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 or mixtures of PSMs may play a role in determining preference of PSMs within herbivore species.

Keywords: Cottontail rabbit; Generalist; Monoterpenes; Plant secondary metabolite; Pygmy rabbit; Sagebrush; Specialist.

Fig. 1

Mean proportions (± SE) of total mass consumed by mountain cottontails (Sylvilagus nuttalli, white bars) and pygmy rabbits (Brachylagus idahoensis, grey bars) from a feeding station consisting of a diet of commercial rabbit chow containing a single monoterpene paired with a diet containing a mixture of monoterpenes. When the single monoterpene constitutes a 0.50 proportion of total food consumed, rabbits are considered to have no preference. An asterisk above bars denotes proportions consumed of the single monoterpene that were significantly different from 0.5 for each species with α = 0.05. A plus sign above sets of bars denotes a significant difference between species in the proportion consumed of the single monoterpene

Fig. 2

Mean percent difference (± SE) of single monoterpenes after 15 minutes of reaction with microsomal enzymes isolated from mountain cottontails (Sylvilagus nuttalli, white bars) and pygmy rabbits (Brachylagus idahoensis, grey bars) compared to the paired reaction at zero minutes. Rates of detoxification differed significantly between species for all five single monoterpenes. Different letters denote significantly different rates of detoxification among single monoterpenes within a single species