Comparative thermoregulatory physiology of two dunnarts, Sminthopsis macroura and Sminthopsis ooldea (Marsupialia : Dasyuridae)
Sean Tomlinson A C , Philip C. Withers A and Shane K. Maloney B
+ Author Affiliations
- Author Affiliations
A School of Animal Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, WA 6009, Australia.
B School of Anatomy, Physiology and Human Biology, Faculty of Life and Physical Sciences, The University of Western Australia, Crawley, WA 6009, Australia.
C Corresponding author. Email: sean.tomlinson@bgpa.wa.gov.au
Australian Journal of Zoology 60(1) 54-63 https://doi.org/10.1071/ZO12034
Submitted: 4 April 2012 Accepted: 27 June 2012 Published: 16 July 2012
Abstract
Metabolic rate and evaporative water loss (EWL) were measured to quantify the thermoregulatory patterns of two dasyurids, the stripe-faced dunnart (Sminthopsis macroura) and the Ooldea dunnart (S. ooldea) during acute exposure to Ta between 10 and 35°C. S. macroura maintained consistent Tb across the Ta range, whereas S. ooldea was more thermolabile. The metabolic rate of both species decreased from Ta = 10°C to BMR at Ta = 30°C. Mass-adjusted BMR at Ta = 30°C was the same for the two species, but there was no common regression of metabolic rate below the thermoneutral zone (TNZ). There was no significant difference between the species in allometrically corrected EWL at Ta = 30°C. Total EWL increased significantly at Ta = 10 and 35°C compared with the TNZ for S. macroura, but was consistent across the Ta range for S. ooldea. At any Ta below the TNZ, S. macroura required more energy per gram of body mass than S. ooldea, and had a higher EWL at the lower critical Ta. By being thermolabile S. ooldea reduced its energetic requirements and water loss at low Ta. The more constant thermoregulatory strategy of S. macroura may allow it to exploit a broad climatic envelope, albeit at the cost of higher energetic and water requirements. Since S. ooldea does not expend as much energy and water on thermoregulation this may be a response to the very low productivity, ‘hyperarid’ conditions of its central Australian distribution.
Additional keywords: evaporative water loss, metabolic rate, thermoregulation.
References
Angilletta, M. J. J. (2009). ‘Thermal Adaptation: a Theoretical and Empirical Synthesis.’ (Oxford University Press: Oxford.)Angilletta, M. J. J., Cooper, B. S., Schuler, M. S., and Boyles, J. G. (2010). The evolution of thermal physiology in endotherms. Frontiers in Bioscience E2, 861–881.
| The evolution of thermal physiology in endotherms.Crossref | GoogleScholarGoogle Scholar |
Archer, M. (1981). Results of the Archbold Expeditions. No. 104: Systematic revision of the marsupial dasyurid genus Sminthopsis Thomas. Bulletin of the American Museum of Natural History 168, 65–223.
Aslin, H. J. (1983). Ooldea Dunnart (Sminthopsis ooldea). In ‘The Australian Museum Complete Book of Australian Mammals’. (Ed. R. Strahan.) pp. 54. (Angus and Robertson: Sydney.)
Blacket, M. J., Krajewski, C., Labrinidis, A., Cambron, B., Cooper, S., and Westerman, M. (1999). Systematic relationships within the dasyurid marsupial tribe Sminthopsini – a multigene approach. Molecular Phylogenetics and Evolution 12, 140–155.
| Systematic relationships within the dasyurid marsupial tribe Sminthopsini – a multigene approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFWrsLc%3D&md5=ef234c83818b9ccf69d96f578c0b5198CAS |
Boyles, J. G., Smit, B., Sole, C. L., and McKechnie, A. E. (2012). Body temperature patterns in two syntopic elephant shrew species during winter. Comparative Biochemistry and Physiology. A. Comparative Physiology 161, 89–94.
| Body temperature patterns in two syntopic elephant shrew species during winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2ku7%2FN&md5=aae0c86e4f703e5d14e412408269e1bcCAS |
Bradley, W. G., and Yousef, M. K. (1972). Small mammals in the desert. In ‘Physiological Adaptations: Desert and Mountain’. (Eds M. K. Yousef, S. M. Horvath and R. W. Bullard.) pp. 127–142. (Academic Press: New York.)
Cohen, B. H. (2008). ‘Explaining Psychological Statistics.’ (John Wiley & Sons: New Jersey.)
Cooper, C. E., and Withers, P. C. (2009). Thermal, metabolic, hygric and ventilatory physiology of the sandhill dunnart (Sminthopsis psammophila; Marsupialia, Dasyuridae). Comparative Biochemistry and Physiology. A. Comparative Physiology 153, 317–323.
Cooper, C. E., and Withers, P. C. (2010). Comparative physiology of Australian quolls (Dasyurus; Marsupialia). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 180, 857–868.
| Comparative physiology of Australian quolls (Dasyurus; Marsupialia).Crossref | GoogleScholarGoogle Scholar |
Cooper, C. E., McAllan, B. M., and Geiser, F. (2005). Effect of torpor on the water economy of an arid-zone marsupial, the stripe-faced dunnart (Sminthopsis macroura). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 175, 323–328.
| Effect of torpor on the water economy of an arid-zone marsupial, the stripe-faced dunnart (Sminthopsis macroura).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MzksFSrug%3D%3D&md5=237e05dc9b8d7bb75b6f16976ac8454bCAS |
Cooper, C. E., Withers, P. C., and Cruz-Neto, A. P. (2009). Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiological and Biochemical Zoology 82, 153–162.
| Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7ltVWlsA%3D%3D&md5=f28500e476f6eec9f35b75436ab95e38CAS |
Degen, A. A. (1997). ‘Ecophysiology of Small Desert Mammals.’ (Springer-Verlag: Berlin.)
Ellison, G. T. H., and Skinner, J. D. (1992). The influences of ambient temperature on spontaneous daily torpor in pouched mice (Saccstomus campestris: Rodentia – Cricetidae) from southern Africa. Journal of Thermal Biology 17, 25–31.
| The influences of ambient temperature on spontaneous daily torpor in pouched mice (Saccstomus campestris: Rodentia – Cricetidae) from southern Africa.Crossref | GoogleScholarGoogle Scholar |
Ewer, R. F. (1968). A preliminary survey of the behaviour in captivity of the dasyurid marsupial, Sminthopsis crassicaudata (Gould). Zeitschrift für Tierpsychologie 25, 319–365.
| 1:STN:280:DyaF1M%2FhtlWmtg%3D%3D&md5=d7dd359a7514068f77b655ae38701df4CAS |
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.
| Phylogenies and the comparative method.Crossref | GoogleScholarGoogle Scholar |
Garland, T. J., and Adolph, S. C. (1994). Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67, 797–828.
Geiser, F. (2004). The role of torpor in the life of arid zone mammals. Australian Mammalogy 26, 125–134.
Geiser, F., and Baudinette, R. V. (1985). The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 156, 129–134.
| The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia).Crossref | GoogleScholarGoogle Scholar |
Geiser, F., and Baudinette, R. V. (1987). Seasonality of torpor and thermoregulation in three dasyurid marsupials. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 157, 335–344.
| Seasonality of torpor and thermoregulation in three dasyurid marsupials.Crossref | GoogleScholarGoogle Scholar |
Hart, J. S. (1971). Rodents. In ‘Comparative Physiology of Thermoregulation’. (Ed. G. C. Whittow.) pp. 1–149. (Academic Press: New York.)
Hayes, J. P., and Shonkwiler, J. S. (2006). Allometry, antilog transformations, and the perils of prediction on the original scale. Physiological and Biochemical Zoology 79, 665–674.
| Allometry, antilog transformations, and the perils of prediction on the original scale.Crossref | GoogleScholarGoogle Scholar |
Hinds, D. S., and MacMillen, R. E. (1986). Scaling of evaporative water loss in marsupials. Physiological Zoology 59, 1–9.
Hinds, D. S., Baudinette, R. V., MacMillen, R. E., and Halpern, E. A. (1993). Maximum metabolism and the aerobic factorial scope of endotherms. The Journal of Experimental Biology 182, 41–56.
| 1:STN:280:DyaK2c%2FksFCitw%3D%3D&md5=9100c07957d59a6876569f73a4cf46f6CAS |
Holloway, J. C., and Geiser, F. (1995). Influence of torpor on daily energy expenditure of the dasyurid marsupial Sminthopsis crassicaudata. Comparative Biochemistry and Physiology 112A, 59–66.
| 1:CAS:528:DyaK2MXnvVylu7k%3D&md5=466407261c53b97cd6f20bb80b4433bdCAS |
Körtner, G., and Geiser, F. (2009). The key to winter survival: daily torpor in a small arid-zone marsupial. Naturwissenschaften 96, 525–530.
| The key to winter survival: daily torpor in a small arid-zone marsupial.Crossref | GoogleScholarGoogle Scholar |
Lawrence, E. (2005). ‘Henderson’s Dictionary of Biology.’ 13th edn. (Pearson Educational: Harlow.)
Lovegrove, B. G. (2003). The influence of climate on the basal metabolic rate of small mammals: a slow–fast metabolic continuum. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 173, 87–112.
| 1:STN:280:DC%2BD3s7htVyksQ%3D%3D&md5=f62179672e9aba02ff60dd0566517728CAS |
MacMillen, R. E. (1983). Adaptive physiology of heteromyid rodents. Great Basin Naturalist Memoirs 7, 65–76.
MacMillen, R. E. (1990). Water economy of granivorous birds: a predictive model. The Condor 92, 379–392.
| Water economy of granivorous birds: a predictive model.Crossref | GoogleScholarGoogle Scholar |
MacMillen, R. E., and Baudinette, R. V. (1993). Water economy of granivorous birds: Australian parrots. Functional Ecology 7, 704–712.
| Water economy of granivorous birds: Australian parrots.Crossref | GoogleScholarGoogle Scholar |
MacMillen, R. E., and Hinds, D. S. (1983). Water regulatory efficiency in heteromyid rodents: a model and its application. Ecology 64, 152–164.
| Water regulatory efficiency in heteromyid rodents: a model and its application.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., Burbidge, A. A., and Baynes, A. (2006). Australian Mammal Map Updates. Available at www.naturebase.com.au/science/mupdates.html.
McNab, B. K., and Morrison, P. (1963). Body temperature and metabolism in subspecies of Peromyscus from arid and mesic environments. Ecological Monographs 33, 63–82.
| Body temperature and metabolism in subspecies of Peromyscus from arid and mesic environments.Crossref | GoogleScholarGoogle Scholar |
Morton, S. R. (1978). Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia). Journal of Mammalogy 59, 569–575.
| Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia).Crossref | GoogleScholarGoogle Scholar |
Morton, S. R. (1983a). Fat-tailed Dunnart Sminthopsis crassicaudata. In ‘The Australian Museum Complete Book of Australian Mammals’. (Ed. R. Strahan.) pp. 61–62. (Angus and Robertson Publishers: Sydney.)
Morton, S. R. (1983b). Stipe-faced Dunnart Sminthopsis macroura. In ‘The Australian Museum Complete Book of Australian Mammals’. (Ed. R. Strahan.) pp. 63–64. (Angus and Robertson Publishers: Sydney.)
Noll-Banholzer, U. G. (1979). Body temperature, oxygen consumption, evaporative water loss and heart rate in the fennec. Comparative Biochemistry and Physiology. A. Comparative Physiology 62, 585–592.
| Body temperature, oxygen consumption, evaporative water loss and heart rate in the fennec.Crossref | GoogleScholarGoogle Scholar |
Ostrowski, S., Williams, J. B., Mésochina, P., and Sauerwein, H. (2006). Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to long-term food and water restriction. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 176, 191–201.
| Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to long-term food and water restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvFajtLg%3D&md5=d0d0724ac45ca69bdd84be9ea00760f7CAS |
Ricklefs, R. E. (1973). ‘Ecology.’ (Chiron Press: Newton, MA.)
Schmidt, S., Withers, P. C., and Cooper, C. E. (2009). Metabolic, ventilatory and hygric physiology of the chuditch (Dasyurus geoffroii; Marsupialia, Dasyuridae). Comparative Biochemistry and Physiology. A. Comparative Physiology 154, 92–97.
| 1:STN:280:DC%2BD1MvnslWltA%3D%3D&md5=18c1a71dbce19f1907fbdfb5cbb8e3a4CAS |
Song, X., and Geiser, F. (1997). Daily torpor and energy expenditure in Sminthopsis macroura: interactions between food and water availability and temperature. Physiological Zoology 70, 331–337.
| 1:STN:280:DyaK2sznsFSgsA%3D%3D&md5=31a7ed8c10a5fa88fd58f5dd56c04ce5CAS |
Song, X., Körtner, G., and Geiser, F. (1995). Reduction of metabolic rate and thermoregulation during daily torpor. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 165, 291–297.
| Reduction of metabolic rate and thermoregulation during daily torpor.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2FksFGisw%3D%3D&md5=a0fc2e9103cca8d5e862b3288209af21CAS |
Song, X., Körtner, G., and Geiser, F. (1998). Temperature selection and use of torpor by the marsupial Sminthopsis macroura. Physiology & Behavior 64, 675–682.
| Temperature selection and use of torpor by the marsupial Sminthopsis macroura.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXms1Gju7w%3D&md5=73fcd6f8e80b9570481ab4f0afb10078CAS |
Tomlinson, S. (2012). Physiological and behavioural responses of Western Australian dunnarts (Sminthopsis spp.) to energetic challenge. Ph.D. Thesis, University of Western Australia, Perth.
Tomlinson, S., Withers, P. C., and Cooper, C. (2007). Hypothermia versus torpor in response to cold stress in the native Australian mouse Pseudomys hermannsburgensis and the introduced house mouse Mus musculus. Comparative Biochemistry and Physiology. A. Comparative Physiology 148, 645–650.
Warnecke, L., Cooper, C. E., Geiser, F., and Withers, P. C. (2010). Environmental physiology of a small marsupial inhabiting arid floodplains. Comparative Biochemistry and Physiology. A. Comparative Physiology 157, 73–78.
| 1:STN:280:DC%2BC3cnot1Sjtg%3D%3D&md5=013afa5e513da0bdf7c5cd7e8c1a91f6CAS |
Williams, J. B., Lenain, D., Ostrowski, S., Tieleman, B. I., and Seddon, P. J. (2002). Energy expenditure and water flux of Rüppell’s foxes in Saudi Arabia. Physiological and Biochemical Zoology 75, 479–488.
| Energy expenditure and water flux of Rüppell’s foxes in Saudi Arabia.Crossref | GoogleScholarGoogle Scholar |
Withers, P. C. (1992). ‘Comparative Animal Physiology.’ (Saunders College Publishing: Fort Worth, TX.)
Withers, P. C. (2001). Design, calibration and calculation for flow-through respirometry systems. Australian Journal of Zoology 49, 445–461.
Withers, P. C., and Cooper, C. E. (2009). Thermal, metabolic and hygric physiology of the little red kaluta, Dasykaluta rosamondae (Dasyuromorphia: Dasyuridae). Journal of Mammalogy 90, 752–760.
| Thermal, metabolic and hygric physiology of the little red kaluta, Dasykaluta rosamondae (Dasyuromorphia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Withers, P. C., and Cooper, C. E. (2011). Using a priori contrasts for multivariate repeated-measures ANOVA to analyze thermoregulatory responses of the dibbler (Parantechinus apicalis; Marsupialia, Dasyuridae). Physiological and Biochemical Zoology 84, 514–521.
| Using a priori contrasts for multivariate repeated-measures ANOVA to analyze thermoregulatory responses of the dibbler (Parantechinus apicalis; Marsupialia, Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Withers, P. C., Richardson, K. C., and Wooller, R. D. (1990). Metabolic physiology of euthermic and torpid honey possums. Australian Journal of Zoology 37, 685–693.
| Metabolic physiology of euthermic and torpid honey possums.Crossref | GoogleScholarGoogle Scholar |
Withers, P. C., Cooper, C. E., and Buttermer, W. A. (2004). Are day-active small mammals rare and small birds abundant in Australian desert environments because small mammals are not such good thermoregulators? Australian Mammalogy 26, 117–124.
Withers, P. C., Cooper, C. E., and Larcombe, A. N. (2006). Environmental correlates of physiological variables in marsupials. Physiological and Biochemical Zoology 79, 437–453.
| Environmental correlates of physiological variables in marsupials.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283ms1WhsQ%3D%3D&md5=add45459cc89227dbea0080dfcfd1b71CAS |
Zar, J. H. (1999). ‘Biostatistical Analysis.’ (Prentice Hall: Upper Saddle River, NJ.)
