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Western palearctic salamander susceptibility to the skin disease caused by the amphibian chytrid fungus Batrachochytrium salamandrivorans (Bsal) was recognized in 2014, eliciting concerns for a potential novel wave of amphibian declines following the B. dendrobatidis (Bd) chytridiomycosis global pandemic. Although Bsal had not been detected in North America, initial experimental trials supported the heightened susceptibility of caudate amphibians to Bsal chytridiomycosis, recognizing the critical threat this pathogen poses to the North American salamander biodiversity hotspot. Here, we take stock of 10 years of research, collaboration, engagement, and outreach by the North American Bsal Task Force. We summarize main knowledge and conservation actions to both forestall and respond to Bsal invasion into North America. We address the questions: what have we learned; what are current challenges; and are we ready for a more effective reaction to Bsal’s eventual detection? We expect that the many contributions to preemptive planning accrued over the past decade will pay dividends in amphibian conservation effectiveness and can inform future responses to other novel wildlife diseases and extreme threats.

Wildlife disease management decisions often require rapid responses to situations that are fraught with uncertainty. By recognizing that management is implemented to achieve specific objectives (whether defined explicitly or not), resource managers and science partners can identify an analysis technique and develop a plan to collect necessary data that will allow for the evaluation of management actions.

Western palearctic salamander susceptibility to the skin disease caused by the amphibian chytrid fungus Batrachochytrium salamandrivorans (Bsal) was recognized in 2014, eliciting concerns for a potential novel wave of amphibian declines following the B. dendrobatidis (Bd) chytridiomycosis global pandemic. Although Bsal had not been detected in North America, initial experimental trials supported the heightened susceptibility of caudate amphibians to Bsal chytridiomycosis.

1. Surveillance programs are essential for detecting emerging pathogens and often rely on molecular methods to make inference about the presence of a target disease agent. However, molecular methods rarely detect target DNA perfectly. For example, molecular pathogen detection methods can result in misclassification (i.e., false positives and false negatives) or partial detection errors (i.e., detections with ‘ambiguous’, ‘uncertain’, or ‘equivocal’ results). Then, when data are to be analyzed, these?partial observations?are?either?discarded?or censored;?this, however, disregards information that could be used to make inference about the true state of the system. There is a critical need for more direction and guidance related to how many samples is enough to declare a unit of interest ‘pathogen-free’.
2. Here, we develop a Bayesian hierarchal framework that accommodates false negative, false positive, and uncertain detections to improve inference related to the occupancy of a pathogen. We apply our modeling framework to a case study of the fungal pathogen Pseudogymnoascus destructans (Pd) identified in Texas bats at the invasion front of white-nose syndrome. To improve future surveillance programs, we provide guidance on sample sizes required to be 95% certain a target organism is absent from a site.
3. We found that the presence of uncertain detections increased the variability of resulting posterior probability distributions of pathogen occurrence, and that our estimates of required sample size were very sensitive to prior information about pathogen occupancy, pathogen prevalence, and diagnostic test specificity. In the Pd case study, we found that the posterior probability of occupancy was very low in 2018, but occupancy probability approached 1 in 2020, reflecting increasing prior probabilities of occupancy and prevalence elicited from the site manager.
4. Our modeling framework provides the user a posterior probability distribution of pathogen occurrence, which allows for subjective interpretation by the decision-maker. To help readers apply and use the methods we developed, we provide an interactive?RShiny?app?that generates target species?occupancy estimation and sample size estimates to make these methods more accessible?to the scientific community (https://rmummah.shinyapps.io/ambigDetect_sampleSize).?This modeling framework and sample size guide may be useful for improving inferences from molecular surveillance data about emerging pathogens, non-native invasive species, and endangered species where misclassifications and ambiguous detections occur.

The problem of global amphibian declines has prompted extensive research over the last three decades; initially the focus was on identifying and characterizing the extent of the problem, but more recently efforts have shifted to evidence-based research designed to improve conservation outcomes. Using input from participants at the 9th World Congress of Herpetology, a US Geological Survey Powell Center symposium, amphibian listservs, the IUCN Assisted Reproductive Technologies and Gamete Biobanking group, and respondents to a survey, we developed a list of 25 priority research questions for amphibian conservation at this stage of the Anthropocene. These research needs represent critical knowledge gaps for amphibian conservation.

Data used in manuscript that examines several potential factors influencing disease dynamics in the boreal toad–disease system: geographic isolation of populations, amphibian community richness, elevational differences, and habitat permanence.

Emerging infectious disease outbreaks are one of multiple stressors responsible for amphibian declines globally. In the northeastern United States, ranaviral diseases are prevalent in amphibians and other ectothermic species, but there is still uncertainty as to whether their presence is leading to population level effects. Further, there is also uncertainty surrounding the potential interactions among disease infection prevalence in free-ranging animals and habitat degradation (co-occurrence of chemical stressors). The current study was designed to provide field-based estimates of the relationship between amphibian disease and chemical stressors. We visited 40 wetlands across three protected areas, estimated the prevalence of ranavirus among populations of larval wood frogs and spotted salamanders, and assessed chemical and biological stressors in wetland habitats and larval amphibians using a suite of selected bioassays, screening tools and chemical analyses. Estimated ranavirus occupancy varied among the three protected areas and ranged from https://0.27 to https://0.55 with considerable variation within protected area. Of the stressors evaluated, ranavirus prevalence was strongly and positively related to concentrations of metalloestrogens (metals with the potential to bind to estrogen receptors) and total metals in wetland sediments and weakly and negatively related to total pesticide concentrations in larval amphibians. These results can be used by land managers to refine habitat assessments to include such environmental factors with the potential to influence disease susceptibility.

The emerging amphibian pathogen Batrachochytrium salamandrivorans (Bsal) is a severe threat to global urodelan (salamanders, newts, and related taxa) biodiversity. Bsal has not been detected, to date, in North America, but the risk is high because North America is one of the global hotspots for urodelan biodiversity. The North American and United States response to the discovery of Bsal in Europe was to take a risk-based approach to preventive management actions, including interim regulations on importation of captive salamanders and a large-scale surveillance effort. Risk-based approaches to decision-making can extend to adaptive management cycles by periodically incorporating new information that reduces uncertainty in an estimate of risk or to assess the effect of mitigation actions which reduce risk directly. Our objectives were to evaluate the effects of regulatory action on the introduction of Bsal to the U.S., quantify how a large-scale surveillance effort impacted consequence risk, and to combine other new information on species susceptibility to re-evaluate Bsal risk to the U.S. Import regulations effectively reduced import volume of targeted species, but new research on species susceptibility suggests the list of regulated species was incomplete regarding Bsal reservoir species. Not detecting Bsal in an intensive surveillance effort improved confidence that Bsal was not present, however, the overall risk-reduction impact was limited because of the expansive area of interest (conterminous United States) and limited time frame of sampling. Overall, the preventive actions in response to the Bsal threat did reduce Bsal risk in the U.S. and we present an updated risk assessment to provide information for adaptive decision-making.

Biodiversity loss is a major threat to the integrity of ecosystems and is projected to
worsen, yet the path to successful conservation remains elusive. Decision support
frameworks (DSFs) are increasingly applied by resource managers to navigate the
complexity, uncertainty, and differing socio-ecological objectives inherent to
conservation problems. Most published conservation research that uses DSFs focuses
on analytical stages (e.g., identifying an optimal decision), making it difficult to assess
and learn from previous examples in a conservation practice context. Here, we (1)
evaluate the relationship between the application of decision science and the resulting
conservation outcomes, and (2) identify and address existing barriers to the application
of DSFs to conservation practice. To do this, we develop a framework for evaluating
conservation initiatives using decision science that emphasizes setting attainable
goals, building momentum, and obtaining partner buy-in. We apply this framework to a
systematic review of amphibian conservation decision support projects, including a
follow-up survey of the pertinent conservation practitioners, stakeholders, and
scientists. We found that all projects identified optimal solutions to reach stated
objectives, but positive conservation outcomes were limited when implementation
challenges arose. Further, we identified multiple barriers (e.g., dynamic and
hierarchical leadership, scale complexity, limited resource availability) that can inhibit
the progression from decision identification to action implementation (i.e., ‘decision-implementation gap’), and to successful conservation outcomes. Based on these results, we provide potential actionable steps and avenues for future development of DSFs to facilitate the transition from decision to action and the realization of conservation successes.

Understanding the demographic consequences of interactions among pathogens, hosts, and weather conditions is critical in determining how amphibian populations respond to disease and in identifying site-specific conservation actions that can be developed to bolster persistence of amphibian populations. We investigated population dynamics in Boreal Toads relative to abiotic (fall temperatures and snowpack) and biotic (the abundance of another anuran host and disease) characteristics of the local environment in Wyoming, USA. We used capture-recapture data and a multi-state model where state is treated as a hidden Markov process to incorporate disease state uncertainty and assess our a priori hypotheses. Our results indicate that snowpack during the coldest week of the winter is more influential to toad survival, disease transition probabilities, and the population-level prevalence of the amphibian chytrid fungus (Batrachochytrium dendrobatidis) in the spring, than temperatures in the fall or the presence of another host. As hypothesized, apparent survival at low (i.e., <25 cm) snowpack (https://0.22 [CI: 0.15–0.31]) was lower than apparent survival at high snowpack (https://90.65 [CI: 0.50–0.78]). Our findings highlight the potential for local environmental factors, like snowpack, to influence disease and host persistence, and demonstrate the ecological complexity of disease effects on population demography in natural environments. This work further emphasizes the need for improved understanding of how climate change may influence the relationships among pathogens, hosts, and their environment for wild animal populations challenged by disease.

Despite increasing interest in determining the population-level effects of emerging infectious diseases on wildlife, estimating effects of disease on survival rates remains difficult. Even for a well-studied disease such as amphibian chytridiomycosis (caused by the fungus Batrachochytrium dendrobatidis [Bd]), there are few estimates of how survival of wild hosts is affected. We applied hierarchical models to long-term capture-mark-recapture data (mean&#8239;=&#8239;10.6&#8239;yrs, range&#8239;=&#8239;6?15&#8239;yrs) from >5500 uniquely-marked individuals to estimate the effect of Bd on apparent survival of four threatened or endangered ranid frog species (Rana draytonii, R. muscosa, R. pretiosa, R. sierrae) at 14 study sites in California and Oregon (USA) and one bufonid toad (Anaxyrus boreas) at two study sites in Wyoming and Montana. Our models indicated that the presence of Bd on an individual reduced apparent survival of ranid frogs by ~6?15% depending on species and sex. The estimated difference between toads with and without Bd was 19% for the Montana population and 55% for the Wyoming population; however, the 95% Credible Interval of these estimates included zero. These results provide evidence for negative effects of Bd on survival in wild populations even in the absence of obvious die-offs. Determining what factors influence the magnitude of the effects of Bd on wildlife populations is an important next step toward identifying management actions. These estimates of Bd effects are important for understanding the extent and severity of disease, whether disease effects have changed over time, and for informing management actions.

Molecular techniques are powerful conservation tools used in applications ranging from early detection of invasive species to understanding host-pathogen dynamics. However, communication barriers among resource managers, ecologists, and laboratories often preclude the efficient use of molecular data for ecological inference and conservation decision-making. The disconnect largely stems from a lack of specific knowledge about the approaches, decisions, methods, and terminology that each partner uses. As a result, data generated by molecular assays are sometimes of limited utility to managers. We outline a collaborative framework to assist partners with different areas of expertise to more effectively translate their scientific and management needs to other partners. The use of molecular methods in conservation science will continue to expand; therefore, the aim of our paper is to enable the conservation community to harness the full utility of these methods by developing effective collaborative partnerships among managers, ecologists, and laboratory scientists.

Understanding the distribution of pathogens across landscapes and within host populations is a common aim of wildlife managers. Despite the need for unbiased inferences about these parameters to plan effective management interventions, many researchers fail to account for imperfect pathogen detection and instead report only raw data, which may lead to improper management. We demonstrate analyses of ranavirus detection data in the Patuxent Research Refuge using an occupancy modeling approach, which yields unbiased estimates of pathogen occurrence and prevalence. To improve inference and reporting of pathogen and disease parameters, we describe our approach in-text and provide a written tutorial on how to fit these models using the freely available software Program PRESENCE. In our case study, ranavirus prevalence was underestimated up to 30% if imperfect detection was ignored. After accounting for imperfect detection, estimates of ranavirus prevalence in larval wood frogs (Lithobates sylvaticus) were higher than in larval spotted salamanders (Ambystoma maculatum). In addition, we found that the odds of detecting ranavirus in tail samples were 6.7 times higher than detecting ranavirus in liver samples. We discuss how this information can be used to design ranavirus surveillance studies. Our tutorial provides a clear guide for practitioners and researchers wishing to make unbiased inference in a variety of host-pathogen systems.

Understanding the ecosystem-level persistence of pathogens is essential for predicting
and measuring host-pathogen dynamics. However, this process is often masked, in
part due to a reliance on host-based pathogen detection methods. The amphibian
pathogens Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are
pathogens of global conservation concern. Despite having free-living life stages, little is
known about the distribution and persistence of these pathogens outside of their
amphibian hosts. We combine historic amphibian monitoring data with contemporary
host- and environment-based pathogen detection data to obtain estimates of Bd
occurrence independent of amphibian host distributions. We also evaluate differences
in filter- and swab-based detection probability and assess inferential differences arising
from using different decision criteria used to classify samples as positive or negative.
Water filtration-based detection probabilities were lower than those from swabs but
were >10%, and swab-based detection probabilities varied seasonally, declining in the
early fall. The decision criterion used to classify samples as positive or negative was
important; using a more liberal criterion yielded higher estimates of Bd occurrence than
when a conservative criterion was used. Different covariates were important when
using the liberal or conservative criterion in modeling Bd detection. We found evidence
of long-term Bd persistence for several years after an amphibian host species of
conservation concern, the boreal toad (Anaxyrus boreas boreas), was last detected.
Our work provides evidence of long-term Bd persistence in the ecosystem and
underscores the importance of environmental samples for understanding and
mitigating disease-related threats to amphibian biodiversity.

Emerging infectious diseases are an increasingly common threat to wildlife. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), is an emerging infectious disease that has been linked to amphibian declines around the world. Few studies exist that explore amphibian-Bd dynamics at the landscape scale, limiting our ability to identify which factors are associated with variation in population susceptibility and to develop effective in situ disease management. Declines of boreal toads (Anaxyrus boreas boreas) in the Southern Rocky Mountains are largely attributed to chytridiomycosis but variation exists in local extinction of boreal toads across this metapopulation. Using a large-scale historic dataset, we explored several potential factors influencing disease dynamics in the boreal toad-Bd system: geographic isolation of populations, amphibian community richness, elevational differences, and habitat permanence. We found evidence that boreal toad extinction risk was lowest at high elevations where temperatures may be sub-optimal for Bd growth and where small boreal toad populations may be below the threshold needed for efficient pathogen transmission. In addition, boreal toads were more likely to recolonize high elevation sites after local extinction, again suggesting that high elevations may provide refuge from disease for boreal toads. We illustrate a modeling framework that will be useful to natural resource managers striving to make decisions in amphibian-Bd systems.

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.

The calls of frogs on warm nights in the spring are a welcome sound, telling listeners that the seasons are changing and summer is coming. Today, however, ponds that once echoed with the chirps, chuckles and calls of frogs and toads are falling silent around the world.

This loss is worrying. Amphibians are the environment's canaries in the coal mine. Their declines provide early warning signs to scientists that stressors like habitat loss, climate change, pollution and disease are making ecosystems unhealthy. Without amphibians, insect and algae populations multiply, causing cascading effects on other organisms ? including humans...

Read full article here: https://theconversation.com/saving-amphibians-from-a-deadly-fungus-means-acting-without-knowing-all-the-answers-81739

Associated ARMI publication: https://armi.usgs.gov/search/results.php?productid=184774

Emerging infectious diseases (EIDs) are a salient threat to many animal taxa, causing local and global extinctions, altering communities and ecosystem function. The EID chytridiomycosis is a prominent driver of amphibian declines, which is caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). To guide conservation policy, we developed a predictive decision-analytic model that combines empirical knowledge of host-pathogen metapopulation dynamics with expert judgment regarding effects of management actions, to select from potential conservation strategies. We apply our approach to a boreal toad (Anaxyrus boreas boreas) and Bd system, identifying optimal strategies that balance tradeoffs in maximizing toad population persistence and landscape-level distribution, while considering costs. The most robust strategy is expected to reduce the decline of toad breeding sites from 53% to 21% over 50 years. Our findings are incorporated into management policy to guide conservation planning. Our online modeling application provides a template for managers of other systems challenged by EIDs.

Our work is motivated by the impacts of the emerging infectious disease chytridiomycosis, a disease of amphibians that associated with declines of many species worldwide. Using this host-pathogen system as a general example, we first illustrate how misleading inferences can result from failing to incorporate pathogen dynamics into the modeling process, especially when the pathogen is difficult or impossible to survey in the absence of a host species. We found that traditional modeling techniques can underestimate the effect of a pathogen on host species occurrence and dynamics when the pathogen can only be detected in the host, and pathogen information is treated as a covariate. We propose a dynamic multistate modeling approach that is flexible enough to account for the detection structures that may be present in complex multistate systems, especially when the sampling design is limited by a species’ natural history or sampling technology.