Skip to main content
SpringerLink
Log in

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

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Summary

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BMR:

basal metabolic rate

ICM:

independent comparisons method

MWR:

mean warm-up rate

PMR:

peak metabolic rate

PWR:

peak·warm-up rate

Tbactivity :

body temperature during activity

Tbtorpor :

body temperature during torpor

ΔT arousal :

increase in body temperature during arousal

References

  • Anon (1987) Glossary of terms for thermal physiology. The commission for thermal physiology of the international union of physiological sciences. Pflügers Arch 410: 567–587

    Google Scholar 

  • 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 15–72

    Google Scholar 

  • 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 633–808

    Google Scholar 

  • Baker RJ, Qumsiyeh MB, Hood CS (1987) Role of chromosomal banding patterns in understanding mammalian evolution. Curr Mammal 1:67–96

    Google Scholar 

  • 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 46–78

    Google Scholar 

  • Bartholomew GA, Cade TJ (1957) Temperature regulation, hibernation and aestivation in the little pocker mouse, Perognathus longimembris. J Mammol 38:60–72

    Google Scholar 

  • Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of the pigmy possum, Cercartetus nanus. Physiol Zool 35:94–107

    Google Scholar 

  • Bartholomew GA, MacMillen RE (1961) Oxygen consumption, estivation and hibernation in the kangaroo mouse, Microdipodops pallidus. Physiol Zool 34:177–183

    Google Scholar 

  • Bartholomew GA, Howell TR, Cade TJ (1957) Torpidity in the white-throated swift, Anna hummingbird and poorwill. Condor 59:145–155

    Google Scholar 

  • Bartholomew GA, Dawson WR, Lasiewski RC (1970) Thermoregulation and heterothermy in some of the smaller flying foxes (Megachiroptera) of New Guinea. Z Vgl Physiol 70:196–209

    Google Scholar 

  • 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 229–234

    Google Scholar 

  • Bradley SR, Deavers DR (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol 65:465–476

    Google Scholar 

  • Brower JE (1970) Metabolic and thermal adaptations of heteromyid rodents to the desert. PhD thesis, Syracuse University

  • Cade TJ (1963) Observations on torpidity in captive chipmunks of the genus Eutamias. Ecology 44:255–261

    Google Scholar 

  • 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 pp

    Google Scholar 

  • Chew RM, Lindberg RG, Hyden P (1967) Temperature regulation in the little pocket mouse, Perognathus longimembris. Comp Biochem Physiol 21:487–505

    Google Scholar 

  • Corbet GB, Hill JE (1986) A world list of mammalian species, 2nd edn. British Museum (Natural History) London

    Google Scholar 

  • Cranford JA (1983) Body temperature, heart rate and oxygen consumption of normothermic and heterothermic western jumping mice (Zapus princeps). Comp Biochem Physiol 74A:595–599

    Google Scholar 

  • Davis DE (1976) Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 51:477–514

    Google Scholar 

  • Eisenberg JF (1981) The mammalian radiations. Athlone Press, London

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Google Scholar 

  • Fleming MR (1980) Thermoregulation and torpor in the sugar glider Petaurus breviceps (Marsupialia: Petauridae). Austr J Zool 28:521–534

    Google Scholar 

  • Fleming MR (1982) Thermal strategies of three small possums from southeastern Australia. PhD thesis, Monash University

  • Fleming MR (1985) The thermal physiology of the feathertail glider Acrobates pygmaeus (Marsupialia: Burramyidae). Austr J Zool 33:667–681

    Google Scholar 

  • Frey H (1980) Le métabolism énérgetique de Suncus etruscus (Soricidae, Insectivora) en torpeur. Rev Suisse Zool 87:739–748

    Google Scholar 

  • Gaertner RA, Hart JS, Roy OZ (1973) Seasonal spontaneous torpor in the white-footed mouse Peromyscus leucopus. Comp Biochem Physiol 45A:169–181

    Google Scholar 

  • Geiser F (1986) Thermoregulation and torpor in the kultarr, Antechinomys laniger (Marsupialia: Dasyuridae). J Comp Physiol B 156:751–757

    Google Scholar 

  • Geiser F (1987) Hibernation and daily torpor in two pygmy possums (Cercartetus spp., Marsupialia). Physiol Zool 60:93–102

    Google Scholar 

  • Geiser F (1988) Daily torpor and thermoregulation in the small dasyurid marsupials Planigale gilesi and Ningaui yvonneae. Austr J Zool 36:473–481

    Google Scholar 

  • 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

    Google Scholar 

  • Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp. Physiol B 157:335–344

    Google Scholar 

  • Geiser F, Baudinette RV (1990) The relationship between body mass and rate of rewarming from hibernation and daily torpor in mammals. J Exp Biol 151:349–359

    Google Scholar 

  • 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 42:543–547

    Google Scholar 

  • Godfrey GK (1968) Body temperatures and torpor in Sminthopsis crassicaudata and Sminthopsis larapinta (Marsupialia: Dasyuridae). J Zool Soc Lond 156:499–511

    Google Scholar 

  • Grafen A (1989) The phylogenetic regression. Phil Trans R Soc Lond Ser B: 326:119–157

    Google Scholar 

  • 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 3–23

    Google Scholar 

  • 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 195–216

    Google Scholar 

  • Hart JS (1953) Energy metabolism of the white-footeed mouse, Peromyscus leucopus noveboracensis after acclimation at various environmental temperatures. Can J Zool 31:99–105

    Google Scholar 

  • Hart JS (1971) Rodents. In: Whittow GC (ed) Comparative physiology of thermoregulation Academic Press, New York, pp 1–149

    Google Scholar 

  • 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 346–361

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Heinrich B (1975) Thermoregulation in bumblebees. 2. Energetics of warm-up and free flight. J Comp Physiol 96:155–166

    Google Scholar 

  • Heinrich B, Bartholomew GA (1971) An analysis of pre-flight warm-up in the sphinx moth Manduca sexta. J Exp Biol 55:223–239

    Google Scholar 

  • Heldmaier G (1971) In: Jansky L (ed) Non-shivering thermogenesis. Swcts and Zeitlinger, Amsterdam, pp 73–74

    Google Scholar 

  • Heldmaier G (1978) Rewarming rates from torpor in mammals and birds. J Therm Biol 3:100–101

    Google Scholar 

  • Hight ME, Goodman M, Prychodko W (1974) Immunological studies of the Sciuridae. Syst Zool 23:12–25

    Google Scholar 

  • Hudson JW (1964) Temperature regulation in the round-tailed ground squirrel, Citellus tereticaudis. Ann Acad Sci Fenn Ser A 71:219–233

    Google Scholar 

  • Hudson JW (1964) Temperature regulation and torpidity in the pygmy mouse Baiomys taylori. Physiol Zool 38:243–254

    Google Scholar 

  • 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 66–108

    Google Scholar 

  • Hudson JW, Scott JM (1979) Daily torpor in the laboratory mouse Mus musculus var. albino. Physiol Zool 52:205–218

    Google Scholar 

  • Johansen K, Krog J (1959) Diurnal body temperature variations and hibernation in the birch mouse, Sicista betulina. Am J Physiol 196:1200–1204

    Google Scholar 

  • Kalter VG, Folk GE (1979) Humoral induction of mammalian hibernation. Comp Biochem Physiol 63A:7–13

    Google Scholar 

  • Kleiber M (1961) The fire of life: an introduction to animal energetics. Wiley, New York

    Google Scholar 

  • La Barbera M (1989) Analyzing body size as a factor in ecology and evolution. Annu Rev Ecol Syst 20:97–117

    Google Scholar 

  • 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 227–276

  • Lyman CP, O'Brien RC (1960) Circulatory changes in the 13-lined ground squirrel during the hibernating cycle. Bull Mus Comp Zool Harv Univ 124:353–372

    Google Scholar 

  • MacMillen RE, Nelson JE (1969) Bioenergetics and body size in dasyurid marsupials. Am J Physiol 217:1246–1251

    Google Scholar 

  • Martins, EP, Garland TH (1991) Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution, in press

  • McCullagh P, Nelder JA (1983) Generalised linear models. Chapman and Hall, London

    Google Scholar 

  • McNab BK (1986) The influence of food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19

    Google Scholar 

  • Morhardt JE (1970) Body temperatures of white footed mice (Peromyscus spp.) during daily torpor. Comp Biochem Physiol 33:423–439

    Google Scholar 

  • Morrison P, McNab BK (1962) Daily torpor in a Brazilian murine opossum (Marmosa). Comp Biochem Physiol 6:57–68

    Google Scholar 

  • Morrison P, Ryser FA (1959) Body temperature in the white-footed mouse, Peromyscus leucopus noveboracensis. Physiol Zool 32:90–103

    Google Scholar 

  • Morton SR, Lee AK (1978) Thermoregulation and metabolism in Planigale maculata (Marsupialia: Dasyuridae). J Therm Biol 3:117–120

    Google Scholar 

  • 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 49:78–90

    Google Scholar 

  • Nagel A (1977) Torpor in the European white-toothed shrews. Experientia 33:1455–6

    Google Scholar 

  • Neumann RL, Cade TJ (1965) Torpidity in the mexican ground squirrel Citellus mexicanus parvidens (Mearns). Can J Zool 43:133–140

    Google Scholar 

  • 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 31–71

    Google Scholar 

  • Nowak RM, Paradiso JL (1983) Walker's mammals of the world, 4th edn. Johns Hopkins University Press, Baltimore London

    Google Scholar 

  • Pagel MD, Harvey PH (1988) The comparative method. Q Rev Biol 63:413–440

    Google Scholar 

  • Pagel MD, Harvey PH (1989) Comparative methods for examining adaptation in primates depend on evolutionary models. Folia Primatol 53:203–220

    Google Scholar 

  • Patton JL, Sherwood SW, Yang SY (1980) Biochemical systematics of chaetodipine pocket mice, genus Perognathus. J Mammal 62:477–492

    Google Scholar 

  • Peiponen VA (1965) On hypothermia and torpidity in the nightjar (Caprimulgus europaeus L.). Ann Acad Sci Fenn Ser A 87:15 pp

    Google Scholar 

  • Pettigrew JD, Jamieson BGM (1987) Are flying foxes (Chiroptera: Pteropodidae) really primates? Austr Mammal 10:119–124

    Google Scholar 

  • 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 325:489–559

    Google Scholar 

  • Promislow DEL (1991) The evolution of mammalian blood parameters: patterns and their interpretation. Physiol. Zool, 64:393–431

    Google Scholar 

  • Ridley M (1983) The explanation of organic diversity: the comparative method and adaptations for mating. University Press, Oxford

    Google Scholar 

  • Rogers DS, Greenbaum IF, Gunn SJ, Engstrom MD (1984) Cytosystematic value of chromosomal inversion data in the genus Peromyscus (Rodentia: Cricetidae). J Mammal 65:457–465

    Google Scholar 

  • Sarich VM (1985) Rodent macromolecular systematics. In: Luckett WP, Hartenberger J (eds) Evolutionary relationships among rodents; a multidisciplinary analysis, pp 423–452

  • Stone GN (1990) Endothermy and thermoregulation in solitary bees. DPhil thesis, Oxford University

  • 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 147:303–328

    Google Scholar 

  • Tucker VA (1965a) Oxygen consumption, thermal conductance and torpor in the California pocket mouse Perognathus californicus. J Cell Comp Physiol 65:393–404

    Google Scholar 

  • Tucker VA (1965b) The relation between the torpor cycle and heat exchange in the California pocket mouse Perognathus californicus. J Cell Comp Physiol 65:405–414

    Google Scholar 

  • Twente JW, Twente JA (1965) Regulation of hibernating periods by temperature. Proc Natl Acad Sci USA 54:1058–1061

    Google Scholar 

  • Tyndale-Biscoe H (1973) Life of marsupials. Elsevier, Amsterdam

    Google Scholar 

  • Wallis RL (1976) Torpor in the dasyurid marsupial Antechinus stuartii. Comp Biochem Physiol 53A:319–322

    Google Scholar 

  • 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 285–291

    Google Scholar 

  • Wang LC, Hudson JW (1970) Some physiological aspects of temperature regulation in the normothermic and torpid hispid pocket mouse Perognathus hispidus. Comp Biochem Physiol 32:275–293

    Google Scholar 

  • Wang LCH, Hudson JW (1971) Temperature regulation in normothermic and hibernating eastern chipmunks, Tamias striatus. Comp Biochem Physiol 38A:59–90

    Google Scholar 

  • Wickler SJ (1980) Maximal thermogenic capacity and body temperatures of whitefooted mice (Peromyscus) in summer and winter. Physiol Zool 53:338–346

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Oxford University, South Parks Road, OX1 3PS, Oxford, UK

    Graham N. Stone & Andy Purvis

Authors
  1. Graham N. Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andy Purvis
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stone, G.N., Purvis, A. Warm-up rates during arousal from torpor in heterothermic mammals: physiological correlates and a comparison with heterothermic insects. J Comp Physiol B 162, 284–295 (1992). https://doi.org/10.1007/BF00357536

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00357536

Key words

Search

Navigation