Abstract
Quolls (Dasyurus) are medium-sized carnivorous dasyurid marsupials. Tiger (3,840 g) and eastern quolls (780 g) are mesic zone species, northern quolls (516 g) are tropical zone, and chuditch (1,385 g) were once widespread through the Australian arid zone. We found that standard physiological variables of these quolls are consistent with allometric expectations for marsupials. Nevertheless, inter-specific patterns amongst the quolls are consistent with their different environments. The lower T b of northern quolls (34°C) may provide scope for adaptive hyperthermia in the tropics, and they use torpor for energy/water conservation, whereas the larger mesic species (eastern and tiger quolls) do not appear to. Thermolability varied from little in eastern (0.035°C °C−1) and tiger quolls (0.051°C ºC−1) to substantial in northern quolls (0.100°C ºC−1) and chuditch (0.146°C ºC−1), reflecting body mass and environment. Basal metabolic rate was higher for eastern quolls (0.662 ± 0.033 ml O2 g−1 h−1), presumably reflecting their naturally cool environment. Respiratory ventilation closely matched metabolic demand, except at high ambient temperatures where quolls hyperventilated to facilitate evaporative heat loss; tiger and eastern quolls also salivated. A higher evaporative water loss for eastern quolls (1.43 ± 0.212 mg H2O g−1 h−1) presumably reflects their more mesic distribution. The point of relative water economy was low for tiger (−1.3°C), eastern (−12.5°C) and northern (+3.3) quolls, and highest for the chuditch (+22.6°C). We suggest that these differences in water economy reflect lower expired air temperatures and hence lower respiratory evaporative water loss for the arid-zone chuditch relative to tropical and mesic quolls.
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Abbreviations
- BMR:
-
Basal metabolic rate
- C dry :
-
Dry (non-evaporative) thermal conductance
- C wet :
-
Wet (evaporative and non-evaporative) thermal conductance
- EHL:
-
Evaporative heat loss
- EO2:
-
Oxygen extraction
- EQ:
-
Evaporative quotient
- EWL:
-
Evaporative water loss
- f R :
-
Respiratory frequency
- MHP:
-
Metabolic heat production
- MWP:
-
Metabolic water production
- MR:
-
Metabolic rate
- PRWE:
-
Point of relative water economy
- RER:
-
Respiratory exchange ratio
- RH:
-
Relative humidity
- RWE:
-
Relative water economy
- SNK:
-
Student–Newman–Keuls post hoc multiple comparison test
- T a :
-
Ambient temperature
- T b :
-
Body temperature
- VCO2:
-
Carbon dioxide production rate
- V I :
-
Minute volume
- VO2:
-
Oxygen consumption rate
- V T :
-
Tidal volume
References
Arnold J (1976) Growth and bioenergetics of the chuditch, Dasyurus geoffroii. Ph.D. thesis, Department of Zoology, University of Western Australia, Perth
Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of Cercaertus nanus. Physiol Zool 35:94–107
Belcher CA, Nelson JL, Darrant JP (2007) Diet of the tiger quoll (Dasyurus maculatus) in south-eastern Australia. Aust J Zool 55:117–122
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SAR, Vos A, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512
Blackhall S (1980) Diet of the eastern native-cat, Dasyurus viverrinus (Shaw), in southern Tasmania. Aust Wildl Res 7:191–197
Braithwaite RW, Griffiths AD (1994) Demographic variation and range contraction in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae). Wildl Res 21:203–217
Careau V, Morand-Ferron J, Thomas D (2007) Basal metabolic rate of canids from hot deserts to cold arctic climates. J Mamm 88:394–400
Cheverud JM, Dow MM (1985) An autocorrelation analysis of genetic variation due to lineal fission in social groups of Rhesus macaques. Am J Phys Anth 67:113–121
Cooper CE, Cruz-Neto AP (2009) Metabolic, hygric and ventilatory physiology of a hypermetabolic marsupial, the honey possum (Tarsipes rostratus). J Comp Physiol B 179:773–781
Cooper CE, Geiser F (2008) The “minimum boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review. J Comp Physiol B 178:1–8
Cooper CE, Withers PC (2002) Metabolic physiology of the numbat (Myrmecobius fasciatus). J Comp Physiol 172:669–675
Cooper CE, Withers PC (2004) Ventilatory physiology of the numbat (Myrmecobius fasciatus). J Comp Physiol B 174:107–111
Cooper CE, Withers PC (2006) Numbats and aardwolves—how low is low? A re-affirmation of the need for statistical rigour in evaluating regression predictions. J Comp Physiol B 176:623–629
Cooper CE, Withers PC (2008) Allometry of evaporative water loss in marsupials: implications of the effect of ambient relative humidity on the physiology of brushtail possums (Trichosurus vulpecula). J Exp Biol 211:2759–2766
Cooper CE, Withers PC (2009) Effects of measurement duration on the determination of basal metabolic rate and evaporative water loss of small marsupials: How long is long enough? Physiol Biochem Zool 82:438–446
Cooper CE, Geiser F, McAllan B (2005) Effect of torpor on the water economy of an arid-zone dasyurid, the stripe-faced dunnart (Sminthopsis macroura). J Comp Physiol B 175:323–328
Cooper CE, Withers PC, Cruz-Neto AP (2009) Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol Biochem Zool 82:153–162
Cooper CE, Withers PC, Cruz-Neto AP (2010) Metabolic, ventilatory and hygric physiology of a South American marsupial, the long-furred woolly mouse opossum. J Mamm (in press)
Degabriele R, Dawson TJ (1979) Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol 134:293–301
Edgar R, Belcher C (1995) Spotted-tailed quoll. In: Strahan R (ed) The mammals of Australia, 2nd edn. Australian Museum/Reed Books, Sydney, pp 67–69
Elgar MA, Harvey PH (1987) Basal metabolic rates in mammals: allometry, phylogeny and ecology. Funct Ecol 1:25–36
Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16
Geiser F (2003) Thermal biology and energetics of carnivorous marsupials. In: Jones M, Dickman C, Archer M (eds) Predators with pouches: the biology of carnivorous marsupials CSIRO, Melbourne, pp 238–253
Geiser F (2004) The role of torpor in the life of Australian arid zone mammals. Aust Mammal 26:125–134
Glen AS, Cardoso MJ, Dickman CR, Firestone KB (2009) Who’s your daddy? Paternity testing reveals promiscuity and multiple paternity in the carnivorous marsupial Dasyurus maculatus (Marsupialia: Dasyuridae). Biol J Linn Soc 96:1–7
Godsell J (2002) Eastern quoll. In: Strahan R (ed) The mammals of Australia. Reed New Holland, Sydney
Harvey PH, Pagel MD, Rees JA (1991) Mammalian metabolism and life histories. Am Nat 137:556–566
Hayes JP, Shonkwiler JS (2006) Allometry, antilog transformations, and the perils of prediction on the original scale. Physiol Biochem Zool 79:665–674
Hayes JP, Shonkwiler JS (2007) Erratum: Allometry, antilog transformations, and the perils of prediction on the original scale. Physiol Biochem Zool 80:556
Hayssen V, Lacy C (1985) Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol A 81:741–754
Hinds DS, MacMillen RE (1986) Scaling of evaporative water loss in marsupials. Physiol Zool 59:1–9
Hinds DS, Baudinette RV, MacMillen RE, Halpern EA (1993) Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol 182:41–56
Hudson JW (1962) The role of water in the biology of the antelope ground squirrel Citellus leucurus. Univ Calif Pub Zool 64:1–56
Jones ME, Barmuta LA (1998) Diet overlap and relative abundance of sympatric dasyurid carnivores: a hypothesis of competition. J An Ecol 67:410–421
Jones ME, Rose RK (2001) Dasyurus viverrinus. Mamm Species 677:1–9
Jones ME, Grigg GC, Beard LA (1997) Body temperatures and activity patterns of Tasmanian devils (Sarcophilus harrisii) and eastern quolls (Dasyurus viverrinus) through a subalpine winter. Physiol Zool 70:53–60
Jones ME, Rose RK, Barnett S (2001) Dasyurus maculatus. Mamm Species 676:1–9
Koteja P (1996) Measuring energy metabolism with open-flow respirometric systems: Which design to choose? Func Ecol 10:675–677
Larcombe AN (2002) Effects of temperature on metabolism, ventilation, and oxygen extraction in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae). Physiol Biochem Zool 75:405–411
Larcombe AN (2004) Comparative metabolic, thermoregulatory and ventilatory physiology of bandicoots (Peramelidae). Ph.D. thesis, Zoology, University of Western Australia, Perth
Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219
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
MacMillen RE (1965) Aestivation in the cactus mouse Peromyscus eremicus. Comp Biochem Physiol 16:227–248
MacMillen RE (1990) Water economy of granivorous birds: a predictive model. Condor 92:379–392
MacMillen RE, Hinds DS (1983) Water regulatory efficiency in heteromyid rodents: a model and its application. Ecology 64:152–164
MacMillen RE, Nelson JE (1969) Bioenergetics and body size in dasyurid marsupials. Am J Physiol 217:1246–1251
Malan A (1973) Ventilation measured by body plethysmography in hibernating mammals and in poikilotherms. Respir Physiol 17:32–44
McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47:712–733
McNab BK (1980a) Food habits, energetics, and the population biology of mammals. Am Nat 116:106–124
McNab BK (1980b) On estimating thermal conductance in endotherms. Physiol Zool 53:145–156
McNab BK (1983) Ecological and behavioural consequences of adaptation to various food resources. In Eisenberg JF, Kleiman DG (eds) Advances in the study of mammalian behaviour. Special publication 7 Am Soc Mamm, Kansas, pp 664–697
McNab BK (1984) Physiological convergence amongst ant-eating and termite-eating mammals. J Zool (Lond) 203:485–510
McNab BK (1986a) The influence of food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19
McNab BK (1986b) Food habits, energetics, and the reproduction of marsupials. J Zool (Lond) 208:595–614
McNab BK (1988) Complications in the scaling basal rate of metabolism in mammals. Q Rev Biol 63:25–54
McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, Ithaca
McNab BK (2005) Uniformity in the basal metabolic rate of marsupials: its causes and consequences. Rev Chilena de Hist Nat 78:183–198
McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28
Menkhorst P, Knight F (2004) A field guide to the mammals of Australia. Oxford University Press, Melbourne
Morton SR, Dickman CR, Fletcher TP (1989) Dasyuridae. In: Walton DW, Richardson BJ (eds) Fauna of Australia. Mammalia. Australian Government Publishing Service, Canberra, pp 560–582
Muñoz-Garcia A, Williams JB (2005) Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny. Physiol Biochem Zool 78:1039–1056
Nicol SC, Maskrey M (1980) Thermoregulation, respiration and sleep in the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae). J Comp Physiol 140: 241–248
Nowak RM, Dickman CR (2005) Walker’s Marsupials of the World. Johns Hopkins University Press, Baltimore
Oakwood M (2002) Spatial and social organization of a carnivorous marsupial Dasyurus hallucatus (Marsupialia: Dasyuridae) J Zool Lond 257:237–248
Reardon (1999) Quolls on the run. Aust Geog 54: 89–105
Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160
Rounsevell DE, Taylor RJ, Hocking GJ (1991) Distribution records of native terrestrial mammals in Tasmania. Wildl Res 18:699–717
Rübsamen K, Hume ID, Foley WJ, Rübsamen U (1984) Implications of the large surface area to body mass ratio on heat balance of the greater glider (Petauroides volans: Marsupialia). J Comp Physiol 154:105–111
Schmidt S, Withers PC, Cooper CE (2009) Metabolic, ventilatory and hygric physiology of the chuditch (Dasyurus geoffroii; Marsupialia, Dasyuridae). Comp Physiol Biochem 154:92–97
Serena M, Soderquist T (1989) Spatial organization of a riparian population of the carnivorous marsupial Dasyurus geoffroii. J Zool 219:373–383, 519
Serena M, Soderquist T (2008) Western quoll. In: Van Dyck S, Strahan R (eds) The mammals of Australia. Reed New Holland, Sydney, pp 54–56
Soderquist T, Serena M (1994) Dietary niche of the western quoll, Dasyurus geoffroii, in the jarrah forest of Western Australia. Aust Mammal 17:133–136
Szewczak JM, Powell FL (2003) Open-flow plethysmography with pressure-decay compensation. Resp Physiol Neurobiol 134:57–67
Taggart DA, Shimmin GA, Dickman CR, Breed WG (2003) Reproductive biology of carnivorous marsupials: clues to the likelihood of sperm competition. In: Jones ME, Dickman CR, Archer M (eds) Predators with pouches; the biology of carnivorous marsupials. CSIRO, Collingwood
Withers PC (1977) Metabolic, respiratory and haematological adjustments of the little pocket mouse to circadian torpor cycles. Resp Physiol 31:295–307
Withers PC (1992a) Comparative animal physiology. Saunders College Publishing, Philedelphia
Withers PC (1992b) Metabolism, water balance and temperature regulation in the golden bandicoot (Isoodon auratus). Aust J Zool 40:523–531
Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445–461
Withers PC, Cooper CE (2008) Dormancy. In: Jørgensen SE, Fath BD (eds) Encyclopaedia of ecology V2. Elsevier, Oxford, pp 952–957
Withers PC, Cooper CE (2009a) Thermal, metabolic, hygric and ventilatory physiology of the sandhill dunnart (Sminthopsis psammophila Marsupialia. Dasyuridae) Comp Physiol Biochem 153:317–323
Withers PC, Cooper CE (2009b) The metabolic and hygric physiology of the little red kaluta. J Mamm 90:752–760
Withers PC, Richardson KC, Wooller RD (1990) Metabolic physiology of the euthermic and torpid honey possums, Tarsipes rostratus. Aust J Zool 37:685–693
Withers PC, Thompson GG, Seymour RS (2000) Metabolic physiology of the north-western marsupial mole Notoryctes caurinus (Marsupialia: Notoryctidae). Aust J Zool 48:241–258
Withers PC, Cooper CE, Buttemer WA (2004) Are day-active small mammals rare and small birds abundant in Australian desert environments because small mammals are inferior thermoregulators? Aust Mamm 26:117–124
Withers PC, Cooper CE, Larcombe A (2006) Environmental correlates of physiological variables in marsupials. Physiol Biochem Zool 79:437–453
Acknowledgments
We thank Malcolm and Valerie Douglas, and staff at the Malcolm Douglas Wildlife Park, Broome, Western Australia for allowing us to measure their quolls, and for providing us with accommodation and laboratory space. We also thank Helen Robertson and staff of the Australian section, Perth Zoo, for access to their tiger quolls, and for providing laboratory space. Scott and Graham Thompson kindly caught and donated a northern quoll. This study was funded by an Australian Research Council Discovery grant (DP0665044).
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Communicated by I. D. Hume.
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Cooper, C.E., Withers, P.C. Comparative physiology of Australian quolls (Dasyurus; Marsupialia). J Comp Physiol B 180, 857–868 (2010). https://doi.org/10.1007/s00360-010-0452-3
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DOI: https://doi.org/10.1007/s00360-010-0452-3