Abstract
Microcebus murinus exhibits highly seasonal biological rhythms to cope with extreme seasonality in availability of resources. To study the role of daylength on seasonal changes in body mass and reproductive function, we exposed male and female gray mouse lemurs to natural, constant, or alternating light cycles for 2 years under constant environmental conditions. When exposed to either constant short (SD: 10 h light/day), long (LD: 14 h light/day), or intermediate (ID: 12 h light/day) daylength, males and females maintained a constant body mass with no spontaneous cyclic variation. We only observed typical seasonal body mass changes in subjects exposed to alternating periods of SD and LD, the weight gain being triggered by SD, whereas weight loss occurred under LD. Reproductive activity in females proceeded from an endogenous rhythm that was expressed under constant daylengths. In contrast, changes in reproductive activity in males depended on daylength variation. In both sexes, SD and LD have direct inhibitory or stimulatory effects on reproductive activity. In females, daylength regulates breeding season by synchronizing an endogenous sexual rhythm with the season, whereas in males, the perception of a critical photoperiod is used to determine the subsequent onset or arrest of their breeding season. These sexual differences in the effect of daylength could be related to sex-specific differences in reproductive constraints.
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REFERENCES
Aujard, F., Boissy, I., and Claustrat, B. (1998). Melatonin secretion in a nocturnal prosimian primate: effect of photoperiod and aging. In Touitou, Y. (ed.), Biological Clocks. Mechanisms and Applications, Elsevier Science, Amsterdam, pp. 337–340.
Aujard, F., Perret, M., and Vannier, G. (1998). Thermoregulatory responses to variations of photoperiod and ambient temperature in the male lesser mouse lemur: a primitive or advanced adaptive character? J. Comp. Physiol. B 168: 540–548.
Bartness, T. J. (1996). Photoperiod, sex, gonadal steroids, and housing density affect body fat in hamsters. Physiol. Behav. 60: 517–529.
Bartness, T. J., and Wade, G. N. (1989). Photoperiodic control of seasonal body weight in hamsters. Neurosci. Biobehav. Rev. 9: 599–612.
Beasley, L. J., and Zucker, I. (1986). Circannual cycles of body mass, food intake and reproductive condition in male pallid bats. Physiol. Behav. 38: 697–702.
Boissin J., and Canguilhem, B. (1988). Les rythmes circannuels chez les Mammifères. Arch. Int. Physiol. Biochem. 94: 289–345.
Brockmann, D. K. (1994). Reproduction and mating system of Verreaux's Sifaka, Propithecus verreauxi, at Beza Mahafaly, Madagascar. PhD thesis, Yale University, New Haven, CT.
Bronson, F. H. (1989). Mammalian Reproductive Biology, University of Chicago Press, Chicago.
Bronson, F. H. (1998). Seasonal variation in human reproduction: environmental factors. Quart. Rev. Biol. 70: 141–164.
Charles-Dominique, P., and Hladik, C. M. (1971). Le lépilemur du sud de Madagascar: écologie, alimentation et vie sociale. Terre et Vie 1: 3–66.
Chik, C. L., Osborne, F. X., Libe, A. E., Booth, J. D., Renquist, D., and Merriam, G. R. (1991). Photoperiod-driven changes in reproductive function in male rhesus monkeys. J. Clin. Endocrinol. Metabol. 74: 1068–1074.
Craven, R. P., and Clarke, J. R. (1986). Gonadal and gonadotrophin secretion in the male vole (Microtus agrestis) after an abrupt change in photoperiod. J. Reprod. Fert. 76: 513–518.
Curlewis, J. D., and Loudon, A. S. I. (1989). The role of refractoriness to long daylength in the annual reproductive cycle of the female Bennett's wallaby (Macropus rufogriseus rufogriseus). J. Exp. Zool. 252: 200–206.
Dark, J., and Zucker, I. (1986). Photoperiodic regulation of body mass and fat reserves in the meadow vole. Physiol. Behav. 38: 851–854.
Delgadillo, J. A., Leboeuf, B., and Chemineau, P. (1993). Maintenance of sperm production in bucks during a third year of short photoperiodic cycles. Reprod. Nut. Dev. 33: 609–617.
Ellison, G. T. H., Skinner, J. D., and Haim, A. (1992). The relative importance of photoperiod and temperature as cues for seasonal acclimation in pouched mice (Saccostomus campestris) from southern africa. J. Comp. Physiol. B 162: 740–746.
Fietz, J. (1998). Body mass in wild Microcebus murinus over the dry season. Folia Primatol. 34: 221–244.
Fiezt, J. (1999). Mating system of Microcebus murinus. Am. J. Primatol. 48(2): 127–133.
Foerg, R. (1982). Reproduction in Cheirogaleus medius. Folia Primatol. 38: 108–121.
Follet, B. K., and Pearce-Kelly, A. (1990). Photoperiodic control of the termination of reproduction in japanese quail (Coturnix coturnix japonica). Proc. R. Soc. Lond. B 242: 225–230.
Gorman, M. R., and Zucker, I. (1995). Seasonal adaptations of Siberian hamsters. Pattern of changes in daylength controls annual testicular and body weight rhythms. Biol. Reprod. 53: 116–125.
Hladik, A. (1980). The dry forest of the west coast of Madagascar: Climate, phenology and food available for prosimians. In Charles-Dominique, P., Cooper, H. M., Hladik, A., Hladik, C. M., Pages, E., Pariente, G., Petter-Rousseaux, A., Petter, J. J., and Schilling, A. (eds.), Nocturnal Malagasy Primates, Academic Press, New York, pp. 1–40.
Kappeler, P. M., and Ganzhorn, J. U. (1993). Lemur Social Systems and Their Ecological Basis, Plenum Press, New York.
Keverne, E. B. (1987). Processing of environmental stimuli and primate reproduction. J. Zool. 213: 345–408.
Kriegsfeld, L. J., and Nelson, R. J. (1996). Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie voles. Am. J. Physiol. 270R: 1013–1018.
Malpaux, B., Robinson, J. E., Wayne, N. L., Karsch, F. J. (1988). Regulation of the onset of the breeding season of the ewe: Importance of long days and of an endogenous reproductive rhythm. J. Endocrinol. 122: 269–278.
Martin, R. D. (1973). A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus). In Michael, R. P., and Crooks, J. H. (eds.), Comparative Ecology and Behaviour of Primates, Academic Press, London, pp. 1–68.
Michener, G. R. (1998). Sexual differences in reproductive effort of richardson's ground squirrels. J. Mammal 79: 1–19.
Nagy, T. M., and Negus, N. C. (1993). Energy acquisition and allocation in male collared lemmings (Dicrostonyx groenlandicus): Effects of photoperiod, temperature and diet quality. Physiol. Zool. 66: 537–560.
Nicholls, T. J., Goldsmith, A. R., and Dawson, A. (1988). Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68: 133–176.
O'Callaghan, D., Karsch, F. J., Boland, M. P., and Roche, J. F. (1991). Role of short days in timing the onset and duration of reproductive activity in ewes under artificial photoperiods. Biol. Reprod. 44: 23–28.
O'Callaghan, D., Karsch, F. J., Boland, M. P., Hanrahan, J. P., and Roche, J. F. (1992). Variation in the timing of the reproductive season among breeds of sheep in relation to differences in photoperiodic synchronization of an endogenous rhythm. J. Reprod. Fert. 96: 443–452.
O'Jile, J. R., and Bartness, T. J. (1992). Effects of thyroxine on the photoperiodic control of energy balance and reproductive status in siberian hamsters. Physiol. Behav. 52: 267–270.
Ogilvie, K. M., and Stetson, M. H. (1990).The timing of gonadal refractoriness in the female turkish hamster (Mesocricetus branbti) is not dependent on the timing of gonadal regression. Biol. Reprod. 42: 787–791.
Overdoff, D. J., Strait, S. G., and Telo, A. (1997). Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. Am. J. Primatol. 43: 211–223.
Pages-Feuillade, E. (1988). Modalités de l'occupation de l'espace et relations interindividuelles chez un prosimien nocturne malgache (Microcebus murinus). Folia Primatol. 50: 204–220.
Pereira, M. E. (1993). Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In Kappeler, P. M., and Ganzhorn, J. U. (eds.), Lemur Social Systems and Their Ecological Basis, Plenum Press, New York, pp. 205–222.
Perret, M. (1980). Influence de la captivité et du groupement social sur la physiologie du Microcébe (Microcebus murinus, Cheirogaleinae, Primates). Doctoral thesis, University Paris XI.
Perret, M. (1992). Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol. 59: 1–25.
Perret, M. (1996). Manipulation of sex ratio at birth by urinary cues in a prosimian primate. Behav. Ecol. Sociobiol. 38: 259–266.
Perret, M., and Predine, J. (1984). Effects of long-term grouping on plasma corticol levels in Microcebus murinus (Prosimii). Horm. Behav. 18: 346–358.
Perret, M., Aujard, F., and Vannier, G. (1998). Influence of daylength on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus. Comp. Biochem. Physiol. A 119: 981–989.
Petter, J. J., Albignac, R., and Rumpler, Y. (1977). Mammifères Lémuriens (Primates, Prosimiens). In Orstom-CNRS (eds.), Faune de Madagascar, Vol. 44, Paris, pp. 1–514.
Petter-Rousseaux, A. (1975). Activité sexuelle de Microcebus murinus soumis à des régimes photopériodiques expérimentaux. Ann. Biol. Anim. Biophys. 15: 503–508.
Petter-Rousseaux, A. (1979). Age of Microcebus murinus at the onset of testicular development. Preliminary observations on photoperiod effect. Ann. Biol. Anim. Biochem. Biophys. 19: 1801–1806.
Petter-Rousseaux, A. (1980). Seasonal activity rhythms, reproduction and body weight variations in five sympatric nocturnal prosimians in simulated light and climatic conditions. In Charles-Dominique, P., Cooper, H. M., Hladik, A., Hladik, C. M., Pages, E., Pariente, G., Petter-Rousseaux, A., Petter, J. J., and Schilling, A. (eds.), Nocturnal Malagasy Primates, Academic Press, New York, pp. 137–152.
Petter-Rousseaux, A. (1984). Annual variations in the plasma thyroxine level in Microcebus murinus. Gen. Comp. Endocr. 55: 405–409.
Plant, T. M. (1988). Puberty in Primates. In Knobil, E., and Neil, J. (eds.), The Physiology of Reproduction, Raven Press, New York, pp. 1763–1788.
Rolf, H. J., and Fisher, K. (1996). Serum testosterone, 5 alpha-dihydrotestosterone and different sex characteristics in male fallow deer (Cervus dama): A long-term experiment with accelerated photoperiod. Comp. Biochem. Physiol. A 115: 207–221.
Rowe, N. (1996). The Pictorial Guide to the Living Primates, Pogonias Press, New York.
Schlatt, S., De Geyter, M., Kliesch, S., Nieschlag, E., and Bergmann, M. (1995). Spontaneous recrudescence of spermatogenesis in the photoinhibited male Djungarian Hamster, Phodopus sungorus. Biol. Reprod. 53: 1169–1177.
Schmid, J., and Kappeler, P. M. (1998). Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behav. Ecol. Sociobiol. 43: 125–132.
Sorg, J.-P., and Rohner, U. (1996). Climate and phenology of the dry deciduous forest of the Kirindy forest. Primate Report 46: 57–80.
Stanger, K. F., Coffman, B. S., and Izard, M. K. (1995). Reproduction in coquerel's dwarf lemur (Mirza coquereli). Am. J. Primatol. 36: 223–237.
Steger, R. W., and Bartke, A. (1991). Temporal sequence of neuroendocrine events associated with the transfert of male golden hamsters from a stimulatory to a nonstimulatory photoperiod. Biol. Reprod. 44: 76–82.
SYSTAT. (1997). New Statistics, SPSS, Inc., Chicago, IL, 303 pp.
Turek, F. W., and van Cauter, E. (1988). Rhythms in reproduction. In Knobil, E., Neil, J. D., Greenwald, G. S., Markert, C. L., and Pfaff, D. W. (eds.), The Physiology of Reproduction, Raven Press, New York, pp. 1789–1800.
Van Horn, R. N., and Eaton, G. G. (1976). Reproductive physiology and behaviour in Prosimians. In Doyle, G. A., and Martin, R. D. (eds.), The Study of Prosimian Behaviour, Academic Press, New York, pp. 79–122.
Wayne, N. L., Malpaux, B. M., and Karsch, F. J. (1990). Photoperiodic requirements for timing the onset and duration of the breeding season in the ewe. J. Comp. Physiol. A 166: 835–842.
Woodfill, C. J., Robinson, J. E., Malpaux, B. M., and Karsch, F. J. (1991). Synchronization of the circannual reproductive rhythms of the ewe by discrete photoperiodic signals. Biol. Reprod. 45: 110–121.
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Perret, M., Aujard, F. Regulation by Photoperiod of Seasonal Changes in Body Mass and Reproductive Function in Gray Mouse Lemurs (Microcebus murinus): Differential Responses by Sex. International Journal of Primatology 22, 5–24 (2001). https://doi.org/10.1023/A:1026457813626
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DOI: https://doi.org/10.1023/A:1026457813626