Behavioral Strategies of Mammal Herbivores Against Plant Secondary Metabolites: The Avoidance–Tolerance Continuum

Abstract

We review the evidence for behavioral avoidance of plant secondary metabolites (PSMs) and identify how, and the circumstances under which it occurs. Behavioral strategies of avoidance of PSM can only be fully understood in relation to the underlying physiological processes or constraints. There is considerable evidence that animals learn to avoid PSMs on the basis of negative postingestive effects. The extent to which this process determines foraging choices is limited by the ability of animals to experience the consequences of their behaviors and associate particular cues in foods with their specific effects in the body. The proposed learning mechanisms require that animals must at least "sample" plants that contain PSMs. They do not completely avoid PSMs, but there is evidence that they restrict their ingestion to within limits that they are physiologically able to tolerate, and that the amounts of PSM ingested result from a balance between toxicological considerations and the nutrient content of the plant material. These limits are influenced by the kinetics of PSM elimination, which underlies patterns of bite and patch selection from plant parts to landscapes. We suggest that altering spatial location of feeding (to alternative food patches or alternative foods within patches, including plant parts), and temporal distribution of feeding activity, by either cessation of feeding or by continuing to feed, but on alternative foods, can both lead to reduction of the intake and toxic effects of PSMs. We propose that the strategy of avoidance or reduction of intake of PSMs coevolved with the animal's ability to physiologically tolerate their ingestion, and that avoidance and tolerance are inversely related (the avoidance-tolerance continuum). The animals' propensity and ability to seek alternatives also vary with the dispersion of their food resources. Further work is required to test these proposals and integrate temporal and spatial aspects of foraging behavior and its nutritional consequences in relation to PSMs.

Early experience with diverse foods increases intake of nonfamiliar flavors and feeds in sheep1,2

“…Plants vary not only in nutritional but also toxicological profi les, challenging herbivores to compose a nutritionally balanced diet but reducing negative digestive or physiological effects of plant toxins (Iason and Villalba, 2006). In our study, plant toxins affected dietary preferences and the diversity of feeds selected by lambs.…”

Woody Plant-Herbivore Interactions in Semi-Arid Savanna Ecosystems

“…Some herbivores are able to develop behavioural and physiological counter adaptations against chemical plant defences (Iason & Villalba, 2006). For example, browsers such as goats secrete tannin-binding salivary proteins which counter the digestibility-reducing effect of ingested condensed tannins (Robbins et al, 1987).…”

Vancouver Island Marmots (<em>Marmota vancouverensis</em>) Consume Plants Containing Toxic Secondary Compounds

“…126 to neutralize other toxins (Foley et al 1999;Rozman and Klaassen 2001), to enhance amino acid absorption (Iason 2005), to strengthen the immune system and/or to fight parasites (Marley et al 2003) in mammalian herbivores. The consumption of Green False Hellebore by Vancouver Island Marmots likely contributes to a coherent nutritional strategy (Foley et al 1999;Iason and Villalba 2006), and this finding has important implications for our understanding of marmot ecology and plant-herbivore interactions.…”