Abstract
Physiological mechanisms causing reduction of metabolic rate during torpor in heterothermic endotherms are controversial. The original view that metabolic rate is reduced below the basal metabolic rate because the lowered body temperature reduces tissue metabolism has been challenged by a recent hypothesis which claims that metabolic rate during torpor is actively downregulated and is a function of the differential between body temperature and ambient temperature, rather than body temperature per se. In the present study, both the steady-state metabolic rate and body temperature of torpid stripe-faced dunnarts, Sminthopsis macroura (Dasyuridae: Marsupialia), showed two clearly different phases in response to change of air temperature. At air temperatures between 14 and 30°C, metabolic rate and body temperature decreased with air temperature, and metabolic rate showed an exponential relationship with body temperature (r 2=0.74). The Q 10 for metabolic rate was between 2 and 3 over the body temperature range of 16 to 32°C. The difference between body temperature and air temperature over this temperature range did not change significantly, and the metabolic rate was not related to the difference between body temperature and air temperature (P=0.35). However, the apparent conductance decreased with air temperature. At air temperatures below 14°C, metabolic rate increased linearly with the decrease of air temperature (r 2=0.58) and body temperature was maintained above 16°C, largely independent of air temperature. Over this air temperature range, metabolic rate was positively correlated with the difference between body temperature and air temperature (r 2=0.61). Nevertheless, the Q 10 for metabolic rate between normothermic and torpid thermoregulating animals at the same air temperature was also in the range of 2–3. These results suggest that over the air temperature range in which body temperature of S. macroura was not metabolically defended, metabolic rate during daily torpor was largely a function of body temperature. At air temperatures below 14°C, at which the torpid animals showed an increase of metabolic rate to regulate body temperature, the negative relationship between metabolic rate and air temperature was a function of the differential between body temperature and air temperature as during normothermia. However, even in thermoregulating animals, the reduction of metabolic rate from normothermia to torpor at a given air temperature can also be explained by temperature effects.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Abbreviations
- BM :
-
body mass
- BMR :
-
basal metabolic rate
- C :
-
apparent conductance
- MR :
-
metabolic rate
- RMR :
-
resting metabolic rate
- RQ :
-
respiratory quotient
- T a :
-
air temperature
- T b :
-
body temperature
- T lc :
-
lower critical temperature
- T tc :
-
critical air temperature during torpor
- TMR :
-
metabolic rate during torpor
- TNZ :
-
thermoneutral zone
- αT :
-
difference between body temperature and air temperature
- VO2 :
-
rate of oxygen consumption
References
Aloia RC, Raison JK (1989) Membrane function in mammalian hibernation. Biochim Biophys Acta 988: 123–146
Doran HE, Guise JWB (1984) Single equation methods in econometrics: applied regression analysis. University of New England Press, Armidale, Australia
Davis WH, Reite OB (1967) Responses of bats from temperate regions to changes in ambient temperature. Biol Bull 132: 320–328
Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158: 25–37
Geiser F (1993) Metabolic rate reduction during hibernation. In: Carey C et al. (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 549–552
Geiser F, McMurchie EJ (1984) Differences in the thermotropic behaviour of mitochondrial membrane respiratory enzymes from homeothermic and heterothermic endotherms. J Comp Physiol B 155: 125–133
Geiser F, Baudinette RV (1985) The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia). J Comp Physiol B 156: 129–134
Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157: 335–344
Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61: 442–449
Hainsworth FR, Wolf LL (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168: 368–369
Heldmaier G, Ruf T (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162:696–706
Heller HC, Colliver GW (1972) CNS regulation of body temperature during hibernation. Am J Physiol 227: 583–589
Heller HC, Hammel HT (1972) CNS control of body temperature during hibernation. Comp Biochem Physiol 41A: 349–359
Henshaw RE (1968) Thermoregulation during hibernation: application of Newton's law of cooling. J Theor Biol 20: 79–90
Hock RJ (1951) The metabolic rates and body temperatures of bats. Biol Bull 101: 289–299
Kayser C (1964) La dépense d'énergie des mammiferes en hibernation. Arch Sci Physiol 18: 137–150
Lyman CP, Willis JS, Malan A, Wang LCH (eds) (1982) Hibernation and torpor in mammals and birds. Academic Press, New York
Malan A (1986) pH as a control factor in hibernation. In: Heller HC et al. (eds) Living in the cold. Elsevier, New York, pp 61–70
Malan A (1988) pH and hypometabolism in mammalian hibernation. Can J Zool 66: 95–98
Malan A (1993) Temperature regulation, enzyme kinetics, and metabolic depression in mammalian hibernation. In: Carey C et al (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 241–251
Morrison P, Ryser FA (1962) Metabolism and body temperature in a small hibernator, the meadow jumping mouse, Zapus hudsonicus. J Cell Comp Physiol 60: 169–180
Morton SR (1983) Stripe-faced dunnart, Sminthopsis macroura. In: Strahan R (ed) Complete book of Australian mammals. Angus and Robertson, Sydney, pp 63–64
Nagel A (1985) Sauerstoffverbrauch, Temperaturregulation und Herzfrequenz bei europäischen Spitzmäusen (Soricidae). Z Säugetierkunde 50: 249–266
Roberts JC, Smith RE (1967) Effect of temperature on metabolic rates of liver and brown fat homogenates. Can J Biochem 45: 1763–1771
Schmidt-Nielsen K (1990) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge
Snapp BD, Heller HC (1981) Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54: 297–307
Snyder GK, Nestler JR (1990) Relationship between body temperature, thermal conductance, Q 10 and energy metabolism during daily torpor and hibernation in rodents. J Comp Physiol B 159: 667–675
Song X, Zeng J (1991) Seasonal variation in energy metabolism of the ground squirrel (Citellus dauricus). Acta Theriologica Sinica 11:48–55
Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65: 145–174
Tähti H (1978) Seasonal differences in O2 consumption and respiratory quotient in a hibernator (Erinaceus europaeus L). Ann Zool Fenn 15: 69–75
Tucker VA (1965) Oxygen consumption, thermal conductance, and torpor in the California pocket mouse Perognathus californicus. J Cell Comp Physiol 65: 393–404
Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative environmental physiology 4. Springer-Verlag, Berlin
Withers PC (1977) Measurement of 297-1, 297-2, and evaporative water loss with a flow-through mask. J Appl Physiol 42: 120–123
Wolf LL, Hainsworth FR (1972) Environmental influence on regulated body temperature in torpid hummingbirds. Comp Biochem Physiol 41A: 167–173
Yeager DP, Ultsch GR (1989) Physiological regulation and conformation: a BASIC program for the determination of critical points. Physiol Zool 62: 888–907
Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs
Author information
Authors and Affiliations
Additional information
Communicated by H. Langer
Rights and permissions
About this article
Cite this article
Song, X., Körtner, G. & Geiser, F. Reduction of metabolic rate and thermoregulation during daily torpor. J Comp Physiol B 165, 291–297 (1995). https://doi.org/10.1007/BF00367312
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00367312