Abstract
Photoperiodic cues provide nonequatorial animals a reliable schedule for adaptive changes in metabolism, developmental rate, reproductive effort, and behavior. This study discovered seasonal adjustments of growth rate and adult body weight in semi-free-ranging ringtailed lemurs (Lemur cafta) that were correlated with changes in rate of hair growth, thermoregulatory behavior, and social behavior but independent of changes in food availability. Infants increased body weight with 3 to 12g/day, accelerating growth rate annually just after summer solstices. Adult males and females gained weight one to two months later, just before longterm suppressions of growth rate in immatures. Correlations between this set of results and the annual schedule of rainfall in Madagascar led me to propose a new model of life-history strategy for the large-bodied lemurs. Harsh but predictable seasonality of nutritive resources seems to have led these primates to evolve life histories comprehensively geared toward the conservation of energy, including suppression of metabolic rate for much of the Malagasy dry season. This life-history tactic would be analogous to diverse torpid states that enhance survival and reproduction in nonprimate mammals living in harshly seasonal environments. The overall life-history strategy, however, requires rates of infant growth that are uncommonly high among group-living primates relative to maternal size. Like many other animal parents, lemur mothers suffer high costs of investment to help offspring meet a deadline: lemur infants must grow large and perhaps store energy before the dry season, so they can safely reduce metabolic rate and grow little during the dry season. The high cost of lactation is suggested to have promoted wide-spread evolution of female dominance and male-committed infanticide among lemurid and indrid species. Continued research on the environmental regulation of life histories will be required before a deep understanding of primate natural history can be achieved.
Keywords
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.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Benirschke, K. and Miller, C.J., 1981, Weights and neonatal growth of ringtailed lemurs (Lemur cafta) and ruffed lemurs (Lemur variegatus), J. ZooAnim. Med. 12: 107.
Bogart, M.H., Kumamoto, A.T. and Lasley, B.L., 1977, A comparison of the reproductive cycle of three species of Lemur, Folia Primatol. 28: 134.
Boyce, M.S., 1988, Evolution of life histories: theory and patterns from mammals, in: “ Evolution of Life Histories of Mammals,” M.S. Boyce, ed., Yale University Press, New Haven.
Bradley, S.R. and Hudson, J.W., 1974, Temperature regulation in the tree shrew Tupaia glis, Comp. Biochem. Physiol. 48A: 55.
Brizzee, K.R. and Dunlap, W.P., 1986, Growth, in: “ Comparative Primate Biology, Vol. 3: Reproduction and Development,” J. Erwin and G. Mitchell, eds., Alan R. Liss, New York.
Bronson, F.H., 1989, “Mammalian Reproductive Biology,” University of Chicago Press, Chicago.
Buss, D.H., Cooper, R.W. and Wallen, K., 1976, Composition of lemur milk, Folia Primatol. 26: 301.
Chik, C.L., Almeida, O.F.X., Libre, EA., Booth, J.D., Renquist, D. and Merriam, G.R., 1992, Photoperiod-driven changes in reproductive function in male rhesus monkeys, J. Clin. Endocrinol. Metabol. 74: 1068.
Daniels, H., 1984, Oxygen consumption in Lemur fulvus: deviation from the ideal model, J. Mammal. 65: 584.
Dark, J. and Zucker, I., 1983, Short photoperiods reduce winter energy requirements of the meadow vole, Microtus pennsylvanicus, Physiol. Behay. 31: 699.
DuMond, F.V., 1968, The squirrel monkey in a seminatural environment, in: “The Squirrel Monkey,” LA. Rosenblum and R.W. Cooper, Academic Press, New York.
Eisenberg, J.F., 1981, “The Mammalian Radiations,” University of Chicago Press, Chicago.
Engqvist, A. and Richard, A., 1991, Diet as a possible determinant of cathemeral activity patterns in primates, Folia Primatol. 57: 169.
Foerg, R., 1982, Reproduction in Cheirogaleus medius, Folia Primatol. 39: 49.
Foerg, R. and Hoffman, R., 1982, Seasonal and daily activity changes in captive Cheirogaleus medius, Folia Primatol. 38: 259.
Glassman, D., Coelho, A., Carey, K. and Bramblett, C., 1984, Weight growth in savannah baboons: A longitudinal study from birth to adulthood, Growth 48: 425.
Glick, B.B., 1979, Testicular size, testosterone level, and body weight in male Macaca radiata, Maturational and seasonal effects, Folia Primatol. 32: 268.
Griffiths, J.J. and Ranaivoson, R., 1972, Madagascar in: “Climates of Africa,” J.F. Griffiths, ed., Elsevier, New York.
Hoffmann, K., 1981, Photoperiodism in vertebrates, in: “Biological Rhythms, Handbook of Behavioral Neurobiology,” Vol 4, J. Aschoff, ed., Plenum Press, New York.
Hrdy, S.B., 1981, “The Woman That Never Evolved,” Harvard University Press, Cambridge.
Janson, C.H. and van Schaik, C.P., 1993, Slow and steady wins the race: ecological risk aversion in juvenile primates, in: “Juvenile Primates: Life History, Development and Behavior,” M.E. Pereira and LA. Fairbanks, eds., Oxford University Press, New York.
Jolly, A., 1966, “Lemur Behavior: A Madagascar Field Study,” University of Chicago Press, Chicago.
Jolly, A., 1984, The puzzle of female feeding priority, in: “Female Primates: Studies by Women Primatologists,” M. Small, ed., Alan R. Liss, Inc., New York.
Kappeler, P.M., 1992, “Female dominance in Malagasy primates,”, Ph.D. thesis, Duke University, Durham.
Kirkwood, J.K., 1985, Patterns of growth in primates, J. Zool., Lond. 205: 123.
Koyama, N., 1988, “Mating behavior of ring-tailed lemurs (Lemur cafta) at Berenty, Madagascar, Primates, 29: 163.
Koyama, N., 1991, Troop division and inter-troop relationships of ring-tailed lemurs (Lemur cafta) at Berenty, Madagascar, in: “Primatol. Today,” A. Ehara, T. Kimura, O. Takenaka, and M. Iwamoto, eds., Elsevier, Amsterdam.
Koyama, N., 1992, Some demographic data of ring-tailed lemurs (Lemur cafta) at Berenty, Madagascar, in: “Social Structure of Madagascar Higher Vertebrates in Relation to Their Adaptive Radiation,” S. Yamagishi, ed., Osaka City University, Osaka.
Lee, T.M. and Zucker, I., 1988, Vole infant development is influenced perinatally by maternal photoperiodic history, Am. J. Physiol., 255, RICP 24: 831.
Lindburg, D.G., 1987, Seasonality of reproduction in primates, in: “Comparative Primate Biology, Vol. 2B: Behavior, Cognition, and Motivation,” J. Erwin and G.D. Mitchell, eds., Alan R. Liss., New York.
Loudon, A.S.I. and Racey, PA., (eds.), 1987., “Reproductive Energetics in Mammals”, Clarendon Press, Oxford.
Matsubayashi, K. and Enomoto, T., 1983, Longitudinal studies on annual changes in plasma testosterone, body weight and spermatogenesis in adult Japanese monkeys (Macaca fuscata fuscata) under laboratory conditions, Primates, 24: 521.
McClintock, M.K., 1983, Pheromonal regulation of the ovarian cycle: enhancement, suppression, and synchrony, in: “Pheromones and Reproduction in Mammals,” J. Vandenberg, ed., Academic Press, New York.
McCormick, SA., 1981, Oxygen consumption and torpor in the fat-tailed dwarf lemur (Cheirogaleus medius): rethinking prosimian metabolism, Comp. Biochem. Physiol. A 68: 605.
McNab, B.K., 1988, Energy conservation in a tree-kangaroo (Dendrolagus matschiei) and the red panda (Ailu,us fulgens), Physiol. Zool. 61: 280.
Morland, H.S., 1992, Seasonal behavioral variation and its relationship to thermoregulation in ruffed lemurs (Varecia variegata variegata), in: “Lemur Social Systems and Their Ecological Basis,” P.M. Kappeler and J.U. Ganzhorn, eds., Plenum Press, New York.
Müller, E.F., 1985, Basal metabolic rates in primates - the possible role of phylogenetic and ecological factors, Comp. Biochem. Physiol. A 81: 707.
Pereira, M.E., 1991, Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae), Physiol. Behay. 49: 47.
Pereira, M.E., 1993, Agonistic interaction, dominance relation, and ontogenetic trajectories in ringtailed lemurs, in: “Juvenile Primates: Life History, Development, and Behavior,” M. E. Pereira and L. A. Fairbanks, eds., Oxford University Press, New York.
Pereira, M.E. and Fairbanks, LA.(eds.), 1993, “Juvenile Primates: Life History, Development, and Behavior,” Oxford University Press, New York.
Pereira, M.E. and Weiss, M.L., 1991, Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs, Behay. Ecol. Sociobiol. 28: 141.
Pereira, M.E., Klepper, A. and Simons, E.L., 1987, Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests, parking, and biparental guarding, Am. J. Primato!. 13: 129.
Petter-Rousseaux, A., 1968, Cycles genitaux saisonniers des lémuriens malgaches, in: “Cycles Genitaux Saisonniers du Mammifères Sauvages,” R. Canivenc, ed., Masson, Paris.
Petter-Rousseaux, A., 1974, Photoperiod, sexual activity and body weight variation of Microcebus murinus (Miller 1777), in: “Prosimian Biology,” R.D. Martin, GA. Doyle and A.C. Walker, eds., Duckworth, London.
Petter-Rousseaux, A., 1980, Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions, in: “Nocturnal Malagasy Primates,” P. Charles-Dominique, H.M. Cooper, A. Hladik, C.M. Hladik, E. Pages, G.F. Pariente, A. Petter-Rousseaux, J.J. Petter and A. Schilling, eds., Academic Press, New York.
Pond, C.M., 1978, Morphological aspects and the ecological and mechanical consequences of fat deposition in wild vertebrates, Ann. Rev. Ecol. Syst. 9: 519.
Rasmussen, D.T., 1985, A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur and Varecia), Int. J. Primatol. 6: 501.
Richard, A.F., 1987, Malagasy prosimians: female dominance, in: “Primate Societies,” B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, eds., University of Chicago Press, Chicago.
Richard, A.F. and Nicoll, M.E., 1987, Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi, Am. J. Primatol. 12: 309.
Russell, R.I., 1975, Body temperatures and behavior of captive Cheirogaleids, in: “Lemur Biology,” I. Tattersall and R. Sussman, eds., Plenum Press, London.
Rutenberg, G. and Coelho, A., 1988, Neonatal nutrition and longitudinal growth from birth to adolescence in baboons, Am. J. Phys. Anthropol. 75: 529.
Sackett, G.P. and Ruppenthal, G.C., 1992, Growth of nursery-raised Macaca nemestrina infants: Effects of feeding schedules, sex, and birth weight, Am. J. Primatol. 27: 177.
Sauther, M.L., 1991, Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar, Am. J. Phys. Anthropol. 84: 463.
Strum, S.C., 1991, Weight and age in wild olive baboons, Am. J. Primatol. 25: 219.
Sussman, R.W., 1991, Demography and social organization of free-ranging Lemur cafta in the Beza Mahafaly Reserve, Madagascar, Am. J. Phys. Anthropol. 84: 43.
Taylor, L.L. and Sussman, R.W., 1985, A preliminary study of kinship and social organization in a semifree-ranging group of Lemur cafta, Int. J. Primatol. 6: 601.
van Horn, R.N., 1975, Primate breeding season: photoperiodic regulation in captive Lemur cafta, Folia Primatol. 24: 203.
van Horn, R.N., 1980. Seasonal reproductive patterns in primates, in: “Progress in Reproductive Biology,” P.O. Hubinont, ed., Karger, Basel.
van Horn, R.N. and Eaton, G.G., 1979, Reproductive physiology and behavior in prosimians in: “The Study of Prosimian Behavior,” G.A. Doyle and R.D. Martin, eds., Academic Press, New York.
van Horn, R.N. and Resko, JA., 1977, The reproductive cycle of the ring-tailed lemur Lemur catta: sex steroid levels and sexual receptivity under controlled photoperiods, Endocrinol. 101: 1579.
van Schaik, C.P., 1989, The ecology of social relationships amongst female primates, in: “Comparative Socioecology: The Behavioural Ecology of Humans and Other Mammals,” V. Standen and RA. Foley, eds., Blackwell Scientific Publ., Boston.
van Schaik, C.P. and P.M. Kappeler, 1993, Life history, activity period and lemur social systems, in: “Lemur Social Systems and Their Ecological Basis,” P.M. Kappeler and J U Ganzhorn, eds., Plenum Press, New York.
Vick, L.G. and Pereira, M.E., 1989, Episodic targeting aggression and the histories of Lemur social groups, Behay. Ecol. Sociobiol. 25: 3.
Wilen, R. and Naftolin, F., 1978, Pubertal age, weight, and weight gain in the individual female New World monkey (Cebus albifrons), Primates 19: 769.
Winfree, A.T., 1980, “The Geometry of Biological Time,” Springer, New York.
Young, A.L., Richard, A.F. and Aiello, L.C., 1990, Female dominance and maternal investment in strepsirhine primates, Am. Nat. 135: 473.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1993 Springer Science+Business Media New York
About this chapter
Cite this chapter
Pereira, M.E. (1993). Seasonal Adjustment of Growth Rate and Adult Body Weight in Ringtailed Lemurs. In: Kappeler, P.M., Ganzhorn, J.U. (eds) Lemur Social Systems and Their Ecological Basis. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-2412-4_15
Download citation
DOI: https://doi.org/10.1007/978-1-4899-2412-4_15
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4899-2414-8
Online ISBN: 978-1-4899-2412-4
eBook Packages: Springer Book Archive