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Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans . Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes.

Conservation Science and Practice

Early action to address an emerging wildlife disease

A deadly fungal pathogen, Batrachochytrium salamandrivorans ( Bsal ) that affects amphibian skin was discovered during a die-off of European fire salamanders ( Salamandra salamandra ) in 2014. This pathogen has the potential to worsen already severe worldwide amphibian declines. Bsal is a close relative to another fungal disease known as Batrachochytrium dendrobatidis ( Bd ). Many scientists consider Bd to be the greatest threat to amphibian biodiversity of any disease because it affects a large number of species and has the unusual ability to drive species and populations to extinction. Although not yet detected in the United States, the emergence of Bsal could threaten the salamander population, which is the most diverse in the world. The spread of Bsal likely will lead to more State and federally listed threatened or endangered amphibian species, and associated economic effects. Because of the concern expressed by resource management agencies, the U.S. Geological Survey (USGS) has made Bsal and similar pathogens a priority for research.

Fact Sheet

Wildlife diseases

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Southeastern Veterinarian

Soil reservoir dynamics of ophidiomyces ophidiicola, the causative agent of snake fungal disease

Wildlife diseases pose an ever-growing threat to global biodiversity. Understanding how wildlife pathogens are distributed in the environment and the ability of pathogens to form environmental reservoirs is critical to understanding and predicting disease dynamics within host populations. Snake fungal disease (SFD) is an emerging conservation threat to North American snake populations. The causative agent, Ophidiomyces ophidiicola (Oo), is detectable in environmentally derived soils. However, little is known about the distribution of Oo in the environment and the persistence and growth of Oo in soils. Here, we use quantitative PCR to detect Oo in soil samples collected from five snake dens. We compare the detection rates between soils collected from within underground snake hibernacula and associated, adjacent topsoil samples. Additionally, we used microcosm growth assays to assess the growth of Oo in soils and investigate whether the detection and growth of Oo are related to abiotic parameters and microbial communities of soil samples. We found that Oo is significantly more likely to be detected in hibernaculum soils compared to topsoils. We also found that Oo was capable of growth in sterile soil, but no growth occurred in soils with an active microbial community. A number of fungal genera were more abundant in soils that did not permit growth of Oo, versus those that did. Our results suggest that soils may display a high degree of both general and specific suppression of Oo in the environment. Harnessing environmental suppression presents opportunities to mitigate the impacts of SFD in wild snake populations.

Journal of Fungi

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Wildlife diseases are a major global threat to biodiversity. Boreal toads ( Anaxyrus [Bufo] boreas ) are a state-endangered species in the southern Rocky Mountains of Colorado and New Mexico, and a species of concern in Wyoming, largely due to lethal skin infections caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis ( Bd ). We performed conservation and landscape genomic analyses using single nucleotide polymorphisms from double-digest, restriction site-associated DNA sequencing in combination with the development of the first boreal toad (and first North American toad) reference genome to investigate population structure, genomic diversity, landscape connectivity and adaptive divergence. Genomic diversity ( π = 0.00034–0.00040) and effective population sizes ( N e = 8.9–38.4) were low, likely due to post-Pleistocene founder effects and Bd -related population crashes over the last three decades. Population structure was also low, likely due to formerly high connectivity among a higher density of geographically proximate populations. Boreal toad gene flow was facilitated by low precipitation, cold minimum temperatures, less tree canopy, low heat load and less urbanization. We found >8X more putatively adaptive loci related to Bd intensity than to all other environmental factors combined, and evidence for genes under selection related to immune response, heart development and regulation and skin function. These data suggest boreal toads in habitats with Bd have experienced stronger selection pressure from disease than from other, broad-scale environmental variations. These findings can be used by managers to conserve and recover the species through actions including reintroduction and supplementation of populations that have declined due to Bd .

Colorado

The role of native birds and other wildlife on the emergence of zoonotic diseases

Wildlife can be an important source of transmission of infectious disease to humans. One potential transmission route involves hunting and fishing, both common activities in the United States and worldwide. For example, during 1996, approximately 11 million Americans, about 40 percent of the total population 16 years of age and older, took part in some recreational activity relating to wildlife and fish. Another potential route of infection focuses on urban and suburban environments. These locations are of special concern because of their increasing role as wildlife habitat, the greater interface between humans and wildlife that takes place within those environments, the paucity of knowledge about disease in those wildlife populations, and the general lack of orderly management for wildlife within those environments. In the wild, several trends are contributing to the growing importance of zoonotic diseases. First, the spectrum of infectious diseases affecting wildlife today is greater than at any time during the previous century. Second, the occurrence of infectious diseases has changed, from sporadic, self-limiting outbreaks that generally resulted in minor losses to frequently occurring events that generally result in major losses of wildlife. Third, disease emergence has occurred on a worldwide scale in a broad spectrum of wildlife species and habitats. Given the scope of the problem, current disease surveillance efforts are inadequate. Few state wildlife agencies allocate personnel and resources to address wildlife disease, despite their statutory responsibility for managing nonmigratory wildlife. Some state agencies provide minimal support for regional programs based at universities. At the federal level, the primary surveillance effort is conducted by the National Wildlife Health Center, operated by the U.S. Geological Survey. Outside of government, some veterinary schools, agriculture diagnostic laboratories, and other programs provide additional information on animal diseases, primarily by examining carcasses of dead wildlife submitted for analysis, and individual university-based researchers carry out a variety of studies. Typically, information about the occurrence of disease in free-ranging wildlife is derived from surveys and mortality events in areas where wildlife observations by agencies and the public are frequent enough to detect their occurrence before carcasses are removed by scavengers and predatory animals. The result is that disease occurrence is grossly underreported, heavily biased toward mortality events, and biased toward species of special concern and interest, such as game and endangered species. Therefore, the available information should be viewed as the “proverbial tip of the iceberg” relative to disease activity within wildlife populations.

National Academy of Science.

A coupled human and natural systems framework to characterize emerging infectious diseases: The case of fibropapillomatosis in marine turtles

Emerging infectious diseases of wildlife have markedly increased in the last few decades. Unsustainable, continuous, and rapid alterations within and between coupled human and natural systems have significantly disrupted wildlife disease dynamics. Direct and indirect anthropogenic effects, such as climate change, pollution, encroachment, urbanization, travel, and trade, can promote outbreaks of infectious diseases in wildlife. We constructed a coupled human and natural systems framework identifying three main wildlife disease risk factors behind these anthropogenic effects: (i) immune suppression, (ii) viral spillover, and (iii) disease propagation. Through complex and convoluted dynamics, each of the anthropogenic effect listed in our framework can lead, to some extent, to one or more of the identified risk factors accelerating disease outbreaks in wildlife. In this review, we present a novel framework to study anthropogenic impacts within coupled human and natural systems that facilitate emergence of infectious disease involving wildlife. We demonstrate the utility of the framework by applying it to Fibropapillomatosis disease of marine turtles. We aim to articulate the intricate and complex nature of anthropogenically-exacerbated wildlife infectious diseases as multifactorial. This paper supports the adoption of a One Health approach and invites the collaboration of multiple disciplines for the achievement of effective and long-lasting conservation and wildlife emerging diseases mitigation outcomes.

Animals

Emerging and reemerging diseases of avian wildlife

Of the many important avian wildlife diseases, aspergillosis, West Nile virus, avipoxvirus, Wellfleet Bay virus, avian influenza, and inclusion body disease of cranes are covered in this article. Wellfleet Bay virus, first identified in 2010, is considered an emerging disease. Avian influenza and West Nile virus have recently been in the public eye because of their zoonotic potential and links to wildlife. Several diseases labeled as reemerging are included because of recent outbreaks or, more importantly, recent research in areas such as genomics, which shed light on the mechanisms whereby these adaptable, persistent pathogens continue to spread and thrive.

Veterinary Clinics of North America: Exotic Animal

Global trends in emerging viral diseases of wildlife origin

Fifty years ago, infectious diseases were rarely considered threats to wildlife populations, and the study of wildlife diseases was largely a neglected endeavor. Furthermore, public health leaders at that time had declared that “it is time to close the book on infectious diseases and the war against pestilence won,” a quote attributed to Dr. William H. Stewart in 1967. There is some debate whether he actually said these words; however, they reflect the widespread belief at that time (Spellberg, 2008). Leap forward to today, and the book on infectious diseases has been dusted off. There is general consensus that the global environment favors the emergence of infectious diseases, and in particular, diseases of wildlife origin (Taylor et al., 2001). Examples of drivers of these infectious diseases include climate and landscape changes, human demographic and behavior changes, global travel and trade, microbial adaptation, and lack of appropriate infrastructure for wildlife disease control and prevention (Daszak et al., 2001). The consequences of these emerging diseases are global and profound with increased burden on the public health system, negative impacts on the global economy and food security, declines and extinctions of wildlife species, and subsequent loss of ecosystem integrity. For example, 35 million people are currently living with HIV infection globally (http://www.who.int/gho/hiv/en); 400 million poultry have been culled since 2003 as a result of efforts to control highly pathogenic H5N1 avian influenza (http://www.fao.org/avianflu/en/index.html), and there are increasing biological and ecological consequences. Examples of health threats to biodiversity include the “spillover” of human diseases to great ape populations (Köndgen et al., 2008), the near-extirpation of the black-footed ferret from canine distemper and sylvatic plague (for a review see Abbott et al., 2012), and threats to Hawaiian forest birds from introduced pathogens such as avian malaria and avian pox (van Riper et al., 1986, 2002). There are also newly discovered pathogens or diseases that have resulted in population declines, and global extinctions of several species. Examples include Batrachochytrium dendrobatidis, which causes a cutaneous fungal infection of amphibians and is linked to declines of amphibians globally (Kriger and Hero, 2009); and recently discovered Pseudogymnoascus (Geomyces) destructans, the etiologic agent of white-nose syndrome (WNS), which has caused precipitous declines of North American bat species (Blehert et al., 2009). Furthermore, there is increasing evidence of the subsequent impacts on human and ecosystem health; for example, increasing risk of exposure to Lyme disease as a consequence of decreased biodiversity (LoGiudice et al., 2003) as well as the economic cost of the loss of bats due to decreased insect control services (Boyles et al., 2011). Figure A12-1 is a timeline of important diseases investigated by the U.S. Geological Survey since the 1970s, which illustrates three factors: 1. The unprecedented emergence of new pathogens and geographic spread of known pathogens since the 1990s; 2. Diseases are increasingly causing large-scale, negative impacts on wildlife populations and spreading over larger geographic areas rather than remaining localized; and 3. Diseases are increasingly of concern for multiple sectors, including public health, agriculture and wildlife management agencies. Of increasing concern are these novel diseases such as WNS as they are hard to anticipate, particularly devastating to human health or wildlife populations, challenging to manage, spread over large geographic areas in short time periods, and may result in ecological ripple effects that are difficult to predict. The following article provides examples of recently emerged viral diseases of wildlife origin. The examples have been selected to illustrate the drivers of emerging viral diseases, both novel pathogens and previously known diseases, the impacts of these diseases, as well as the role of wildlife both as “villains” or reservoirs as well as “victims” of these viral diseases. The article also discusses potential management strategies for emerging viral diseases in wildlife populations and future science directions in wildlife health to prevent, prepare, respond to, and recover from these disease events. Finally, the concept of One Health and its potential role in developing solutions to these issues of mutual concern is discussed.

Conference Paper

Contact and contagion: Probability of transmission given contact varies with demographic state in bighorn sheep

Understanding both contact and probability of transmission given contact are key to managing wildlife disease. However, wildlife disease research tends to focus on contact heterogeneity, in part because the probability of transmission given contact is notoriously difficult to measure. Here, we present a first step towards empirically investigating the probability of transmission given contact in free-ranging wildlife. We used measured contact networks to test whether bighorn sheep demographic states vary systematically in infectiousness or susceptibility to Mycoplasma ovipneumoniae , an agent responsible for bighorn sheep pneumonia. We built covariates using contact network metrics, demographic information and infection status, and used logistic regression to relate those covariates to lamb survival. The covariate set contained degree, a classic network metric describing node centrality, but also included covariates breaking the network metrics into subsets that differentiated between contacts with yearlings, ewes with lambs, and ewes without lambs, and animals with and without active infections. Yearlings, ewes with lambs, and ewes without lambs showed similar group membership patterns, but direct interactions involving touch occurred at a rate two orders of magnitude higher between lambs and reproductive ewes than between any classes of adults or yearlings, and one order of magnitude higher than direct interactions between multiple lambs. Although yearlings and non-reproductive bighorn ewes regularly carried M. ovipneumoniae , our models suggest that a contact with an infected reproductive ewe had approximately five times the odds of producing a lamb mortality event of an identical contact with an infected dry ewe or yearling. Consequently, management actions targeting infected animals might lead to unnecessary removal of young animals that carry pathogens but rarely transmit. This analysis demonstrates a simple logistic regression approach for testing a priori hypotheses about variation in the odds of transmission given contact for free-ranging hosts, and may be broadly applicable for investigations in wildlife disease ecology.

Journal of Animal Ecology

Wildlife health and disease investigations

Wildlife population management requires knowledge of factors that affect population sustainability. Mortality is one of the most important of those factors. Without a clear understanding of the causes of mortality, decisions by managers of whether or how to intercede may be inappropriate. Wildlife biologists are usually the first to discover, assess, and respond to wildlife mortality. Biologists who make accurate, complete and timely field investigations, and proper collection and shipment of samples to a diagnostic facility are essential for an accurate diagnosis. In combination with wildlife disease specialists, biologists can identify causes of wildlife mortality, detect long-term patterns in factors that affect the survival of populations, and take appropriate corrective action to minimize the impact of some mortality factors on wildlife populations.

Book chapter

Identifying common decision problem elements for the management of emerging fungal diseases of wildlife

Emerging infectious diseases (EIDs) of wildlife have characteristics that make them difficult to manage, leading to reactive and often ineffective management strategies. Currently, two fungal pathogens, Pseudogymnoascus destructans (Pd) and Batrachochytrium salamandrivorans (Bsal), are causing declines in novel host species. To improve the application of management strategies addressing the risk of these pathogens to North American wildlife, we queried wildlife managers about their concerns regarding managing populations of bats and amphibians potentially impacted by Pd and Bsal. Using these responses, we identified aspects of each decision problem that were shared across pathogens, regions and agencies – and found similarities in decision-problem elements for disease management. Reframing management problems as decisions can enable managers to identify similarities across EIDs, i.e. uncertainties within management actions, and improve reactive responses if proactive management is not possible. Such an approach recognizes context-specific constraints and identifies relevant uncertainties that must be reduced in developing a response.

Society and Natural Resources

Retrospective analysis of the epidemiologic literature, 1990–2015, on wildlife-associated diseases from the Republic of Korea

To assess the status of research on wildlife diseases in the Republic of Korea (ROK) and to identify trends, knowledge gaps, and directions for future research, we reviewed epidemiologic publications on wildlife-associated diseases in the ROK. We identified a relatively small but rapidly increasing body of literature. The majority of publications were focused on public or livestock health and relatively few addressed wildlife health. Most studies that focused on human and livestock health were cross-sectional whereas wildlife health studies were mostly case reports. Fifteen diseases notifiable to the World Organisation for Animal Health were identified and 21 diseases were identified as notifiable to either the Korean Ministry of Health, Welfare, and Family Affairs or the Korean Ministry of Agriculture. Two diseases were reported as occurring as epidemics; highly pathogenic avian influenza (HPAI) and virulent Newcastle disease. Six diseases or disease agents were described in the literature as emerging including HPAI, rabies, Babesia microti , avian coronaviruses, scrub typhus, and severe fever thrombocytopenia syndrome virus. The diseases for which there were the largest number of publications were HPAI and rabies. The majority of wildlife-associated zoonotic disease publications focused on food-borne parasitic infections or rodent-associated diseases. Several publications focused on the potential of wildlife as reservoirs of livestock diseases; in particular, water deer ( Hydropotes inermis ) and wild boar ( Sus scrofa ). In contrast, there were few publications on diseases of concern for wildlife populations or research to understand the impacts of these diseases for wildlife management. Increased focus on prospective studies would enhance understanding of disease dynamics in wildlife populations. For the high-consequence diseases that impact multiple sectors, a One Health approach, with coordination among the public health, agricultural, and environmental sectors, would be important. This type of review can provide useful information for countries or regions planning or implementing national wildlife health programs.

Journal of Wildlife Diseases