Jennifer S. Forbey

Phytochemistry Predicts Habitat Selection by an Avian Herbivore at Multiple Spatial Scales

Animal habitat selection is a process that functions at multiple, hierarchically. structured spatial scales. Thus multi-scale analyses should be the basis for inferences about factors driving the habitat selection process. Vertebrate herbivores forage selectively on the basis of phytochemistry, but few studies have investigated the influence of selective foraging (i.e., fine-scale habitat selection) on habitat selection at larger scales. We tested the hypothesis that phytochemistry is integral to the habitat selection process for vertebrate herbivores. We predicted that habitats selected at three spatial scales would be characterized by higher nutrient concentrations and lower concentrations of plant secondary metabolites (PSMs) than unused habitats. We used the Greater Sage-Grouse (Centrocercus urophasianus), an avian herbivore with a seasonally specialized diet of sagebrush, to test our hypothesis. Sage-Grouse selected a habitat type (black sagebrush, Artemisia nova) with lower PSM concentrations than the alternative (Wyoming big sagebrush, A. tridentata wyomingensis). Within black sagebrush habitat, Sage-Grouse selected patches and individual plants within those patches that were higher in nutrient concentrations and lower in PSM concentrations than those not used. Our results provide the first evidence for multi-scale habitat selection by an avian herbivore on the basis of phytochemistry, and they suggest that phytochemistry may be a fundamental driver of habitat selection for vertebrate herbivores.

The dilemma of foraging herbivores: dealing with food and fear

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant–herbivore and predator–prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.

Ambient Temperature Influences Diet Selection and Physiology of an Herbivorous Mammal, Neotoma albigula

The whitethroat woodrat (Neotoma albigula) eats juniper (Juniperus monosperma), but the amount of juniper in its diet varies seasonally. We tested whether changes in juniper consumption are due to changes in ambient temperature and what the physiological consequences of consuming plant secondary compounds (PSCs) at different ambient temperatures might be. Woodrats were acclimated to either 20°C or 28°C. Later, they were given two diets to choose from (50% juniper and a nontoxic control) for 7 d. Food intake, resting metabolic rate (RMR), and body temperature (Tb) were measured over the last 2 d. Woodrats at 28°C ate significantly less juniper, both proportionally and absolutely, than woodrats at 20°C. RMRs were higher for woodrats consuming juniper regardless of ambient temperature, and Tb was higher for woodrats consuming juniper at 28°C than for woodrats eating control diet at 28°C. Thus, juniper consumption by N. albigula is influenced by ambient temperature. We conclude that juniper may influence thermoregulation in N. albigula in ways that are helpful at low temperatures but harmful at warmer temperatures in that juniper PSCs may be more toxic at warmer temperatures. The results suggest that increases in ambient temperature associated with climate change could significantly influence foraging behavior of mammalian herbivores.

Plant protein and secondary metabolites influence diet selection in a mammalian specialist herbivore

Abstract For herbivores, nutrient intake is limited by the relatively low nutritional quality of plants and high concentrations of potentially toxic defensive compounds (plant secondary metabolites [PSMs]) produced by many plants. In response to phytochemical challenges, some herbivores selectively forage on plants with higher nutrient and lower PSM concentrations relative to other plants. Pygmy rabbits (Brachylagus idahoensis) are dietary specialists that feed on sagebrush (Artemisia spp.) and forage on specific plants more than others within a foraging patch. We predicted that the plants with evidence of heavy foraging (browsed plants) would be of higher dietary quality than plants that were not browsed (unbrowsed). We used model selection to determine which phytochemical variables best explained the difference between browsed and unbrowsed plants. Higher crude protein increased the odds that plants would be browsed by pygmy rabbits and the opposite was the case for certain PSMs. Additionally, because pygmy rabbits can occupy foraging patches (burrows) for consecutive years, their browsing may influence the nutritional and PSM constituents of plants at the burrows. In a post hoc analysis, we did not find a significant relationship between phytochemical concentrations, browse status, and burrow occupancy length. We concluded that pygmy rabbits use nutritional and chemical cues while making foraging decisions.

A Pharm-Ecological Perspective of Terrestrial and Aquatic Plant-Herbivore Interactions

We describe some recent themes in the nutritional and chemical ecology of herbivores and the importance of a broad pharmacological view of plant nutrients and chemical defenses that we integrate as “Pharm-ecology”. The central role that dose, concentration, and response to plant components (nutrients and secondary metabolites) play in herbivore foraging behavior argues for broader application of approaches derived from pharmacology to both terrestrial and aquatic plant-herbivore systems. We describe how concepts of pharmacokinetics and pharmacodynamics are used to better understand the foraging phenotype of herbivores relative to nutrient and secondary metabolites in food. Implementing these concepts into the field remains a challenge, but new modeling approaches that emphasize tradeoffs and the properties of individual animals show promise. Throughout, we highlight similarities and differences between the historic and future applications of pharm-ecological concepts in understanding the ecology and evolution of terrestrial and aquatic interactions between herbivores and plants. We offer several pharm-ecology related questions and hypotheses that could strengthen our understanding of the nutritional and chemical factors that modulate foraging behavior of herbivores across terrestrial and aquatic systems.

Inhibition of Snowshoe Hare Succinate Dehydrogenase Activity as a Mechanism of Deterrence for Papyriferic Acid in Birch

The plant secondary metabolite papyriferic acid (PA) deters browsing by snowshoe hares (Lepus americanus) on the juvenile developmental stage of the Alaska paper birch (Betula neoalaskana). However, the physiological mechanism that reduces browsing remains unknown. We used pharmacological assays and molecular modeling to test the hypothesis that inhibition of succinate dehydrogenase (SDH) is a mode of action (MOA) of toxicity of PA in snowshoe hares. We tested this hypothesis by measuring the effect of PA on the activity of SDH in liver mitochondria isolated from wild hares. In addition, we used molecular modeling to determine the specific binding site of PA on SDH. We found that PA inhibits SDH from hares by an uncompetitive mechanism in a dose-dependent manner. Molecular modeling suggests that inhibition of SDH is a result of binding of PA at the ubiquinone binding sites in complex II. Our results provide a MOA for toxicity that may be responsible for the concentration-dependent anti-feedant effects of PA. We propose that snowshoe hares reduce the dose-dependent toxic consequences of PA by relying on efflux transporters and metabolizing enzymes that lower systemic exposure to dietary PA.

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

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.

Modeling Trade-Offs Between Plant Fiber and Toxins: A Framework for Quantifying Risks Perceived by Foraging Herbivores

When selecting habitats, herbivores must weigh multiple risks, such as predation, starvation, toxicity, and thermal stress, forcing them to make fitness trade-offs. Here, we applied the method of paired comparisons (PC) to investigate how herbivores make trade-offs between habitat features that influence selection of food patches. The method of PC measures utility and the inverse of utility, relative risk, and makes trade-offs and indifferences explicit by forcing animals to make choices between two patches with different types of risks. Using a series of paired-choice experiments to titrate the equivalence curve and find the marginal rate of substitution for one risk over the other, we evaluated how toxin-tolerant (pygmy rabbit Brachylagus idahoensis) and fiber-tolerant (mountain cottontail rabbit Sylviagus nuttallii) herbivores differed in their hypothesized perceived risk of fiber and toxins in food. Pygmy rabbits were willing to consume nearly five times more of the toxin 1,8-cineole in their diets to avoid consuming higher levels of fiber than were mountain cottontails. Fiber posed a greater relative risk for pygmy rabbits than cottontails and cineole a greater risk for cottontails than pygmy rabbits. Our flexible modeling approach can be used to (1) quantify how animals evaluate and trade off multiple habitat attributes when the benefits and risks are difficult to quantify, and (2) integrate diverse risks that influence fitness and habitat selection into a single index of habitat value. This index potentially could be applied to landscapes to predict habitat selection across several scales.

Hungry grouse in a warming world: emerging risks from plant chemical defenses and climate change

Conservation and management of habitat is central to the conservation of grouse. Identifying thresholds of biotic and abiotic risks that may reduce habitat quality is therefore a component of habitat management of grouse. We propose that dietary phytochemicals, specifically plant secondary metabolites (PSMs), represent an ecological risk to grouse, which are not often considered in the management of grouse. Most species of grouse consume PSMs, which have negative consequences at some concentration. Moreover, several studies provide evidence that the risks posed by PSMs will likely increase under projected climate change scenarios. We discuss potential risks of PSMs for grouse and propose theoretical models, which can be used to test current and future physiological, behavioural and ecological risks of PSMs. We propose that dose-response thresholds can be used to predict and monitor the synergistic risks of PSMs and climate change for grouse. We further suggest that identifying dose-response thresholds to PSMs is needed in the management of vertebrate herbivores in general.

Selection of food patches by sympatric herbivores in response to concealment and distance from a refuge

Summary Small herbivores face risks of predation while foraging and are often forced to trade off food quality for safety. Life history, behaviour, and habitat of predator and prey can influence these trade‐offs. We compared how two sympatric rabbits (pygmy rabbit, Brachylagus idahoensis; mountain cottontail, Sylvilagus nuttallii) that differ in size, use of burrows, and habitat specialization in the sagebrush‐steppe of western North America respond to amount and orientation of concealment cover and proximity to burrow refuges when selecting food patches. We predicted that both rabbit species would prefer food patches that offered greater concealment and food patches that were closer to burrow refuges. However, because pygmy rabbits are small, obligate burrowers that are restricted to sagebrush habitats, we predicted that they would show stronger preferences for greater cover, orientation of concealment, and patches closer to burrow refuges. We offered two food patches to individuals of each species during three experiments that either varied in the amount of concealment cover, orientation of concealment cover, or distance from a burrow refuge. Both species preferred food patches that offered greater concealment, but pygmy rabbits generally preferred terrestrial and mountain cottontails preferred aerial concealment. Only pygmy rabbits preferred food patches closer to their burrow refuge. Different responses to concealment and proximity to burrow refuges by the two species likely reflect differences in perceived predation risks. Because terrestrial predators are able to dig for prey in burrows, animals like pygmy rabbits that rely on burrow refuges might select food patches based more on terrestrial concealment. In contrast, larger habitat generalists that do not rely on burrow refuges, like mountain cottontails, might trade off terrestrial concealment for visibility to detect approaching terrestrial predators. This study suggests that body size and evolutionary adaptations for using habitat, even in closely related species, might influence anti‐predator behaviors in prey species.