Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores

Abstract

Constraints on rates of detoxification and elimination of plant toxins are thought to be responsible for limiting dietary specialization in mammalian herbivores. This hypothesis, known as the detoxification limitations hypothesis, suggests that most mammalian herbivores are generalists to avoid overdosing on toxins from a single plant species. The hypothesis also predicts that the few mammalian specialists that exist should have adaptations for rapid detoxification and elimination of plant secondary compounds. We took a pharmacological approach to test whether specialists eliminate toxins from the bloodstream faster than generalists. We compared elimination rate and total exposure of alpha-pinene in closely related dietary specialist and generalist woodrats, Neotoma stephensi and N. albigula, respectively. Animals were orally gavaged with alpha-pinene, a plant secondary compound present in the natural diets of both woodrat species. We collected venous blood at 3, 6, 10, 15, and 20 min post-ingestion of alpha-pinene. Blood was analyzed for alpha-pinene concentration using gas chromatography. We found that specialist and generalist woodrats did not differ in elimination rates of alpha-pinene. However, specialists had lower exposure levels of alpha-pinene than generalists due to lower initial delivery of alpha-pinene to the general circulation. The levels of alpha-pinene detected in the bloodstream of specialists were 4.7-5.3x lower over all time intervals than generalists. Thus, specialists encounter a functionally lower dose of toxin than generalists. We suggest that the lower exposure level of specialist woodrats may be due to mechanisms in the gut that decrease toxin absorption. Regardless of mechanism, lower exposure to plant toxins may allow specialists to forage on diets with high toxin concentrations thereby facilitating dietary specialization.

Functional characterization of cytochromes P450 2B from the desert woodrat Neotoma lepida

“…Most Neotoma species consume plants with high levels of secondary compounds, which present a considerable toxic challenge to these herbivores. In response, woodrats have evolved a variety of mechanisms for dealing with these toxins including caching behaviors, efflux transporters in the gut, bacterial endosymbioses, and liver enzyme biotransformation (Sorensen and Dearing, 2003; Haley et al , 2008; Torregrossa and Dearing, 2009; Kohl and Dearing, 2012). The importance of the liver in biotransformation has been demonstrated multiple times within Neotoma , but the question remains as to how liver enzymes have adapted to the challenges of ingesting diets containing complex mixtures of potential toxins (Haley et al , 2007b; Haley et al , 2008).…”

Herbivory and Body Size: Allometries of Diet Quality and Gastrointestinal Physiology, and Implications for Herbivore Ecology and Dinosaur Gigantism

“…This actually suggests not similarity between metabolic and detoxification rates, but a trade-off between the two [40]. PSM elimination has also been associated with mechanisms not directly linked to metabolism, such as the prevention of absorption in the gut [41]. So far, a strict link between overall metabolic rate and mechanisms of toxin avoidance or detoxification has not been presented conclusively.…”

Biochemical Mechanisms for Geographical Adaptations to Novel Toxin Exposures in Butterflyfish

“…auriga may function as multipurpose detoxification enzymes of dietary chemicals. If the fish is capable of detoxifying a broad range of lipophilic compounds, this species of fish may exploit a larger range of prey as a generalist feeder [ 13 – 15 , 37 ]. Conversely, C .…”

“…This hypothesis has become firmly entrenched in the ecological literature to the extent that it is accepted as the predominant factor regulating the foraging ecology of generalist herbivores e.g. [ 13 ]. However, there have been relatively few empirical tests to confirm this hypothesis [ 13 – 15 ].…”

“…[ 13 ]. However, there have been relatively few empirical tests to confirm this hypothesis [ 13 – 15 ]. Specialists, such as Chaetodon multicinctus , consume three species of corals [ 16 ], limiting their range of available food and potentially increasing their capacity to detoxify specific toxins in high concentrations.…”