Disease Ecology and Adaptive Management of Brucellosis in Greater Yellowstone Elk

Brucellosis is a bacterial infection that primarily affects livestock and can also be transmitted to humans. In the Greater Yellowstone Ecosystem (GYE), elk (Cervus canadensis) and bison (Bison bison) are habitual carriers of Brucella abortus, which arrived to the region with cattle over a century ago. The disease was eliminated from cattle in the United States through widespread control efforts, but is now periodically transmitted back to cattle on open rangelands where they can come into contact with fetal tissues and fluids from disease-induced abortions that occur among elk during the late winter and spring. In Wyoming, south of Yellowstone National Park, there are 23 supplemental feedgrounds that operate annually and feed the majority of the region’s elk during a portion of the winter. The feedgrounds are controversial because of their association with brucellosis and may be shuttered in the future in part due to the arrival of chronic wasting disease. Using data collected at these feedgrounds, this study investigates the role of winter feedgrounds in the ecology of this host-pathogen relationship: it evaluates the full reproductive costs of the disease to affected elk, how herd demography influences pathogen transmission, and assesses management strategies aimed at reducing pathogen spread among elk. Using blood tests for pregnancy status and brucellosis exposure in female elk, I demonstrated a previously undocumented fertility cost associated with the pathogen which is not due to abortions, but which nearly doubles the estimated fertility cost to affected individuals. I also built mechanistic transmission models using time-series disease and count data from feedgrounds. Within that framework, I assessed various management actions including test-and-slaughter of test-positive elk, which I found to be counterproductive due to rapid recovery times and the protective effects of herd immunity. The overall picture that emerges of winter feedgrounds is one of imperfect practicality driven by social and political consideration, not pathogen control. These results illustrate the underappreciated importance that recruitment and population turnover have on the transmission dynamics of brucellosis in elk, a pathogen which itself flourishes in the reproductive tracts of individual animals and thus impacts vital rates at the population level. Together, this study contributes to the field of disease ecology using a unique long term disease data set of free-ranging wild ungulates

Parsing the Effects of Demography, Climate and Management on Recurrent Brucellosis Outbreaks in Elk

Zoonotic pathogens can harm human health and well‐being directly or by impacting livestock. Pathogens that spillover from wildlife can also impair conservation efforts if humans perceive wildlife as pests. Brucellosis, caused by the bacterium Brucella abortus, circulates in elk and bison herds of the Greater Yellowstone Ecosystem and poses a risk to cattle and humans. Our goal was to understand the relative effects of climatic drivers, host demography and management control programmes on disease dynamics. Using \u3e20 years of serologic, demographic and environmental data on brucellosis in elk, we built stochastic compartmental models to assess the influences of climate forcing, herd immunity, population turnover and management interventions on pathogen transmission. Data were collected at feedgrounds visited in winter by free‐ranging elk in Wyoming, USA. Snowpack, hypothesized as a driver of elk aggregation and thus brucellosis transmission, was strongly correlated across feedgrounds. We expected this variable to drive synchronized disease dynamics across herds. Instead, we demonstrate asynchronous epizootics driven by variation in demographic rates. We evaluated the effectiveness of test‐and‐slaughter of seropositive female elk at two feedgrounds. Test‐and‐slaughter temporarily reduced herd‐level seroprevalence but likely reduced herd immunity while removing few infectious individuals, resulting in subsequent outbreaks once the intervention ceased. We simulated an alternative strategy of removing seronegative female elk and found it would increase herd immunity, yielding fewer infections. We evaluated a second experimental treatment wherein feeding density was reduced at one feedground, but we found no evidence for an effect despite a decade of implementation. Synthesis and applications. Positive serostatus is often weakly correlated with infectiousness but is nevertheless used to make management decisions including lethal removal in wildlife disease systems. We show how this can have adverse consequences whereas efforts that maintain herd immunity can have longer‐term protective effects. Climatic drivers may not result in synchronous disease dynamics across populations unless vital rates are also similar because demographic factors have a large influence on disease patterns

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

Elk female age, brucellosis status, and pregnancy status collected over \u3e20 years at winter feedgrounds in Wyoming

We investigated the impacts of brucellosis (Brucella abortus) on elk (Cervus canadensis) productivity using serological data from over 6000 captures since 1990 in the Greater Yellowstone Ecosystem, USA. Over 1000 of these records included known age and pregnancy status. Using Bayesian multilevel models, we estimated the age-specific pregnancy probabilities of exposed and native 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 native 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 native 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

R code. Function to create a smoother line using generalised additive models. from Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics

This file is called in to other code files and is necessary for the generation of smoothed brucellosis prevalence estimates, including in years for which there is no data

R code for seroprevalence of unfed herds (fig 3) from Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics

Reads in serology data from 3 unfed elk populations and generates a plot illustrating brucellosis prevalence, sample sizes, and trends over time

Test and slaughter serology data. from Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics

This is the serology data used to generate figure 4 in .csv format

R code. Function to create prevalence estimates by location and year. from Winter feeding of elk in the Greater Yellowstone Ecosystem and its effects on disease dynamics

This file is called in to other code files and is necessary for the generation of brucellosis prevalence estimates by site and year (and 95% confidence intervals)