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

Antioxidant Capacity of Wyoming Big Sagebrush (\u3cem\u3eArtemisia tridentata\u3c/em\u3e SSP. \u3cem\u3eWyomingensis\u3c/em\u3e) Varies Spatially and is Not Related to the Presence of a Sagebrush Dietary Specialist

Sagebrush (Artemisia spp.) in North America is an abundant native plant species that is ecologically and evolutionarily adapted to have a diverse array of biologically active chemicals. Several of these chemicals, specifically polyphenols, have antioxidant activity that may act as biomarkers of biotic or abiotic stress. This study investigated the spatial variation of antioxidant capacity, as well as the relationship between a mammalian herbivore and antioxidant capacity in Wyoming big sagebrush (Artemisia tridentata wyomingensis). We quantified and compared total polyphenols and antioxidant capacity of leaf extracts from sagebrush plants from different spatial scales and at different levels of browsing by a specialist mammalian herbivore, the pygmy rabbit (Brachylagus idahoensis). We found that antioxidant capacity of sagebrush extracts was positively correlated with total polyphenol content. Antioxidant capacity varied spatially within and among plants. Antioxidant capacity in sagebrush was not related to either browsing intensity or duration of association with rabbits. We propose that the patterns of antioxidant capacity observed in sagebrush may be a result of spatial variation in abiotic stress experienced by sagebrush. Antioxidants could therefore provide a biomarker of environmental stress for sagebrush that could aid in management and conservation of this plant in the threatened sagebrush steppe

Spectral Fingerprints Predict Functional Chemistry of Native Plants Across Sagebrush-Steppe Landscapes

Landscapes are changing and under threat from anthropogenic activities, decreasing land cover, contaminated air and water quality, and climate change. These changes impact native communities and their functions at all spatial scales. A major functional trait being affected across these communities is nitrogen. Nitrogen supports plant nutrient cycling and growth, serves as an indicator for crude protein and productivity, and offers quality forage for wild and domestic herbivores. We need better ways to monitor nitrogen across space and time. Current monitoring is elaborate, time-consuming, and expensive. We propose drawing from agricultural methodologies to incorporate near-infrared spectroscopy as a technique in detecting and monitoring nitrogen concentrations across a threatened shrub-steppe ecosystem. We are currently developing calibration equations for nitrogen in sagebrush across four species (Artemisia tridentata wyomingensis, A. tripartita, A. arbuscula, A. nova), three study sites and two seasons. Preliminary results suggest that nitrogen can be accurately predicted across all sites, species, and seasons, explaining 75-90% of the variation in nitrogen. These results indicate that near infrared spectroscopy offers a rapid, noninvasive diagnostic tool for assessing nitrogen in wild systems. This advancing technology is important because it economizes the collection of ecological data in rapidly changing landscapes and provides land managers and researchers with valuable information about the health and sustainability of their lands

Unifying Community Detection Across Scales from Genomes to Landscapes

Biodiversity science encompasses multiple disciplines and biological scales from molecules to landscapes. Nevertheless, biodiversity data are often analyzed separately with discipline-specific methodologies, constraining resulting inferences to a single scale. To overcome this, we present a topic modeling framework to analyze community composition in cross-disciplinary datasets, including those generated from metagenomics, metabolomics, field ecology and remote sensing. Using topic models, we demonstrate how community detection in different datasets can inform the conservation of interacting plants and herbivores. We show how topic models can identify members of molecular, organismal and landscape-level communities that relate to wildlife health, from gut microbes to forage quality. We conclude with a future vision for how topic modeling can be used to design cross-scale studies that promote a holistic approach to detect, monitor and manage biodiversity

Low Activities of Digestive Enzymes in the Guts of Herbivorous Grouse (Aves: Tetraoninae)

Avian herbivores face the exceptional challenge of digesting recalcitrant plant material while under the selective pressure to reduce gut mass as an adaptation for fight. One mechanism by which avian herbivores may overcome this challenge is to maintain high activities of intestinal enzymes that facilitate the digestion and absorption of nutrients. However, previous studies in herbivorous animals provide equivocal evidence as to how activities of digestive enzymes may be adapted to herbivorous diets. For example, “rate-maximizing” herbivores generally exhibit rapid digesta transit times and high activities of digestive enzymes. Conversely, “yield-maximizing” herbivores utilize long gut retention times and express lower activities of digestive enzymes. Here, we investigated the activities of digestive enzymes (maltase, sucrase, aminopeptidase-N) in the guts of herbivorous grouse (Aves: Tetraoninae) and compared them to activities measured in several other avian species. We found that several grouse species exhibit activities of enzymes that are dramatically lower than those measured in other birds. We propose that grouse may use a “yield-maximizing” strategy of digestion, which is characterized by relatively long gut retention times and generally lower enzyme activities. These low activities of intestinal digestive enzyme could have ecological and evolutionary consequences, as grouse regularly consume plants with compounds known to inhibit digestive enzymes. However, more comprehensive studies on passage rates, digestibility, and microbial contributions will be necessary to understand the full process of digestion in herbivorous birds

Metagenomic Sequencing Provides Insights into Microbial Detoxification in the Guts of Small Mammalian Herbivores (\u3cem\u3eNeotoma\u3c/em\u3e spp.)

Microbial detoxification of plant toxins influences the use of plants as food sources by herbivores. Stephen’s woodrats (Neotoma stephensi) specialize on juniper, which is defended by oxalate, phenolics and monoterpenes, while closely related N. albigula specialize on cactus, which only contains oxalate. Woodrats maintain two gut chambers harboring dense microbial communities: a foregut chamber proximal to the major site of toxin absorption, and a cecal chamber in their hindgut. We performed several experiments to investigate the location and nature of microbial detoxification in the woodrat gut. First, we measured toxin concentrations across gut chambers of N. stephensi. Compared to food material, oxalate concentrations were immediately lower in the foregut, while concentrations of terpenes remained high in the foregut, and were lowest in the cecal chamber. We conducted metagenomic sequencing of the foregut chambers of both woodrat species and cecal chambers of N. stephensi to compare microbial functions. We found that most genes associated with detoxification were more abundant in the cecal chambers of N. stephensi. However, some genes associated with degradation of oxalate and phenolic compounds were more abundant in the foregut chambers. Thus, microbial detoxification may take place in various chambers depending on the class of chemical compound

Plant Protein and Secondary Metabolites Influence Diet Selection in a Mammalian Specialist Herbivore

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

Toxic Scat: A Mechanism to Prevent Overdosing on Plant Chemicals by Grouse

Although abundant and accessible, plants pose significant challenges to herbivores. The high fiber content and relatively low nutritional value of plants compared to animals makes plants a particularly difficult food source for birds. For example, birds lack teeth required to reduce particle size and flight limits the size and complexity of the gastrointestinal tract (Dudley and Vermeij 1992) required for fiber digestion. These limitations are thought to explain why herbivory is a rare foraging strategy in birds. A less studied explanation for limited herbivory in birds may also be the diversity of chemical defenses in plants. These chemical defenses can be toxic to herbivores and energetically costly to detoxify (e.g. Glick and Joslyn 1970, Lindroth and Batzli 1984, Robbins et al. 1987, Guglielmo et al. 1996, Sorensen et al. 2005). Similar to the limited digestive capacity, flight may limit the size of the liver which is the major organ used to detoxify and eliminate ingested toxins

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