Abstract
Marsupials have a slow rate of development and this allows a detailed examination of thermoregulatory developmental changes and stages. We quantified the cooling rates of marsupial dunnarts (Sminthopsis crassicaudata) at 40–56 days (d) old, and torpor and basking behaviour in animals given the option to bask in four age groups from 60 to 150 d. The development of thermoregulation was a continuum, but was characterised by three major thermoregulatory stages: (1) at 40 d, animals were unable to maintain a constant high body temperature during short-term cold exposure; (2) at 60 d, animals could maintain a high T b for the first part of the night at an ambient temperature of 15.0 ± 0.7 °C; later in the night, they entered an apparent torpor bout but could only rewarm passively when basking under a heat lamp; (3) from ~90 d, they expressed prolonged torpor bouts and were able to rewarm endogenously. Young newly weaned 60 d animals were able to avoid hypothermia by basking. In this case, basking was not an optional behavioural method of reducing the cost of rewarming from torpor, but was essential for thermoregulation independent of the nest temperature. Results from our study suggest that basking is a crucial behavioural trait that permits young marsupials and perhaps other juvenile altricial mammals to overcome the developmental stage between poikilothermy early in development and full endothermy later in life.
Similar content being viewed by others
References
Arnold W (1988) Social thermoregulation during hibernation in alpine marmots (Marmota marmota). J Comp Physiol B 158:151–156. doi:10.1007/BF01075828
Barclay RMR, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79:1885–1890. doi:10.1139/z01-138
Bartholomew GA (1956) Temperature regulation in the macropod marsupial, Setonix brachyurus. Physiol Zool 29:26–40
Bartholomew GA, Rainy M (1971) Regulation of body temperature in the rock hyrax, Heterohyrax brucei. J Mammal 52:81–95. doi:10.2307/1378434
Bradley SR, Deavers DR (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol A 65A:465–476. doi:10.1016/0300-9629(80)90060-2
Currie SE, Noy K, Geiser F (2015) Passive rewarming from torpor in hibernating bats: minimizing metabolic costs and cardiac demands. Am J Physiol 308:R34–R41. doi:10.1152/ajpregu.00341.2014
Dawson WR, Evans FC (1960) Relation of growth and development to temperature regulation in nestling vesper sparrows. Condor 62:329–340. doi:10.2307/1365163
Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol A 150:176–180. doi:10.1016/j.cbpa.2007.02.041
Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world. Springer, Berlin, Heidelberg, New York, pp 109–121. doi:10.1007/978-3-642-28678-0_10
Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothermy? Naturwissenschaften 89:412–414. doi:10.1007/s00114-002-0349-4
Geiser F, Drury RL, Körtner G, Turbill C, Pavey C, 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: 12th international hibernation symposium. Institute of Arctic Biology, University of Alaska, Fairbanks, pp 51–62
Geiser F, Westman W, McAllan BM, Brigham RM (2006) Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications. J Comp Physiol B 176:107–116. doi:10.1007/s00360-005-0026-y
Geiser F, Currie SE, O’Shea KA, Hiebert SM (2014) Torpor and hypothermia: reversed hysteresis of metabolic rate and body temperature. Am J Physiol 307:R1324–R1329. doi:10.1152/ajpregu.00214.2014
Geiser F, Gasch K, Bieber C, Stalder GL, Gerritsmann H, Ruf T (2016) Basking hamsters reduce resting metabolism, body temperature and energy costs during rewarming from torpor. J Exp Biol 219:2166–2172. doi:10.1242/jeb.137828
Gilbert C, Blanc S, Trabalon SG, Maho YL, Perret M, Ancel A (2007) Role of huddling on the energetic of growth in a newborn altricial mammal. Am J Physiol Regul Integr Comp Physiol 293:R867–R976. doi:10.1152/ajpregu.00081.2007
Gilbert C, McCafferty D, Maho YL, Martrette J, Giroud S, Blanc S, Ancel A (2010) One for all and all for one: the energetic benefits of huddling in endotherms. Biol Rev Camb Philos Soc 85:545–569. doi:10.1111/j.1469-185X.2009.00115.x
Giroud S, Zahn S, Criscuolo F, Chery I, Blanc S, Turbill C, Ruf T (2014) Late-born intermittently fasted juvenile garden dormice use torpor to grow and fatten prior to hibernation: consequences for ageing processes. Proc Roy Soc Lond B Biol 281:1–9. doi:10.1098/rspb.2014.1131
Godfrey GK, Crowcroft P (1971) Breeding the fat-tailed marsupial mouse Sminthopsis crassicaudata. Int Zoo Yearb 11:33–38. doi:10.1111/j.1748-1090.1971.tb01839.x
Hill RW (1976) The ontogeny of homeothermy in neonatal Peromyscus leucopus. Physiol Zool 49:292–306
Hulbert AJ (1988) Metabolism and the development of endothermy. In: Tyndale-Biscoe CH, Janssens PA (eds) The developing marsupial: models for biomedical research. Springer, Berlin, pp 148–161. doi:10.1007/978-3-642-88402-3_11
Janssens PA, Hulbert AJ, Baudinette RV (1997) Development of pouch young from birth to pouch vacation. In: Saunders N, Hinds L (eds) Marsupial biology: recent research, new perspectives. University of New South Wales Press LTD, Sydney, pp 71–89
Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic, New York
Morrison P, Petajan JH (1962) The development of temperature regulation in the opossum, Didelphis marsupialis virginiana. Physiol Zool 35:52–65
Mortola JP, Frappell PB, Woolley PA (1999) Breathing through skin in a newborn mammal. Nature 397:660–661. doi:10.1038/17713
Petajan JH, Morrison P (1962) Physical and physiological factors modifying the development of temperature regulation in the opossum. J Exp Biol 149:45–57. doi:10.1002/jez.1401490106
Rojas AD, Körtner G, Geiser F (2012) Cool running: locomotor performance at low body temperature in mammals. Biol Lett 8:868–870. doi:10.1098/rsbl.2012.0269
Ruf T, Geiser F (2015) Daily torpor and hibernaton in birds and mammals. Biol Rev 90:891–926. doi:10.1111/brv.12137
Russell EM (1982) Patterns of parental care and parental investment in marsupials. Biol Rev 57:423–486. doi:10.1111/j.1469-185X.1982.tb00704.x
Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. 5th edition. Cambridge University Press, Cambridge
Schradin C, Schubert M, Pillay N (2006) Winter huddling groups in the striped mouse. Can J Zool 84:693–698. doi:10.1139/z06-048
Schradin C, Krackow S, Schubert M, Keller C, Schradin B, Pillay N (2007) Regulation of activity in desert-living striped mice: the importance of basking. Ethology 113:606–614. doi:10.1111/j.1439-0310.2007.01361.x
Sealander JA (1952) The relationship of nest protection and huddling to survival of Peromyscus at low temperature. Ecology 33:63–71
Signer C, Ruf T, Arnold W (2011) Hypometabolism and basking: the strategies of Alpine ibex to endure harsh over-wintering conditions. Funct Ecol 25:537–547. doi:10.1111/j.1365-2435.2010.01806.x
Steudel K, Porter WP, Sher D (1994) The biophysics of Bergmann’s rule: a comparison of the effects of pelage and body size variation on metabolic rate. Can J Zool 72:70–77. doi:10.1139/z94-010
Terrien J, Perret M, Aujard F (2011) Behavioral thermoregulation in mammals: a review. Front Biosci 16:1428–1444. doi:10.2741/3797
Thompson ML, Mzilikazi N, Bennett NCM, McKechnie AE (2015) Solar radiation during rewarming from torpor in Elephant Shrews: supplementation or substitution of endogenous heat production? PLoS One. doi:10.1371/journal.pone.0120442
Tyndale-Biscoe CH, Renfree M (1987) Reproductive physiology of marsupials. Cambridge University Press, Cambridge
Wacker CB, Rojas AD, Geiser F (2012) The use of small subcutaneous transponders for quantifying thermal biology and torpor in small mammals. J Therm Biol 37:250–254. doi:10.1016/j.jtherbio.2011.11.007
Wacker CB, McAllan BM, Körtner G, Geiser F (2016) The functional requirements of mammalian hair: a compromise between crypsis and thermoregulation? The Science of Nature 103:1–9. doi:10.1007/s00114-016-1376-x
Warnecke L, Turner J, Geiser F (2008) Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95:73–78. doi:10.1007/s00114-007-0293-4
Warnecke L, Schleucher E, Geiser F (2010) Basking behaviour in relation to energy use and food availability in one of the smallest marsupials. Physiol Behav 101:389–393. doi:10.1016/j.physbeh.2010.07.003
Westman W, Körtner G, Geiser F (2002) Developmental thermoenergetics of the dasyurid marsupial, Antechinus stuartii. J Mammal 83:81–90. doi:10.1644/1545-1542(2002)083<0081:DTOTDM>2.0.CO;2
Withers PC (1977) Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask. J Appl Physiol 42:120–123
Acknowledgements
This project was funded by an Australian Postgraduate Award to CW and an Australian Research Council Grant (DP130101506) to FG.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Additional information
Communicated by I. D. Hume.
Rights and permissions
About this article
Cite this article
Wacker, C.B., McAllan, B.M., Körtner, G. et al. The role of basking in the development of endothermy and torpor in a marsupial. J Comp Physiol B 187, 1029–1038 (2017). https://doi.org/10.1007/s00360-017-1060-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-017-1060-2