Abstract
Mammalian hibernation, which lasts on average for about 6 months, can reduce energy expenditure by >90% in comparison to active individuals. In contrast, the widely held view is that daily torpor reduces energy expenditure usually by about 30%, is employed for a few hours every few days, and often occurs only under acute energetic stress. This interpretation is largely based on laboratory studies, whereas knowledge on daily torpor in the field is scant. We used temperature telemetry to quantify thermal biology and activity patterns of a small arid-zone marsupial, the stripe-faced dunnart Sminthopsis macroura (16.9 g), in the wild and to test the hypothesis that daily torpor is a crucial survival strategy of this species in winter. All individuals entered torpor daily with the exception of a single male that remained normothermic for a single day (torpor on 212 of 213 observation days, 99.5%). Torpor was employed at air temperatures (T a) ranging from approximately −1°C to 36°C. Dunnarts usually entered torpor during the night and aroused at midday with the daily increase of T a. Torpor was on average about twice as long (mean 11.0 ± 4.7 h, n = 8) than in captivity. Animals employed sun basking during rewarming, reduced foraging time significantly, and occasionally omitted activity for several days in sequence. Consequently, we estimate that daily torpor in this species can reduce daily energy expenditure by up to 90%. Our study shows that for wild stripe-faced dunnarts daily torpor is an essential mechanism for overcoming energetic challenges during winter and that torpor data obtained in the laboratory can substantially underestimate the ecological significance of daily torpor in the wild.
References
Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften. doi:10.1007/s00114-008-0471-z
Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181
Cooper CE, McAllan BM, Geiser F (2005) Effect of torpor on the water economy of an arid-zone marsupial, the striped-faced dunnart (Sminthopsis macroura). J Comp Physiol B 175:323–328
Dickman CR (2003) Distributional ecology of dasyurid marsupials. In: Jones M, Dickman CR, Archer M (eds) Predators with pouches: the biology of carnivorous marsupials. CSIRO Publishing, Collingwood, pp 318–331
French AR (1985) Allometrics of the duration of torpid and euthermic intervals during mammalian hibernation: a test of the theory of metabolic control of the timing of changes in body temperature. J Comp Physiol B 156:13–19
Geiser F (2004) The role of torpor in the life of arid zone mammals. Aust Mammal 26:125–134
Geiser F (2007) Yearlong hibernation in a marsupial mammal. Naturwissenschaften 94:941–944
Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344
Geiser F, Drury RL (2003) Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B 173:55–60
Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patters. Physiol Zool 68:935–966
Geiser F, Holloway JC, Körtner G, Maddocks TA, Turbill C, Brigham RM (2000) Do patterns of torpor differ between free-ranging and captive mammals and birds? In: Heldmaier G, Klingenspor M (eds) Life in the cold: 11th International Hibernation Symposium. Springer, Berlin, pp 95–102
Geiser F, Drury RL, Körtner G, Maddocks TA, Turbill C, Pavey CR, Brigham RM (2004) Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation, and application. 12th International Hibernation Symposium. Biological Papers of the University of Alaska No. 27, Fairbanks, pp 51–62
Godfrey GK (1968) Body temperatures and torpor in Sminthopsis crassicaudata and S. larapinta (Marsupialia: Dasyuridae). J Zool (Lond) 156:499–511
Gutman R, Choshniak I, Kronfeld-Schor N (2006) Defending body mass during food restriction in Acomys russatus: a desert rodent that does not store food. Am J Physiol 290:R881–R891
Holloway JC, Geiser F (1995) Influence of torpor on daily energy expenditure of the dasyurid marsupial Sminthopsis crassicaudata. Comp Biochem Physiol 112A:59–66
Holloway JC, Geiser F (1996) Reproductive status and torpor of the marsupial Sminthopsis crassicaudata: effects of photoperiod. J Therm Biol 21:373–380
Hiebert SM, Fulkerson E, Lindermayer K, McClure S (2000) The effect of temperature on preference for dietary unsaturated fatty acids in the Djungarian hamster (Phodopus sungorus). Can J Zool 78:1361–1368
Körtner G, Geiser F (1998) Ecology of natural hibernation in the marsupial mountain pygmy-possum (Burramys parvus). Oecologia 113:170–178
Körtner G, Geiser F (2000a) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128
Körtner G, Geiser F (2000b) Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123:350–357
Körtner G, Pavey CR, Geiser F (2008) Thermal biology, torpor and activity in free-living mulgaras in arid zone Australia during the winter reproductive season. Physiol Biochem Zool 81:442–451
Lovegrove BG, Körtner G, Geiser F (1999) The energetic cost of arousal in the marsupial Sminthopsis macroura: benefits from summer ambient temperature cycles. J Comp Physiol B 169:11–18
Lynch GR, Vogt FD, Smith HR (1978) Seasonal study of spontaneous daily torpor in the white-footed mouse Peromyscus leucopus. Physiol Zool 51:289–297
McAllan BM (2003) Timing of reproduction in carnivorous marsupials. In: Jones M, Dickman CR, Archer M (eds) Predators with pouches: the biology of carnivorous marsupials. CSIRO, Collingwood, pp 147–168
Morton SR (1978) Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia). J Mammal 59:569–575
Morton SR, Dickman CR (2008) Stripe-faced dunnart, Sminthopsis macroura. In: Van Dyck S, Strahan R (eds) The mammals of Australia. Reed New Holland, Sydney, pp 150–152
Ruf T, Heldmaier G (1992) The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol Zool 65:994–1010
Ruf T, Klingenspor M, Preis H, Heldmaier G (1991) Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity, and social behaviour. J Comp Physiol B 60:609–515
Song X, Körtner G, Geiser F (1995) Reduction of metabolic rate and thermoregulation during daily torpor. J Comp Physiol B 165:291–297
Stamper JL, Dark J, Zucker I (1999) Photoperiod modulates torpor and food intake in Siberian hamsters challenged with metabolic inhibitors. Physiol Behav 66:113–118
Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol 293:R468–R473
Warnecke L, Turner JM, Geiser F (2008) Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95:73–78
Withers PC (1992) Comparative animal physiology. Saunders, Fort Worth
Acknowledgements
We wish to thank the Queensland Parks and Wildlife Service for allowing us to use their facilities and helping with transport of fuel. Aaron Trachtenberg and Paul Story helped with trapping and radio-tracking the animals. Stuart Cairns and Thomas Ruf helped with some of the statistical procedures. The study was conducted under permits from the Queensland Environmental Protection Agency and the University of New England Animal Ethics Committee. The study was supported by the Australian Research Council and a fellowship from the Vice Chancellor of UNE.
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Körtner, G., Geiser, F. The key to winter survival: daily torpor in a small arid-zone marsupial. Naturwissenschaften 96, 525–530 (2009). https://doi.org/10.1007/s00114-008-0492-7
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DOI: https://doi.org/10.1007/s00114-008-0492-7