The Bioenergetics of Reproduction in Prosimian Primates: is it Related to Female Dominance?

  • Christopher D. Tilden
  • Olav T. Oftedal


Primates have been characterized as having relatively low reproductive rates, as indicated by extended periods of gestation, lactation, and infant dependency (Sacher and Staffeldt, 1974; Martin, 1975; Eisenberg, 1981; Ankel-Simons, 1983; Harvey and Clutton-Brock, 1985; Rasmussen, 1986; Rasmussen and Izard, 1988). Nonetheless, among primates there have evolved diverse patterns of reproduction and parental care. For example, in some species care is provided solely by the mother, while in other species other members of the family are primary care-givers. Infants may be carried nearly continuously; or they may be left in a nest, in tree holes, or on branches for extended periods of time. Some species may exhibit communal care and nursing. Rearing patterns are especially diverse among prosimian primates. Patterns vary from those of the social, diurnal lemurs of Madagascar in which females of most species carry their dependent young, and in some species with the assistance of family members (Klopfer and Klopfer, 1970; Klopfer, 1974; Wright, 1990) to those of the small, solitary, nocturnal bushbabies and lorises of Asia and Africa in which females provide nearly all care, and frequently must park their infants to forage for food (Doyle et al., 1969; Rosenson, 1971, 1972; Harcourt, 1984; Rasmussen, 1986).


Milk Yield Basal Metabolic Rate Gestation Length Female Dominance Agricultural Research Council 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adolph, E. F. (1970). Physiological stages in the development of mammals. Growth, 34, 113 – 124.PubMedGoogle Scholar
  2. Adolph, E. F., & Heggeness, F. W. (1971). Age changes in body water and fat in fetal and infant mammals. Growth, 35, 55–63.PubMedGoogle Scholar
  3. Agricultural Research Council. (1980). The Nutrient Requirements of Ruminant Livestock. Farnham Royal, England: Commonwealth Agricultural Bureaux. Ankel-Simons, F. (1983). A Survey of Living Primates and Their Anatomy. New York: MacMillan Publishing Co.Google Scholar
  4. Association of Official Analytical Chemists. (1990). Official Methods of Analysis. Fifteenth edition. Arlington, Virginia: Association of Official Analytical Chemists.Google Scholar
  5. Belek, J., & Jenness, R. (1962). Dephosphorization of casein by heat treatment. I. In caseinate solutions. Journal of Dairy Science, 45, 12–19.Google Scholar
  6. Blaxter, K. L. (1989). Energy Metabolism in Animals and Man. Cambridge: Cambridge University Press.Google Scholar
  7. Brouwer, E. (1965). Report of subcommittee on constants and factors. In K. L. Blaxter (Ed.), Energy metabolism: proceedings of 3rcd symposium (pp. 441–443). London: Academic Press.Google Scholar
  8. Buss, D. H., & Voss, W. R. (1971). Evaluation of four methods for estimating the milk yield of baboons. Journal of Nutrition. 101. 901–910PubMedGoogle Scholar
  9. Charles-Dominique, P., Cooper, H. M., Hladik, A., Hladik, C. M., Pages, E., Pariente, G. F., Petter-Rousseaux, A., Petter, J. J. & Schilling, A. (1980). Nocturnal Malagasy Prosimians. New York: Academic Press.Google Scholar
  10. Clutton-Brock, T. H., and Harvey, P. H. (1983). The functional significance of variation in body size among mammals. In J. F. Eisenberg & D. G. Kleiman (Eds.), Recent advances in the study of mammalian behavior (pp. 632–663). Shippenburg. PA: American Society of Mammologists.Google Scholar
  11. Coward, W. A., Sawyer, M. B., Whitehead, R. G., Prentice, A.M. & Evan, J. (1979). New method for measuring milk intakes in breast-fed babies. Lancet, 1979 (2), 13–14.CrossRefGoogle Scholar
  12. Daniels, H. L. (1984). Oxygen consumption in Lemur fulvus: deviation from the ideal model. Journal of Mammalogy, 65 (4), 584–592.CrossRefGoogle Scholar
  13. Doyle, G.A., Andersson, A. & Bearder, S. K. (1969). Maternal behavior in the lesser bushbaby (Galago senegalensis moholi) under semi-natural conditions. Folia Primatologica, 11, 215–238.CrossRefGoogle Scholar
  14. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P.A. & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28 (3), 350–356.CrossRefGoogle Scholar
  15. Eisenberg, J. F. (1981). The Mammalian Radiations. Chicago: University of Chicago PressGoogle Scholar
  16. Eisenberg, J. F., Muckenhirn, N. A. & Rudran, R. (1972). The relationship between ecology and social structure. Science, 176, 863–874.PubMedCrossRefGoogle Scholar
  17. Gittleman, J. L. (1988). Behavioral energetics of lactation in a herbivorous carnivore, the red panda (Ailurus fulgens). Ethology, 7, 13–24.Google Scholar
  18. Gittleman, J. L., & Oftedal, O. T. (1987). Comparative growth and lactational energetics in carnivores. In A. Loudon & P. A. Racey (Eds.), Reproductive energetics in mammals (pp. 41–77). Oxford: Oxford University Press.Google Scholar
  19. Gittleman, J. L., & Thompson, S. D. (1989). Energy allocation in mammalian reproduction. American Zoology, 28, 863–875.Google Scholar
  20. Hanwell, A., & Peaker, M. (1977). Physiological effects of lactation on the mother. Symposium of the Zoological Society of London, 41, 297–312.Google Scholar
  21. Harcourt, C. S. (1984). The behaviour and ecology ot galagos in Kenyan coastal forest. Ph.D. thesis, Cambridge University, Cambridge, England.Google Scholar
  22. Harvey, P. H., & Clutton-Brock, T. H. (1985). Life history variation in primates. Evolution, 39, 559–581.CrossRefGoogle Scholar
  23. Jolly, A. (1966). Lemur Behavior. Chicago: Chicago University Press.Google Scholar
  24. Jolly, A. (1984). The puzzle of female feeding priority. In M. E. Small (Ed.), Female Primates: Studies by Women Primatologists (pp. 197–215). New York: Alan Liss.Google Scholar
  25. Kappeler, P. M. (1992). Female dominance in Malagasy prosimians. Ph.D. thesis, Duke University, Durham, NC.Google Scholar
  26. Klopfer, P. H. (1974). Mother-young relations in lemurs. In R. D. Martin, G. A. Doyle & A. C. Walker (Eds.), Prosimian Biology (pp. 273–292). Pittsburgh: University of Pittsburgh Press.Google Scholar
  27. Klopfer, P. H., & Klopfer, M. S. (1970). Patterns of maternal care in three species of Lemur. I. Normative description. Zeitschrift für Tierpsychologie, 27, 984–996.Google Scholar
  28. Leutenegger, W. (1973). Maternal-fetal weight relationships in primates. Folia Primatologica, 20, 280–293.CrossRefGoogle Scholar
  29. Loveridge, G. G. (1986). Bodyweight changes and energy intake in cats during gestation and lactation. Animal Technology, 37: 7–15.Google Scholar
  30. Marier, J. R., & Boulet, M. (1959). Direct analysis of lactose in milk and serum. Journal of Dairy Science, 4, 1390–1391.CrossRefGoogle Scholar
  31. Martin, R. D. (1975). The bearing of reproductive behavior and ontogeny on strepsirhine phylogeny. In W. P. Luckett and F. S. Szalay (Eds.), Phylogeny of the Primates: a multidisciplinary approach (pp. 265–297). New York: Plenum Press.CrossRefGoogle Scholar
  32. Martin, R. D. (1984). Scaling effects and adaptive strategies in mammalian lactation. Symposium of the Zoological Society of London, 51, 87–117.Google Scholar
  33. Martin, R. D., & MacLarnon, A. M. (1985). Gestation period, neonatal size and maternal investment in placental mammals. Nature, London, 313 (17), 220–223.CrossRefGoogle Scholar
  34. Martin, R. D., & MacLarnon, A. M. (1988). Comparative quantitative studies of growth and reproduction. Symposium of the Zoological Society of London, 60, 39–80.Google Scholar
  35. Maynard, L. A., Loosli, J. K., Hintz, H. F. & Warner, R. G. (1979). Animal Nutrition. Seventh edition. New York: McGraw-Hill Book Co.Google Scholar
  36. McNab, B. K., & Wright, P. C. (1987). Temperature regulation and oxygen consumption in the Phillipine tarsier Tarsius syrichta. Physiological Zoology, 60, 596–600.Google Scholar
  37. Müller, E. F. (1979). Energy metabolism, thermoregulation, and water budget in the slow loris (Nycticebus coucang, Boddaert 1785). Comparative Biochemistry and Physiology, 64A, 109–119.Google Scholar
  38. Müller, E. F. (1985). Basal metabolic rates in primates: the possible role of phylogenetic and ecological factors. Comparative Biochemistry and Physiology, 81A, 707–711.Google Scholar
  39. Müller, E. F., & Jaksche, H. (1980). Thermoregulation, oxygen consumption, heart rate and evaporative water loss in the thick-tailed bushbaby (Galago crassicaudatus Geoffroy, 1812). Zeitschrift für Säugetierkunde, 45, 269–278.Google Scholar
  40. Oftedal, O. T. (1984a). Body size and reproductive strategy as correlates of milk energy output in lactating mammals. Acta Zoologica Fennica, 17, 183–186.Google Scholar
  41. Oftedal, O. T. (1984b). Milk composition, milk yield and energy output at peak lactation: a comparative review. Symposium qf the Zoological Society of London, 51, 33–85.Google Scholar
  42. Oftedal, O. T. (1985). Pregnancy and lactation. In R. J. Hudson & R. G. White (Eds.), Bioenergetics of Wild Herbivores (pp. 216–238). Boca Raton, FL: CRC Press.Google Scholar
  43. Oftedal, O. T. (1986). Growth rate and milk composition: a critical appraisal. In L. J. Filer & S. J. Fomon (Eds.), The breastfed infant: a model for performance. Report on the 91st Ross conference on pediatric research (pp. 50–58). Columbus, OH: Ross Laboratories.Google Scholar
  44. Oftedal, O. T., Hintz, H. F. & Schryver, H. F. (1983). Lactation in the horse: milk composition and intake by foals. Journal of Nutrition, 113, 2196–2206.Google Scholar
  45. Oftedal, O. T., and Iverson, S. J. (1987). Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling young. In A. C. Huntley, D. P. Costa, G. A. J. Worthy & M. A. Castellini (Eds.), Approaches to Marine Mammal Energetics (pp. 67–96). Lawrence, KS: Allen Press.Google Scholar
  46. Oftedal, O. T., and Jenness, R. (1988). Interspecies variation in milk composition among horses, zebras, and asses (Perissodactyla, Equidae). Journal of Dairy Research, 55, 57–66.PubMedCrossRefGoogle Scholar
  47. Pereira, M. D. (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
  48. Pereira, M. E., Kaufman, R., Kappeler, P. M. & Overdorff, D. J. (1990). Female dominance does not characterize all of the Lemuridae. Folia Primatologica, 55, 96–103.CrossRefGoogle Scholar
  49. Perrin, D. R. (1958). The calorific value of milk of different species. Journal of Dairy Research, 25, 215–220.CrossRefGoogle Scholar
  50. Power, M. L. (1991). Digestive function, energy intake and the response to dietary gum in captive callitrichids. Ph.D. thesis, University of California at Berkeley, Berkely, CA.Google Scholar
  51. Prentice, A. M., & Prentice, A. (1988). Energy costs of lactation. Annual Review of Nutrition, 8, 63–79.PubMedCrossRefGoogle Scholar
  52. Rasmussen, D. T. (1986). Life history and behavior of slow lorises and slender lorises. Ph.D. thesis, Duke University. Durham, NC.Google Scholar
  53. Rasmussen, D. T., & Izard, M. K. (1988). Scaling of growth and life history traits relative to body size, brain size, and metabolic rate in lorises and galagos (Lorisidae, Primates). American Journal of Physical Anthropology, 75, 357–367.PubMedCrossRefGoogle Scholar
  54. Richard, A. F., & Nicoll, M. E. (1987). Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi. American Journal of Physical Anthropology, 12, 309–314.Google Scholar
  55. Roberts, S. B., Cole, T. J. & Coward, W. A. (1985). Lactational performance in relation to energy intake in the baboon. American Journal of Clinical Nutrition, 41, 1270–1276.PubMedGoogle Scholar
  56. Rosenson, L. M. (1971). Social behavior of the greater bushbaby. Ph.D. thesis, Duke University, Durham, NC.Google Scholar
  57. Rosenson, L. M. (1972). Observations of the maternal behaviour of two captive greater bushbabies (Galago crassicaudatus argentatus). Animal Behavior, 20, 677–688.CrossRefGoogle Scholar
  58. Ross, C. (1992). Basal metabolic rate, body weight and diet in primates: an evaluation of the evidence. Folia Primatologica, 58, 7–23.CrossRefGoogle Scholar
  59. Sacher, G. A., & Staffeldt, E. F. (1974). Relation of gestation time to brain weight for placental mammals: implications for the theory of vertebrate growth. American Naturalist. 108 (963) 593–615.CrossRefGoogle Scholar
  60. Sadleir, R. M. F. S. (1984). Ecological consequences of lactation. Acta Zoologica Fennica, 171, 179–182.Google Scholar
  61. Salmon-Legagneur, E. (1967). Prenatal development in the pig and some other multiparous animals. In G. A. Lodge and G. E. Lamming (Eds.), Growth and Development of Mammals (pp. 158–191). London: Butterworths.Google Scholar
  62. Sauther, M. L., & Nash, L. T. (1987). Effect of reproductive state and body size on food consumption in captive Galago senegalensis braccatus. American Journal of Physical Anthropology, 73, 81–88.CrossRefGoogle Scholar
  63. Schoeller, D. A., & Fjeld, C. R. (1986). Measurement of human milk consumption by deuterium oxide kinetics. In L. J. Filer & S. J. Fomon (Eds.), The breastfed infant: a model for performance. Report on the 91st Ross conference on pediatric research (pp. 13–22). Columbus, OH: Ross Laboratories.Google Scholar
  64. R. Sokal, R., & Rohlf, F. J. (1981). Biometry. New York: W. H. Freeman and Co.Google Scholar
  65. Spray, C. M., & Widdowson, E. M. (1950). The effect of growth and development on the composition of mammals. British Journal of Nutrition, 4, 332–353.PubMedCrossRefGoogle Scholar
  66. Thompson, S. D. (1992). Gestation and lactation in small mammals: basal metabol1c rate and the limits of energy use. In T. E. Tomasi & T. H. Horton (Eds.), Mammalian energetics: interdisciplinary views of metabolism and reproduction (pp. 213–259). Ithaca, NY: Comstrock Publishing Associates (Cornell University Press).Google Scholar
  67. Tilden, C. D. (1993). The reproductive energetics of prosimian primates. Ph.D. thesis, Duke University. Durham, NC.Google Scholar
  68. Wright, P. C. (1990). Patterns of paternal care in primates. International Journal of Primatology, 11 (2), 89–102.CrossRefGoogle Scholar
  69. Young, A. L., Richard, A. F. and Aiello, L. C. (1990). Female dominance and maternal investment in strepsirhine primates. American Naturalist, 135, 473–488.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Christopher D. Tilden
    • 1
  • Olav T. Oftedal
    • 2
  1. 1.Department of Biological Anthropology and AnatomyDuke UniversityDurhamUSA
  2. 2.Department of Zoological Research National Zoological ParkSmithsonian InstitutionUSA

Personalised recommendations