M. Denise Dearing

Determining biological tissue turnover using stable isotopes: the reaction progress variable.

The reaction progress variable is applied to stable isotope turnover of biological tissues. This approach has the advantage of readily determining whether more than one isotope turnover pool is present; in addition, the normalization process inherent to the model means that multiple experiments can be considered together although the initial and final isotope compositions are different. Consideration of multiple isotope turnover pools allows calculation of diet histories of animals using a time sequence of isotope measurements along with isotope turnover pools. The delayed release of blood cells from bone marrow during a diet turnover experiment can be quantified using this approach. Turnover pools can also be corrected for increasing mass during an experiment, such as when the animals are actively growing. Previous growth models have been for exponential growth; the approach here can be used for several different growth models.

Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores

Ingestion of plant secondary metabolites (PSMs) presents a physiological and behavioral challenge for mammalian herbivores. Herbivores must not only detoxify PSMs, but they may also deal with energetic constraints such as reduced food intake, mass loss, increased excretion of energy, and increased metabolic demands. We hypothesized that the energetic consequences of consuming PSMs will significantly compromise apparent metabolizable energy intake (AMEI) and energy expenditure in mammalian herbivores. Furthermore, we hypothesized that foraging strategy would influence the degree to which plant consumption impacts energy budgets, such that dietary specialists would be less impacted than generalists when both are consuming the plant species preferred by the specialist. Hypotheses were tested by comparing AMEI and energy expended on basal metabolic rate (BMR) and locomotion in a juniper specialist ( Neotoma stephensi) and generalist (N. albigula) woodrat fed control diet and diet containing juniper foliage ( Jun- iperus monosperma). In general, the intake of PSMs in juniper increased the energy excreted in urine and feces in both specialist and generalist woodrats. Specialist woodrats minimized the costs associated with the intake of juniper by ingesting more juniper diet, thereby increasing energy intake, and reducing energy expended on BMR and locomotor activity. Generalist woodrats also decreased locomotor activity on a juniper diet but did not increase intake and maintained BMR. In turn, specialist woodrats had twice as much energy available for activities such as reproduction when consuming a juniper diet than generalists. These results suggest that the intake of PSMs impinges on AMEI and compromises energy ex- penditure, but that the impact of PSMs on energy budgets is relative to ecological experience with PSMs. Moreover, compensatory feeding, metabolic depression, and low activity may

Gut microbes of mammalian herbivores facilitate intake of plant toxins.

The foraging ecology of mammalian herbivores is strongly shaped by plant secondary compounds (PSCs) that defend plants against herbivory. Conventional wisdom holds that gut microbes facilitate the ingestion of toxic plants; however, this notion lacks empirical evidence. We investigated the gut microbiota of desert woodrats (Neotoma lepida), some populations of which specialise on highly toxic creosote bush (Larrea tridentata). Here, we demonstrate that gut microbes are crucial in allowing herbivores to consume toxic plants. Creosote toxins altered the population structure of the gut microbiome to facilitate an increase in abundance of genes that metabolise toxic compounds. In addition, woodrats were unable to consume creosote toxins after the microbiota was disrupted with antibiotics. Last, ingestion of toxins by naïve hosts was increased through microbial transplants from experienced donors. These results demonstrate that microbes can enhance the ability of hosts to consume PSCs and therefore expand the dietary niche breadth of mammalian herbivores.

THE MANIPULATION OF PLANT TOXINS BY A FOOD‐HOARDING HERBIVORE, OCHOTONA PRINCEPS

Generalist mammalian herbivores typically avoid plant species containing high levels of plant secondary compounds because generalists are thought to lack the ability to process large quantities of these chemicals. Here I propose and test two hypotheses: (1) that food-hoarding herbivores behaviorally overcome consumption limits imposed by secondary compounds by storing food until the toxins degrade; and (2) that the presence of secondary compounds in cached plant material facilitates the preservation of these items, as well as other cached items that lack such compounds. To evaluate these hypotheses, I conducted a number of field and laboratory experiments using the North American pika, Ochotona princeps, a generalist herbivore that consumes low-phenolic vegetation in the summer while it simultaneously collects and stores high-phenolic vegetation for subsequent consumption during winter. In experiments investigating decomposition of summer and winter diets of pikas, after 10 mo of storage, the winter diet retained 20.5% more biomass, and was higher in energy, lower in fiber, and equal in nitrogen compared to the summer diet. Moreover, a common food item in the winter diet, Acomastylis rossii, which contains high levels of phenolics, was the only plant extract to deter bacterial growth in a bioassay. Acomastylis rossii leaves with experimentally reduced phenolic levels retained significantly less biomass than leaves with natural phenolic concentrations. However, the presence of A. rossii in artificial caches containing a low-phenolic species, Trifolium parryi, did not facilitate the preservation of T. parryi. Approximately halfway through the typical storage period, phenolic concentrations of pika winter diet samples in artificial caches decreased to levels readily consumed by pikas in their summer diet. Examination of natural haypiles of pikas before and after storage revealed that pikas do increase their intake of A. rossii from the haypile sometime during the winter. In experiments with captive pikas, pikas preferred A. rossii with experimentally reduced phenolic concentrations over those with natural concentrations. Observations of pikas foraging from natural and artificial haypiles suggested that pikas do not increase their intake of A. rossii from the haypile until phenolics levels decrease. Taken together, the results support both of the hypotheses. Pikas manipulate plant chemistry by storing plants rich in allelochemicals and by delaying consumption of these plants until the toxins decay. Moreover, plants with high levels of secondary compounds exhibit superior preservation qualities so that more biomass and nutrients are retained during storage. As food caching is a common strategy among several animal classes and many foods contain potentially deleterious compounds, the manipulation of food toxins by storage may be a prevalent phenomenon.

Ecology of hantavirus in a changing world.

Hantavirus is a genus of virus represented by 45 different species and is hosted by small mammals, predominantly rats and mice. Roughly, half of all hantaviruses cause diseases in humans that vary in morbidity from mild to severe. The natural and anthropogenic changes occurring in the environment appear to be impacting the ecology of hantaviruses and their natural hosts as well as the incidence of hantaviral diseases in humans. Although such studies are limited at this time, there is evidence that natural climate cycles such as El Niño as well as anthropogenic climate change enhance hantavirus prevalence when host population dynamics are driven by food availability. Climate appears to have less of an effect on hantavirus when host populations are controlled by predators. Human alteration to the landscape also appears to enhance hantavirus prevalence when the disturbance regime enriches the environment for the host, for example, agriculture. More long‐term studies on multiple species of hantavirus are needed to accurately predict the outcome of changing environmental conditions on prevalence in hosts as well as disease incidence in humans.

Atmospheric CO2 as a Global Change Driver Influencing Plant-Animal Interactions

Abstract Plants respond to changes in atmospheric carbon dioxide. To herbivores, the decreased leaf protein contents and increased C/N ratios common to all leaves under elevated atmospheric carbon dioxide imply a reduction in food quality. In addition to these fine-scale adjustments, the abundance of C3 and C4 plants (particularly grasses) are affected by atmospheric carbon dioxide. C4 grasses currently predominate over C3 grasses in warmer climates and their distributions expand as atmospheric carbon dioxide levels decreased during glacial periods. C4 grasses are a less nutritious food resource than C3 grasses both in terms of reduced protein content and increased C/N ratios. There is an indication that as C4-dominated ecosystems expanded 6–8 Ma b.p., there were significant species-level changes in mammalian grazers. Today there is evidence that mammalian herbivores differ in their preference for C3 versus C4 food resources, although the factors contributing to these patterns are not clear. Elevated carbon dioxide levels will likely alter food quality to grazers both in terms of fine-scale (protein content, C/N ratio) and coarse-scale (C3 versus C4) changes.

Efflux Transporters as a Novel Herbivore Countermechanism to Plant Chemical Defenses

The recent discovery of efflux transporters in the gut has revolutionized our understanding of the absorption and bioavailability of pharmaceuticals and other xenobiotics in humans. Despite the celebrity of efflux transporters in the areas of pharmacology and medicine, their significance is only beginning to be realized in the area of plant–herbivore interactions. This review integrates reports on the importance of gut efflux transporters to diet selection by herbivores. The diets of herbivores are laden with toxic plant secondary metabolites (PSMs) that until recently were thought to be processed almost exclusively by detoxification enzymes in the liver. We describe how efflux transporters in the gut may play a critical role in regulating the absorption of PSMs in herbivores and dictating diet selection. Recent studies suggest that the role of efflux transporters in mediating diet selection in herbivores may be as critical as detoxification enzymes. In addition to diet selection, gut efflux transporters have implications for other aspects of plant–animal interactions. They may be significant components of the evolutionary arms race that influences chemical diversity in plants. Furthermore, in agricultural systems, gut efflux transporters may play an important role in the effectiveness of pesticides. This synthesis paper introduces a new direction in plant–herbivore interactions by providing a complementary mechanism, regulated absorption, to detoxification that may define tolerance to PSMs by herbivores.

Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission

Heterogeneities within disease hosts suggest that not all individuals have the same probability of transmitting disease or becoming infected. This heterogeneity is thought to be due to dissimilarity in susceptibility and exposure among hosts. As such, it has been proposed that many host–pathogen systems follow the general pattern whereby a small fraction of the population accounts for a large fraction of the pathogen transmission. This disparity in transmission dynamics is often referred to as ‘20/80 Rule’, i.e. approximately 20 per cent of the hosts are responsible for 80 per cent of pathogen transmission. We investigated the role of heterogeneity in contact rates among potential hosts of a directly transmitted pathogen by examining Sin Nombre virus (SNV) in deer mice (Peromyscus maniculatus). Using foraging arenas and powder marking, we documented contacts between wild deer mice in Great Basin Desert, central Utah. Our findings demonstrated heterogeneity among deer mice, both in frequency and in duration of contacts with other deer mice. Contact dynamics appear to follow the general pattern that a minority of the population accounts for a majority of the contacts. We found that 20 per cent of individuals in the population were responsible for roughly 80 per cent of the contacts observed. Larger-bodied individuals appear to be the functional group with the greatest SNV transmission potential. Contrary to our predictions, transmission potential was not influenced by breeding condition or sex.

Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts

Many animals face unpredictable food sources and periods of prolonged fasting, which likely present significant challenges to gut microorganisms. While several studies have demonstrated that fasting impacts the gut microbiota, experiments have not been carried out in a comparative context. We used 16S rRNA gene sequencing to document changes in colonic and cecal microbiomes of animals representing five classes of vertebrates at four time points through prolonged fasting: tilapia, toads, geckos, quail, and mice. We found differences in the starvation-induced changes in the microbiome across host species and across gut regions. Microbial phylogenetic diversity increased as a result of fasting in the colons of fish, toads, and mice, while quail exhibited a decrease in diversity; geckos exhibited no change. Microbial diversity in the cecum decreased in fish and exhibited no change in mice. Alterations in relative abundances of microbial taxa varied across hosts. Fish exhibited the most significant changes due to fasting, while geckos maintained a stable community over 28 days of fasting. We uncovered several shared responses of the microbiota across hosts. For example, all tetrapods exhibited decreases in the abundances of Coprobacillus and Ruminococcus in response to fasting. We also discuss host-mediated physiological mechanisms that may underlie these community changes.

Sin Nombre virus and rodent species diversity: A test of the dilution and amplification hypotheses

Background Species diversity is proposed to greatly impact the prevalence of pathogens. Two predominant hypotheses, the “Dilution Effect” and the “Amplification Effect”, predict divergent outcomes with respect to the impact of species diversity. The Dilution Effect predicts that pathogen prevalence will be negatively correlated with increased species diversity, while the Amplification Effect predicts that pathogen prevalence will be positively correlated with diversity. For many host-pathogen systems, the relationship between diversity and pathogen prevalence has not be empirically examined. Methodology/Principal Findings We tested the Dilution and Amplification Effect hypotheses by examining the prevalence of Sin Nombre virus (SNV) with respect to diversity of the nocturnal rodent community. SNV is directly transmitted primarily between deer mice (Peromyscus maniculatus). Using mark-recapture sampling in the Spring and Fall of 2003–2005, we measured SNV prevalence in deer mice at 16 landscape level sites (3.1 hectares each) that varied in rodent species diversity. We explored several mechanisms by which species diversity may affect SNV prevalence, including reduced host density, reduced host persistence, the presence of secondary reservoirs and community composition. We found a negative relationship between species diversity and SNV prevalence in deer mice, thereby supporting the Dilution Effect hypothesis. Deer mouse density and persistence were lower at sites with greater species diversity; however, only deer mouse persistence was positively correlated with SNV prevalence. Pinyon mice (P. truei) may serve as dilution agents, having a negative effect on prevalence, while kangaroo rats (Dipodomys ordii), may have a positive effect on the prevalence of SNV, perhaps through effects on deer mouse behavior. Conclusions/Significance While previous studies on host-pathogen systems have found patterns of diversity consistent with either the Dilution or Amplification Effects, the mechanisms by which species diversity influences prevalence have not been investigated. Our study indicates that changes in host persistence, coupled with interspecific interactions, are important mechanisms through which diversity may influence patterns of pathogens. Our results reveal the complexity of rodent community interactions with respect to SNV dynamics.