Heterothermy in pouched mammals - a review

Journal of Zoology

Volumn 292, Issue 2, 2014, Pages 74-85

  Riek, A ^a,b   Geiser, F ^b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

Heterothermy; Hibernation; Marsupials; Phylogeny; Torpor

Indexed keywords

BODY TEMPERATURE; DATA SET; HIBERNATION; MARSUPIAL; PHYLOGENY; TORPOR;

DASYURUS; EUTHERIA; MAMMALIA; METATHERIA; PLANIGALE;

EID: 84892867568     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/jzo.12102     Document Type: Article

References (85)

1. Armati, P.J., Dickman, C.R. & Hume, I.D. (2006). Marsupials. Cambridge: Cambridge University Press.
2. Arnold, J.M. (1976). Growth and bioenergetics of the Chuditch, Dasyurus geoffroii. Ph.D. Thesis, University of Western Australia, Perth.
3. Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee, R.D.E., Beck, R.M.D., Grenyer, R., Price, S.A., Vos, R.A., Gittleman, J.L. & Purvis, A. (2008). The delayed rise of present-day mammals. Nature 456, 274.
4. Bozinovic, F., Ruiz, G. & Rosenmann, M. (2004). Energetics and torpor of a South American 'living fossil', the microbiotheriid Dromiciops gliroides. J. Comp. Physiol. [B.] 174, 293-297.
5. Bruggeman, J., Heringa, J. & Brandt, B.W. (2009). PhyloPars: estimation of missing parameter values using phylogeny. Nucleic Acids Res. 37, W179-W184.
6. Capellini, I., Venditti, C. & Barton, R.A. (2010). Phylogeny and metabolic scaling in mammals. Ecology 91, 2783-2793.
7. Clarke, A., Rothery, P. & Isaac, N.J.B. (2010). Scaling of basal metabolic rate with body mass and temperature in mammals. J. Anim. Ecol. 79, 610-619.
8. Cooper, C.E. & Geiser, F. (2008). The 'minimal boundary curve for endothermy' as a predictor of heterothermy in mammals and birds: a review. J. Comp. Physiol. [B.] 178, 1-8.
9. Cooper, C.E. & Withers, P.C. (2004). Patterns of body temperature variation and torpor in the numbat, Myrmecobius fasciatus (Marsupialia: Myrmecobiidae). J. Therm. Biol. 29, 277-284.
10. Cooper, C.E. & Withers, P.C. (2010). Comparative physiology of Australian quolls (Dasyurus: Marsupialia). J. Comp. Physiol. [B.] 180, 857-868.
11. Cooper, C.E., Withers, P.C. & Cruz-Neto, A.P. (2009). Metabolic, ventilatory, and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol. Biochem. Zool. 82, 153-162.
12. th International Hibernation Symposium: 327-336. Lovegrove, B.G. & McKechnie, A.E. (Eds). Pietermaritzburg: University of KwaZulu-Natal.
13. Dawson, T.J. & Hulbert, A.J. (1970). Standard metabolism, body temperature and surface area of Australian marsupials. Am. J. Physiol. 218, 1233-1238.
14. Dawson, T.J. & Wolfers, J.M. (1978). Metabolism, thermoregulation and torpor in shrew sized marsupials of the genus Planigale. Comp. Biochem. Physiol. A 59, 305-309.
15. Douglas, T.A. & Nicol, S.C. (1993). Thermoregulation in the South American grey, short-tailed opossum (Monodelphis domestica). Proc. Aust. N. Z. Soc. Comp. Physiol. Biochem. 10, 19.
16. Dunbar, M.B. & Brigham, R.M. (2010). Thermoregulatory variation among populations of bats along a latitudinal gradient. J. Comp. Physiol. [B.] 180, 885-893.
17. Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15.
18. Fleming, M.R. (1980). Thermoregulation and torpor in the sugar glider, Petaurus breviceps (Marsupialia: Petauridae). Aust. J. Zool. 28, 521-534.
19. Freckleton, R.P., Harvey, P.H. & Pagel, M. (2002). Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712-726.
20. Garland, T., Dickerman, A.W., Janis, C.M. & Jones, J.A. (1993). Phylogenetic analysis of covariance by computer-simulation. Syst. Biol. 42, 265-292.
21. Garland, T. & Ives, A.R. (2000). Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346-364.
22. Geiser, F. (1986). Thermoregulation and torpor in the Kultarr, Antechinomys laniger (Marsupiala: Dasyuridae). J. Comp. Physiol. [B.] 156, 751-757.
23. Geiser, F. (1987). Hibernation and daily torpor in 2 pygmy possums (Cercartetus spp.: Marsupialia). Physiol. Zool. 60, 93-102.
24. Geiser, F. (1988). Daily torpor and thermoregulation in antechinus (Marsupialia): Influence of body mass, season, development, reproduction and sex. Oecologia 77, 395-399.
25. Geiser, F. (1993). Hibernation in the Eastern pygmy possum, Cercartetus nanus (Marsupialia: Burramyidae). Aust. J. Zool. 41, 1993.
26. Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274.
27. Geiser, F. (2008). Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp. Biochem. Physiol. A 150, 176-180.
28. Geiser, F. & Baudinette, R.V. (1987). Seasonality of torpor and thermoregulation in 3 dasyurid marsupials. J. Comp. Physiol. [B.] 157, 335-344.
29. Geiser, F. & Baudinette, R.V. (1988). Daily torpor and thermoregulation in the small dasyurid marsupials: Planigale gilesi and Ningaui yvonneae. Aust. J. Zool. 36, 473-481.
30. Geiser, F. & Broome, L.S. (1991). Hibernation in the mountain pygmy possum Burramys parvus (Marsupialia). J. Zool. (Lond.) 223, 593-602.
31. Geiser, F. & Ferguson, C. (2001). Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J. Comp. Physiol. [B.] 171, 569-576.
32. Geiser, F. & Körtner, G. (2010). Hibernation and daily torpor in Australian mammals. Aust. Zool. 35, 204-215.
33. Geiser, F. & Masters, P. (1994). Torpor in relation to reproduction in the mulgara, Dasycercus cristicauda (Dasyuridae: Marsupiala). J. Therm. Biol. 19, 33-40.
34. Geiser, F. & Pavey, C.R. (2007). Basking and torpor in a rock-dwelling desert marsupial: survival strategies in a resource-poor environment. J. Comp. Physiol. [B.] 177, 885-892.
35. Geiser, F. & Ruf, T. (1995). Hibernation versus daily torpor in mammals and birds - physiological variables and classification of torpor patterns. Physiol. Zool. 68, 935-966.
36. Geiser, F., McCarron, H.C.K., Augee, M.L. & Raison, J.K. (1984). Correlates of torpor in the insectivorous dasyurid marsupial Sminthopsis murina. Aust. Mamm. 7, 185-191.
37. Geiser, F., Westman, W., McAllan, B.M. & Brigham, R.M. (2006). Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications. J. Comp. Physiol. [B.] 176, 107-116.
38. Gotts, D. (1976). Energetics in Antechinus swainsonii. M.Sc. Thesis, Monash University, Melbourne.
39. Grafen, A. (1989). The phylogenetic regression. Philos. Trans. Roy. Soc. Lond. B 326, 119-157.
40. Harmon, L.J., Weir, J.T., Brock, C.D., Glor, R.E. & Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129-131.
41. Ihaka, R. & Gentleman, R. (1996). R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5, 299-314.
42. Körtner, G. & Geiser, F. (2000). Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123, 350-357.
43. Körtner, G. & Geiser, F. (2009). The key to winter survival: daily torpor in a small arid-zone marsupial. Naturwissenschaften 96, 525-530.
44. Körtner, G., Pavey, C.R. & Geiser, F. (2008). Thermal biology, torpor, and activity in free-living mulgaras in arid zone Australia during the winter reproductive season. Physiol. Biochem. Zool. 81, 442-451.
45. Körtner, G., Rojas, A.D. & Geiser, F. (2010). Thermal biology, torpor use and activity patterns of a small marsupial from a tropical desert: sexual differences. J. Comp. Physiol. [B.] 180, 869-876.
46. Lovegrove, B.G. (2012). The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol. Rev. Camb. Philos. Soc. 87, 128-162.
47. MacMillen, R.E. & Nelson, J.E. (1969). Bioenergetics and body size in dasyurid marsupials. Am. J. Physiol. 217, 1246-1251.
48. Martins, E.P. & Hansen, T.F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646-667.
49. McKechnie, A.E. & Lovegrove, B.G. (2002). Avian facultative hypothermic responses: a review. Condor 104, 705-724.
50. McNab, B.K. (1978). The comparative energetic of neotropical marsupials. J. Comp. Physiol. 125, 115-128.
51. Menkhorst, P. & Knight, F. (2004). Mammals of Australia. Oxford: Oxford University Press.
52. Morrison, P.R. & McNab, B.K. (1962). Daily torpor in a Brazilian murine opossum (Marmosa). Comp. Biochem. Physiol. A 6, 57-68.
53. Morton, S.R. & Lee, A.K. (1978). Thermoregulation and metabolism in Planigale maculata (Marsupialia: Dasyuridae). J. Therm. Biol. 3, 117-120.
54. Moyle, D. unpublished in Reardon, M. (1999). Quolls on the run. Aust. Geogr. 54, 89-105.
55. Muller, J. (1996). Torpor in Sminthopsis douglasi. Honours thesis, La Trobe University, Melbourne.
56. Nicol, S., Pavlides, D. & Andersen, N.A. (1997). Nonshivering thermogenesis in marsupials: absence of thermogenic response to b3-adrenergic agonists. Comp. Biochem. Physiol. A 117, 399-405.
57. O'Leary, M.A., Bloch, J.I., Flynn, J.J., Gaudin, T.J., Giallombardo, A., Giannini, N.P., Goldberg, S.L. etal. (2013). The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339, 662-667.
58. Opazo, J.C., Nespolo, R.F. & Bozinovic, F. (1999). Arousal from torpor in the Chilean mouse-opposum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp. Biochem. Physiol. A 123, 393-397.
59. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877-884.
60. Pagel, M., Meade, A. & Barker, D. (2004). Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 948-957.
61. Paradis, E., Claude, J. & Strimmer, K. (2004). APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
62. Paull, D.C. (2013). Refuge sites, activity and torpor in wild common dunnarts (Sminthopsis murina) in a temperate heathland. Aust. Mamm. 35, 153-159. (online ahead of print, DOI: 10.1071/AM12016)
63. Pusey, H., Cooper, C.E. & Withers, P.C. (2013). Metabolic, hygric and ventilatory physiology of the red-tailed phascogale (Phascogale calura; Marsupialia, Dasyuridae): adaptations to aridity or arboreality? Mamm. Biol. 78, 397-405. (online ahead of print, DOI: 10.1016/j.mambio.2012.11.008)
64. Riek, A. & Bruggeman, J. (2013). Estimating field metabolic rates for Australian marsupials using phylogeny. Comp. Biochem. Physiol. A 164, 598-604.
65. Riek, A. & Geiser, F. (2012). Developmental phenotypic plasticity in a marsupial mammal. J. Exp. Biol. 215, 1552-1558.
66. Riek, A. & Geiser, F. (2013). Allometry of thermal variables in mammals: consequences of body size and phylogeny. Biol. Rev. Camb. Philos. Soc. 88, 564-572.
67. Rohlf, F. (2001). Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55, 2143-2160.
68. Silva-Duran, I.P. & Bozinovic, F. (1999). Food availability regulates energy expenditure and torpor in the Chilean mouse-opossum Thylamys elegans. Rev. Chil. Hist. Nat. 72, 371-375.
69. Song, X., Körtner, G. & Geiser, F. (1997). Thermal relations of metabolic rate reduction in a hibernating marsupial. Am. J. Physiol. 273, R2097-R2104.
70. Stawski, C. & Geiser, F. (2011). Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics? Am. J. Physiol. 301, R542-R547.
71. Stawski, C., Willis, C.K.R. & Geiser, F. (2013). The importance of heterothermy in bats. J. Zool. (Lond.). (Online DOI: doi:10.1111/jzo.12105)
72. Tomlinson, S., Withers, P.C. & Maloney, S.K. (2012). Flexibility in thermoregulatory physiology of two dunnarts, Sminthopsis macroura and Sminthopsis ooldea (Marsupialia: Dasyuridae). J. Exp. Biol. 215, 2235-2246.
73. Tøien, Ø., Blake, J., Edgar, D.M., Grahn, D.A., Heller, H.C. & Barnes, B.M. (2011). Hibernation in black bears: independance of metabolic suppression from body temperature. Science 331, 906-909.
74. Turner, J.M., Körtner, G., Warnecke, L. & Geiser, F. (2012). Summer and winter torpor use by a free-ranging marsupial. Comp. Biochem. Physiol. A 162, 274-280.
75. Tyndale-Biscoe, H. (2005). Life of marsupials. Collingwood: CSIRO Publishing.
76. Tyndale-Biscoe, H. & Renfree, M.B. (1987). Reproductive physiology of marsupials. Cambridge: Cambridge University Press.
77. Wallis, R.L. (1976). Torpor in dasyurid marsupial, Antechinus stuartii. Comp. Biochem. Physiol. A 53, 319-322.
78. Warnecke, L., Turner, J.M. & Geiser, F. (2008). Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95, 73-78.
79. White, C.R., Blackburn, T.M. & Seymour, R.S. (2009). Phylogenetically informed analysis of the allometry of mammalian basal metabolic rate supports neither geometric nor quarter-power scaling. Evolution 63, 2658-2667.
80. Withers, P.C. & Cooper, C.E. (2009a). Thermal, metabolic, and hygric physiology of the little red kaluta, Dasykaluta rosamondae (Dasyuromorphia: Dasyuridae). J. Mammal. 90, 752-760.
81. Withers, P.C. & Cooper, C.E. (2009b). Thermal, metabolic, hygric and ventilatory physiology of the sandhill dunnart (Sminthopsis psammophila; Marsupialia, Dasyuridae). Comp. Biochem. Physiol. A 153, 317-323.
82. Withers, P.C., Richardson, K.C. & Wooller, R.D. (1990). Metabolic physiology of euthermic and torpid honey possums, Tarsipes rostratus. Aust. J. Zool. 37, 685-693.
83. Withers, P.C., Thompson, G.G. & Seymour, R.S. (2000). Metabolic physiology of the north-western marsupial mole, Notoryctes caurinus (Marsupialia: Notoryctidae). Aust. J. Zool. 48, 241-258.
84. Withers, P.C., Cooper, C.E. & Nespolo, R.F. (2012). Evaporative water loss, relative water economy and evaporative partitioning of a heterothermic marsupial, the monito del monte (Dromiciops gliroides). J. Exp. Biol. 215, 2806-2813.
85. Zervanos, S.M., Maher, C.R., Waldvogel, J.A. & Florant, G.L. (2010). Latitudinal differences in the hibernation characteristics of woodchucks (Marmota monax). Phyiol. Biochem. Zool. 83, 135-141.