Journal of Comparative Physiology B

, Volume 162, Issue 3, pp 284–295 | Cite as

Warm-up rates during arousal from torpor in heterothermic mammals: physiological correlates and a comparison with heterothermic insects

  • Graham N. Stone
  • Andy Purvis


This study examines the relationship between warm-up rate, body mass, metabolic rate, thermal conductance and normothermic body temperature in heterothermic mammals during arousal from torpor. Predictions based on the assumption that the energetic cost of arousal has been minimised are tested using data for 35 species. The observation that across-species warm-up rate correlates negatively with body mass is confirmed using a comparative technique which removes confounding effects due to the non-independence of species data due to shared common ancestry. Mean warm-up rate during arousal correlates negatively with basal metabolic rate and positively with the temperature difference through which the animal warms, having controlled for other factors. These results suggest that selection has operated to minimise the overall energetic, cost of warm-up. In contrast, peak warm-up rate during arousal correlates positively with peak metabolic rate during arousal, and negatively with thermal conductance, when body mass has been taken into account. These results suggest that peak warm-up rate is more sensitive to the fundamental processes of heat generation and loss. Although heterothermic marsupials have lower normothermic body temperatures and basal metabolic rates, marsupials and heterothermic eutherian mammals do not differ systematically in warm-up rate. Pre-flight warm-up rates in one group of endothermic insects, the bees, are significantly higher than predictions based on rates of arousal of a mammal of the same body mass.

Key words

Mammals Torpor Arousal Warm-up rate Metabolic rate Comparative method 



basal metabolic rate


independent comparisons method


mean warm-up rate


peak metabolic rate


peak·warm-up rate


body temperature during activity


body temperature during torpor


increase in body temperature during arousal


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  1. Anon (1987) Glossary of terms for thermal physiology. The commission for thermal physiology of the international union of physiological sciences. Pflügers Arch 410: 567–587Google Scholar
  2. Aplin KP, Archer M (1987) Recent advances in marsupial systematics with a new syncretic classification. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons Pty Ltd. Chipping Norton, England, pp 15–72Google Scholar
  3. Archer M (1984) The Australian marsupial radiation. In: Archer M, Clayton G (eds) Vertebrate zoogeography and evolution in Australasia (animals in space and time). Hesperian Press, Carlisle, Western Australia, pp 633–808Google Scholar
  4. Baker RJ, Qumsiyeh MB, Hood CS (1987) Role of chromosomal banding patterns in understanding mammalian evolution. Curr Mammal 1:67–96Google Scholar
  5. Bartholomew GA (1981) A matter of size: an examination of endothermy in insects and terrestrial vertebrates. In: Heinrich B (ed) Insect thermoregulation. Wiley, New York, pp 46–78Google Scholar
  6. Bartholomew GA, Cade TJ (1957) Temperature regulation, hibernation and aestivation in the little pocker mouse, Perognathus longimembris. J Mammol 38:60–72Google Scholar
  7. Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of the pigmy possum, Cercartetus nanus. Physiol Zool 35:94–107Google Scholar
  8. Bartholomew GA, MacMillen RE (1961) Oxygen consumption, estivation and hibernation in the kangaroo mouse, Microdipodops pallidus. Physiol Zool 34:177–183Google Scholar
  9. Bartholomew GA, Howell TR, Cade TJ (1957) Torpidity in the white-throated swift, Anna hummingbird and poorwill. Condor 59:145–155Google Scholar
  10. Bartholomew GA, Dawson WR, Lasiewski RC (1970) Thermoregulation and heterothermy in some of the smaller flying foxes (Megachiroptera) of New Guinea. Z Vgl Physiol 70:196–209Google Scholar
  11. Baverstock PR, Birrel J, Krieg M (1987) Albumin immunological relationships among Australian possums: a progress report. In: Archer M (ed) Possums and opossums: studies in evolution. Beatty, Chipping Norton, England, pp 229–234Google Scholar
  12. Bradley SR, Deavers DR (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol 65:465–476Google Scholar
  13. Brower JE (1970) Metabolic and thermal adaptations of heteromyid rodents to the desert. PhD thesis, Syracuse UniversityGoogle Scholar
  14. Cade TJ (1963) Observations on torpidity in captive chipmunks of the genus Eutamias. Ecology 44:255–261Google Scholar
  15. Carpenter RE (1966) A comparison of thermoregulation and water metabolism in the kangaroo rats Dipodomys agilis and Dipodomys merriami. Univ Calif, Berkeley, Publ Zool 78:36 ppGoogle Scholar
  16. Chew RM, Lindberg RG, Hyden P (1967) Temperature regulation in the little pocket mouse, Perognathus longimembris. Comp Biochem Physiol 21:487–505Google Scholar
  17. Corbet GB, Hill JE (1986) A world list of mammalian species, 2nd edn. British Museum (Natural History) LondonGoogle Scholar
  18. 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
  19. Davis DE (1976) Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 51:477–514Google Scholar
  20. Eisenberg JF (1981) The mammalian radiations. Athlone Press, LondonGoogle Scholar
  21. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15Google Scholar
  22. Fleming MR (1980) Thermoregulation and torpor in the sugar glider Petaurus breviceps (Marsupialia: Petauridae). Austr J Zool 28:521–534Google Scholar
  23. Fleming MR (1982) Thermal strategies of three small possums from southeastern Australia. PhD thesis, Monash UniversityGoogle Scholar
  24. Fleming MR (1985) The thermal physiology of the feathertail glider Acrobates pygmaeus (Marsupialia: Burramyidae). Austr J Zool 33:667–681Google Scholar
  25. Frey H (1980) Le métabolism énérgetique de Suncus etruscus (Soricidae, Insectivora) en torpeur. Rev Suisse Zool 87:739–748Google Scholar
  26. Gaertner RA, Hart JS, Roy OZ (1973) Seasonal spontaneous torpor in the white-footed mouse Peromyscus leucopus. Comp Biochem Physiol 45A:169–181Google Scholar
  27. Geiser F (1986) Thermoregulation and torpor in the kultarr, Antechinomys laniger (Marsupialia: Dasyuridae). J Comp Physiol B 156:751–757Google Scholar
  28. Geiser F (1987) Hibernation and daily torpor in two pygmy possums (Cercartetus spp., Marsupialia). Physiol Zool 60:93–102Google Scholar
  29. Geiser F (1988) Daily torpor and thermoregulation in the small dasyurid marsupials Planigale gilesi and Ningaui yvonneae. Austr J Zool 36:473–481Google Scholar
  30. Geiser F, Baudinette RV (1985) The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia). J Comp Physiol B 156:129–134Google Scholar
  31. Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp. Physiol B 157:335–344Google Scholar
  32. Geiser F, Baudinette RV (1990) The relationship between body mass and rate of rewarming from hibernation and daily torpor in mammals. J Exp Biol 151:349–359Google Scholar
  33. Geiser F, Baudinette RV, McMurchie EJ (1986) Seasonal changes in the critical arousal temperature of the marsupial Sminthopsis crassicaudata correlate with the thermal transition in mitochondrial respiration. Experientia 42:543–547Google Scholar
  34. Godfrey GK (1968) Body temperatures and torpor in Sminthopsis crassicaudata and Sminthopsis larapinta (Marsupialia: Dasyuridae). J Zool Soc Lond 156:499–511Google Scholar
  35. Grafen A (1989) The phylogenetic regression. Phil Trans R Soc Lond Ser B: 326:119–157Google Scholar
  36. Hafner DJ (1984) Evolutionary relationships of the nearctic Sciuridae. In: Murie JO, Michener GR (eds) The biology of grounddwelling squirrels. Annual cycles, behavioural ecology and sociality. University of Nebraska Press, Lincoln and London, pp 3–23Google Scholar
  37. Harding HR (1987) Interrelationships of the families of the Diprotodonta—a view based on spermatozoan ultrastructure. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons Pty. Ltd., Chipping Norton, England, pp 195–216Google Scholar
  38. Hart JS (1953) Energy metabolism of the white-footeed mouse, Peromyscus leucopus noveboracensis after acclimation at various environmental temperatures. Can J Zool 31:99–105Google Scholar
  39. Hart JS (1971) Rodents. In: Whittow GC (ed) Comparative physiology of thermoregulation Academic Press, New York, pp 1–149Google Scholar
  40. Harvey PH, Mace GM (1982) Comparisons between taxa and adaptive trends: problems of methodology. In: Kings College Sociobiology Group, (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, UK, pp 346–361Google Scholar
  41. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  42. Heinrich B (1975) Thermoregulation in bumblebees. 2. Energetics of warm-up and free flight. J Comp Physiol 96:155–166Google Scholar
  43. Heinrich B, Bartholomew GA (1971) An analysis of pre-flight warm-up in the sphinx moth Manduca sexta. J Exp Biol 55:223–239Google Scholar
  44. Heldmaier G (1971) In: Jansky L (ed) Non-shivering thermogenesis. Swcts and Zeitlinger, Amsterdam, pp 73–74Google Scholar
  45. Heldmaier G (1978) Rewarming rates from torpor in mammals and birds. J Therm Biol 3:100–101Google Scholar
  46. Hight ME, Goodman M, Prychodko W (1974) Immunological studies of the Sciuridae. Syst Zool 23:12–25Google Scholar
  47. Hudson JW (1964) Temperature regulation in the round-tailed ground squirrel, Citellus tereticaudis. Ann Acad Sci Fenn Ser A 71:219–233Google Scholar
  48. Hudson JW (1964) Temperature regulation and torpidity in the pygmy mouse Baiomys taylori. Physiol Zool 38:243–254Google Scholar
  49. Hudson JW, Bartholomew GA (1964) Terrestrial animals in dry heat: aestivators. In: Wang LCH, Hudson JW (eds) Natural torpidity and thermogenesis. Academic Press, New York, pp 66–108Google Scholar
  50. Hudson JW, Scott JM (1979) Daily torpor in the laboratory mouse Mus musculus var. albino. Physiol Zool 52:205–218Google Scholar
  51. Johansen K, Krog J (1959) Diurnal body temperature variations and hibernation in the birch mouse, Sicista betulina. Am J Physiol 196:1200–1204Google Scholar
  52. Kalter VG, Folk GE (1979) Humoral induction of mammalian hibernation. Comp Biochem Physiol 63A:7–13Google Scholar
  53. Kleiber M (1961) The fire of life: an introduction to animal energetics. Wiley, New YorkGoogle Scholar
  54. La Barbera M (1989) Analyzing body size as a factor in ecology and evolution. Annu Rev Ecol Syst 20:97–117Google Scholar
  55. Luckett WP (1986) Superordinal and intraordinal affinities of rodents: development evidence from the dentition and placentation. In: Luckett WP, Hartenberger J (eds) Evolutionary relationships among rodents; a multidisciplinary analysis. pp 227–276Google Scholar
  56. Lyman CP, O'Brien RC (1960) Circulatory changes in the 13-lined ground squirrel during the hibernating cycle. Bull Mus Comp Zool Harv Univ 124:353–372Google Scholar
  57. MacMillen RE, Nelson JE (1969) Bioenergetics and body size in dasyurid marsupials. Am J Physiol 217:1246–1251Google Scholar
  58. Martins, EP, Garland TH (1991) Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution, in pressGoogle Scholar
  59. McCullagh P, Nelder JA (1983) Generalised linear models. Chapman and Hall, LondonGoogle Scholar
  60. McNab BK (1986) The influence of food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19Google Scholar
  61. Morhardt JE (1970) Body temperatures of white footed mice (Peromyscus spp.) during daily torpor. Comp Biochem Physiol 33:423–439Google Scholar
  62. Morrison P, McNab BK (1962) Daily torpor in a Brazilian murine opossum (Marmosa). Comp Biochem Physiol 6:57–68Google Scholar
  63. Morrison P, Ryser FA (1959) Body temperature in the white-footed mouse, Peromyscus leucopus noveboracensis. Physiol Zool 32:90–103Google Scholar
  64. Morton SR, Lee AK (1978) Thermoregulation and metabolism in Planigale maculata (Marsupialia: Dasyuridae). J Therm Biol 3:117–120Google Scholar
  65. Nadler CF, Lyupanova EA, Hoffman RS, Vorontsov NN, Shaitarova LL, Borisov YM (1984) Chromosomal evolution in holarctic ground squirrels (Spermophilus) II. Giemsa-band homologies of chromosomes and the tempo of evolution. Z Säugetierkunde 49:78–90Google Scholar
  66. Nagel A (1977) Torpor in the European white-toothed shrews. Experientia 33:1455–6Google Scholar
  67. Neumann RL, Cade TJ (1965) Torpidity in the mexican ground squirrel Citellus mexicanus parvidens (Mearns). Can J Zool 43:133–140Google Scholar
  68. Novacek MJ, Wyss AR, McKenna MC (1988) The major groups of eutherian mammals. In: Benton SJ (ed) The phylogeny and classification of the tetrapods. Clarendon Press, Oxford, pp 31–71Google Scholar
  69. Nowak RM, Paradiso JL (1983) Walker's mammals of the world, 4th edn. Johns Hopkins University Press, Baltimore LondonGoogle Scholar
  70. Pagel MD, Harvey PH (1988) The comparative method. Q Rev Biol 63:413–440Google Scholar
  71. Pagel MD, Harvey PH (1989) Comparative methods for examining adaptation in primates depend on evolutionary models. Folia Primatol 53:203–220Google Scholar
  72. Patton JL, Sherwood SW, Yang SY (1980) Biochemical systematics of chaetodipine pocket mice, genus Perognathus. J Mammal 62:477–492Google Scholar
  73. Peiponen VA (1965) On hypothermia and torpidity in the nightjar (Caprimulgus europaeus L.). Ann Acad Sci Fenn Ser A 87:15 ppGoogle Scholar
  74. Pettigrew JD, Jamieson BGM (1987) Are flying foxes (Chiroptera: Pteropodidae) really primates? Austr Mammal 10:119–124Google Scholar
  75. Pettigrew JD, Jamieson BGM, Robson SK, Hall LS, McNally KI, Cooper HM (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Phil Trans R Soc Lond Ser B 325:489–559Google Scholar
  76. Promislow DEL (1991) The evolution of mammalian blood parameters: patterns and their interpretation. Physiol. Zool, 64:393–431Google Scholar
  77. Ridley M (1983) The explanation of organic diversity: the comparative method and adaptations for mating. University Press, OxfordGoogle Scholar
  78. Rogers DS, Greenbaum IF, Gunn SJ, Engstrom MD (1984) Cytosystematic value of chromosomal inversion data in the genus Peromyscus (Rodentia: Cricetidae). J Mammal 65:457–465Google Scholar
  79. Sarich VM (1985) Rodent macromolecular systematics. In: Luckett WP, Hartenberger J (eds) Evolutionary relationships among rodents; a multidisciplinary analysis, pp 423–452Google Scholar
  80. Stone GN (1990) Endothermy and thermoregulation in solitary bees. DPhil thesis, Oxford UniversityGoogle Scholar
  81. Stone GN, Willmer PG (1989) Warm-up rates and body temperatures in bees; the importance of body size, thermal regime and phylogeny. J Exp Biol 147:303–328Google Scholar
  82. Tucker VA (1965a) Oxygen consumption, thermal conductance and torpor in the California pocket mouse Perognathus californicus. J Cell Comp Physiol 65:393–404Google Scholar
  83. 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
  84. Twente JW, Twente JA (1965) Regulation of hibernating periods by temperature. Proc Natl Acad Sci USA 54:1058–1061Google Scholar
  85. Tyndale-Biscoe H (1973) Life of marsupials. Elsevier, AmsterdamGoogle Scholar
  86. Wallis RL (1976) Torpor in the dasyurid marsupial Antechinus stuartii. Comp Biochem Physiol 53A:319–322Google Scholar
  87. Wallis RL (1982) Adaptation to low environmental temperatures in the carnivorous marsupials. In: Archer M (ed) Carnivorous marsupials. Royal Zoological Society of New South Wales, Sydney, pp 285–291Google Scholar
  88. Wang LC, Hudson JW (1970) Some physiological aspects of temperature regulation in the normothermic and torpid hispid pocket mouse Perognathus hispidus. Comp Biochem Physiol 32:275–293Google Scholar
  89. Wang LCH, Hudson JW (1971) Temperature regulation in normothermic and hibernating eastern chipmunks, Tamias striatus. Comp Biochem Physiol 38A:59–90Google Scholar
  90. Wickler SJ (1980) Maximal thermogenic capacity and body temperatures of whitefooted mice (Peromyscus) in summer and winter. Physiol Zool 53:338–346Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Graham N. Stone
    • 1
  • Andy Purvis
    • 1
  1. 1.Department of ZoologyOxford UniversityOxfordUK

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