Troublesome toxins: time to re-think plant-herbivore interactions in vertebrate ecology
© Swihart et al; licensee BioMed Central Ltd. 2009
Received: 22 October 2008
Accepted: 24 February 2009
Published: 24 February 2009
Earlier models of plant-herbivore interactions relied on forms of functional response that related rates of ingestion by herbivores to mechanical or physical attributes such as bite size and rate. These models fail to predict a growing number of findings that implicate chemical toxins as important determinants of plant-herbivore dynamics. Specifically, considerable evidence suggests that toxins set upper limits on food intake for many species of herbivorous vertebrates. Herbivores feeding on toxin-containing plants must avoid saturating their detoxification systems, which often occurs before ingestion rates are limited by mechanical handling of food items. In light of the importance of plant toxins, a new approach is needed to link herbivores to their food base. We discuss necessary features of such an approach, note recent advances in herbivore functional response models that incorporate effects of plant toxins, and mention predictions that are consistent with observations in natural systems. Future ecological studies will need to address explicitly the importance of plant toxins in shaping plant and herbivore communities.
The importance of plant-herbivore interactions
By definition herbivores depend on plants to survive. The need to obtain suitable food in sufficient amounts drives innumerable herbivore behaviors; for example, movement decisions often are related to the distribution and abundance of plant resources . By the same token, herbivores can exert strong effects on plant growth, survival, and population size by virtue of their feeding habits. Plant demographic effects are especially severe during cyclical peaks or irruptions in herbivore populations [2, 3]. Moreover, the ecological effects of herbivores can extend beyond populations. Differential foraging among species can affect outcomes of competition, facilitate invasion of extant communities, and alter patterns of plant succession, diversity, and dominance [4–6].
Conventional modeling approaches
When focusing on optimal diet choice by herbivores, ecologists traditionally have relied on linear programming or linear dynamic programming methods [7, 8]. Given a choice of two or more non-equivalent food types, these methods solve for optimal diet composition subject to constraints imposed by daily energy requirements, feeding time, digestive capacity, or nutrient requirements. Linear programming appears to provide reasonable predictions of diet composition for many species . However, it does not address population-level dynamics of herbivores and plants.
Consumer-resource interactions at the population level can be modeled using equations that relate the rate of resource intake by a consumer to resource abundance . These so-called "functional-response" models link herbivore behavior and plant characteristics to population- and community-level consequences. In these models, upper limits to rates of consumption by herbivores are determined, either implicitly or analytically, by combining mechanical factors such as bite size and rate with plant quantity [11–13].
Ignore plant toxins
A problem with conventional plant-herbivore models is their failure to incorporate factors related to plant quality into decelerating functional responses. For many herbivores, plant toxicity plays an important role in diet choice [14, 15]. Indeed, plants in both tropical and temperate systems appear to have evolved a variety of chemical defenses, many of which are unique to particular plant species . For instance, many Australian Eucalyptus trees produce 1,8-cineole, a monoterpene that serves as a potent deterrent to herbivorous marsupials such as brushtail possum, Trichosurus vulpecula . Creosote bush (Larrea tridentata) in the western United States produces phenolic resins containing nordihydroguaiaretic acid, which limits intake by desert woodrats, Neotoma lepida . Tree birches (Betula) in boreal North America produce the triterpene papyriferic acid as a deterrent to feeding by snowshoe hares, Lepus americanus . Although most work on chemical defenses against vertebrate herbivores has involved mammals , plant toxins also influence herbivorous birds. For instance, aspen (Populus tremuloides) produces coniferyl benzoate, a phenylpropanoid ester that inhibits feeding by ruffed grouse, Bonasa umbellus .
In addition to interspecific differences, production of toxins varies ontogenetically within plants, and among individuals and populations within species. Intraspecific variation in chemical defense often contains strong genetic components [21–23]. When combined with spatial variation in environmental conditions and herbivory, substantial geographic variation in defense can occur within species [24, 25]. Ontogenetic variation in defensive responses of many plants is shaped by constraints on resource allocation and sensitivity to fitness consequences of herbivory . For instance, winter browsing of plants by mammals has severe repercussions for fitness during the juvenile stage and was linked to greater defense of juveniles in a review of 37 woody species .
And coping strategies of herbivores
One consequence of feeding on plants containing toxins is that rates of ingestion may be limited by an herbivore's ability to avoid toxins or detoxify food rather than to mechanically process food. Not surprisingly, herbivores have developed a host of physiological and behavioral mechanisms to deal with plant secondary metabolites . Physiologically, vertebrates can regulate absorption of plant toxins by gut cells, respond to chemically mediated taste and trigeminal stimulation, and detoxify lipophilic compounds via enzymatic biotransformation . For instance, marsupial folivores oxidize plant terpenes using P450 enzymes, and species with diets high in monoterpenes exhibit greater capacity for biotransformation of toxins than their generalist counterparts . Behaviorally, vertebrates can select plants or plant parts containing low concentrations of a toxin , manage food to leach toxins from plants [31, 32], self-medicate to ameliorate effects of toxins , and adjust meal duration and intake per meal [34, 35]. An ability to regulate intake of plant secondary metabolites has been reported for several species of vertebrate herbivores [17, 34, 36]. For instance, brushtail possums ate more of the toxin benzoate when the rate at which it could be detoxified by conjugation was increased by adding glycine to the diet . Herbivores also achieve greater intake of nutrients by selecting mixed diets containing foods processed by different detoxification pathways, thereby avoiding saturation of any particular pathway [38, 39]. Regardless of the strategies used by herbivores, costs of detoxification often are high. For desert woodrats subsisting on a diet containing a toxin-rich juniper (Juniperus monosperma), detoxification costs are comparable to energy needed for reproduction . For ruffed grouse feeding on aspen, 10 percent of metabolizable energy is lost each day in biotransformation conjugates; additional losses of energy in the conjugation process and of nitrogen due to excretion of amino acid conjugates elevate the cost further . In the face of such costs, vertebrate herbivores face life-history tradeoffs associated with allocation of resources to growth and reproduction .
Needed: A toxin-determined functional response
So in (2), the presence of toxin simply results in an effective increase in the handling time that is proportional to 1/G.
N1 and N2 represent the concentrations of nutrients limiting plant growth, Cmax is the maximum possible rate of nutrient-limited plant growth, and K1 and K2 are constants reflecting the stoichiometry of the two nutrients in the plant. Note that in the limiting case, as N1/N2 approaches zero, (3) reduces to the traditional Michaelis-Menten equation for N1, with K1 as a half-saturation coefficient . More importantly from our perspective, increasing availability of the co-limiting nutrient, N2, causes growth rate to increase in (3), whereas in (2) an increasing concentration of toxin in food relative to the rate of toxin ingestion the herbivore can tolerate, 1/G, decreases growth rate. In both equations, this change in C is due to a change in size of the third term in the denominator.
The toxin-determined functional response (1) differs from plant-nutrient models (3) because toxins can do more than reduce feeding rate. Specifically, when 1/G is large (and hence each gram of plant is quite toxic to herbivores), the functional response can represent a more serious deterioration of the herbivore's ability to feed or survive. Analysis has demonstrated the critical importance of σ to herbivore dynamics; in the presence of a toxin, selection should act strongly to regulate intake below the herbivore's detoxification threshold .
Evidence for the importance of plant toxins as determinants of herbivore functional response is indisputable. Recent modeling efforts implicate toxins as potentially key drivers of change in plant communities and herbivore populations. Future models should consider the role of resource patchiness and tri-trophic interactions on plant communities. For instance, adaptive foraging by herbivores is hypothesized to have important effects on ecosystem processes such as nutrient cycling rates, and predators may alter herbivore effects by changing their density or behavior . How do tradeoffs from toxin-induced resource patchiness and risk of predation influence ecosystem properties? From the perspective of evolutionary ecology, models of tradeoffs in plant growth and defense  as well as spatio-temporal variation in selection for toxin production  may afford greater insight into genetic diversity and geographic structuring of plant populations. At the very least, ecologists conducting work in the future should address explicitly the importance of plant toxins as potential agents of change for plant and herbivore communities.
N. I. Lichti and members of the BMC editorial board provided helpful comments on the manuscript. The ideas presented here were supported in part by National Science Foundation grant DMS-0719697 (Z. Feng), the James S. McDonnell Foundation 21st Century Science Initiative (Z. Feng and R. K. Swihart), and the USGS – Florida Integrated Science Center (D. L. DeAngelis).
- Ares JO, Dignani J, Bertiller MB: Cost analysis of remotely sensed foraging paths in patchy landscapes with plant anti-herbivore defences (Patagonia, Argentina). Landscape Ecol. 2007, 22: 1291-1301.View ArticleGoogle Scholar
- Wolff JO: The role of habitat patchiness in the population dynamics of snowshoe hares. Ecol Monogr. 1980, 50: 111-130.View ArticleGoogle Scholar
- Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM: Ecological impacts of deer overabundance. Ann Rev Ecol Evol Syst. 2004, 35: 113-147.View ArticleGoogle Scholar
- Harper JL: Population Biology of Plants. 1977, London: Academic PressGoogle Scholar
- Crawley MJ: Herbivory. The Dynamics of Animal-Plant Interactions. 1983, Oxford: Blackwell ScientificGoogle Scholar
- Long ZT, Pendergast , TH IV, Carson WP: The impact of deer on relationships between tree growth and mortality in an old-growth beech-maple forest. Forest Ecol Mgt. 2007, 252: 230-238.View ArticleGoogle Scholar
- Belovsky GE: Herbivore optimal foraging: A comparative test of three models. Amer Naturalist. 1984, 124: 97-115.View ArticleGoogle Scholar
- Mangel M, Clark CW: Dynamic Modeling in Behavioral Ecology. 1988, Princeton U. PressGoogle Scholar
- Belovsky GE: How good must models and data be in ecology?. Oecologia. 1994, 100: 475-480.View ArticleGoogle Scholar
- Holling CS: The components of predation as revealed by a study of small mammal predation on the European pine sawfly. Canadian Entomol. 1959, 91: 293-320.View ArticleGoogle Scholar
- Lundberg P: Functional response of a small mammalian herbivore: The disc equation revisited. J Anim Ecol. 1988, 57: 999-1006.View ArticleGoogle Scholar
- Hobbs NT, Gross JE, Shipley LA, Spalinger DE, Wunder BA: Herbivore functional response in heterogeneous environments: A contest among models. Ecology. 2003, 84: 666-681.View ArticleGoogle Scholar
- Owen-Smith N: Adaptive Herbivore Ecology: From Resources to Populations in Variable Environments. 2002, Cambridge U. PressView ArticleGoogle Scholar
- Dearing MD, Foley WJ, McLean S: The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Ann Rev Ecol Evol Syst. 2005, 36: 169-189.View ArticleGoogle Scholar
- Belovsky GE, Schmitz OJ: Plant defenses and optimal foraging by mammalian herbivores. J Mammalogy. 1994, 75: 816-832.View ArticleGoogle Scholar
- Stamp N: Out of the quagmire of plant defense hypotheses. Quart Rev Biol. 2003, 78: 23-55.View ArticlePubMedGoogle Scholar
- Boyle RR, McLean S, Brandon S, Wiggins N: Rapid absorption of dietary 1,8-cineole results in critical blood concentration of cineole and immediate cessation of eating in the common brushtail possum (Trichosurus vulpecula). J Chem Ecol. 2005, 31: 2775-2789.View ArticlePubMedGoogle Scholar
- Mangione AM, Dearing MD, Karasov WH: Detoxification in relation to toxin tolerance in desert woodrats eating creosote bush. J Chem Ecol. 2001, 27: 2559-2578.View ArticlePubMedGoogle Scholar
- Reichardt PB, Bryant JP, Clausen TP, Wieland GD: Defense of winter-dormant Alaska paper birch against snowshoe hare. Oecologia. 1984, 65: 58-69.View ArticleGoogle Scholar
- Jakubas WJ, Gullion GW: Coniferyl benzoate in quaking aspen-a ruffed grouse feeding deterrent. J Chem Ecol. 1990, 16: 1077-1087.View ArticlePubMedGoogle Scholar
- Silen RR, Randall WK, Mandel NL: Estimates of genetic parameters for deer browsing of Douglas fir. For Sci. 1986, 32: 178-184.Google Scholar
- Laitinen J, Julkenen-Tiitto R, Rousi M, Heinonen J, Tahvanainen J: Ontogeny and environment as determinants of the secondary chemistry of three species of white birch. J Chem Ecol. 2005, 31: 2243-2262.View ArticlePubMedGoogle Scholar
- Andrew RL, Wallis IR, Harwood CE, Henson M, Foley WJ: Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia. 2007, 153: 891-901.View ArticlePubMedGoogle Scholar
- Swihart RK, Bryant JP, Newton L: Latitudinal patterns in consumption of woody plants by snowshoe hares in the eastern United States. Oikos. 1994, 70: 427-434.View ArticleGoogle Scholar
- Andrew RL, Peakall R, Wallis IR, Foley WJ: Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology. 2007, 88: 716-728.View ArticlePubMedGoogle Scholar
- Boege K, Marquis RJ: Facing herbivory as you grow up: The ontogeny of resistance in plants. Trends Ecol Evol. 2005, 20: 441-448.View ArticlePubMedGoogle Scholar
- Swihart RK, Bryant JP: Winter herbivory by mammals: The importance of biogeography and ontogeny of woody plants. J Mammalogy. 2001, 82: 1-21.View ArticleGoogle Scholar
- Karban R, Agrawal AA: Herbivore offense. Ann Rev Ecol Syst. 2002, 33: 641-664.View ArticleGoogle Scholar
- Boyle R, McLean S, Foley WJ, Davies NW: Comparative metabolism of dietary terpene, p-cymene, in generalist and specialist folivorous marsupials. J Chem Ecol. 1999, 25: 2109-2126.View ArticleGoogle Scholar
- Bryant JP, Kuropat P: Subarctic browsing vertebrate winter forage selection: The role of plant chemistry. Ann Rev Ecol Syst. 1980, 11: 261-285.View ArticleGoogle Scholar
- Dearing MD: Effects of Acomastylis rossii tannins on a mammalian herbivore, the North American pika, Ochotona princeps. Oecologia. 1997, 109: 122-131.View ArticleGoogle Scholar
- Muller-Schwarze D, Brashear H, Kinnel R, Hintz KA, Lioubomirov A, Skibo C: Food processing by animals: Do beavers leach tree bark to improve palatability?. J Chem Ecol. 2001, 27: 1011-1028.View ArticlePubMedGoogle Scholar
- Villalba JJ, Provenza FD, Shaw R: Sheep self-medicate when challenged with illness-inducing foods. Anim Behav. 2006, 71: 1131-1139.View ArticleGoogle Scholar
- Sorensen JS, Heward E, Dearing MD: Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida). Oecologia. 146: 415-422.
- Marsh KJ, Wallis IR, Foley WJ: Behavioural contributions to the regulated intake of plant secondary metabolites in koalas. Oecologia. 2007, 154: 283-290.View ArticlePubMedGoogle Scholar
- Jakubas WJ, Karasov WH, Guglielmo CG: Ruffed grouse tolerance and biotransformation of the plant secondary metabolite coniferyl benzoate. Condor. 1993, 95: 625-640.View ArticleGoogle Scholar
- Marsh KJ, Wallis IR, Foley WJ: Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology. 2005, 86: 2946-2954.View ArticleGoogle Scholar
- Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ: Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology. 2006, 87: 2103-2112.View ArticlePubMedGoogle Scholar
- Provenza FD, Villalba JJ, Haskell J, MacAdam JW, Griggs TC, Weidmeier RD: The value to herbivores of plant physical and chemical diversity in time and space. Crop Sci. 2007, 47: 382-398.View ArticleGoogle Scholar
- Sorensen JS, McLister JD, Dearing MD: Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology. 2005, 86: 125-139.View ArticleGoogle Scholar
- Simard MA, Côté SD, Weladji RB, Huot J: Feedback effects of chronic browsing on life-history traits of a large herbivore. J Anim Ecol. 2008, 77: 678-686.View ArticleGoogle Scholar
- Li Y, Feng Z, Swihart R, Bryant J, Huntly N: Modeling the impact of plant toxicity on plant-herbivore dynamics. J Dynamics and Diff Equations. 2006, 18: 1021-1024.View ArticleGoogle Scholar
- Feng Z, Liu R, DeAngelis DL: Plant-herbivore interactions mediated by plant toxicity. Theor Popul Biol. 2007, 73: 449-459.View ArticlePubMedGoogle Scholar
- Liu R, Feng Z, Zhu H, DeAngelis DL: Bifurcation analysis of a plant herbivore model with toxin-determined functional response. J Diff Equations. 2008, 245: 442-467.View ArticleGoogle Scholar
- Tilman D: Resource Competition and Community Structure. 1982, Princeton U. PressGoogle Scholar
- O'Neill RV, DeAngelis DL, Pastor JJ, Post WM: Multiple nutrient limitations in ecological models. Ecol Modelling. 1988, 46: 147-163.View ArticleGoogle Scholar
- Hsu SB, Hubbell SP, Waltman P: A contribution to the theory of competing predators. Ecol Monogr. 1978, 48: 337-349.View ArticleGoogle Scholar
- Feng Z, Liu R, DeAngelis DL, Bryant JP, Kielland K, Chapin FS, Swihart RK: Plant toxicity, adaptive herbivory, and plant community dynamics. Ecosystems. 2009Google Scholar
- Bergvall UA, Rautio P, Kesti K, Tuomi J, Leimar O: Associational effects of plant defences in relation to within- and between-patch food choice by a mammalian herbivore: neighbour contrast susceptibility and defence. Oecologia. 2006, 147: 253-260.View ArticleGoogle Scholar
- Miller AM, McArthur C, Smethers PJ: Effects of within-patch characteristics on the vulnerability of a plant to herbivory. Oikos. 2007, 116: 41-52.View ArticleGoogle Scholar
- Kielland K, Bryant JP: Moose herbivory in taiga: Effects on biogeochemistry and vegetation dynamics in primary succession. Oikos. 1998, 82: 377-383.View ArticleGoogle Scholar
- Butler LG, Kielland K: Acceleration of vegetation turnover and element cycling by mammalian herbivory in riparian ecosystems. J Ecol. 2008, 96: 136-144.Google Scholar
- Pastor J, Naiman RJ: Selective foraging and ecosystem processes in boreal forests. Amer Naturalist. 1992, 139: 690-705.View ArticleGoogle Scholar
- Clay K, Holah J, Rudgers JA: Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci USA. 2005, 102: 12465-12470.PubMed CentralView ArticlePubMedGoogle Scholar
- Kent A, Jensen SP, Doncaster CP: Model of microtine cycles caused by lethal toxins in non-preferred food plants. J Theor Biol. 2005, 234 (4): 593-604.View ArticlePubMedGoogle Scholar
- Schmitz OJ, Grabowski JH, Peckarsky BL, Preisser EL, Trussell GC, Vonesh JR: From individuals to ecosystem function: Toward an integration of evolutionary and ecosystem ecology. Ecology. 2008, 89: 2436-2445.View ArticlePubMedGoogle Scholar
- Bryant JP, Clausen TP, Swihart RK, Landhäusser SM, Hawkins CDB, Stevens MT, Carrière S, Kirilenko AP, Veitch AM, Popko RA, Cleland DT, Williams JH, Jakubas WJ, Carlson MR, Lemkhul Bodony KL, Cebrian M, Paragi TF, Picone PM, Moore JE, Packee EC, Malone TT: Fire drives transcontinental variation in tree birch defense against browsing by snowshoe hares. Amer Naturalist. 2009Google Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.