period of adolescent sterility and related problems. Endocrinology 3:121–154

    Google Scholar 

  • Ziegler T, Hodges K, Winkler P, Heistermann M (2000) Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus). Am J Primatol 51:119–134

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dean P. Anderson.

About this article

Cite this article

Anderson, D.P., Nordheim, E.V. & Boesch, C. Environmental factors influencing the seasonality of estrus in chimpanzees. Primates 47, 43–50 (2006). https://doi.org/10.1007/s10329-005-0143-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-005-0143-y

Keywords

Navigation