Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-17T14:43:31.810Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of plant secondary metabolites in mammalian herbivory: ecological perspectives

Published online by Cambridge University Press:  07 March 2007

Glenn Iason
Glenn Iason
Affiliation:
Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Plant secondary metabolites (PSM) have many ecological functions, but have long been considered as defences against pathogens or herbivores (vertebrate or invertebrate), reducing the likelihood and extent of attack. However, mammalian herbivores ingest many foods containing PSM and use both behavioural methods and physiological strategies to limit their negative effects. Most physiological counter-adaptations are inducible in response to ingested PSM, providing efficient protection against toxic effects. Possible positive effects of PSM include antioxidant and anthelminthic properties and complex formation between protein and condensed tannins that protects dietary protein from degradation by the symbiotic microflora of foregut fermenters, increasing its utilisation by the animal. This protein effect is probably only beneficial to animals under a narrow range of nutrient-rich conditions found mainly in agricultural systems. There are many examples of PSM causing food avoidance or reducing food intake, but there is as yet relatively little evidence for positive selection of them by herbivores. Although the feedback mechanisms relating the post-ingestive consequences of PSM to subsequent foraging behaviour are beginning to be understood, knowledge of the integration of behavioural and physiological strategies for regulating the effects of PSM is relatively poor. The opportunities for learned avoidance of PSM may be restricted in animals with complex diets that cannot associate a particular feedback signal with a given food type. A greater emphasis on the study of subclinical effects of PSM rather than acute effects, on pharmaco-kinetic studies in relation to behavioural studies and on the use of realistic experimental models is advocated.

Keywords

Plant secondary metabolitesToxic effectsCounter-adaptationForaging behaviour
Type
Symposium on ‘Plants as animal foods: a case of catch 22?’
Information
Proceedings of the Nutrition Society , Volume 64 , Issue 1 , February 2005 , pp. 123 - 131
Copyright
Copyright © The Nutrition Society 2005

References

Alessio, HM, Hagerman, AE, Romanello, M, Carando, S, Threlkeld, MS, Rogers, J, Dimitrova, Y, Muhammed, S & Wiley, RL (2002) Consumption of green tea protects rats from exercise-induced oxidative stress in kidney and liver. Nutrition Research 22, 1177–1188 CrossRefGoogle Scholar
Appel, HM (1993) Phenolics in ecological interactions: the importance of oxidation. Journal of Chemical Ecology 7, 1521–1552 CrossRefGoogle Scholar
Athanasiadou, S & Kyriazakis, I (2004) Plant secondary metabolites: antiparasitic effects and their role in ruminant production systems. Proceedings of the Nutrition Society 63, 631–639 Google Scholar
Augner, M (1994) Should a plant always signal its defense against herbivores? Oikos 70, 322–332 CrossRefGoogle Scholar
Austin, PJ, Suchar, LA, Robbins, CT & Hagerman, AE (1989) Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. Journal of Chemical Ecology 15, 1335–1347 CrossRefGoogle ScholarPubMed
Barry, TN, Hoskin, SO & Wilson, PR (2002) Novel forages for growth and health in farmed deer. New Zealand Veterinary Journal 50, 244–251 Google Scholar
Barry, TN & Manley, TR (1984) The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 2. Quantitative digestion of carbohydrates and proteins. British Journal of Nutrition 51, 493–504 Google Scholar
Barry, TN, Manley, TR & Duncan, SJ (1986) The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 4. Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentration. British Journal of Nutrition 55, 123–137 CrossRefGoogle ScholarPubMed
Barton, RA & Whiten, A (1994) Reducing complex diets to simple rules: food selection by olive baboons. Behavioural Ecology and Sociobiology 35, 283–293 Google Scholar
Boyle, RR & Dearing, MD (2003) Ingestion of juniper foliage reduces metabolic rates in woodrat (Neotoma) herbivores. Zoology 106, 151–158 CrossRefGoogle ScholarPubMed
Boyle, RR & McLean, S (2004) Constraint of feeding by chronic ingestion of 1,8-cineole in the brushtail possum ( Trichosurus vulpecula). Journal of Chemical Ecology 30, 757–775 CrossRefGoogle ScholarPubMed
Brattsten, LB (1979) Biochemical defense mechanisms in herbivores against plant allelochemicals. In Herbivores: Their Interactions with Plant Secondary Metabolites, pp. 199–270 [Rosenthal, GA, Janzen, DH, editots]. New York: Academic Press.Google Scholar
Bryant, JP & Kuropat, PJ (1980) Selection of winter forage by subartic browsing vertebrates: the role of plant chemistry. Annual Reviews of Ecology and Systematics 11, 261–285 CrossRefGoogle Scholar
Bryant, JP, Reichardt, PB, Clausen, TP, Provenza, FD & Kuropat, PJ (1991) Woody plant-mammal interactions. In Herbivores: Their Interaction with Secondary Plant Metabolites. Vol. 2 Ecological and Evolutionary Processes, 344 – 370 [Rosenthal, GA, Berenbaum, MR, editors]. London: Academic Press.Google Scholar
Carrière, V, Chambaz, J & Rousset, M (2001) Intestinal responses to xenobiotics. Toxicology in vitro 15, 373–378 Google Scholar
Cheeke, PR (1988) Toxicity and metabolism of pyrrolizidine alkaloids. Journal of Animal Science 66, 2343–2350 CrossRefGoogle ScholarPubMed
Cheeke, PR (1994) A review of the functional and evolutionary roles of the liver in the detoxification of poisonous plants with special reference to pyrrolizidine alkaloids. Veterinary and Human Toxicology 36, 240–247 Google Scholar
Close, DC & McArthur, C (2002) Rethinking the role of many plant phenolics – protection from photodamage not herbivores? Oikos 99, 166–172 CrossRefGoogle Scholar
Cornell, HV & Hawkins, BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolutionary theory. American Naturalist 161, 507–522 CrossRefGoogle Scholar
Dearing, MD, Magnione, AM & Karasov, WH (2001) Plant secondary compounds as diuretics: an overlooked consequence. American Zoologist 41, 890–901 Google Scholar
Duncan, AJ (1991) Glucosinolates In Toxic Substances in Crop Plants pp. 124 – 147 [d' Mello, JPF, Duffus, CM and Duffus, JH, editors]. Cambridge: The Royal Society of Chemistry.Google Scholar
Duncan, AJ & Young, SA (2002) Can goats learn about foods through conditioned food aversions and preferences when multiple food options are simultaneously available? Journal of Animal Science 80, 2091–2098 Google ScholarPubMed
Duncan, P, Tixier, H, Hofman, RR & Lechner-Doll, M (1998) Feeding strategies and the physiology of digestion in roe deer. In The European Roe Deer: The Biology of Success, 91 – 116 [Andersen, R, Duncan, P and Linnell, JDC, editors]. Oslo: Scandinavian University Press Google Scholar
Earl, CRA & Smith, RH (1982) Dimethyl disulphide in the blood of cattle fed on brassicas. Journal of the Science of Food and Agriculture 34, 23–28 CrossRefGoogle Scholar
Feeney, P (1991) The evolution of chemical ecology: contributions from the study of herbivorous insects. In Herbivores: Their Interaction with Secondary Plant Metabolites. Vol. 2, Ecological and Evolutionary Processes, pp. 1–44 [Rosenthal, GA, Berenbaum, MR, editors]. London: Academic Press.Google Scholar
Feeny, PP (1976) Plant apparency and chemical defense. Recent Advances in Phytochemistry 10, 1–40 Google Scholar
Foley, WJ, Iason, GR & McArthur, C (1999) The role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years. In Nutritional Ecology of Herbivores, pp. 130–209 [Jung, H-JG, Fahey, GC, editors]. Savoy, IL: American Society of Animal Science.Google Scholar
Foley, WJ & McArthur, C (1994) The effects and costs of allelochemicals for mammalian herbivores: an ecological prospective. In The Digestive System in Mammals: Food, Form and Function, pp. 370–391 [Chivers, DJ, Langer, P, editors]. Cambridge: Cambridge University Press.Google Scholar
Foley, WJ, McLean, S & Cork, SJ (1995) Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals – a final common pathway. Journal of Chemical Ecology 21, 721–774 Google Scholar
Fraenkel, GS (1959) The raison d'etre of secondary plant substances. Science 129, 1466–1470 CrossRefGoogle ScholarPubMed
Freeland, WJ (1991) Plant secondary metabolites: biochemical coevolution with herbivores. In Plant Defenses Against Mammalian Herbivory, pp. 61–81 [Palo, RT, Robbins, CT, editors]. Boca Raton, FL: CRC Press Inc.Google Scholar
Freeland, WJ, Calcott, PH & Anderson, LR (1985a) Tannin and saponins: interaction in herbivore diets. Biochemical Systematics and Ecology 13, 189–193 Google Scholar
Freeland, WJ, Calcott, PH & Geiss, D (1985b) Allelochemicals, minerals and herbivore population size. Biochemical Systematics and Ecology 13, 195–206 Google Scholar
Freeland, WJ & Janzen, DH (1974) Strategies in herbivory by mammals: The role of plant secondary compounds. American Naturalist 108, 269–287 Google Scholar
Ginane, C, Duncan, AJ, Young, SA, Elston, DA & Gordon, IJ (2004) Herbivore diet selectivity on response to simulated variation in nutrient rewards and plant secondary metabolites concentrations of food plants Animal Behaviour Google Scholar
Goldstein, WS & Spencer, KC (1985) Inhibition of cyanogenesis by tannins. Journal of Chemical Ecology 11, 847–858 CrossRefGoogle ScholarPubMed
Guengerich, FP (1997) Comparisons of catalytic selectivity of cytochrome P450 subfamily enzymes from different species. Chemico-Biological Interactions 106, 161–182 Google Scholar
Hagerman, AE & Butler, LG (1981) The specificity of proanthocyanidin-protein interactions. Journal of Biological Chemistry 256, 4494–4497 Google Scholar
Hagerman, AE, Robbins, CT, Weerasuriya, Y, Wilson, TC & McArthur, C (1992) Tannin chemistry in relation to digestion. Journal of Range Management 45, 57–62 Google Scholar
Hatcher, PE, Moore, J, Taylor, JE, Tinney, GW & Paul, ND (2004) Phytohormones and plant–herbivore–pathogen interactions: Integrating the molecular with the ecological. Ecology 85, 59–69 Google Scholar
Herms, DA & Mattson, WJ (1992) The dilemma of plants to grow or defend. Quarterly Reviews of Biology 67, 283–335 Google Scholar
Hofmann, RR (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants – a comparative view of their digestive system. Oecologia 78, 443–457 CrossRefGoogle ScholarPubMed
Hollman, PCH & Katan, MB (1997) Absorption, metabolism and health effects of dietary flavonoids in man. Biomedicine and Pharmacotherapy 51, 305–310 CrossRefGoogle ScholarPubMed
Honkanen, T, Haukioja, E & Kitunen, V (1999) Responses of Pinus sylvestris branches to simulated herbivory are modified by tree sink/source dynamics and by external resources. Functional Ecology 13, 126–140 CrossRefGoogle Scholar
Hunter, J & Hirst, BH (1997) Intestinal secretion of drugs. The role of P-glycoprotein and related drug efflux systems in limiting oral drug absorption. Advanced Drug Delivery Reviews 25, 129–157 CrossRefGoogle Scholar
Iason, GR & Murray, AH (1996) The energy costs of ingestion of naturally occurring nontannin plant phenolics by sheep. Physiological Zoology 69, 532–546 Google Scholar
Iason, GR & Palo, RT (1991) Effects of birch phenolics on a grazing and a browsing mammal: a comparison of hares. Journal of Chemical Ecology 17, 1733–1743 Google Scholar
Illius, AW & Jessop, NS (1995) Modeling metabolic costs of allelochemical ingestion by foraging herbivores. Journal of Chemical Ecology 21, 693 CrossRefGoogle ScholarPubMed
Kahl, R (1991) Protective and adverse biological actions of phenolic antioxidants. In Oxidative Stress: Oxidants and Antioxidants, 245–273 [Sies, H, editors]. London: Academic Press.Google Scholar
Kosuge, T (1969) The role of phenolics in the host response to infection. Annual Reviews of phytopathology 7, 195–222 Google Scholar
Kyriazakis, I, Anderson, DH & Duncan, AJ (1998) Conditioned flavour aversions in sheep: the relationship between the dose rate of a secondary plant compound and the acquisition and persistence of aversions. British Journal of Nutrition 79, 55–62 CrossRefGoogle ScholarPubMed
Kyriazakis, I, Papachristou, TG, Duncan, AJ & Gordon, IJ (1997) Mild conditioned food aversions developed by sheep towards flavors associated with plant secondary compounds. Journal of Chemical Ecology 23, 727–746 Google Scholar
Lawler, IR, Foley, WJ & Eschler, BM (2000) Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81, 1327–1338 Google Scholar
McArthur, C, Hagerman, AE & Robbins, CT (1991) Physiological strategies of mammalian herbivores against plant defences. In Plant Defenses Against Mammalian Herbivory, 103–114 [Palo, RT, Robbins, CT, editors]. Boca Raton, FL: CRC Press Inc.Google Scholar
McArthur, C, Robbins, CT, Hagerman, AE & Hanley, TA (1993) Diet selection by a ruminant generalist browser in relation to plant chemistry. Canadian Journal of Zoology 71, 2236–2243 CrossRefGoogle Scholar
McArthur, C, Sanson, GD & Beal, AM (1995) Salivary proline-rich proteins in mammals: roles in oral homeostasis and counteracting dietary tannin. Journal of Chemical Ecology 21, 663–691 Google Scholar
McInnes, PF, Naiman, RJ, Pastor, J & Cohen, Y (1992) Effects of moose browsing on vegetation and litter of the boreal forest, Isle Royale, Michigan, USA. Ecology 73, 2059–2075 Google Scholar
McLean, S, Foley, WJ, Davies, NW, Brandon, S, Duo, L & Blackman, AJ (1993) The metabolic fate of dietary terpenes from Eucalyptus radiata in the common ringtail possum ( Pseudocheirus peregrinus ). Journal of Chemical Ecology 19, 1625–1643 Google Scholar
Marley, CL, Cook, R, Barrett, J, Keatlinge, R, Lampkin, NH & McBride, SD (2003) The effect of dietary forage on the development and survival of helminth parasites in ovine faeces. Veterinary Parasitology 118, 93–107 Google Scholar
Mehansho, H, Hagerman, A, Clements, S, Butler, L, Rogler, J & Carlson, DM (1983) Modulation of proline-rich protein biosynthesis in rat parotid glands by sorghums with tannin levels. Proceedings of the National Academy of Sciences USA 80, 3948–3952 Google Scholar
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. Animal Feed Science and Technology 106, 1–4 Google Scholar
Mitjavila, S, Lacombe, C, Carrera, C & Derache, R (1977) Tannic acid and oxidized tannic acid on the functional state of rat epithelium. Journal of Nutrition 107, 2113–2121 CrossRefGoogle Scholar
Mole, S, Butler, LG & Iason, G (1990) Defense against dietary tannin in herbivores: a survey for proline rich salivary proteins in mammals. Biochemical Systematics and Ecology 18, 287–293 Google Scholar
Mole, S & Waterman, PG (1985) Stimulatory effects of tannins and cholic acid on tryptic hydrolysis of proteins: ecological implications. Journal of Chemical Ecology 11, 1323–1332 Google Scholar
Murray, AH, Iason, GR & Stewart, C (1996) Effect of simple phenolic compounds of heather ( Calluna vulgaris ) on rumen microbial activity in vitro. Journal of Chemical Ecology 22, 1493–1504 Google Scholar
Odenyo, AA & Osuji, PO (1998) Tannin-tolerant ruminal bacteria from East African ruminants. Canadian Journal of Microbiology 44, 904–909 Google Scholar
Osawa, R & Sly, LI (1992) Occurrence of tannin-protein complex degrading Streptococcus species in feces of various animals. Systematic and Applied Microbiology 15, 144–147 CrossRefGoogle Scholar
Palo, RT (1987) Chemical defenses in a woody plant and the role of digestive systems of herbivores. In Proceedings of the Symposium on Plant-Herbivore Interactions. USDA Forest Service Intermountain Research Station General Technical Report INT-222, pp. 103–107 [Provenza, FD, Flinders, JT, McArthur, ED, editors]. Ogden, UT: USDA Forest Service Intermountain Region.Google Scholar
(1991) Plant Defenses Against Mammalian Herbivory Palo RT Robbins CT Boca Raton, FL CRC PressGoogle Scholar
Panter, KE, Keeler, RF & Baker, DC (1988) Toxicoses in livestock from the hemlocks ( Conium and Cicuta spp.). Journal of Animal Science 66, 2407–2413 Google Scholar
Pass, GJ, McLean, S, Stupans, I & Davies, N (2001) Microsomal metabolism of the terpene 1,8-cineole in the common brushtail possum ( Trichosurus vulpecula ), koala ( Phascolarctos cinereus ), rat and human. Xenobiotica 31, 205–221 Google Scholar
Pass, GJ, McLean, S, Stupans, I & Davies, N (2002) Microsomal metabolism and enzyme kinetics of the terpene p -cymene in the common brushtail possum ( Trichosurus vulpecula ), koala ( Phascolarctos cinereus ) and rat. Xenobiotica 32, 383–397 Google Scholar
Pastor, J & Naiman, RJ (1992) Selective foraging and ecosystem processes in boreal forests. American Naturalist 139, 690–705 Google Scholar
Pehrson, A (1983) Digestibility and retention of food components in caged mountain hares Lepus timidus during the winter. Holarctic Ecology 6, 395–403 Google Scholar
Pfister, JA, Provenza, FD, Manners, GD, Gardner, DR & Ralphs, MH (1997) Tall larkspur ingestion, can cattle regulate intake below toxic levels. Journal of Chemical Ecology 23, 759–777 Google Scholar
Powell, GM, Miller, JJ, Olavesen, AH & Curtis, CG (1974) Liver as a major organ of phenol detoxication. Nature 252, 234–235 Google Scholar
Provenza, FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. Journal of Range Management 48, 2–17 Google Scholar
Provenza, FD (1996) Acquired aversions as the basis for varied diets of foraging ruminants on rangelands. Journal of Animal Science 74, 2010–2020 Google Scholar
Provenza, FD, Villalba, JJ & Bryant, JP (2002) Foraging by herbivores: linking the biochemical diversity of plants to herbivore culture and landscape diversity. In Landscape Ecology and Resource Management: Linking Theory with Practice, 387–421 [Bissonette, JA, Storch, I, editors]. New York: Island Press.Google Scholar
Reichardt, PB, Bryant, JP, Clausen, TP & Wieland, GD (1984) Defense of winter-dominant Alaska paper birch against snowshoe hares. Oecologia 65, 58–69 Google Scholar
Reichardt, PB, Bryant, JP, Mattes, BR, Clausen, TP, Chapin, FS & Meyer, M (1990) Winter chemical defense of Alaskan balsam poplar against snowshoe hares. Journal of Chemical Ecology 16, 1941–1959 Google Scholar
Rhoades, DF & Cates, RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry 10, 168–213 Google Scholar
Robbins, CT, Hagerman, AE, Austin, PJ, McArthur, C & Hanley, TA (1991) Variation in mammalian physiological responses to a condensed tannin and its ecological implications. Journal of Mammalogy 72, 480–486 Google Scholar
Rosenthal, GA & Berenbaum, MR (editors) (1991) Herbivores: Their Interaction with Secondary Plant Metabolites. Vol. 2, Ecological and Evolutionary Processes Rosenthal GA Berenbaum MR London Academic PressGoogle Scholar
Rozman, KK & Klaassen, CD (2001) Absorption, distribution, and excretion of toxicants. In Casarett and Doull's Toxicology: The Basic Science of Poisons, pp. 107–132 [Klaassen, CD, editor] New York: McGraw-Hill.Google Scholar
Ryan, CA (1979) Proteinase inhibitors. In Herbivores: Their Interaction with Plant Secondary Metabolites, pp. 599–618 [Rosenthal, GA, Janzen, DH, editors]. New York:Academic Press.Google Scholar
Scheline, RR (1991) Handbook of Mammalian Metabolism of Plant Compounds, Boca Raton, FL: CRC Press.Google Scholar
Singleton, VI (1981) Naturally occurring food toxicants: phenolic substances of plant origin in common foods. Advances in Food Research 27, 149–242 CrossRefGoogle Scholar
Singleton, VI & Kratzer, FH (1969) Toxicity and related physiological activity of phenolic substances of plant origin. Journal of Agricultural and Food Chemistry 17, 497–512 Google Scholar
Smith, GS (1992) Toxification and detoxification of plant compounds by ruminants: an overview. Journal of Range Management 45, 25–30 Google Scholar
Smith, GS & Watkins, JB (1984) Biotransformations of xenobiotics in tissues of cattle and sheep. Canadian Journal of Animal Science 64, 278–280 Suppl.CrossRefGoogle Scholar
Sorensen, JS & Dearing, MD (2003) Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores. Oecologia 134, 88–94 Google Scholar
Stapley, J, Foley, WJ, Cunningham, R & Eschler, B (2000) How well can common brushtail possums regulate their intake of Eucalyptus toxins. Journal of Comparative Physiology 170, 211–218 Google Scholar
Stephens, DW & Krebs, JR (1986) Foraging Theory 247 Princeton, NJ Princeton University PressGoogle Scholar
Thomas, DW, Samson, C & Bergeron, JM (1988) Metabolic costs associated with the ingestion of plant phenolics by Microtus pennsylvanicus. Journal of Mammalogy 69, 512–515 CrossRefGoogle Scholar
Tixier, H, Duncan, P, Scehovic, P, Yani, J, Gleizes, M & Lila, M (1997) Food selection by European roe deer ( Capreolus capreolus ): Effects of plant chemistry and consequences for the nutritional value of their diets. Journal of Zoology 242, 229–245 Google Scholar
van Dam, NM, Harvey, JA, Wäckers, FL, Bezemer, TM, van der, Putten, WH, Vet LEM (2003) Interactions between aboveground phytophages and belowground induced responses against phytophages. Basic and Applied Ecology 4, 63–77 Google Scholar
Van Soest, PJ (1982) Nutritional Ecology of the Ruminant Corvallis, OR O & B BooksGoogle Scholar
Verheyden-Tixier, H & Duncan, P (2000) Selection for small amounts of hydrolysable tannins by a concentrate-selecting mammalian herbivore. Journal of Chemical Ecology 26, 351–358 Google Scholar
Villalba, JJ, Provenza, FD & Bryant, JP (2002) Consequences of the interaction between nutrients and plant secondary metabolites on herbivore selectivity: benefits or detriment for plants. Oikos 97, 282–292 Google Scholar
Villalba, JJ, Provenza, FD, Guo-Dong, Han (2004) Experience influences diet mixing by herbivores: implications for plant biochemical diversity Oikos Google Scholar
Wallace, RJ (2004) Antimicrobial properties of plant secondary metabolites. Proceedings of the Nutrition Society 63, 621–629 Google Scholar
Watkins, JB, Smith, GS & Hallford, DM (1987) Characterization of xenobiotic biotransformation in hepatic, renal and gut tissues of cattle and sheep. Journal of Animal Science 65, 186–195 Google Scholar
Whiten, A, Bryce, RW, Barton, RA, Waterman, PG & Heinzi, SP (1991) Dietary and foraging strategies of baboons. Philosophical Transactions of the Royal Society (London) 334, 187–197 Google Scholar
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. Journal of Chemical Ecology 29, 1447–1464 Google Scholar