Tropical Heterothermy: Does the Exception Prove the Rule or Force a Re-Definition?

  • Cindy I. Canale
  • Danielle L. Levesque
  • Barry G. Lovegrove


Recent interest in heterothermy in the tropics and the subtropics has raised issues with the existing definitions of torpor. The current methods used to distinguish and define patterns of heterothermy are insufficient in face of the numerous forms of torpor expression and high daily variation in normothermic body temperature (T b) observed in species inhabiting the tropics. Tropical heterothermy often occurs at highly variable ambient temperatures that may lead to a continuum between hibernation, daily torpor and normothermia with no clear distinction between states. While we do not seek to redefine torpor in this review, by listing torpor patterns that fall outside the usual categories (the exceptions to the rule), we discuss these thermoregulatory behaviours in terms of the energetics and evolution of heterothermy under warm climates.


Basal Metabolic Rate Mouse Lemur Torpor Bout Daily Torpor Periodic Arousal 
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.



The authors thank Prof. Fritz Geiser for suggested improvements to the manuscript. The research was financed by incentive grants from the University of KwaZulu-Natal, the National Research Foundation, South Africa and a Claude Leon Foundation Postdoctoral Fellowship to CIC and a post-graduate scolarship from National Science and Engineering Research Council (Canada) to DLL.


  1. Angilletta MJJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E 2:861–881CrossRefGoogle Scholar
  2. Arlettaz R, Ruchet RC, Aeschimann J, Brun E, Genoud M, Vogel P (2000) Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis. Ecology 81:1004–1014Google Scholar
  3. Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ, Wilkinson L, Brigham RM (1996) Can external radiotransmitters be used to assess body temperature and torpor in bats? J Mammal 77:1102–1106CrossRefGoogle Scholar
  4. Barclay RMR, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79:1885–1890CrossRefGoogle Scholar
  5. Boyles JG, Smit B, McKechnie AE (2011a) Does use of the torpor cut-off method to analyze variation in body temperature cause more problems than it solves? J Therm Biol 36:373–375CrossRefGoogle Scholar
  6. Boyles JG, Smit B, McKechnie AE (2011b) A new comparative metric for estimating heterothermy in endotherms. Phys Biochem Zool 84:115–123CrossRefGoogle Scholar
  7. Brice PH (2009) Thermoregulation in monotremes: riddles in a mosaic. Aust J Zool 57(3–4):255–263CrossRefGoogle Scholar
  8. Brice PH, Grigg GC, Beard LA, Donovan JA (2002) Patterns of activity and inactivity in echidnas (Tachyglossus aculeatus) free-ranging in a hot dry climate: correlates with ambient temperature, time of day and season. Aust J Zool 50:461–475CrossRefGoogle Scholar
  9. Brigham R, Willis C, Geiser F, Mzilikazi N (2011) Baby in the bathwater: should we abandon the use of body temperature thresholds to quantify expression of torpor? J Therm Biol 36:376–379CrossRefGoogle Scholar
  10. Canale CI, Henry PY (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43:135–147CrossRefGoogle Scholar
  11. Canale CI, Henry PY (2011) Energetic costs of the immune response and torpor use in a primate. Funct Ecol 25:557–565CrossRefGoogle Scholar
  12. Canale CI, Perret M, Thery M, Henry PY (2011) Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol 214:551–560PubMedCrossRefGoogle Scholar
  13. Canale CI, Perret M, Henry P-Y (2012) Torpor use during gestation and lactation in a heterothermic primate. Naturwissenschaften 99:159–163Google Scholar
  14. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181PubMedGoogle Scholar
  15. Cory Toussaint D, McKechnie AE, van der Merwe M (2010) Heterothermy in free-ranging male Egyptian free-tailed bats (Tadarida aegyptiaca) in a subtropical climate. Mammal Biol 75:466–470CrossRefGoogle Scholar
  16. Cossins AR, Barnes BM (1996) Southern discomfort. Nature 382:582–583CrossRefGoogle Scholar
  17. Daniel S, Korine C, Pinshow B (2010) The use of torpor in reproductive female hemprich’s long-eared bats (Otonycteris hemprichii). Physiol Biochem Zool 83:142–148PubMedCrossRefGoogle Scholar
  18. Dausmann KH (2005) Measuring body temperature in the field-evaluation of external vs. implanted transmitters in a small mammal. J Therm Biol 30:195–202CrossRefGoogle Scholar
  19. 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
  20. Dausmann KH, Glos J, Heldmaier G (2009) Energetics of tropical hibernation. J Comp Physiol B 179:345–357PubMedCrossRefGoogle Scholar
  21. Geiser F (1996) Torpor in reproductive endotherms. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold, 10th international hibernation symposium, University of New England Press, pp 81–86Google Scholar
  22. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274PubMedCrossRefGoogle Scholar
  23. Geiser F, Mzilikazi N (2011) Does torpor of elephant shrews differ from that of other heterothermic mammals? J Mammal 92:452–459CrossRefGoogle Scholar
  24. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds—physiological variables and classification of torpor patterns. Physiol Zool 68:935–966Google Scholar
  25. Geiser F, Stawski C (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr Comp Biol 51:337–348PubMedCrossRefGoogle Scholar
  26. Geiser F, Drury RL, Körtner G, Turbill C, Pavey CR, Brigham RM (2004) Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. In: Barnes BM, Carey HV (eds) Life in the cold. Evolution, mechanisms, adaptation, and application, vol 27. Biological Papers of the University of Alaska, University of Alaska, Fairbanks, pp 199–208Google Scholar
  27. Geiser F, Christian N, Cooper CE, Körtner G, McAllan BM, Pavey CR, Turner JM, Warnecke L, Willis CKR, Brigham M (2008) Torpor in marsupials: recent advances. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: hibernation, torpor and cryobiology. Interpack Books, Pietermaritzburg, pp 297–306Google Scholar
  28. Geiser F, Stawski C, Bondarenco A, Pavey CR (2011) Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals? Naturwissenschaften 98:447–452PubMedCrossRefGoogle Scholar
  29. Giroud S, Perret M, Gilbert C, Zahariev A, Goudable J, Le Maho Y, Oudart H, Momken I, Aujard F, Blanc S (2009) Dietary palmitate and linoleate oxidations, oxidative stress, and DNA damage differ according to season in mouse lemurs exposed to a chronic food deprivation. Am J Physiol Reg I 297:R950–R959Google Scholar
  30. Gordon CJ (2009) Quantifying the instability of core temperature in rodents. J Therm Biol 34:213–219CrossRefGoogle Scholar
  31. Grigg GC (2004) An evolutionary framework for studies of hibernation and short term torpor. In: Barnes BM, Carey HV (eds) Life in the cold. Evolution, mechanisms, adaptation, and application, vol 27. Biological Papers of the University of Alaska, University of Alaska, Fairbanks, pp 1–11Google Scholar
  32. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Resp Physiol Neurobiol 141:317–329CrossRefGoogle Scholar
  33. Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179PubMedCrossRefGoogle Scholar
  34. Kobbe S, Dausmann KH (2009) Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96:1221–1227PubMedCrossRefGoogle Scholar
  35. Kobbe S, Ganzhorn JU, Dausmann KH (2011) Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). J Comp Physiol B 181:165–173PubMedCrossRefGoogle Scholar
  36. Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219PubMedCrossRefGoogle Scholar
  37. Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow–fast metabolic continuum. J Comp Physiol B 173:87–112PubMedGoogle Scholar
  38. Lovegrove BG (2012) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev 87:128–162PubMedCrossRefGoogle Scholar
  39. Lovegrove BG, Genin F (2008) Torpor and hibernation in a basal placental mammal, the Lesser Hedgehog Tenrec Echinops telfairi. J Comp Physiol B 178:691–698PubMedCrossRefGoogle Scholar
  40. Lovegrove BG, Smith GA (2003) Is “nocturnal hypothermia” a valid physiological concept in small birds? A study on Bronze Mannikins (Spermestes cuccullatus). Ibis 145:547–557CrossRefGoogle Scholar
  41. Lovegrove BG, Kortner G, Geiser F (1999a) The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol B 169:11–18PubMedCrossRefGoogle Scholar
  42. Lovegrove BG, Lawes MJ, Roxburgh L (1999b) Confirmation of pleisiomorphic daily torpor in mammals: the round-eared elephant shrew Macroscelides proboscideus (Macroscelidea). J Comp Physiol B 169:453–460PubMedCrossRefGoogle Scholar
  43. Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New YorkGoogle Scholar
  44. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724CrossRefGoogle Scholar
  45. McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Integr Comp Biol 51:1–15Google Scholar
  46. McKechnie AE, Chetty K, Lovegrove BG (2007) Phenotypic flexibility in the basal metabolic rate of laughing doves: responses to short-term thermal acclimation. J Exp Biol 210:97–106PubMedCrossRefGoogle Scholar
  47. Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285–296PubMedCrossRefGoogle Scholar
  48. Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am J Physiol Reg I 282:R1054–R1062Google Scholar
  49. Roth TC, Rattenborg NC, Pravosudov VV (2010) The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation. Philos Trans Royal Soc B Biol Sci 365:945–959CrossRefGoogle Scholar
  50. Schleucher E, Prinzinger R (2006) Heterothermia and torpor in birds: highly specialized physiological ability or just deep “nocturnal hypothermia”? The limitations of terminology. Acta Zool Sinica 52:393–396Google Scholar
  51. Schmid J, Ganzhorn JU (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737–741PubMedCrossRefGoogle Scholar
  52. Stawski C, Geiser F (2010) Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J Exp Biol 213:393–399PubMedCrossRefGoogle Scholar
  53. Stawski C, Geiser F (2011) Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics? Am J Physiol Reg I 301:R542–R547Google Scholar
  54. Stawski C, Turbill C, Geiser F (2009) Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179:433–441PubMedCrossRefGoogle Scholar
  55. Stephenson PJ, Racey PA (1994) Seasonal variation in resting metabolic rate and body temperature of streaked tenrecs, Hemicentetes nigriceps and H. semispinosus (Insectivora: Tenrecidae). J Zool 232:285–294CrossRefGoogle Scholar
  56. Warnecke L, Geiser F (2009) Basking behaviour and torpor use in free-ranging Planigale gilesi. Aust J Zool 57:373–375CrossRefGoogle Scholar
  57. Wein J (2010) Effects of ambient temperature on tropical hibernation in the lesser hedgehog tenrec, Echinops telfairi. Ph.D. dissertation, Universität Hamburg, HamburgGoogle Scholar
  58. Willis CKR (2007) An energy-based body temperature threshold between torpor and normothermia for small mammals. Physiol Biochem Zool 80:643–651PubMedCrossRefGoogle Scholar
  59. Willis CKR, Brigham RM (2003) Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature. J Comp Physiol B 173:379–389PubMedCrossRefGoogle Scholar
  60. Wilz M, Heldmaier G (2000) Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis. J Comp Physiol B 170:511–521PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Cindy I. Canale
    • 1
  • Danielle L. Levesque
    • 1
  • Barry G. Lovegrove
    • 1
  1. 1.School of Biological and Conservation SciencesUniversity of KwaZulu-NatalScottsvilleSouth Africa

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