Sistrurus Catenatus Research Articles

Drift, selection and adaptive variation in small populations of a threatened rattlesnake.

An important goal of conservation genetics is to determine if the viability of small populations is reduced by a loss of adaptive variation due to genetic drift. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the eastern massasauga rattlesnake (Sistrurus catenatus), a threatened reptile that exists in small isolated populations. We estimated levels of individual polymorphism in 46 toxin loci and 1,467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation of S.catenatus and its closest relative, the western massasauga (S.tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long- and short-term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that pre-date the effects of recent drift, and that functional variation in these loci persists despite small short-term effective sizes. This suggests that much of the adaptive variation present in populations may represent an example of "drift debt," a nonequilibrium state where present-day levels of variation overestimate the amount of functional genetic diversity present in future populations.

A Long-Term Study on Massasaugas (Sistrurus catenatus) Inhabiting a Partially Mined Peatland: A Standardized Method to Characterize Snake Overwintering Habitat

Temperate snakes occupy overwintering sites for most of their annual life cycle. Microhabitat characteristics of the hibernaculum are largely undescribed, yet are paramount in ensuring snake overwintering survival. We hypothesized that snakes survive hibernation within a vertical subterranean space that we termed a “life zone” (LZ), that is aerobic and flood and frost free throughout winter. We studied an isolated, endangered population of Massasaugas (Sistrurus catenatus) inhabiting an anthropogenically altered peatland and monitored the subterranean habitat during a period of environmental stochasticity. Initial radio telemetry confirmed that snakes moved between altered and natural habitats during the active season and showed hibernation-site fidelity to either habitat. We used a grid of groundwater wells and frost tubes installed in each hibernation area to measure LZ characteristics over 11 consecutive winters. The LZ within the impacted area was periodically reduced to zero during a flood–freeze cycle, but the LZ in the natural area was maintained. Model selection analysis revealed that soil depth and flood status best predicted LZ size. Thermal buffering and groundwater dissolved oxygen increased with LZ size, and annual Massasauga encounters were significantly correlated with LZ size. This analysis suggests a population decline occurred when LZ size was reduced by flooding. Our data give support to the importance and maintenance of an LZ for successful snake hibernation. Our methods apply to subterranean hibernation habitats that are at risk of environmental stochasticity, causing flooding, freezing, or hypoxia.

Factors Affecting the Detection of an Imperiled and Cryptic Species

Population surveying and monitoring are important for identifying conservation needs and tracking trends in populations, communities, and ecosystems over time and laying the groundwork for conservation management and policy decisions. If species or populations go undetected because of inadequate effort or sampling design, protection and management cannot be properly provided. Due to the widespread loss of populations, the Eastern Massasauga (a rattlesnake) was recently listed as a federally threatened species in the United States; it is also listed as threatened in Canada. Given its current conservation status, there is considerable interest at state and federal levels in determining how to best survey for Eastern Massasaugas to aid in management decisions. Using a 16-year dataset, we examined the relationships among environmental, temporal, area, management, and search effort factors on the detection probability of Eastern Massasaugas. We found that four abiotic parameters (solar irradiance, shaded air temperature, three-day maximum air temperature, and humidity) and three search parameters (effort per researcher, search area, and search time of day) influenced detection of Eastern Massasaugas. As the current biodiversity crisis continues, the cost-effective use of resources and scientific expertise will continue to increase in importance. We hope our results stimulate similar analyses in other taxa, which will be critical for designing and implementing regional survey and monitoring programs.

Temporal variability of overwintering conditions for a species-at-risk snake: Implications for climate change and habitat management

The suitability of overwintering habitat in response to temporal fluctuations in winter temperatures and water table position, and variability in timing and intensity of snowfall and rainfall is critical to informing management strategies for climate-sensitive species such as the Eastern Massasauga rattlesnake (Sistrurus catenatus). Important subterranean conditions contributing to the suitability of overwintering habitat for S. catenatus includes the availability of an unflooded space and temperatures above 0 °C which is conceptualized as the resilience zone. Here, we show that the timing and duration of resilience zone loss varies between years and among sites in response to variable weather conditions. Peatland habitat occupied by snakes lost the resilience zone fewer times and for shorter durations than unconfirmed habitat. In some cases occupied habitat continuously provided a resilience zone, suggesting that snakes may only be able to tolerate short periods of unsuitable conditions. As expected, larger precipitation events resulted in greater reduction of the resilience zone size. In particular, rain on snow events resulted in the greatest change in resilience zone size and could increase the risk of mortality events. With extreme weather-related events predicted to increase with climate change, long-term conservation of climate-sensitive species should focus on protecting habitats that are naturally resilient to changing and variable weather conditions and identifying vulnerable habitats that would benefit from additional research on adaptive management strategies.

Molecular and morphological analysis of a Caryospora-like isolate (Apicomplexa: Eimeriidae) from the magpie-lark (Grallina cyanoleuca) (Latham, 1801) in Western Australia.

A new Caryospora-like isolate is described from a magpie-lark (Grallina cyanoleuca) in Western Australia. Sporulated oocysts of the Caryospora-like isolate (n = 35) are subspherical with a shape index of 1.13 ((21.5 (19.7-23.6) × 19.0 (18.1-19.8) μm). The bilayered oocyst wall is smooth. Micropyle, polar granule and oocyst residuum are absent. The sporocyst is ellipsoidal, 18.9 (17.2-20.8) × 12.3 (11.9-12.8) μm, with a shape index (length/width) of 1.54. The sporocyst wall is bilayered. Stieda and substieda bodies are present, the Stieda body is small and flattened and the substieda is trapezoidal. Sporocyst with eight sporozoites arranged head to tail. The sporozoites are vermiform, 18.9 (17.2-20.8) × 12.3 (11.9-12.8) μm and have striations at the anterior end. Each sporozoite has both anterior and posterior refractile bodies. A sporocyst residuum is present. Molecular characterization of the isolated Caryospora-like oocysts was conducted at the 18S ribosomal RNA and the mitochondrial cytochrome oxidase (COI) loci. At the 18S rRNA locus, the Caryospora-like isolate exhibited 88.8% to 96.5% similarity with other Caryospora spp. from different hosts. At the COI locus, it showed 91.5% similarity to Caryospora cf. bigenetica JB-2013 (KF859856) from the rattlesnake, Sistrurus catenatus.

POSTNATAL MORTALITY IN NEONATE RATTLESNAKES ASSOCIATED WITH OPHIDIOMYCES OPHIODIICOLA.

Ophidiomycosis, historically referred to as snake fungal disease (SFD), caused by Ophidiomyces ophiodiicola, is a significant disease of snakes characterized by crusty scales, pustules, subcutaneous nodules, and death. Ophidiomycosis is a proposed threat to sustainability of free-ranging snake populations throughout the United States and Europe, but the clinical progression during periods of reproductive activity (gravid females, neonates) is unknown. In spring 2012, five apparently healthy gravid eastern massasauga (Sistrurus catenatus) rattlesnakes from Clinton County, Illinois, were brought into captivity to give birth and be returned into the population. While in captivity, one adult female and 21 neonates died. Five individuals were subsequently confirmed positive for O. ophiodiicola by using quantitative polymerase chain reaction (qPCR). In 2016, a gravid timber rattlesnake (Crotalus horridus) with ophidiomycosis from Jackson County, Illinois, gave birth in captivity to 13 neonates. Skin swabs were taken from all neonates immediately after birth and confirmed negative for O. ophiodiicola by using qPCR. The neonates remained housed with the positive female for 10 days before all animals were reswabbed and released back into the wild. One neonate was O. ophiodiicola positive at time of release. The initial negative result followed by a positive result several days postpartum suggests that the neonate was infected by the female after direct contact. Both case series represent natural infection of neonates after parturition and highlight the importance of this disease in a demographically important age class.

Survey methodology for detecting eastern massasauga rattlesnakes in southern Michigan

ABSTRACTThe U.S. Fish and Wildlife Service listed the eastern massasauga rattlesnake (Sistrurus catenatus catenatus) as threatened in 2016 under the 1973 Endangered Species Act. We tested a visual‐encounter survey method during 2016 to aid researchers and managers in successfully detecting massasaugas in occupied habitat in southern Michigan, USA. We conducted 54 surveys (paired, independent searchers) in 2‐ha areas occupied by telemetered massasaugas. Our detection process parameters included environmental conditions (air temperature, humidity, solar radiation, surface temperature, precipitation) and searcher characteristics (e.g., experience, time spent searching). We detected massasaugas on 11 of 54 surveys. Detection probability from the null model was 0.31; however, we found that time spent searching and minimum air temperature improved detection probability. Detection probability approached 1.00 as time searched by an individual exceeded 90 minutes and approached 0.80 on cooler mornings (12.8° C). Our findings provide survey protocol guidance to increase massasauga detections during visual encounter surveys, which offer useful information to help guide habitat management decisions. © 2019 The Wildlife Society.

Road avoidance and its energetic consequences for reptiles.

Roads are one of the most widespread human‐caused habitat modifications that can increase wildlife mortality rates and alter behavior. Roads can act as barriers with variable permeability to movement and can increase distances wildlife travel to access habitats. Movement is energetically costly, and avoidance of roads could therefore impact an animal's energy budget. We tested whether reptiles avoid roads or road crossings and explored whether the energetic consequences of road avoidance decreased individual fitness. Using telemetry data from Blanding's turtles (Emydoidea blandingii; 11,658 locations of 286 turtles from 15 sites) and eastern massasaugas (Sistrurus catenatus; 1,868 locations of 49 snakes from 3 sites), we compared frequency of observed road crossings and use of road‐adjacent habitat by reptiles to expected frequencies based on simulated correlated random walks. Turtles and snakes did not avoid habitats near roads, but both species avoided road crossings. Compared with simulations, turtles made fewer crossings of paved roads with low speed limits and more crossings of paved roads with high speed limits. Snakes made fewer crossings of all road types than expected based on simulated paths. Turtles traveled longer daily distances when their home range contained roads, but the predicted energetic cost was negligible: substantially less than the cost of producing one egg. Snakes with roads in their home range did not travel further per day than snakes without roads in their home range. We found that turtles and snakes avoided crossing roads, but road avoidance is unlikely to impact fitness through energetic expenditures. Therefore, mortality from vehicle strikes remains the most significant impact of roads on reptile populations.

Genetic signatures of small effective population sizes and demographic declines in an endangered rattlesnake, Sistrurus catenatus.

Endangered species that exist in small isolated populations are at elevated risk of losing adaptive variation due to genetic drift. Analyses that estimate short‐term effective population sizes, characterize historical demographic processes, and project the trajectory of genetic variation into the future are useful for predicting how levels of genetic diversity may change. Here, we use data from two independent types of genetic markers (single nucleotide polymorphisms [SNPs] and microsatellites) to evaluate genetic diversity in 17 populations spanning the geographic range of the endangered eastern massasauga rattlesnake (Sistrurus catenatus). First, we use SNP data to confirm previous reports that these populations exhibit high levels of genetic structure (overall Fst = 0.25). Second, we show that most populations have contemporary Ne estimates <50. Heterozygosity–fitness correlations in these populations provided no evidence for a genetic cost to living in small populations, though these tests may lack power. Third, model‐based demographic analyses of individual populations indicate that all have experienced declines, with the onset of many of these declines occurring over timescales consistent with anthropogenic impacts (<200 years). Finally, forward simulations of the expected loss of variation in relatively large (Ne = 50) and small (Ne = 10) populations indicate they will lose a substantial amount of their current standing neutral variation (63% and 99%, respectively) over the next 100 years. Our results argue that drift has a significant and increasing impact on levels of genetic variation in isolated populations of this snake, and efforts to assess and mitigate associated impacts on adaptive variation should be components of the management of this endangered reptile.

Implications of Small Population Size in a Threatened Pitviper Species

Abstract Destruction and fragmentation of wildlife habitat often results in small, isolated populations that are highly susceptible to extirpation. In many cases, however, estimates of population size are lacking, precluding accurate assessments of population viability and sound conservation management recommendations. The Eastern Massasauga (Sistrurus catenatus) is a federally threatened pitviper species that has been extirpated throughout much of its historic range attributable to agricultural conversion of wetland habitat and other synergistic threats. Population size is generally unknown among extant massasauga populations, making site-specific management difficult. In this study, we estimated genetic effective population size (Ne) and census population size (Nc) for Eastern Massasaugas at two sites in southwest Michigan. For each population, we used mark–recapture models to estimate Nc and the linkage disequilibrium method to estimate Ne. Our results revealed small Nc, with approximately 108 (95% CI ...

Sensitivity Analysis Using Site-Specific Demographic Parameters to Guide Research and Management of Threatened Eastern Massasaugas

Long-term demographic data are important for conserving populations of threatened and endangered species. Collecting data specific to the population of interest can improve conservation success by allowing managers to make informed decisions, evaluate the efficacy of habitat management, and assess extinction risk. Population viability analysis (PVA), a tool commonly used to estimate extinction risk in threatened populations, is most informative when precise, population-specific data are available. We used mark-recapture data spanning ten years (2008–2017) to estimate annual adult survival rates in a population of threatened Eastern Massasauga rattlesnakes (Sistrurus catenatus) in Barry County, Michigan. Using these survival estimates and ten additional parameter values obtained from our site and a nearby population, we modeled population viability over the next 100 years. We performed sensitivity analysis using Latin hypercube sampling, followed by logistic regression to assess the relative influence of model parameters on extinction risk. We estimated annual apparent survival rates of 0.79 (95% CI = 0.69–0.87) for adult males and 0.78 (95% CI = 0.69–0.85) for adult females, which are higher than expected given the population's locality. Results of our sensitivity analysis suggest that actions promoting high survival of adult females should be a management priority, followed by activities that facilitate high reproductive output and neonate survival. We recommend focusing future research and monitoring efforts on these parameters.

Temporal Patterns of Genetic Diversity in an Imperiled Population of the Eastern Massasauga Rattlesnake (Sistrurus catenatus)

The Eastern Massasauga (Sistrurus catenatus) is a small, grassland-dependent rattlesnake species declining throughout its native range, and is thus a species of high conservation priority. In Illinois, only a single population remains of a once widespread distribution. We documented genetic diversity in this population over a ten-year period and assessed levels of heterozygosity, allelic diversity, inbreeding (FIS), and effective population size (Ne). Neither heterozygosity nor levels of inbreeding differed significantly among periods. We identified 21 alleles that occurred in a single time period, some of which may have been lost from the population given our estimated detection probability of 93%. Effective population size (Ne) was numerically small and showed a decreasing trend through time. Despite small population size and a lack of connectivity, there was no significant decline in genetic diversity over the ten-year study. Aspects of life history, coupled with a preference for a historically patchy ...

Identifying resilient Eastern Massasauga Rattlesnake (Sistrurus catenatus) peatland hummock hibernacula

At the northern limit of the Eastern Massasauga Rattlesnake’s (Sistrurus catenatus (Rafinesque, 1818)) range, individuals spend up to half the year overwintering. In hummock hibernacula found in peatlands, it is likely that subsurface temperature and water table position are contributing factors dictating habitat suitability. As a step towards assessing the vulnerability of hibernacula to anthropogenic changes, we combined subsurface temperature and water table dynamics to assess the likelihood that unflooded and unfrozen conditions were present in hummock hibernacula. Our results indicate that taller hummocks are more resilient to an advancing frost line and fluctuating water table by providing a larger area and duration of unfrozen and unflooded conditions, and a critical overwintering depth that is farther from the hummock surface. In two study sites along eastern Georgian Bay, an unflooded and unfrozen zone was present for over 90% of the overwintering period for hummocks taller than 25–27 cm. Our findings highlight the vulnerability of peatland hummocks to variability of winter weather where deep freezing and (or) water table rise may nonlinearly reduce resilience. This suggests that height is not the only component affecting the suitability of hummock hibernacula and that further research should examine the structure and spatial arrangement of hummocks within a peatland.

Snake fungal disease alters skin bacterial and fungal diversity in an endangered rattlesnake

Snake Fungal Disease (SFD), caused by Ophidiomyces ophiodiicola, is the most recently described fungal disease afflicting wildlife populations across North America and Europe. It has been proposed as a significant conservation threat yielding high mortality and yet much its ecology is unknown. We collected 144 skin swabs from Eastern Massasaugas (Sistrurus catenatus) in 2015 and 2016 to determine document ongoing prevalence and assess differences in microbial assemblages between positive and negative individuals. Alpha diversity of fungi was reduced in SFD positive animals, while beta diversity identified distinct assemblages of microbes between SFD–positive and –negative samples. Ophidiomyces was present on the skin of affected animals, even on body sites distant to lesions indicating that the microbiome on entire surface of the skin is altered. Ophidiomyces was not detected in any non-SFD snake. There were smaller, but significant, influences of year sampled. Bacterial genera Janthinobacterium and Serratia were significantly increased in SFD snakes, while Xylanimicrobium, Cellulosimicrobium, and Rhodococcus were the only bacterial taxa significantly reduced. The relative abundance of fungi within the orders Pleosporales and Canopdiales was reduced in SFD-positive samples, though Pyrenochaetopsis pratorum was the only species found to differ significantly. This is the first study to determine the impact that this fungal pathogen has on the skin microbiome.

Delaying conservation actions matters for species vulnerable to climate change

Abstract Climate change vulnerability assessments are commonly used to identify species or populations at risk from global climate change, but few translate impact assessments to climate change adaptation actions. Furthermore, most climate change adaptation efforts emphasize where to implement management actions, whereas timing remains largely overlooked. The rate of modern climate change introduces urgency in evaluating whether delaying conservation actions compromises their efficacy for reaching important conservation targets. We evaluated the importance of multiple climate change adaptation strategies including timing of actions on preventing extinctions for a threatened climate‐sensitive species, the Eastern Massasauga rattlesnake (Sistrurus catenatus). We parameterized a range‐wide population viability analysis model that related demographic sensitivities to drought events and human‐modified land cover to assess vulnerability to future climate change. Using simulations, we assessed the efficacy and trade‐offs associated with alternative climate adaptation strategies aimed at maximizing the number of future populations including when to initiate conservation actions, duration of management, number of managed populations, and local management effectiveness. Population‐level projections under future climate change scenarios revealed a broad‐scale pattern of range contraction in the southwestern portion of the current range. Along the extinction gradient, we identified demographic strongholds and refugia critical for population persistence under climate change as well as populations at high risk of extinction and candidates for climate change adaptation actions. In the context of future climate change, the timing of conservation actions was crucial; acting earlier maximized chances of achieving conservation targets. Even considering uncertainty in climate change projections, delaying actions was less efficient and introduced undesirable trade‐offs including the need to implement conservation actions for longer or targeting more populations to achieve a similar conservation target. Synthesis and applications. Our findings highlight how acting quickly reduces risk and improves outcomes for a highly vulnerable species under future climate change. Climate change vulnerability assessments require translation of model‐based outputs into tractable information for climate change adaptation planning. Quantifying trade‐offs associated with the multidimensional decision space related to species conservation and recovery planning is a critical step in climate change adaptation.

Evaluation of environmental DNA to detect Sistrurus catenatus and Ophidiomyces ophiodiicola in crayfish burrows

Environmental DNA represents a potentially cost-effective method for detection of rare and cryptic species, for which traditional sampling can be logistically costly. We tested species-specific probe-based assays to detect eDNA for the federally threatened eastern massasauga rattlesnake and the causative agent of snake fungal disease, Ophidiomyces ophiodiicola. We collected water samples from 100 crayfish burrows (over-wintering refugia) during spring emergence and screened them for snake and fungal DNA. We detected snake DNA in two samples and failed to detect O. ophiodiicola DNA. Given the high density of both target species at the sites, we suggest these methods may not offer a logistical and financial improvement over traditional sampling protocols.

Eastern massasauga demography and extinction risk under prescribed‐fire scenarios

ABSTRACTThe use of poorly estimated or surrogate population parameter estimates to assess population viability may result in misleading predictions. Consequently, a critical first step to understanding population health and the effects of land management practices on threatened species is estimation of site‐specific demographic parameters. A major threat to the eastern massasauga (Sistrurus catenatus) is habitat loss due to encroachment of woody vegetation and invasive species. Current land management practices require periodic burning or mowing to maintain habitat suitability. Although these methods improve habitat quality, they may also increase the risk of depredation due to reduced ground cover if burns are too extensive or cause mortality if conducted when snakes are active. We fitted contemporary capture–recapture and matrix models to an 8‐year dataset to estimate population parameters for an eastern massasauga population near the range center of the species, where the largest number of eastern massasauga populations may still persist. From 2009 to 2016, we captured 826 eastern massasaugas 1,776 times. In general, annual survival increased with increasing age (age 0 = 0.38, age 1 = 0.65, age 2 = 0.67, age ≥3 females = 0.71, age ≥3 males = 0.66). Abundance estimates ranged from 84 to 140 adults and annual reproductive frequency was 0.44 (95% CI = 0.29–0.59). We simulated increased mortality due to prescribed burns during spring, fall, and late fall for 50 and 100 years. The baseline model, which incorporated current prescribed‐fire practices, indicated a stable population with only a 0.2–0.6% probability of extinction over 100 years, suggesting that management practices at this site are sustainable if they remain unchanged. Simulations of conservative increases in mortality due to fire changed the probability of extinction little over 50 years (≤0.7%) but increased probability of extinction up to 24.5% over 100 years in the most pessimistic prescribed‐burn scenario. These prescribed‐burn simulations may be comparable to burn regimes used at other eastern massasauga sites. The population parameters estimated here provide information needed for assessing range‐wide population viability and investigating geographic variation in eastern massasauga demography. © 2018 The Wildlife Society.

Development of a Species Status Assessment Process for Decisions under the U.S. Endangered Species Act

Abstract Decisions under the U.S. Endangered Species Act (ESA) require scientific input on the risk that the species will become extinct. A series of critiques on the role of science in ESA decisions have called for improved consistency and transparency in species risk assessments and clear distinctions between science input and policy application. To address the critiques and document the emerging practice of the U.S. Fish and Wildlife Service (USFWS), we outline an assessment process based on principles and practices of risk and decision analyses that results in a scientific report on species status. The species status assessment (SSA) process has three successive stages: 1) document the life history and ecological relationships of the species in question to provide the foundation for the assessment, 2) describe and hypothesize causes for the current condition of the species, and 3) forecast the species' future condition. The future condition refers to the ability of a species to sustain populations in the wild under plausible future scenarios. The scenarios help explore the species' response to future environmental stressors and to assess the potential for conservation to intervene to improve its status. The SSA process incorporates modeling and scenario planning for prediction of extinction risk and applies the conservation biology principles of representation, resiliency, and redundancy to evaluate the current and future condition. The SSA results in a scientific report distinct from policy application, which contributes to streamlined, transparent, and consistent decision-making and allows for greater technical participation by experts outside of the USFWS, for example, by state natural resource agencies. We present two case studies based on assessments of the eastern massasauga rattlesnake Sistrurus catenatus and the Sonoran Desert tortoise Gopherus morafkai to illustrate the process. The SSA builds upon the past threat-focused assessment by including systematic and explicit analyses of a species' future response to stressors and conservation, and as a result, we believe it provides an improved scientific analysis for ESA decisions.

The importance of historical land use in the maintenance of early successional habitat for a threatened rattlesnake

Understanding how historic habitat changes have impacted species and searching the past for clues to better understand the current plight of threatened species can help inform and improve future conservation efforts. We coupled species distribution modeling with historical imagery analysis to assess how changes in land use/land cover have influenced the distribution of eastern massasauga rattlesnake (Sistrurus catenatus), a federally threatened species, and its habitat in northeastern Ohio over the past ∼75 years. We also examined land use/land cover changes throughout southern Michigan for a broader perspective on the influence of historical processes on contemporary habitat. There was a pronounced shift in northeastern Ohio land cover from 1938 to 2011 with forest cover becoming the predominant land cover type as agricultural fields were abandoned and succession occurred. Most known eastern massasauga locations in the area were at some point used for agriculture and higher habitat suitability values were associated with agricultural fields that were eventually abandoned. We observed more stable habitat conditions across southern Michigan populations indicating agricultural abandonment was not as necessary for habitat creation in this part of their range. We present a new approach for linking historical landscapes to present day habitat suitability models; permitting inferences on how prior land use/land cover states have influenced the current distribution of species and their habitats. We demonstrate how agricultural abandonment was an important source of early successional habitat for a species that requires an open canopy, a finding applicable to a broad array of species with similar habitat requirements.

Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

ABSTRACTPathogenic fungi have become a global concern to wildlife populations over the last 2 decades. However, the threat of snake fungal disease (SFD; caused by Ophidiomyces ophiodiicola) to snake populations is still largely unknown. From 2014–2016, we monitored 3 disjunct populations of the federally threated eastern massasauga (Sistrurus catenatus) in Michigan, USA. We used clinical signs of SFD, quantitative TaqMan polymerase chain reaction (qPCR), repeated sampling of individuals and sites, and single‐season occupancy models to estimate site‐specific prevalence of Ophidiomyces. Point estimates of Ophidiomyces prevalence in 2016 were larger at the northernmost study site (0.17, 95% CI = 0.04–0.50), where 17 of 34 snakes were implanted with radio‐transmitters, and smaller at southern sites (0.03, 95% CI = 0.00–0.19). However, Ophidiomyces prevalence was not different between snakes with transmitters and snakes without transmitters. Swabbing snakes with 1 applicator resulted in a high probability of failure in detecting Ophidiomyces DNA for individuals with clinical signs of SFD and the probability was even higher for individuals without clinical signs of SFD. Repeated sampling of individuals reduced the probability of obtaining a false‐negative qPCR result by 72% for snakes with clinical signs and 12% for snakes without clinical signs when we swabbed individuals with 5 applicators. We recommend resampling individuals and sites as a sampling design for estimating fine‐scale, site‐specific Ophidiomyces prevalence and population‐level responses to SFD. If clinical signs are used as a surrogate for SFD, we recommend researchers standardize diagnosis of clinical signs of SFD by providing technicians adequate field training and educational materials, and minimize the number of observers recording clinical signs. We discourage the use of radio‐telemetry methods where SFD occurs unless sterile surgical, handling, and equipment protocols can be ensured and the benefits to the population from such activities outweigh the increased health risks to individuals. © 2017 The Wildlife Society.