Broad-Scale Assessment of Methylmercury in Adult Amphibians.

Mercury (Hg) is a toxic contaminant that has been mobilized and distributed worldwide and is a threat to many wildlife species. Amphibians are facing unprecedented global declines due to many threats including contaminants. While the biphasic life history of many amphibians creates a potential nexus for methylmercury (MeHg) exposure in aquatic habitats and subsequent health effects, the broad-scale distribution of MeHg exposure in amphibians remains unknown. We used nonlethal sampling to assess MeHg bioaccumulation in 3,241 juvenile and adult amphibians during 2017-2021. We sampled 26 populations (14 species) across 11 states in the United States, including several imperiled species that could not have been sampled by traditional lethal methods. We examined whether life history traits of species and whether the concentration of total mercury in sediment or dragonflies could be used as indicators of MeHg bioaccumulation in amphibians. Methylmercury contamination was widespread, with a 33-fold difference in concentrations across sites. Variation among years and clustered subsites was less than variation across sites. Life history characteristics such as size, sex, and whether the amphibian was a frog, toad, newt, or other salamander were the factors most strongly associated with bioaccumulation. Total Hg in dragonflies was a reliable indicator of bioaccumulation of MeHg in amphibians (R2 ≥ 0.67), whereas total Hg in sediment was not (R2 ≤ 0.04). Our study, the largest broad-scale assessment of MeHg bioaccumulation in amphibians, highlights methodological advances that allow for nonlethal sampling of rare species and reveals immense variation among species, life histories, and sites. Our findings can help identify sensitive populations and provide environmentally relevant concentrations for future studies to better quantify the potential threats of MeHg to amphibians.

Time-to-detection occupancy methods: performance and utility for improving efficiency of surveys.

Occupancy methods propelled the quantitative study of species distributions forward by separating the observation process, or the imperfect detectability of species, from the ecological processes of interest governing species distributions. Occupancy studies come at a cost, however: the collection of additional data to account for nondetections at sites where the species is present. The most common occupancy designs (repeated-measures designs) require repeat visits to sites or the use of multiple observers or detection methods. Time-to-detection methods have been identified as a potentially efficient alternative, requiring only one visit to each site by a single observer. A comparison of time-to-detection methods to repeated-measures designs for visual encounter surveys would allow researchers to evaluate whether time-to-detection methods might be appropriate for their study system and can inform optimal survey design. We collected time-to-detection data during two different repeated-measures design occupancy surveys for four amphibians and compared the performance of time-to-detection methods to the other designs using the location (potential bias) and precision of posterior distributions for occurrence parameters. We further used results of time-to-detection surveys to optimize survey design. Time-to-detection methods performed best for species that are widespread and have high detection probabilities and rates, but performed less well for cryptic species with lower probability of occurrence or whose detection was strongly affected by survey conditions. In all cases, single surveys were most efficient in terms of person-hours expended, but under some conditions the survey duration required to achieve high detection probabilities would be prohibitively long for a single survey. Regardless of occupancy survey design, time-to-detection methods provide important information that can be used to optimize surveys, allowing researchers and resource managers to efficiently achieve monitoring and conservation goals. Collecting time-to-detection data while conducting repeated-measures occupancy surveys requires only small modifications to field methods but could have large benefits in terms of time spent surveying in the long term.

Thermal quality influences habitat use of two anole species.

Regeneration of secondary forests on previously deforested or degraded land is one of the most dominant forms of land-use change in the tropics. However, the response of animal communities to forest regeneration is poorly understood. To evaluate support for thermal quality as a mechanism driving reptile species distributions during secondary forest succession, we measured operative temperatures and occupancy in three successional forest stages (pasture, secondary forest, and old growth forest) for two anole species common in the landscape (Norops humilis and Norops limifrons). We then measured thermal preference in laboratory experiments and used operative temperature and temperature preference measurements to determine how thermal quality of habitat changes over the course of secondary forest succession, and if occupancy varies as a function of thermal quality. We found that thermal quality was lowest in pasture habitat because of a large frequency of temperatures above the thermal preference range. However, in low thermal quality pasture sites, riparian habitats and remnant trees provided a thermal refuge for both lizard species. Our results support thermal quality as a mechanism for reptile species distributions in altered landscapes and highlight the importance of the maintenance of riparian corridors.

A Dataset of Amphibian Species in U.S. National Parks.

National parks and other protected areas are important for preserving landscapes and biodiversity worldwide. An essential component of the mission of the United States (U.S.) National Park Service (NPS) requires understanding and maintaining accurate inventories of species on protected lands. We describe a new, national-scale synthesis of amphibian species occurrence in the NPS system. Many park units have a list of amphibian species observed within their borders compiled from various sources and available publicly through the NPSpecies platform. However, many of the observations in NPSpecies remain unverified and the lists are often outdated. We updated the amphibian dataset for each park unit by collating old and new park-level records and had them verified by regional experts. The new dataset contains occurrence records for 292 of the 424 NPS units and includes updated taxonomy, international and state conservation rankings, hyperlinks to a supporting reference for each record, specific notes, and related fields which can be used to better understand and manage amphibian biodiversity within a single park or group of parks.

Comparing reintroduction strategies for the endangered San Francisco gartersnake (Thamnophis sirtalis tetrataenia) using demographic models.

For endangered species persisting in a few populations, reintroductions to unoccupied habitat are a popular conservation action to increase viability in the long term. Identifying the reintroduction strategy that is most likely to result in viable founder and donor populations is essential to optimally use resources available for conservation. The San Francisco gartersnake (Thamnophis sirtalis tetrataenia) is an endangered sub-species that persists in a small number of populations in a highly urbanized region of California. Most of the extant populations of San Francisco gartersnakes have low adult abundance and effective population size, heightening the need for establishment of more populations for insurance against the risk of extinction. We used simulations from demographic models to project the probability of quasi-extinction for reintroduced populations of San Francisco gartersnakes based on the release of neonate, juvenile, adult, or mixed-age propagules. Our simulation results indicated that the release of head-started juveniles resulted in the greatest viability of reintroduced populations, and that releases would need to continue for at least 15 years to ensure a low probability of quasi-extinction. Releasing captive-bred juvenile snakes would also have less effect on the viability of the donor population, compared to strategies that require more adult snakes to be removed from the donor population for translocation. Our models focus on snake demography, but the genetic makeup of donor, captive, and reintroduced populations will also be a major concern for any proposed reintroduction plan. This study demonstrates how modeling can be used to inform reintroduction strategies for highly imperiled species.

KEEPING THE HEAT ON: WEIGHTED SURVEILLANCE FOR CHYTRID FUNGUS (BATRACHOCHYTRIUM DENDROBATIDIS) IN DIXIE VALLEY TOADS (ANAXYRUS [= BUFO] WILLIAMSI).

Introduced fungal pathogens have caused declines and extinctions of naïve wildlife populations across vertebrate classes. Consequences of introduced pathogens to hosts with small ranges might be especially severe because of limited redundancy to rescue populations and lower abundance that may limit the resilience of populations to perturbations like disease introduction. As a complement to biosecurity measures to prevent the spread of pathogens, surveillance programs may enable early detection of pathogens, when management actions to limit the effects of pathogens on naïve hosts might be most beneficial. We analyzed surveillance data for the endangered and narrowly endemic Dixie Valley toad (Anaxyrus [= Bufo] williamsi) from two time periods (2011-2014 and 2019-2021) to estimate the minimum detectable prevalence of the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd). We assessed if detection efficiency could be improved by using samples from both Dixie Valley toads and co-occurring introduced American bullfrogs (Lithobates catesbeianus) and literature-derived surveillance weights. We further evaluated a weighted surveillance design to increase the efficiency of surveillance efforts for Bd within the toad's small (<6 km2) range. We found that monitoring adult and larval American bullfrogs would probably detect Bd more efficiently than monitoring Dixie Valley toads alone. Given that no Bd was detected, minimum detectable prevalence of Bd was <3% in 2011-2014, and <5% (Dixie Valley toads only) and <10% (American bullfrogs only) in 2019-2021. Optimal management for Bd depends on the mechanisms underlying its apparent absence from the range of Dixie Valley toads, but a balanced surveillance scheme that includes sampling American bullfrogs to increase the likelihood of detecting Bd, and adult Dixie Valley toads to ensure broad spatial coverage where American bullfrogs do not occur, would probably result in efficient surveillance, which might permit timely management of Bd if it is detected.

Integrating growth and survival models for flexible estimation of size-dependent survival in a cryptic, endangered snake.

Estimates of demographic rates for animal populations and individuals have many applications for ecological and conservation research. In many animals, survival is size-dependent, but estimating the form of the size-survival relationship presents challenges. For elusive species with low recapture rates, individuals' size will be unknown at many points in time. Integrating growth and capture-mark-recapture models in a Bayesian framework empowers researchers to impute missing size data, with uncertainty, and include size as a covariate of survival, capture probability, and presence on-site. If there is no theoretical expectation for the shape of the size-survival relationship, spline functions can allow for fitting flexible, data-driven estimates. We use long-term capture-mark-recapture data from the endangered San Francisco gartersnake (Thamnophis sirtalis tetrataenia) to fit an integrated growth-survival model. Growth models showed that females reach longer asymptotic lengths than males and that the magnitude of sexual size dimorphism differed among populations. The capture probability and availability of San Francisco gartersnakes for capture increased with snout-vent length. The survival rate of female snakes exhibits a nonlinear relationship with snout-vent length (SVL), with survival flat between 300 mm and 550 mm SVL before decreasing for females between 550 mm and 700 mm SVL. For male snakes, survival decreased for adult males >550 mm SVL. The survival rates of the smallest and largest San Francisco gartersnakes were highly uncertain because recapture rates were very low for these sizes. By integrating growth and survival models and using penalized splines, we found support for size-dependent survival in San Francisco gartersnakes. Our results have applications for devising management activities for this endangered subspecies, and our methods could be applied broadly to the study of size-dependent demography among animals.

Increased growth rates of stream salamanders following forest harvesting.

Timber harvesting can influence headwater streams by altering stream productivity, with cascading effects on the food web and predators within, including stream salamanders. Although studies have examined shifts in salamander occupancy or abundance following timber harvest, few examine sublethal effects such as changes in growth and demography. To examine the effect of upland harvesting on growth of the stream-associated Ouachita dusky salamander (Desmognathus brimleyorum), we used capture-mark-recapture over three years at three headwater streams embedded in intensely managed pine forests in west-central Arkansas. The pine stands surrounding two of the streams were harvested, with retention of a 14- and 21-m-wide forested stream buffer on each side of the stream, whereas the third stream was an unharvested control. At the two treatment sites, measurements of newly metamorphosed salamanders were on average 4.0 and 5.7 mm larger post-harvest compared with pre-harvest. We next assessed the influence of timber harvest on growth of post-metamorphic salamanders with a hierarchical von Bertalanffy growth model that included an effect of harvest on growth rate. Using measurements from 839 individual D. brimleyorum recaptured between 1 and 6 times (total captures, n = 1229), we found growth rates to be 40% higher post-harvest. Our study is among the first to examine responses of individual stream salamanders to timber harvesting, and we discuss mechanisms that may be responsible for observed shifts in growth. Our results suggest timber harvest that includes retention of a riparian buffer (i.e., streamside management zone) may have short-term positive effects on juvenile stream salamander growth, potentially offsetting negative sublethal effects associated with harvest.

Correction: Combining genetic and demographic monitoring better informs conservation of an endangered urban snake.

[This corrects the article DOI: 10.1371/journal.pone.0231744.].

Metal accumulation varies with life history, size, and development of larval amphibians.

Amphibian larvae are commonly used as indicators of aquatic ecosystem health because they are susceptible to contaminants. However, there is limited information on how species characteristics and trophic position influence contaminant loads in larval amphibians. Importantly, there remains a need to understand whether grazers (frogs and toads [anurans]) and predators (salamanders) provide comparable information on contaminant accumulation or if they are each indicative of unique environmental processes and risks. To better understand the role of trophic position in contaminant accumulation, we analyzed composite tissues for 10 metals from larvae of multiple co-occurring anuran and salamander species from 20 wetlands across the United States. We examined how metal concentrations varied with body size (anurans and salamanders) and developmental stage (anurans) and how the digestive tract (gut) influenced observed metal concentrations. Across all wetlands, metal concentrations were greater in anurans than salamanders for all metals tested except mercury (Hg), selenium (Se), and zinc (Zn). Concentrations of individual metals in anurans decreased with increasing weight and developmental stage. In salamanders, metal concentrations were less correlated with weight, indicating diet played a role in contaminant accumulation. Based on batches of similarly sized whole-body larvae compared to larvae with their digestive tracts removed, our results indicated that tissue type strongly affected perceived concentrations, especially for anurans (gut represented an estimated 46-97% of all metals except Se and Zn). This suggests the reliability of results based on whole-body sampling could be biased by metal, larval size, and development. Overall, our data shows that metal concentrations differs between anurans and salamanders, which suggests that metal accumulation is unique to feeding behavior and potentially trophic position. To truly characterize exposure risk in wetlands, species of different life histories, sizes and developmental stages should be included in biomonitoring efforts.

Combining genetic and demographic monitoring better informs conservation of an endangered urban snake.

Conversion and fragmentation of wildlife habitat often leads to smaller and isolated populations and can reduce a species' ability to disperse across the landscape. As a consequence, genetic drift can quickly lower genetic variation and increase vulnerability to extirpation. For species of conservation concern, quantification of population size and connectivity can clarify the influence of genetic drift in local populations and provides important information for conservation management and recovery strategies. Here, we used genome-wide single nucleotide polymorphism (SNP) data and capture-mark-recapture methods to evaluate the genetic diversity and demography within seven focal sites of the endangered San Francisco gartersnake (Thamnophis sirtalis tetrataenia), a species affected by alteration and isolation of wetland habitats throughout its distribution. The primary goals were to determine the population structure and degree of genetic isolation among T. s. tetrataenia populations and estimate effective size and population abundance within sites to better understand the present and future importance of genetic drift. We also used temporally sampled datasets to examine the magnitude of genetic change over time. We found moderate population genetic structure throughout the San Francisco Peninsula that partitions sites into northern and southern regional clusters. Point estimates of both effective size and population abundance were generally small (≤ 100) for a majority of the sites, and estimates were particularly low in the northern populations. Genetic analyses of temporal datasets indicated an increase in genetic differentiation, especially for the most geographically isolated sites, and decreased genetic diversity over time in at least one site (Pacifica). Our results suggest that drift-mediated processes as a function of small population size and reduced connectivity from neighboring populations may decrease diversity and increase differentiation. Improving genetic diversity and connectivity among T. s. tetrataenia populations could promote persistence of this endangered snake.

Batrachochytrium salamandrivorans (Bsal) not detected in an intensive survey of wild North American amphibians.

The salamander chytrid fungus (Batrachochytrium salamandrivorans [Bsal]) is causing massive mortality of salamanders in Europe. The potential for spread via international trade into North America and the high diversity of salamanders has catalyzed concern about Bsal in the U.S. Surveillance programs for invading pathogens must initially meet challenges that include low rates of occurrence on the landscape, low prevalence at a site, and imperfect detection of the diagnostic tests. We implemented a large-scale survey to determine if Bsal was present in North America designed to target taxa and localities where Bsal was determined highest risk to be present based on species susceptibility and geography. Our analysis included a Bayesian model to estimate the probability of occurrence of Bsal given our prior knowledge of the occurrence and prevalence of the pathogen. We failed to detect Bsal in any of 11,189 samples from 594 sites in 223 counties within 35 U.S. states and one site in Mexico. Our modeling indicates that Bsal is highly unlikely to occur within wild amphibians in the U.S. and suggests that the best proactive response is to continue mitigation efforts against the introduction and establishment of the disease and to develop plans to reduce impacts should Bsal establish.

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.