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This is an ARMI Product. Batrachochytrium salamandrivorans and the risk of a second amphibian pandemic
Authors: Yap Tiffany A, Nguyen Natalie T, Serr Megan, Shepack Alexander, Vredenburg Vance T | Date: 2017-11-16 | Outlet: EcoHealth doi.org/10.1007/s10393-017-1278-1
Amphibians are experiencing devastating population declines globally. A major driver is chytridiomycosis, an emerging infectious disease caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Bd was described in 1999 and has been linked with declines since the 1970s, while Bsal is a more recently discovered pathogen that was described in 2013. It is hypothesized that Bsal originated in Asia and spread via international trade to Europe, where it has been linked to salamander die-offs. Trade in live amphibians thus represents a significant threat to global biodiversity in amphibians. We review the current state of knowledge regarding Bsal and describe the risk of Bsal spread. We discuss regional responses to Bsal and barriers that impede a rapid, coordinated global effort. The discovery of a second deadly emerging chytrid fungal pathogen in amphibians poses an opportunity for scientists, conservationists, and governments to improve global biosecurity and further protect humans and wildlife from a growing number of emerging infectious diseases.

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BA Mosher  
This is an ARMI Product. Design- and model-based recommendations for detecting and quantifying an amphibian pathogen in environmental samples
Authors: Mosher BA, Huyvaert KP, Chestnut T, Kerby JL, Madison JD, Bailey LL | Date: 2017-12 | Outlet: Ecology and Evolution | Format: .PDF
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.

This is an ARMI Product. Imperfect pathogen detection from non-invasive skin swabs biases disease inference
Authors: DiRenzo, GV, Grant, EHC, Longo, AV, Che-Castaldo, C, Zamudio, K, Lips, KR
1. Conservation managers rely on accurate estimates of disease parameters, such as pathogen prevalence and infection intensity, to assess disease status of a host population. However, these disease metrics may be biased if low-level infection intensities are missed by sampling methods or laboratory diagnostic tests. These false negatives underestimate pathogen prevalence and overestimate mean infection intensity of infected individuals.

2. Our objectives were two-fold. First, we quantified false negative error rates of Batrachochytrium dendrobatidis on non-invasive skin swabs collected from an amphibian community in El Cop?, Panama. We swabbed amphibians twice in sequence, and we used a recently developed hierarchical Bayesian estimator to assess disease status of the population. Second, we developed a novel hierarchical Bayesian model to simultaneously account for imperfect pathogen detection from field sampling and laboratory diagnostic testing. We evaluated the performance of the model using simulations to quantify the magnitude of bias in estimates of pathogen prevalence and infection intensity.

3. We show that Bd detection probability from skin swabs was related to host infection intensity, where Bd infections < 10 zoospores have < 95 % probability of being detected. If imperfect Bd detection was not considered, then Bd prevalence was underestimated by as much as 16%. In the Bd-amphibian system, this indicates a need to correct for imperfect pathogen detection. More generally, our results have implications for study designs in other disease systems, particularly those with similar objectives, biology, and sampling decisions.

4. Uncertainty in pathogen detection is an inherent property of most sampling protocols and diagnostic tests, where the magnitude of bias depends on the study system, type of infection, and false negative error rates. Given that it may be difficult to know this information in advance, we advocate that the most cautious approach is to assume all errors are possible and to accommodate them by adjusting sampling designs. The modeling framework presented here improves the accuracy in estimating pathogen prevalence and infection intensity.

This is an ARMI Product. A pesticide paradox: Fungicides indirectly increase fungal infections
Authors: Rohr JR, Brown J, Battaglin WA, McMahon TA, Relyea RA | Date: 2017-07-28 | Outlet: Ecological Applications, in press DOI: 10.1002/eap.1607
Abstract. There are many examples where the use of chemicals have had profound unanticipated consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis (Bd), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog (Osteopilus septentrionalis) tadpoles exposed simultaneously to any of these fungicides and Bd, and fungicide exposure actually increased Bd-induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd-induced mortality when challenged with Bd post-metamorphosis, an average of 71 days after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog (Litoria booroolongensis) more susceptible to Bd. Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd, these results suggest that, if fungicides do not completely eradicate Bd or if Bd re-colonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

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USGS Point Reyes  
This is an ARMI Product. Population Trends, Survival, and Sampling Methodologies for a Population of Rana draytonii
Authors: Fellers GM, Kleeman PM, Miller DAW, Halstead BJ | Date: 2017-11-09 | Outlet: Journal of Herpetology 51:567-573 | Format: URL
Estimating population trends provides valuable information for resource managers, but monitoring programs face trade-offs between the quality and quantity of information gained and the number of sites surveyed. We compared the effectiveness of monitoring techniques for estimating population trends of Rana draytonii at Point Reyes National Seashore, California, USA, over a 13-year period. Our primary goals were 1) to estimate trends for a focal pond at Point Reyes National Seashore, and 2) to evaluate whether egg mass counts could reliably estimate an index of abundance relative to more intensive capture-mark-recapture methods. Capture-mark-recapture surveys of males indicated a stable population from 2005 through 2009, despite low annual apparent survival (26.3%). Egg mass counts from 2000 through 2012 indicated that despite some large fluctuations, the breeding female population was generally stable or increasing, with annual abundance varying between 26 and 130 individuals. Minor modifications to egg mass counts, such as marking egg masses, can allow estimation of egg mass detection probabilities necessary to convert counts to abundance estimates, even when closure of egg mass abundance cannot be assumed within a breeding season. High egg mass detection probabilities (mean per-survey detection probability = 0.98 [0.89-0.99]) indicate that egg mass surveys can be an efficient and reliable method for monitoring population trends of federally threatened R. draytonii. Combining egg mass surveys to estimate trends at many sites with capture-mark-recapture methods to evaluate factors affecting adult survival at focal populations is likely a profitable path forward to enhance understanding and conservation of R. draytonii.

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Brown C  
This is an ARMI Product. Identifying Species Conservation Strategies to Reduce Disease-Associated Declines
Authors: Gerber B, Converse S, Muths E, Crokett H, Mosher B, Larissa B | Date: 2017 | Outlet: Conservation Letters | Format: .PDF
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.

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P Bartelt  
This is an ARMI Product. Response of anurans to wetland restoration on a midwestern agricultural landscape
Authors: Bartelt P E, Klaver R W | Date: 2017-09-01 | Outlet: Journal of Herpetology 51:504-514 | Format: .PDF
Since the early 1990s, > 5,000 ha of historic wetlands (and adjacent prairie)
have been restored on the row-crop agricultural landscape of Winnebago County, Iowa, USA.
From 2008?2011, we surveyed 22 of these sites for probabilities of occupancy and colonization
by Boreal Chorus Frogs (BCF; Pseudacris maculata), Northern Leopard Frogs (NLF; Lithobates
pipiens), and American Toads (AT; Anaxyrus americanus). We used radio telemetry to measure
patterns of movement and habitat use by 22 NLF and 54 AT, and deployed biophysical models
in available habitats to estimate their physiological costs. BCF occupied 100% of restored
wetlands; NLF and AT occupied 59?91% and 71?89%, respectively, varying according to annual
weather conditions. BCF colonized new sites within a year; NLF and AT required 3 and 2 yr,
respectively.

This is an ARMI Product. Declines revisited: long-term recovery and spatial population dynamics of tailed frog larvae after wildfire
Authors: Hossack BR, Honeycutt RK | Outlet: Biological Conservation
Drought has fueled an increased frequency and severity of large wildfires in many ecosystems. Despite an increase in research on wildfire effects on vertebrates, the vast majority of it has focused on short-term (<5 yrs) effects and there is still little information on the time scale of population recovery for species that decline in abundance after fire. In 2003, a large wildfire in Montana (USA) burned the watersheds of four of eight streams that we sampled for larval Rocky Mountain tailed frogs (Ascaphus montanus) in 2001. Surveys during 2004?2005 revealed reduced abundance of larvae in burned streams relative to unburned streams, with greater declines associated with increased fire extent. Rocky Mountain tailed frogs have low vagility and have several unusual life-history traits that could slow population recovery, including an extended larval period (4 yrs), delayed sexual maturity (6?8 yrs), and low fecundity (<50 eggs/yr). To determine if abundance remained depressed since the 2003 wildfire, we repeated surveys during 2014?2015 and found relative abundance of larvae in burned and unburned streams had nearly converged to pre-fire conditions within two generations. The negative effects of burn extent on larval abundance weakened >58% within 12 yrs after the fire. We also found moderate synchrony among populations in unburned streams and negative spatial autocorrelation among populations in burned streams. We suspect negative spatial autocorrelation among spatially-clustered burned streams reflected increased post-fire patchiness in resources and different rates of local recovery. Our results add to a growing body of work that suggests populations in intact ecosystems tend to be resilient to habitat changes caused by wildfire. Our results also provide important insights into recovery times of populations that have been negatively affected by severe wildfire.

This is an ARMI Product. Pathogenic lineage of Perkinsea causes mass mortality of frogs across the United States
Authors: Isidoro-Ayza M, Lorch JM, Grear DA, Winzeler M, Calhoun DL, Barichivich W | Date: 2017-08-31 | Outlet: Scientific Reports 7, Article number: 10288 | Format: .PDF
Emerging infectious diseases such as chytridiomycosis and ranavirus infections are considered important contributors to the worldwide decline of amphibian populations. We reviewed data on 247 anuran mortality events in 43 states of the United States from 1999 ? 2015. Our findings suggest that a severe infectious disease of tadpoles caused by a protist belonging to the phylum Perkinsea might represent the third most common infectious disease of anurans after ranavirus infections and chytridiomycosis. Severe Perkinsea infections (SPI) were systemic and led to multiorganic failure and death. The SPI mortality events affected numerous anuran species and occurred over a broad geographic area, from boreal to subtropical habitats. Livers from all PCR-tested SPI-tadpoles were positive for the Novel Alveolate Group 01 (NAG01) of Perkinsea, while only 2.5% of apparently normal tadpole livers tested positive, suggesting that subclinical infections are uncommon. Phylogenetic analysis demonstrated that SPI is associated with a genetically distinct clade of NAG01 Perkinsea. These data suggest that this virulent Perkinsea clade is an important pathogen of frogs in the United States. Given its association with mortality events and tendency to be overlooked, the potential role of this emerging pathogen in amphibian declines on a broad geographic scale warrants further investigation

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This is an ARMI Product. Early action to address an emerging wildlife disease
Authors: Adams MJ, Harris MC, Grear DA | Date: 2017-02 | Outlet: USGS Fact Sheet | Format: .PDF
Although not yet detected in the United States, the emergence of Bsal (a fungal pathogen) 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 concern expressed by resource management agencies, the U. S. Geological Survey has made Bsal and similar pathogens a priority for research.


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