Afrotropical Heterothermy: A Continuum of Possibilities

  • Kathrin H. Dausmann
  • Julia Nowack
  • Susanne Kobbe
  • Nomakwezi Mzilikazi
Chapter

Abstract

The three closely related primate species Cheirogaleus medius , Microcebus griseorufus , and Galago moholi employ a spectrum of thermoregulatory responses to environmental bottlenecks. C. medius is an obligate hibernator, M. griseorufus shows extreme flexibility in patterns of heterothermy, ranging from daily torpor to prolonged torpor and hibernation, whereas G. moholi becomes heterothermic under extremely adverse conditions only. To gain further insights into the proximate and ultimate factors that favour and constrain torpor use in small primates, we compared the characteristics of M. griseorufus, C. medius and G. moholi as well as the prevailing ambient conditions where each of the species are found. Our analyses did not reveal any fundamental differences in the physiological parameters of heterothermy between the three species that would indicate different underlying physiological mechanisms. Instead we propose that the different modes of reproduction, connected to climatic differences, are the key ultimate causes of the differences in thermoregulatory strategies between the three species. We suggest that the common ancestor of the strepsirrhine primates was a heterothermic endotherm and that the ability to express daily torpor/hibernation is closely linked to ecological and evolutionary forces that favour and prioritise activities such as reproduction.

Keywords

Mouse Lemur Torpor Bout Daily Torpor Prolonged Torpor Thermoregulatory Strategy 
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.

References

  1. Bearder SK (1969) Territorial and intergroup behaviour of the lesser bushbaby, Galago senegalensis moholi, in semi-natural conditions and in the field. Dissertation, University of the Witwatersrand, JohannesburgGoogle Scholar
  2. Bearder SK, Martin RD (1980) Acacia gum and its use by bushbabyies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1(2):103–128CrossRefGoogle Scholar
  3. Dausmann KH (2008) Hypometabolism in primates: torpor and hibernation. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor, hibernation and cryobiology. University of KwaZulu-Natal, Pietermaritzburg, pp 327–336Google Scholar
  4. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429(6994):825–882PubMedCrossRefGoogle Scholar
  5. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175(3):147–155PubMedCrossRefGoogle Scholar
  6. Dausmann KH, Glos J, Heldmaier G (2009) Energetics of tropical hibernation. J Comp Physiol B 179(3):345–357PubMedCrossRefGoogle Scholar
  7. Farmer CG (2000) Parental care: the key to understanding endothermy and other convergent features in birds and mammals. Am Nat 155(3):326–334PubMedCrossRefGoogle Scholar
  8. Fietz J, Dausmann KH (2003) Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol 74(5–6):246–258PubMedCrossRefGoogle Scholar
  9. Fietz J, Dausmann KH (2006) Big is beautiful: fat storage and hibernation as a strategy to cope with marked seasonality in the fat-tailed dwarf lemus (Cheirogaleus medius). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, Berlin, pp 97–111Google Scholar
  10. Geiser F (1988) Daily torpor and thermoregulation in antechinus (Marsupialia): influence of body mass, season, development, reproduction, and sex. Oecologia 77(3):395–399CrossRefGoogle Scholar
  11. Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol A 150(2):176–180CrossRefGoogle Scholar
  12. Génin F (2008) Life in unpredictable environments: first investigation of the natural history of M. griseorufus. Int J Primatol 29(2):303–321CrossRefGoogle Scholar
  13. Génin F (2010) Who sleeps with whom? Sleeping association and socio-territoriality in Microcebus griseorufus. J Mammal 91(4):942–951CrossRefGoogle Scholar
  14. Kobbe S, Dausmann KH (2009) Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96(10):1221–1227PubMedCrossRefGoogle Scholar
  15. Kobbe S, Dausmann KH, Ganzhorn JU (2011) Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). J Comp Physiol B 181(1):165–173PubMedCrossRefGoogle Scholar
  16. Lahann P, Dausmann KH (2011) Live fast, die young: flexibility of life-history traits in the fat-tailed dwarf lemur (Cheirogaleus medius). Behav Ecol Sociobiol 65(2):381–390CrossRefGoogle Scholar
  17. Lovegrove B (2011) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev. doi: 10.1111/j.1469-185X.2011.00188.x PubMedGoogle Scholar
  18. Lovegrove B (2012) A single origin of heterothermy in mammals. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer, BerlinGoogle Scholar
  19. Lovegrove BG, Génin F (2008) Torpor and hibernation in a basal placental mammal, the lesser hedgehog tenrec (Echinops telfairi). J Comp Physiol B 178(6):691–698PubMedCrossRefGoogle Scholar
  20. McKechnie AE, Mzilikazi N (2011). Heterothermy in Afrotropical mammals and birds: a review. Integr Comp Biol:1–15. doi: 10.1093/icb/icr035
  21. Mzilikazi N, Masters JC, Lovegrove B (2006) Lack of torpor in free-ranging southern lesser galagos, Galago moholi: ecological and physiological considerations. Folia Primatol 77(6):465–476PubMedCrossRefGoogle Scholar
  22. Nicol SC, Andersen NA (1996) Hibernation in the echidna: not an adaptation to cold? In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold. University of New England Press, Armidale, pp 7–12Google Scholar
  23. Nowack J, Mzilikazi N, Dausmann KH (2010) Torpor on demand: heterothermy in the non-lemur primate Galago moholi. PLoS One 5(5):e10797. doi: 10.1371/journal.pone.0010797 PubMedCrossRefGoogle Scholar
  24. Nowack J, Mzilikazi N, Dausmann KH (submitted) Surviving the cold and dry period in Africa: behavioural thermoregulation as an alternative to heterothermy in Galago moholi Google Scholar
  25. Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84(1):28–32PubMedCrossRefGoogle Scholar
  26. Pullen SL, Bearder SK, Dixson AF (2000) Preliminary observations on sexual behavior and the mating system in free-ranging lesser galagos (Galago moholi). Am J Primatol 51(1):79–88PubMedCrossRefGoogle Scholar
  27. Rakotondranary SJ, Hapke A, Ganzhorn JU (2011) Distribution and morphological variation of Microcebus spp. along an environmental gradient in southeastern Madagascar. Int J Primatol 32(5):1037–1057CrossRefGoogle Scholar
  28. Ratovonamana RY, Rajeriarison C, Roger E, Kiefer I, Ganzhorn JU (submitted). Impact of livestock grazing on vegetation characteristics in southwest Madagascar. Plant Ecol EvolGoogle Scholar
  29. Schmid J (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal 80(3):749–757CrossRefGoogle Scholar
  30. Schmid J, Ruf J, 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(1):59–68PubMedCrossRefGoogle Scholar
  31. Scholes RJ, Walker BH (1993) An African savannah: synthesis of the Nylsvlei study. Cambridge University Press, CambridgeGoogle Scholar
  32. Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B 278(1723):3355–3363PubMedCrossRefGoogle Scholar
  33. Wein J (2010) Effects of ambient temperature on tropical hibernation in the lesser hedgehog tenrec, Echinops telfairi. Dissertation, University Hamburg, GermanyGoogle Scholar
  34. Wilde CJ, Knight CH, Racey PA (1999) Influence of torpor on milk protein composition and secretion in lactating bats. J Exp Zool 284(1):35–41PubMedCrossRefGoogle Scholar
  35. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. AJPA 110(29):31–72Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Kathrin H. Dausmann
    • 1
  • Julia Nowack
    • 1
  • Susanne Kobbe
    • 1
  • Nomakwezi Mzilikazi
    • 2
  1. 1.Department of Animal Ecology and Conservation, Biocentre GrindelUniversity of HamburgHamburgGermany
  2. 2.Centre for African Conservation Ecology, Department of ZoologyNelson Mandela Metropolitan UniversityPort ElizabethSouth Africa

Personalised recommendations