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Stakeholder attitudes and perspectives on wildlife disease surveillance as a component of a One Health approach in Thailand

Coordinated wildlife disease surveillance (WDS) can help professionals across disciplines effectively safeguard human, animal, and environmental health. The aims of this study were to understand how WDS in Thailand is utilized, valued, and can be improved within a One Health framework. An online questionnaire was distributed to 183 professionals (55.7% response rate) across Thailand working in wildlife, marine animal, livestock, domestic animal, zoo animal, environmental, and public health sectors. Twelve semi-structured interviews with key professionals were then performed. Three-quarters of survey respondents reported using WDS data and information. Sectors agreed upon ranking disease control (76.5% of respondents) as the most beneficial outcome of WDS, while fostering new ideas through collaboration was valued by few participants (2.0%). Accessing data collected by ones own sector was identified as the most challenging (50%) yet least difficult to improve (88.3%). Having legal authority to conduct WDS was the second most frequently identified challenge. Interviewees explained that legal documentation required for crossinstitutional collaborations posed a barrier to efficient communication and use of human resources. Survey respondents identified allocation of human resources (75.5%), adequate budget (71.6%), and having a clear communication system between sectors (71.6%) as highest priority areas for improvement to WDS in Thailand. Authorization from administrative officials and support from local community members were identified as challenges during in-person interviews. Future outreach should be directed towards these groups. As 42.9% of marine health professionals had difficulty knowing whom to contact in other sectors and 28.4% of survey respondents indicated that communication with marine health professionals was not applicable to their work, connecting the marine sector with other sectors may be prioritized. This study identifies priorities for addressing current challenges in the establishment of a general WDS system and information management system in Thailand while presenting a model for such evaluation in other regions.

One Health Newsletter

Bovine tuberculosis management in northwest Minnesota and implications of the Risk Information Seeking and Processing (RISP) model for wildlife disease management

Bovine tuberculosis (bTB) is an infectious, zoonotic disease caused by Mycobacterium bovis that can spread between domestic and wild animals, as well as to humans. The disease is characterized by the progressive development of lesions that compromise the victim's lungs and lymph system. The disease was first identified in northwest Minnesota in both cattle and white-tailed deer ( Odocoileus virginianus ) in 2005. Due to its risks to human and animal health, bTB has numerous implications related to population management, policy outcomes, stakeholder relations, and economic impacts. When dealing with complicated risks, like bTB, individuals often seek out and process information as a method to learn about, and cope, with the risk. We developed a questionnaire that adapted components of the Risk Information Seeking and Processing (RISP) model and surveyed northwest Minnesota deer hunters. Our objectives were to better understand how stakeholders perceive and act on information regarding disease management in wildlife and to understand the utility of the RISP model for such management contexts. We drew a random proportional sample of licensed deer hunters ( n = 2100) from the area affected by bTB and conducted a multi-contact mail survey. We found that 43% of the variability in the information-seeking behaviors of respondents was explained by demographics, hunting importance, personal risk perceptions, attitudes, and subjective norms. However, these results are largely attributable to the factors in the RISP model encompassed by components of the Theory of Planned Behavior (i.e., attitudes, subjective norms, perceived behavioral control, and behavioral intentions). This information can help managers contextualize individuals' perceived risks to better frame communication efforts to address stakeholder concerns and develop best practices for disease communication. While the state of Minnesota is currently considered free of bTB, future outbreaks remain possible in Minnesota and elsewhere. Understanding the key factors in the processes through which deer hunters seek out information pertaining to the disease can help managers collect the data necessary to aid decisions about desired future management outcomes. In addition, testing RISP model performance in applied research improves its future use across a broad spectrum of topics throughout veterinary disease management.

Minnesota

Decision making for mitigating wildlife diseases: From theory to practice for an emerging fungal pathogen of amphibians

Conservation science can be most effective in its decision‐support role when seeking answers to clearly formulated questions of direct management relevance. Emerging wildlife diseases, a driver of global biodiversity loss, illustrate the challenges of performing this role: in spite of considerable research, successful disease mitigation is uncommon. Decision analysis is increasingly advocated to guide mitigation planning, but its application remains rare. Using an integral projection model, we explored potential mitigation actions for avoiding population declines and the ongoing spatial spread of the fungus Batrachochytrium salamandrivorans ( Bsal ). This fungus has recently caused severe amphibian declines in north‐western Europe and currently threatens Palearctic salamander diversity. Available evidence suggests that a Bsal outbreak in a fire salamander ( Salamandra salamandra ) population will lead to its rapid extirpation. Treatments such as antifungals or probiotics would need to effectively interrupt transmission (reduce probability of infection by nearly 90%) in order to reduce the risk of host extirpation and successfully eradicate the pathogen. Improving the survival of infected hosts is most likely to be detrimental as it increases the potential for pathogen transmission and spread. Active removal of a large proportion of the host population has some potential to locally eradicate Bsal and interrupt its spread, depending on the presence of Bsal reservoirs and on the host's spatial dynamics, which should therefore represent research priorities. Synthesis and applications . Mitigation of Batrachochytrium salamandrivorans epidemics in susceptible host species is highly challenging, requiring effective interruption of transmission and radical removal of host individuals. More generally, our study illustrates the advantages of framing conservation science directly in the management decision context, rather than adapting to it a posteriori .

Journal of Applied Ecology

Learning complex spatial dynamics of wildlife diseases with machine learning-guided partial differential equations

Emerging wildlife pathogens often display geographic variability due to landscape heterogeneity. Modeling approaches capable of learning complex, non-linear spatial dynamics of diseases are needed to rigorously assess and mitigate the effects of pathogens on wildlife health and biodiversity. We propose a novel machine learning (ML)-guided approach that leverages prior physical knowledge of ecological systems, using partial differential equations. We present our approach, taking advantage of the universal function approximation property of neural networks for flexible representation of the underlying dynamics of the geographic spread and growth of wildlife diseases. We demonstrate the benefits of our approach by comparing its forecasting power with commonly used methods and highlighting the obtained insights on disease dynamics. Additionally, we show the theoretical guarantees for the approximation error of our model. We illustrate the implementation of our ML-guided approach using data from white-nose syndrome (WNS) outbreaks in bat populations across the US. WNS is an infectious fungal disease responsible for significant declines in bat populations. Our results on WNS are useful for disease surveillance and bat conservation efforts. Our methods can be broadly used to assess the effects of environmental and anthropogenic drivers impacting wildlife health and biodiversity.

Environmental Data Science

Bayesian spatio-temporal survival analysis for all types of censoring with application to a wildlife disease study

In this article, we consider modeling arbitrarily censored survival data with spatio-temporal covariates. We demonstrate that under the piecewise constant hazard function, the likelihood for uncensored or right-censored subjects is proportional to the likelihood of multiple conditionally independent Poisson random variables. To address left- or interval-censored subjects, we propose to impute the exact event times and convert them into uncensored subjects, enabling the application of the integrated nested Laplace approximation to update model parameters using the imputed data. We introduce an iterative algorithm that alternates between imputing event times for left- and interval-censored subjects and re-estimating model parameters. The proposed method is assessed through a simulation study and applied to analyze a spatio-temporal survival dataset in a wildlife disease study investigating bovine tuberculosis in white-tailed deer in Michigan.

Environmetrics

Expanding national-scale wildlife disease surveillance systems with research networks

Efficient learning about disease dynamics in free-ranging wildlife systems can benefit from active surveillance that is standardized across different ecological contexts. For example, active surveillance that targets specific individuals and populations with standardized sampling across ecological contexts (landscape-scale targeted surveillance) is important for developing a mechanistic understanding of disease emergence, which is the foundation for improving risk assessment of zoonotic or wildlife-livestock disease outbreaks and predicting hotspots of disease emergence. However, landscape-scale targeted surveillance systems are rare and challenging to implement. Increasing experience and infrastructure for landscape-scale targeted surveillance will improve readiness for rapid deployment of this type of surveillance in response to new disease emergence events. Here, we describe our experience developing and rapidly deploying a landscape-scale targeted surveillance system for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in two free-ranging deer species across their ranges in the United States. Our surveillance system was designed to collect data across individual, population, and landscape scales for future analyses aimed at understanding mechanisms and risk factors of SARS-CoV-2 transmission, evolution, and persistence. Our approach leveraged partnerships between state and federal public service sectors and academic researchers in a landscape-scale targeted surveillance research network. Methods describe our approach to developing the surveillance network and sampling design. Results report challenges with implementing our intended sampling design, specifically how the design was adapted as different challenges arose and summarize the sampling design that has been implemented thus far. In the discussion, we describe strategies that were important for the successful deployment of landscape-scale targeted surveillance, development and operation of the research network, construction of similar networks in the future, and analytical approaches for the data based on the sampling design.

Ecology and Evolution

Three steps to minimize wildlife disease transmission via construction equipment

Aquatic wildlife can be harmed by viruses, bacteria, fungi, and parasites introduced into wetlands. These infectious pathogens can survive in mud, soil, vegetation, and other debris that collect on the bodies and crevices of drivable equipment. Construction and habitat restoration projects can accidentally transport pathogens from a contaminated aquatic habitat into a healthy one. These three steps can help minimize the spread of pathogens to amphibians, reptiles, and fishes. The information provided in this fact sheet has been extracted from the publication, "Minimizing the Spread of Herpetofaunal Pathogens in Aquatic Habitats by Decontaminating Construction Equipment " (http://northeastparc.org/wp-content/uploads/2021/01/Julian-2020-Decontamination-for-Herps-for-large-equipment.pdf)

Report

Quantitative support for the benefits of proactive management for wildlife disease control

Finding effective pathogen mitigation strategies is one of the biggest challenges humans face today. In the context of wildlife, emerging infectious diseases have repeatedly caused widespread host morbidity and population declines of numerous taxa. In areas yet unaffected by a pathogen, a proactive management approach has the potential to minimize or prevent host mortality. However, typically critical information on disease dynamics in a novel host system is lacking, empirical evidence on efficacy of management interventions is limited, and there is a lack of validated predictive models. As such, quantitative support for identifying effective management interventions is largely absent, and the opportunity for proactive management is often missed. We considered the potential invasion of the chytrid fungus, Batrachochytrium salamandrivorans (Bsal), whose expected emergence in North America poses a severe threat to hundreds of salamander species in this global salamander biodiversity hotspot. We developed and parameterized a dynamic multistate occupancy model to forecast host and pathogen occurrence, following expected emergence of the pathogen, and evaluated the response of salamander populations to different management scenarios. Our model forecasted that taking no action is expected to be catastrophic to salamander populations. Proactive action was predicted to maximize host occupancy outcomes relative to wait-and-see reactive management, thus providing quantitative support for proactive management opportunities. The eradication of Bsal was unlikely under all the evaluated management options. Contrary to our expectations, even early pathogen detection had little effect on Bsal or host occupancy outcomes. Our results provide quantitative support that proactive management is the optimal strategy for promoting persistence of disease-threatened salamander populations. Our approach fills a critical gap by defining a framework for evaluating management options prior to pathogen invasion and can thus serve as a template for addressing novel disease threats that jeopardize wildlife and human health.

Conservation Biology

Development of conjugated secondary antibodies for wildlife disease surveillance

Disease monitoring in free-ranging wildlife is a challenge and often relies on passive surveillance. Alternatively, proactive surveillance that relies on the detection of specific antibodies could give more reliable and timely insight into disease presence and prevalence in a population, especially if the evidence of disease occurs below detection thresholds for passive surveillance. Primary binding assays, like the indirect ELISA for antibody detection in wildlife, are hampered by a lack of species-specific conjugates. In this study, we developed anti-kudu ( Tragelaphus strepsiceros ) and anti-impala ( Aepyceros melampus ) immunoglobulin-specific conjugates in chickens and compared them to the binding of commercially available protein-G and protein-AG conjugates, using an ELISA-based avidity index. The conjugates were evaluated for cross-reaction with sera from other wild herbivores to assess future use in ELISAs. The developed conjugates had a high avidity of >70% against kudu and impala sera. The commercial conjugates (protein-G and protein-AG) had significantly low relative avidity (<20%) against these species. Eighteen other wildlife species demonstrated cross-reactivity with a mean relative avidity of >50% with the impala and kudu conjugates and <40% with the commercial conjugates. These results demonstrate that species-specific conjugates are important tools for the development and validation of immunoassays in wildlife and for the surveillance of zoonotic agents along the livestock-wildlife-human interface.

Frontiers in Immunology

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

PLoS ONE

Wildlife disease and environmental health in Alaska

Environmental health is defined by connections between the physical environment, ecological health, and human health. Current research within the U.S. Geological Survey (USGS) recognizes the importance of this integrated research philosophy, which includes study of disease and pollutants as they pertain to wildlife and humans. Due to its key geographic location and significant wildlife resources, Alaska is a critical area for future study of environmental health.

Alaska

Response to “Prepublication communication of research results”: The need for a coordinated wildlife disease surveillance laboratory network

In “Prepublication Communication of Research Results”, Adams et al. ( 2018 ) outline the importance of timeliness in providing scientific results with consequential implications for wildlife management to responsible government agencies. The authors discuss various impediments to sharing of scientific results and provide well-reasoned arguments why scientists should not fear that sharing these results with wildlife management agencies will preclude their ability to subsequently publish this information in the peer-reviewed literature.

EcoHealth

Batrachochytrium salamandriovrans (Bsal) in Appalachia—Using scenario building to proactively prepare for a wildlife disease outbreak caused by an invasive amphibian chytrid fungus

Batrachochytrium salamandrivorans ( Bsal ), a pathogenic chytrid fungus, is nonnative to the United States and poses a disease threat to vulnerable amphibian hosts. The Bsal fungus may lead to increases in threatened, endangered, and sensitive status listings at State, Tribal, and Federal levels, resulting in financial costs associated with implementing the Endangered Species Act of 1973. The United States is a global biodiversity hotspot for salamanders, an order of amphibians that is particularly vulnerable to developing a disease called chytridiomycosis when exposed to Bsal . Published Bsal risk assessments for North America have suggested that salamanders within the Appalachian region of the United States are at a high risk. In May 2017, a workshop was facilitated by the Department of the Interior’s Strategic Sciences Group. During the workshop, a discussion-based incident-response exercise focused on a hypothetical Bsal disease outbreak in Appalachia was led by U.S. Geological Survey staff members. Participants included representatives of the Eastern Band of the Cherokee Indians, U.S. Fish and Wildlife Service, National Park Service, Appalachian Landscape Conservation Cooperative, Tennessee Wildlife Resources Agency, and U.S. Department of Agriculture’s U.S. Forest Service. Scenario building was used to brainstorm cascading consequences (social, economic, and ecological) of a Bsal disease outbreak in the Appalachian region. This report highlights the management and science actions that could be undertaken to ensure an effective, rapid response to a Bsal introduction into the United States.

Open-File Report

Cognitive and behavioral coping in response to wildlife disease: The case of hunters and chronic wasting disease

The transactional model of stress and coping (TMSC) provides a conceptual framework for understanding adaptations to stressors like chronic wasting disease (CWD). Understanding hunter response to stressors is important because decreased participation and satisfaction can affect individual well-being, cultural traditions, agency revenue, and local economies. Using TMSC, we explored how deer hunters coped with CWD. We also compared involvement, and impacts and emotions related to CWD, inside and outside a CWD management zone. Then we examined coping related to CWD presence, and if the disease affected human health. Most hunters would cope using product shift (i.e., eating meat after a negative test result) rather than displacement (i.e., hunting elsewhere) or dropout. Hunters who may be displaced reported lower involvement in deer hunting, and increased worry about CWD. Results suggest that CWD information and testing may increase hunter worry. Funding expanded testing without prompting displacement or dropout are important management considerations.

Minnesota

Utilizing hunter harvest effort to survey for wildlife disease: a case study of West Nile virus in greater sage-grouse

Greater sage-grouse ( Centrocercus urophasianus ; sage-grouse) are highly susceptible to infection with West Nile virus (WNV), with substantial mortality reported in wild populations and in experimentally infected birds. Although sage-grouse are hunted throughout much of their range, they have also recently been considered for protection under the Endangered Species Act. We used blood samples collected on filter-paper strips during the 2006&ndash;2010 Oregon, USA, annual sage-grouse hunt to survey for specific WNV-neutralizing antibodies that indicate a previous infection with WNV. During this period, hunters submitted 1,880 blood samples from sage-grouse they harvested. Samples obtained were proportional for all 12 Oregon sage-grouse hunting units. Laboratory testing of 1,839 samples by the WNV epitope-blocking enzyme-linked immunosorbent assay (bELISA) followed by plaque reduction neutralization test on bELISA-positive samples yielded 19 (1%) and 1 (0.05%) positive samples, respectively. These data provided early baseline information for future comparisons regarding the prevalence of WNV-specific neutralizing antibodies in sage-grouse in Oregon. This methodology may provide other states where sage-grouse (or other species) populations are hunted and where WNV constitutes a species conservation concern with a viable option to track the relative prevalence of the virus in populations.

Oregon

Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea)

Native Hawaiian forest birds are facing a major extinction crisis with more than 75% of species recorded in historical times either extinct or endangered. Reasons for this catastrophe include habitat destruction, competition with non-native species, and introduction of predators and avian diseases. We tested susceptibility of Iiwi (Vestiaria coccinea), a declining native species, and Nutmeg Mannikins (Lonchura punctulata), a common non-native species, to an isolate of Plasmodium relictum from the island of Hawaii. Food consumption, weight, and parasitaemia were monitored in juvenile Iiwi that were infected by either single (low-dose) or multiple (high-dose) mosquito bites. Mortality in both groups was significantly higher than in uninfected controls, reaching 100% of high-dose birds and 90% of low-dose birds. Significant declines in food consumption and a corresponding loss of body weight occurred in malaria-infected birds. Both sex and body weight had significant effects on survival time, with males more susceptible than females and birds with low initial weights more susceptible than those with higher initial weights. Gross and microscopic lesions in malaria fatalities included massive enlargement of the spleen and liver, hyperplasia of the reticuloendothelial system with extensive deposition of malarial pigment, and overwhelming anaemia in which over 30% of the circulating erythrocytes were parasitized. Nutmeg Mannikins, by contrast, were completely refractory to infection. Our findings support previous studies documenting high susceptibility of native Hawaiian forest birds to avian malaria. This disease continues to threaten remaining high elevation populations of endangered native birds.

Hawai'i

Sex-biased infections scale to population impacts for an emerging wildlife disease

Demographic factors are fundamental in shaping infectious disease dynamics. Aspects of populations that create structure, like age and sex, can affect patterns of transmission, infection intensity and population outcomes. However, studies rarely link these processes from individual to population-scale effects. Moreover, the mechanisms underlying demographic differences in disease are frequently unclear. Here, we explore sex-biased infections for a multi-host fungal disease of bats, white-nose syndrome, and link disease-associated mortality between sexes, the distortion of sex ratios and the potential mechanisms underlying sex differences in infection. We collected data on host traits, infection intensity and survival of five bat species at 42 sites across seven years. We found females were more infected than males for all five species. Females also had lower apparent survival over winter and accounted for a smaller proportion of populations over time. Notably, female-biased infections were evident by early hibernation and likely driven by sex-based differences in autumn mating behaviour. Male bats were more active during autumn which likely reduced replication of the cool-growing fungus. Higher disease impacts in female bats may have cascading effects on bat populations beyond the hibernation season by limiting recruitment and increasing the risk of Allee effects.

Proceedings of the Royal Society B: Biological Sci