Christopher S. Jennelle

STATE-SPECIFIC DETECTION PROBABILITIES AND DISEASE PREVALENCE

Investigations of disease dynamics in wild animal populations often use estimated prevalence or incidence as a measure of true disease frequency. Such indices, almost always based solely on raw counts of infected and uninfected individuals, are often used as the basis for analysis of temporal and spatial dynamics of diseases. Generally, such studies do not account for potential differences in observer detection probabilities of host individuals stratified by biotic and/or abiotic factors. We demonstrate the potential effects of heterogeneity in state-specific detection probabilities on estimated disease prevalence using mark-recapture data from previous work in a House Finch (Carpodacus mexicanus) and Mycoplasma gallisepticum system. In this system, detection probabilities of uninfected finches were generally higher than infected individuals. We show that the magnitude and seasonal pattern of variation in estimated prevalence, corrected for differences in detection probabilities, differed markedly from uncorrected (apparent) prevalence. When the detection probability of uninfected individuals is higher than infected individuals (as in our study), apparent prevalence is negatively biased, and vice versa. In situations where state-specific detection probabilities strongly interact over time, we show that the magnitude and pattern of apparent prevalence can change dramatically; in such cases, observed variations in prevalence may be completely spurious artifacts of variation in detection probability, rather than changes in underlying disease dynamics. Accounting for differential detection probabilities in estimates of disease frequency removes a potentially confounding factor in studies seeking to identify biotic and/or abiotic drivers of disease dynamics. Given that detection probabilities of different groups of individuals are likely to change temporally and spatially in most field studies, our results underscore the importance of estimating and incorporating detection probabilities in estimated disease prevalence (specifically), and more generally, any ecological index used to estimate some parameter of interest. While a mark-recapture approach makes it possible to estimate detection probabilities, it is not always practical, especially at large scales. We discuss several alternative approaches and categorize the assumptions under which analysis of uncorrected prevalence may be acceptable.

Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites.

Ever since Mycoplasma gallisepticum emerged among house finches in North America, it has been suggested that bird aggregations at feeders are an important cause of the epidemic of mycoplasmal conjunctivitis because diseased birds could deposit droplets of pathogen onto the feeders and thereby promote indirect transmission by fomites. In this paper we bring the first experimental evidence that such transmission (bird-to-feeder-to-bird) does actually take place. House finches infected via this route, however, developed only mild disease and recovered much more rapidly than birds infected from the same source birds but directly into the conjunctiva. While it is certainly probable that house finch aggregations at artificial feeders enhance pathogen transmission, to some degree transmission of M. gallisepticum by fomites may serve to immunize birds against developing more severe infections. Some such birds develop M. gallisepticum antibodies, providing indication of an immune response, although no direct evidence of protection.

Deer Carcass Decomposition and Potential Scavenger Exposure to Chronic Wasting Disease

Abstract Chronic wasting disease (CWD) is a transmissible spongiform encephalopathy afflicting the Cervidae family in North America, causing neurodegeneration and ultimately death. Although there are no reports of natural cross-species transmission of CWD to noncervids, infected deer carcasses pose a potential risk of CWD exposure for other animals. We placed 40 disease-free white-tailed deer (Odocoileus virginianus) carcasses and 10 gut piles in the CWD-affected area of Wisconsin (USA) from September to April in 2003 through 2005. We used photos from remotely operated cameras to characterize scavenger visitation and relative activity. To evaluate factors driving the rate of carcass removal (decomposition), we used Kaplan–Meier survival analysis and a generalized linear mixed model. We recorded 14 species of scavenging mammals (6 visiting species) and 14 species of scavenging birds (8 visiting species). Prominent scavengers included American crows (Corvus brachyrhynchos), raccoons (Procyon lotor), and Virginia opossums (Didelphis virginiana). We found no evidence that deer consumed conspecific remains, although they visited gut piles more often than carcasses relative to temporal availability in the environment. Domestic dogs, cats, and cows either scavenged or visited carcass sites, which could lead to human exposure to CWD. Deer carcasses persisted for 18 days to 101 days depending on the season and year, whereas gut piles lasted for 3 days. Habitat did not influence carcass decomposition, but mammalian and avian scavenger activity and higher temperatures were positively associated with faster removal. Infected deer carcasses or gut piles can serve as potential sources of CWD prions to a variety of scavengers. In areas where surveillance for CWD exposure is practical, management agencies should consider strategies for testing primary scavengers of deer carcass material.

Characterization of Experimental Mycoplasma gallisepticum Infection in Captive House Finch Flocks

Abstract The use of controlled, horizontal-transmission experiments provides detailed information on the spread of disease within fixed social groups, which informs our understanding of disease dynamics both in an empirical and theoretical context. For that reason, we characterized in 2002, horizontal transmission of Mycoplasma gallisepticum (MG) in two flocks of 11 wild-caught house finches housed in outdoor aviaries over a 6-mo period. All birds were initially free of MG by a polymerase chain reaction (PCR)-based test, rapid plate agglutination (RPA), and the scoring of physical signs. We inoculated one flock member bilaterally in the palpebral conjunctiva and reintroduced it into its cage. Index birds developed conjunctivitis within 3 to 5 days but died 13 and 20 days postinfection (PI) possibly because of very severe weather. The proportion of birds with physical signs increased gradually, reached 40% at 6 wk PI, and fluctuated around 40% until 21 wk PI. By the time our experiment ended at 24.5 wk PI, 28% of the birds still exhibited physical signs. Across both flocks, 80% of the birds developed unilateral or bilateral conjunctivitis, and several birds relapsed. The appearance of physical signs in new individuals occurred between 10 and 144 days PI (median 41 days PI). Physical signs lasted 1–172 days (median 42 days). Birds that became infected earlier during the experiment developed more severe conjunctivitis, and there was a tendency for birds that developed bilateral conjunctivitis to develop physical signs earlier. Most birds that developed physical signs of MG were also PCR- and RPA-positive, although we detected a single asymptomatic carrier and a single symptomatic false negative. No birds died as a result of secondary MG infection.

Transmission of Chronic Wasting Disease in Wisconsin White-Tailed Deer: Implications for Disease Spread and Management

Few studies have evaluated the rate of infection or mode of transmission for wildlife diseases, and the implications of alternative management strategies. We used hunter harvest data from 2002 to 2013 to investigate chronic wasting disease (CWD) infection rate and transmission modes, and address how alternative management approaches affect disease dynamics in a Wisconsin white-tailed deer population. Uncertainty regarding demographic impacts of CWD on cervid populations, human and domestic animal health concerns, and potential economic consequences underscore the need for strategies to control CWD distribution and prevalence. Using maximum-likelihood methods to evaluate alternative multi-state deterministic models of CWD transmission, harvest data strongly supports a frequency-dependent transmission structure with sex-specific infection rates that are two times higher in males than females. As transmissible spongiform encephalopathies are an important and difficult-to-study class of diseases with major economic and ecological implications, our work supports the hypothesis of frequency-dependent transmission in wild deer at a broad spatial scale and indicates that effective harvest management can be implemented to control CWD prevalence. Specifically, we show that harvest focused on the greater-affected sex (males) can result in stable population dynamics and control of CWD within the next 50 years, given the constraints of the model. We also provide a quantitative estimate of geographic disease spread in southern Wisconsin, validating qualitative assessments that CWD spreads relatively slowly. Given increased discovery and distribution of CWD throughout North America, insights from our study are valuable to management agencies and to the general public concerned about the impacts of CWD on white-tailed deer populations.

Surveillance for transmissible spongiform encephalopathy in scavengers of white-tailed deer carcasses in the chronic wasting disease area of Wisconsin.

Chronic wasting disease (CWD), a class of neurodegenerative transmissible spongiform encephalopathies (TSE) occurring in cervids, is found in a number of states and provinces across North America. Misfolded prions, the infectious agents of CWD, are deposited in the environment via carcass remains and excreta, and pose a threat of cross-species transmission. In this study tissues were tested from 812 representative mammalian scavengers, collected in the CWD-affected area of Wisconsin, for TSE infection using the IDEXX HerdChek enzyme-linked immunosorbent assay (ELISA). Only four of the collected mammals tested positive using the ELISA, but these were negative when tested by Western blot. While our sample sizes permitted high probabilities of detecting TSE assuming 1% population prevalence in several common scavengers (93%, 87%, and 87% for raccoons, opossums, and coyotes, respectively), insufficient sample sizes for other species precluded similar conclusions. One cannot rule out successful cross-species TSE transmission to scavengers, but the results suggest that such transmission is not frequent in the CWD-affected area of Wisconsin. The need for further surveillance of scavenger species, especially those known to be susceptible to TSE (e.g., cat, American mink, raccoon), is highlighted in both a field and laboratory setting.

Using Auxiliary Information to Improve Wildlife Disease Surveillance When Infected Animals Are Not Detected: A Bayesian Approach

There are numerous situations in which it is important to determine whether a particular disease of interest is present in a free-ranging wildlife population. However adequate disease surveillance can be labor-intensive and expensive and thus there is substantial motivation to conduct it as efficiently as possible. Surveillance is often based on the assumption of a simple random sample, but this can almost always be improved upon if there is auxiliary information available about disease risk factors. We present a Bayesian approach to disease surveillance when auxiliary risk information is available which will usually allow for substantial improvements over simple random sampling. Others have employed risk weights in surveillance, but this can result in overly optimistic statements regarding freedom from disease due to not accounting for the uncertainty in the auxiliary information; our approach remedies this. We compare our Bayesian approach to a published example of risk weights applied to chronic wasting disease in deer in Colorado, and we also present calculations to examine when uncertainty in the auxiliary information has a serious impact on the risk weights approach. Our approach allows “apples-to-apples” comparisons of surveillance efficiencies between units where heterogeneous samples were collected.

Bird Mortality at a Wind-Energy Facility Near a Wetland of International Importance

Abstract. Wind turbines provide a source of renewable energy to meet increasing human demand and offset the costs of fossil fuel usage and nuclear power generation. Birds are killed and displaced at wind facilities, so increased understanding of the drivers of mortality and displacement will assist planners considering the future placement and use of wind facilities. Our objectives were to assess the effect on birds of a wind facility in southeastern Wisconsin by (1) recording the species composition of recovered bird carcasses, (2) estimating mortality rates, and (3) identifying variables correlated with fatalities. We found 20 bird carcasses during scheduled searches. On this basis, we estimated that over two springs and two autumns of study from 2008 to 2010, 607 birds (0.026 per turbine per day, 0.017 per megawatt per day) were killed over 277 days of searching at this facility containing 86 turbines. Nocturnally migrating passerines accounted for 50% of the birds found killed. We found a significant negative relationship between bird fatalities and northward movement of birds through the wind facility. Despite the close proximity of Horicon Marsh National Wildlife Refuge, a wetland of international importance, we found no relationship between distance to Horicon Marsh and bird fatalities. Our study provides a timely assessment of fatal bird collisions with turbines at a wind facility in agricultural lands, uniquely located near a large wetland at which migrating birds stage.

Regional Analysis of Wind Turbine-Caused Bat Mortality

Wind energy has been the fastest-growing renewable energy source in the world. Studies have estimated bat fatalities at wind facilities, but direct comparisons of results is difficult and can be misleading due to numerous differences in protocols and methods used. We had a unique opportunity to compare fatality estimates from three wind facilities in southeastern Wisconsin. These three facilities are located within two neighboring counties with similar land use and land cover, used similar post-construction study methodologies, have turbine models that are close in size and nameplate capacity, and all became operational within seven months of each other. Our objectives were to analyze bat mortality data across all three wind facilities to: 1) examine species composition; and 2) investigate whether select structural, habitat, and landscape features influence mortality at a fine and broad scale. Corrected estimates of bat mortality were higher than reported in most other previous research in Midwestern agricultural lands in the United States. Similarities within the data were shared by all three wind facilities, but differences across them included species composition of bat mortalities and raw and corrected number of bat carcasses recovered. Our analysis suggested that select habitat and landscape features were among the predictor variables that explained bat mortality at the broad scale. Given heterogeneity in mortality estimates within the upper Midwest region, we recommend that individual wind facilities conduct project-specific pre- and postconstruction monitoring rather than infer mortality effects based on published results from other wind facilities.