Biomarkers of Animal Nutrition: From Seasonal to Lifetime Indicators of Environmental Conditions.

Nutrition underpins survival and reproduction in animal populations; reliable nutritional biomarkers are therefore requisites to understanding environmental drivers of population dynamics. Biomarkers vary in scope of inference and sensitivity, making it important to know what and when to measure to properly quantify biological responses. We evaluated the repeatability of three nutritional biomarkers in a large, iteroparous mammal to evaluate the level of intrinsic and extrinsic contributions to those traits. During a long-term, individual-based study in a highly variable environment, we measured body fat, body mass, and lean mass of mule deer (Odocoileus hemionus) each autumn and spring. Lean mass was the most repeatable biomarker (0.72 autumn; 0.61 spring), followed by body mass (0.64 autumn; 0.53 spring), and then body fat (0.22 autumn; 0.01 spring). High repeatability in body and lean mass likely reflects primary structural composition, which is conserved across seasons. Low repeatability of body fat supports that it is the primary labile source of energy that is largely a product of environmental contributions of the previous season. Based on the disparate levels in repeatability among nutritional biomarkers, we contend that body and lean mass are better indicators of nutritional legacies (e.g., maternal effects), whereas body fat is a direct and sensitive reflection of recent nutritional gains and losses.

Effects of supplemental feeding on the fecal bacterial communities of Rocky Mountain elk in the Greater Yellowstone Ecosystem.

Supplemental feeding of wildlife is a common practice often undertaken for recreational or management purposes, but it may have unintended consequences for animal health. Understanding cryptic effects of diet supplementation on the gut microbiomes of wild mammals is important to inform conservation and management strategies. Multiple laboratory studies have demonstrated the importance of the gut microbiome for extracting and synthesizing nutrients, modulating host immunity, and many other vital host functions, but these relationships can be disrupted by dietary perturbation. The well-described interplay between diet, the microbiome, and host health in laboratory and human systems highlights the need to understand the consequences of supplemental feeding on the microbiomes of free-ranging animal populations. This study describes changes to the gut microbiomes of wild elk under different supplemental feeding regimes. We demonstrated significant cross-sectional variation between elk at different feeding locations and identified several relatively low-abundance bacterial genera that differed between fed versus unfed groups. In addition, we followed four of these populations through mid-season changes in supplemental feeding regimes and demonstrated a significant shift in microbiome composition in a single population that changed from natural forage to supplementation with alfalfa pellets. Some of the taxonomic shifts in this population mirrored changes associated with ruminal acidosis in domestic livestock. We discerned no significant changes in the population that shifted from natural forage to hay supplementation, or in the populations that changed from one type of hay to another. Our results suggest that supplementation with alfalfa pellets alters the native gut microbiome of elk, with potential implications for population health.

Wave-like Patterns of Plant Phenology Determine Ungulate Movement Tactics.

Animals exhibit a diversity of movement tactics [1]. Tracking resources that change across space and time is predicted to be a fundamental driver of animal movement [2]. For example, some migratory ungulates (i.e., hooved mammals) closely track the progression of highly nutritious plant green-up, a phenomenon called "green-wave surfing" [3-5]. Yet general principles describing how the dynamic nature of resources determine movement tactics are lacking [6]. We tested an emerging theory that predicts surfing and the existence of migratory behavior will be favored in environments where green-up is fleeting and moves sequentially across large landscapes (i.e., wave-like green-up) [7]. Landscapes exhibiting wave-like patterns of green-up facilitated surfing and explained the existence of migratory behavior across 61 populations of four ungulate species on two continents (n = 1,696 individuals). At the species level, foraging benefits were equivalent between tactics, suggesting that each movement tactic is fine-tuned to local patterns of plant phenology. For decades, ecologists have sought to understand how animals move to select habitat, commonly defining habitat as a set of static patches [8, 9]. Our findings indicate that animal movement tactics emerge as a function of the flux of resources across space and time, underscoring the need to redefine habitat to include its dynamic attributes. As global habitats continue to be modified by anthropogenic disturbance and climate change [10], our synthesis provides a generalizable framework to understand how animal movement will be influenced by altered patterns of resource phenology.

Hidden cost of disease in a free-ranging ungulate: brucellosis reduces mid-winter pregnancy in elk.

Demonstrating disease impacts on the vital rates of free-ranging mammalian hosts typically requires intensive, long-term study. Evidence for chronic pathogens affecting reproduction but not survival is rare, but has the potential for wide-ranging effects. Accurately quantifying disease-associated reductions in fecundity is important for advancing theory, generating accurate predictive models, and achieving effective management. We investigated the impacts of brucellosis (Brucella abortus) on elk (Cervus canadensis) productivity using serological data from over 6,000 captures since 1990 in the Greater Yellowstone Ecosystem, USA. Over 1,000 of these records included known age and pregnancy status. Using Bayesian multilevel models, we estimated the age-specific pregnancy probabilities of exposed and naïve elk. We then used repeat-capture data to investigate the full effects of the disease on life history. Brucellosis exposure reduced pregnancy rates of elk captured in mid- and late-winter. In an average year, we found 60% of exposed 2-year-old elk were pregnant compared to 91% of their naïve counterparts (a 31 percentage point reduction, 89% HPDI = 20%-42%), whereas exposed 3- to 9-year-olds were 7 percentage points less likely to be pregnant than naïve elk of their same age (89% HPDI = 2%-11%). We found these reduced rates of pregnancy to be independent from disease-induced abortions, which afflict a portion of exposed elk. We estimate that the combination of reduced pregnancy by mid-winter and the abortions following mid-winter reduces the reproductive output of exposed female elk by 24%, which affects population dynamics to a similar extent as severe winters or droughts. Exposing hidden reproductive costs of disease is essential to avoid conflating them with the effects of climate and predation. Such reproductive costs cause complex population dynamics, and the magnitude of the effect we found should drive a strong selection gradient if there is heritable resistance.

Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics.

Providing food to wildlife during periods when natural food is limited results in aggregations that may facilitate disease transmission. This is exemplified in western Wyoming where institutional feeding over the past century has aimed to mitigate wildlife-livestock conflict and minimize winter mortality of elk (Cervus canadensis). Here we review research across 23 winter feedgrounds where the most studied disease is brucellosis, caused by the bacterium Brucella abortus Traditional veterinary practices (vaccination, test-and-slaughter) have thus far been unable to control this disease in elk, which can spill over to cattle. Current disease-reduction efforts are being guided by ecological research on elk movement and density, reproduction, stress, co-infections and scavengers. Given the right tools, feedgrounds could provide opportunities for adaptive management of brucellosis through regular animal testing and population-level manipulations. Our analyses of several such manipulations highlight the value of a research-management partnership guided by hypothesis testing, despite the constraints of the sociopolitical environment. However, brucellosis is now spreading in unfed elk herds, while other diseases (e.g. chronic wasting disease) are of increasing concern at feedgrounds. Therefore experimental closures of feedgrounds, reduced feeding and lower elk populations merit consideration.This article is part of the theme issue 'Anthropogenic resource subsidies and host-parasite dynamics in wildlife'.

Shifting brucellosis risk in livestock coincides with spreading seroprevalence in elk.

Tracking and preventing the spillover of disease from wildlife to livestock can be difficult when rare outbreaks occur across large landscapes. In these cases, broad scale ecological studies could help identify risk factors and patterns of risk to inform management and reduce incidence of disease. Between 2002 and 2014, 21 livestock herds in the Greater Yellowstone Area (GYA) were affected by brucellosis, a bacterial disease caused by Brucella abortus, while no affected herds were detected between 1990 and 2001. Using a Bayesian analysis, we examined several ecological covariates that may be associated with affected livestock herds across the region. We showed that livestock risk has been increasing over time and expanding outward from the historical nexus of brucellosis in wild elk on Wyoming's feeding grounds where elk are supplementally fed during the winter. Although elk were the presumed source of cattle infections, occurrences of affected livestock herds were only weakly associated with the density of seropositive elk across the GYA. However, the shift in livestock risk did coincide with recent increases in brucellosis seroprevalence in unfed elk populations. As increasing brucellosis in unfed elk likely stemmed from high levels of the disease in fed elk, disease-related costs of feeding elk have probably been incurred across the entire GYA, rather than solely around the feeding grounds. Our results suggest that focused disease mitigation in areas where seroprevalence in unfed elk is high could reduce the spillover of brucellosis to livestock. We also highlight the need to better understand the epidemiology of spillover events with detailed histories of disease testing, calving, and movement of infected livestock. Finally, we recommend using case-control studies to investigate local factors important to livestock risk.

Risk assessment and management of brucellosis in the southern greater Yellowstone area (II): Cost-benefit analysis of reducing elk brucellosis prevalence.

Recent cases of bovine brucellosis (Brucella abortus) in cattle (Bos taurus) and domestic bison (Bison bison) of the southern Greater Yellowstone Area (SGYA) have been traced back to free-ranging elk (Cervus elaphus). Several management activities have been implemented to reduce brucellosis seroprevalence in elk, including test-and-slaughter, low-density feeding at elk winter feedgrounds, and elk vaccination. It is unclear which of these activities are most cost-effective at reducing the risk of elk transmitting brucellosis to cattle. In a companion paper, a stochastic risk model was used to translate a reduction in elk seroprevalence to a reduction in the risk of transmission to cattle. Here, we use those results to estimate the expected economic benefits and costs of reducing seroprevalence in elk using three different management activities: vaccination of elk with Brucella strain 19 (S19), low-density feeding of elk, and elk test-and-slaughter. Results indicate that the three elk management activities yield negative expected net benefits, ranging from -$2983 per year for low-density feeding to -$595,471 per year for test-and-slaughter. Society's risk preferences will determine whether strategies that generate small negative net benefit, such as low-density feeding, are worth implementing. However, activities with large negative net benefits, such as test-and-slaughter and S19 vaccination, are unlikely to be economically worthwhile. Given uncertainty about various model parameters, we identify some circumstances in which individual management activities might generate positive expected net benefit.

Risk assessment and management of brucellosis in the southern greater Yellowstone area (I): A citizen-science based risk model for bovine brucellosis transmission from elk to cattle.

Livestock producers and state wildlife agencies have used multiple management strategies to control bovine brucellosis in the Greater Yellowstone Area (GYA). However, spillover from elk to domestic bison and cattle herds continues to occur. Although knowledge is increasing about the location and behavior of elk in the SGYA, predicting spatiotemporal overlap between elk and cattle requires locations of livestock operations and observations of elk contact by producers. We queried all producers in a three-county area using a questionnaire designed to determine location of cattle and whether producers saw elk comingle with their animals. This information was used to parameterize a spatially-explicit risk model to estimate the number of elk expected to overlap with cattle during the brucellosis transmission risk period. Elk-cattle overlap was predicted in areas further from roads and forest boundaries in areas with wolf activity, with higher slopes, lower hunter densities, and where the cost-distance to feedgrounds was very low or very high. The model was used to estimate the expected number of years until a cattle reactor will be detected, under alternative management strategies. The model predicted cattle cases every 4.28 years in the highest risk herd unit, a higher prediction than the one case in 26 years we have observed. This difference likely indicates that ongoing management strategies are at least somewhat effective in preventing potential elk-cattle brucellosis transmission in these areas. Using this model, we can infer the expected effectiveness of various management strategies for reducing the risk of brucellosis spillover from elk to cattle.

Large herbivores surf waves of green-up during spring.

The green wave hypothesis (GWH) states that migrating animals should track or 'surf' high-quality forage at the leading edge of spring green-up. To index such high-quality forage, recent work proposed the instantaneous rate of green-up (IRG), i.e. rate of change in the normalized difference vegetation index over time. Despite this important advancement, no study has tested the assumption that herbivores select habitat patches at peak IRG. We evaluated this assumption using step selection functions parametrized with movement data during the green-up period from two populations each of bighorn sheep, mule deer, elk, moose and bison, totalling 463 individuals monitored 1-3 years from 2004 to 2014. Accounting for variables that typically influence habitat selection for each species, we found seven of 10 populations selected patches exhibiting high IRG-supporting the GWH. Nonetheless, large herbivores selected for the leading edge, trailing edge and crest of the IRG wave, indicating that other mechanisms (e.g. ruminant physiology) or measurement error inherent with satellite data affect selection for IRG. Our evaluation indicates that IRG is a useful tool for linking herbivore movement with plant phenology, paving the way for significant advancements in understanding how animals track resource quality that varies both spatially and temporally.

Supplemental feeding alters migration of a temperate ungulate.

Conservation of migration requires information on behavior and environmental determinants. The spatial distribution of forage resources, which migration exploits, often are altered and may have subtle, unintended consequences. Supplemental feeding is a common management practice, particularly for ungulates in North America and Europe, and carryover effects on behavior of this anthropogenic manipulation of forage are expected in theory, but have received limited empirical evaluation, particularly regarding effects on migration. We used global positioning system (GPS) data to evaluate the influence of winter feeding on migration behavior of 219 adult female elk (Cervus elaphus) from 18 fed ranges and 4 unfed ranges in western Wyoming. Principal component analysis revealed that the migratory behavior of fed and unfed elk differed in distance migrated, and the timing of arrival to, duration on, and departure from summer range. Fed elk migrated 19.2 km less, spent 11 more days on stopover sites, arrived to summer range 5 days later, resided on summer range 26 fewer days, and departed in the autumn 10 days earlier than unfed elk. Time-to-event models indicated that differences in migratory behavior between fed and unfed elk were caused by altered sensitivity to the environmental drivers of migration. In spring, unfed elk migrated following plant green-up closely, whereas fed elk departed the feedground but lingered on transitional range, thereby delaying their arrival to summer range. In autumn, fed elk were more responsive to low temperatures and precipitation events, causing earlier departure from summer range than unfed elk. Overall, supplemental feeding disconnected migration by fed elk from spring green-up and decreased time spent on summer range, thereby reducing access to quality forage. Our findings suggest that ungulate migration can be substantially altered by changes to the spatial distribution of resources, including those of anthropogenic origin, and that management practices applied in one season may have unintended behavioral consequences in subsequent seasons.

Inferential consequences of modeling rather than measuring snow accumulation in studies of animal ecology.

It is increasingly common for studies of animal ecology to use model-based predictions of environmental variables as explanatory or predictor variables, even though model prediction uncertainty is typically unknown. To demonstrate the potential for misleading inferences when model predictions with error are used in place of direct measurements, we compared snow water equivalent (SWE) and snow depth as predicted by the Snow Data Assimilation System (SNODAS) to field measurements of SWE and snow depth. We examined locations on elk (Cervus canadensis) winter ranges in western Wyoming, because modeled data such as SNODAS output are often used for inferences on elk ecology. Overall, SNODAS predictions tended to overestimate field measurements, prediction uncertainty was high, and the difference between SNODAS predictions and field measurements was greater in snow shadows for both snow variables compared to non-snow shadow areas. We used a simple simulation of snow effects on the probability of an elk being killed by a predator to show that, if SNODAS prediction uncertainty was ignored, we might have mistakenly concluded that SWE was not an important factor in where elk were killed in predatory attacks during the winter. In this simulation, we were interested in the effects of snow at finer scales (< 1 km2) than the resolution of SNODAS. If bias were to decrease when SNODAS predictions are averaged over coarser scales, SNODAS would be applicable to population-level ecology studies. In our study, however, averaging predictions over moderate to broad spatial scales (9-2200 km2) did not reduce the differences between SNODAS predictions and field measurements. This study highlights the need to carefully evaluate two issues when using model output as an explanatory variable in subsequent analysis: (1) the model's resolution relative to the scale of the ecological question of interest and (2) the implications of prediction uncertainty on inferences when using model predictions as explanatory or predictor variables.

Status of brucellosis in free-ranging elk and bison in Wyoming.

Brucella abortus is the causative agent of brucellosis, a disease enzootic in populations of free-ranging elk (Cervus elaphus) and bison (Bison bison) in the Greater Yellowstone Ecosystem, USA. We define the distribution of the disease in elk throughout Wyoming, USA, using three epidemiologic/geographic classifications based on winter-foraging opportunity. Antibody prevalence for >3,300 yearling and adult, female elk, sampled from supplemental feedgrounds in western Wyoming, USA, since 1985, was 21.9%. Surveillance of nearly 3,800 winter free-ranging, adult, female elk, sampled from herd units adjacent to feedgrounds from 1991 to 2008, indicated a total antibody prevalence of 3.7%. In contrast, none of the 1,930 male and female elk sampled from 1991 to 2008 in herd units distant from feedgrounds in Wyoming, USA, demonstrated exposure to B. abortus. In comparison to elk, bison had a higher incidence of brucellosis. Surveillance of 321 cow bison harvested within the Absaroka and Jackson bison herds in western Wyoming, USA, from 1992 to 2008 yielded an antibody prevalence of 63.9%.

Mapping brucellosis increases relative to elk density using hierarchical Bayesian models.

The relationship between host density and parasite transmission is central to the effectiveness of many disease management strategies. Few studies, however, have empirically estimated this relationship particularly in large mammals. We applied hierarchical Bayesian methods to a 19-year dataset of over 6400 brucellosis tests of adult female elk (Cervus elaphus) in northwestern Wyoming. Management captures that occurred from January to March were over two times more likely to be seropositive than hunted elk that were killed in September to December, while accounting for site and year effects. Areas with supplemental feeding grounds for elk had higher seroprevalence in 1991 than other regions, but by 2009 many areas distant from the feeding grounds were of comparable seroprevalence. The increases in brucellosis seroprevalence were correlated with elk densities at the elk management unit, or hunt area, scale (mean 2070 km(2); range = [95-10237]). The data, however, could not differentiate among linear and non-linear effects of host density. Therefore, control efforts that focus on reducing elk densities at a broad spatial scale were only weakly supported. Additional research on how a few, large groups within a region may be driving disease dynamics is needed for more targeted and effective management interventions. Brucellosis appears to be expanding its range into new regions and elk populations, which is likely to further complicate the United States brucellosis eradication program. This study is an example of how the dynamics of host populations can affect their ability to serve as disease reservoirs.

Effects of management, behavior, and scavenging on risk of brucellosis transmission in elk of western Wyoming.

Brucellosis is endemic in elk (Cervus elaphus nelsoni) using winter feedgrounds of western Wyoming, USA presumably because of increased animal density, duration of attendance, and subsequent contact with aborted fetuses. However, previous research addressed antibody prevalence rather than more direct measures of transmission and did not account for elk behavior or scavenging in transmission risk. Throughout March and early April 2005-07, we monitored 48 sets of culture-negative, pseudoaborted elk fetuses, placentas, and fluids (fetal units, FUs) on one winter free-ranging (WFR) location and four sites (Feedline, High Traffic, Low Traffic, Adjacent) associated with four feedgrounds. "At-risk" elk (total elk within 5 m of FU) and proportions of elk sniffing and contacting FUs were highest on Feedlines and decreased toward Low Traffic sites. We did not observe elk investigating FUs Adjacent to feedgrounds or on the WFR location. At-risk elk on Feedline and High Traffic sites decreased throughout the sampling period, whereas proportions of elk investigating FUs were correlated positively to at-risk elk among all sites within feedgrounds. At-risk elk and proportions of elk investigating FUs were correlated with total feedground elk density and population only on High Traffic and Low Traffic sites. Proportions of sex/age groups (female, juvenile, male) investigating FUs did not differ from background populations. Females, however, spent more time (mean [SE], 21.07 [3.47] sec) investigating FUs than juveniles (14.73 [3.53] sec) and males (10.12 [1.45] sec), with positive correlation between total investigations and time spent investigating per female. Eight species of scavengers consumed FUs, removing FUs faster on feedgrounds than WFR locations and reducing proportions of elk that investigated FUs. Our results suggest that 1) reduction of elk density and time attending feedgrounds, particularly on Feedlines; and 2) protection of scavengers on and adjacent to feedgrounds would likely reduce intraspecific transmission risk of brucellosis.

Effects of management and climate on elk brucellosis in the Greater Yellowstone Ecosystem.

Every winter, government agencies feed approximately 6000 metric tons (6 x 10(6) kg) of hay to elk in the southern Greater Yellowstone Ecosystem (GYE) to limit transmission of Brucella abortus, the causative agent of brucellosis, from elk to cattle. Supplemental feeding, however, is likely to increase the transmission of brucellosis in elk, and may be affected by climatic factors, such as snowpack. We assessed these possibilities using snowpack and feeding data from 1952 to 2006 and disease testing data from 1993 to 2006. Brucellosis seroprevalence was strongly correlated with the timing of the feeding season. Longer feeding seasons were associated with higher seroprevalence, but elk population size and density had only minor effects. In other words, the duration of host aggregation and whether it coincided with peak transmission periods was more important than just the host population size. Accurate modeling of disease transmission depends upon incorporating information on how host contact rates fluctuate over time relative to peak transmission periods. We also found that supplemental feeding seasons lasted longer during years with deeper snowpack. Therefore, milder winters and/or management strategies that reduce the length of the feeding season may reduce the seroprevalence of brucellosis in the elk populations of the southern GYE.