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

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Book cover Living in a Seasonal World

Abstract

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.

Cindy I. Canale and Danielle L. Levesque contributed equally to the study.

Cindy I. Canale is Claude Leon Postdoctoral Fellow at University of KwaZulu-Natal

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References

  • Angilletta MJJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E 2:861–881

    Article  Google Scholar 

  • 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 81:1004–1014

    Google Scholar 

  • 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 77:1102–1106

    Article  Google Scholar 

  • 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 79:1885–1890

    Article  Google Scholar 

  • 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 36:373–375

    Article  Google Scholar 

  • Boyles JG, Smit B, McKechnie AE (2011b) A new comparative metric for estimating heterothermy in endotherms. Phys Biochem Zool 84:115–123

    Article  Google Scholar 

  • Brice PH (2009) Thermoregulation in monotremes: riddles in a mosaic. Aust J Zool 57(3–4):255–263

    Article  Google Scholar 

  • 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 50:461–475

    Article  Google Scholar 

  • 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 36:376–379

    Article  Google Scholar 

  • Canale CI, Henry PY (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43:135–147

    Article  Google Scholar 

  • Canale CI, Henry PY (2011) Energetic costs of the immune response and torpor use in a primate. Funct Ecol 25:557–565

    Article  Google Scholar 

  • Canale CI, Perret M, Thery M, Henry PY (2011) Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol 214:551–560

    Article  PubMed  Google Scholar 

  • Canale CI, Perret M, Henry P-Y (2012) Torpor use during gestation and lactation in a heterothermic primate. Naturwissenschaften 99:159–163

    Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    PubMed  CAS  Google Scholar 

  • 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 75:466–470

    Article  Google Scholar 

  • Cossins AR, Barnes BM (1996) Southern discomfort. Nature 382:582–583

    Article  CAS  Google Scholar 

  • Daniel S, Korine C, Pinshow B (2010) The use of torpor in reproductive female hemprich’s long-eared bats (Otonycteris hemprichii). Physiol Biochem Zool 83:142–148

    Article  PubMed  Google Scholar 

  • Dausmann KH (2005) Measuring body temperature in the field-evaluation of external vs. implanted transmitters in a small mammal. J Therm Biol 30:195–202

    Article  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155

    Article  PubMed  Google Scholar 

  • Dausmann KH, Glos J, Heldmaier G (2009) Energetics of tropical hibernation. J Comp Physiol B 179:345–357

    Article  PubMed  CAS  Google Scholar 

  • 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 81–86

    Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  PubMed  CAS  Google Scholar 

  • Geiser F, Mzilikazi N (2011) Does torpor of elephant shrews differ from that of other heterothermic mammals? J Mammal 92:452–459

    Article  Google Scholar 

  • Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds—physiological variables and classification of torpor patterns. Physiol Zool 68:935–966

    Google Scholar 

  • 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 51:337–348

    Article  PubMed  Google Scholar 

  • 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 199–208

    Google Scholar 

  • 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 297–306

    Google Scholar 

  • 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 98:447–452

    Article  PubMed  Google Scholar 

  • 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–R959

    CAS  Google Scholar 

  • Gordon CJ (2009) Quantifying the instability of core temperature in rodents. J Therm Biol 34:213–219

    Article  Google Scholar 

  • 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 1–11

    Google Scholar 

  • Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Resp Physiol Neurobiol 141:317–329

    Article  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Article  PubMed  Google Scholar 

  • Kobbe S, Dausmann KH (2009) Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96:1221–1227

    Article  PubMed  CAS  Google Scholar 

  • Kobbe S, Ganzhorn JU, Dausmann KH (2011) Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). J Comp Physiol B 181:165–173

    Article  PubMed  Google Scholar 

  • Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219

    Article  PubMed  Google Scholar 

  • Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow–fast metabolic continuum. J Comp Physiol B 173:87–112

    PubMed  CAS  Google Scholar 

  • Lovegrove BG (2012) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev 87:128–162

    Article  PubMed  Google Scholar 

  • Lovegrove BG, Genin F (2008) Torpor and hibernation in a basal placental mammal, the Lesser Hedgehog Tenrec Echinops telfairi. J Comp Physiol B 178:691–698

    Article  PubMed  Google Scholar 

  • Lovegrove BG, Smith GA (2003) Is “nocturnal hypothermia” a valid physiological concept in small birds? A study on Bronze Mannikins (Spermestes cuccullatus). Ibis 145:547–557

    Article  Google Scholar 

  • 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 169:11–18

    Article  PubMed  CAS  Google Scholar 

  • 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 169:453–460

    Article  PubMed  CAS  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724

    Article  Google Scholar 

  • McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Integr Comp Biol 51:1–15

    Google Scholar 

  • 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 210:97–106

    Article  PubMed  Google Scholar 

  • Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285–296

    Article  PubMed  Google Scholar 

  • 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–R1062

    CAS  Google Scholar 

  • 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 365:945–959

    Article  Google Scholar 

  • 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 52:393–396

    Google Scholar 

  • Schmid J, Ganzhorn JU (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737–741

    Article  PubMed  CAS  Google Scholar 

  • Stawski C, Geiser F (2010) Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J Exp Biol 213:393–399

    Article  PubMed  CAS  Google Scholar 

  • 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–R547

    CAS  Google Scholar 

  • Stawski C, Turbill C, Geiser F (2009) Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179:433–441

    Article  PubMed  Google Scholar 

  • 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 232:285–294

    Article  Google Scholar 

  • Warnecke L, Geiser F (2009) Basking behaviour and torpor use in free-ranging Planigale gilesi. Aust J Zool 57:373–375

    Article  Google Scholar 

  • Wein J (2010) Effects of ambient temperature on tropical hibernation in the lesser hedgehog tenrec, Echinops telfairi. Ph.D. dissertation, Universität Hamburg, Hamburg

    Google Scholar 

  • Willis CKR (2007) An energy-based body temperature threshold between torpor and normothermia for small mammals. Physiol Biochem Zool 80:643–651

    Article  PubMed  Google Scholar 

  • 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 173:379–389

    Article  PubMed  CAS  Google Scholar 

  • Wilz M, Heldmaier G (2000) Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis. J Comp Physiol B 170:511–521

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, 3209, South Africa

    Cindy I. Canale, Danielle L. Levesque & Barry G. Lovegrove

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  1. Cindy I. Canale
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  2. Danielle L. Levesque
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  3. Barry G. Lovegrove
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Correspondence to Barry G. Lovegrove .

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Editors and Affiliations

  1. Forschungsinst. Wildtierkunde und, Ökologie, Veterinärmedizinische Universität Wien, Veterinärplatz 1, Wien, 1210, Austria

    Thomas Ruf

  2. Research Institute of Wildlife Ecology, Savoyenstr. 1, Vienna, 1160, Austria

    Claudia Bieber

  3. Research Institute of Wildlife Ecology, Savoyenstr. 1, Vienna, 1160, Austria

    Walter Arnold

  4. , Dept. of Behavioural Biology, University of Vienna, Althanstr. 14, Vienna, 1160, Austria

    Eva Millesi

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Canale, C.I., Levesque, D.L., Lovegrove, B.G. (2012). Tropical Heterothermy: Does the Exception Prove the Rule or Force a Re-Definition?. In: Ruf, T., Bieber, C., Arnold, W., Millesi, E. (eds) Living in a Seasonal World. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28678-0_3

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