Skip to main content
SpringerLink
Log in

Seasonal thermoregulatory responses in mammals

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

Abstract

This study examined the proportional seasonal winter adjustments of total and mass-specific basal power (watts and watts g−1, respectively), thermal conductance (watts g−1 °C−1), non-shivering thermogenesis capacity (ratio of NST/basal power), body temperature (°C), and body mass (g) of mammals. The responses are best summarized for three different body size classes; small mammals (<100 g), intermediate-sized mammals (0.1–10 kg), and large mammals (>10 kg). The principal adjustments of the small mammals center on energy conservation, especially the Dehnel Effect, the winter reduction in body size of as much as 50%, accompanied by reductions in mass-specific basal power. On average, these reductions reduce the total basal power approximately in direct proportion to the mass reductions. Reductions in mass-specific basal power are matched by concomitant reductions in conductance to maintain the setpoint body temperature during winter. The overall thermoregulatory adjustments in small mammals serve to (a) lower overall winter power consumption, (b) maintain the setpoint body temperature, and (c) lower the lower critical limit of thermoneutrality and hence thermoregulatory costs. In intermediate-size mammals, the seasonal response is centered more on increasing thermogenic capacity by increasing basal power and NST capacity, accompanied by predictable and large reductions in conductance. The Dehnel effect is negligible. Very large mammals undergo the largest reductions in total and mass-specific basal power and conductance. However, there are too few data to resolve whether the reductions in total basal power can be attributed to the Dehnel effect, because the moderate decreases in body mass may also be caused by nutritional stress. Apart from the seasonal changes in basal power, these observations are consistent with the predictions of Heldmaier’s seasonal acclimatization model.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Andrews RV, Belnap RW (1985) Metabolic and thermoregulatory effects of photoperiod and melatonin on Peromyscus maniculatus acclimatizaton. Comp Biochem Physiol 82A:725–729

    Google Scholar 

  • Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Sci 206:649–654

    Google Scholar 

  • Bozinovic F, Fernando Novoa F, Veloso C (1990) Seasonal changes in energy expenditure and digestive tract of Abrothrix andinus (Cricetidae) in the Andes range. Physiol Zool 63:1216–1231

    Google Scholar 

  • Bozinovic F, Lagos JA, Marquet PA (1999) Geographical energetics of the Andean mouse, Abrothrix andinus. J Mammal 80:205–209

    Google Scholar 

  • Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584

    Google Scholar 

  • Brown JH, Taper ML, Marquet PA (1996) Darwinian fitness and reproductive power: reply to Kozlowski. Am Nat 147:1092–1097

    Google Scholar 

  • Casey TM, Withers PC, Casey KK (1979) Metabolic and respiratory responses of Arctic mammals to ambient temperature during summer. Comp Biochem Physiol 64A:331–341

    Google Scholar 

  • Chappel RW, Hudson RJ (1978) Winter bioenergetics of Rocky Mountain bighorn sheep. Can J Zool 56:2388–2393

    Google Scholar 

  • Chown SL, Gaston KJ (1997) The species-body size distribution: energy, fitness and optimality. Funct Ecol 11:365–375

    Google Scholar 

  • Corp N, Gorman ML, Speakman JR (1997) Seasonal variation in the resting metabolic rate of male wood mice Apodemus sylvaticus from two contrasting habitats 15 km apart. J Comp Physiol B 167:229–239

    Google Scholar 

  • Du Plessis A, Erasmus T, Kerley GIH (1989) Thermoregulatory patterns of two sympatric rodents: Otomys unisulcatus and Parotomys brantsii. Comp Biochem Physiol 94A:215–220

    Google Scholar 

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

    Article  Google Scholar 

  • Fuglei E, Øritsland NA (1999) Seasonal trends in body mass, food intake and resting metabolic rate, and induction of metabolic depression in Arctic foxes (Alopex lagopus) at Svalbard. J Comp Physiol B 169:361–369

    Google Scholar 

  • Fuller WA, Stebbins LL, Dyke GR (1969) Overwintering of small mammals near Great Slave Lake northern Canada. Arctic 22:34–55

    Google Scholar 

  • Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

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

    Google Scholar 

  • Gockel J, Ruf T (2001) Alternative seasonal reproductive strategies in wild rodent populations. J Mammal 82:1034–1046

    Google Scholar 

  • Gorecki A (1969) Metabolic rate and energy budget of the striped field mouse. Acta Theriol 14:181–190

    Google Scholar 

  • Gorecki A (1971) Metabolism and energy budget in the Harvest mouse. Acta Theriol 15:213–220

    Google Scholar 

  • Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecol 84:2809–2815

    Google Scholar 

  • Haim A (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil Sekeetamys calurus: The role of photoperiod manipulations. J Therm Biol 21:37–42

    Google Scholar 

  • Haim A, Yahav S (1982) Non-shivering thermogenesis in winter-acclimatized and in long-scotophase and cold acclimated Apodemus mystacinus (Rodentia). J therm Biol 7:193–195

    Google Scholar 

  • Haim A, Racey PA, Speakman JR, Ellison GTH, Skinner JD (1991) Seasonal acclimation and thermoregulation in the pouched mouse Saccostomus campestris. J Therm Biol 16:13–17

    Google Scholar 

  • Haim A, McDevitt RM, Speakman JR (1995a) Daily Variations in the response of wood mice Apodemus sylvaticus to noradrenaline. J Exp Biol 198:561–565

    Google Scholar 

  • Haim A, McDevitt RM, Speakman JR (1995b) Thermoregulatory responses to manipulations of photoperiod in wood mice Apodemus sylvaticus from high latitudes (57°N). J Therm Biol 20:437–443

    Google Scholar 

  • Haim A, Shabtay A, Arad Z (1998) Thermoregulatory responses of mesic and xeric rodent species to photoperiod manipulations. Comp Biochem Physiol 120A:187–191

    Google Scholar 

  • Harrington LA, Biggins DE, Alldredge AW (2003) Basal metabolism of the black-footed ferret (Mustela nigripes) and the Siberian polecat (M. eversmannii). J Mammal 84:497–504

    Google Scholar 

  • Hart JS, Pohl H, Tener JS (1965) Seasonal acclimatization in varying hare (Lepus americanus). Can J Zool 43:731–744

    Google Scholar 

  • Hayes JP, Garland T (1995) The evolution of endothermy: Testing the aerobic capacity model. Evol 49:836–847

    Google Scholar 

  • Heldmaier G (1989) Seasonal acclimatization of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. In: Wieser W, Gnaiger E (eds) Energy transformations in cells and organisms. Georg Thieme Verlag, Stuttgart, pp 130–139

    Google Scholar 

  • Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian Hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol [B] 142:429–437

    Google Scholar 

  • Heydon MJ, Sibbald AM, Milne JA, Brinklow BR, Loudon ASI (1993) The interaction of food availability and endogenous physiological cycles on the grazing ecology of red deer hinds (Cervus elephus). Funct Ecol 7:216–222

    Google Scholar 

  • Heydon MJ, Milne JA, Brinklow BR, Loudon ASI (1995) Manipulating melatonin in red deer (Cervus elaphus): differences in the response to food restriction and lactation on the timing of the breeding season and prolactin-dependent pelage changes. J Exp Zool 273:12–20

    Google Scholar 

  • Hinds DS (1973) Acclimatization of thermoregulation in the desert cottontail, Sylvilagus audubonii. J Mammal 54:708–728

    Google Scholar 

  • Hyvärinen H (1984) Wintering strategy of voles and shrews in Finland. In: Merrit JF (ed) Winter ecology of small mammals. Carnegie Museum of Natural History, Pittsburgh, pp 139–148

    Google Scholar 

  • Iverson SL, Turner BN (1974) Winter weight dynamics in Microtus pennsylvanicus. Ecol 55:1030–1041

    Google Scholar 

  • Keesing F (1998) Ecology and behaviour of the pouched mouse, Saccostomus mearnsi, in Central Kenya. J Mammal 79:919–931

    Google Scholar 

  • Klaus S, Heldmaier G, Ricquier D (1988) Seasonal acclimation of bank voles and wood mice: nonshivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J Comp Physiol B 158:157–164

    Google Scholar 

  • Korhonen H, Harri M (1984) Seasonal changes in thermoregulation of the racoon dog (Nyctereutes procyonoides Gray 1834). Comp Biochem Physiol 77A:213–219

    Google Scholar 

  • Korn H (1989) The annual cycle in body weight of small mammals from the Transvaal, South Africa, as an adaptation to a subtropical seasonal environment. J Zool Lond 218:223–231

    Google Scholar 

  • Kozlowski J (1996) Energetic definition of fitness? Yes, but not that one. Am Nat 147:1087–1091

    Google Scholar 

  • Kozlowski J, Weiner J (1997) Interspecific allometries are the by-products of body size optimization. Am Nat 149:352–380

    Article  Google Scholar 

  • Lindstedt SL (1980) Energetics and water economy of the smallest desert mammal. Physiol Zool 53:82–97

    Google Scholar 

  • Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219

    Google Scholar 

  • Lovegrove BG (2001) The evolution of body armor in mammals: plantigrade constraints of large body size. Evol 55:1464–1473

    Google Scholar 

  • Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112

    Google Scholar 

  • Lovegrove BG, Haines L (2004) The evolution of placental mammal body sizes: Evolutionary history, form, and function. Oecological 138:13–27

    Google Scholar 

  • Lovegrove BG, Heldmaier G, Knight M (1991a) Seasonal and circadian energetic patterns in an arboreal rodent, Thallomys paedulcus, and a burrow-dwelling rodent, Aethomys namaquensis, from the Kalahari Desert. J Therm Biol 16:199–209

    Google Scholar 

  • Lovegrove BG, Heldmaier G, Ruf T (1991b) Perspectives of endothermy revisited: the endothermic temperature range. J Therm Biol 16:185–197

    Google Scholar 

  • Mcdevitt R, Andrews JF (1995) Seasonal variation in the metabolic rate of the pygmy shrew, Sorex minutus: Can resting metabolic rate be measured in post- absorptive shrews? J therm Biol 20:255–261

    Google Scholar 

  • McDevitt RM, Speakman JR (1996) Summer acclimatization in the short-tailed field vole, Microtus agrestis. J Comp Physiol B 166:286–293

    Google Scholar 

  • Merritt JF (1995) Seasonal thermogenesis and changes in body mass of masked shrews, Sorex cinereus. J Mammal 76:1020–1035

    Google Scholar 

  • Mesteig K, Huot J, Nault R, Blix AS (2000) Seasonal changes in heart rate and food intake in reindeer (Rangifer tarandus tarandus). Acta Physiol Scand 170:145–151

    Google Scholar 

  • Mezhzherin VA (1964) Dehnel’s phenomenon and its possible explanation. Acta Theriol 8:95–114

    Google Scholar 

  • Mitchell B, McCowan D, Nicholson IA (1976) Annual cycles of body weight and condition in Scottish red deer, Cervus elephas. J Zool 180:107–127

    Google Scholar 

  • Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285–296

    Google Scholar 

  • Nieminen M (2003) Nutritional and seasonal effects on the haematology and blood chemistry in reindeer (Rangifer tarandus tarandus L.). Comp Biochem Physiol 66A:399–413

    Google Scholar 

  • Nilssen KJ, Sundsfjord JA, Blix AS (1984) Regulation of metabolic rate in Svalbard and Norwegian reindeer. Am J Physiol 247:R837-R841

    Google Scholar 

  • Platt WJ (1974) Metabolic rates of short-tailed shrews. Physiol Zool 47:75–90

    Google Scholar 

  • Pokrovskij AV (1971) Seasonal changes in biological cycles in some rodents and the problem of absolute age determination. Ann Zool Fenn 8:94–96

    Google Scholar 

  • Reynolds PS, Lavigne DM (1988) Photoperiod effects on body size and energetics of the collared lemming, Dicrostonyx groenlandicus. Can J Zool 66:835–841

    Google Scholar 

  • Rogowitz GL (1990) Seasonal energetics of the white-tailed jackrabbit (Lepus townsendii). J Mammal 71:277–285

    Google Scholar 

  • Rosenmann M, Morrison PR, Feist P (1975) Seasonal changes in the metabolic capacity of red-backed voles. Physiol Zool 48:303–313

    Google Scholar 

  • Ruben J (1995) The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol 57:69–95

    Google Scholar 

  • Schmidt-Nielsen K (1983) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Scholander PF, Hock R, Walters V, Irving L (1950a) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol Bull 99:259–271

    Google Scholar 

  • Scholander PF, Hock R, Walters V, Johnson F, Irving L (1950b) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:225–236

    CAS  PubMed  Google Scholar 

  • Stewart AP, Barnett SA (1983) Seasonal changes in body weight and composition of Australian bush rats, Rattus fuscipes, and adaptation to winter. Aust J Zool 31:29–37

    Google Scholar 

  • Wang D, Wang Z (1996) Seasonal variations in thermogenesis and energy requirements of plateau pikas Ochotona curzoniae and root voles Microtus oeconomus. Acta Theriol 41:225–236

    Google Scholar 

  • Wang D, Wang Z, Lui 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

    Google Scholar 

  • Webster JR, Corson ID, Littlejohn RP, Stuart SK, Suttie JM (1999) Effects of photoperiod on the cessation of growth during autumn in male red deer and growth hormone and insulin-like growth factor-l secretion. Gen Comp Endocrinol 113:464–477

    Google Scholar 

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

    Google Scholar 

  • Worden KA, Pekins PJ (1995) Seasonal change in feed intake, body composition, and metabolic rate of white-tailed deer. Can J Zool 73:452–457

    Google Scholar 

  • Wunder BA, Dobkin DS, Gettinger RD (1977) Shifts of thermogenesis in the prairie vole (Microtus ochrogaster): strategies for survival in a seasonal environment. Oecol 29:11–26

    Google Scholar 

Download references

Acknowledgements

This research was financed by grants from the National Research Foundation and the University of Natal Research Fund.

Author information

Authors and Affiliations

  1. School of Biological and Conservation Sciences, University of KwaZulu-Natal, X01, Scottsville, 3209, South Africa

    Barry G. Lovegrove

Authors
  1. Barry G. Lovegrove
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barry G. Lovegrove.

Additional information

Communicated by G. Heldmaier

Appendices

Appendix 1

Table a Seasonal thermoregulatory parameters for mammals that were either acclimated to laboratory summer and winter conditions (photoperiod and ambient temperature) or were acclimatized in their natural habitats or outside enclosures. Abbreviations for zoogeographical zones: AfAfrotropical, HHolarctic, AuAustralasian, NNeotropical.
Full size table

Appendix 2

The phylogeny of all mammals whose data were used in the various multiple regression models. The letters that follow each species indicate whether the species data was used in each of the four major analyses, namely (a) the winter change in body mass, (b) the winter change in total basal power, (c) the winter change in body temperature, and d) the winter change in NST. Branch lengths were assigned according to an arbitrary algorithm (Pagel 1992). The topologies were taken from Lovegrove (2002, 2003) and Lovegrove and Haines (2004).

figure a

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lovegrove, B.G. Seasonal thermoregulatory responses in mammals. J Comp Physiol B 175, 231–247 (2005). https://doi.org/10.1007/s00360-005-0477-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-005-0477-1

Keywords

Search

Navigation