International Journal of Primatology

, Volume 31, Issue 5, pp 715–735 | Cite as

It’s All in the Timing: Birth Seasonality and Infant Survival in Eulemur rubriventer

Article

Abstract

Highly seasonal breeding has been considered one of the keys to understanding Malagasy primate socioecology. Strict seasonal breeding may be particularly critical for Malagasy primates because they live in such energetically challenging seasonal environments. Lemurs also live in highly unpredictable environments, and there is growing evidence that reproductive timing may be mediated by additional factors, suggesting that more relaxed breeding seasonality is adaptive in some cases. I tested the adaptive breadth of the birth peak in Eulemur rubriventer, which breed in several different months. I describe reproduction in the species by determining the timing and extent of the birth season (period in which all births occur) and birth peak (period in which the majority of births occur); test whether relaxed reproductive seasonality might increase reproductive success by comparing infant mortality within and outside the birth peak; and model the extent to which fruit availability has an influence on the timing of reproduction. I collected birth data on 5 groups in 2003–2005, which I combined with demographic data that D. Overdorff collected from 5 focal groups and additional censused groups between 1988 and 1996. Thirty births occurred in 8 different months. Births were significantly seasonal, with a unimodal birth peak in late August/September/October, and a mean birth date of October 11. Twenty-three births (76.7%) occurred within 54 d (14.79%) of the year. No births occurred May–July, indicating that conceptions did not occur from late December through late February, and cycling (estimated using gestation length) did not occur until ca. 101 d after the austral summer solstice (December 21). Of 22 infants followed regularly, 18 were born in the birth peak, of which 2 died (11%). All 4 infants born out of season died. Based on fruit availability, I calculated a Theoretical Overlap index (T), which indicated a 3-mo window with optimal food conditions for reproduction. This window corresponded to the timing and breadth of the birth peak in Eulemur rubriventer. These results indicate that a breeding season >3 mo within a given year is not adaptive in the species, likely due in large part to the availability of fruit during key reproductive stages, particularly before breeding.

Keywords

Eulemur rubriventer infant mortality relaxed breeding reproductive strategies seasonal reproduction 

Supplementary material

10764_2010_9423_MOESM1_ESM.pdf (69 kb)
Supplement Table 1.Monthly Fecundity and Mortality in Eulemur rubriventer (PDF 69.2 KB)
10764_2010_9423_MOESM2_ESM.pdf (70 kb)
Supplement Table 2.Theoretical maximum (T) of fruit availability and reproduction (PDF 69.8 KB)

References

  1. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–267.PubMedCrossRefGoogle Scholar
  2. Altmann, J. (1980). Baboon mothers and infants. Cambridge: Harvard University Press.Google Scholar
  3. Balko, E. A., & Underwood, H. B. (2005). Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. American Journal of Primatology, 66, 45–70.PubMedCrossRefGoogle Scholar
  4. Batschelet, E. (1981). Circular statistics in biology. London: Academic Press.Google Scholar
  5. Bogart, M. H., Kumamoto, A. T., & Lasley, B. L. (1977). A comparison of the reproductive cycle of three species of Lemur. Folia Primatologica, 28, 134–143.CrossRefGoogle Scholar
  6. Bollen, A., & Donati, G. (2005). Phenology of the littoral forest of Sainte Luce, southeastern Madagascar. Biotropica, 37, 32–43.CrossRefGoogle Scholar
  7. Borries, C., Koenig, A., & Winkler, P. (2001). Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behavioral Ecology and Sociobiology, 50, 391–402.CrossRefGoogle Scholar
  8. Boskoff, K. J. (1978). The oestrous cycle of the brown lemur, Lemur fulvus. Journal of Reproduction and Fertility, 54, 313–318.PubMedCrossRefGoogle Scholar
  9. 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
  10. Brockman, D. K., & Whitten, P. L. (1996). Reproduction in free-ranging Propithecus verreauxi: estrus and the relationship between multiple partner mating and fertilization. American Journal of Physical Anthropology, 100, 57–69.PubMedCrossRefGoogle Scholar
  11. Brockman, D. K., Whitten, P. L., Russell, E., Richard, A. F., & Izard, M. K. (1995). Application of fecal steroid techniques to the reproductive endocrinology of female Verreaux's sifaka (Propithecus verreauxi). American Journal of Primatology, 36, 313–325.CrossRefGoogle Scholar
  12. Bronson, F. H., & Heideman, P. D. (1994). Seasonal regulation of reproduction in mammals. In E. Knobil & J. D. Neil (Eds.), The physiology of reproduction (2nd ed.). New York: Raven Press.Google Scholar
  13. Budnitz, N., & Dainis, K. (1975). Lemur catta: Ecology and behavior. In I. Tattersall & R. W. Sussman (Eds.), Lemur biology (pp. 219–236). New York: Plenum Press.Google Scholar
  14. Butynski, T. M. (1988). Guenon birth seasons and correlates with rainfall and food. In A. Gautier-Hion, F. Bourliere, & J.-P. Gautier (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 284–322). Cambridge: Cambridge University Press.Google Scholar
  15. Clutton-Brock, T., Albon, S., & Guiness, F. (1989). Fitness costs of gestation and lactation in wild mammals. Nature, 337, 260–262.PubMedCrossRefGoogle Scholar
  16. Curtis, D. J., Zaramody, A., Green, D. I., & Pickard, A. R. (2000). Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Reproduction, Fertility, and Development, 12, 21–29.PubMedCrossRefGoogle Scholar
  17. Daan, S., & Tinbergen, J. M. (1997). Adaptation to life histories. In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (pp. 311–333). Oxford: Blackwell Science.Google Scholar
  18. Dewar, R. E., & Richard, A. F. (2007). Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the United States of America, 104, 13723–13727.PubMedCrossRefGoogle Scholar
  19. DiBitetti, M. S., & Janson, C. H. (2000). When will the stork arrive? Patterns of birth seasonality in Neotropical primates. American Journal of Primatology, 50, 109–130.CrossRefGoogle Scholar
  20. Drent, R. H., & Daan, S. (1980). The prudent parent: energetic adjustments in avian breeding. Ardea, 68, 225–252.Google Scholar
  21. Durham, D. L. (2002). Variation in birth rates and birth seasons among Eulemur rubriventer living in a selectively logged region of Ranomafana National Park, Madagascar. American Journal of Primatology, 57, 37.Google Scholar
  22. Durham, D. L. (2003). Variation in responses to forest disturbance and the risk of local extinction: A comparative study of wild eulemurs at Ranomafana National Park, Madagascar. Dissertation, Davis: University of California, Davis.Google Scholar
  23. Eberle, M., & Kappeler, P. M. (2004). Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behavioral Ecology and Sociobiology, 27, 77–90.CrossRefGoogle Scholar
  24. Evans, C. S., & Goy, R. W. (1968). Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). Journal of Zoology, 156, 181–190.CrossRefGoogle Scholar
  25. Foerg, R. (1982). Reproductive behavior in Varecia variegata. Folia Primatologica, 38, 108–121.CrossRefGoogle Scholar
  26. Freed, B. Z. (1996). Co-occurrence among crowned lemurs (Lemur coronatus) and Sanford’s lemurs (Lemur fulvus sanfordi) of Madagascar. Dissertation, St. Louis: Washington University.Google Scholar
  27. Ganzhorn, J. U., Fietz, J., Rakotovao, E., Schwab, D., & Zinner, D. (1999a). Lemurs and the regeneration of dry deciduous forest in Madagascar. Conservation Biology, 13, 794–804.CrossRefGoogle Scholar
  28. Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, H. J. (1999b). Primate communities: Madagascar. In J. G. Fleagle, C. H. Janson, & K. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  29. Glander, K. E., Wright, P. C., Daniel, P. S., & Merenlender, A. M. (1992). Morphometrics and testicle size of rain forest lemur species from southeastern Madagascar. Journal of Human Evolution, 22, 1–17.CrossRefGoogle Scholar
  30. Gould, L., Sussman, R. W., & Sauther, M. L. (1999). Natural disasters and primate populations: the effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in southwestern Madagascar. International Journal of Primatology, 20, 69–84.CrossRefGoogle Scholar
  31. Grassi, C. (2001). The behavioral ecology of Hapalemur griseus griseus: Influences of microhabitat and population density on this small-bodied prosimian folivore. Dissertation, University of Texas–Austin.Google Scholar
  32. Harley, D. (1988). Patterns of reproduction and mortality in two captive colonies of Hanuman langur monkeys (Presbytis entellus). American Journal of Primatology, 15, 103–114.CrossRefGoogle Scholar
  33. Hemingway, C. A. (1995). Feeding and reproductive strategies of Propithecus diadema edwardsi Dissertation. Durham: Duke University.Google Scholar
  34. Hemingway, C. A. (1996). Morphology and phenology of seeds and whole fruit eaten by Milne-Edwards’ sifaka in Ranomafana National Park, Madagascar. International Journal of Primatology, 17, 637–657.CrossRefGoogle Scholar
  35. Hemingway, C. A. (1998). Selectivity and variability in the diet of Milne-Edwards' sifakas (Propithecus diadema edwardsi): Implications for folivory and seed-eating. International Journal of Primatology, 19, 355–377.CrossRefGoogle 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. Johnson, S. E., & Overdorff, D. J. (1999). Census of brown lemurs (Eulemur fulvus spp.) in southeastern Madagascar: methods-testing and conservation implications. American Journal of Primatology, 47, 51–60.PubMedCrossRefGoogle Scholar
  38. Jolly, A. (1966). Lemur behavior: A Madagascar field study. Chicago: University of Chicago Press.Google Scholar
  39. Jolly, A. (1967). Breeding synchrony in wild Lemur catta. Social communication among primates (pp. 3–14). Chicago: University of Chicago Press.Google Scholar
  40. Jolly, A. (1984). The puzzle of female feeding priority. In M. Small (Ed.), Female primates: Studies by women primatologists (pp. 197–215). New York: Alan R. Liss.Google Scholar
  41. Jolly, A., Dobson, A., Rasamimanana, H. M., Walker, J., O'Connor, S., Solberg, M., et al. (2002). Demography of Lemur catta at Berenty Reserve, Madagascar: effects of troop size, habitat and rainfall. International Journal of Primatology, 23, 327–353.CrossRefGoogle Scholar
  42. Jury, M. R. (2003). The climate of Madagascar. In S. M. Goodman & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 75–87). Chicago: University of Chicago Press.Google Scholar
  43. Kappeler, P. M. (1987). Reproduction in the crowned lemur in captivity. American Journal of Primatology, 12, 497–503.CrossRefGoogle Scholar
  44. King, S. J., Arrigo-Nelson, S. J., Pochron, S. T., Semprebon, G. M., Godfrey, L. R., Wright, P. C., et al. (2005). Dental senescence in a long-lived primate links infant survival to rainfall. Proceedings of the National Academy of Sciences of the United States of America, 102, 16579–16583.PubMedCrossRefGoogle Scholar
  45. Koenig, A., Borries, C., Chalise, M. K., & Winkler, P. (1997). Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur. Journal of Zoology, London, 243, 215–235.CrossRefGoogle Scholar
  46. Kowalewski, M., & Zunino, G. E. (2004). Birth seasonality in Alouatta caraya in Northern Argentina. International Journal of Primatology, 25, 383–400.CrossRefGoogle Scholar
  47. Koyama, N., Nakamichi, M., Oda, R., Miyamoto, N., & Takahata, Y. (2001). A ten-year summary of reproductive parameters for ring-tailed lemurs at Berenty, Madagascar. Primates, 42, 1–14.CrossRefGoogle Scholar
  48. Lahann, P., Schmid, J., & Ganzhorn, J. U. (2006). Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule? International Journal of Primatology, 27, 983–999.CrossRefGoogle Scholar
  49. 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
  50. Lee, P. C. (1996). The meanings of weaning: growth, lactation, and life history. Evolutionary Anthropology, 5, 87–98.CrossRefGoogle Scholar
  51. Lewis, R. J., & Kappeler, P. M. (2005). Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. American Journal of Primatology, 67, 347–364.PubMedCrossRefGoogle Scholar
  52. Lichtenbelt, W. D. V. (1993). Optimal foraging of a herbivorous lizard, the Green Iguana in a seasonal environment. Oecologia, 95, 246–256.CrossRefGoogle Scholar
  53. Martin, R. D. (1972). Review lecture: adaptive radiation and behaviour of the Malagasy lemurs. Philosophical Transactions of the Royal Society B: Biological Sciences, 264, 295–352.CrossRefGoogle Scholar
  54. Merenlender, A. M. (1993). The effects of sociality on the demography and genetic structure of Lemur fulvus rufus (polygamous) and Lemur rubriventer (Monogamous) and the conservation implications. Dissertation: University of Rochester, Rochester, NY.Google Scholar
  55. Mittermeier, R. A., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., et al. (2006). Lemurs of Madagascar (2nd ed.). Washington, DC: Conservation International.Google Scholar
  56. Morelli, T. L., King, S. J., Pochron, S. T., & Wright, P. C. (2009). The rules of disengagement: takeovers, infanticide, and dispersal in a rainforest lemur, Propithecus edwardsi. Behaviour, 146, 499–523.CrossRefGoogle Scholar
  57. Morland, H. S. (1991). Preliminary report on the social organization of ruffed lemurs (Varecia variegata variegata) in a northeast Madagascar rainforest. Folia Primatologica, 56, 157–161.CrossRefGoogle Scholar
  58. Mutschler, T. (1999). Folivory in a small-bodied lemur: The nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In B. Rakotosamimanana, H. Rasamimanana, J. U. Ganzhorn, & S. M. Goodman (Eds.), New directions in lemur studies (pp. 221–239). New York: Plenum Press.Google Scholar
  59. Mutschler, T. C., Nievergelt, C. M., & Feistner, A. T. C. (2000). Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). American Journal of Primatology, 50, 9–24.PubMedCrossRefGoogle Scholar
  60. Negus, N. C., & Berger, P. J. (1972). Environmental factors and reproductive processes in mammalian populations. In J. T. Velardo & B. A. Kasprow (Eds.), Biology of reproduction: Basic and clinical studies (pp. 89–98). New Orleans: Pan American Association of Anatomy.Google Scholar
  61. Overdorff, D. J. (1991). Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufus and Eulemur rubriventer in Madagascar. Dissertation: Duke University, Durham.Google Scholar
  62. Overdorff, D. J. (1993a). Similarities, differences, and seasonal patterns in diets of Eulemur rubriventer and Eulemur fulvus rufus in Ranomafana National Park, Madagascar. International Journal of Primatology, 14, 721–753.CrossRefGoogle Scholar
  63. Overdorff, D. J. (1993b). Ecological and reproductive correlates to range use in red-bellied (Eulemur rubriventer) and rufous (Eulemur fulvus rufus) lemurs. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 167–178). New York: Plenum Press.Google Scholar
  64. Overdorff, D. J. (1996a). Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar. American Journal of Primatology, 40, 327–342.CrossRefGoogle Scholar
  65. Overdorff, D. J. (1996b). Ecological correlates to social structure in two lemur species in Madagascar. American Journal of Physical Anthropology, 100, 487–506.CrossRefGoogle Scholar
  66. Overdorff, D. J., & Strait, S. G. (1998). Seed handling by three prosimian primates in southeastern Madagascar: implications for seed dispersal. American Journal of Primatology, 45, 69–82.PubMedCrossRefGoogle Scholar
  67. Overdorff, D. J., & Tecot, S. R. (2006). Social pair-bonding and resource defense in wild red-bellied lemurs (Eulemur rubriventer). In L. Gould & M. L. Sauther (Eds.), Lemurs: Ecology and adaptation (pp. 235–245). New York: Springer.Google Scholar
  68. Overdorff, D. J., Merenlender, A. M., Talata, P., Telo, A., & Forward, Z. A. (1999). Life history of Eulemur fulvus rufus from 1988–1998 in SE Madagascar. American Journal of Physical Anthropology, 108, 295–310.PubMedCrossRefGoogle Scholar
  69. Pereira, M. E. (1991). Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Physiology & Behavior, 49, 47–52.CrossRefGoogle Scholar
  70. Pereira, M. (1993). Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 205–221). New York: Plenum Press.Google Scholar
  71. Pereira, M. E., Strohecker, R. A., Cavigelli, S. A., Hughes, C. L., & Pearson, D. D. (1999). Metabolic strategy and social behavior in Lemuridae. In B. Rakotosamimanana, H. Rasamimanana, J. U. Ganzhorn, & S. M. Goodman (Eds.), New directions in lemur studies (pp. 93–118). New York: Kluwer Academic.Google Scholar
  72. Perry, J. M., Izard, M. K., & Fail, P. A. (1992). Observations on reproduction, hormones, copulatory behavior, and neonatal mortality in captive Lemur mongoz. Zoo Biology, 11, 81–97.CrossRefGoogle Scholar
  73. Petter, J.-J. (1977). The aye-aye. In Prince Rainier III & G. H. Bourne (Eds.), Primate conservation (pp. 37–57). New York: Academic Press.Google Scholar
  74. Petter, J.-J., & Peyriéras, A. (1970). Nouvelle contribution a l’étude d’un lémurien Malgache, le aye-aye (Daubentonia madagascariensis E. Geoffroy). Mammalia, 34, 167–193.CrossRefGoogle Scholar
  75. Petter-Rousseaux, A. (1980). Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions. In P. Charles-Dominique, H. M. Cooper, A. Hladik, C. M. Hladik, E. Pages, G. F. Pariente, et al. (Eds.), Nocturnal Malagasy primates: Ecology, physiology, and behavior (pp. 137–152). New York: Academic Press.Google Scholar
  76. Pochron, S. T., Tucker, W. T., & Wright, P. C. (2004). Demography, life history and social structure in Propithecus edwardsi in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 125, 61–72.PubMedCrossRefGoogle Scholar
  77. Radespiel, U. (2000). Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology, 51, 21–40.PubMedCrossRefGoogle Scholar
  78. Rasmussen, D. (1985). A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur and Varecia). International Journal of Primatology, 6, 501–517.CrossRefGoogle Scholar
  79. Ratsimbazafy, J. (2003). On the brink of extinction and the process of recovery: Responses of black-and-white ruffed lemurs (Varecia variegata variegata) to disturbance in Manombo Forest, Madagascar [Dissertation]. Stony Brook: Stony Brook University.Google Scholar
  80. Richard, A. (1974). Patterns of mating in Propithecus verreauxi verreauxi. Prosimian biology (pp. 49–74). London: Duckworth.Google Scholar
  81. Richard, A. F., & Dewar, R. E. (1991). Lemur ecology. Annual Review of Ecology and Systematics, 22, 145–175.CrossRefGoogle Scholar
  82. Richard, A. F., Dewar, R. E., Schwartz, M., & Ratsirarson, J. (2002). Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi). Journal of Zoology, London, 256, 421–436.Google Scholar
  83. Sadlier, R. M. F. S. (1972). Environmental effects. In C. R. Austin & R. V. Short (Eds.), Reproduction in mammals, book 4: Reproductive patterns (pp. 69–94). Cambridge: Cambridge University Press.Google Scholar
  84. Sauther, M. L. (1993). Resource competition in wild populations of ringtailed lemurs (Lemur catta): Implications for female dominance. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 135–152). New York: Plenum Press.Google Scholar
  85. Sauther, M. L. (1998). Meeting the stresses of reproduction: reproductive and ecological synchrony in free-ranging ring-tailed lemurs (Lemur catta). Folia Primatologica, 69, 414–415.CrossRefGoogle Scholar
  86. Schmelting, B., Ehresmann, P., Lutermann, H., Randrianambinina, B., & Zimmermann, E. (2000). Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: First results of a long term study. In W. R. Lourenço & S. M. Goodman (Eds.), Diversité et endémisme à Madagascar (pp. 165–175). Paris: Memoires de la Société de Biogéographie.Google Scholar
  87. Shideler, S. E., Czekala, N. M., Benirschke, K., & Lasley, B. L. (1983). Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biology of Reproduction, 28, 963–969.PubMedCrossRefGoogle Scholar
  88. Stanger, K. F., Coffman, B. S., & Izard, M. K. (1995). Reproduction in Coquerel’s dwarf lemur (Mirza coquereli). American Journal of Primatology, 36, 223–237.CrossRefGoogle Scholar
  89. Stearns, S. C. (1976). Life-history tactics: a review of the ideas. The Quarterly Review of Biology, 51, 3–47.PubMedCrossRefGoogle Scholar
  90. Sterling, E. J. (1993). Patterns of range use and social organization in aye-ayes (Daubentonia madagascariensis) on Nosy Mangabe. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 1–10). New York: Plenum Press.Google Scholar
  91. Sterling, E. J. (1994). Evidence for nonseasonal reproduction in wild aye-ayes. Folia Primatologica, 62, 46–53.CrossRefGoogle Scholar
  92. Tecot, S. (2008). Seasonality and predictability: The hormonal and behavioral responses of Eulemur rubriventer in Southeastern Madagascar [Dissertation]. Austin: University of Texas-Austin.Google Scholar
  93. Tecot, S., & Overdorff, D. (2005). Aseasonal births and reproductive patterns in Eulemur rubriventer in southeastern Madagascar. American Journal of Primatology, 66, 111–112.CrossRefGoogle Scholar
  94. Terranova, C. J., & Coffman, B. S. (1997). Body weights of wild and captive lemurs. Zoo Biology, 16, 17–30.CrossRefGoogle Scholar
  95. van Horn, R. N. (1975). Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatologica, 24, 203–220.CrossRefGoogle Scholar
  96. van Horn, R. N. (1980). Seasonal reproductive patterns in primates. Progress in Reproductive Biology, 5, 181–221.Google Scholar
  97. van Schaik, C., & van Noordwijk, M. A. (1985). Interannual variability in fruit abundance and reproductive seasonality in Sumatran long-tailed macaques. Journal of Zoology, 206, 533–549.CrossRefGoogle Scholar
  98. Wasser, S. K. (1996). Reproductive control in wild baboons measured by fecal steroids. Biology of Reproduction, 55, 393–399.PubMedCrossRefGoogle Scholar
  99. Whitten, P. L., & Brockman, D. K. (2001). Strepsirrhine reproductive ecology. In P. Ellison (Ed.), Reproductive ecology and human evolution (pp. 321–350). New York: A. de Gruyter.Google Scholar
  100. Wright, P. C. (1997). The future of biodiversity in Madagascar: A view from Ranomafana National Park. In S. G. Goodman & B. D. Patterson (Eds.), Natural change and human impact in Madagascar (pp. 381–405). Washington, DC: Smithsonian Institution Press.Google Scholar
  101. Wright, P. C. (1999). Lemur traits and Madagascar ecology: coping with an island environment. Yearbook Physical Anthropology, 42, 31–72.CrossRefGoogle Scholar
  102. Wright, P. C., Razafindratsita, V. R., Pochron, S. T., & Jernvall, J. (2005). The key to Madagascar frugivores. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 121–138). Dordrecht: Springer.CrossRefGoogle Scholar
  103. Wright, P., King, S. J., Baden, A., & Jernvall, J. (2008). Aging in wild female lemurs: Sustained fertility with increased infant mortality. In S. Atsalis, S. W. Margulis, & P. R. Hof (Eds.), Primate reproductive aging: Cross-taxon perspectives on reproduction (pp. 17–28). Basel: Karger.CrossRefGoogle Scholar
  104. Young, A. L., Richard, A. F., & Aiello, L. C. (1990). Female dominance and maternal investment in Strepsirhine primates. The American Naturalist, 135, 473–488.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.School of AnthropologyUniversity of ArizonaTucsonUSA
  2. 2.Interdepartmental Program in Anatomical SciencesStony Brook UniversityStony BrookUSA
  3. 3.Department of Ecology and EvolutionStony Brook UniversityStony BrookUSA
  4. 4.Institute for the Conservation of Tropical EnvironmentsStony Brook UniversityStony BrookUSA
  5. 5.Centre ValBioRanomafanaMadagascar
  6. 6.Department of AnthropologyUniversity of TexasAustinUSA

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