The population genetics of the causative agent of snake fungal disease indicate recent introductions to the USA.

Snake fungal disease (SFD; ophidiomycosis), caused by the pathogen Ophidiomyces ophiodiicola (Oo), has been documented in wild snakes in North America and Eurasia, and is considered an emerging disease in the eastern United States of America. However, a lack of historical disease data has made it challenging to determine whether Oo is a recent arrival to the USA or whether SFD emergence is due to other factors. Here, we examined the genomes of 82 Oo strains to determine the pathogen's history in the eastern USA. Oo strains from the USA formed a clade (Clade II) distinct from European strains (Clade I), and molecular dating indicated that these clades diverged too recently (approximately 2,000 years ago) for transcontinental dispersal of Oo to have occurred via natural snake movements across Beringia. A lack of nonrecombinant intermediates between clonal lineages in Clade II indicates that Oo has actually been introduced multiple times to North America from an unsampled source population, and molecular dating indicates that several of these introductions occurred within the last few hundred years. Molecular dating also indicated that the most common Clade II clonal lineages have expanded recently in the USA, with time of most recent common ancestor mean estimates ranging from 1985 to 2007 CE. The presence of Clade II in captive snakes worldwide demonstrates a potential mechanism of introduction and highlights that additional incursions are likely unless action is taken to reduce the risk of pathogen translocation and spillover into wild snake populations.

Seeking Alfalfa Resistance to a Rhizophagous Pest, the Clover Root Curculio (Sitona hispidulus F.).

Since the cancellation of broad-spectrum soil-active insecticides in alfalfa (Medicago sativa L.) production, clover root curculio (Sitona hispidulus F.) (CRC) larval root damage has increased. Current CRC management practices are limited in their ability to suppress larval feeding belowground. First, we field screened developmental alfalfa populations for CRC damage. Subsequently, we developed a soil-less arena to observe nodule feeding and development (head capsule width) of larvae in the lab. This method was used to evaluate five alfalfa populations (two CRC-susceptible (control) and three CRC-resistant populations) against larvae. Further, one CRC-resistant population paired with its genetically similar susceptible population were tested against adult leaf consumption and oviposition in the greenhouse. Field screening revealed that the alfalfa populations selected for little or no larval root feeding damage were more resistant to CRC larval feeding than their corresponding unselected cultivars and significantly more resistant than populations selected for susceptibility. The development of a soil-less arena provided a useful method for evaluation of root-larva interactions. Although larval development was similar across susceptible and resistant alfalfa populations, one CRC-resistant population (NY1713) displayed overall increased nodulation and, thus, had a significantly lower proportion of nodules consumed by larvae. Adult feeding and oviposition aboveground were similar across all populations tested. These results provide possible candidates and screening method for the development and evaluation of alfalfa cultivars that may reduce the impacts of larval feeding and that offer an additional option for CRC management.

Confirmed Cases of Ophidiomycosis in Museum Specimens from as Early as 1945, United States.

Ophidiomycosis represents a conservation threat to wild snake populations. The disease was reported in North America early in the 21st century, but the history of ophidiomycosis has not been investigated. We examined museum specimens and confirmed cases of ophidiomycosis >50 years before the disease's reported emergence.

Effects of snake fungal disease on short-term survival, behavior, and movement in free-ranging snakes.

Pathogenic fungi are increasingly associated with epidemics in wildlife populations. Snake fungal disease (SFD, also referred to as Ophidiomycosis) is an emerging threat to snakes, taxa that are elusive and difficult to sample. Thus, assessments of the effects of SFD on populations have rarely occurred. We used a field technique to enhance detection, Passive Integrated Transponder (PIT) telemetry, and a multi-state capture-mark-recapture model to assess SFD effects on short-term (within-season) survival, movement, and surface activity of two wild snake species, Regina septemvittata (Queensnake) and Nerodia sipedon (Common Watersnake). We were unable to detect an effect of disease state on short-term survival for either species. However, we estimated Bayesian posterior probabilities of >0.99 that R. septemvittata with SFD spent more time surface-active and were less likely to permanently emigrate from the study area. We also estimated probabilities of 0.98 and 0.87 that temporary immigration and temporary emigration rates, respectively, were lower in diseased R. septemvittata. We found evidence of elevated surface activity and lower temporary immigration rates in diseased N. sipedon, with estimated probabilities of 0.89, and found considerably less support for differences in permanent or temporary emigration rates. This study is the first to yield estimates for key demographic and behavioral parameters (survival, emigration, surface activity) of snakes in wild populations afflicted with SFD. Given the increase in surface activity of diseased snakes, future surveys of snake populations could benefit from exploring longer-term demographic consequences of SFD and recognize that disease prevalence in surface-active animals may exceed that of the population as a whole.

Evidence of Vertical Transmission of the Snake Fungal Pathogen Ophidiomyces ophiodiicola.

Snake fungal disease (ophidiomycosis) is an emerging infection of snakes caused by Ophidiomyces ophiodiicola. Little is known about mechanisms of this pathogen's transmission and its implications for conservation of wild snake populations. We report four cases with evidence of vertical transmission of O. ophiodiicola from dam to offspring.

Field Diagnostics and Seasonality of Ophidiomyces ophiodiicola in Wild Snake Populations.

Snake fungal disease (SFD) is an emerging disease caused by the fungal pathogen, Ophidiomyces ophiodiicola. Clinical signs of SFD include dermal lesions, including regional and local edema, crusts, and ulcers. Snake fungal disease is widespread in the Eastern United States, yet there are limited data on how clinical signs of SFD compare with laboratory diagnostics. We compared two sampling methods for O. ophiodiicola, scale clip collection and swabbing, to evaluate whether collection method impacted the results of polymerase chain reaction (PCR). In addition, we evaluated the use of clinical signs to predict the presence of O. ophiodiicola across seasons, snake habitat affiliation (aquatic or terrestrial) and study sites. We found no significant difference in PCR results between sampling methods. Clinical signs were a strong predictor of O. ophiodiicola presence in spring and summer seasons. Snakes occupying terrestrial environments had a lower overall probability of testing positive for O. ophiodiicola compared to snakes occupying aquatic environments. Although our study indicates that both clinical signs of SFD and prevalence of O. ophiodiicola vary seasonally and based on habitat preferences of the host, our analysis suggests that clinical signs can serve as a reliable indicator of O. ophiodiicola presence, especially during spring and summer.

Quantifying climate sensitivity and climate-driven change in North American amphibian communities.

Changing climate will impact species' ranges only when environmental variability directly impacts the demography of local populations. However, measurement of demographic responses to climate change has largely been limited to single species and locations. Here we show that amphibian communities are responsive to climatic variability, using >500,000 time-series observations for 81 species across 86 North American study areas. The effect of climate on local colonization and persistence probabilities varies among eco-regions and depends on local climate, species life-histories, and taxonomic classification. We found that local species richness is most sensitive to changes in water availability during breeding and changes in winter conditions. Based on the relationships we measure, recent changes in climate cannot explain why local species richness of North American amphibians has rapidly declined. However, changing climate does explain why some populations are declining faster than others. Our results provide important insights into how amphibians respond to climate and a general framework for measuring climate impacts on species richness.

Influence of damming on anuran species richness in riparian areas: A test of the serial discontinuity concept.

Almost all large rivers worldwide are fragmented by dams, and their impacts have been modeled using the serial discontinuity concept (SDC), a series of predictions regarding responses of key biotic and abiotic variables. We evaluated the effects of damming on anuran communities along a 245-km river corridor by conducting repeated, time-constrained anuran calling surveys at 42 locations along the Broad and Pacolet Rivers in South Carolina, USA. Using a hierarchical Bayesian analysis, we test the biodiversity prediction of the SDC (modified for floodplain rivers) by evaluating anuran occupancy and species diversity relative to dams and degree of urbanized land use. The mean response of the anuran community indicated that occupancy and species richness were maximized when sites were farther downstream from dams. Sites at the farthest distances downstream of dams (47.5 km) had an estimated ~3 more species than those just below dams. Similarly, species-specific occupancy estimates showed a trend of higher occupancy downstream from dams. Therefore, using empirical estimation within the context of a 245-km river riparian landscape, our study supports SDC predictions for a meandering river. We demonstrate that with increasing distance downstream from dams, riparian anuran communities have higher species richness. Reduced species richness immediately downstream of dams is likely driven by alterations in flow regime that reduce or eliminate flows which sustain riparian wetlands that serve as anuran breeding habitat. Therefore, to maintain anuran biodiversity, we suggest that flow regulation should be managed to ensure water releases inundate riparian wetlands during amphibian breeding seasons and aseasonal releases, which can displace adults, larvae, and eggs, are avoided. These outcomes could be achieved by emulating pre-dam seasonal discharge data, mirroring discharge of an undammed tributary within the focal watershed, or by basing real-time flow releases on current environmental conditions.

Mass mortality of eastern box turtles with upper respiratory disease following atypical cold weather.

Emerging infectious diseases cause population declines in many ectotherms, with outbreaks frequently punctuated by periods of mass mortality. It remains unclear, however, whether thermoregulation by ectotherms and variation in environmental temperature is associated with mortality risk and disease progression, especially in wild populations. Here, we examined environmental and body temperatures of free-ranging eastern box turtles Terrapene carolina during a mass die-off coincident with upper respiratory disease. We recorded deaths of 17 turtles that showed clinical signs of upper respiratory disease among 76 adult turtles encountered in Berea, Kentucky (USA), in 2014. Of the 17 mortalities, 11 occurred approximately 14 d after mean environmental temperature dropped 2.5 SD below the 3 mo mean. Partial genomic sequencing of the major capsid protein from 1 sick turtle identified a ranavirus isolate similar to frog virus 3. Turtles that lacked clinical signs of disease had significantly higher body temperatures (23°C) than sick turtles (21°C) during the mass mortality, but sick turtles that survived and recovered eventually warmed (measured by temperature loggers). Finally, there was a significant negative effect of daily environmental temperature deviation from the 3 mo mean on survival, suggesting that rapid decreases in environmental temperature were correlated with mortality. Our results point to a potential role for environmental temperature variation and body temperature in disease progression and mortality risk of eastern box turtles affected by upper respiratory disease. Given our findings, it is possible that colder or more variable environmental temperatures and an inability to effectively thermoregulate are associated with poorer disease outcomes in eastern box turtles.

Shunt Testing In Vivo: Observational Study of Problems with Ventricular Catheter.

Most shunt obstructions happen at the inlet of the ventricular catheter. Three hundred six infusion studies from 2007 to 2011 were classified as having a typical pattern of either proximal occlusion or patency. We describe different patterns of shunt ventricular obstruction.Solid block: Cerebrospinal fluid (CSF) aspiration was impossible. Baseline pressure was without pulse waveform (respiratory waveform may be visible). A quick increase of pressure to a level compatible with the shunt's setting was recorded in response to infusion. Distal occlusion of the shunt via transcutaneous compression resulted in a rapid increase in pressure to levels above 50 mmHg. This pattern was attributed to a solid ventricular block.Slit ventricles: At baseline, a pattern similar to that of the solid block was observed. After compression, the pressure increases, the pulse waveform appears, and the intracranial pressure is often stabilized at 25-40 mmHg. It is probable that previously slit ventricles were opened during the test.Partial block: In a partial block of the ventricular catheter by an in-growing choroid plexus, the pulse waveform at baseline was observed and CSF aspiration was possible. During infusion, the pressure increased, but the pulse amplitude disappeared. During the increase in the pressure in the shunt prechamber, the connection with the ventricles is disturbed by repositioning of the plexus.Infusion study via the shunt prechamber is able to visualize ventricular obstruction of the hydrocephalus shunt.

Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines.

Since amphibian declines were first proposed as a global phenomenon over a quarter century ago, the conservation community has made little progress in halting or reversing these trends. The early search for a "smoking gun" was replaced with the expectation that declines are caused by multiple drivers. While field observations and experiments have identified factors leading to increased local extinction risk, evidence for effects of these drivers is lacking at large spatial scales. Here, we use observations of 389 time-series of 83 species and complexes from 61 study areas across North America to test the effects of 4 of the major hypothesized drivers of declines. While we find that local amphibian populations are being lost from metapopulations at an average rate of 3.79% per year, these declines are not related to any particular threat at the continental scale; likewise the effect of each stressor is variable at regional scales. This result - that exposure to threats varies spatially, and populations vary in their response - provides little generality in the development of conservation strategies. Greater emphasis on local solutions to this globally shared phenomenon is needed.

Using citizen science data to identify the sensitivity of species to human land use.

Conservation practitioners must contend with an increasing array of threats that affect biodiversity. Citizen scientists can provide timely and expansive information for addressing these threats across large scales, but their data may contain sampling biases. We used randomization procedures to account for possible sampling biases in opportunistically reported citizen science data to identify species' sensitivities to human land use. We analyzed 21,044 records of 143 native reptile and amphibian species reported to the Carolina Herp Atlas from North Carolina and South Carolina between 1 January 1990 and 12 July 2014. Sensitive species significantly associated with natural landscapes were 3.4 times more likely to be legally protected or treated as of conservation concern by state resource agencies than less sensitive species significantly associated with human-dominated landscapes. Many of the species significantly associated with natural landscapes occurred primarily in habitats that had been nearly eradicated or otherwise altered in the Carolinas, including isolated wetlands, longleaf pine savannas, and Appalachian forests. Rare species with few reports were more likely to be associated with natural landscapes and 3.2 times more likely to be legally protected or treated as of conservation concern than species with at least 20 reported occurrences. Our results suggest that opportunistically reported citizen science data can be used to identify sensitive species and that species currently restricted primarily to natural landscapes are likely at greatest risk of decline from future losses of natural habitat. Our approach demonstrates the usefulness of citizen science data in prioritizing conservation and in helping practitioners address species declines and extinctions at large extents.

Snake fungal disease: an emerging threat to wild snakes.

Since 2006, there has been a marked increase in the number of reports of severe and often fatal fungal skin infections in wild snakes in the eastern USA. The emerging condition, referred to as snake fungal disease (SFD), was initially documented in rattlesnakes, where the infections were believed to pose a risk to the viability of affected populations. The disease is caused by Ophidiomyces ophiodiicola, a fungus recently split from a complex of fungi long referred to as the Chrysosporium anamorph of Nannizziopsis vriesii (CANV). Here we review the current state of knowledge about O. ophiodiicola and SFD. In addition, we provide original findings which demonstrate that O. ophiodiicola is widely distributed in eastern North America, has a broad host range, is the predominant cause of fungal skin infections in wild snakes and often causes mild infections in snakes emerging from hibernation. This new information, together with what is already available in the scientific literature, advances our knowledge of the cause, pathogenesis and ecology of SFD. However, additional research is necessary to elucidate the factors driving the emergence of this disease and develop strategies to mitigate its impacts.This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.

Turbines and Terrestrial Vertebrates: Variation in Tortoise Survivorship Between a Wind Energy Facility and an Adjacent Undisturbed Wildland Area in the Desert Southwest (USA).

With the recent increase in utility-scale wind energy development, researchers have become increasingly concerned how this activity will affect wildlife and their habitat. To understand the potential impacts of wind energy facilities (WEF) post-construction (i.e., operation and maintenance) on wildlife, we compared differences in activity centers and survivorship of Agassiz's desert tortoises (Gopherus agassizii) inside or near a WEF to neighboring tortoises living near a wilderness area (NWA) and farther from the WEF. We found that the size of tortoise activity centers varied, but not significantly so, between the WEF (6.25 ± 2.13 ha) and adjacent NWA (4.13 ± 1.23 ha). However, apparent survival did differ significantly between the habitat types: over the 18-year study period apparent annual survival estimates were 0.96 ± 0.01 for WEF tortoises and 0.92 ± 0.02 for tortoises in the NWA. High annual survival suggests that operation and maintenance of the WEF has not caused considerable declines in the adult population over the past two decades. Low traffic volume, enhanced resource availability, and decreased predator populations may influence annual survivorship at this WEF. Further research on these proximate mechanisms and population recruitment would be useful for mitigating and managing post-development impacts of utility-scale wind energy on long-lived terrestrial vertebrates.

Using motion-sensor camera technology to infer seasonal activity and thermal niche of the desert tortoise (Gopherus agassizii).

Understanding the relationships between environmental variables and wildlife activity is an important part of effective management. The desert tortoise (Gopherus agassizii), an imperiled species of arid environments in the southwest US, may have increasingly restricted windows for activity due to current warming trends. In summer 2013, we deployed 48 motion sensor cameras at the entrances of tortoise burrows to investigate the effects of temperature, sex, and day of the year on the activity of desert tortoises. Using generalized estimating equations, we found that the relative probability of activity was associated with temperature (linear and quadratic), sex, and day of the year. Sex effects showed that male tortoises are generally more active than female tortoises. Temperature had a quadratic effect, indicating that tortoise activity was heightened at a range of temperatures. In addition, we found significant support for interactions between sex and day of the year, and sex and temperature as predictors of the probability of activity. Using our models, we were able to estimate air temperatures and times (days and hours) that were associated with maximum activity during the study. Because tortoise activity is constrained by environmental conditions such as temperature, it is increasingly vital to conduct studies on how tortoises vary their activity throughout the Sonoran Desert to better understand the effects of a changing climate.

Effects of river-flow regulation on anuran occupancy and abundance in riparian zones.

The natural flow regimes of rivers worldwide have been heavily altered through anthropogenic activities, and dams in particular have a pervasive effect on riverine ecosystems. Flow-regulation effects of dams negatively affect species diversity and abundance of a variety of aquatic animals, including invertebrates and fishes. However, the effects on semiaquatic animals are relatively unknown. We conducted anuran calling surveys at 42 study locations along the Broad and Pacolet Rivers in South Carolina to address the potential effects of flow regulation by damming on anuran occupancy and abundance. We estimated occupancy and abundance with Program PRESENCE. Models incorporated distance upstream and downstream from the nearest dam as covariates and urbanization pressure as an alternative stressor. Distance from dam was associated with occupancy of 2 of the 9 anuran species in our analyses and with abundance of 6 species. In all cases, distance downstream from nearest dam was a better predictor of occupancy and abundance than distance upstream from nearest dam. For all but one species, distance downstream from nearest dam was positively correlated with both occupancy and abundance. Reduced occupancy and abundance of anurans likely resulted from downstream alterations in flow regime associated with damming, which can lead to reduced area of riparian wetlands that serve as anuran breeding habitat. Our results showed that damming has a strong negative effect on multiple anuran species across large spatial extents and suggest that flow regulation can affect semiaquatic animals occupying riparian zones.

Effects of urbanization on occupancy of stream salamanders.

Urban development is the most common form of land conversion in the United States. Using a before-after control-impact study design, we investigated the effects of urbanization on larval and adult stages of southern two-lined salamanders (Eurycea cirrigera) and northern dusky salamanders (Desmognathus fuscus). Over 5 years, we estimated changes in occupancy and probabilities of colonization and survival in 13 stream catchments after urbanization and in 17 catchments that were not urbanized. We also examined effects of proportion of urbanized area in a catchment and distance of the salamander population to the nearest stream on probabilities of colonization and survival. Before urbanization, adult and larval stages of the two salamander species occupied nearly all surveyed streams, with occupancy estimates ranging from 1.0 to 0.78. Four years after urbanization mean occupancy of larval and adult two-lined salamanders had decreased from 0.87 and 0.78 to 0.57 and 0.39, respectively. Estimates of mean occupancy of larval northern dusky salamanders decreased from 1.0 to 0.57 in urban streams 4 years after urbanization; however, adult northern dusky salamander occupancy remained close to 1.0 in urban streams over 5 years. Occupancy estimates in control streams were similar for each species and stage over 5 years. Urbanization was associated with decreases in survival probabilities of adult and larval two-lined salamanders and decreases in colonization probabilities of larval dusky salamanders. Nevertheless, proportion of impervious surface and distance to nearest stream had little effect on probabilities of survival and colonization. Our results imply that in the evaluation of the effects of urbanization on species, such as amphibians, with complex life cycles, consideration of the effects of urbanization on both adult and larval stages is required.

Patterns of trombiculid mite (Hannemania dunni) parasitism among plethodontid salamanders in the western Piedmont of North Carolina.

Trombiculid mites are known to parasitize a variety of amphibian species, yet few comparisons of mite parasitism among amphibian species have been made. In this study, we investigated patterns of trombiculid mite parasitism among 3 plethodontid salamanders (Desmognathus fuscus, Eurycea cirrigera, and Plethodon cylindraceus) in the western Piedmont of North Carolina. All 3 salamander species were parasitized by a single species, Hannemania dunni. Desmognathus fuscus harbored mites more frequently (60.4% of individuals) than E. cirrigera (11.1%) or P. cylindraceus (14.6%). Desmognathus fuscus also had higher parasite loads than E. cirrigera or P. cylindraceus (P < 0.001). Mites on D. fuscus were found more frequently on the limbs than other body locations (P < 0.001). We found no correlation between salamander size and mite abundance (P = 0.689), but salamander collection sites influenced the abundance of mites on D. fuscus (P = 0.002). We found no effect of season on mite abundance in D. fuscus (P = 0.952). Salamander habitat preferences and edaphic or climatic differences among study sites may influence patterns of Hannemania sp. parasitism of salamanders.

Working through a migraine: addressing the hidden costs of workplace headaches.

The financial and personal impact of migraines in the workplace is substantial. Effective management of workplace migraines includes screening, prevention, and effective treatment. Worksite screeners are available to detect the burden of undiagnosed migraine in the workplace. Decreasing the personal and financial impact of migraines in the workplace requires a variety of strategies predicated on collaborative efforts among workers, occupational health nurses, other providers, and management.