Abstract
Marsupials, unlike placental mammals, are believed to be unable to increase heat production and thermal performance after cold-acclimation. It has been suggested that this may be because marsupials lack functional brown fat, a thermogenic tissue, which proliferates during cold-acclimation in many placentals. However, arid zone marsupials have to cope with unpredictable, short-term and occasionally extreme changes in environmental conditions, and thus they would benefit from an appropriate physiological response. We therefore investigated whether a sequential two to four week acclimation in Sminthopsis macroura (body mass approx. 25 g) to both cold (16°C) and warm (26°C) ambient temperatures affects the thermal physiology of the species. Cold-acclimated S. macroura were able to significantly increase maximum heat production (by 27%) and could maintain a constant body temperature at significantly lower effective ambient temperatures (about 9°C lower) than when warm-acclimated. Moreover, metabolic rates during torpor were increased following cold-acclimation in comparison to warm-acclimation. Our study shows that, despite the lack of functional brown fat, short-term acclimation can have significant effects on thermoenergetics of marsupials. It is likely that the rapid response in S. macroura reflects an adaptation to the unpredictability of the climate in their habitat.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ADMR:
-
average daily metabolic rate
- BMR:
-
basal metabolic rate
- C :
-
apparent thermal conductance
- CA:
-
cold-acclimation
- HPmax :
-
maximum cold-induced heat production
- MR:
-
metabolic rate
- RMR:
-
resting metabolic rate
- T a :
-
ambient temperature
- T b :
-
body temperature
- TMR:
-
torpor metabolic rate
- WA:
-
warm-acclimation
References
Clements F, Hope P, Daniels C, Chapman I, Wittert G (1998) Thermogenesis in the marsupial Sminthopsis crassicaudata: effect of catecholamines and diet. Aust J Zool 46:381–390
Dawson TJ (1989) Responses to cold of monotremes and marsupials. In: Wang LCH (ed) Animal adaptation to cold. Springer, Berlin Heidelberg New York, pp 255–288
Dawson TJ, Olsen JM (1988) Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials. Comp Biochem Physiol 89A:85–91
Eldershaw TPD, Ye J, Clark MG, Colquhoun EQ (1996) Vasoconstrictor-induced thermogenic switching in endotherm and ectotherm muscle. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: 10th international hibernation symposium. UNE Press, Armidale, Australia, pp 311–317
Feist DD, White RG (1989) Terrestrial mammals in cold. In: Wang LCH (ed) Animal adaptation to cold. Springer, Berlin Heidelberg New York, pp 327–360
Geiser F (2003) Thermal biology and energetics of carnivorous marsupials. In: Jones M, Dickman C, Archer M (eds) Predators with pouches: the biology of carnivorous marsupials. CSIRO, Melbourne, pp 238–253
Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344
Geiser F, Song X, Körtner G (1996) The effect of He-O2 exposure on metabolic rate, thermoregulation and thermal conductance during normothermia and daily torpor. J Comp Physiol B 166:190–196
Geiser F, Körtner G, Schmidt I (1998) Leptin increases energy expenditure of a marsupial by inhibition of daily torpor. Am J Physiol 275:R1627–R1632
Hinds DS, MacMillen RE (1984) Energy scaling in marsupials and eutherians. Science 225:335–336
Hinds DS, Baudinette RV, MacMillen RE, Halpern EA (1993) Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol 182:41–56
Holloway JC, Geiser F (2001a) Effects of helium/oxygen and temperature on aerobic metabolism in the marsupial sugar glider, Petaurus breviceps. Physiol Biochem Zool 74:219–225
Holloway JC, Geiser F (2001b) Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps. J Comp Physiol B 171:643–650
Hudson JW, Scott IM (1979) Daily torpor in the laboratory mouse Mus musculus var. albino. Physiol Zool 52:205–218
Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge
Lovegrove BG (1996) The low basal metabolic rates of marsupials: the influence of torpor and zoogeography. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: 10th international hibernation symposium. UNE Press, Armidale, Australia, pp 141–151
MacMillen RE, Nelson JE (1969) Bioenergetics and body size in dasyurid marsupials. Am J Physiol 217:1246–1251
May EL (2003) Shivering and nonshivering thermogenesis in a marsupial: the response to cold acclimation in the kowari, Dasyuroides byrnei. J Thermal Biol (in press)
Menkhurst P, Knight F (2001) A field guide to the mammals of Australia. Oxford University Press, Melbourne
Merritt JF, Zegers DA, Rose LR (2001) Seasonal thermogenesis of southern flying squirrels (Glaucomys volans). J Mammal 82:51–64
Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimation. J Exp Biol 205:2697–2703
Nicol SC, Pavlides D, Andersen NA (1997) Nonshivering thermogenesis in marsupials: absence of thermogenic response to 3-adrenergic agonists. Comp Biochem Physiol 117A:399–405
Opazo JC, Nespolo RF, Bozinovic F (1999) Arousal from torpor in the Chilean mouse-opossum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp Biochem Physiol 123A:393–397
Rose RW, West AK, Ye J-M, McCormack GH, Colquhoun EQ (1999) Nonshivering thermogenesis in a marsupial (the Tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699–704
Rosenmann M, Morrison P (1974) Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-O2. Am J Physiol 226:490–497
Smith BK, Dawson TJ (1985) Use of helium-oxygen to examine the effect of cold acclimation on the summit metabolism of a marsupial, Dasyuroides byrnei. Comp Biochem Physiol 81A:445–449
Song X, Körtner G, Geiser F (1995) Reduction of metabolic rate and thermoregulation during daily torpor. J Comp Physiol B 165:291–297
Wang D, Sun R, Wang Z, Liu J (1999) Effects of temperature and photoperiod on thermogenesis in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). J Comp Physiol B 169:77–83
Withers KW, Hulbert AJ (1988) Cold acclimation in the marsupial Antechinus stuartii: thyroid function and metabolic rate. Aust J Zool 36:421–427
Withers PC (1977) Measurements of V̇O2, V̇CO2 and evaporative water loss with a flow through mask. J Appl Physiol 42:120–123
Wunder BA, Gettinger RD (1996) Effects of body mass and temperature acclimation on the nonshivering thermogenic response of small mammals. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: 10th international hibernation symposium. UNE Press, Armidale, Australia, pp 131–139
Acknowledgements
We thank Wendy Westman for help with experiments. Supported by a grant from the Australian Research Council to F.G. and the Chinese Academy of the Sciences to D.-H.W.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume
Rights and permissions
About this article
Cite this article
Geiser, F., Drury, R.L., McAllan, B.M. et al. Effects of temperature acclimation on maximum heat production, thermal tolerance, and torpor in a marsupial. J Comp Physiol B 173, 437–442 (2003). https://doi.org/10.1007/s00360-003-0352-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-003-0352-x