Advertisement

Journal of Chemical Ecology

, Volume 37, Issue 1, pp 71–84 | Cite as

Foliage Chemistry Influences Tree Choice and Landscape Use of a Gliding Marsupial Folivore

  • Kara N. Youngentob
  • Ian R. Wallis
  • David B. Lindenmayer
  • Jeff T. Wood
  • Matthew L. Pope
  • William J. Foley
Article

Abstract

The chemical quality of forage may determine landscape use and habitat quality for some herbivorous species. However, studies that investigate the relationship between foliar chemistry and foraging choices in wild vertebrates are rare. Petauroides volans (the greater glider) is unique among Australian marsupial folivores because it glides. It also frequently consumes foliage from both major Eucalyptus subgenera, Eucalyptus (common name “monocalypt”) and Symphyomyrtus (common name “symphyomyrtle”), which differ markedly in their foliar chemistry. Such differences are thought to be a product of co-evolution that also led to guild-specific plant secondary metabolite (PSM) specialization among other marsupial eucalypt folivores. To explore whether foliar chemistry influences tree use, we analyzed foliage from eucalypt trees in which we observed P. volans during a radio tracking study and from eucalypt trees in which animals were never observed. We used a combination of chemical assays and near infrared spectrophotometry (NIRS) to determine concentrations of nitrogen (N), in vitro available nitrogen (AvailN), and in vitro digestible dry matter (DDM) from foliage sampled from the monocalypt and symphyomyrtle species, and total formylated phloroglucinol compounds (FPCs) and sideroxylonals (a class of FPCs) from the symphyomyrtle species (FPCs do not occur in monocalypts). Tree size and spatially-dependent, intraspecific variations in sideroxylonals and DDM concentrations in the symphyomyrtle foliage and of N, AvailN, and DDM in the monocalypt species were important indicators of tree use and habitat suitability for P. volans. The results i) demonstrate that guild-specific PSMs do not always lead to guild-specific foraging; ii) provide a compelling co-evolutionary case for the development of gliding in P. volans; and iii) have implications for the management and conservation of this and other folivorous species.

Key Words

Herbivory Available nitrogen Plant secondary metabolite Plant-animal interaction Eucalyptus Petauroides volans Specialist Coevolution 

Notes

Acknowledgements

The authors thank Dr. Karen Marsh for assistance with the field and laboratory components of this research. We also thank Nicole Coggan, Sarah Ugalde, Jeff Whiting, and Stewart Archer for help in the field. Two reviewers provided constructive comments that improved our original manuscript. This research was made possible by the support of The Hermon Slade Foundation, The Wilderness Society, Ecological Society of Australia, The Fenner School of Environment and Society and Botany and Zoology in the Research School of Biology at Australian National University. This research was conducted with the permission of State Forests New South Wales (permit CO32438) and National Parks (permit S12036). This project was approved by the Animal Experimentation Ethics Committee at Australian National University (project number C.RE.47.06).

References

  1. Andrew R. L., Peakall R., Wallis I. R., Wood J. T., Knight E. J., and Foley W. J. 2005. Marker-based quantitative genetics in the wild: The heritability and genetic correlation of chemical defenses in Eucalyptus. Genetics 171:1989–1998.CrossRefPubMedGoogle Scholar
  2. Andrew R. L., Peakall R., Wallis I. R., and Foley W. J. 2007. Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88:716–728.CrossRefPubMedGoogle Scholar
  3. Becerra J. X. 2007. The impact of herbivore-plant coevolution on plant community structure. Proc. Natl. Acad. Sci. USA 104:7483–7488.CrossRefPubMedGoogle Scholar
  4. Braithwaite L. W., Dudzinski M. L., and Turner J. 1983. Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden, NSW. 2. Relationship between the fauna density, richness and diversity, and measured variables of habitat. Aust. Wildl. Res. 10:231–247.CrossRefGoogle Scholar
  5. Chilcott M. J., and Hume I. D. 1984. Nitrogen and urea metabolism and nitrogen requirements of the common ringtail possum, Pseudocheirus peregrinus, fed Eucalyptus andrewsii foliage. Aust. J. Zool. 32:615–622.CrossRefGoogle Scholar
  6. Choo G. M., Waterman P. G., McKey D. B., and Gartlan J. S. 1981. A simple enzyme assay for dry matter digestibility and its value in studying food selection by generalist herbivores. Oecologia 49:170–178.CrossRefGoogle Scholar
  7. Cork S. J., and Foley W. J. 1991. Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defenses in temperate and tropical forests, pp. 133–166, in R. T. Palo and C. T. Robbins (eds.). Plant Chemical Defenses and Mammalian Herbivory. CRC Press, Boca Raton.Google Scholar
  8. Cunningham R. B., Pope M. L., and Lindenmayer D. B. 2004. Patch use by the greater glider (Petauroides volans) in a fragmented forest ecosystem. III. Night-time use of trees. Wildl. Res. 31:579–585.CrossRefGoogle Scholar
  9. DeGabriel J. L., Wallis I. R., Moore B. D., and Foley W. J. 2008. A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156:107–116.CrossRefPubMedGoogle Scholar
  10. DeGabriel J. L., Moore B. D., Foley W. J., and Johnson C. N. 2009. The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711–719.CrossRefPubMedGoogle Scholar
  11. Dyckmans J., Flessa H., Brinkmann K., Mai C., and Polle A. 2002. Carbon and nitrogen dynamics in acid detergent fibre lignins of beech (Fagus sylvatica L.) during the growth phase. Plant Cell Environ. 25:469–478.CrossRefGoogle Scholar
  12. Ehrlich P. R., and Raven P. H. 1964. Butterflies and plants: A study in coevolution. Evolution 18:586–608.CrossRefGoogle Scholar
  13. Elisseeff A., and Pontil M. 2002. Leave-one-out error and stability of learning algorithms with applications. pp. 415 in J.A.K. Suykens (ed.). Advances in Learning Theory: Methods, Models, and Applications. IOS Press, Leuven.Google Scholar
  14. Eschler B. M., Pass D. M., Wallis I. R., and Foley W. J. 2000. Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem. Syst. Ecol. 28:813–824.CrossRefPubMedGoogle Scholar
  15. Foley W. J., and Hume I. D. 1987. Nitrogen requirements and urea metabolism in 2 arboreal marsupials, the greater glider (Petauroides volans) and the brushtail possum (Trichosurus vulpecula), fed eucalyptus foliage. Physiol. Zool. 60:241–250.Google Scholar
  16. Futuyma D. J. 2000. Some current approaches to the evolution of plant-herbivore interactions. Plant Species Biol. 15:1–9.CrossRefGoogle Scholar
  17. Gleadow R. M., Foley W. J., and Woodrow I. E. 1998. Enhanced CO2 alters the relationship between photosynthesis and defense in cyanogenic Eucalyptus cladocalyx. Plant Cell Environ. 21:12–22.CrossRefGoogle Scholar
  18. Hollander M., and Wolfe D. 1999. Nonparametric Statistical Methods. Wiley, New York.Google Scholar
  19. Jackson S.M. 2000. Glide angle in the genus Petaurus and a review of gliding in mammals. Mamm. Rev. 30:9–30.CrossRefGoogle Scholar
  20. Kavanagh R. P., and Lambert M. J. 1990. Food selection by the greater glider, Petauroides volans—is foliar nitrogen a determinant of habitat quality? Aust. Wildl. Res. 17:285–299.CrossRefGoogle Scholar
  21. Knepp R. G., Hamilton J. G., Mohan J. E., Zangerl A. R., Berenbaum M. R., and DeLucia E. H. 2005. Elevated CO2 reduces leaf damage by insect herbivores in a forest community. New Phytol. 167:207–218.CrossRefPubMedGoogle Scholar
  22. Lawler I. R., Foley W. J., Woodrow I. E., and Cork S. J. 1997. The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109:59–68.CrossRefGoogle Scholar
  23. Lawler I. R., Foley W. J., Eschler B. M., Pass D. M., and Handasyde K. 1998a. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160–169.CrossRefGoogle Scholar
  24. Lawler I. R., Foley W., Pass D. M., and Eschler B. M. 1998b. Administration of a 5-HT3 receptor antagonist increases the intake of diets containing Eucalyptus secondary metabolites by marsupials. J. Comp. Physiol. B 168:611–618.CrossRefPubMedGoogle Scholar
  25. Lindenmayer D. B. 1997. Differences in the biology and ecology of arboreal marsupials in forests of southeastern Australia. J. Mammal. 78:1117–1127.CrossRefGoogle Scholar
  26. Lindenmayer D. B., Cunningham R. B., and Pope M. L. 1999. A large-scale “experiment” to examine the effects of landscape context and habitat fragmentation on mammals. Biol. Conserv. 88:387–403.CrossRefGoogle Scholar
  27. Lindroth, R. L. 2010. Impacts of elevated atmospheric CO2 and O3 on forests: Phytochemistry, trophic interactions, and ecosystem dynamics. J. Chem. Ecol. 36:2–21.CrossRefGoogle Scholar
  28. Mansfield J. L., Curtis P. S., Zak D. R., and Pregitzer K. S. 1999. Genotypic variation for condensed tannin production in trembling aspen (Populus tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. Am. J. Bot. 86:1154–1159.CrossRefPubMedGoogle Scholar
  29. Marsh K. J., Foley W. J., Cowling A., and Wallis I. R. 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 173:69–78.PubMedGoogle Scholar
  30. Marsh K. J., Wallis I .R., and Foley W. J. 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. 51:31–42.CrossRefGoogle Scholar
  31. Marsh K. J., Wallis I. R., Andrew R., and Foley W. J. 2006. The detoxification limitation hypothesis: Where did it come from and where is it going? J. Chem. Ecol. 32:1247–1266.CrossRefPubMedGoogle Scholar
  32. McArthur C., and Sanson G. D. 1991. Effects of tannins on digestion in the common ringtail possum (Pseudocheirus peregrinus), a specialized marsupial folivore. J. Zool. 225:233–251.CrossRefGoogle Scholar
  33. McIlwee A. M., Lawler I. R., Cork S. J., and Foley W. J. 2001. Coping with chemical complexity in mammal-plant interactions: near-infrared spectroscopy as a predictor of Eucalyptus foliar nutrients and of the feeding rates of folivorous marsupials. Oecologia 128:539–548.CrossRefGoogle Scholar
  34. Moore B. D., and Foley W. J. 2005. Tree use by koalas in a chemically complex landscape. Nature 435:488–490.CrossRefPubMedGoogle Scholar
  35. Moore B. D., Wallis I. R., Marsh K. J., and Foley W. J. 2004. The role of nutrition in the conservation of the marsupial folivores of eucalypt forests, pp. 549–575, in D. Lunny (ed.). Conservation of Australia’s Forest Fauna. CSIRO, Collingwood.Google Scholar
  36. Moore B. D., Foley W. J., Wallis I. R., Cowling A., and Handasyde K. A. 2005. Eucalyptus foliar chemistry explains selective feeding by koalas. Biol. Lett. 1:64–67.CrossRefPubMedGoogle Scholar
  37. Moore B. D., Lawler I. R., Wallis I. R., Beale C. M., and Foley W. J. 2010. Palatability mapping: A koala’s eye view of spatial variation in habitat quality. Ecology 91:3165–3176.CrossRefPubMedGoogle Scholar
  38. Osawa R., and Sly L. I. 1992. Occurrence of tannin-protein complex degrading Streptococcus sp. in feces of various animals. Syst. Appl. Microbiol. 15:144–147.Google Scholar
  39. Osborne B. G., Fearn T., Hindle P. T., and Osborne B. G. 1993. Practical NIR Spectroscopy with Applications in Food and Beverage Analysis. Longman Publishing Group, Essex.Google Scholar
  40. Pinto, D. M., Blande, J. D., Souza, S. R., Nerg, A.-M., and Holopainen, J. K. 2010. Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: The ecological effects. J. Chem. Ecol. 36:22–34.CrossRefGoogle Scholar
  41. Pope M. L., Lindenmayer D.B., and Cunningham R. B. 2004. Patch use by the greater glider (Petauroides volans) in a fragmented forest ecosystem. I. Home range size and movements. Wildl. Res. 31:559–568.CrossRefGoogle Scholar
  42. Pryor L. D. 1959. Species distribution and association in Eucalyptus. pp. 461–471, in Keast A., Crocker R. L., and Christian C. S. (eds.). Biogeography and Ecology in Australia. Junk, The Hague.Google Scholar
  43. Rausher M. D. 2001. Coevolution and plant resistance to natural enemies. Nature 411:857–864.CrossRefPubMedGoogle Scholar
  44. Scrivener N. J., Johnson C. N., Wallis I. R., Takasaki M., Foley W. J., and Krockenberger A. K. 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. 6:77–87.Google Scholar
  45. Shenk J. S., and Westerhaus M. O. 1991. Population structuring of near-infrared spectra and modified partial least-squares regression. Crop Sci. 31:1548–1555.CrossRefGoogle Scholar
  46. Shipley L. A., Forbey J. S., and Moore B. D. 2009. Revisiting the dietary niche: when is a mammalian herbivore a specialist? Integr. Comp. Biol. 49:274–290.CrossRefGoogle Scholar
  47. Silanikove N., Gilboa N., Nir I., Pervolotsky A., and Nitsan Z. 1996. Effect of a daily supplementation of polyethylene glycol on intake and digestion of tannin-containing leaves (Quercus calliprinos, Pistacia lentiscus, and Ceratonia siliqua) by goats. J. Agr. Food Chem. 44:199–205.CrossRefGoogle Scholar
  48. Stephens D. W., and Krebs J.R. 1986. Foraging Theory. Princeton University Press, Princeton.Google Scholar
  49. Thompson J. N. 1994. The Coevolutionary Process. University of Chicago Press, Chicago.Google Scholar
  50. Wallis I. R., and Foley W. J. 2005. The rapid determination of sideroxylonals in Eucalyptus foliage by extraction with sonication followed by HPLC. Phytochem. Anal. 16:49–54.CrossRefPubMedGoogle Scholar
  51. Wallis I. R., Watson M. L., and Foley W. J. 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.CrossRefGoogle Scholar
  52. Wallis I. R., Nicolle D., and Foley W. J. 2010. Available and not total nitrogen in leaves explains key chemical differences between the eucalypt subgenera. For. Ecol. Manag. 260:814–821CrossRefGoogle Scholar
  53. Zvereva E. L., and Kozlov M. V. 2006. Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta-analysis. Glob. Change Biol. 12:27–41.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Kara N. Youngentob
    • 1
  • Ian R. Wallis
    • 2
  • David B. Lindenmayer
    • 1
  • Jeff T. Wood
    • 1
  • Matthew L. Pope
    • 1
  • William J. Foley
    • 2
  1. 1.The Fenner School of Environment and SocietyThe Australian National UniversityCanberraAustralia
  2. 2.Botany and Zoology, Research School of BiologyThe Australian National UniversityCanberraAustralia

Personalised recommendations