Abstract
Most woody plants contain a diverse array of plant secondary metabolites (PSMs) that deter vertebrate herbivores. However, mammalian folivores have evolved a complex of physiological and behavioural strategies to counter these compounds, leading to the development of an “evolutionary arms race”. Marsupial folivores are ideal models to investigate the role of PSMs in the interaction between the external foraging environment and the digestive physiology of mammalian herbivores, as we have a very strong understanding of the diversity and modes of action of PSMs in Eucalyptus, as well as the mechanisms by which animals overcome the effects of these compounds. Studies of marsupial folivores have benefited from the facts that: these herbivores subsist on relatively poor quality diets; they include feeding types from specialist species such as the koala, to generalists; and life history factors such as maternal investment in reproduction can be measured more easily than in eutherians. Here, we describe patterns of spatial variation in the types and distributions of plant secondary metabolites in Australian forests and discuss how this variation influences foraging behaviour, habitat selection and life history strategies in arboreal, folivorous marsupials. We also provide a summary of our understanding of the mechanisms by which marsupials detect and regulate their intake of toxic compounds. While our examples are drawn largely from studies of the interaction between marsupials and Eucalyptus, this knowledge is applicable to advancing our understanding of interactions in plant–mammal systems more broadly. We also identify and discuss key areas that should be the focus of future research.
Similar content being viewed by others
References
Agrawal AA (2004) Plant defense and density dependence in the population growth of herbivores. Am Nat 164:113–120
Andrew RL, Peakall R, Wallis IR, Foley WJ (2007) Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88:716–728
Andrews PL, Horn CC (2006) Signals for nausea and emesis: Implications for models of upper gastrointestinal diseases. Auton Neurosci 125:100–115
Andrews PLR, Rudd JA (2004) The role of tachykinins and the tachykinin NK1 receptor in nausea and emesis. Handb Exp Pharmacol 164:359–440
Braithwaite LW (1996) Conservation of arboreal herbivores: The Australian scene. Aust J Ecol 21:21–30
Braithwaite LW, Turner J, Kelly J (1984) Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden N.S.W. III. Relationships between faunal densities, eucalypt occurrence and foliage nutrients, and soil parent materials. Aust Wildl Res 11:41–48
Bryant JP, Kuropat PJ (1980) Selection of winter forage by sub-arctic browsing vertebrates—the role of plant chemistry. Annu Rev Ecol Syst 11:261–285
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
Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR (2004) Predicting folivorous primate abundance: Validation of a nutritional model. Am J Primatol 62:55–69
Clinchy M, Taylor AC, Zanette LY, Krebs CJ, Jarman PJ (2004) Body size, age and paternity in common brushtail possums (Trichosurus vulpecula). Mol Ecol 13:195–202
Close DC, McArthur C (2002) Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99:166–172
Close DC, McArthur C, Hagerman AE, Fitzgerald H (2005) Differential distribution of leaf chemistry in eucalypt seedlings due to variation in whole-plant nutrient availability. Phytochemistry 66:215–221
Cork SJ (1992) Polyphenols and the distribution of arboreal, folivorous marsupials in Eucalyptus forests of Australia. In: Hemingway RW, Laks PE (eds) Plant polyphenols: synthesis, properties, significance. Plenum Press, New York, pp 653–663
Cork SJ, Catling PC (1996) Modelling distributions of arboreal and ground-dwelling mammals in relation to climate, nutrients, plant chemical defences and vegetation structure in the eucalypt forests of southeastern Australia. For Ecol Manage 85:163–175
Cork SJ, Dove H (1989) Lactation in the tammar wallaby (Macropus eugenii). 2. Intake of milk components and maternal allocation of energy. J Zool 219:399–409
Cork SJ, Hume ID, Dawson TJ (1983) Digestion and metabolism of a natural foliar diet (Eucalyptus punctata) by an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol B Biochem Syst Environ Physiol 153:181–190
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
DeGabriel JL (2008) Demographic constraints imposed by plant nutrients and secondary chemistry on the common brushtail possum (Trichosurus vulpecula Kerr). Ph.D. thesis, The Australian National University
DeGabriel JL, Wallis IR, Moore BD, Foley WJ (2008) A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156:107–116
DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009a) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711–719
DeGabriel JL, Moore BD, Shipley LA, Krockenberger AK, Wallis IR, Johnson CN, Foley WJ (2009b) Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites. Oecologia 161:539–548
Edwards MJ, Wallis IR, Foley WJ (2009) Acid loads induced by the detoxification of plant secondary metabolites do not limit feeding by the common brushtail possum (Trichosurus vulpecula). J Comp Physiol B Biochem Syst Environ Physiol. doi:10.1007/s00360-009-0404-y
Eschler BM, Pass DM, Willis R, Foley WJ (2000) Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem Syst Ecol 28:813–824
Foley WJ, Hume ID (1987) Digestion and metabolism of high-tannin Eucalyptus foliage by the brushtail possum (Trichosurus vulpecula) (Marsupialia: Phalangeridae). J Comp Physiol B Biochem Syst Environ Physiol 157:67–76
Foley WJ, McArthur C (1994) The effects and costs of allelochemicals for mammalian herbivores: an ecological perspective. In: Chivers DJ, Langer P (eds) The Digestive System in Mammals: Food, Form and Function. Cambridge University Press, Cambridge
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 21:721–743
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, Illinois, pp 130–209
Forbey JS, Foley WJ (2009) PharmEcology: A pharmacological approach to understanding plant–herbivore interactions: an introduction to the symposium. Integr Comp Biol 49:267–273
Forbey JS, Harvey AL, Huffman MA, Provenza FD, Sullivan R, Tasdemir D (2009) Exploitation of secondary metabolites by animals: A response to homeostatic challenges. Integr Comp Biol 49:314–328
Fox LR, Macauley BJ (1977) Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia 29:145–162
Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–287
Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests. Test of a hypothesis. Oecologia 91:540–547
Garcia J (1989) Food for Tolman: Cognition and cathexis in concert. In: Archer T, Nilsson L (eds) Aversion, avoidance and anxiety. Erlbaum, Hillsdale, N.J., pp 45–85
Hagerman AE, Robbins CT, Weerasuriya Y, Wilson TC, McArthur C (1992) Tannin chemistry in relation to digestion. J Range Manage 45:57–62
Henery ML, Moran GF, Wallis IR, Foley WJ (2007) Identification of quantitative trait loci influencing foliar concentrations of terpenes and formylated phloroglucinol compounds in Eucalyptus nitens. New Phytol 176:82–95
Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge, U.K
Huttunen L, Niemela P, Julkunen-Tiitto R, Heiska S, Tegelberg R, Rousi M, Kellomaki S (2008) Does defoliation induce chemical and morphological defenses in the leaves of silver birch seedlings under changing climate? Chemoecology 18:85–98
Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc 64:123–131
Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton JK, Sim DA, Elston DA (2005) Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecol Lett 8:364–369
Johnson CN, Vernes K, Payne A (2005) Demography in relation to two herbivorous marsupials: testing for source-sink dynamics versus independent regulation of population size. Oecologia 143:70–76
Jones BA, How RA, Kitchener DJ (1994) A field study of Pseudocheirus occidentalis (Marsupialia, Petauridae).1. Distribution and habitat. Wildl Res 21:175–187
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
Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108:421–430
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. Austral Ecol 26:165–172
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 21:748–756
Krockenberger AK, Hume ID, Cork SJ (1998) Production of milk and nutrition of the dependent young of free-ranging koalas (Phascolarctos cinereus). Physiol Zool 71:45–56
Landau S, Dvash L, Decandia M, Cabiddu A, Shapiro F, Molle G, Silanikove N (2004) Determination of poly(ethylene glycol)-binding to browse foliage, as an assay of tannin, by near-infrared reflectance spectroscopy. J Agric Food Chem 52:638–642
Lawler IR, Foley WJ, Woodrow IE, Cork SJ (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
Lawler IR, Foley WJ, Pass GJ, Eschler BM (1998) Administration of a 5HT3 receptor antagonist increases the intake of diets containing Eucalyptus secondary metabolites by marsupials. J Comp Physiol B Biochem Syst Environ Physiol 168:611–618
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
Levin DA (1976) Chemical defenses of plants to pathogens and herbivores. Annu Rev Ecol Syst 7:121–159
Mangione AM, Dearing MD, Karasov WH (2000) Interpopulation differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology 81:2067–2076
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 Biochem Syst Environ Physiol 173:69–78
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 51:31–42
Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86:2946–2954
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 32:1247–1266
Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006b) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103–2112
Martin JK, Martin AA (2007) Resource distribution influences mating system in the bobuck (Trichosurus cunninghami: Marsupialia). Oecologia 154:227–236
Mattson WJ, Kuokkanen K, Niemela P, Julkunen-Tiitto R, Kellomaki S, Tahvanainen J (2004) Elevated CO2 alters birch resistance to Lagomorpha herbivores. Glob Chang Biol 10:1402–1413
McArt SH, Spalinger DE, Collins WB, Schoen ER, Stevenson T, Bucho M (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology 90:1400–1411
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
McKay GM (1983) Greater glider (Petuaroides volans). In: Strahan R (ed) The Australian Museum complete book of Australian mammals. Angus and Robertson, Sydney
McKey D, Waterman PG, Mbi CN, Gartlan JS, Struhsaker TT (1978) Phenolic content of vegetation in two African rain forests: ecological implications. Science 202:61–63
McLean S, Boyle RR, Brandon S, Davies NW, Sorensen JS (2007) Pharmacokinetics of 1, 8-cineole, a dietary toxin, in the brushtail possum (Trichosurus vulpecula): Significance for feeding. Xenobiotica 37:903–922
Min BR, Barry TN, Attwood GT, McNabb WC (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim Feed Sci Technol 106:3–19
Mole S, Waterman PG (1987) A critical analysis of techniques for measuring tannins in ecological studies. I. Techniques for chemically defining tannins. Oecologia 72:137–147
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 edition edn. Royal Zoological Society of New South Wales, Mosman, NSW, pp 549–575
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
Moore BD, Wallis IR, Wood J, Foley WJ (2004c) Foliar nutrition, site quality and temperature affect foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol Monogr 74:553–568
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
Munks S (1995) The breeding biology of Pseudocheirus peregrinus viverrinus on Flinders Island, Bass Strait. Wildl Res 22:521–534
Munks SA, Green B (1997) Milk consumption and growth in a marsupial arboreal folivore, the common ringtail possum, Pseudocheirus peregrinus. Physiol Zool 70:691–700
O’Reilly-Wapstra JM, McArthur C, Potts BM (2004) Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species. Funct Ecol 18:677–684
Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, Dasilva GL, Mole S (1990) Determinants of variation in tropical forest primate biomass: new evidence from West Africa. Ecology 71:328–343
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
Pausas JG, Braithwaite LW, Austin MP (1995) Modelling habitat quality for arboreal marsupials in the south coastal forests of New South Wales, Australia. For Ecol Manage 78:39–49
Pettorelli N, Gaillard JM, Duncan P, Ouellet JP, Van Laere G (2001) Population density and small-scale variation in habitat quality affect phenotypic quality in roe deer. Oecologia 128:400–405
Provenza FD (1996) Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J Anim Sci 74:2010–2020
Provenza FD, Lynch JJ, Burritt EA, Scott CB (1994) How goats learn to distinguish between novel foods that differ in postingestive consequences. J Chem Ecol 20:609–624
Provenza FD, Kimball BA, Villalba JJ (2000) Roles of odor, taste, and toxicity in the food preferences of lambs: implications for mimicry in plants. Oikos 88:424–432
Robbins CT (1993) Wildlife feeding and nutrition. Academic Press Inc., Orlando
Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107
Sanger GJ (2008) 5-Hydroxytryptamine and the gastrointestinal tract: where next? Trends Pharmacol Sci 29:465–471
Scrivener NJ, Johnson CN, Wallis IR, Takasaki M, Foley WJ, 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 6:77–87
Shipley LA, Sorensen JS, Moore BD (2009) Revisiting the dietary niche: When is a mammalian herbivore a specialist? Integr Comp Biol 49:274–290
Silanikove N, Shinder D, Gilboa N, Eyal M, Nitsan Z (1996) Binding of poly(ethylene glycol) to samples of forage plants as an assay of tannins and their negative effects on ruminal degradation. J Agric Food Chem 44:3230–3234
Sorensen JS, Skopec MM, Dearing MD (2006) Application of pharmacological approaches to plant–mammal interactions. J Chem Ecol 32:1229–1246
Sotka EE, Forbey J, Horn M, Poore AGB, Raubenheimer D, Whalen KE (2009) The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems. Integr Comp Biol 49:291–313
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
Tewksbury JJ, Nabhan GP (2001) Seed dispersal—directed deterrence by capsaicin in chillies. Nature 412:403–404
Tewksbury JJ, Reagan KM, Machnicki NJ, Carlo TA, Haak DC, Penaloza ALC, Levey DJ (2008) Evolutionary ecology of pungency in wild chilies. Proc Natl Acad Sci USA 105:11808–11811
Torregrossa AM, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56
Turner J, Kelly J (1981) Relationships between soil nutrients and vegetation in a north coast forest, New South Wales. Aust For Res 11:201–208
Veteli TO, Mattson WJ, Niemela P, Julkunen-Tiitto R, Kellomaki S, Kuokkanen K, Lavola A (2007) Do elevated temperature and CO2 generally have counteracting effects on phenolic phytochemistry of boreal trees? J Chem Ecol 33:287–296
Villalba JJ, Provenza FD (2000a) Discriminating among novel foods: effects of energy provision on preferences of lambs for poor-quality foods. Appl Anim Behav Sci 66:87–106
Villalba JJ, Provenza FD (2000b) Roles of novelty, generalization, and postingestive feedback in the recognition of foods by lambs. J Anim Sci 78:3060–3069
Wayne AF, Rooney JF, Ward CG, Vellios CV, Lindenmayer DB (2005a) The life history of Pseudocheirus occidentalis (Pseudocheiridae) in the jarrah forest of south-western Australia. Aust J Zool 53:325–337
Wayne AF, Ward CG, Rooney JF, Vellios CV, Lindenmayer DB (2005b) The life history of Trichosurus vulpecula hypoleucus (Phalangeridae) in the jarrah forest of south-western Australia. Aust J Zool 53:265–278
Westoby M (1978) What are the biological bases of varied diets? Am Nat 112:627–631
Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci USA 104:20427–20431
White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin
Wiggins NL, McArthur C, Davies NW, McLean S (2006) Spatial scale of the patchiness of plant poisons: A critical influence on foraging efficiency. Ecology 87:2236–2243
Williams JE, Woinarski J (1997) Eucalypt ecology: Individuals to ecosystems. Cambridge University Press, Cambridge
Wright S (1943) Isolation by distance. Genetics 28:114–138
Acknowledgments
This paper is based on a talk given at the symposium “Chemical Communication Within, Among and Around Plants” organised and sponsored by the Fondation Jean-Marie Delwart. WJF wishes to thank Monsieur Jean-Marie Delwart, Ms Raphaëlle Holender and the chair of the scientific committee, Dr Jacques Pasteels, for the invitation to speak. The research described in this paper was supported by grants from the Australian Research Council to WJF.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
DeGabriel, J.L., Moore, B.D., Marsh, K.J. et al. The effect of plant secondary metabolites on the interplay between the internal and external environments of marsupial folivores. Chemoecology 20, 97–108 (2010). https://doi.org/10.1007/s00049-009-0037-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-009-0037-3