Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor

Abstract

The high expenditure of energy required for endogenous rewarming is one of the widely perceived disadvantages of torpor. However, recent evidence demonstrates that passive rewarming either by the increase of ambient temperature or by basking in the sun appears to be common in heterothermic birds and mammals. As it is presently unknown how radiant heat affects energy expenditure during rewarming from torpor and little is known about how it affects normothermic thermoregulation, we quantified the effects of radiant heat on body temperature and metabolic rate of the small (body mass 25 g) marsupial Sminthopsis macroura in the laboratory. Normothermic resting individuals exposed to radiant heat were able to maintain metabolic rates near basal levels (at 0.91 ml O2 g-1 h-1) and a constant body temperature down to an ambient temperature of 12 °C. In contrast, metabolic rates of individuals without access to radiant heat were 4.5-times higher at an ambient temperature of 12 °C and body temperature fell with ambient temperature. During radiant heat-assisted passive rewarming from torpor, animals did not employ shivering but appeared to maximise uptake of radiant heat. Their metabolic rate increased only 3.2-times with a 15-°C rise of body temperature (Q10=2.2), as predicted by Q10 effects. In contrast, during active rewarming shivering was intensive and metabolic rates showed an 11.6-times increase. Although body temperature showed a similar absolute change between the beginning and the end of the rewarming process, the overall energetic cost during active rewarming was 6.3-times greater than that during passive, radiant heat-assisted rewarming. Our study demonstrates that energetic models assuming active rewarming from torpor at low ambient temperatures can substantially over-estimate energetic costs. The low energy expenditure during passive arousal provides an alternative explanation as to why daily torpor is common in sunny regions and suggests that the prevalence of torpor in low latitudes may have been under-estimated in the past.

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Abbreviations

ADMR :

average daily metabolic rate

BMR :

basal metabolic rate

C :

apparent thermal conductance

MR :

metabolic rate

RMR :

resting metabolic rate

T a :

ambient temperature

T b :

body temperature

TMR :

torpor metabolic rate

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Acknowledgements

We thank Nereda Christian, Frank Falkenstein, Nicole Feay, Antje Seckerdieck, Chris Turbill and Wendy Westman for their comments on the manuscript and Bronwyn McAllan for providing experimental animals. This work was supported by a grant from the Australian Research Council. The UNE Animal Ethics Committee approved permits for animal experimentation.

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Correspondence to F. Geiser.

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Communicated by I.D. Hume

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Geiser, F., Drury, R.L. Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B 173, 55–60 (2003). https://doi.org/10.1007/s00360-002-0311-y

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Keywords

  • Arid zone
  • Thermoenergetics
  • Marsupial mammal
  • Sminthopsis macroura
  • Torpor