Monoterpenes as inhibitors of digestive enzymes and counter-adaptations in a specialist avian herbivore

Abstract

Many plants produce plant secondary metabolites (PSM) that inhibit digestive enzymes of herbivores, thus limiting nutrient availability. In response, some specialist herbivores have evolved digestive enzymes that are resistant to inhibition. Monoterpenes, a class of PSMs, have not been investigated with respect to the interference of specific digestive enzymes, nor have such interactions been studied in avian herbivores. We investigated this interaction in the Greater Sage-Grouse (Phasianidae: Centrocercus urophasianus), which specializes on monoterpene-rich sagebrush species (Artemisia spp.). We first measured the monoterpene concentrations in gut contents of free-ranging sage-grouse. Next, we compared the ability of seven individual monoterpenes present in sagebrush to inhibit a protein-digesting enzyme, aminopeptidase-N. We also measured the inhibitory effects of PSM extracts from two sagebrush species. Inhibition of aminopeptidase-N in sage-grouse was compared to inhibition in chickens (Gallus gallus). We predicted that sage-grouse enzymes would retain higher activity when incubated with isolated monoterpenes or sagebrush extracts than chicken enzymes. We detected unchanged monoterpenes in the gut contents of free-ranging sage-grouse. We found that three isolated oxygenated monoterpenes (borneol, camphor, and 1,8-cineole) inhibited digestive enzymes of both bird species. Camphor and 1,8-cineole inhibited enzymes from chickens more than from sage-grouse. Extracts from both species of sagebrush had similar inhibition of chicken enzymes, but did not inhibit sage-grouse enzymes. These results suggest that specific monoterpenes may limit the protein digestibility of plant material by avian herbivores. Further, this work presents additional evidence that adaptations of digestive enzymes to plant defensive compounds may be a trait of specialist herbivores.

Metagenomic sequencing provides insights into the location of microbial detoxification in the gut of a small mammalian herbivore

“…Instead, concentrations of terpenes were lowest in the cecum, where some terpene compounds were not even detected. These results are similar to those observed in sage-grouse, where terpene concentrations are also lowest in the cecal chambers [31]. Neotoma stephensi has physiological adaptations that reduce terpene absorption in the gut [32], perhaps allowing terpene metabolism to be delayed until the food reaches the cecum.…”

Distinct microbiotas of anatomical gut regions display idiosyncratic seasonal variation in an avian folivore

“…1) in western North America [15]. Sagebrush foliage is rich in toxic monoterpenes [16][17][18][19][20][21], phenolics [20,22], and sesquiterpene lactones [23] that inhibit browsing by ungulates [24][25][26]. The greater sage-grouse feeds exclusively on evergreen sagebrush foliage in the winter and browses frequently on sagebrush during snow-free months [27].…”

The influence of plant defensive chemicals, diet composition, and winter severity on the nutritional condition of a free‐ranging, generalist herbivore

“…Many plant secondary metabolites (PSMs) deter herbivores by being toxic in one way or another (Freeland and Janzen , Provenza et al ). For example, PSMs can inhibit activity of enzymes (Forbey et al , Kohl et al ) and reduce nutrient uptake, energy budgets and reproductive output (Sorensen et al , DeGabriel et al , Au et al ). In response, herbivores have developed various physiological mechanisms to detoxify and excrete ingested PSMs (McLean and Duncan , Sorensen et al ).…”