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Journal of Comparative Physiology B

, Volume 162, Issue 8, pp 696–706 | Cite as

Body temperature and metabolic rate during natural hypothermia in endotherms

  • G. Heldmaier
  • T. Ruf
Article

Abstract

During daily torpor and hibernation metabolic rate is reduced to a fraction of the euthermic metabolic rate. This reduction is commonly explained by temperature effects on biochemical reactions, as described by Q10 effects or Arrhenius plots. This study shows that the degree of metabolic suppression during hypothermia can alternatively be explained by active downregulation of metabolic rate and thermoregulatory control of heat production. Heat regulation is fully adequate to predict changes in metabolic rate, and Q10 effects are not required to explain the reduction of energy requirements during hibernation and torpor.

Key words

Dally torpor Body temperature Metabolic rate Hibernation Hamster, Phodopus sungorus 

Abbreviations

BMR

basal metabolic rate

BW

body weight

C

thermal conductance

CHL

thermal conductance as derived from HL

CHP

thermal conductance as derived from HP

HL

heat loss

HP

heat production

MR

metabolic rate

RQ

respiratory quotient

Ta

ambient temperature

Tb

body temperature

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References

  1. Aschoff J (1981) Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp Biochem Physiol 69A:611–619Google Scholar
  2. Aschoff J (1982) The circadian rhythm of body temperature as a function of body size. In: Taylor CR (ed) A companion to animal physiology. Cambridge Univ. Press, pp 173–188Google Scholar
  3. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0°C in an arctic hibernator. Science 244:1593–1595Google Scholar
  4. Bartholomew GA, Hudson JW (1960) Aestivation in the mohave ground squirrel Citellus mohavensis. Bull Mus Comp Zool Harv Univ 124:193–208Google Scholar
  5. Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of the pigmy possum, Cercaertus nanus. Physiol Zool 35:94–107Google Scholar
  6. Biebach H (1977) Reduktion des Energiestoffwechsels und der Körpertemperatur hungernder Amseln (Turdus merula). J Ornit 118:294–300Google Scholar
  7. Brown JH, Bartholomew GA (1969) Periodicity and energetics of torpor in the Kangaroo mouse, Microdipodops pallidus. Ecology 50:705–709Google Scholar
  8. Brummermann M, Rautenberg W (1989) Interaction of autonomic and behavioral thermoregulation in osmotically stressed pigeons (Columbia livia). Physiol Zool 62:1102–1116Google Scholar
  9. Cannon B, Nedergaard J (1985) Biochemical mechanisms of thermogenesis. In: Gilles R (ed) Circulation, respiration and metabolism. Springer, Heidelberg, pp 502–518Google Scholar
  10. Cranford JA (1983) Body temperature, heart rate and oxygen consumption of normothermic and heterothermic western jumping mice (Zapus princeps). Comp Biochem Physiol 74A:595–599Google Scholar
  11. Christophersen J (1973) Basic aspects of temperature action on microorganisms. In: Precht H (ed) Temperature and life. Springer, Heidelberg, pp 3–59Google Scholar
  12. Fleming MR (1980) Thermoregulation and torpor in the sugar glider, Petaurus breviceps (Marsupialia: Petauridae). Austr J Zool 28:521–534Google Scholar
  13. Florant G, Heller HC (1977) CNS regulation of body temperature in euthermic and hibernating marmosts (Marmota flaviventris). Am J Physiol 232:R203-R208Google Scholar
  14. French AR (1985) Allometries of the durations of torpid and euthermic intervals during mammalian hibernation: A test of the theory of hibernation control of the timing of changes in body temperature. J Comp Physiol B 156:13–19Google Scholar
  15. Geiser F (1986) Thermoregulation and torpor in the kultarr, Antechinomys laniger (Marsupialia: Dasyuridae). J Comp Physiol B 156:751–757Google Scholar
  16. Geiser F (1987) Hibernation and daily torpor in two pygmy possums (Cercartetus spp., Marsupialia). Physiol Zool 60:93–102Google Scholar
  17. Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158:25–37Google Scholar
  18. Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344Google Scholar
  19. Hainsworth FR, Wolf LL (1970) Regulation of oxygen consumption and body temperature during torpor in a humming bird, Eulampis jugularis. Science 168:368–369Google Scholar
  20. Hammel HT, Dawson TJ, Abrams RM, Andersen HT (1968) Total calorimetric measurements on Citellus lateralis in hibernation. Physiol Zool 41:341–357Google Scholar
  21. Hayssen V, Lacy RC (1985) Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol 81A:741–754Google Scholar
  22. Heldmaier G (1970) Variations of body temperature and metabolism during entrance into cold lethargy in the bat Myotis myotis. Bijdr Dierkd 40:45–50Google Scholar
  23. Heldmaier G (1975) Metabolic and thermoregulatory responses to heat and cold in the Djungarian hamster, Phodopus sungorus. J Comp Physiol 102:115–122Google Scholar
  24. Heldmaier G, Steinlechner S (1981) Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 48:265–270Google Scholar
  25. Heller HC, Colliver GW (1974) CNS regulation of body temperature during hibernation. Am J Physiol 227:583–589Google Scholar
  26. Heller HC, Colliver GW, Beard J (1977) Thermoregulation during entrance into hibernation. Pflügers Arch 369:55–59Google Scholar
  27. Heller HC, Walker JM, Florant GL, Glotzbach SF, Berger RJ (1978) Sleep and hibernation: electrophysiological and thermoregulatory homologies. In: Wang LCH, Hudson JW (eds) Strategies in cold: natural torpidity and thermogenesis. Academic Press, New York, pp 225–265Google Scholar
  28. Heusner A (1957) Variations nycthémérales de la calorification et de l'activité chez le rat: rapports entre le métabolisme de repos et le niveau d'activité. J de Physiol (Paris) 49:205–210Google Scholar
  29. Hiebert SM (1990) Energy costs and temporal organization of torpor in the rufous hummingbird (Selasphorus rufus). Physiol Zool 63:1082–1097Google Scholar
  30. Hill RW (1975) Daily torpor in Peromyscus leucopus on an adequate diet. Comp Biochem Physiol 51A:413–423Google Scholar
  31. Hudson JW, Scott IM (1979) Daily torpor in the laboratory mouse, Mus musculus var. Albino. Physiol Zool 52:205–218Google Scholar
  32. Johansen K, Krog J (1959) Diurnal body temperature variatons and hibernation in the birchmouse, Sicista betulina. Am J Physiol 196:1200–1204Google Scholar
  33. Kayser C (1950) Le problème de la loi des tailles et de la loi des surfaces tel qu'il apparait dans l'étude de la calorification des batrachens et reptiles et des mammifères hibernants. Arch Sci Physiol 4:361–378Google Scholar
  34. Kayser C (1961) The physiology of natural hibernation. Pergamon Press, OxfordGoogle Scholar
  35. Kayser C (1964) La dépense d'énergie des mammifères en hibernation. Arch Sci Physiol 18:137–150Google Scholar
  36. Kinnear A, Shield JW (1975) Metabolism and temperature regulation in marsupials Comp Biochem Physiol 52A:235–245Google Scholar
  37. Lyman CP (1948) The oxygen consumption and temperature regulation of hibernating hamsters. J Exp Zool 109:55–78Google Scholar
  38. Lyman CP (1958) Oxygen consumption, body temperature and heart rate of woodchucks entering hibernation. Am J Physiol 194:83–91Google Scholar
  39. Lyman CP, O'Brien RC (1972) Sensitivity to low temperature in hibernating rodents. Am J Physiol 222:864–869Google Scholar
  40. Malan A (1986) pH as a control factor in hibernation. In: Heller HC et al. (eds) Living in the cold. Elsevier, New York, pp 61–70Google Scholar
  41. Mrosovsky N (1971) Hibernation and the hypothalamus. In: Towe A (ed) Neuroscience, series (3). Appleton-Century-Crofts, New YorkGoogle Scholar
  42. Nagai H (1909) Der Stoffwechsel des Winterschläfers. Z Allg Physiol 9:243–367Google Scholar
  43. Nestler JR (1990) Relationships between respiratory quotient and metabolic rate during entry to and arousal from daily torpor in deer mice (Peromyscus maniculatus). Physiol Zool 63:504–515Google Scholar
  44. Neumann RL, Cade TJ (1965) Torpidity in the Mexican ground squirrel Citellus mexicanus parvidens (Mearns). Can J Zool 43:133–140Google Scholar
  45. O'Connor JM, McKeever WP (1950) The influence of temperature on mammalian tissue oxidation and its relation to the normal body temperature. Proc R Ir Acad Sect B 53:33–44Google Scholar
  46. Ortmann S (1992) Bedeutung des Winterschlafes für den Energichaushalt des Alpennmurmeltieres. Verh Dtsch Zool Ges 85:156Google Scholar
  47. Pohl H (1962) Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern (Untersuchungen an Myotis myotis Borkh. Glis glis L. und Mesocricetus auratus Waterh). Z Vergl Physiol 45:8–153Google Scholar
  48. Prinzinger R, Göppel R, Lorenz A, Kulzer E (1981) Body temperature and metabolism in the red-backed mousebird (Colius castanotus) during fasting and torpor. Comp Biochem Physiol 69A:689–692Google Scholar
  49. Rautenberg W (1989) Shivering thermogenesis and its interaction with other autonomic controlled systems. In: Malan A, Canguilhem B (eds) Living in the cold II. Elsevier, New York, pp 409–418Google Scholar
  50. Reinertsen RE (1989) The regular use of nocturnal hypothermia and torpor during energetically-demanding periods in the annual cycles of birds. In: Malan A, Canguilhem B (eds) Living in the cold II. Elsevier, New York, pp 107–116Google Scholar
  51. Ruf T, Heldmaier G (1987) Computerized body temperature telemetry in small animals: use of simple equipment and advanced noise suppression. Comp Biol Med 17:331–340Google Scholar
  52. Ruf T, Heldmaier G (1992) The impact of daily torpor on energy requirements in the Djungarian hamster (Phodopus sungorus). Physiol Zool 65Google Scholar
  53. Scholander PF, Hock R, Walters V, Hohnson F, Irving L (1950) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:237–258Google Scholar
  54. Scholl P (1974) Temperaturregulation beim madegassischen Igeltanrek Echinops telfairi (Martin, 1838). J Comp Physiol 89:175–195Google Scholar
  55. Snapp BD, Heller HC (1981) Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54:297–307Google Scholar
  56. Snyder GK, Nestler JR (1990) Relationships between body temperature, thermal conductance, Q 10, and energy metabolism during daily torpor and hibernation in rodents. J Comp Physiol B 159:667–675Google Scholar
  57. Storey KB (1987) Regulation of liver metabolism by enzyme phosphorylation during mammalian hibernation. J Biol Chem 262:1670–1673Google Scholar
  58. Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174Google Scholar
  59. Tucker VA (1965a) Oxygen consumption, thermal conductance, and torpor in the California pocket mouse Perognathus californicus. J Cell Comp Physiol 65:393–404Google Scholar
  60. Tucker VA (1965b) The relation between the torpor cycle and heat exchange in the California Pocket mouse, Perognathus californicus. J Cell Comp Physiol 65:405–414Google Scholar
  61. Wang LCH (1978) Energetics and field aspects of mammalian torpor: the Richardson's ground squirrel. In: Wang LCH, Hudson JW (eds) Strategies in cold, natural torpidity and thermogenesis. Academic Press, New York, pp 109–145Google Scholar
  62. Wang LCH, Hudson JW (1971) Temperature regulation in normothermic and hibernating eastern chipmunk, Tamias striatus. Comp Biochem Physiol 38A:59–90Google Scholar
  63. Wyss OAM (1932) Winterschalf und Wärmehaushalt, untersucht am Siebenschläfer (Myoxus glis). Pflügers Arch Gesamte Physiol Menschen Tiere 229:599–635Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • G. Heldmaier
    • 1
  • T. Ruf
    • 1
  1. 1.Department of Biology, ZoologyPhilipps UniversitätMarburgFederal Republic of Germany

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