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Design- and model-based recommendations for detecting and quantifying an amphibian pathogen in environmental samples

Accurate pathogen detection is essential for developing management strategies to address emerging infectious diseases, an increasingly prominent threat to wildlife. Sampling for free-living pathogens outside of their hosts has benefits for inference and study efficiency, but is still uncommon. We used a laboratory experiment to evaluate the influences of pathogen concentration, water type, and qPCR inhibitors on the detection and quantification of Batrachochytrium dendrobatidis ( Bd ) using water filtration. We compared results pre- and post-inhibitor removal, and assessed inferential differences when single versus multiple samples were collected across space or time. We found that qPCR inhibition influenced both Bd detection and quantification in natural water samples, resulting in biased inferences about Bd occurrence and abundance. Biases in occurrence could be mitigated by collecting multiple samples in space or time, but biases in Bd quantification were persistent. Differences in Bd concentration resulted in variation in detection probability, indicating that occupancy modeling could be used to explore factors influencing heterogeneity in Bd abundance among samples, sites, or over time. Our work will influence the design of studies involving amphibian disease dynamics and studies utilizing environmental DNA (eDNA) to understand species distributions.

Ecolology and Evolution↗

Estimating occurrence, prevalence, and detection of amphibian pathogens: Insights from occupancy models

Understanding the distribution of pathogens across landscapes and their prevalence within host populations is a common aim of wildlife managers. Despite the need for unbiased estimates of pathogen occurrence and prevalence for planning effective management interventions, many researchers fail to account for imperfect pathogen detection. Instead raw data are often reported, which may lead to ineffective, or even detrimental, management actions. We illustrate the utility of occupancy models for generating unbiased estimates of disease parameters by 1) providing a written tutorial describing how to fit these models in Program PRESENCE and 2) presenting a case study with the pathogen ranavirus. We analyzed ranavirus detection data from a wildlife refuge (Maryland, US) using occupancy modeling, which yields unbiased estimates of pathogen occurrence and prevalence. We found ranavirus prevalence was underestimated by up to 30% if imperfect pathogen detection was ignored. The unbiased estimate of ranavirus prevalence in larval wood frog ( Lithobates sylvaticus ; 0.73) populations was higher than in larval spotted salamander ( Ambystoma maculatum ; 0.56) populations. In addition, the odds of detecting ranavirus in tail samples were 6.7 times higher than detecting ranavirus in liver samples. Therefore, tail samples presented a nonlethal sampling method for ranavirus that may be able to detect early (nonsystemic) infections.

Maryland↗

Salmonellosis in a captive heron colony

Salmonellosis caused by Salmonella typhimurium was one of several factors responsible for losses among young herons being held at the Patuxent Wildlife Research Center. The infection was demonstrated in five black-crowned night herons ( Nycticorax nycticorax ), three common egrets ( Casmerodius albus ), two little blue herons ( Florida caerulea ), one cattle egret ( Bubulcus ibis ), one snowy egret ( Leucophoyx thula ) and one Louisiana heron ( Hydranassa tricolor ). The disease was characterized by emaciation, focal liver necrosis, and frequently by a caseo-necrotic enteritis.

Maryland↗

Existing evidence on the effects of climate variability and climate change on ungulates in North America: A systematic map

Background Climate is an important driver of ungulate life-histories, population dynamics, and migratory behaviors. Climate conditions can directly impact ungulates via changes in the costs of thermoregulation and locomotion, or indirectly, via changes in habitat and forage availability, predation, and species interactions. Many studies have documented the effects of climate variability and climate change on North America’s ungulates, recording impacts to population demographics, physiology, foraging behavior, migratory patterns, and more. However, ungulate responses are not uniform and vary by species and geography. Here, we present a systematic map describing the abundance and distribution of evidence on the effects of climate variability and climate change on native ungulates in North America. Methods We searched for all evidence documenting or projecting how climate variability and climate change affect the 15 ungulate species native to the U.S., Canada, Mexico, and Greenland. We searched Web of Science, Scopus, and the websites of 62 wildlife management agencies to identify relevant academic and grey literature. We screened English-language documents for inclusion at both the title and abstract and full-text levels. Data from all articles that passed full-text review were extracted and coded in a database. We identified knowledge clusters and gaps related to the species, locations, climate variables, and outcome variables measured in the literature. Review findings We identified a total of 674 relevant articles published from 1947 until September 2020. Caribou ( Rangifer tarandus ), elk ( Cervus canadensis ), and white-tailed deer ( Odocoileus virginianus ) were the most frequently studied species. Geographically, more research has been conducted in the western U.S. and western Canada, though a notable concentration of research is also located in the Great Lakes region. Nearly 75% more articles examined the effects of precipitation on ungulates compared to temperature, with variables related to snow being the most commonly measured climate variables. Most studies examined the effects of climate on ungulate population demographics, habitat and forage, and physiology and condition, with far fewer examining the effects on disturbances, migratory behavior, and seasonal range and corridor habitat. Conclusions The effects of climate change, and its interactions with stressors such as land-use change, predation, and disease, is of increasing concern to wildlife managers. With its broad scope, this systematic map can help ungulate managers identify relevant climate impacts and prepare for future changes to the populations they manage. Decisions regarding population control measures, supplemental feeding, translocation, and the application of habitat treatments are just some of the management decisions that can be informed by an improved understanding of climate impacts. This systematic map also identified several gaps in the literature that would benefit from additional research, including climate effects on ungulate migratory patterns, on species that are relatively understudied yet known to be sensitive to changes in climate, such as pronghorn ( Antilocapra americana ) and mountain goats ( Oreamnos americanus ), and on ungulates in the eastern U.S. and Mexico.

Environmental Evidence↗

Plague

Plague offers readers an overview of this highly complex disease caused by the bacteria Yersinia pestis . The history of the disease, as well as information about Yersinia pestis and its transmission by fleas, is described. The section Geographic Distribution presents areas of the world and United States where plague occurs most commonly in rodents and humans. Species Susceptibility describes infection and disease rates in rodents, humans, and other animals. Disease Ecology considers the complex relationship among rodents, domestic and wild animals, and humans and explores possible routes of transmission and maintenance of the organism in the environment. The effects of climate change, the potential for Y. pestis to be used as a bioweapon, and the impact of plague on conservation of wildlife are considered in Points to Ponder . Disease Prevention and Control outlines methods of prevention and treatment including vaccination for prairie dogs and black-footed ferrets. A glossary of technical terms is included. Tonie E. Rocke, the senior author and an epizootiologist at the USGS National Wildlife Health Center (NWHC), is a prominent researcher on oral vaccination of prairie dogs to prevent plague. She is currently working to transfer her success in the laboratory to the field to control plague in prairie dogs. Rachel C. Abbott, a biologist at the NWHC, is assisting Dr. Rocke in this process and will coordinate field trials of the vaccine. Milt Friend, first director of the NWHC, wrote the foreword. Plague is intended for scholars and the general public. The material is presented in a simple, straightforward manner that serves both audiences. Numerous illustrations and tables provide easily understood summaries of key points and information.

Circular↗

Alaska Interagency Ecosystem Health Work Group

The Alaska Interagency Ecosystem Health Work Group is a community of practice that recognizes the interconnections between the health of ecosystems, wildlife, and humans and meets to facilitate the exchange of ideas, data, and research opportunities. Membership includes the Alaska Native Tribal Health Consortium, U.S. Geological Survey, Alaska Department of Environmental Conservation, Alaska Department of Health and Social Services, Centers for Disease Control and Prevention, U.S. Fish and Wildlife Service, Alaska Sea Life Center, U.S. Environmental Protection Agency, and Alaska Department of Fish and Game.

Fact Sheet↗

Mycoplasmal conjunctivitis in wild songbirds: The spread of a new contagious disease in a mobile host population

A new mycoplasmal conjunctivitis was first reported in wild house finches ( Carpodacus mexicanus ) in early 1994. The causative agent was identified as Mycoplasma gallisepticum (MG), a nonzoonotic pathogen of poultry that had not been associated with disease in wild songbirds. Since the initial observations of affected house finches in the mid-Atlantic region, the disease has become widespread and has been reported throughout the eastern United States and Canada. By late 1995, mycoplasmal conjunctivitis had spread to an additional species, the American goldfinch ( Carduelis tristis ). This new disease exemplifies the rapid spread of a pathogen following introduction into a mobile wildlife population and provides lessons that may apply to emerging human diseases.

Emerging Infectious Diseases↗

Urban landscapes can change virus gene flow and evolution in a fragmentation-sensitive carnivore

Urban expansion has widespread impacts on wildlife species globally, including the transmission and emergence of infectious diseases. However, there is almost no information about how urban landscapes shape transmission dynamics in wildlife. Using an innovative phylodynamic approach combining host and pathogen molecular data with landscape characteristics and host traits, we untangle the complex factors that drive transmission networks of Feline Immunodeficiency Virus (FIV) in bobcats ( Lynx rufus ). We found that the urban landscape played a significant role in shaping FIV transmission. Even though bobcats were often trapped within the urban matrix, FIV transmission events were more likely to occur in areas with more natural habitat elements. Urban fragmentation also resulted in lower rates of pathogen evolution, possibly owing to a narrower range of host genotypes in the fragmented area. Combined, our findings show that urban landscapes can have impacts on a pathogen and its evolution in a carnivore living in one of the most fragmented and urban systems in North America. The analytical approach used here can be broadly applied to other host-pathogen systems, including humans.

Molecular Ecology↗

Characterizing the interface between wild ducks and poultry to evaluate the potential of transmission of avian pathogens

Background Characterizing the interface between wild and domestic animal populations is increasingly recognized as essential in the context of emerging infectious diseases (EIDs) that are transmitted by wildlife. More specifically, the spatial and temporal distribution of contact rates between wild and domestic hosts is a key parameter for modeling EIDs transmission dynamics. We integrated satellite telemetry, remote sensing and ground-based surveys to evaluate the spatio-temporal dynamics of indirect contacts between wild and domestic birds to estimate the risk that avian pathogens such as avian influenza and Newcastle viruses will be transmitted between wildlife to poultry. We monitored comb ducks ( Sarkidiornis melanotos melanotos ) with satellite transmitters for seven months in an extensive Afro-tropical wetland (the Inner Niger Delta) in Mali and characterise the spatial distribution of backyard poultry in villages. We modelled the spatial distribution of wild ducks using 250-meter spatial resolution and 8-days temporal resolution remotely-sensed environmental indicators based on a Maxent niche modelling method. Results Our results show a strong seasonal variation in potential contact rate between wild ducks and poultry. We found that the exposure of poultry to wild birds was greatest at the end of the dry season and the beginning of the rainy season, when comb ducks disperse from natural water bodies to irrigated areas near villages. Conclusions Our study provides at a local scale a quantitative evidence of the seasonal variability of contact rate between wild and domestic bird populations. It illustrates a GIS-based methodology for estimating epidemiological contact rates at the wildlife and livestock interface integrating high-resolution satellite telemetry and remote sensing data.

Inner Niger Delta↗

Trust Species and Habitat Branch: using the innovative approaches of today to conserve biodiversity for tomorrow

Some of the biggest challenges facing wildlife today are changes to their environment from both natural and anthropogenic causes. Natural resource managers, planners, policy makers, industry and private landowners must make informed decisions and policies regarding management, conservation, and restoration of species, habitats, and ecosystem function in response to these changes. Specific needs include (1) a better understanding of population status and trends; (2) understanding of species’ habitat needs and roles in supporting ecosystem functions; (3) the ability to assess species’ responses to environmental changes and predict future responses; and (4) the development of innovative techniques and tools to better understand, minimize or prevent any unintended consequences of environmental change. The Trust Species and Habitats Branch of the Fort Collins Science Center includes a diverse group of scientists encompassing both traditional and specialized expertise in wildlife biology, ecosystem ecology, quantitative ecology, disease ecology, molecular genetics, and stable isotope geochemistry. Using our expertise and collaborating with others around the world, our goal is to provide the information, tools, and technologies that our partners need to support conservation, management, and restoration of terrestrial vertebrate populations, habitats, and ecosystem function in a changing world.

Fact Sheet↗

Oral Sampling of little brown bat (Myotis lucifugus) maternity colonies for SARS-CoV-2 in the Northeast and Mid-Atlantic, USA

T he potential introduction of SARS-CoV-2, the virus responsible for the COVID-19 pandemic, into North American bat populations is of interest to wildlife managers due to recent disease-mediated declines of several species. Populations of little brown bats ( Myotis lucifugus ) have collapsed due to white-nose syndrome (WNS), a disease caused by the introduction and spread of the fungal pathogen Pseudogymnoascus destructans ( Pd ). Throughout much of the United States and southern Canada, large colonies of the species routinely established diurnal roosts in anthropogenic structures, thereby creating the potential for direct human contact and cross-species disease transmission. Given recent declines and the potential for further disease impacts, we collected oral swabs from eight little brown bat maternity colonies to assess the presence and prevalence of SARS-CoV-2 by RT-qPCR analysis. Little brown bat colonies in Maryland ( n = 1), New Hampshire ( n = 1), New Jersey ( n = 2), New York ( n = 1), Rhode Island ( n = 2), and Virginia ( n = 1) were taken during May-August, 2022. From 235 assayed individuals, no bat tested positive for SARS-CoV-2. Our results indicate that little brown bats may not contract SARS-CoV-2 or that the virus persists at undetectable levels in populations of the Mid-Atlantic and Northeast during summer months. Nonetheless, continued monitoring and future work addressing other seasons may still be warranted to conclusively determine infection status.

Maryland, New Hampshire, New Jersey, New York, Rho↗

Wildlife health implications of sewage disposal in wetlands

Wildlife health concerns associated with disposal of sewage effluent in wetlands are of three primary types: (1) introduction of pathogens, (2) introduction of pollutants that adversely impact on host body defense mechanisms, and (3) changes in the physical and chemical properties of wetlands that favor the development and maintenance of disease problems. Unlike the situation with human health concerns, introduction of pathogens is not the major concern regarding wildlife health. Instead, the focus of attention needs to be directed at environmental changes likely to take place as a result of effluent discharges into different types of wetlands. Unless these changes are adequately addressed from a disease perspective, marshes utilized for sewage disposal could become disease incubators and wildlife death traps. This result would be unfortunate because the backlash would likely negate the potentially beneficial aspects of the use of sewage wastewater for the creation of new wetlands and have a severe impact on progress being made towards evaluation of the compatibility of wildlife and sewage effluents.

Book chapter↗

Elk personality and anthropogenic food subsidy: Managing conflict and migration loss

The continued decline of long-distance ungulate migrations threatens to decouple important ecological processes that increase biodiversity and wildlife abundance. Past research has focused on preserving migration paths where habitat fragmentation and loss disrupt movement corridors. However, shifting residency-migration trade-offs are the stronger driver of migration loss in some populations. Suburban residential developments may provide ungulates with anthropogenic food sources and refuge from predators, which can increase population growth among short-distance migrants relative to long-distance migrants. This trend can increase wildlife vehicle collisions and other human–wildlife conflicts while simultaneously reducing hunting opportunities. Yet, individual animals vary in their tolerance of human disturbance. We investigated how interindividual variation relative to conflict and human habituation influences elk migration and space use on shared winter range. We used a clustering algorithm applied to GPS collar data to identify elk use of anthropogenic food resources in suburban habitat. Cluster locations identified all known anthropogenic subsidy locations during the study period. Elk that used suburban anthropogenic food sources also migrated 60% shorter distances between summer and winter ranges than elk with no known use of these food subsidies. Elk use of protected wintering grounds was spatially structured such that conflict-prone, short-distance migrants disproportionately used areas with more human activity. Clustering algorithms applied to GPS collar data may allow managers to identify foci of concentrated use that generates human–wildlife conflict, and where prion deposition and environmental contamination facilitate the spread of chronic wasting disease, particularly in suburban areas with anthropogenic food subsidies. The apparent spatial structuring of shared winter range according to the conflict potential and migration strategy of individual elk may also permit managers to assess relative recruitment among cryptic population segments using different migration strategies and facilitate targeted, adaptive management actions. These associations between conflict, human habituation, and migration shed light on the urbanization of wildlife species, inform efforts to manage human–wildlife conflict and disease spread, and emphasize that a multipronged approach beyond maintaining habitat corridors may be necessary to conserve long-distance migrations for species that can become human-habituated.

Wyoming↗

Different management strategies are optimal for combating disease in East Texas cave versus culvert hibernating bat populations

Management decisions for species impacted by emerging infectious diseases are challenging when there are uncertainties in the effectiveness of management actions. Wildlife managers must balance trade‐offs between mitigating the effects of the disease and the associated consequences on other aspects of the managed system. An example of this challenge is exemplified in the response to white‐nose syndrome (WNS), a disease of hibernating bats. The fungal pathogen that causes WNS, Pseudogymnoascus destructans , continues to spread throughout North America. Texas, recently confirmed positive for the fungus, has documented 33 bat species in the state, with nearly half of those species naïve to the pathogen. We explicitly incorporated multiple management objectives, uncertainty, and risk in the Texas Parks and Wildlife Department decision to manage East Texas populations of the tri‐colored bat ( Perimyotis subflavus ), a species highly susceptible to WNS. Alternatives included individual actions that act against P . destructans or benefit bats, a no active management option, and combinations of actions. Although our main objective was to identify WNS mitigation measures for tri‐colored bats in culverts, we also considered the transferability of the decision for natural caves. In this scenario, the optimal decision differed for culverts and caves, with a “portfolio” combination of actions ranking as the best alternative for culverts and a single vaccine alternative for caves. Because the top management alternatives differed markedly between these two systems, finding treatments that have broad application is likely infeasible, given that each management decision is characterized by different mixtures of competing objectives.

Texas↗

Contact heterogeneities in feral swine: implications for disease management and future research

Contact rates vary widely among individuals in socially structured wildlife populations. Understanding the interplay of factors responsible for this variation is essential for planning effective disease management. Feral swine ( Sus scrofa ) are a socially structured species which pose an increasing threat to livestock and human health, and little is known about contact structure. We analyzed 11 GPS data sets from across the United States to understand the interplay of ecological and demographic factors on variation in co-location rates, a proxy for contact rates. Between-sounder contact rates strongly depended on the distance among home ranges (less contact among sounders separated by >2 km; negligible between sounders separated by >6 km), but other factors causing high clustering between groups of sounders also seemed apparent. Our results provide spatial parameters for targeted management actions, identify data gaps that could lead to improved management and provide insight on experimental design for quantitating contact rates and structure.

Ecosphere↗

Getting ahead of the crises: Developing an avian malaria disease management plan for Hawaiian forest birds

Avian malaria is an existential threat to a majority of native Hawaiian forest birds. Climate change is facilitating the spread of malaria to historically disease-free areas, and despite the risk of native Hawaiian forest bird extinctions from malaria outbreaks, no comprehensive disease management plans exist for forest bird conservation areas. Hakalau Forest National Wildlife Refuge, Hawai‘i, supports a thriving bird community in a historically disease-free area that is now vulnerable to malaria incursion. Drawing on the expertise of land managers and research scientists, we developed an approach that could be used to proactively address the risk of expanding malaria into the Refuge. The plan lays out a multi-level approach that includes options for monitoring and management actions depending on defined threat levels: Vigilant, High Alert, Disease Outbreak, and Crisis levels. Initial Vigilant and High Alert levels monitor bird populations, climate conditions, and mosquito occurrence for signs of possible disease outbreaks, with higher levels shifting toward more direct management responses. While specific actions will change as new tools become available, the proactive approach can help Refuge managers better respond to changing malaria levels in the future and provide a model for managing disease here in Hawai‘i and elsewhere.

Hawaii↗

Special considerations for specimen collections that may be involved in law enforcement cases

Causes of mortality in wildlife include natural conditions—such as the viral, bacterial, and fungal diseases discussed in other chapters of this manual—and human intervention. Direct human intervention in wildlife deaths may be associated with individual human actions, such as gunshot or poisonings, or with institutions, such as wind farms or mining operations. Mortality that can be directly attributed to humans may be considered a crime based on the animal(s) affected and (or) the agent used. Wildlife laws were established to protect our nation’s wildlife resources and assist in conserving healthy populations of native wildlife. A variety of laws pertain to wildlife, such as the Migratory Bird Treaty Act, which makes it illegal, except as permitted, to capture, kill, or possess a portion or all of any migratory bird, a member of the group that includes the vast majority of wild birds present in the United States. Similar to pathogens that can spread unchecked through a wild population, a person or an institution that illegally kills wildlife may continue this practice indefinitely or until the illegal activities are detected and addressed. Convicting the perpetrator of a crime, however, requires that certain practices and procedures be followed so that a solid legal case can be constructed. As with any crime, investigation of the event is led by law enforcement personnel who are well-versed in the applicable laws, oversee the collection of evidence, and pursue persons or entities of interest. These individuals are uniquely qualified and trained to maintain the integrity of evidence, evaluate suspects to effectively prosecute the case, and effect the penalties of the law. The investigation of direct crimes against humans may involve teams of 5–10 law enforcement agents and specialists—each with a certain focus such as blood spatter, fingerprints, or ballistics—in processing a crime scene. In contrast, investigations of crimes against wildlife generally involve markedly fewer wildlife law enforcement agents, and in many instances of unlawful wildlife death, only one law enforcement agent is available to process an entire crime scene and work on a case. Thus, the assistance of individuals familiar with the geographical area, the endemic animal populations, and the local ecology can be very important for building an effective case. The aims of this chapter are to 1) help biologists or field personnel recognize the signs that indicate a crime may have been committed, and 2) to give readers a basic understanding of how a wildlife crime scene is processed. This chapter is not intended to give readers the tools to investigate a crime scene alone, but will hopefully make them a valuable asset to law enforcement agents who respond to the scene. An effectively processed case, resulting in prosecution of a suspect, supports the law as a deterrent to future acts that could endanger the conservation of wildlife.

Techniques and Methods↗

The WOAH global wildlife health collaborating centre network (WOAH-WildNet): A coordinated and transformative approach to global wildlife health challenges

Wildlife health is integral to functioning, complex ecosystems [ 1 ], directly and indirectly influencing the health of people, animals, plants, and the environment [ 2 – 4 ]. Healthy wildlife populations are essential for ecosystem services and are at the heart of the One Health approach [ 3 , 4 ], which aims to sustainably balance and optimize the health of people, animals, and ecosystems through multisectoral and transdisciplinary collaboration [ 5 ]. Despite its importance, wildlife health initiatives often operate in silos, limiting capacity to address transboundary threats such as emerging diseases, pollution, and environmental changes. Anthropogenic changes, including habitat loss, degradation, fragmentation, and unsustainable harvesting, exacerbate wildlife health challenges [6–9]. These pressures disrupt species biology and alter host-pathogen dynamics [10–12], underscoring the importance of coordinated collective action in addressing harmful effects on the health of wild animals. While local conservation efforts are vital, long-term success in safeguarding biodiversity requires a unified, global network. For instance, without harmonized surveillance and response systems, individual institutions cannot effectively track pathogens across borders or share diagnostic capabilities. The World Organisation for Animal Health (WOAH) Collaborating Centre Network for Wildlife Health—WOAH-WildNet—was established to bridge these gaps. By fostering global collaboration, sharing resources, and enabling data exchange, WOAH-WildNet provides a transformative, systems-based approach to wildlife health, managing risks, and enhancing ecosystem resilience. Central to this mission is breaking down silos to promote intersectoral coordinated responses to complex wildlife health challenges.

PLOS Sustainability and Transformation↗