International Journal of Primatology

, Volume 36, Issue 4, pp 855–870 | Cite as

Seasonality of Conceptions in Captive Rhesus Macaques (Macaca mulatta)

  • Ryan D. P. Dunk
  • Andrew J. Petto
  • Gregory C. Mayer
  • Benjamin C. Campbell


Environmental variables have an effect on patterns of seasonality in conceptions across many animal species. Rhesus macaques (Macaca mulatta) are well documented as seasonal breeders, and it has been proposed that rhesus macaques are “relaxed income breeders.” This means they should respond to changes in photoperiod but that endogenous cues can allow deviations from photoperiod-timed seasonality. Despite this, little is known about what factors cause seasonal reproduction in rhesus macaques. We present the results of a natural experiment on the influence of different housing conditions (featuring different levels of environmental exposure) on the seasonal pattern of reproduction in rhesus macaques. The data come from a captive colony of rhesus macaques, housed in a variety of conditions between 1970 and 1990: indoors with regulated temperature and photoperiod, in enclosures with an open window allowing for photoperiod and temperature variation, or in outdoor enclosures with even more available natural environmental exposure. Conceptions (measured by day-of-year) occurred throughout the year and in a seasonal pattern in all treatment conditions, but the seasonal pattern differed for each treatment. The variability in conception dates was highest for the outdoor groups. These results are consistent with rhesus macaques as “relaxed income breeders.” However, comparison with other macaque species for which similar data are available casts doubt on previous applications of the income and capital breeder model to the macaques.


Capital breeding Conception date Income breeding Reproduction Rhesus seasonality 



The data used in this work were collected as part of a breeding program funded by NIH grant RR00168 to New England Primate Research Center (Harvard Medical School). This work was conducted as part of the requirements leading to completion of a Master of Science degree in the Biological Sciences department at the University of Wisconsin–Milwaukee. Ryan D. P. Dunk thanks the Biological Sciences department for their support preceding and during this study. The authors also thank Reinhold Hutz, Gerry Bergtrom, Karen Bales, Joanna Setchell, and four anonymous reviewers for their helpful and insightful comments, and C. H. Janson for his kind and helpful clarifications regarding his work.


  1. Abdi, H. (2010). Holm’s sequential Bonferroni procedure. In N. Salkind (Ed.), Encyclopedia of research design (pp. 1–8). Thousand Oaks: SAGE.Google Scholar
  2. Altmann, S. A. (1962). A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Sciences, 102(2), 338–435.CrossRefPubMedGoogle Scholar
  3. Andreazzi, C. S., Pires, A. S., Pimenta, C. S., & Fernandez, F. A. S. (2012). Increased female reproduction favours the large-seeded palm Attalea humilis in small Atlantic Forest fragments. Journal of Tropical Ecology, 28(3), 321–325.CrossRefGoogle Scholar
  4. Basset, Y. (2000). Insect herbivores foraging on seedlings in an unlogged rain forest in Guyana: Spatial and temporal considerations. Studies on Neotropical Fauna and Environment, 35(2), 115–129.CrossRefGoogle Scholar
  5. Bauer, D., Goetz, M. N. B., Müller, A., & Schmitt, J. L. (2012). Fenologia de três espécies de Myrsine L. em floresta secundária semidecídua no Sul do Brasil. Revista Árvore, 36(5), 859–868.CrossRefGoogle Scholar
  6. Bernstein, I. S. (1993). Seasonal influences on rhesus monkey (Macaca mulatta) behavior. International Journal of Primatology, 14(3), 383–403.CrossRefGoogle Scholar
  7. Bielert, C., & Vandenbergh, J. G. (1981). Seasonal influences on births and male sex skin coloration in rhesus monkeys (Macaca mulatta) in the Southern Hemisphere. Journal of Reproductive Fertility, 62, 229–233.CrossRefGoogle Scholar
  8. Birkner, F. E. (1970). Photic influences on primate (Macaca mulatta) reproduction. Laboratory Animal Care, 20(2), 181–185.PubMedGoogle Scholar
  9. Both, C., Kaefer, Í. L., Santos, T. G., & Cechin, S. T. Z. (2008). An austral anuran assemblage in the Neotropics: seasonal occurrence correlated with photoperiod. Journal of Natural History, 42(3-4), 205–222.CrossRefGoogle Scholar
  10. Brand, D. J. (1963). Records of mammals bred in the National Zoological Gardens of South Africa during the period 1908 to 1960. Proceedings of the Zoological Society of London, 140, 617–659.CrossRefGoogle Scholar
  11. Brockman, D. K., & van Schaik, C. P. (2005). Seasonality and reproductive function. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 269–305). New York: Cambridge University Press.CrossRefGoogle Scholar
  12. Bronson, F. H., & Heideman, P. D. (1994). Seasonal regulation of reproduction in mammals. In E. Knobil & J. D. Neill (Eds.), The Physiology of Reproduction, 2nd ed., Vols. 1-2, Vol. 2 (pp. 541–583). New York: Raven Press.Google Scholar
  13. Carnegie, S. D., Fedigan, L. M., & Melin, A. D. (2011). Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. International Journal of Primatology, 32(5), 1076–1090.CrossRefGoogle Scholar
  14. Carpenter, C. R. (1942). Sexual behavior of free ranging rhesus monkeys ( Macaca mulatta). I. Specimens, procedures and behavioral characteristics of estrus. Journal of Comparative Psychology, 33(1), 113–142.CrossRefGoogle Scholar
  15. Coimbra-Filho, A. F., & de Maia, A. A. (1977). As fases do processo reproductivo de Macaca mulatta Zimmerman, 1780, na ilha do pinheiro, Rio de Janeiro, Brasil (Cercopithecidae, Primates). Revista Brasileira de Biologia, 37, 71–78.PubMedGoogle Scholar
  16. Conaway, C. H., & Koford, C. B. (1964). Estrous cycles and mating behavior in a free-ranging band of rhesus monkeys. Journal of Mammalogy, 45(4), 577–588.CrossRefGoogle Scholar
  17. Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001). Photoperiodic control of seasonality in birds. Journal of Biological Rhythms, 16(4), 365–380.CrossRefPubMedGoogle Scholar
  18. Diniz, P., Ramos, D. M., & Chemin, N. (2013). Breeding biology of coal-crested finches. The Wilson Journal of Ornithology, 125(3), 592–599.CrossRefGoogle Scholar
  19. Drickamer, L. C. (1974). Social rank, observability, and sexual behaviour of rhesus monkeys (Macaca mulatta). Journal of Reproduction and Fertility, 37(1), 117–120.CrossRefPubMedGoogle Scholar
  20. Eckstein, P., & Kelly, W. A. (1966). A survey of the breeding performance of rhesus monkeys in the laboratory. Symposia of the Zoological Society of London, 17, 91–111.Google Scholar
  21. Fisher, N. I. (1993). Statistical analysis of circular data. New York: Cambridge University Press.CrossRefGoogle Scholar
  22. Ghosh, D., & Sengupta, J. (1992). Patterns of ovulation, conception and pre-implantation embryo development during the breeding season in rhesus monkeys kept under semi-natural conditions. Acta Endocrinologica, 127(2), 168–173.PubMedGoogle Scholar
  23. Girard-Buttoz, C., Heistermann, M., Krummel, S., & Engelhardt, A. (2009). Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiology & Behavior, 98(1-2), 168–175.CrossRefGoogle Scholar
  24. Girard-Buttoz, C., Heistermann, M., Rahmi, E., Agil, M., Ahmad Fauzan, P., & Engelhardt, A. (2014). Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): physiological stress and aggression. Hormones and Behavior, 66(4), 637–648.CrossRefPubMedGoogle Scholar
  25. Gomes, D. F., & Bicca-Marques, J. C. (2003). An inversion in the timing of reproduction of captive Macaca mulatta in the southern hemisphere. Laboratory Primate Newsletter, 42(4), 6.Google Scholar
  26. González-Martínez, J. (2004). The introduced free-ranging rhesus and patas monkey populations of southwestern Puerto Rico. Puerto Rico Health Sciences Journal, 23(1), 39–46.PubMedGoogle Scholar
  27. Hartman, C. G. (1931). The breeding season in monkeys, with special reference to Pithecus (Macacus) rhesus. Journal of Mammalogy, 12(2), 129–142.CrossRefGoogle Scholar
  28. Heape, W. (1897). The menstruation and ovulation of Macacus rhesus, with observations on the changes undergone by the discharged follicle. Part II. Philosophical Transactions of the Royal Society of London, 188, 135–166.CrossRefGoogle Scholar
  29. Herndon, J. G. (1983). Seasonal breeding in rhesus monkeys: influence of the behavioral environment. American Journal of Primatology, 5(3), 197–204.CrossRefGoogle Scholar
  30. Herndon, J. G., Ruiz de Elvira, M. C., Turner, J. J., & Collins, D. C. (1985). Resumption of seasonal breeding patterns in male and female rhesus monkeys transferred from an indoor to an outdoor environment. Biology of Reproduction, 32(4), 733–744.CrossRefPubMedGoogle Scholar
  31. Hingston, R. W. G. (1920). A naturalist in Himalaya. London: H. F. & G. Witherby.CrossRefGoogle Scholar
  32. Hoffman, C. L., & Maestripieri, D. (2012). Costs of reproduction among rhesus macaque females on Cayo Santiago. In Q. Wang (Ed.), Bones, genetics, and behavior of rhesus macaques (pp. 209–226). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  33. Hoffman, C. L., Ruiz-Lambides, A. V., Davila, E., Maldonado, E., Gerald, M. S., & Maestripieri, D. (2008). Sex differences in survival costs of reproduction in a promiscuous primate. Behavioral Ecology and Sociobiology, 62(11), 1711–1718.PubMedCentralCrossRefPubMedGoogle Scholar
  34. Huang, Z.-P., Cui, L.-W., Scott, M. B., Wang, S.-J., & Xiao, W. (2012). Seasonality of reproduction of wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan, China. Primates, 53(3), 237–245.CrossRefPubMedGoogle Scholar
  35. Hutz, R. J., Dierschke, D. J., & Wolf, R. C. (1985). Seasonal effects on ovarian folliculogenesis in rhesus monkeys. Biology of Reproduction, 33(3), 653–659.CrossRefPubMedGoogle Scholar
  36. Janson, C., & Verdolin, J. (2005). Seasonality of primate births in relation to climate. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 307–350). New York: Cambridge University Press.CrossRefGoogle Scholar
  37. Jarvis, C., & Morris, D. (Eds.). (1962). The breeding seasons of mammals in captivity. International Zoo Yearbook, 3, 292–301.Google Scholar
  38. Johnson, R. L., & Kapsalis, E. (1995). Ageing, infecundity and reproductive senescence in free-ranging female rhesus monkeys. Journal of Reproduction and Fertility, 105(2), 271–278.CrossRefPubMedGoogle Scholar
  39. Johnson, L. D., Petto, A. J., Boy, D. S., Sehgal, P. K., & Beland, M. E. (1986). The effect of perinatal and juvenile mortality on colony-born production at the New England Primate Research Center. In K. Benirschke (Ed.), Primates: The road to self-sustaining populations (pp. 771–779). New York: Springer-Verlag.CrossRefGoogle Scholar
  40. Johnson, L. D., Biggers, J. D., Sehgal, P., Petto, A. J., & Avis, J. (1989). The effect of heterologous gonadotropins on the fecundity of rhesus monkeys. Journal of In Vitro Fertilization and Embryo Transfer, 6(6), 328–334.CrossRefPubMedGoogle Scholar
  41. Kaumanns, W., Singh, M., & Schwibbe, M. (2013). Environmental change and housing conditions result in disappearance and return of reproductive seasonality in rhesus macaques (Macaca mulatta). Current Science, 105(4), 517–521.Google Scholar
  42. Koford, C. B. (1965). Population dynamics of rhesus monkeys on Cayo Santiago. In I. DeVore (Ed.), Primate behavior: Field studies of monkeys and apes (pp. 160–174). New York: Holt, Rinehart, and Winston.Google Scholar
  43. Koford, C. B. (1966). Population changes in rhesus monkeys: Cayo Santiago, 1960–1964. Tulane Studies in Zoology, 13(1), 1–7.Google Scholar
  44. Kovach, W. L. (2011). Oriana–circular statistics for Windows. Pentraeth: Kovach Computing Services.Google Scholar
  45. Lancaster, J. B., & Lee, R. B. (1965). The annual reproductive cycle in monkeys and apes. In I. DeVore (Ed.), Primate behavior: Field studies of monkeys and apes (pp. 486–513). New York: Holt, Rinehart, and Winston.Google Scholar
  46. Lehman, S. M., Taylor, L. L., & Easley, S. P. (1994). Climate and reproductive seasonality in two free-ranging island populations of rhesus macaques (Macaca mulatta). International Journal of Primatology, 15(1), 115–128.CrossRefGoogle Scholar
  47. Lindburg, D. G. (1971). The rhesus monkey in north India: An ecological and behavioral study. In L. A. Rosenblum (Ed.), Primate behavior: Developments in field and laboratory research (Vol. 2, pp. 1–106). New York: Academic Press.CrossRefGoogle Scholar
  48. Lindburg, D. G. (1987). Seasonality of reproduction in primates. In G. Mitchell & J. Erwin (Eds.), Comparative primate biology, vol. 2B: Behavior, cognition, and motivation (pp. 167–218). New York: Alan R. Liss.Google Scholar
  49. Malpaux, B. (2006). Seasonal regulation of reproduction in mammals. In J. D. Neill (Ed.), Knobil and Neill’s physiology of reproduction, vols. 1-2, vol. 2 (3rd ed., pp. 2231–2281). St. Louis: Elsevier.CrossRefGoogle Scholar
  50. Mello, M. A. R., Kalko, E. K. V., & Silva, W. R. (2009). Ambient temperature is more important than food availability in explaining reproductive timing of the bat Sturnira lilium (Mammalia: Chiroptera) in a montane Atlantic Forest. Canadian Journal of Zoology, 87, 239–245.CrossRefGoogle Scholar
  51. Novak, M. A., & Petto, A. J. (Eds.). (1991). Through the looking glass: Issues of psychological well-being in captive nonhuman primates, Vol. xiii. Washington, DC: American Psychological Association.Google Scholar
  52. Ponce de Lugo, C. G. (1964). Length of menstrual cycles in relation to time of successful mating in Macaca mulatta. Biologia Neonatorum, 6(1–2), 104–111.CrossRefGoogle Scholar
  53. Prakash, I. (1958). The breeding season of the rhesus monkey Macaca mulatta (Zimmermann) in Rajasthan. Journal of the Bombay Natural History Society, 55, 154.Google Scholar
  54. Prakash, I. (1962). Group organization, sexual behaviour and breeding season of certain Indian monkeys. Japanese Journal of Ecology, 12(3), 83–86.Google Scholar
  55. Rawlins, R. G., & Kessler, M. J. (1985). Climate and seasonal reproduction in the Cayo Santiago macaques. American Journal of Primatology, 9(2), 87–99.CrossRefGoogle Scholar
  56. Riesen, J. W., Meyer, R. K., & Wolf, R. C. (1971). The effect of season on occurrence of ovulation in the rhesus monkey. Biology of Reproduction, 5(2), 111–114.PubMedGoogle Scholar
  57. Rowell, T. E. (1963). Behaviour and female reproductive cycles of rhesus macaques. Journal of Reproduction and Fertility, 6(2), 193–203.CrossRefPubMedGoogle Scholar
  58. Ruiz de Elvira, M. C., Herndon, J. G., & Collins, D. C. (1983). Effect of estradiol-treated females on all-female groups of rhesus monkeys during the transition between the nonbreeding and breeding seasons. Folia Primatologica, 41(3–4), 191–203.CrossRefGoogle Scholar
  59. Savini, T., Boesch, C., & Reichard, U. H. (2008). Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand. American Journal of Physical Anthropology, 135(1), 1–12.CrossRefPubMedGoogle Scholar
  60. Sokal, R. R., & Rohlf, F. J. (2012). Biometry (4th ed.). New York: W.H. Freeman.Google Scholar
  61. Southwick, C. H., Beg, M. A., & Siddiqi, M. R. (1961). A population survey of rhesus monkeys in northern India: II. Transportation routes and forest areas. Ecology, 42(4), 698–710.CrossRefGoogle Scholar
  62. Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3(3), 259–268.CrossRefGoogle Scholar
  63. Tian, J.-D., Wang, Z.-L., Lu, J.-Q., Wang, B.-S., & Chen, J.-R. (2013). Reproductive parameters of female Macaca mulatta tcheliensis in the temperate forest of Mount Taihangshan, Jiyuan, China. American Journal of Primatology, 75(6), 605–612.CrossRefPubMedGoogle Scholar
  64. Toloczko McIntyre, D., & Petto, A. J. (1993). Effect of group size on behavior of group-housed female rhesus macaques (Macaca mulatta). Laboratory Primate Newsletter, 32(3), 1–4.Google Scholar
  65. Valerio, D. A., Miller, R. L., Innes, J. R. M., Courtney, K. D., Pallotta, A. J., & Guttmacher, R. M. (1969a). Macaca mulatta: Management of a laboratory breeding colony. New York: Academic Press.Google Scholar
  66. Valerio, D. A., Pallotta, A. J., & Courtney, K. D. (1969b). Experiences in large-scale breeding of simians for medical experimentation. Annals of the New York Academy of Sciences, 162(1), 282–296.CrossRefPubMedGoogle Scholar
  67. Van Horn, R. N. (1980). Seasonal reproductive patterns in primates. In R. J. Reiter & B. K. Follett (Eds.), Seasonal reproduction in higher vertebrates (Vol. 5, pp. 181–221). Basel: S. Karger.Google Scholar
  68. Van Schaik, C. P., & Brockman, D. K. (2005). Seasonality in primate ecology, reproduction, and life history: An overview. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 3–20). New York: Cambridge University Press.CrossRefGoogle Scholar
  69. Van Wagenen, G., Catchpole, H. R., Negri, J., & Butzko, D. (1965). Growth of the fetus and placenta of the monkey (Macaca mulatta). American Journal of Physical Anthropology, 23(1), 23–33.CrossRefGoogle Scholar
  70. Vandenbergh, J. G. (1973). Environmental influences on breeding in rhesus monkeys. In C. H. Phoenix (Ed.), Primate reproductive behavior, vol. 2 (pp. 1–19). Basel: S. Karger.Google Scholar
  71. Vandenbergh, J. G., & Vessey, S. H. (1968). Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. Journal of Reproduction and Fertility, 15(1), 71–79.CrossRefPubMedGoogle Scholar
  72. Wang, J., Feng, M., & Li, Y. (1996). The study on population ecology of Macaca mulatta at Longhushan Nature Reserve, Guangxi. Acta Theriologica Sinica, 16, 264–271.Google Scholar
  73. Zar, J. H. (1999). Biostatistical analysis (4th ed.). Upper Saddle River: Prentice Hall.Google Scholar
  74. Zuckerman, S. (1931). The menstrual cycle of the primates. Part III: the alleged breeding-season of primates, with special reference to the Chacma Baboon (Papio porcarius). Proceedings of the Zoological Society of London, 101, 325–343.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ryan D. P. Dunk
    • 1
    • 4
  • Andrew J. Petto
    • 1
  • Gregory C. Mayer
    • 2
  • Benjamin C. Campbell
    • 3
  1. 1.Department of Biological SciencesUniversity of Wisconsin–MilwaukeeMilwaukeeUSA
  2. 2.Department of Biological SciencesUniversity of Wisconsin–ParksideKenoshaUSA
  3. 3.Department of AnthropologyUniversity of Wisconsin–MilwaukeeMilwaukeeUSA
  4. 4.Department of BiologySyracuse UniversitySyracuseUSA

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