Flexibility in thermoregulatory physiology of two dunnarts, Sminthopsis macroura and Sminthopsis ooldea (Marsupialia; Dasyuridae)

Journal of Experimental Biology

Volumn 215, Issue 13, 2012, Pages 2236-2246

  Tomlinson, Sean ^a   Withers, Philip C ^a   Maloney, Shane K ^b  

^a School of Animal Biology   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Acclimation; Evaporative water loss; Metabolic rate; Physiological flexibility; Sminthopsis macroura; Sminthopsis ooldea; Thermoregulation

Indexed keywords

WATER;

ACCLIMATIZATION; ANIMAL; ARTICLE; BASAL METABOLIC RATE; BODY TEMPERATURE; MARSUPIAL; METABOLISM; PHYSIOLOGY; THERMOREGULATION;

ACCLIMATIZATION; ANIMALS; BASAL METABOLISM; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; MARSUPIALIA; WATER;

DASYURIDAE; METATHERIA; SMINTHOPSIS; SMINTHOPSIS MACROURA; SMINTHOPSIS OOLDEA;

EID: 84863611785     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.065516     Document Type: Article

References (78)

1. Angilletta, M. J. J., Cooper, B. S., Schuler, M. S. and Boyles, J. G. (2010). The evolution of thermal physiology in endotherms. Front. Biosci. E2, 861-881.
2. Archer, M. (1981). Results of the Archbold Expeditions No. 104: systematic revision of the marsupial dasyurid genus Sminthopsis Thomas. Bull. Am. Mus. Nat. Hist. 168, 65-223.
3. Aslin, H. J. (1983). Ooldea dunnart (Sminthopsis ooldea). In The Australian Museum Complete Book of Australian Mammals (ed. R. Strahan), p. 54. Sydney: Angus and Robertson.
4. 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. Mol. Phylogenet. Evol. 12, 140-155. (Pubitemid 129499296)
5. Bozinovic, F., Novoa, F. and Veloso, C. (1990). Season changes in energy expenditure and digestive tract of Abrothrix andinus (Cricetidae) in the Andes Ranges. Physiol. Zool. 63, 1216-1231.
6. Chappell, M. A. and Hammond, K. A. (2004). Maximal aerobic performance of deer mice in combined cold and exercise challenges. J. Comp. Physiol. B 174, 41-48. (Pubitemid 38184765)
7. Cohen, B. H. (2008). Explaining Psychological Statistics. Hoboken, NJ: John Wiley & Sons.
8. Cooper, C. E. and Withers, P. C. (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.
9. Cooper, C. E. and Withers, P. C. (2009). Thermal, metabolic, hygric and ventilatory physiology of the sandhill dunnart (Sminthopsis psammophila; Marsupialia, Dasyuridae). Comp. Biochem. Physiol. 153A, 317-323.
10. 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). J. Comp. Physiol. B 175, 323-328. (Pubitemid 40938471)
11. Cooper, C. E., Withers, P. C. and Cruz-Neto, A. P. (2009). Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol. Biochem. Zool. 82, 153-162.
12. Dawson, T. J. and Olson, J. M. (1988). Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials. Comp. Biochem. Physiol. 89A, 85-91.
13. Dawson, W. R. (2003). Plasticity in avian responses to thermal challenges - an essay in honor of Jacob Marder. Isr. J. Zool. 49, 95-109. (Pubitemid 38265680)
14. Ewer, R. F. (1968). A preliminary survey of the behaviour in captivity of the dasyurid marsupial, Sminthopsis crassicaudata (Gould). Zeit. Tierpsych. 25, 319-365.
15. Feder, M. E. (1987). The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. In New Directions in Ecological Physiology (ed. M. E. Feder, A. F. Bennett, W. G. Burggren and R. B. Huey), pp. 38-75. Cambridge: Cambridge University Press.
16. Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15.
17. Frey, H. (1991). Energetic significance of torpor and other energy-conserving mechanisms in free-living Sminthopsis crassicaudata (Marsupialia: Dasyuridae). Aust. J. Zool. 39, 689-708. (Pubitemid 23395859)
18. Garland, T. J. and Adolph, S. C. (1994). Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol. Zool. 67, 797-828.
19. Geiser, F. (1994). Hibernation and daily torpor in marsupials: a review. Aust. J. Zool. 42, 1-16.
20. Geiser, F. and Baudinette, R. V. (1985). The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia). J. Comp. Physiol. B 156B, 129-134.
21. Geiser, F. and Baudinette, R. V. (1987). Seasonality of torpor and thermoregulation in three dasyurid marsupials. J. Comp. Physiol. B 157, 335-344.
22. Geiser, F. and Ferguson, C. (2001). Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J. Comp. Physiol. B 71, 569-576. (Pubitemid 32948796)
23. Geiser, F. and Turbill, C. (2009). Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96, 1235-1240.
24. 2 exposure on metabolic rate, thermoregulation and thermal conductance during normothermia and daily torpor. J. Comp. Physiol. B 166, 190-196. (Pubitemid 26309629)
25. Geiser, F., Drury, R. L., McAllan, B. M. and Wang, D. H. (2003). Effects of temperature acclimation on maximum heat production, thermal tolerance, and torpor in a marsupial. J. Comp. Physiol. B 173, 437-442. (Pubitemid 36990265)
26. Godfrey, G. (1968). Body-temperatures and torpor in Sminthopsis crassicaudata and S. larapinta (Marsupialia - Dasyuridae). J. Zool. 156, 499-511.
27. Grigg, G. C. and Beard, L. A. (2000). Hibernation by echidnas in mild climates: hints about the evolution of endothermy? In Life in the Cold. Eleventh International Hibernation Symposium (ed. G. Heldemaier and M. Klingenspor), pp. 5-20. Berlin: Springer-Verlag.
28. Hart, J. S. (1971). Rodents. In Comparative Physiology of Thermoregulation (ed. G. C. Whittow), pp. 1-149. New York: Academic Press.
29. Heldmaier, G., Boeckler, H., Buchberger, A., Klaus, S., Puchalski, W., Steinlacher, S. and Wiesinger, H. (1986). Seasonal variation of thermogenesis. In Living in the Cold (ed. H. C. Heller, X. J. Musacchia and L. C. H. Wang), pp. 361-372. New York: Elsevier.
30. Hill, R. W. (1983). Thermal physiology and energetics of Peromyscus: ontogeny, body temperature, metabolism, insulation, and microclimatology. J. Mammal. 64, 19-37.
31. Hinds, D. S., Baudinette, R. V., MacMillen, R. E. and Halpern, E. A. (1993). Maximum metabolism and the aerobic factorial scope of endotherms. J. Exp. Biol. 182, 41-56.
32. Holloway, J. C. and Geiser, F. (1995). Influence of torpor on daily energy expenditure of the dasyurid marsupial Sminthopsis crassicaudata. Comp. Biochem. Physiol. 112A, 59-66.
33. Holloway, J. C. and Geiser, F. (2001). Effects of helium/oxygen and temperature on aerobic metabolism in the marsupial sugar glider, Petaurus breviceps. Physiol. Biochem. Zool. 74, 219-225. (Pubitemid 32296077)
34. Hudson, J. W. (1978). Shallow, daily torpor: a thermoregulatory adaptation. In Strategies in Cold: Natural Torpidity and Thermogenesis (ed. L. C. H. Wang and J. W. Hudson), pp 67-108. New York: Academic Press.
35. Klingenspor, M., Niggemann, H. and Heldmaier, G. (2000). Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J. Comp. Physiol. B 170, 37-43. (Pubitemid 30351563)
36. Koteja, P. (1996). Limits to the energy budget in a rodent, Peromyscus maniculatus: the central limitation hypothesis. Physiol. Zool. 69, 981-993.
37. Lee, P. and Schmidt-Nielsen, K. (1971). Respiratory and cutaneous evaporation in the zebra finch: effect on water balance. Am. J. Physiol. 220, 1598-1605.
38. Lewontin, R. C. (1969). The bases of conflict in biological explanation. J. Hist. Biol. 2, 35-53.
39. Malan, A. (1996). The origins of hibernation: a reappraisal. In Adaptations to the Cold (ed. F. Geiser, A. J. Hulbert and S. C. Nicol), pp. 1-6. Armindale, NSW: University of New England Press.
40. McKechnie, A. E. (2008). Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review J. Comp. Physiol. B 178, 235-247. (Pubitemid 351640696)
41. McKenzie, N. L., Burbidge, A. A. and Baynes, A. (2006). Australian Mammal Map Updates. Available at http://www.dec.wa.gov.au/content/view/2588/1813/.
42. Menon, G. K., Baptista, L. F., Brown, B. E. and Elias, P. M. (1989). Avian epidermal differnetiation II: adaptive response of permeability barrier to water deprivation and replenishment. Tissue Cell 21, 83-92.
43. Morton, S. R. (1978). Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia). J. Mammal. 59, 569-575.
44. Morton, S. R. (1983a). Fat-tailed dunnart Sminthopsis crassicaudata. In The Australian Museum Complete Book of Australian Mammals (ed. R. Strahan), pp. 61-62. Sydney: Angus and Robertson.
45. Morton, S. R. (1983b). Stripe-faced dunnart Sminthopsis macroura. In The Australian Museum Complete Book of Australian Mammals (ed. R. Strahan), pp. 63-64. Sydney: Angus and Robertson.
46. Munn, A. J., Kern, P. and McAllan, B. M. (2010). Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Naturwissenschaften 97, 601-605.
47. Nagy, K. A., Lee, A. K., Martin, R. W. and Fleming, M. R. (1988). Field metabolic rate and food requirement of a small dasyurid marsupial, Sminthopsis crassicaudata. Aust. J. Zool. 36, 293-299. (Pubitemid 20419943)
48. Nespolo, R. F., Bacigalupe, L. D., Rezende, E. L. and Bozinovic, F. (2001). When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol. Biochem. Zool. 74, 325-332. (Pubitemid 32501219)
49. Nespolo, R. F., Bacigalupe, L. D., Sabat, P. and Bozinovic, F. (2002). Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouseopossum Thylamys elegans: the role of thermal acclimation. J. Exp. Biol. 205, 2697- 2703.
50. Nicol, S. C. and Anderson, N. A. (1996). HIbernation in the echidna: not an adaptation to the cold. In Adaptations to the Cold (ed. F. Geiser, A. J. Hulbert and S. C. Nicol), pp. 7-12. Armindale, NSW: University of New England Press.
51. Opazo, J. C., Nespolo, R. F. and Bozinovic, F. (1999). Arousal from torpor in the Chilean mouse-opossum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp. Biochem. Physiol. 123, 393-397. (Pubitemid 29414845)
52. Ostrowski, S., Williams, J. B., Mésochina, P. and Sauerwein, H. (2006). Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to longterm food and water restriction. J. Comp. Physiol. B 176, 191-201. (Pubitemid 43320228)
53. Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228-233. (Pubitemid 36551227)
54. Reynolds, W. and Hulbert, A. J. (1982). Cold acclimation in a small dasyurid marsupial: Antechinus stuartii. In Carnivorous Marsupials (ed. M. Archer), pp. 279- 283. Sydney: Royal Zoological Society of New South Wales.
55. Rezende, E. L., Chappell, M. A. and Hammond, K. A. (2004). Cold-acclimation in Peromyscus: temporal effects and individual variation in maximum metabolism and ventilatory rates. J. Exp. Biol. 207, 295-305. (Pubitemid 38106733)
56. Rose, R. W., West, A. K., Ye, J. M., McCormack, G. H. and Colquhoun, E. Q. (1999). Nonshivering thermogenesis in a marsupial (the Tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol. Biochem. Zool. 72, 699-704. (Pubitemid 30156940)
57. 2. Am. J. Physiol. 226, 490-494.
58. Russell, G. A. and Chappell, M. A. (2007). Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude. J. Comp. Physiol. B 177, 75-87. (Pubitemid 44974297)
59. Smith, B. K. and Dawson, T. J. (1984). Changes in the thermal balance of a marsupial (Dasyuroides byrnei) during cold and warm acclimation. J. Therm. Biol. 9, 199-204.
60. Smith, B. K. and Dawson, T. J. (1985). Use of helium-oxygen to examine the effect of cold acclimation on the summit metabolism of a marsupial, Dasyuroides byrnei. Comp. Biochem. Physiol. 81A, 445-449. (Pubitemid 15039750)
61. Song, X. and Geiser, F. (1997). Daily torpor and energy expenditure in Sminthopsis macroura: interactions between food and water availability and temperature. Physiol. Zool. 70, 331-337.
62. Song, X., Körtner, G. and Geiser, F. (1995). Reduction of metabolic rate and thermoregulation during daily torpor. J. Comp. Physiol. B 165, 291-297.
63. Song, X., Kortner, G. and Geiser, F. (1998). Temperature selection and use of torpor by the marsupial Sminthopsis macroura. Physiol. Behav. 64, 675-682. (Pubitemid 28470584)
64. Soobramoney, S., Downs, C. T. and Adams, N. J. (2003). Physiological variability in the fiscal shrike Lanius collaris along an altitudinal gradient in South Africa. J. Therm. Biol. 28, 581-594. (Pubitemid 37309954)
65. Thomas, D. W., Pacheco, M. A., Fournier, F. and Fortine, D. (1998). Validation of the effect of helox on thermal conductance in homeotherms using heated models. J. Therm. Biol. 23, 377-380. (Pubitemid 29032155)
66. Tomlinson, S. (2012). Physiological and behavioural responses of Western Australian dunnarts (Sminthopsis spp.) to energetic challenge. PhD thesis, University of Western Australia, Crawley, WA.
67. 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. Comp. Biochem. Physiol. 148A, 645-650. (Pubitemid 47484236)
68. Wang, L. H. C. (1989). Ecological, physiological and biochemical aspects of torpor in mammals and birds. In Advances in Comparative and Environmental Physiology (ed. L. C. H. Wang), pp. 361-401. Berlin: Springer-Verlag.
69. Williams, J. B. and Tieleman, B. I. (2000). Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures. J. Exp. Biol. 203, 3153-3159.
70. Withers, K. W. and Hulbert, A. J. (1988). Cold acclimation in the marsupial Antechinus stuartii: thyroid function and metabolic rate. Aust. J. Zool. 36, 421-427.
71. Withers, P. C. (1992). Comparative Animal Physiology. Fort Worth, TX: Saunders College Publishing.
72. Withers, P. C. (2001). Design, calibration and calculation for flow-through respirometry systems. Aust. J. Zool. 49, 445-461. (Pubitemid 33001817)
73. Withers, P. C. and Cooper, C. E. (2009). Thermal, metabolic and hygric physiology of the little red kaluta, Dasykaluta rosamondae (Dasyuromorphia: Dasyuridae). J. Mammal. 90, 752-760.
74. Withers, P. C., Richardson, K. C. and Wooller, R. D. (1990). Metabolic physiology of euthermic and torpid honey possums. Aust. J. Zool. 37, 685-693.
75. Withers, P. C., Cooper, C. E. and Larcombe, A. N. (2006). Environmental correlates of physiological variables in marsupials. Physiol. Biochem. Zool. 79, 437-453. (Pubitemid 43846261)
76. Zar, J. H. (1999). Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.
77. Zosky, G. R. (2002). The parasympathetic nervous system: its role during torpor in the fat-tailed dunnart (Sminthopsis crassicaudata). J. Comp. Physiol. B 172, 677-684. (Pubitemid 36072759)
78. Zosky, G. R. and O'Shea, J. E. (2003). The cardiac innervation of a marsupial heterotherm, the fat-tailed dunnart (Sminthopsis crassicaudata). J. Comp. Physiol. B 173, 293-300. (Pubitemid 36832227)