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Rapid risk assessment framework to estimate potential for spillback at human-wildlife interfaces

More than 60% of emerging infectious diseases of humans have a wildlife origin, and when these diseases spread through human populations to new geographical areas, there is a considerable risk of spillback from humans to wildlife species. Spillback events can have severe consequences for wildlife populations, where the disease may cause morbidity and mortality, and human populations, where the establishment in wildlife may lead to prolonged transmission or new exposures in humans. Mitigating these consequences requires identifying the key risk factors that lead to human–wildlife transmission events and implementing risk-reducing actions, a challenge given that cross-species transmission events are rare and often data deficient. To identify potential species and locations that are most likely to lead to these rare events, we developed a spatially explicit, rapid risk assessment framework that incorporates three components of the spillback process: wildlife susceptibility, wildlife exposure, and pathogen introduction pressure. To demonstrate the broad applicability of our framework, we conducted a rapid risk assessment on two recent emerging zoonotic pathogens in humans, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and mpox, to determine the relative spillback risk to wild mammalian species in the continental United States. The rapid risk assessment identified both species and locations with higher than expected spillback risk, providing managers and researchers with valuable information to prioritize surveillance and risk-mitigation actions. Our framework represents a rapid and flexible approach to assess the risks of spillback to wildlife populations during rapidly evolving zoonotic disease outbreaks.

Transboundary and Emerging Diseases↗

Elk migration influences the risk of disease spillover in the Greater Yellowstone Ecosystem

Wildlife migrations provide important ecosystem services, but they are declining. Within the Greater Yellowstone Ecosystem (GYE) some elk ( Cervus canadensis ) herds are losing migratory tendencies, which may increase spatiotemporal overlap between elk and livestock (domestic bison [ Bison bison ] and cattle [ Bos taurus ]), potentially exacerbating pathogen transmission risk. We combined disease, movement, demographic, and environmental data from eight elk herds in the GYE to examine the differential risk of brucellosis transmission (through aborted fetuses) from migrant and resident elk to livestock. For both migrants and residents, we found that transmission risk from elk to livestock occurred almost exclusively on private ranchlands as opposed to state or federal grazing allotments. Weather variability affected the estimated distribution of spillover risk from migrant elk to livestock, with a 7‐12% increase in migrant abortions on private ranchlands during years with heavier snowfall. In contrast, weather variability did not affect spillover risk from resident elk. Migrant elk were responsible for the majority (68%) of disease spillover risk to livestock because they occurred in greater numbers than resident elk. On a per‐capita basis, however, our analyses suggested that resident elk disproportionately contributed to spillover risk. In five of seven herds, we estimated that the per‐capita spillover risk was greater from residents than from migrants. Averaged across herds, an individual resident elk was 23% more likely than an individual migrant elk to abort on private ranchlands. Our results demonstrate links between migration behavior, spillover risk, and environmental variability, and highlight the utility of integrating models of pathogen transmission and host movement to generate new insights about the role of migration in disease spillover risk. Further, they add to the accumulating body of evidence across taxa that suggests that migrants and residents should be considered separately during investigations of wildlife disease ecology. Finally, our findings have applied implications for elk and brucellosis in the GYE, and suggest that managers should prioritize actions that maintain spatial separation of elk and livestock on private ranchlands during years when snowpack persists into the risk period.

Wyoming↗

Disease relationship of domestic stock and wildlife

From the time that western civilization established itself on the North American continent until very recent years, little thought was given to the diseases, or other forms of loss, in game. In the process of bringing civilization and the incidental domestic arts and trades to the United States it appears to have been the policy to establish domestic farm stock on the land just as abundantly as the carrying capacity of land would tolerate. And judged by the low quality of many of our present farm animals, it is evident that in many cases the land was, and is now, overstocked and undermanaged. In traveling over this country one is impressed by the lack of uniformity, imperfect physical development, and poor state of nutrition of much of the domestic livestock. It would appear that the wild animals unhampered by fencing and other restraint such as controlled mating, feed selection, and enforced habitat in contaminated or polluted environment, have a better chance for perfect growth and complete development to a size and proportion normal for those species. While all of the factors mentioned produce a definitely deleterious result on the welfare of animal life, that of contaminated or polluted environment is by no means the least. The stunting action of disease on the growth of the young is too well known to admit of controversy. The impairment of function of vital organs due to minute cellular changes resulting from sub-acute or chronic infections prevents normal growth. Through centuries of enforced survival in densely congested pastures, pens, and stables, a certain degree of acquired resistance to many diseases has been built up in farm stock. If it were not so, very few barnyard animals would ever survive the conditions generally seen in our agricultural districts. Manure heaps, quantities of partly spoiled feed, and decaying masses of vegetation and refuse have come to be regarded as a natural part of the barnyard scene.

Conference Paper↗

Urbanization and host relatedness shape virome composition in a widespread, generalist carnivore

Urban wildlife species have the potential to serve as links in disease transmission between wildlife, humans and domestic animals at the wildland–urban interface (WUI), contributing to both sustained cross-species transmission of pathogens and the emergence of diseases in susceptible populations. However, the relative roles of host and environmental factors in shaping the composition of pathogen communities in urban wildlife is understudied. In this study, we integrated DNA and RNA virome data with host genomic and GPS datasets to investigate factors shaping virome composition in bobcats ( Lynx rufus ) at the WUI in the Tucson Mountains, Arizona, USA. Using a hybrid-capture approach for 31 scats and 17 buccal swabs, we identified multiple viruses that could affect carnivore health at the WUI, including canine parvovirus, feline astrovirus, Felis catus papillomaviruses 2 and 3 and Lyon-IARC polyomavirus. Models of virome composition and distribution of viral taxa indicated contributions of host genetic relatedness and factors relating to urbanisation (such as percentages of urban land cover, road and building densities and distances to roads). Genetic associations with virome compositions were particularly influenced by females. While females exhibit significant isolation by distance, partial Mantel tests revealed a significant correlation between beta diversity and host genetic distance in females only. To our knowledge, this study represents the first assessment of factors shaping virome composition in a wild felid. Our finding of known feline and canine pathogens in bobcats underscores the potential of the WUI to facilitate cross-species transmission between wild and domestic animals.

Arizona↗

Managing the livestock– Wildlife interface on rangelands

On rangelands the livestock–wildlife interface is mostly characterized by management actions aimed at controlling problems associated with competition, disease, and depredation. Wildlife communities (especially the large vertebrate species) are typically incompatible with agricultural development because the opportunity costs of wildlife conservation are unaffordable except in arid and semi-arid regions. Ecological factors including the provision of supplementary food and water for livestock, together with the persecution of large predators, result in livestock replacing wildlife at biomass densities far exceeding those of indigenous ungulates. Diseases are difficult to eradicate from free-ranging wildlife populations and so veterinary controls usually focus on separating commercial livestock herds from wildlife. Persecution of large carnivores due to their depredation of livestock has caused the virtual eradication of apex predators from most rangelands. However, recent research points to a broad range of solutions to reduce conflict at the livestock–wildlife interface. Conserving wildlife bolsters the adaptive capacity of a rangeland by providing stakeholders with options for dealing with environmental change. This is contingent upon local communities being empowered to benefit directly from their wildlife resources within a management framework that integrates land-use sectors at the landscape scale. As rangelands undergo irreversible changes caused by species invasions and climate forcings, the future perspective favors a proactive shift in attitude towards the livestock–wildlife interface, from problem control to asset management.

Book chapter↗

Is your bird feeder safe?

Bird feeding is a popular activity for millions of Americans. Some of our favorite bird species commonly visit bird feeders and these stations may be an important factor in their well-being during some segments of their life-cycle. However, poorly maintained feeding stations may contribute to the occurrence of infectious disease and mortality. In recent years there have been unprecedented reports of songbird mortality events and the occurrence of a previously unreported disease in songbirds. The National Wildlife Health Center of the U.S. Geological Survey conducts research on diseases in wildlife, their causes, and means of preventing or reducing disease outbreaks.

Bird Conservation↗

Vaccination of endangered wildlife as a conservation tool: Hindsights and new horizons in the pandemic era

Vaccines are an established conservation tool that can reduce the threat of infectious disease in endangered wildlife populations. Vaccines exist for many infectious pathogens, and at a time of rapid technological advances in vaccinology, developing vaccines and vaccination programs for free-living endangered wildlife could help efforts to prevent extinctions from disease threats. Vaccination efforts could focus on protecting members of the target species or could be directed at reservoir populations to prevent pathogen spillover. Vaccination strategies need to be substantiated by research on safety and effectiveness, include risk and feasibility assessments, account for differences in host biology and disease epidemiology, and align with relevant regulatory frameworks. Engagement with stakeholders and the public is important to ensure the success of endangered species vaccination programs. Challenges such as funding, regulation, and societal acceptance are barriers to progress in vaccination programs for some species and geographic regions. We recommend the development of scientifically based international guidelines and a transdisciplinary forum with a specific emphasis on endangered wildlife vaccination. New technologies could be used collaboratively to prevent transmission of diseases for which vaccines are not currently available. Careful approaches and enhanced collaborations could help ensure the successful development of wildlife vaccination programs and promote resilience of endangered wildlife populations to increasing anthropogenic and environmental stressors on biodiversity.

Biological Conservation↗

Changes in the prevalence of avian disease and mosquito vectors at Hakalau Forest National Wildlife Refuge: a 14-year perspective and assessment of future risk

Throughout the main Hawaiian Islands, introduced mosquito-borne disease has had, and continues to have, a profound impact on the distributions and abundance of native Hawaiian forest birds. Populations of remaining native forest birds are largely restricted to high elevation forests where mean temperatures are marginal for vector and parasite development and limited availability of larval mosquito habitat constrains mosquito populations and disease transmission. Hakalau Forest National Wildlife Refuge (HFNWR) was established for the preservation of endemic avifauna in 1985. Since its creation, native bird communities there have remained intact and most species populations are stable or increasing. However, avian malaria had been detected at HFNWR in the past and, in light of documented climate change, new concerns have been raised regarding the long-term fate of the refuge’s forest birds. To examine the possible changes in avian malaria transmission at HFNWR we sampled forest birds for blood parasites, trapped adult mosquitoes and surveyed larval mosquito habitat at three sites during 2012 and compared our results with similar data collected between 1998 and 1999. We tested blood samples by polymerase chain reaction (PCR), immunoblotting, and microscopy to determine prevalence of acute and chronic infection and used attractive gravid traps to sample the vector mosquito Culex quinquefasciatus. Our study documented spatial trends and temporal changes in the prevalence of avian malaria, mosquito presence, larval mosquito habitat and feral pig activity at HFNWR. We found evidence of local transmission in high elevation forests, a general pattern of increasing prevalence at lower elevations and along a South to North gradient and a two-fold decrease in the prevalence of avian malaria in the intervening 14 years. Despite considerable effort, we were unable to detect larval C. quinquefasciatus and captured only one adult indicating that the vector of avian malaria has a very limited presence at HFNWR. We did, however, document the establishment of another invasive mosquito, Aedes japonicus japonicus , and its occurrence in tree fern cavities and rock pools as larval habitat in the lower forests of HFNWR. We suggest that interspecific competition by A. j. japonicus and predation by a suite of native predators may provide biotic resistance to the establishment of permanent C. quinquefasciatus populations. While current predictions of climate change in the Hawaiian Islands include a gradual warming and enhanced transmission by mid-century, the current cooling trend recorded at high elevation HFNWR illustrates the importance of monitoring to document fine scale temporal and site specific changes in prevalence. Long term changes in precipitation may have a more profound effect on local transmission of malaria than temperature and we may have already seen some potential impacts of an extended drought at HFNWR with a decrease in feral pig activity and pig associated larval mosquito habitat and increases in stream-associated larval mosquito habitat.

Hawaii↗

Giardia and Cryptosporidium in resident wildlife species in Arctic Alaska

Giardia and Cryptosporidium are zoonotic protozoan parasites that can infect humans and other taxa, including wildlife, often causing gastrointestinal illness. Both have been identified as One Health priorities in the Arctic, where climate change is expected to influence the distribution of many wildlife and zoonotic diseases, but little is known about their prevalence in local wildlife. To help fill information gaps, we collected fecal samples from four wildlife species that occur seasonally on the northern Alaska coastline or in nearshore marine waters—Arctic fox ( Vulpes lagopus ), polar bear ( Ursus maritimus ), Pacific walrus ( Odobenus rosmarus divergens ), and caribou ( Rangifer tarandus )—and used immunofluorescence assays to screen for Giardia cysts and Cryptosporidium oocysts. We detected Giardia cysts in 18.3% and Cryptosporidium oocysts in 16.5% of Arctic foxes ( n = 109), suggesting that foxes may be potentially important hosts in this region. We also detected Giardia cysts in a single polar bear (12.5%; n = 8), which to our knowledge represents the first such report for this species. Neither parasite was detected in walruses or caribou.

Food and Waterborne Parasitology↗

Estimating transmission of avian influenza in wild birds from incomplete epizootic data: implications for surveillance and disease spreac

Estimating disease transmission in wildlife populations is critical to understand host–pathogen dynamics, predict disease risks and prioritize surveillance activities. However, obtaining reliable estimates for free-ranging populations is extremely challenging. In particular, disease surveillance programs may routinely miss the onset or end of epizootics and peak prevalence, limiting the ability to evaluate infectious processes. We used profile likelihood to estimate the force of infection (FOI) in a low pathogenic avian influenza virus (LPAIv) epizootic model from censored time series of LPAIv prevalence in hatch-year waterfowl (order Anseriformes) at postbreeding and migration sites in North America. We found a mean LPAIv FOI of 0·12 day −1 [95% CI, 0·00–0·39], corresponding to an incidence rate of 0·11 day −1 , with geographic heterogeneity (min–max: 0·02–0·23 day −1 ) among study sites. These high infection rates indicate that most hatch-year waterfowl are likely infected with LPAIv early in the fall migration. Comparison of model-predicted and observed immunity confirmed our assumption of naïve hatch-year waterfowl and suggested long-term immunity (>6 months) for adults. Using the mean LPAIv incidence rate, we predict a shorter and lower epizootic curve for highly pathogenic avian influenza virus (HPAIv; 5 weeks with peak prevalence of 28% and 30% mortality) than LPAIv (8 weeks with peak prevalence of 50%). These findings indicate it is harder to detect HPAIv than LPAIv with swabs from live birds, which are commonly used during disease surveillance. Synthesis and applications . Our study highlights the potential of integrating incomplete surveillance data with epizootic models to quantify disease transmission and immunity. This modelling approach provides an important tool to understand spatial and temporal epizootic dynamics and inform disease surveillance. Our findings suggest focusing highly pathogenic avian influenza virus (HPAIv) surveillance on postbreeding areas where mortality of immunologically naïve hatch-year birds is most likely to occur, and collecting serology to enhance HPAIv detection. Our modelling approach can integrate various types of disease data facilitating its use with data from other surveillance programs (as illustrated by the estimation of infection rate during an HPAIv outbreak in mute swans Cygnus olor in Europe).

Journal of Applied Ecology↗

Toxoplasmosis

Toxoplasmosis ( Toxoplasma gondii ), one of the better known and more widespread zoonotic diseases, originated in wildlife species and is now well established as a human malady. Food- and waterborne zoonoses, such as toxoplasmosis, are receiving increasing attention as components of disease emergence and resurgence. Toxoplasmosis is transmitted to humans via consumption of contaminated food or water, and nearly one-third of humanity has been exposed to this parasite. The role of wildlife in this transmission process is becoming more clearly known and is outlined in this report. This zoonotic disease also causes problems in wildlife species across the globe. Future generations of humans will continue to be jeopardized by toxoplasmosis infections in addition to many of the other zoonotic diseases that have emerged during the past century. Through monitoring toxoplasmosis infection levels in wildlife populations, we will be better able to predict future human infection levels of this important zoonotic disease.

Circular↗

U.S. Geological Survey science strategy for highly pathogenic avian influenza in wildlife and the environment (2016–2020)

Introduction Through the Science Strategy for Highly Pathogenic Avian Influenza (HPAI) in Wildlife and the Environment, the USGS will assess avian influenza (AI) dynamics in an ecological context to inform decisions made by resource managers and policymakers from the local to national level. Through collection of unbiased scientific information on the ecology of AI viruses and wildlife hosts in a changing world, the U.S. Geological Survey (USGS) will enhance the development of AI forecasting tools and ensure this information is integrated with a quality decision process for managing HPAI. The overall goal of this USGS Science Strategy for HPAI in Wildlife and the Environment goes beyond document­ing the occurrence and distribution of AI viruses in wild birds. The USGS aims to understand the epidemiological processes and environmental factors that influence HPAI distribution and describe the mechanisms of transmission between wild birds and poultry. USGS scientists developed a conceptual model describing the process linking HPAI dispersal in wild waterfowl to the outbreaks in poul­try. This strategy focuses on five long-term science goals, which include: Science Goal 1—Augment the National HPAI Surveillance Plan; Science Goal 2—Determine mechanisms of HPAI disease spread in wildlife and the environment; Science Goal 3—Characterize HPAI viruses circulating in wildlife; Science Goal 4—Understand implications of avian ecol­ogy on HPAI spread; and Science Goal 5—Develop HPAI forecasting and decision-making tools. These goals will help define and describe the processes outlined in the conceptual model with the ultimate goal of facilitating biosecurity and minimizing transfer of diseases across the wildlife-poultry interface. The first four science goals are focused on scientific discovery and the fifth goal is application-based. Decision analyses in the fifth goal will guide prioritization of proposed actions in the first four goals.

Open-File Report↗

Modeling elk‐to‐livestock transmission risk to predict hotspots of brucellosis spillover

Wildlife reservoirs of infectious disease are a major source of human‐wildlife conflict because of the risk of potential spillover associated with commingling of wildlife and livestock. In the Greater Yellowstone Ecosystem, the presence of brucellosis ( Brucella abortus ) in free‐ranging elk ( Cervus canadensis ) populations is of significant management concern because of the risk of disease transmission from elk to livestock. We identified how spillover risk changes through space and time by developing resource selection functions using telemetry data from 223 female elk to predict the relative probability of female elk occurrence daily during the transmission risk period. We combined these spatiotemporal predictions with elk seroprevalence, demography, and transmission timing data to identify when and where abortions (the primary transmission route of brucellosis) were most likely to occur. Additionally, we integrated our predictions of transmission risk with spatiotemporal data on areas of potential livestock use to estimate the daily risk to livestock. We predicted that approximately half of the transmission risk occurred on areas where livestock may be present (i.e., private property or grazing allotments). Of the transmission risk that occurred in livestock areas, 98% of it was on private ranchlands as opposed to state or federal grazing allotments. Disease prevalence, transmission timing, host abundance, and host distribution were all important factors in determining the potential for spillover risk. Our fine‐resolution (250‐m spatial, 1‐day temporal), large‐scale (17,732 km 2 ) predictions of potential elk‐to‐livestock transmission risk provide wildlife and livestock managers with a useful tool to identify higher risk areas in space and time and proactively focus actions in these areas to separate elk and livestock to reduce spillover risk.

Montana↗

Mycobacterial infection in Northern snakehead ( Channa argus ) from the Potomac River catchment

The Northern snakehead, Channa argus (Cantor), is a non-native predatory fish that has become established regionally in some temperate freshwater habitats within the United States. Over the past decade, Northern snakehead populations have developed within aquatic ecosystems throughout the eastern USA, including the Potomac River system within Virginia, Maryland and Washington, D.C. Since this species was initially observed in this region in 2002, the population has expanded considerably (Odenkirk & Owens 2007 ). In the Chesapeake Bay watershed, populations of Northern snakehead exist in the lower Potomac River and Rappahannock Rivers on the Western shore of the Bay, and these fish have also been found in middle or upper reaches of river systems on the Eastern shore of the Bay, including the Nanticoke and Wicomico Rivers among others. Over the past several years, many aspects of Northern snakehead life history in the Potomac River have been described, including range and dispersal patterns, microhabitat selection and diet (Lapointe, Thorson & Angermeier 2010 ; Saylor, Lapointe & Angermeier 2012 ; Lapointe, Odenkirk & Angermeier 2013 ). However, comparatively little is known about their health status including susceptibility to parasitism and disease and their capacity to serve as reservoirs of disease for native wildlife. Although considered hardy by fisheries biologists, snakehead fish have demonstrated susceptibility to a number of described piscine diseases within their native range and habitat in Asia. Reported pathogens of significance in snakehead species in Asia include snakehead rhabdovirus (Lio-Po et al . 2000 ), aeromonad bacteria (Zheng, Cao & Yang 2012 ), Nocardia (Wang et al . 2007 ) and Mycobacterium spp . (Chinabut, Limsuwan & Chantatchakool 1990 ; ). Mycobacterial isolates recovered from another snakehead species ( Channa striata ) in the previous studies have included M. marinum and M. fortuitum , as identified through molecular-based diagnostics (Puttinaowarat et al . 2002 ). We have conducted health screenings of Northern snakehead from the Potomac River system over the past several years and have detected few associated pathogens. Typical observations have largely consisted of incidental identification of parasitism with protozoal, monogenean or trematode organisms (unpublished data). We have also identified largemouth bass virus (LMBV) in clinically normal Northern snakehead collected from the Potomac River (Iwanowicz et al . 2013 ). Continued research concerning these and other pathogens of this introduced species is important to fully understand the potential impacts of these fish on indigenous wildlife and aquatic ecosystems.

Potomac River, Pohick Bay↗

Guidelines for the field evaluation of desert tortoise health and disease

Field evaluation of free-ranging wildlife requires the systematic documentation of a variety of environmental conditions and individual parameters of health and disease, particularly in the case of rare or endangered species. In addition, defined criteria are needed for the humane salvage of ill or dying animals. The purpose of this paper is to describe, in detail, the preparation, procedures, and protocols we developed and tested for the field evaluation of wild desert tortoises ( Gopherus agassizii ). These guidelines describe: preparations for the field, including developing familiarity with tortoise behavior and ecology, and preparation of standardized data sheets; journal notes to document background data on weather conditions, temperature, rainfall, locality, and historic and recent human activities; procedures to prevent the spread of disease and parasites; data sheets for live tortoises to record tortoise identification, location, sex, body measurements and activity; health profile forms for documenting and grading physical abnormalities of tortoise posture and movements, general condition (e.g., lethargy, cachexia), external parasites, and clinical abnormalities associated with shell and upper respiratory diseases; permanent photographic records for the retrospective analysis of progression and regression of upper respiratory and eye diseases, analysis of shell lesions and evaluation of growth and age; and indications and methods for salvaging ill or dying tortoises for necropsy evaluation. These guidelines, tested on 5,000 to 20,000 tortoises over a 10 to 27 yr period, were designed to maximize acquisition of data for demographic, ecological, health and disease research projects; to reduce handling and stress of individual animals; to avoid spread of infectious disease; to promote high quality and consistent data sets; and to reduce the duration and number of field trips. The field methods are adapted for desert tortoise life cycle, behavior, anatomy, physiology, and pertinent disease; however the model is applicable to other species of reptiles. Comprehensive databases of clinical signs of disease and health are crucial to research endeavors and essential to decisions on captive release, epidemiology of disease, translocation of wild tortoises, breeding programs, and euthanasia.

Journal of Wildlife Diseases↗