Preferences of Specialist and Generalist Mammalian Herbivores for Mixtures Versus Individual Plant Secondary Metabolites

Abstract

Herbivores that forage on chemically defended plants consume complex mixtures of plant secondary metabolites (PSMs). However, the mechanisms by which herbivores tolerate mixtures of PSMs are relatively poorly understood. As such, it remains difficult to predict how PSMs, singly or as complex mixtures, influence diet selection by herbivores. Although relative rates of detoxification of PSMs have been used to explain tolerance of PSMs by dietary specialist herbivores, few studies have used the rate of detoxification of individual PSMs to understand dietary preferences of individual herbivores for individual versus mixtures of PSMs. We coupled in vivo experiments using captive feeding trials with in vitro experiments using enzymatic detoxification assays to evaluate the dietary preferences and detoxification capacities of pygmy rabbits (Brachylagus idahoensis), dietary specialists on sagebrush (Artemisia spp.), and mountain cottontails (Sylvilagus nuttallii), dietary generalists. We compared preference for five single PSMs in sagebrush compared to a mixture containing those same five PSMs. We hypothesized that relative preference for individual PSMs would coincide with faster detoxification capacity for those PSMs by specialists and generalists. Pygmy rabbits generally showed little preference among individual PSMs compared to mixed PSMs, whereas mountain cottontails exhibited stronger preferences. Pygmy rabbits had faster detoxification capacities for all PSMs and consumed higher concentrations of individual PSMs versus a mixture than cottontails. However, detoxification capacity for an individual PSM did not generally coincide with preferences or avoidance of individual PSMs by either species. Cottontails avoided, but pygmy rabbits preferred, camphor, the PSM with the slowest detoxification rate by both species. Both species avoided β-pinene despite it having one of the fastest detoxification rate. Taken together our in vivo and in vitro results add to existing evidence that detoxification capacity is higher in dietary specialist than generalist herbivores. However, results also suggest that alternative mechanisms such as absorption and the pharmacological action of individual mixtures of PSMs may play a role in determining preference of PSMs within herbivore species.

Are there phylogenetic differences in salivary tannin‐binding proteins between browsers and grazers, and ruminants and hindgut fermenters?

“…We speculate that the oribi is at the body size threshold for being a grazing ruminant (Clauss et al., 2003; Demment & Van Soest, 1985; Gordon & Illius, 1994). Future studies should determine whether the effectiveness of the salivary proteins for binding tannins is integral to the fact that five of the six small herbivores are browsers, or whether behavioral avoidance by virtue of their small mouthparts (Iason & Villalba, 2006; Nobler et al., 2019; Provenza & Balph, 1987) can explain their abilities to access high‐value food items.…”

Unifying community detection across scales from genomes to landscapes

“…While several herbivores rely on sagebrush as forage year‐round, the volatile monoterpene features of this plant influence selection by herbivores at the species, patch and plant scale (Frye et al 2013). Although there are known concentration‐dependent consequences of individual monoterpenes, the unique mixtures of metabolites in plants may better explain intake by herbivores (Nobler et al 2019). Moreover, foraging herbivores consume mixtures of metabolites, not individual metabolites.…”

Molecular Approaches for Analyzing Organismal and Environmental Interactions

“…We argue that studying gut microbiomes has great potential to develop a more complete understanding of herbivore ecology, particularly if multiple scales are incorporated into analyses. Herbivores, such as the pygmy rabbits in our study, make foraging decisions at individual metabolite, leaf, plant, and landscape scales (Ulappa et al, 2014;Nobler et al, 2019). In turn, foraging herbivores can influence patterns of habitat structure and plant species composition (Eldridge et al, 2016).…”

“…At the individual sampling unit (plant) level, three-tip sagebrush (Artemisia tripartita) had a high probability of Community 4, whereas Wyoming big sagebrush was dominated by Communities 1 and 3 (Figure 2.4c). Concentrations of Unk 21.0 (in Community 4) and Unk 21.5 (in Community 3) predict diet selection by free-ranging sage-grouse(Fremgen-Tarantino et al 2020) and β-pinene was avoided by captive mountain cottontails (Sylvilagus nuttallii)(Nobler et al, 2019). Our results demonstrate how LDA can reveal communities of metabolite features that predict foraging decisions by herbivores.…”

“…While several herbivores rely on sagebrush as forage year-round, the volatile monoterpene features of this plant influence selection by herbivores at the species, patch and plant scale (Frye et al, 2013). Although there are known concentration-dependent consequences of individual monoterpenes, the unique mixtures of metabolites in plants may better explain intake by herbivores (Nobler et al, 2019).…”