Journal of Comparative Physiology B

, Volume 180, Issue 6, pp 857–868

Comparative physiology of Australian quolls (Dasyurus; Marsupialia)

Original Paper

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 Tb 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.

Keywords

Allometry Body temperature Evaporative water loss Metabolic rate Relative water economy Thermal conductance Ventilation 

Abbreviations

BMR

Basal metabolic rate

Cdry

Dry (non-evaporative) thermal conductance

Cwet

Wet (evaporative and non-evaporative) thermal conductance

EHL

Evaporative heat loss

EO2

Oxygen extraction

EQ

Evaporative quotient

EWL

Evaporative water loss

fR

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

Ta

Ambient temperature

Tb

Body temperature

VCO2

Carbon dioxide production rate

VI

Minute volume

VO2

Oxygen consumption rate

VT

Tidal volume

References

  1. Arnold J (1976) Growth and bioenergetics of the chuditch, Dasyurus geoffroii. Ph.D. thesis, Department of Zoology, University of Western Australia, PerthGoogle Scholar
  2. Bartholomew GA, Hudson JW (1962) Hibernation, estivation, temperature regulation, evaporative water loss, and heart rate of Cercaertus nanus. Physiol Zool 35:94–107Google Scholar
  3. Belcher CA, Nelson JL, Darrant JP (2007) Diet of the tiger quoll (Dasyurus maculatus) in south-eastern Australia. Aust J Zool 55:117–122CrossRefGoogle Scholar
  4. 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 446:507–512CrossRefPubMedGoogle Scholar
  5. Blackhall S (1980) Diet of the eastern native-cat, Dasyurus viverrinus (Shaw), in southern Tasmania. Aust Wildl Res 7:191–197CrossRefGoogle Scholar
  6. Braithwaite RW, Griffiths AD (1994) Demographic variation and range contraction in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae). Wildl Res 21:203–217CrossRefGoogle Scholar
  7. Careau V, Morand-Ferron J, Thomas D (2007) Basal metabolic rate of canids from hot deserts to cold arctic climates. J Mamm 88:394–400CrossRefGoogle Scholar
  8. 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 67:113–121CrossRefGoogle Scholar
  9. Cooper CE, Cruz-Neto AP (2009) Metabolic, hygric and ventilatory physiology of a hypermetabolic marsupial, the honey possum (Tarsipes rostratus). J Comp Physiol B 179:773–781CrossRefPubMedGoogle Scholar
  10. 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 178:1–8CrossRefPubMedGoogle Scholar
  11. Cooper CE, Withers PC (2002) Metabolic physiology of the numbat (Myrmecobius fasciatus). J Comp Physiol 172:669–675Google Scholar
  12. Cooper CE, Withers PC (2004) Ventilatory physiology of the numbat (Myrmecobius fasciatus). J Comp Physiol B 174:107–111CrossRefPubMedGoogle Scholar
  13. 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 176:623–629CrossRefPubMedGoogle Scholar
  14. 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 211:2759–2766CrossRefPubMedGoogle Scholar
  15. 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 82:438–446CrossRefPubMedGoogle Scholar
  16. 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 175:323–328CrossRefPubMedGoogle Scholar
  17. Cooper CE, Withers PC, Cruz-Neto AP (2009) Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol Biochem Zool 82:153–162CrossRefPubMedGoogle Scholar
  18. 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)Google Scholar
  19. Degabriele R, Dawson TJ (1979) Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol 134:293–301Google Scholar
  20. Edgar R, Belcher C (1995) Spotted-tailed quoll. In: Strahan R (ed) The mammals of Australia, 2nd edn. Australian Museum/Reed Books, Sydney, pp 67–69Google Scholar
  21. Elgar MA, Harvey PH (1987) Basal metabolic rates in mammals: allometry, phylogeny and ecology. Funct Ecol 1:25–36CrossRefGoogle Scholar
  22. Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16CrossRefGoogle Scholar
  23. 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 238–253Google Scholar
  24. Geiser F (2004) The role of torpor in the life of Australian arid zone mammals. Aust Mammal 26:125–134Google Scholar
  25. 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 96:1–7CrossRefGoogle Scholar
  26. Godsell J (2002) Eastern quoll. In: Strahan R (ed) The mammals of Australia. Reed New Holland, SydneyGoogle Scholar
  27. Harvey PH, Pagel MD, Rees JA (1991) Mammalian metabolism and life histories. Am Nat 137:556–566CrossRefGoogle Scholar
  28. Hayes JP, Shonkwiler JS (2006) Allometry, antilog transformations, and the perils of prediction on the original scale. Physiol Biochem Zool 79:665–674CrossRefPubMedGoogle Scholar
  29. Hayes JP, Shonkwiler JS (2007) Erratum: Allometry, antilog transformations, and the perils of prediction on the original scale. Physiol Biochem Zool 80:556CrossRefGoogle Scholar
  30. Hayssen V, Lacy C (1985) Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol A 81:741–754CrossRefPubMedGoogle Scholar
  31. Hinds DS, MacMillen RE (1986) Scaling of evaporative water loss in marsupials. Physiol Zool 59:1–9Google Scholar
  32. Hinds DS, Baudinette RV, MacMillen RE, Halpern EA (1993) Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol 182:41–56PubMedGoogle Scholar
  33. Hudson JW (1962) The role of water in the biology of the antelope ground squirrel Citellus leucurus. Univ Calif Pub Zool 64:1–56Google Scholar
  34. Jones ME, Barmuta LA (1998) Diet overlap and relative abundance of sympatric dasyurid carnivores: a hypothesis of competition. J An Ecol 67:410–421CrossRefGoogle Scholar
  35. Jones ME, Rose RK (2001) Dasyurus viverrinus. Mamm Species 677:1–9CrossRefGoogle Scholar
  36. 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 70:53–60PubMedGoogle Scholar
  37. Jones ME, Rose RK, Barnett S (2001) Dasyurus maculatus. Mamm Species 676:1–9CrossRefGoogle Scholar
  38. Koteja P (1996) Measuring energy metabolism with open-flow respirometric systems: Which design to choose? Func Ecol 10:675–677CrossRefGoogle Scholar
  39. Larcombe AN (2002) Effects of temperature on metabolism, ventilation, and oxygen extraction in the southern brown bandicoot Isoodon obesulus (Marsupialia: Peramelidae). Physiol Biochem Zool 75:405–411CrossRefPubMedGoogle Scholar
  40. Larcombe AN (2004) Comparative metabolic, thermoregulatory and ventilatory physiology of bandicoots (Peramelidae). Ph.D. thesis, Zoology, University of Western Australia, PerthGoogle Scholar
  41. Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219CrossRefPubMedGoogle Scholar
  42. Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112PubMedGoogle Scholar
  43. MacMillen RE (1965) Aestivation in the cactus mouse Peromyscus eremicus. Comp Biochem Physiol 16:227–248CrossRefPubMedGoogle Scholar
  44. MacMillen RE (1990) Water economy of granivorous birds: a predictive model. Condor 92:379–392CrossRefGoogle Scholar
  45. MacMillen RE, Hinds DS (1983) Water regulatory efficiency in heteromyid rodents: a model and its application. Ecology 64:152–164CrossRefGoogle Scholar
  46. MacMillen RE, Nelson JE (1969) Bioenergetics and body size in dasyurid marsupials. Am J Physiol 217:1246–1251PubMedGoogle Scholar
  47. Malan A (1973) Ventilation measured by body plethysmography in hibernating mammals and in poikilotherms. Respir Physiol 17:32–44CrossRefPubMedGoogle Scholar
  48. McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47:712–733CrossRefGoogle Scholar
  49. McNab BK (1980a) Food habits, energetics, and the population biology of mammals. Am Nat 116:106–124CrossRefGoogle Scholar
  50. McNab BK (1980b) On estimating thermal conductance in endotherms. Physiol Zool 53:145–156Google Scholar
  51. 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 664–697Google Scholar
  52. McNab BK (1984) Physiological convergence amongst ant-eating and termite-eating mammals. J Zool (Lond) 203:485–510CrossRefGoogle Scholar
  53. McNab BK (1986a) The influence of food habits on the energetics of eutherian mammals. Ecol Monogr 56:1–19CrossRefGoogle Scholar
  54. McNab BK (1986b) Food habits, energetics, and the reproduction of marsupials. J Zool (Lond) 208:595–614Google Scholar
  55. McNab BK (1988) Complications in the scaling basal rate of metabolism in mammals. Q Rev Biol 63:25–54CrossRefPubMedGoogle Scholar
  56. McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, IthacaGoogle Scholar
  57. McNab BK (2005) Uniformity in the basal metabolic rate of marsupials: its causes and consequences. Rev Chilena de Hist Nat 78:183–198Google Scholar
  58. McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28CrossRefGoogle Scholar
  59. Menkhorst P, Knight F (2004) A field guide to the mammals of Australia. Oxford University Press, MelbourneGoogle Scholar
  60. Morton SR, Dickman CR, Fletcher TP (1989) Dasyuridae. In: Walton DW, Richardson BJ (eds) Fauna of Australia. Mammalia. Australian Government Publishing Service, Canberra, pp 560–582Google Scholar
  61. Muñoz-Garcia A, Williams JB (2005) Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny. Physiol Biochem Zool 78:1039–1056CrossRefPubMedGoogle Scholar
  62. Nicol SC, Maskrey M (1980) Thermoregulation, respiration and sleep in the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae). J Comp Physiol 140: 241–248Google Scholar
  63. Nowak RM, Dickman CR (2005) Walker’s Marsupials of the World. Johns Hopkins University Press, BaltimoreGoogle Scholar
  64. Oakwood M (2002) Spatial and social organization of a carnivorous marsupial Dasyurus hallucatus (Marsupialia: Dasyuridae) J Zool Lond 257:237–248Google Scholar
  65. Reardon (1999) Quolls on the run. Aust Geog 54: 89–105Google Scholar
  66. Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160PubMedGoogle Scholar
  67. Rounsevell DE, Taylor RJ, Hocking GJ (1991) Distribution records of native terrestrial mammals in Tasmania. Wildl Res 18:699–717CrossRefGoogle Scholar
  68. 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 154:105–111Google Scholar
  69. Schmidt S, Withers PC, Cooper CE (2009) Metabolic, ventilatory and hygric physiology of the chuditch (Dasyurus geoffroii; Marsupialia, Dasyuridae). Comp Physiol Biochem 154:92–97CrossRefGoogle Scholar
  70. Serena M, Soderquist T (1989) Spatial organization of a riparian population of the carnivorous marsupial Dasyurus geoffroii. J Zool 219:373–383, 519Google Scholar
  71. Serena M, Soderquist T (2008) Western quoll. In: Van Dyck S, Strahan R (eds) The mammals of Australia. Reed New Holland, Sydney, pp 54–56Google Scholar
  72. Soderquist T, Serena M (1994) Dietary niche of the western quoll, Dasyurus geoffroii, in the jarrah forest of Western Australia. Aust Mammal 17:133–136Google Scholar
  73. Szewczak JM, Powell FL (2003) Open-flow plethysmography with pressure-decay compensation. Resp Physiol Neurobiol 134:57–67CrossRefGoogle Scholar
  74. 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, CollingwoodGoogle Scholar
  75. Withers PC (1977) Metabolic, respiratory and haematological adjustments of the little pocket mouse to circadian torpor cycles. Resp Physiol 31:295–307CrossRefGoogle Scholar
  76. Withers PC (1992a) Comparative animal physiology. Saunders College Publishing, PhiledelphiaGoogle Scholar
  77. Withers PC (1992b) Metabolism, water balance and temperature regulation in the golden bandicoot (Isoodon auratus). Aust J Zool 40:523–531CrossRefGoogle Scholar
  78. Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445–461CrossRefGoogle Scholar
  79. Withers PC, Cooper CE (2008) Dormancy. In: Jørgensen SE, Fath BD (eds) Encyclopaedia of ecology V2. Elsevier, Oxford, pp 952–957CrossRefGoogle Scholar
  80. Withers PC, Cooper CE (2009a) Thermal, metabolic, hygric and ventilatory physiology of the sandhill dunnart (Sminthopsis psammophila Marsupialia. Dasyuridae) Comp Physiol Biochem 153:317–323CrossRefGoogle Scholar
  81. Withers PC, Cooper CE (2009b) The metabolic and hygric physiology of the little red kaluta. J Mamm 90:752–760CrossRefGoogle Scholar
  82. Withers PC, Richardson KC, Wooller RD (1990) Metabolic physiology of the euthermic and torpid honey possums, Tarsipes rostratus. Aust J Zool 37:685–693CrossRefGoogle Scholar
  83. Withers PC, Thompson GG, Seymour RS (2000) Metabolic physiology of the north-western marsupial mole Notoryctes caurinus (Marsupialia: Notoryctidae). Aust J Zool 48:241–258CrossRefGoogle Scholar
  84. 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 26:117–124Google Scholar
  85. Withers PC, Cooper CE, Larcombe A (2006) Environmental correlates of physiological variables in marsupials. Physiol Biochem Zool 79:437–453CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Environmental and Aquatic SciencesCurtin University of TechnologyPerthAustralia
  2. 2.Animal Biology M092University of Western AustraliaCrawleyAustralia

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