Jennifer S. Forbey

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

Graham G. Frye et al. — Wed, 15 May 2013 15:45:48 PDT

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.

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

Jennifer Sorensen Forbey et al. — Wed, 15 May 2013 15:45:46 PDT

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.

Mechanisms for Eliminating Monoterpenes of Sagebrush by Specialist and Generalist Rabbits

Lisa A. Shipley et al. — Mon, 12 Nov 2012 15:40:45 PST

Pygmy rabbits (Brachylagus idahoensis) are one of only three vertebrates that subsist virtually exclusively on sagebrush (Artemisia spp.), which contains high levels of monoterpenes that can be toxic. We examined the mechanisms used by specialist pygmy rabbits to eliminate 1,8-cineole, a monoterpene of sagebrush, and compared them with those of cottontail rabbits (Sylvilagus nuttalli), a generalist herbivore. Rabbits were offered food pellets with increasing concentrations of cineole, and we measured voluntary intake and excretion of cineole metabolites in feces and urine. We expected pygmy rabbits to consume more, but excrete cineole more rapidly by using less-energetically expensive methods of detoxification than cottontails. Pygmy rabbits consumed 3–5 times more cineole than cottontails relative to their metabolic body mass, and excreted up to 2 times more cineole metabolites in their urine than did cottontails. Urinary metabolites excreted by pygmy rabbits were 20 % more highly-oxidized and 6 times less-conjugated than those of cottontails. Twenty percent of all cineole metabolites recovered from pygmy rabbits were in feces, whereas cottontails did not excrete fecal metabolites. When compared to other mammals that consume cineole, pygmy rabbits voluntarily consumed more, and excreted more cineole metabolites in feces, but they excreted less oxidized and more conjugated cineole metabolites in urine. Pygmy rabbits seem to have a greater capacity to minimize systemic exposure to cineole than do cottontails, and other cineole-consumers, by minimizing absorption and maximizing detoxification of ingested cineole. However, mechanisms that lower systemic exposure to cineole may come with a higher energetic cost in pygmy rabbits than in other mammalian herbivores.

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

Jennifer Sorensen Forbey et al. — Fri, 28 Sep 2012 08:30:26 PDT

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.

The Herbivore's Prescription: A Pharm-Ecological Perspective on Host Plant Use by Vertebrate and Invertebrate Herbivores

Jennifer Forbey et al. — Tue, 27 Mar 2012 14:24:57 PDT

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

Jennifer Forbey et al. — Wed, 01 Feb 2012 08:59:01 PST

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.

All Leaves Are Not Created Equal: Variation Among Leaves in Chemical Defenses and Nutritional Quality

Xochi Campos et al. — Wed, 30 Nov 2011 14:50:34 PST

Coevolution among plants and herbivores has led to variation in plant defenses and herbivore foraging. Plants must defend against herbivores, whereas herbivores must find ways to overcome plant defenses and meet nutritional needs. Variation in plant quality is important because it can influence selection of plants by herbivores for food. Few studies have investigated the variation occurring within a single plant. Sagebrush offers an excellent system for studying the variation in dietary and chemical quality within a plant. First, variation in nutrition and chemical content exists between subspecies (Kelsey 1982) and between plants of a single subspecies of sagebrush from different geographic locations (Welch 1981). Second, sagebrush has two types of leaves, ephemeral and persistent, and our preliminary data demonstrates that pygmy rabbits prefer ephemeral over persistent leaves leaf types indicating leaf types differ in quality.

Modelling Nutritional Interactions: From Individuals to Communities

Jennifer Forbey — Wed, 30 Nov 2011 14:50:33 PST

Nutrient acquisition is a major context for ecological interactions among species but ecologists and nutritionists have developed theory in isolation from each other. Developments in agent-based modelling, state–space modelling of nutrition and multi-scale modelling of landscape ecology provide the components for a new synthesis in nutritional ecology linking the nutritional biology of individual organisms to population- and community-level processes across multiple scales within an evolutionary context. We review the core elements for such a synthesis and set out the principles for a generic modelling framework that could be used to test specific ecological hypotheses.

Developing New Methods to Quantify Stress in Wildlife Using Liquid Chromatography Tandem Mass Spectrometry

Brandon Harper et al. — Wed, 30 Nov 2011 14:50:31 PST

Stress levels in wildlife species are an accurate indicator of an animal’s well-being and can reflect decreases in habitat quality. Stress levels can be measured by the presence of the stress response hormones cortisol, cortisone, and corticosterone. Analysis of these stress hormones in fecal samples has been widely used because feces can be easily obtained and non-invasively collected in the field. Methods of detecting stress levels from fecal samples of wildlife species are currently limited to enzyme immunoassay testing. This method uses antibodies to bind to target stress hormones. However, immunoassay testing can be time consuming and very expensive². We propose that Liquid Chromatography Tandem Mass Spectrometry (LC-MS/MS) offers a new method to quantify levels of the stress hormones from fecal samples that is less expensive and time consuming than traditional immunoassays¹. As part of the Idaho Science Talent Expansion Program (STEP), we are developing a simple, accurate, and relatively inexpensive method to detect stress hormones in fecal samples from free-ranging pygmy rabbits (Brachylagus idahoensis) and sage grouse (Centrocercus urophasianus) using LC-MS/MS.

To Eat or Not to Eat? Developing Biomarkers for Diet Selection by Herbivores

Kristina Gehlken et al. — Wed, 30 Nov 2011 14:50:29 PST

A major goal in conservation biology is to explain habitat use by animals. Remote sensing has been used for landscape-scale analysis of habitat features. However, studies that directly link specific parameters of habitat quality to selection by wildlife are needed at the microsite-scale before landscape-scale mapping can be validated. We used the sagebrush-pygmy rabbit system to develop spectral biomarkers that can predict how the quality of food influences habitat use.

The Emerging Role of Pharmacology in Understanding Consumer–Prey Interactions in Marine and Freshwater Systems

Erik E. Sotka et al. — Thu, 31 Mar 2011 15:52:01 PDT

Within our lakes, streams, estuaries, and oceans, there is an astounding chemodiversity of secondary metabolites produced by microbes, algae, and invertebrates. Nearly 30 years of study have yielded hundreds of examples in which secondary metabolites alter the foraging behavior or fitness of aquatic consumers, or both. However, our understanding of the mechanisms that mediate the fate and consequences of these metabolites in aquatic consumers remains in its infancy. Interactions between metabolites and consumers at the molecular and biochemical level are the purview of modern pharmacology, which is rooted in the long history of human–drug interactions and can be adopted for ecological studies. Here, we argue that a pharmacological approach to consumer–prey interactions will be as productive within aquatic systems as it has been for understanding terrestrial systems. We review the diversity of secondary metabolites in aquatic organisms, their known effects on the feeding behaviors and performance of aquatic consumers, and the few studies that have attempted to describe their biochemical manipulation within consumer tissues, i.e., their absorption, distribution, metabolism (including detoxification), and excretion. We then highlight vexing issues in the ecology and evolution of aquatic consumer–prey interactions that would benefit from a pharmacological approach, including specialist-versus-generalist feeding strategies, dietary mixing, nutrient–toxin interactions, and taste. Finally, we argue that a pharmacological approach could help to predict how consumer–prey interactions are altered by global changes in pH, water temperature and ultraviolet radiation, or by pollution. Arguably, the state of knowledge of aquatic consumer–prey interactions is equivalent to that faced by ecologists studying terrestrial herbivores in the 1970s; the literature documents profound variation among consumers in their feeding tolerances for secondary metabolites without a thorough understanding of the mechanisms that underlie that variation. The subsequent advancement in our understanding of terrestrial herbivores in the intervening decades provides confidence that applying a pharmacological approach to aquatic consumers will prove equally productive.

PharmEcology: A Pharmacological Approach to Understanding Plant-Herbivore Interactions: An Introduction to the Symposium

Jennifer S. Forbey et al. — Wed, 20 Oct 2010 08:40:20 PDT

A central goal in understanding the ecology and evolution of animals is to identify factors that constrain or expand breadth of diet. Selection of diet in many animals is often constrained by chemical deterrents (i.e., secondary metabolites) in available food items. The integration of chemistry and ecology has led to a significant understanding of the chemical complexity of prey (e.g., animals, plants, and algae) and the resultant foraging behavior of consumers. However, most of the literature on chemical defenses of marine and terrestrial prey lacks a mechanistic understanding of how consumers tolerate, or avoid, chemically-defended foods. In order to understand ecological patterns of foraging and co-evolutionary relationships between prey and consumers, we must advance our understanding of the physiological mechanisms responsible for chemical interactions. Such mechanistic studies require the integration of the discipline of pharmacology with ecology, which we call “PharmEcology.” Pharmacology provides the tools and insight to investigate the fate (what the body does to a chemical) and action (what a chemical does to the body) of chemicals in living organisms, whereas ecology provides the insight into the interactions between organisms (e.g., herbivores) and their environment (e.g., plants). Although, the general concepts of pharmacology were introduced to ecologists studying plant–herbivore interactions over 30 years ago, the empirical use of pharmacology to understand mechanisms of chemical interactions has remained limited. Moreover, many of the recent biochemical, molecular and technical advances in pharmacology have yet to be utilized by ecologists. The PharmEcology symposium held at a meeting of the Society for Integrative and Comparative Biology in January of 2009 was developed to define novel research directions at the interface of pharmacology and ecology.

Exploitation of Secondary Metabolites by Animals: A Response to Homeostatic Challenges

Jennifer S. Forbey et al. — Wed, 20 Oct 2010 08:36:34 PDT

We propose that the exploitation of the bioactive properties of secondary metabolites (SMs) by animals can provide a “treatment” against various challenges that perturb homeostasis in animals. The unified theoretical framework for the exploitation of SMs by animals is based on a synthesis of research from a wide range of fields and although it is focused on providing generalized predictions for herbivores that exploit SMs of plants, predictions can be applied to understand the exploitation of SMs by many animals. In this review, we argue that the probability of SM exploitation is determined by the relative difference between the cost of a homeostatic challenge and the toxicity of the SM and we provide various predictions that can be made when considering behavior under a homeostatic perspective. The notion that animals experience and respond to costly challenges by exploiting therapeutic SMs provides a relatively novel perspective to explain foraging behavior in herbivores, specifically, and behavior of animals in general. We provide evidence that animals can exploit the biological activity of SMs to mitigate the costs of infection by parasites, enhance reproduction, moderate thermoregulation, avoid predation, and increase alertness. We stress that a better understanding of animal behavior requires that ecologists look beyond their biases that SMs elicit punishment and consider a broader view of avoidance or selection of SMs relative to the homeostatic state. Finally, we explain how understanding exploitation of SMs by animals could be applied to advance practices of animal management and lead to discovery of new drugs.

Revisiting the Dietary Niche: When is a Mammalian Herbivore a Specialist?

Lisa A. Shipley et al. — Wed, 20 Oct 2010 08:26:52 PDT

Understanding dietary specialization in herbivores has theoretical and practical implications in ecology, yet defining niche breadth consistently has been problematic. To increase clarity and communication among ecologists and among disciplines (i.e., chemists, pharmacologists), we propose a specialization key for mammalian herbivores that assigns “obligatory” and “facultative” modifiers to the terms “specialist” and “generalist”. These modifiers are assigned based on (1) relative breadth of the animal's realized niche and diet (what it eats), (2) relative breadth of the fundamental niche and available diet (what it could eat), (3) the extent of chemical or physical characteristics, termed “difficulty”, that make food items either low in value or unpalatable to most herbivores, and (4) relevant temporal and spatial scales at which diets and niche breadth were measured. Obligatory specialists always have a narrow realized niche consisting of difficult food items, and morphological adaptations and/or the loss of redundant behavioral flexibility that effectively limit their fundamental niches, precluding them from expanding their diet under changed environmental conditions. Facultative specialists have a consistently narrow realized niche for difficult foods during at least one spatial or temporal scale, but have a broad enough fundamental niche to allow them to expand their diet to include less difficult foods when environmental conditions allow. Facultative generalists have the broadest fundamental niche, allowing them to consume a wide variety of foods. However, they may occasionally demonstrate a narrow realized niche, focused on less difficult plants than is the case with specialists. Finally, the obligatory generalists always have a wide realized niche because of a relatively narrow fundamental niche, precluding them from eating much of any difficult plant. We summarize hypothesized characteristics of mammalian herbivores in each of the four categories of specialization. We demonstrate the need for further work on defining the realized and fundamental niches, comparing among herbivores across categories conducted under similar conditions, and understanding the nature of trade-offs required for specialization and generalization for both community and phylogenetically based analyses.

Invited Symposium Speaker: Positive Effects of PSMs on Ecology and Health of Vertebrates and Invertebrates

Jennifer S. Forbey — Mon, 17 May 2010 10:16:34 PDT

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

M. D. Dearing et al. — Fri, 14 May 2010 11:43:16 PDT

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 20ºC or 28ºC. 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 (T_b) were measured over the last 2 d. Woodrats at 28ºC ate significantly less juniper, both proportionally and absolutely, than woodrats at 20ºC. RMRs were higher for woodrats consuming juniper regardless of ambient temperature, and T_b was higher for woodrats consuming juniper at 28ºC than for woodrats eating control diet at 28ºC. 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.