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.

Replanteamiento del manejo de problemas por enfermedades de fauna mediante el análisis de decisiones Resumen El manejo actual de las enfermedades de la fauna es complejo debido a que los gestores necesitan responder a una amplia gama de actores, varias incertidumbres y compensaciones difíciles que caracterizan los retos interconectados del día de hoy. A pesar de que en general se reconocen estas complejidades, el manejo de las enfermedades tiende a plantearse como un problema científico en el que el principal obstáculo es la falta de conocimiento. El proceso complejo y multifactorial de la toma decisiones está colapsado dentro de un esfuerzo científico para reducir la incertidumbre. Como resultado de esto, las decisiones contemporáneas pueden estar simplificadas en exceso, depender de métodos heurísticos simples y no considerar el contexto legal, social y económico más amplio en el que se toman las decisiones. De manera paralela, las investigaciones científicas sobre las enfermedades de la fauna pueden estar lejos de este contexto de decisiones, lo que deriva en información que puede no ser directamente relevante para las preguntas pertinentes de manejo. Proponemos replantear los obstáculos para el manejo de enfermedades de fauna como problemas de decisión y abordarlos con herramientas analíticas de decisión para dividir los problemas complejos en elementos más manejables de manera cognitiva. En particular, las decisiones estructuradas tienen el potencial de mejorar la calidad, el rigor y la transparencia de las decisiones sobre las enfermedades de la fauna en una variedad de sistemas. Ejemplos como el manejo del coronavirus del síndrome de respiración agudo tipo 2, el síndrome de nariz blanca, la influenza aviar y la quitridiomicosis ilustran los impedimentos más comunes para la toma de decisiones, incluyendo los objetivos en competencia, riesgos, incertidumbre en las predicciones y recursos limitados.

Resolution of Clinical Signs of Sarcoptic Mange in American Black Bears (Ursus americanus), in Ivermectin-Treated and Nontreated Individuals.

The parasitic mite Sarcoptes scabiei causes mange in nearly 150 species of mammals by burrowing under the skin, triggering hypersensitivity responses that can alter animals' behavior and result in extreme weight loss, secondary infections, and even death. Since the 1990s, sarcoptic mange has increased in incidence and geographic distribution in Pennsylvania black bear (Ursus americanus) populations, including expansion into other states. Recovery from mange in free-ranging wildlife has rarely been evaluated. Following the Pennsylvania Game Commission's standard operating procedures at the time of the study, treatment consisted of one subcutaneous injection of ivermectin. To evaluate black bear survival and recovery from mange, from 2018 to 2020 we fitted 61 bears, including 43 with mange, with GPS collars to track their movements and recovery. Bears were collared in triplicates according to sex and habitat, consisting of one bear without mange (healthy control), one scabietic bear treated with ivermectin when collared, and one untreated scabietic bear. Bears were reevaluated for signs of mange during annual den visits, if recaptured during the study period, and after mortality events. Disease status and recovery from mange was determined based on outward gross appearance and presence of S. scabiei mites from skin scrapes. Of the 36 scabietic bears with known recovery status, 81% fully recovered regardless of treatment, with 88% recovered with treatment and 74% recovered without treatment. All bears with no, low, or moderate mite burdens (<16 mites on skin scrapes) fully recovered from mange (n=20), and nearly half of bears with severe mite burden (≥16 mites) fully recovered (n=5, 42%). However, nonrecovered status did not indicate mortality, and mange-related mortality was infrequent. Most bears were able to recover from mange irrespective of treatment, potentially indicating a need for reevaluation of the mange wildlife management paradigm.

Zoonotic implications of white-footed mice habitat selection and territoriality in fragmented landscapes.

White-footed mouse (Peromyscus leucopus) populations can thrive in fragmented suburban and urban parks and residential spaces and play a pivotal role in the spread and prevalence of tick-borne diseases. We collected spatial data on 58 individual mice living at the intersection of county park land and residential land in suburban Howard County, MD, U.S.A. We analyzed mouse density, home-range size and overlap, and a Bayesian mixed-effects model to identify the habitats where they were found relative to where they were caught, as well as a resource selection function for general habitat use. We found that as mouse density increased, home-range size decreased. The overlap indices and the resource selection function supported territoriality coupled with site-specific space use in these suburban mouse populations. While mice occurred in open areas, forest edge, and forest, they showed a strong preference for forested areas. Interestingly, mice captured only 30 to 40 m into the forest rarely used the nearby private yards or human structures and this has direct implications for the placement of rodent-targeted tick control treatments. Our study supports the need for zoonotic disease management frameworks that are based on site-specific land cover characteristics as well as specific management objectives.

Waterfowl show spatiotemporal trends in influenza A H5 and H7 infections but limited taxonomic variation.

Influenza A viruses in wild birds pose threats to the poultry industry, wild birds, and human health under certain conditions. Of particular importance are wild waterfowl, which are the primary reservoir of low-pathogenicity influenza viruses that ultimately cause high-pathogenicity outbreaks in poultry farms. Despite much work on the drivers of influenza A virus prevalence, the underlying viral subtype dynamics are still mostly unexplored. Nevertheless, understanding these dynamics, particularly for the agriculturally significant H5 and H7 subtypes, is important for mitigating the risk of outbreaks in domestic poultry farms. Here, using an expansive surveillance database, we take a large-scale look at the spatial, temporal, and taxonomic drivers in the prevalence of these two subtypes among influenza A-positive wild waterfowl. We document spatiotemporal trends that are consistent with past work, particularly an uptick in H5 viruses in late autumn and H7 viruses in spring. Interestingly, despite large species differences in temporal trends in overall influenza A virus prevalence, we document only modest differences in the relative abundance of these two subtypes and little, if any, temporal differences among species. As such, it appears that differences in species' phenology, physiology, and behaviors that influence overall susceptibility to influenza A viruses play a much lesser role in relative susceptibility to different subtypes. Instead, species are likely to freely pass viruses among each other regardless of subtype. Importantly, despite the similarities among species documented here, individual species still may play important roles in moving viruses across large geographic areas or sustaining local outbreaks through their different migratory behaviors.

Spatiotemporal changes in influenza A virus prevalence among wild waterfowl inhabiting the continental United States throughout the annual cycle.

Avian influenza viruses can pose serious risks to agricultural production, human health, and wildlife. An understanding of viruses in wild reservoir species across time and space is important to informing surveillance programs, risk models, and potential population impacts for vulnerable species. Although it is recognized that influenza A virus prevalence peaks in reservoir waterfowl in late summer through autumn, temporal and spatial variation across species has not been fully characterized. We combined two large influenza databases for North America and applied spatiotemporal models to explore patterns in prevalence throughout the annual cycle and across the continental United States for 30 waterfowl species. Peaks in prevalence in late summer through autumn were pronounced for dabbling ducks in the genera Anas and Spatula, but not Mareca. Spatially, areas of high prevalence appeared to be related to regional duck density, with highest predicted prevalence found across the upper Midwest during early fall, though further study is needed. We documented elevated prevalence in late winter and early spring, particularly in the Mississippi Alluvial Valley. Our results suggest that spatiotemporal variation in prevalence outside autumn staging areas may also represent a dynamic parameter to be considered in IAV ecology and associated risks.

White-Tailed Deer Spatial Distribution in Relation to '4-Poster' Tick Control Devices in Suburbia.

Deer are keystone hosts for adult ticks and have enabled the spread of tick distributions. The '4-Poster' deer bait station was developed by the United States Department of Agriculture to control ticks feeding on free-ranging deer. Although effective in certain scenarios, '4-Poster' deer treatment stations require the use of bait to attract deer to one location, which may cause increased deer disease transmission rates and habitat damage. To better understand and manage the impact of baited '4-Poster' stations on deer movements, we captured and GPS-monitored 35 deer as part of an integrated pest management project. Fifteen '4-Poster' stations were deployed among three suburban county parks to control ticks. To quantify the effects of '4-Poster' stations, we calculated deer movement metrics before and after feeders were filled with whole kernel corn, and we gathered information on visitation rates to feeders. Overall, 83.3% of collared deer visited a feeder and revisited approximately every 5 days. After feeders were refilled, collared deer were ~5% closer to feeders and conspecifics than before filling. Males used a higher percentage of available feeders and visited them more throughout the deployment periods. Although these nuanced alterations in behavior may not be strong enough to increase local deer abundance, in light of infectious diseases affecting deer populations and effective '4-Poster' densities, the core range shifts and clustering after refilling bait may be a cause for concern. As such, trade-offs between conflicting management goals should be carefully considered when deploying '4-Poster' stations.

Patterns of deer ked (Diptera: Hippoboscidae) and tick (Ixodida: Ixodidae) infestation on white-tailed deer (Odocoileus virginianus) in the eastern United States.

BACKGROUND: White-tailed deer (Odocoileus virginianus) host numerous ectoparasitic species in the eastern USA, most notably various species of ticks and two species of deer keds. Several pathogens transmitted by ticks to humans and other animal hosts have also been found in deer keds. Little is known about the acquisition and potential for transmission of these pathogens by deer keds; however, tick-deer ked co-feeding transmission is one possible scenario. On-host localization of ticks and deer keds on white-tailed deer was evaluated across several geographical regions of the eastern US to define tick-deer ked spatial relationships on host deer, which may impact the vector-borne disease ecology of these ectoparasites. METHODS: Ticks and deer keds were collected from hunter-harvested white-tailed deer from six states in the eastern US. Each deer was divided into three body sections, and each section was checked for 4 person-minutes. Differences in ectoparasite counts across body sections and/or states were evaluated using a Bayesian generalized mixed model. RESULTS: A total of 168 white-tailed deer were inspected for ticks and deer keds across the study sites. Ticks (n = 1636) were collected from all surveyed states, with Ixodes scapularis (n = 1427) being the predominant species. Counts of I. scapularis from the head and front sections were greater than from the rear section. Neotropical deer keds (Lipoptena mazamae) from Alabama and Tennessee (n = 247) were more often found on the rear body section. European deer keds from Pennsylvania (all Lipoptena cervi, n = 314) were found on all body sections of deer. CONCLUSIONS: The distributions of ticks and deer keds on white-tailed deer were significantly different from each other, providing the first evidence of possible on-host niche partitioning of ticks and two geographically distinct deer ked species (L. cervi in the northeast and L. mazamae in the southeast). These differences in spatial distributions may have implications for acquisition and/or transmission of vector-borne pathogens and therefore warrant further study over a wider geographic range and longer time frame.

Surveillance of Ticks and Tick-Borne Pathogens in Suburban Natural Habitats of Central Maryland.

Lyme and other tick-borne diseases are increasing in the eastern United States and there is a lack of research on integrated strategies to control tick vectors. Here we present results of a study on tick-borne pathogens detected from tick vectors and rodent reservoirs from an ongoing 5-yr tick suppression study in the Lyme disease-endemic state of Maryland, where human-biting tick species, including Ixodes scapularis Say (Acari: Ixodidae) (the primary vector of Lyme disease spirochetes), are abundant. During the 2017 tick season, we collected 207 questing ticks and 602 ticks recovered from 327 mice (Peromyscus spp. (Rodentia: Cricetidae)), together with blood and ear tissue from the mice, at seven suburban parks in Howard County. Ticks were selectively tested for the presence of the causative agents of Lyme disease (Borrelia burgdorferi sensu lato [s.l.]), anaplasmosis (Anaplasma phagocytophilum), babesiosis (Babesia microti), ehrlichiosis (Ehrlichia ewingii, Ehrlichia chaffeensis, and 'Panola Mountain' Ehrlichia) and spotted fever group rickettsiosis (Rickettsia spp.). Peromyscus ear tissue and blood samples were tested for Bo. burgdorferi sensu stricto (s.s), A. phagocytophilum, Ba. microti, and Borrelia miyamotoi. We found 13.6% (15/110) of questing I. scapularis nymphs to be Bo. burgdorferi s.l. positive and 1.8% (2/110) were A. phagocytophilum positive among all sites. Borrelia burgdorferi s.s. was found in 71.1% (54/76) of I. scapularis nymphs removed from mice and 58.8% (194/330) of captured mice. Results from study on tick abundance and pathogen infection status in questing ticks, rodent reservoirs, and ticks feeding on Peromyscus spp. will aid efficacy evaluation of the integrated tick management measures being implemented.

Pathogen Coinfections Harbored by Adult Ixodes scapularis from White-Tailed Deer Compared with Questing Adults Across Sites in Maryland, USA.

The blacklegged tick, Ixodes scapularis, can acquire and transmit tick-borne pathogens (TBPs) responsible for diseases such as human granulocytic anaplasmosis (Anaplasma phagocytophilum [ANPH]), babesiosis (Babesia microti [BABE]), Lyme borreliosis (Borrelia burgdorferi sensu lato [BBSL]), and the relatively novel relapsing fever-like illness, Borrelia miyamotoi (BMIY) disease in the northeastern United States. Coinfections with these pathogens are becoming increasingly more common in I. scapularis and their hosts, likely attributed to their shared enzootic cycles. Urban habitats are favorable to host species such as white-tailed deer (Odocoileus virginianus) and these ungulates are known to be important to I. scapularis for reproduction and dispersal in North America. To understand the relationship between TBPs, white-tailed deer, and I. scapularis, we sampled eight sites across central Maryland collecting I. scapularis using standard tick dragging/flagging methods and retrieved others from deer carcasses. Pathogenic TBP species in each tick were determined using qPCR. In total, 903 adult ticks (deer: n = 573; questing: n = 330) revealed landscape-level prevalence of ANPH (27.8%), BABE (1.3%), BBSL (14.6%), and BMIY (0.8%) as singular infections overall. However, secondary coinfections of ANPH and BBSL were highest (9.9%) in ticks feeding from deer while associations of BBSL and BABE (4.2%) were highest in questing ticks. Results from this study provide evidence suggesting that adult I. scapularis acquire pathogenic species through phenologically associated host use, and thus, subsequent infections found in adults may provide insights into coinfection relationships.

Trapping White-Tailed Deer (Artiodactyla: Cervidae) in Suburbia for Study of Tick-Host Interaction.

Live capture of white-tailed deer (Odocoileus virginianus) (Zimmermann, 1780) is often necessary for research, population control, disease monitoring, and parasite surveillance. We provide our deer trapping protocol used in a tick-host vector ecology research project and recommendations to improve efficiency of deer trapping programs using drop nets in suburban areas. We captured 125 deer across two trapping seasons. Generally, lower daily minimum temperatures were related to increased capture probability, along with the presence of snow. Our most successful trapping sites were less forested, contained more fragmentation, and greater proportion of human development (buildings, roads, recreational fields). To improve future suburban deer trapping success, trapping efforts should include areas dominated by recreational fields and should not emphasize remote, heavily forested, less fragmented parks. Concurrently, our study illustrated the heterogeneous nature of tick distributions, and we collected most ticks from one trapping site with moderate parameter values between the extremes of the most developed and least developed trapping sites. This emphasized the need to distribute trapping sites to not only increase your capture success but to also trap in areas across varying levels of urbanization and fragmentation to increase the probability of parasite collection.

Multiscale consensus habitat modeling for landscape level conservation prioritization.

Globally, wide-ranging carnivore populations are imperiled due to human-caused habitat fragmentation. Where populations are fragmented, habitat quantification is often the first step in conservation. Presence-only species distribution models can provide robust results when proper scales and data are considered. We aimed to identify habitat for a fragmented carnivore population at two scales and aid conservation prioritization by identifying potential future habitat fragmentation. We used location data and environmental variables to develop a consensus model using Maxent and Mahalanobis distance to identify black bear (Ursus americanus floridanus) habitat across Florida, USA. We compared areas of habitat to areas of predicted sea level rise, development, and protected areas. Local-scale models performed better than state-scale models. We identified 23,798 km2 of habitat at the local-scale and 45,703 km2 at the state-scale. Approximately 10% of state- and 14% of local-scale habitat may be inundated by 2100, 16% of state- and 7% of local-scale habitat may be developed, and 54% of state- and 15% of local-scale habitat is unprotected. Results suggest habitat is at risk of fragmentation. Lack of focused conservation and connectivity among bear subpopulations could further fragmentation, and ultimately threaten population stability as seen in other fragmented carnivore populations globally.

Waterfowl occurrence and residence time as indicators of H5 and H7 avian influenza in North American Poultry.

Avian influenza (AI) affects wild aquatic birds and poses hazards to human health, food security, and wildlife conservation globally. Accordingly, there is a recognized need for new methods and tools to help quantify the dynamic interaction between wild bird hosts and commercial poultry. Using satellite-marked waterfowl, we applied Bayesian joint hierarchical modeling to concurrently model species distributions, residency times, migration timing, and disease occurrence probability under an integrated animal movement and disease distribution modeling framework. Our results indicate that migratory waterfowl are positively related to AI occurrence over North America such that as waterfowl occurrence probability or residence time increase at a given location, so too does the chance of a commercial poultry AI outbreak. Analyses also suggest that AI occurrence probability is greatest during our observed waterfowl northward migration, and less during the southward migration. Methodologically, we found that when modeling disparate facets of disease systems at the wildlife-agriculture interface, it is essential that multiscale spatial patterns be addressed to avoid mistakenly inferring a disease process or disease-environment relationship from a pattern evaluated at the improper spatial scale. The study offers important insights into migratory waterfowl ecology and AI disease dynamics that aid in better preparing for future outbreaks.