acta ethologica

, Volume 10, Issue 1, pp 13–21 | Cite as

Physiological ecology of cheirogaleid primates: variation in hibernation and torpor

Original Article

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.

Keywords

Hibernation Torpor Ambient temperature Seasonality Cheirogaleidae 

Notes

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 K. Dausmann provided an unpublished manuscript, M. Eberle unpublished data and S. Arrigo-Nelson and P. Wright unpublished climate data from Ranomafana.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.

References

  1. Atsalis S (1999a) Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. Int J Primatol 20:193–229CrossRefGoogle Scholar
  2. Atsalis S (1999b) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. Int J Primatol 20:883–910CrossRefGoogle Scholar
  3. 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 51:61–78PubMedCrossRefGoogle Scholar
  4. 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 168:540–548PubMedCrossRefGoogle Scholar
  5. Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female mouse lemur (Microcebus murinus). Am J Primatol 37:317–324CrossRefGoogle Scholar
  6. Dammhahn M, Kappeler PM (2005) Social system of Microcebus berthae—the world’s smallest primate. Int J Primatol 26:407–435CrossRefGoogle Scholar
  7. 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 41–47Google Scholar
  8. Dausmann KH, Glos J, Heldmaier G (2001) Social hibernation in a tropical primate species (Cheirogaleus medius). Advances in Ethology 36:140Google Scholar
  9. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826PubMedCrossRefGoogle Scholar
  10. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155PubMedCrossRefGoogle Scholar
  11. Eberle M, Kappeler PM (2002) Mouse lemurs in space and time: a test of the socioecological model. Behav Ecol Sociobiol 51:131–139CrossRefGoogle Scholar
  12. 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 57:77–90CrossRefGoogle Scholar
  13. Fietz J (1998) Body mass in wild Microcebus murinus over the dry season. Folia Primatol 69:183–190CrossRefGoogle Scholar
  14. Fietz J, Ganzhorn JU (1999) Feeding ecology of the hibernation primate Cheirogaleus medius: how does it get so fat? Oecologia 121:157–164CrossRefGoogle Scholar
  15. Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int J Primatol 19:785–796CrossRefGoogle Scholar
  16. 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 75–89Google Scholar
  17. 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 132–144Google Scholar
  18. Genin F, Perret M (2000) Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiol Behav 71:315–321PubMedCrossRefGoogle Scholar
  19. Genin F, Perret M (2003) Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81PubMedCrossRefGoogle Scholar
  20. 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–R818PubMedGoogle Scholar
  21. Goodman SM (2003) Predation on lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1221–1228Google Scholar
  22. Groves CP (2000) The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. Int J Primatol 21:943–962CrossRefGoogle Scholar
  23. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DCGoogle Scholar
  24. 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 130–139Google Scholar
  25. 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 545–548Google Scholar
  26. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and torpor in mammals. Respir Biol Neurobiol 141:317–329CrossRefGoogle Scholar
  27. 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 41–73Google Scholar
  28. Kappeler PM (2000a) Lemur origins: rafting by groups of hibernators? Folia Primatol 71:422–425PubMedCrossRefGoogle Scholar
  29. Kappeler PM (2000b) Ecologie des microcebes. Primatologie 3:145–171Google Scholar
  30. 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 71:3–26Google Scholar
  31. 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 235:311–322CrossRefGoogle Scholar
  32. Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow–fast continuum. J Comp Physiol B 173:87–112PubMedGoogle Scholar
  33. Lymann CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic, New YorkGoogle Scholar
  34. Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Princeton University Press, PrincetonGoogle Scholar
  35. 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 49:265–280PubMedCrossRefGoogle Scholar
  36. 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 139–158Google Scholar
  37. Müller AE (1999c) The social organisation of the fat-tailed dwarf lemur, Cheirogaleus medius (Lemuriformes; Primates). Ph.D. thesis, University of Zürich, ZürichGoogle Scholar
  38. Ortmann S, Heldmaier G, Schmid J (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32PubMedCrossRefGoogle Scholar
  39. Pastorini J, Thalmann U, Martin RD (2003) A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Nat Acad Sci USA 100:5879–5884PubMedCrossRefGoogle Scholar
  40. Perret M (1998) Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus murinus). J Mammal 79:1093–1102CrossRefGoogle Scholar
  41. 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 119:981–989PubMedCrossRefGoogle Scholar
  42. 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 18:392–401PubMedCrossRefGoogle Scholar
  43. 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 211–223Google Scholar
  44. Petter JJ, Albignac R, Rumpler Y (1977) Mammifères lémuriens (Primates prosimiens). Faune de Madagascar 44:1–513Google Scholar
  45. 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 46:77–84PubMedCrossRefGoogle Scholar
  46. 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 59:139–151PubMedCrossRefGoogle Scholar
  47. 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 44:321–331PubMedCrossRefGoogle Scholar
  48. Reed KE, Fleagle JG (1995) Geographic and climatic control of primate diversity. Proc Nat Acad Sci USA 92:7874–7876PubMedCrossRefGoogle Scholar
  49. Roos C, Schmitz J, Zischler H (2004) Primate jumping genes elucidate strepsirrhine phylogeny. Proc Nat Acad Sci USA 101:10650–10654PubMedCrossRefGoogle Scholar
  50. 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 47–54Google Scholar
  51. Schmid J (1998) Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809CrossRefGoogle Scholar
  52. Schmid J (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal 80:749–757CrossRefGoogle Scholar
  53. Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologia 123:175–183CrossRefGoogle Scholar
  54. Schmid J (2001) Daily torpor in free-ranging mouse gray lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22:1021–1031CrossRefGoogle Scholar
  55. 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 43:125–132CrossRefGoogle Scholar
  56. 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 170:633–641PubMedCrossRefGoogle Scholar
  57. 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 170:59–68PubMedCrossRefGoogle Scholar
  58. 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 55:11–21CrossRefGoogle Scholar
  59. 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 65:331–343CrossRefGoogle Scholar
  60. Schülke O, Ostner J (2001) Predation on Lepilemur by the Harrier hawk and implications for sleeping site quality. Lemur News 6:5Google Scholar
  61. Schülke O, Ostner J (2005) Big times for dwarfs—social organization, sexual selection, and cooperation in the cheirogaleids. Evol Anthropol 14:170–185CrossRefGoogle Scholar
  62. Schwab D (2000) A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf. myoxinus). Am J Primatol 51:41–60PubMedCrossRefGoogle Scholar
  63. Schwab D, Ganzhorn JU (2004) Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogaleids. Int J Primatol 25:307–330CrossRefGoogle Scholar
  64. Tattersall I (1982) The primates of Madagascar. Columbia University Press, New YorkGoogle Scholar
  65. 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 YorkGoogle Scholar
  66. 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 123:40–51PubMedCrossRefGoogle Scholar
  67. 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 45–65Google Scholar
  68. 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) 69:106–114CrossRefGoogle Scholar

Copyright information

© Springer-Verlag and ISPA 2006

Authors and Affiliations

  1. 1.Integrative Primate Socio-Ecology GroupMax-Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.Department of AnthropologyStony Brook UniversityNew YorkUSA

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