, Volume 168, Issue 4, pp 889–899 | Cite as

The limit to the distribution of a rainforest marsupial folivore is consistent with the thermal intolerance hypothesis

  • Andrew K. Krockenberger
  • Will Edwards
  • John Kanowski
Physiological ecology - Original Paper


Models of impacts of climate change on species are generally based on correlations between current distributions and climatic variables, rather than a detailed understanding of the mechanisms that actually limit distribution. Many of the vertebrates endemic to rainforests of northeastern Australia are restricted to upland forests and considered to be threatened by climate change. However, for most of these species, the factors controlling their distributions are unknown. We examined the role of thermal intolerance as a possible mechanism limiting the distribution of Pseudochirops archeri (green ringtail possum), a specialist arboreal folivore restricted to rainforests above an altitude of 300 m in Australia’s Wet Tropics. We measured short-term metabolic responses to a range of ambient temperatures, and found that P. archeri stores heat when ambient temperatures exceed 30°C, reducing water requirements for evaporative cooling. Due to the rate at which body temperature increases with ambient temperatures >30°C, this strategy is not effective over periods longer than 5 h. We hypothesise that the distribution of P. archeri is limited by interactions between (i) the duration and severity of extreme ambient temperatures (over 30°C), (ii) the scarcity of free water in the rainforest canopy in the dry season, and (iii) constraints on water intake from foliage imposed by plant secondary metabolites and fibre. We predict that dehydration becomes limiting for P. archeri where extreme ambient temperatures (>30°C) persist for more than 5 h per day over 4–6 days or more. Consistent with our hypothesis, the abundance of P. archeri in the field is correlated with the occurrence of extreme temperatures, declining markedly at sites where the average maximum temperature of the warmest week of the year is above 30°C. Assuming the mechanism of limitation is based on extreme temperatures, we expect impacts of climate change on P. archeri to occur in discrete, rapid events rather than as a slow contraction in range.


Climate change Limits to distribution Metabolic rate Plant secondary metabolites Temperature extremes Water availability 



We would like to thank the Nasser family for permission to study the possums on their property, and our volunteers, especially Steve McKenna, for assistance with fieldwork. Thanks to Dr John Winter for discussion and stimulating this work, Dr David Westcott, Dr Chris Margules and CSIRO TFRI Atherton for providing laboratory space for the respirometry, and the reviewers for comments that helped us to improve the manuscript. The laboratory measurements were funded by the James Cook University Merit Research Grant Scheme and Rainforest CRC, and ongoing analysis by the Marine and Tropical Sciences Research Facility. The climate data were provided by the Spatial Modelling and Data Exchange project of the Rainforest CRC using the ANUCLIM software and data developed by the Centre for Resource and Environmental Studies at the Australian National University. This study complied with the legal and ethical requirements of the state of Queensland, and was conducted under approvals from the JCU Animal Ethics Committee (A856) and Queensland EPA (WISP01557603).


  1. Adolph EF (1947) Tolerance to heat and dehydration in several species of mammals. Am J Physiol 151:564–575PubMedGoogle Scholar
  2. Bartholomew GA, Rainy M (1971) Regulation of body temperature in the rock hyrax, Heterohyrax brucei. J Mammal 52:81–95PubMedCrossRefGoogle Scholar
  3. Beever EA, Ray C, Mote PW, Wilkening JL (2010) Testing alternative models of climate-mediated extirpations. Ecol Appls 20:164–178CrossRefGoogle Scholar
  4. Berteaux D, Humphries MM, Krebs CJ, Lima M, McAdams AG, Pettorelli N, Réale D, Saitoh T, Tlkadlec E, Weladji RB, NChr Stenseth (2006) Constraints to projecting the effects of climate change on mammals. Clim Res 32:151–158CrossRefGoogle Scholar
  5. Bureau of Meteorology (2011) Climate data online.
  6. Coley PD, Barone JA (1996) Herbivory and plant defences in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  7. Cork SJ (1994) Digestive constraints on dietary scope in small and moderately-small mammals: how much to we really understand? In: Chivers DJ, Langer P (eds) The digestive system in mammals: food, form and function. Cambridge University Press, Cambridge, pp 337–369CrossRefGoogle Scholar
  8. Cork SJ, Foley WJ (1991) Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defences in temperate and tropical forests. In: Palo RT, Robbins CT (eds) Plant defences against mammalian herbivory. CRC Press, Boca Raton, pp 133–166Google Scholar
  9. Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, LondonCrossRefGoogle Scholar
  10. Crowe O, Hume ID (1997) Morphology and function of the gastrointestinal tract of Australian folivorous possums. Aust J Zool 45:357–368CrossRefGoogle Scholar
  11. CSIRO, Bureau of Meteorology (2007) Climate change in Australia (technical report).
  12. Dawson TJ, Hulbert AJ (1970) Standard metabolism, body temperature, and surface area of Australian marsupials. Am J Physiol 218:1233–1238PubMedGoogle Scholar
  13. Dawson T, Blaney C, Munn A, Krockenberger AK, Maloney S (2000a) Thermoregulation by kangaroos from mesic and arid habitats: influence of temperature on routes of heat loss in eastern grey kangaroos (Macropus giganteus) and red kangaroos (Macropus rufus). Physiol Biochem Zool 73:374–381PubMedCrossRefGoogle Scholar
  14. Dawson T, Munn A, Blaney C, Krockenberger AK, Maloney S (2000b) Ventilatory accomodation of oxygen demand and respiratory water loss in kangaroos from mesic and arid environments, the eastern grey kangaroo (Macropus giganteus) and red kangaroo (Macropus rufus). Physiol Biochem Zool 73:382–388PubMedCrossRefGoogle Scholar
  15. Dawson TJ, Blaney CE, McCarron HCK, Maloney SK (2007) Dehydration, with and without heat, in kangaroos from mesic and arid habitats: different thermal responses including varying patterns in heterothermy in the field and laboratory. J Comp Physiol B 177:797–807PubMedCrossRefGoogle Scholar
  16. Dearing MD, Mangione AM, Karasov WH (2001) Plant secondary compounds as diuretics: an overlooked consequence. Am Zool 41:890–901CrossRefGoogle Scholar
  17. Dearing MD, Mangione AM, Karasov WH (2002) Ingestion of plant secondary compounds causes diuresis in desert herbivores. Oecologia 130:576–584CrossRefGoogle Scholar
  18. Foley WJ (1992) Nitrogen and energy retention and acid-base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals. Physiol Zool 65:403–421Google Scholar
  19. Foley WJ, Moore BD (2005) Plant secondary metabolites and vertebrate herbivores—from physiological regulation to ecosystem function. Curr Opin Plant Biol 8:430–435PubMedCrossRefGoogle Scholar
  20. Foley WJ, Kehl JC, Nagy KA, Kaplan IR, Borsboom AC (1990) Energy and water metabolism in free-living greater gliders, Petauroides volans. Aust J Zool 38:1–9CrossRefGoogle Scholar
  21. Foley WJ, McLean S, Cork SJ (1995) Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals—a final common pathway? J Chem Ecol 21:721–743CrossRefGoogle Scholar
  22. Geiser F, Holloway JC, Kortner G (2007) Thermal biology, torpor and behaviour in sugar gliders: a laboratory–field comparison. J Comp Physiol B 177:495–501Google Scholar
  23. Gessaman JA, Nagy KA (1988) Energy metabolism: errors in gas exchange conversion factors. Physiol Zool 61:507–513Google Scholar
  24. Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875Google Scholar
  25. Goudberg N (1990) The feeding ecology of three species of north Queensland upland rainforest possums, Hemibelideus lemuroides, Pseudocheirus herbertensis and Pseudocheirus archeri (Marsupialia: Petauridae) (PhD thesis). James Cook University, TownsvilleGoogle Scholar
  26. Green B (1997) Field energetics and water fluxes in marsupials. In: Saunders NR LA, Hinds LA (eds) Marsupial biology: recent research, new perspectives. UNSW Press, Sydney, pp 143–162Google Scholar
  27. Hilbert DW, Ostendorf B, Hopkins MS (2001) Sensitivity of tropical forests to climate change in the humid tropics of north Queensland. Aust Ecol 26:590–603CrossRefGoogle Scholar
  28. Iason GR, Villalba JJ (2006) Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance–tolerance continuum. J Chem Ecol 32:1115–1132Google Scholar
  29. IPCC (2007) Climate Change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  30. Jessen C (2001) Temperature regulation in humans and other mammals. Springer, BerlinCrossRefGoogle Scholar
  31. Jones KM, Maclagan SJ, Krockenberger AK (2006) Diet selection in the green ringtail possum (Pseudochirops archeri): a specialist folivore in a diverse forest. Aust Ecol 31:799–807CrossRefGoogle Scholar
  32. Kanowski J (2001) Effects of elevated CO2 on the foliar chemistry of seedlings of two rainforest trees from north-east Australia: implications for folivorous marsupials. Aust Ecol 26:165–172CrossRefGoogle Scholar
  33. Kanowski J (2004) Ecological determinants of the distribution and abundance of folivorous possums inhabiting rainforests of the Atherton Tablelands, north-east Queensland. In: Goldingay R, Jackson S (eds) The biology of australian possums and gliders. Surrey Beatty and Sons, Chipping Norton, pp 539–548Google Scholar
  34. Kanowski J, Hopkins MS, Marsh H, Winter JW (2001) Ecological correlates of folivore abundance in north Queensland rainforests. Wildl Res 28:1–8CrossRefGoogle Scholar
  35. Kanowski J, Irvine AK, Winter JW (2003) The relationship between the floristic composition of rain forests and the abundance of folivorous marsupials in north-east Queensland. J Anim Ecol 72:627–632CrossRefGoogle Scholar
  36. Kearney MR, Wintle BA, Porter WP (2010) Correlative and mechanistic models of species distribution provide congruent forecasts under climate change. Conserv Lett 3:203–213CrossRefGoogle Scholar
  37. Krockenberger AK (2003) Meeting the energy demands of reproduction in female koalas, Phascolarctos cinereus: evidence for energetic compensation. J Comp Physiol B 173:531–540PubMedCrossRefGoogle Scholar
  38. Krockenberger AK, Hume ID (2007) A flexible digestive strategy accommodates the nutritional demands of reproduction in a free-living folivore, the Koala (Phascolarctos cinereus). Funct Ecol 21:748–756CrossRefGoogle Scholar
  39. Lawler IR, Foley WJ, Eschler BM (2000) Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81:1327–1338CrossRefGoogle Scholar
  40. Lin HC, Thurmon JC, Benson GJ, Tranquilli WJ (1993) Telazol—a review of its pharmacology and use in veterinary medicine. J Vet Pharmacol Therapeutics 16:383–418Google Scholar
  41. Malan A (1973) Ventilation measured by body plethysmography in hibernating mammals and in poikilotherms. Respir Physiol 17:32–44PubMedCrossRefGoogle Scholar
  42. Maloney SK, Bronner GN, Buffenstein R (1999) Thermoregulation in the Angolan Free-Tailed Bat Mops condylurus: a small mammal that uses hot roosts. Physiol Biochem Zool 72:385–396PubMedCrossRefGoogle Scholar
  43. Marsh KJ, Foley WJ, Cowling A, Wallis IR (2003a) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 173:69–78PubMedGoogle Scholar
  44. Marsh KJ, Wallis IR, Foley WJ (2003b) The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula). Aust J Zool 51:31–42CrossRefGoogle Scholar
  45. Marsh KJ, Wallis IR, Andrew RL, Foley WJ (2006a) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32:1247–1266PubMedCrossRefGoogle Scholar
  46. Marsh KJ, Wallis IR, McLean S, Sorenson JS, Foley WJ (2006b) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103–2112PubMedCrossRefGoogle Scholar
  47. McJannet D, Wallace J, Fitch P, Disher M, Reddell P (2007) Water balance of tropical rainforest canopies in north Queensland, Australia. Hydrol Process 21:3473–3484CrossRefGoogle Scholar
  48. McLean S, Brandon S, Davies NW, Foley WJ, Muller HK (2004) Jensenone: biological reactivity of a marsupial antifeedant from Eucalyptus. J Chem Ecol 30:19–36PubMedCrossRefGoogle Scholar
  49. Miller RE, Jensen R, Woodrow IE (2006) Frequency of cyanogenesis in tropical rainforests of far north Queensland, Australia. Ann Bot 97:1017–1044PubMedCrossRefGoogle Scholar
  50. Mitchell D, Maloney SK, Jessen J, Laburn HP, Kamerman PR, Mitchell G, Fuller A (2002) Adaptive heterothermy and selective brain cooling in arid-zone mammals. Comp Biochem Physiol B 131:571–585PubMedCrossRefGoogle Scholar
  51. Moore BD, Foley WJ, Wallis IR, Cowling A, Handasyde KA (2005) Eucalyptus foliar chemistry explains selective feeding by koalas. Biol Lett 1:64–67PubMedCrossRefGoogle Scholar
  52. Munks SA (1990) Ecological energetics and reproduction in the common ringtail possum, Pseudocheirus peregrinus (PhD thesis). University of Tasmania, HobartGoogle Scholar
  53. Munks SA, Green B (1995) Energy allocation for reproduction in a marsupial arboreal folivore, the common ringtail possum (Pseudocheirus peregrinus). Oecologia 101:94–104CrossRefGoogle Scholar
  54. Nagy KA, Bradshaw SD (2000) Scaling of energy and water fluxes in free-living arid-zone Australian marsupials. J Mammal 81:962–970CrossRefGoogle Scholar
  55. Needham AD, Dawson TJ, Hales JRS (1974) Forelimb blood flow and saliva spreading in the thermoregulation of the red kangaroo, Megaleia rufa. Comp Biochem Physiol 49A:555–565CrossRefGoogle Scholar
  56. Nix HA (1991) Biogeography: pattern and process. In: Nix HA, Switzer MA (eds) Rainforest animals: atlas of vertebrates endemic to Australia’s Wet Tropics. Australian National Parks and Wildlife Service, Canberra, pp 11–39Google Scholar
  57. Ostrowski S, Williams JB (2006) Heterothermy of free-living Arabian sand gazelles (Gazella subgutturosa marica) in a desert environment. J Exp Biol 209:1421–1429PubMedCrossRefGoogle Scholar
  58. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  59. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, ánchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167PubMedCrossRefGoogle Scholar
  60. Procter-Gray E (1985) The behaviour and ecology of Lumholtz’s tree-kangaroo, Dendrolagus lumholtzi (Marsupialia: Macropodidae) (Ph.D. thesis). Harvard University, CambridgeGoogle Scholar
  61. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
  62. Robinson KW, Morrison PR (1957) The reaction to hot atmospheres of various species of Australian marsupial and placental animals. J Cell Comp Physiol 49:455–478CrossRefGoogle Scholar
  63. Rubsamen K, Hume ID, Foley WJ, Rubsamen U (1984) Implications of the large surface area to body mass ratio on the heat balance of the greater glider (Petauroides volans: Marsupialia). J Comp Physiol B 154:105–111CrossRefGoogle Scholar
  64. Schmidt-Nielsen K, Schmidt-Nielsen B, Jornum SA, Haupt TR (1957) Body temperature of the camel and its relation to water economy. Am J Physiol 188:103–112PubMedGoogle Scholar
  65. Scrivener NJ, Johnson CN, Wallis IR, Takasaki M, Krockenberger AK (2004) Which trees do wild common brushtail possums (Trichosurus vulpecula) prefer? Problems and solutions in scaling laboratory findings to diet selection in the field. Evol Ecol Res 6:77–87Google Scholar
  66. Semple HA, Gorecki DK, Farley SD, Ramsay MA (2000) Pharmacokinetics and tissue residues of Telazol in free-ranging polar bears. J Wildl Dis 36:653–662Google Scholar
  67. Sorensen JS, McLister JD, Dearing MS (2005) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139CrossRefGoogle Scholar
  68. Stapley J, Foley WJ, Cunningham R, Eschler B (2000) How well can common brushtail possums regulate their intake of Eucalyptus toxins? J Comp Physiol B 170:211–218PubMedCrossRefGoogle Scholar
  69. Still CJ, Foster NF, Schneider SH (1999) Simulating the effects of climate change on tropical montane cloud forests. Nature 398:608–610CrossRefGoogle Scholar
  70. Thibodeau GA, Patton KT (2006) Anatomy and physiology, 6th edn. Elsevier, PhiladelphiaGoogle Scholar
  71. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont L, Collingham YC, Erasmus BFN, Ferreira de Siqueira M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Townsend Peterson A, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148PubMedCrossRefGoogle Scholar
  72. Torregrossa A-M, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56CrossRefGoogle Scholar
  73. Tracey JG (1982) The vegetation of the humid tropical region of north Queensland. CSIRO, Melbourne, 124 ppGoogle Scholar
  74. Warnecke L, Withers PC, Schleucher E, Maloney SK (2007) Body temperature variation of free-ranging and captive southern brown bandicoots Isoodon obesulus (Marsupialia: Peramelidae). J Therm Biol 32:72–77CrossRefGoogle Scholar
  75. Williams SE, Bolitho E, Fox S (2003) Climate change in Australian tropical rainforests: an impending environmental catastrophe. Proc Roy Soc Lond 270:1887–1892CrossRefGoogle Scholar
  76. Winter JW (1997) Responses of non-volant mammals to late Quaternary climatic changes in the Wet Tropics region of north-eastern Australia. Wildl Res 24:493–511CrossRefGoogle Scholar
  77. Winter JW, Krockenberger AK, Moore NJ (2008) Green Ringtail Possum, Pseudochirops archeri. In: Van Dyke S, Strahan R (eds) The mammals of australia. Reed New Holland Pty Ltd, Sydney, pp 245–247Google Scholar
  78. Withers PC (1977) Measurement of VO2, VCO2 and evaporative water loss with a flow through mask. J Appl Physiol 42:120–123PubMedGoogle Scholar
  79. Withers PC (1992) Comparative animal physiology. WB Saunders, SydneyGoogle Scholar
  80. Withers PC, Thompson GG, Seymour RS (2000) Metabolic physiology of the north-western marsupial mole, Notoryctes caurinus (Marsupialia: Notorycidae). Aust J Zool 48:241–258CrossRefGoogle Scholar
  81. Withers PC, Cooper CE, Larcombe AN (2006) Environmental correlates of physiological variables in marsupials. Physiol Biochem Zool 79:437–453PubMedCrossRefGoogle Scholar
  82. Warthog Systems (2011) Data acquisition and analysis software for the Macintosh. Mark Chappell and the Regents of the University of California, Riverside.
  83. Young BA, Fenton TW, McLean JA (1984) Calibration methods in respiratory calorimetry. J Appl Physiol 56:1120–1125PubMedGoogle Scholar
  84. Zurr AF, Ieno EN, Walker NJ, Savelier AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Andrew K. Krockenberger
    • 1
  • Will Edwards
    • 2
  • John Kanowski
    • 3
  1. 1.Centre for Tropical Biodiversity and Climate Change, School of Marine and Tropical BiologyJames Cook UniversityCairnsAustralia
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityCairnsAustralia
  3. 3.Australian Wildlife Conservancy, North-east Australia, and Environmental Futures CentreGriffith UniversityNathanAustralia

Personalised recommendations