Wildlife Disease Management Research Articles

Early Detection of Wildlife Disease Pathogens Using CRISPR-Cas System Methods.

Wildlife diseases are a considerable threat to human health, conservation, and the economy. Surveillance is a critical component to mitigate the impact of animal diseases in these sectors. To monitor human diseases, CRISPR-Cas (clustered regularly interspaced short palindromic repeats-CRISPR-associated protein) biosensors have proven instrumental as diagnostic tools capable of detecting unique DNA and RNA sequences related to their associated pathogens. However, despite the significant advances in the general development of CRISPR-Cas biosensors, their use to support wildlife disease management is lagging. In some cases, wildlife diseases of concern could be rapidly surveyed using these tools with minimal technical, operational, or cost requirements to end users. This review explores the potential to further leverage this technology to advance wildlife disease monitoring and highlights how concerted standardization of protocols can help to ensure data reliability.

Adaptive interventions for advancing in situ wildlife disease management.

There is a critical need for advancements in disease management strategies for wildlife, but free-living animals pose numerous challenges that can hinder progress. Most disease management attempts involve fixed interventions accompanied by post hoc outcome assessments focused on success or failure. Though these approaches have led to valuable management advances, there are limitations to both the rate of advancement and amount of information that can be gained. As such, strategies that support more rapid progress are required. Sarcoptic mange, caused by epidermal infection with Sarcoptes scabiei mites, is a globally emerging and re-emerging panzootic that exemplifies this problem. The bare-nosed wombat (Vombatus ursinus), a marsupial endemic to southeastern Australia, is impacted by sarcoptic mange throughout its geographic range and enhanced disease management capabilities are needed to improve upon existing in situ methods. We sought to advance in situ wildlife disease management for sarcoptic mange in free-living bare-nosed wombats, implementing an adaptive approach using fluralaner (Bravecto, MSD Animal Health) and a structured process of learning and method-optimisation. By using surveillance of treated wombats to inform real-time management changes, we have demonstrated the efficacy of topically administered fluralaner at 45 and 85 mg/kg against sarcoptic mange. Importantly, we observed variation in the effects of 45 mg/kg doses, but through our adaptive approach found that 85 mg/kg doses consistently reduced mange severity. Through modifying our surveillance program, we also identified individual-level variation in wombat observability and used this to quantify the level of surveillance needed to assess long-term management success. Our adaptive intervention represents the first report of sarcoptic mange management with fluralaner in free-living wildlife and evaluation of its efficacy in situ. This study illustrates how adapting interventions in real time can advance wildlife disease management and may be applicable to accelerating in situ improvements for other host-pathogen systems.

Reframing wildlife disease management problems with decision analysis.

Contemporary wildlife disease management is complex because managers need to respond to a wide range of stakeholders, multiple uncertainties, and difficult trade-offs that characterize the interconnected challenges of today. Despite general acknowledgment of these complexities, managing wildlife disease tends to be framed as a scientific problem, in which the major challenge is lack of knowledge. The complex and multifactorial process of decision-making is collapsed into a scientific endeavor to reduce uncertainty. As a result, contemporary decision-making may be oversimplified, rely on simple heuristics, and fail to account for the broader legal, social, and economic context in which the decisions are made. Concurrently, scientific research on wildlife disease may be distant from this decision context, resulting in information that may not be directly relevant to the pertinent management questions. We propose reframing wildlife disease management challenges as decision problems and addressing them with decision analytical tools to divide the complex problems into more cognitively manageable elements. In particular, structured decision-making has the potential to improve the quality, rigor, and transparency of decisions about wildlife disease in a variety of systems. Examples of management of severe acute respiratory syndrome coronavirus 2, white-nose syndrome, avian influenza, and chytridiomycosis illustrate the most common impediments to decision-making, including competing objectives, risks, prediction uncertainty, and limited resources.

Disease‐smart climate adaptation for wildlife management and conservation

Climate change is a well‐documented driver and threat multiplier of infectious disease in wildlife populations. However, wildlife disease management and climate‐change adaptation have largely operated in isolation. To improve conservation outcomes, we consider the role of climate adaptation in initiating or exacerbating the transmission and spread of wildlife disease and the deleterious effects thereof, as illustrated through several case studies. We offer insights into best practices for disease‐smart adaptation, including a checklist of key factors for assessing disease risks early in the climate adaptation process. By assessing risk, incorporating uncertainty, planning for change, and monitoring outcomes, natural resource managers and conservation practitioners can better prepare for and respond to wildlife disease threats in a changing climate.

Estimating and managing broad risk of chronic wasting disease spillover among cervid species

AbstractThe management of infectious wildlife diseases often involves tackling pathogens that infect multiple host species. Chronic wasting disease (CWD) is a prion disease that can infect most cervid species. CWD was detected in reindeer (Rangifer tarandus) in Norway in 2016. Sympatric populations of red deer (Cervus elaphus) and moose (Alces alces) are at immediate risk. However, the estimation of spillover risk across species and implementation of multispecies management policies are rarely addressed for wildlife. Here, we estimated the broad risk of CWD spillover from reindeer to red deer and moose by quantifying the probability of co‐occurrence based on both (1) population density and (2) habitat niche overlap from GPS data of all three species in Nordfjella, Norway. We describe the practical challenges faced when aiming to reduce the risk of spillover through a marked reduction in the population densities of moose and red deer using recreational hunters. This involves setting the population and harvest aims with uncertain information and how to achieve them. The niche overlap between reindeer and both moose and red deer was low overall but occurred seasonally. Migratory red deer had a moderate niche overlap with the CWD‐infected reindeer population during the calving period, whereas moose had a moderate niche overlap during both calving and winter. Incorporating both habitat overlap and the population densities of the respective species into the quantification of co‐occurrence allowed for more spatially targeted risk maps. An initial aim of a 50% reduction in abundance for the Nordfjella region was set, but only a moderate population decrease of less than 20% from 2016 to 2021 was achieved. Proactive management in the form of marked population reduction is invasive and unpopular when involving species of high societal value, and targeting efforts to zones with a high risk of spillover to limit adverse impacts and achieve wider societal acceptance is important.

Biodiversity indices and Random Forests reveal the potential for striped skunk (Mephitis mephitis) fecal microbial communities to function as a biomarker for oral rabies vaccination.

Wildlife disease surveillance and monitoring poses unique challenges when assessing rates of population vaccination, immunity, or infection prevalence. Non-invasively detected biomarkers can help reduce risk to both animal and field personnel during wildlife disease management activities. In this study, we investigated the utility of fecal microbiome data collected from captive striped skunks (Mephitis mephitis) in predicting rabies virus vaccination and infection status. We sequenced the hypervariable region 4 (V4) of the bacterial 16S gene and estimated alpha and beta diversity across timepoints in three groups of skunks: vaccination then rabies virus infection, sham vaccination then rabies virus infection, and rabies virus infected without vaccination. Alpha diversity did not differ among treatment groups but beta diversity between treatments was statistically significant. The phyla Firmicutes and Proteobacteria were dominant among all samples. Using Random Forests, we identified operational taxonomic units (OTUs) that greatly influenced classification of fecal samples into treatment groups. Each of these OTUs was correlated with fecal volatile organic compounds detected from the samples for companion treatment groups in another study. This research is the first to highlight striped skunk microbiome biodiversity as a vaccination biomarker which pushes the frontier on alternative methods for surveillance and monitoring of vaccination and disease in wildlife populations.

An epidemiological framework for chronic wasting disease in multihost communities

Abstract Many pathogens can infect several host species, which complicates the management of wildlife diseases. Even for generalist pathogens, hosts are not equally competent, and variable niche overlap between hosts leads to different exposure levels within hosts when compared with that between hosts. Hence, the processes determining spillover risk and the subsequent transmission dynamics within and between species differ. Chronic wasting disease (CWD) is a contagious prion disease of the cervids detected across expanded geographic ranges over the last few decades. Multihost management has become topical with CWD detection among reindeer Rangifer tarandus in Europe, with an immediate spillover risk to sympatric species. Here, I argue for the use of a community epidemiological framework that distinguishes between‐ and within‐host dynamics arising from host competence and exposure processes. In CWD, host competence is mainly determined by how variants of the prion protein gene (PRNP) affect susceptibility. The exposure level is not only linked to the density of infected and susceptible hosts both within and between species but also to the spatiotemporal niche overlap between species and social organization within species. Mule deer Odocoileus hemionus and white‐tailed deer Odocoileus virginianus are highly susceptible and expected to show true multihost dynamics; however, mule deer have a higher CWD prevalence in sympatric areas, indicating only partially linked dynamics. Moose Alces alces are highly susceptible, but cases of CWD‐infected moose are few and appear to be spillover events with subsequent epidemic die outs. Elk Cervus canadensis have less susceptible PRNP variants and low levels of prion shedding in lymphoid tissues, indicating lower contagiousness. CWD prevalence in elk is lower and appears to result from spillover and subsequent within‐species emergence, which is partially independent of sympatric deer. Synthesis and applications. Stronger awareness of the different expected CWD dynamics within and between species may facilitate effective surveillance and management. Surveillance should consider the potential lack of linked dynamics between species when designing sampling. Multihost management can target niche overlap at different scales to limit spillover risk: (1) geographic distribution ranges, (2) density reductions in overlap zones and (3) co‐use of transmission hot spots.

Drone-Based Thermal Imaging in the Detection of Wildlife Carcasses and Disease Management

Because animal carcasses often serve as reservoirs for pathogens, their location and removal are crucial in controlling the spread of diseases. During carcass decomposition, heat is emitted due to microbial activity and the development of maggots. Recent studies have shown that infrared sensors can be used to locate animal carcasses, but little is known about the factors influencing detection success. In this study, we investigated the potential of infrared technology to locate wild boar carcasses, as they play an important role in the spread of African swine fever. Specifically, we tested the effects of environmental and carcass conditions on the detection probability. A drone-based thermal camera was used to collect data during 379 flyovers of 42 wild boar carcasses in different stages of decomposition between September 2020 and July 2021. Generalized mixed-effect models and conditional inference trees were used to identify the environmental and carcass conditions that influenced the detection probability. Our results showed that the thermal camera accurately measured carcass temperature (R2 = 0.75, RMSE = 5.89°C). The probability of finding carcasses was higher in open habitats with air temperatures >3.0°C and thus conducive to maggot development (detection rate ≤80%). A forest canopy openness >29.3% and cloudy conditions or flights at dawn increased the detection rate. Moreover, carcasses infested with large amounts of maggots could be detected even in habitats with a more extensive canopy cover, whereas in dense forests, the detection probability was limited (<25%). Carcasses in an advanced stage of decomposition could still be detected as long as the difference between the carcass temperature and the air temperature was >6.4°C (≤62%). Our study demonstrates the utility of thermal imaging in searching for wild boar carcasses under specific environmental and carcass conditions and thus its use in supporting ground searches.

Editorial: Welcome to Wildlife Letters

Editorial: Welcome to <i>Wildlife Letters</i>

Legitimacy and Wildlife Disease: Should Chronic Wasting Disease be Managed without Government?

Natural resource institutions have embraced a deliberative turn to improve how they solve management problems and promote peacebuilding with and among stakeholders. However, actors who would rather not help decide, understand, evaluate, or implement decisions, or, at least not be dictated to in that regard, pose challenges to democratic governance arrangements. Such an inclination can be prevalent among landowner segments and befuddle efforts to safeguard state trust resources such as wildlife. Specifically, landowners’ decision to self-govern can be problematic for wildlife disease management because voluntarism is critical to curbing the negative effects of disease. Researchers suggest that different types of legitimacy play an important role in explaining obedience, interest, or realized engagement or collaboration. We studied which types of legitimacy drive Texas landowners living in the midst of the deadly and highly infectious chronic wasting disease (CWD) to disengage with state-led disease governance that aims to protect deer, elk, and moose populations. Our survey of 481 landowners revealed that a pathway towards landowner willingness to engage CWD management in Texas requires top-down and bottom-up alignment with conceptions of ideological and consequential legitimacy. Given the results of our study, an evolution in contemporary CWD governance would require elements of both socially constructed instrumentally- and value-rational norms (i.e., CWD management in the right way and for the right reasons) to carve a space for political legitimacy at different levels, with aims of rendering voluntarism to benefit the common good culturally normative.

Spatial and temporal responses to incentives: An application to wildlife disease management

When participating in recreation individuals decide on where to go (locations) and when to participate (which time periods), and they respond to changes in external factors (e.g., environmental quality changes, provision of incentives). In examining economic decision-making, economists focus mostly on location choices, thus the behavioral and welfare impacts of the incentives associated with time choices are largely unknown. In this paper, we develop and estimate a flexible econometric model that combines spatial and temporal choices. The model is applied to examine individuals’ location and time choices of their recreation trips in response to extended recreation seasons that are proposed to encourage hunting for wildlife disease management. The data are from an online revealed and stated preference survey of recreational hunters in Alberta, Canada. We find that individuals substitute activities spatially and temporally, take more hunting trips, and gain welfare benefits when they can more flexibly choose the time of activities. Our findings show that increases in time flexibility can be used as an incentive to encourage beneficial outcomes.

Engaging stakeholders in wildlife disease management: Hunters' willingness to adopt and support biosecurity actions to prevent the spread of rabbit hemorrhagic disease

AbstractRabbit hemorrhagic disease virus 2 (RHDV2) is a highly contagious virus that primarily infects rabbits and hares (lagomorphs) and poses a serious threat to lagomorph populations and hunting. Wildlife agencies in the United States rely on hunters to report RHDV2‐related mortalities and engage in voluntary biosecurity actions to prevent the spread of RHDV2. From April 2021 to April 2022, we conducted a nationwide survey of 22,511 hunters to ascertain their willingness to engage in voluntary biosecurity actions and support government‐mandated biosecurity measures. Respondents expressed greatest willingness to report suspicious lagomorph deaths to wildlife agencies. Respondents' willingness to engage in or support biosecurity actions was positively correlated with their risk perceptions pertaining to lagomorph deaths and the economic impacts of RHDV2, perceptions of the importance of biosecurity, and trust in state agencies to manage RHDV2. We found evidence that respondents' willingness to engage in or support biosecurity actions was also positively correlated with their knowledge of RHDV2. Wildlife agencies should clearly communicate about RHDV2 and its adverse impacts on lagomorphs, biodiversity, and hunting to engage hunters in biosecurity measures. Hunters can provide valuable information about lagomorph population trends and mortality events in the areas they hunt, a cost‐effective method to augment agency surveillance.

Habitat connectivity and host relatedness influence virus spread across an urbanising landscape in a fragmentation-sensitive carnivore.

Spatially heterogeneous landscape factors such as urbanisation can have substantial effects on the severity and spread of wildlife diseases. However, research linking patterns of pathogen transmission to landscape features remains rare. Using a combination of phylogeographic and machine learning approaches, we tested the influence of landscape and host factors on feline immunodeficiency virus (FIVLru) genetic variation and spread among bobcats (Lynx rufus) sampled from coastal southern California. We found evidence for increased rates of FIVLru lineage spread through areas of higher vegetation density. Furthermore, single-nucleotide polymorphism (SNP) variation among FIVLru sequences was associated with host genetic distances and geographic location, with FIVLru genetic discontinuities precisely correlating with known urban barriers to host dispersal. An effect of forest land cover on FIVLru SNP variation was likely attributable to host population structure and differences in forest land cover between different populations. Taken together, these results suggest that the spread of FIVLru is constrained by large-scale urban barriers to host movement. Although urbanisation at fine spatial scales did not appear to directly influence virus transmission or spread, we found evidence that viruses transmit and spread more quickly through areas containing higher proportions of natural habitat. These multiple lines of evidence demonstrate how urbanisation can change patterns of contact-dependent pathogen transmission and provide insights into how continued urban development may influence the incidence and management of wildlife disease.

Model Integrated Disease Management to facilitate effective translatable solutions for wildlife disease issues

Abstract There are multiple demands for the development of effective and sustainable disease management practices in wildlife, but solutions are widely lacking. In this perspective, we focus on the need to structure research to support advancement toward enhanced wildlife disease control solutions. We concentrate on the need for improved integration between wildlife disease management undertaken in situ with modelling to guide and assess disease management actions. We recognise that many disease management attempts in wildlife are made in isolation, are not supported by modelling and are not used as a stepping stone to advancement. However, we emphasise that the development of disease control practices in wildlife is greater than any one management attempt, and should be seen and undertaken as a set of systematic steps towards well‐articulated management goals. We describe modelling of disease management and in situ disease management as two complementary phases of investigation, viewed as a feedback loop to support advancements, and highlight established and less established pathways in this loop. We describe how stakeholders engaged in practical management actions can better engage with modellers, and also the need for more fit‐for‐purpose modelling that captures the on‐ground realities of in situ practice to support advancements. The concepts and approaches described in this perspective are captured within a Model Integrated Disease Management for wildlife framework. We illustrate the framework, concepts and challenges proposed in this perspective using a case study for which we have experience: sarcoptic mange (etiologic agent Sarcoptes scabiei) in bare‐nosed wombats (Vombatus ursinus). Synthesis and applications: Effective and sustainable solutions to critical wildlife diseases are needed. Progress can be improved when disease management is guided through iterative and fit‐for‐purpose integration between modelling and in situ practice. We describe and illustrate a Model Integrated Disease Management for wildlife framework. Moving beyond isolated disease management attempts into a structured process of advancement can help overcome barriers to tackling pathogens threatening wildlife.

Strategies for managing marine disease.

The incidence of emerging infectious diseases (EIDs) has increased in wildlife populations in recent years and is expected to continue to increase with global environmental change. Marine diseases are relatively understudied compared with terrestrial diseases but warrant parallel attention as they can disrupt ecosystems, cause economic loss, and threaten human livelihoods. Although there are many existing tools to combat the direct and indirect consequences of EIDs, these management strategies are often insufficient or ineffective in marine habitats compared with their terrestrial counterparts, often due to fundamental differences between marine and terrestrial systems. Here, we first illustrate how the marine environment and marine organism life histories present challenges and opportunities for wildlife disease management. We then assess the application of common disease management strategies to marine versus terrestrial systems to identify those that may be most effective for marine disease outbreak prevention, response, and recovery. Finally, we recommend multiple actions that will enable more successful management of marine wildlife disease emergencies in the future. These include prioritizing marine disease research and understanding its links to climate change, improving marine ecosystem health, forming better monitoring and response networks, developing marine veterinary medicine programs, and enacting policy that addresses marine and other wildlife diseases. Overall, we encourage a more proactive rather than reactive approach to marine wildlife disease management and emphasize that multidisciplinary collaborations are crucial to managing marine wildlife health.

Residents’ concerns and attitudes regarding wildlife disease management: A case of chronic wasting disease in Tennessee

ABSTRACT Most of the literature on the chronic wasting disease (CWD) has focused on the attitudes of deer hunters. Designing public policies to manage CWD requires an understanding of how other stakeholders (landowners, non-hunting public) perceive the risk and react. By surveying a sample of residents in Tennessee, this study compared the concerns, agency trust, and acceptability of management actions among resident groups segmented based on their proximity to CWD presence, hunter status, and land ownership status. Responses from seven CWD counties and four adjacent counties were generally similar, but notable differences were found between hunters and non-hunters and between landowners and non-landowners. Considering that the cooperation from all stakeholders will be critical for the success of a regional CWD management program, it may be important for wildlife agencies to recognize the heterogeneity in preferences and the sensitivity of proposed actions among stakeholders before implementation and enforcement.

Simulating partial vaccine protection: BCG in badgers

In wildlife disease management there are few diseases for which vaccination is a viable option. The human vaccine BCG has been used for the control of bovine tuberculosis in badgers since 2010 and is expected to increase. Understanding the long-term effects of repeated vaccination campaigns on disease prevalence is vital, but modelling thus far has generally assumed that a vaccine provides perfect protection to a proportion of the population, and that animals exposed to a repeated vaccination have a second independent chance of becoming protected. We held a workshop with experts in the field to obtain consensus over the main pathways for partial protection in the badger, and then simulated these using an established model. The available data supported the possibility that some individuals receive no benefit from the BCG vaccine, others may result in a delayed disease progression and in the remaining animals, vaccine protected the individual from any onward transmission. Simulating these pathways using different levels of overall efficacy demonstrated that partial protection leads to a reduced effect of vaccination, but in all of the identified scenarios it was still possible to eradicate disease in an isolated population with no disease introduction. We also identify those potential vaccination failures that require further investigation to determine which of our proposed pathways is the more likely.

An expert‐elicited approach to inform proactive risk assessments for chronic wasting disease in white‐tailed deer

AbstractOne of the most rational and successful ways to mitigate the effects of wildlife disease is to perform proactive management efforts that can either prevent disease prior to first exposure or detect and eradicate disease prior to its establishment. However, estimating the risk of wildlife disease in new locations is often challenged by a lack of tractable linkages between known or presumed disease hazards and comprehensive risk of introduction and spread. In this study, we present a low‐cost approach that estimated comprehensive risk of chronic wasting disease (CWD) in Michigan, United States, based on the localized knowledge of experts and the use of existing datasets. We controlled for sources of expert bias, avoided group conflict that may challenge qualitative risk assessments, and generated estimates of risk that aligned with known positives and can be used in targeted surveillance and mitigation efforts. We found that 97% of CWD detections fell within high risk counties, with only 3 out of 117 cases (3%) falling in counties at low risk. Furthermore, we found coherence between indirect expert‐elicited risk estimates and direct hazard rankings, suggesting that an indirect approach maximized expert knowledge sharing while controlling for sources of potential bias. Lastly, our approach required limited time commitment from group participants and thus, represented a low‐cost decision‐making approach. Taken together, our study may provide an opportunity to mount proactive wildlife disease management in a way that has often been promoted but rarely accomplished.

Using transcriptomics to predict and visualize disease status in bighorn sheep (Ovis canadensis).

Increasing risk of pathogen spillover coupled with overall declines in wildlife population abundance in the Anthropocene make infectious disease a relevant concern for species conservation worldwide. While emerging molecular tools could improve our diagnostic capabilities and give insight into mechanisms underlying wildlife disease risk, they have rarely been applied in practice. Here, employing a previously reported gene transcription panel of common immune markers to track physiological changes, we present a detailed analysis over the course of both acute and chronic infection in one wildlife species where disease plays a critical role in conservation, bighorn sheep (Ovis canadensis). Differential gene transcription patterns distinguished between infection statuses over the course of acute infection and differential correlation (DC) analyses identified clear changes in gene co-transcription patterns over the early stages of infection, with transcription of four genes-TGFb, AHR, IL1b and MX1-continuing to increase even as transcription of other immune-associated genes waned. In a separate analysis, we considered the capacity of the same gene transcription panel to aid in differentiating between chronically infected animals and animals in other disease states outside of acute disease events (an immediate priority for wildlife management in this system). We found that this transcription panel was capable of accurately identifying chronically infected animals in the test dataset, though additional data will be required to determine how far this ability extends. Taken together, our results showcase the successful proof of concept and breadth of potential utilities that gene transcription might provide to wildlife disease management, from direct insight into mechanisms associated with differential disease response to improved diagnostic capacity in the field.

Targeted strategies for the management of wildlife diseases: the case of brucellosis in Alpine ibex

The management of infectious diseases in wildlife reservoirs is challenging and faces several limitations. However, detailed knowledge of host–pathogen systems often reveal heterogeneity among the hosts’ contribution to transmission. Management strategies targeting specific classes of individuals and/or areas, having a particular role in transmission, could be more effective and more acceptable than population-wide interventions. In the wild population of Alpine ibex (Capra ibex—a protected species) of the Bargy massif (French Alps), females transmit brucellosis (Brucella melitensis) infection in ~90% of cases, and most transmissions occur in the central spatial units (“core area”). Therefore, we expanded an individual-based model, developed in a previous study, to test whether strategies targeting females or the core area, or both, would be more effective. We simulated the relative efficacy of realistic strategies for the studied population, combining test-and-remove (euthanasia of captured animals with seropositive test results) and partial culling of unmarked animals. Targeting females or the core area was more effective than untargeted management options, and strategies targeting both were even more effective. Interestingly, the number of ibex euthanized and culled in targeted strategies were lower than in untargeted ones, thus decreasing the conservation costs while increasing the sanitary benefits. Although there was no silver bullet for the management of brucellosis in the studied population, targeted strategies offered a wide range of promising refinements to classical sanitary measures. We therefore encourage to look for heterogeneity in other wildlife diseases and to evaluate potential strategies for improving management in terms of efficacy but also acceptability.