Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites

Oecologia

Volumn 161, Issue 3, 2009, Pages 539-548

  DeGabriel, Jane L ^a,b   Moore, Ben D ^b,c   Shipley, Lisa A ^d   Krockenberger, Andrew K ^b   Wallis, Ian R ^a   Johnson, Christopher N ^b   Foley, William J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Brushtail possum; Diet selection; Herbivory; Local adaptation; Plant defence

Indexed keywords

DIET; FOOD INTAKE; HABITAT TYPE; HERBIVORE; LOCAL ADAPTATION; MARSUPIAL; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; SECONDARY METABOLITE; TOLERANCE;

ADAPTATION; ANIMAL; ARTICLE; AUSTRALIA; CHEMISTRY; DIET; FEEDING BEHAVIOR; MALE; PHYSIOLOGY; PLANT; TRICHOSURUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DIET; FEEDING BEHAVIOR; MALE; PLANTS; QUEENSLAND; TRICHOSURUS;

MAMMALIA; METATHERIA; PHALANGERIDAE; TRICHOSURUS; TRICHOSURUS VULPECULA;

EID: 70349286000     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-009-1407-9     Document Type: Article

References (59)

1. Andrew NR, Hughes L (2005) Herbivore damage along a latitudinal gradient: relative impacts of different feeding guilds. Oikos 108:176-182
2. Ayres MP, Scriber JM (1994) Local adaptation to regional climates in Papiliocanadensis (Lepidoptera: Papilionidae). Ecol Monogr 64:465-482
3. Bachmanov AA, Beauchamp GK (2007) Taste receptor genes. Annu Rev Nutr 27:389-414
4. Boland DJ, Brophy JJ, House APN (eds) (1991) Eucalyptus leaf oils. Use, chemistry, distillation and marketing. Inkata, Melbourne
5. Boyle R, McLean S, Foley WJ, Davies NW (1999) Comparative metabolism of dietary terpene, p-cymene, in generalist and specialist folivorous marsupials. J Chem Ecol 25:2109-2126
6. Boyle R, McLean S, Foley WJ, Moore BD, Davies NW, Brandon S (2000) Fate of the dietary terpene, p-cymene, in the male koala. J Chem Ecol 26:1095-1111
7. Brooker MIH, Kleinig DA (1990) Field guide to eucalypts, vol. 1. South-eastern Australia. Inkata, Melbourne
8. Brophy JJ, Goldsack RJ, Forster PI (2005) The leaf oils of the Australian species of Flindersia (Rutaceae). J Essent Oil Res 17:388-395
9. Bryant JP, Provenza FD, Pastor J, Reichardt PB, Clausen TP, Dutoit JT (1991) Interactions between woody-plants and browsing mammals mediated by secondary metabolites. Annu Rev Ecol Syst 22:431-446
10. Coley PD, Aide TM (1991) Comparison of herbivory and plant defences in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in the tropical and temperate regions. Wiley, New York, pp 25-49
11. Coley PD, Bryant JP, Chapin FSI (1985) Resource availability and plant antiherbivore defence. Science 230:895-899
12. Dearing MD, Foley WJ, McLean SR (2005) The influence of plant secondary metabolites on the nutritional ecology of terrestrial herbivorous vertebrates. Annu Rev Ecol Evol Syst 36:169-189
13. DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711-719
14. Edwards WRN (1978) Effect of salicin content of palatability of Populus foliage to opossum (Trichosurus vulpecula). NZ J Sci 21:103-106
15. Eschler BM, Pass DM, Willis R, Foley WJ (2000) Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem Syst Ecol 28:813-824
16. Foley WJ, Iason GR, McArthur C (1999) Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Jung H-JG, Fahey GCJ (eds) Nutritional ecology of herbivores: Proceedings of the Vth International Symposium on the Nutrition of Herbivores. American Society of Animal Science, Savoy, pp 130-209
17. Fox LR, Morrow PA (1981) Specialization: species property or local phenomenon? Science 211:887-893
18. Freeland WJ, Winter JW (1975) Evolutionary consequences of eating: Trichosurus vulpecula (Marsupialia) and the genus Eucalyptus. J Chem Ecol 1:439-455
19. Glendinning JI (1994) Is the bitter rejection response always adaptive? Physiol Behav 56:1217-1227
20. Hallam A, Read J (2006) Do tropical species invest more in anti-herbivore defence than temperate species? A test in Eucryphia (Cunoniaceae) in eastern Australia. J Trop Ecol 22:41-51
21. Hume ID, Esson C (1993) Nutrients, antinutrients and leaf selection by captive koalas (Phascolarctos cinereus). Aust J Zool 41:379-392
22. Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc 64:123-131
23. Jones KMW, Maclagan SJ, Krockenberger AK (2006) Diet selection in the green ringtail possum (Pseudochirops archeri): a specialist folivore in a diverse forest. Austral Ecol 31:799-807
24. Kanowski J, Hopkins MS, Marsh H, Winter JW (2001) Ecological correlates of folivore abundance in north Queensland rainforests. Wildl Res 28:1-8
25. Kerle JA (2001) Possums. The brushtails, ringtails and greater glider. UNSW Press, Sydney
26. Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998a) Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160-169
27. 3 receptor antagonist increases the intake of diets containing Eucalyptus secondary metabolites by marsupials. J Comp Physiol B Biochem Syst Environ Physiol 168:611-618
28. Lawler IR, Stapley J, Foley WJ, Eschler BM (1999) Ecological example of conditioned flavor aversion in plant-herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. J Chem Ecol 25:401-415
29. Magnanou E, Malenke JR, Dearing MD (2009) Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts. Mol Ecol 18:2401-2414
30. Mangione AM, Dearing MD, Karasov WH (2000) Interpopulation differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology 81:2067-2076
31. Marsh KJ, Foley WJ, Cowling A, Wallis IR (2003) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). J Comp Physiol B Biochem Syst Environ Physiol 173:69-78
32. Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103-2112
33. McArthur C, Sanson GD (1993) Nutritional effects and costs of a tannin in two marsupial arboreal folivores. Funct Ecol 7:697-703
34. McArthur C, Sanson GD, Beal AM (1995) Salivary proline-rich proteins in mammals-roles in oral homeostasis and counteracting dietary tannin. J Chem Ecol 21:663-691
35. McEachern MB, Eagles-Smith CA, Efferson CM, van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes. Oikos 113:440-448
36. McLean S, Pass GJ, Foley WJ, Brandon S, Davies NW (2001) Does excretion of secondary metabolites always involve a measurable metabolic cost? Fate of plant antifeedant salicin in common brushtail possum, Trichosurus vulpecula. J Chem Ecol 27:1077-1089
37. McLean S, Brandon S, Boyle RR, Wiggins NL (2008) Development of tolerance to the dietary plant secondary metabolite 1,8-cineole by the brushtail possum (Trichosurus vulpecula). J Chem Ecol 34:672-680
38. Moore BD, Wallis IR, Marsh KJ, Foley WJ (2004a) The role of nutrition in the conservation of the marsupial folivores of eucalypt forests. In: Lunney D (ed) Conservation of Australia's forest fauna, 2nd edn. Royal Zoological Society of New South Wales, Mosman, pp 549-575
39. Moore BD, Wallis IR, Pala-Paul J, Brophy JJ, Willis RH, Foley WJ (2004b) Antiherbivore chemistry of Eucalyptus-cues and deterrents for marsupial folivores. J Chem Ecol 30:1743-1769
40. Moore BD, Foley WJ, Wallis IR, Cowling A, Handasyde KA (2005) A simple understanding of complex chemistry explains feeding preferences of koalas. Biol Lett 1:64-67
41. Nolte DL, Mason JR, Lewis SL (1994) Tolerance of bitter compounds by an herbivore, Cavia porcellus. J Chem Ecol 20:303-308
42. Osawa R, Sly LI (1992) Occurrence of tannin-protein complex degrading Streptococcus sp. in feces of various animals. Syst Appl Microbiol 15:144-147
43. Palo RT, Robbins CT (1991) Plant defenses against mammalian herbivory. CRC, Boca Raton
44. Pass GJ, Foley WJ (2000) Plant secondary metabolites as mammalian feeding deterrents: separating the effects of the taste of salicin from its post-ingestive consequences in the common brushtail possum (Trichosurus vulpecula). J Comp Physiol B Biochem Syst Environ Physiol 170:185-192
45. Procter-Gray E (1984) Dietary ecology of the coppery brushtail possum, green ringtail possum and Lumholtz's tree kangaroo in north Queensland. In: Smith AP, Hume ID (eds) Possums and gliders. Surrey Beatty & Sons, Chipping-Norton, pp 129-135
46. Provenza FD (1995) Tracking variable environments-there is more than one kind of memory. J Chem Ecol 21:911-923
47. Ratkowsky DA, Evans MA, Alldredge JR (1993) Cross-over experiments: design, analysis, and application. Dekker, New York
48. Sasaki E, Shimada T, Osawa R, Nishitani Y, Spring S, Lang E (2005) Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse, Apodemus speciosus, feeding on tannin-rich acorns. Syst Appl Microbiol 28:358-365
49. Shi P, Zhang JZ (2006) Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23:292-300
50. Shi P, Zhang JZ, Yang H, Zhang YP (2003) Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol Biol Evol 20:805-814
51. Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149-1163
52. Shimada T, Saitoh T, Sasaki E, Nishitani Y, Osawa R (2006) Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. J Chem Ecol 32:1165-1180
53. 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 Biochem Syst Environ Physiol 170:211-218
54. Taylor AC, Foulkes J (2004) Molecules and morphology: a taxonomic analysis of the common brushtail possum Trichosurus vulpecula with an emphasis on the central Australian form. In: Goldingay RL, Jackson SM (eds) The biology of Australian possums and gliders. Surrey Beatty & Sons, Chipping-Norton
55. Torregrossa AM, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48-56
56. Twigg LE, King DR (1991) The impact of fluoroacetate-bearing vegetation on native-Australian fauna-a review. Oikos 61:412-430
57. Tyndale-Biscoe H (2005) Life of marsupials. CSIRO, Collingwood
58. Wallis IR, Watson ML, Foley WJ (2002) Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Aust J Zool 50:507-519
59. Wiggins NL, McArthur C, McLean S, Boyle R (2003) Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. J Chem Ecol 29:1447-1464