Abstract
Torpor (i.e. the reduction of body temperature and metabolic rate for less than 24 h) and hibernation (i.e. torpor phases longer than 24 h) are among the most extreme adaptations to seasonality in primate habitats. Although widespread among mammals, this form of extreme thermoregulation is rare among primates and is reported only for species of the cheirogaleid family. Understanding their physiological ecology is crucial for many aspects of cheirogaleid socioecology like their social organization and their mating systems. This paper first provides an overview of published information on hibernation and torpor and identifies a patchy distribution for the occurrence of hibernation across genera, species and populations. Based on a review of published studies from the wild and from captivity, we then propose a possible explanation for variation in hibernation behavior among Microcebus species and populations. Accordingly, the amount of energy that can be saved during torpor early in the lean dry season, which is determined by the minimum ambient temperature will be decisive. Only where temperatures are low, early dry season torpor bouts will be long enough to save enough energy to build up fat reserves for longer bouts of hibernation. Finally, we summarize information on the causal factors for the occurrence of hibernation by analyzing sex differences within populations. Further physiological studies on other cheirogaleid species are needed to identify the phylogenetic origin of hibernation in primates.
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References
Atsalis S (1999a) Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. Int J Primatol 20:193–229
Atsalis S (1999b) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. Int J Primatol 20:883–910
Atsalis S (2000) Spatial distribution and population composition of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar, and its implications for social organization. Am J Primatol 51:61–78
Aujard F, Perret M, Vannier G (1998) Thermoregulatory responses to variations of photoperiod and ambient temperature in the male lesser mouse lemur: a primitive or an advanced adaptive character? J Comp Physiol B 168:540–548
Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female mouse lemur (Microcebus murinus). Am J Primatol 37:317–324
Dammhahn M, Kappeler PM (2005) Social system of Microcebus berthae—the world’s smallest primate. Int J Primatol 26:407–435
Dausmann KH, Heldmaier G, Ganzhorn JU (2000) Hibernation in the tropics: body temperature and metabolic rates of a hibernating primate in Madagascar—preliminary results from a field study. In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, Berlin Heidelberg New York, pp 41–47
Dausmann KH, Glos J, Heldmaier G (2001) Social hibernation in a tropical primate species (Cheirogaleus medius). Advances in Ethology 36:140
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155
Eberle M, Kappeler PM (2002) Mouse lemurs in space and time: a test of the socioecological model. Behav Ecol Sociobiol 51:131–139
Eberle M, Kappeler PM (2004) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57:77–90
Fietz J (1998) Body mass in wild Microcebus murinus over the dry season. Folia Primatol 69:183–190
Fietz J, Ganzhorn JU (1999) Feeding ecology of the hibernation primate Cheirogaleus medius: how does it get so fat? Oecologia 121:157–164
Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int J Primatol 19:785–796
Ganzhorn JU, Wright PC, Ratsimbazafy J (1999) Primate communities: Madagascar. In: Fleagle JG, Janson CH, Reed KE (eds) Primate communities. Cambridge University Press, Cambridge, pp 75–89
Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primate and nonprimate examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 132–144
Genin F, Perret M (2000) Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiol Behav 71:315–321
Genin F, Perret M (2003) Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81
Genin F, Nibbelink M, Galand M, Perret M, Ambid L (2003) Brown fat and nonshivering thermogenesis in the gray mouse lemur (Microcebus murinus). Am J Physiol Regul Integr Comp Physiol 284:R811–R818
Goodman SM (2003) Predation on lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1221–1228
Groves CP (2000) The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. Int J Primatol 21:943–962
Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC
Heldmaier G (1989) Seasonal acclimatization of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. In: Wieser W, Gnaiger E (eds) Energy transformation in cells and organisms. Georg Thieme, Stuttgart, pp 130–139
Heldmaier G, Steinlechner S (1993) Suppression of metabolic rate during hibernation. In: Carey C, Florant GL, Wunder BA, Horwitz BA (eds) Life in the cold: ecological, physiological and molecular mechanisms. Westview Press, Boulder, pp 545–548
Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and torpor in mammals. Respir Biol Neurobiol 141:317–329
Hladik CM, Charles-Dominique P, Petter JJ (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente G, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates: ecology, physiology, and behavior. Academic, New York, pp 41–73
Kappeler PM (2000a) Lemur origins: rafting by groups of hibernators? Folia Primatol 71:422–425
Kappeler PM (2000b) Ecologie des microcebes. Primatologie 3:145–171
Kappeler PM, Rasoloarison RM, Rasafimananzoa L, Walter L, Roos, C (2005) Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1970, with description of a new species. Primate Rep 71:3–26
Körtner G, Geiser F (1995) Effect of photoperiod and ambient temperature on activity patterns and body weight cycles of mountain pygmy possums, Burramys parvus (Marsupialia). J Zool B 235:311–322
Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow–fast continuum. J Comp Physiol B 173:87–112
Lymann CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic, New York
Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Princeton University Press, Princeton
Müller AE (1999a) Aspects of social life in the fat-tailed dwarf lemur (Cheirogaleus medius): inferences from body weights and trapping data. Am J Primatol 49:265–280
Müller AE (1999b) Social organization of the fat-tailed dwarf lemur (Cheirogaleus medius) in Northwestern Madagascar. In: Rakotosamimanana, B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Plenum, New York, pp 139–158
Müller AE (1999c) The social organisation of the fat-tailed dwarf lemur, Cheirogaleus medius (Lemuriformes; Primates). Ph.D. thesis, University of Zürich, Zürich
Ortmann S, Heldmaier G, Schmid J (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32
Pastorini J, Thalmann U, Martin RD (2003) A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Nat Acad Sci USA 100:5879–5884
Perret M (1998) Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus murinus). J Mammal 79:1093–1102
Perret M, Aujard F, Vannier G (1998) Influence of daylength on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus. Comp Biochem Physiol A Mol Integr Physiol 119:981–989
Perret M, Aujard F, Seguy M, Schilling A (2003) Olfactory bulbectomy modifies photic entrainment and circadian rhythms of body temperature and locomotion in a nocturnal primate. J Biol Rhythms 18:392–401
Petter JJ (1978) Ecological and physiological adaptations of five sympatric nocturnal lemurs to seasonal variations in food production. In: Chivers DJ, Herbert J (eds) Recent advances in primatology, vol. 1: behavior. Academic, New York, pp 211–223
Petter JJ, Albignac R, Rumpler Y (1977) Mammifères lémuriens (Primates prosimiens). Faune de Madagascar 44:1–513
Radespiel U, Cepok S, Zietemann V, Zimmermann E (1998) Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in Northwestern Madagascar. Am J Primatol 46:77–84
Radespiel U, Ehresmann P, Zimmermann E (2003) Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in Northwestern Madagascar. Am J Primatol 59:139–151
Randrianambinina B, Rakotondravony D, Radespiel U, Zimmermann E (2003) Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar. Primates 44:321–331
Reed KE, Fleagle JG (1995) Geographic and climatic control of primate diversity. Proc Nat Acad Sci USA 92:7874–7876
Roos C, Schmitz J, Zischler H (2004) Primate jumping genes elucidate strepsirrhine phylogeny. Proc Nat Acad Sci USA 101:10650–10654
Schmid J (1996) Oxygen consumption and torpor in mouse lemurs (Microcebus murinus and Microcebus myoxinus): preliminary results of a study in western Madagascar. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptions to the cold: tenth international hibernation symposium. University of New England Press, Armidale, pp 47–54
Schmid J (1998) Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809
Schmid J (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal 80:749–757
Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologia 123:175–183
Schmid J (2001) Daily torpor in free-ranging mouse gray lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22:1021–1031
Schmid J, Kappeler PM (1998) Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 43:125–132
Schmid J, Speakman JR (2000) Daily energy expenditure of the gray mouse lemur (Microcebus murinus): a small primate that uses torpor. J Comp Physiol B 170:633–641
Schmid J, Ruf T, Heldmaier G (2000) Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. J Comp Physiol B 170:59–68
Schülke O (2003) To breed or not to breed—food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55:11–21
Schülke O, Kappeler PM (2003) So near and yet so far: territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Anim Behav 65:331–343
Schülke O, Ostner J (2001) Predation on Lepilemur by the Harrier hawk and implications for sleeping site quality. Lemur News 6:5
Schülke O, Ostner J (2005) Big times for dwarfs—social organization, sexual selection, and cooperation in the cheirogaleids. Evol Anthropol 14:170–185
Schwab D (2000) A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf. myoxinus). Am J Primatol 51:41–60
Schwab D, Ganzhorn JU (2004) Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogaleids. Int J Primatol 25:307–330
Tattersall I (1982) The primates of Madagascar. Columbia University Press, New York
Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang, LCH (ed) Advances in comparative and environmental physiology. Springer, Berlin Heidelberg New York
Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E (2004) Social organization of the golden brown mouse lemur (Microcebus ravelobensis). Am J Phys Anthropol 123:40–51
Wright PC, Martin LB (1995) Predation, pollination and torpor in two nocturnal prosimians (Cheirogaleus major and Microcebus rufus) in the rain forest of Madagascar. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 45–65
Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U (1998) Sympatric mouse lemurs in north–west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatol (Basel) 69:106–114
Acknowledgements
We thank J. Fleagle for inspiring this review and P. Kappeler who drew our attention to the awkward socioecology of cathemeral and nocturnal lemurs and since then supported us in countless ways. We thank C. Borries, K. Dausmann, M. Eberle, J. Fleagle, J. Fietz, P. Kappeler and A. Koenig for long discussions and comments on the manuscript. K. Dausmann provided an unpublished manuscript, M. Eberle unpublished data and S. Arrigo-Nelson and P. Wright unpublished climate data from Ranomafana. During writing, both authors were supported by the Feodor Lynen-Fellowships of the Alexander von Humboldt Foundation and by the Stony Brook University.
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Schülke, O., Ostner, J. Physiological ecology of cheirogaleid primates: variation in hibernation and torpor. acta ethol 10, 13–21 (2007). https://doi.org/10.1007/s10211-006-0023-5
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DOI: https://doi.org/10.1007/s10211-006-0023-5