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.

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.

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

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

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.

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.

Traditional trapping methods outperform eDNA sampling for introduced semi-aquatic snakes.

Given limited resources for managing invasive species, traditional survey methods may not be feasible to implement at a regional scale. Environmental DNA (eDNA) sampling has proven to be an effective method for detecting some invasive species, but comparisons between the detection probability of eDNA and traditional survey methods using modern occupancy modeling methods are rare. We developed a qPCR assay to detect two species of watersnake (Nerodia fasciata and Nerodia sipedon) introduced to California, USA, and we compared the efficacy of eDNA and aquatic trapping. We tested 3-9 water samples each from 30 sites near the known range of N. fasciata, and 61 sites near the known range of N. sipedon. We also deployed aquatic funnel traps at a subset of sites for each species. We detected N. fasciata eDNA in three of nine water samples from just one site, but captured N. fasciata in traps at three of ten sites. We detected N. sipedon eDNA in five of six water samples from one site, which was also the only site of nine at which this species was captured in traps. Traditional trapping surveys had a higher probability of detecting watersnakes than eDNA surveys, and both survey methods had higher detection probability for N. sipedon than N. fasciata. Occupancy models that integrated both trapping and eDNA surveys estimated that 5 sites (95% Credible Interval: 4-10) of 91 were occupied by watersnakes (both species combined), although snakes were only detected at four sites (three for N. fasciata, one for N. sipedon). Our study shows that despite the many successes of eDNA surveys, traditional sampling methods can have higher detection probability for some species. We recommend those tasked with managing species invasions explicitly compare eDNA and traditional survey methods in an occupancy framework to inform their choice of the best method for detecting nascent populations.

Infection risk decreases with increasing mismatch in host and pathogen environmental tolerances.

The fungal pathogen Batrachochytrium dendrobatidis (Bd) has caused the greatest known wildlife pandemic, infecting over 500 amphibian species. It remains unclear why some host species decline from disease-related mortality whereas others persist. We introduce a conceptual model that predicts that infection risk in ectotherms will decrease as the difference between host and pathogen environmental tolerances (i.e. tolerance mismatch) increases. We test this prediction using both local-scale data from Costa Rica and global analyses of over 11 000 Bd infection assays. We find that infection prevalence decreases with increasing thermal tolerance mismatch and with increasing host tolerance of habitat modification. The relationship between environmental tolerance mismatches and Bd infection prevalence is generalisable across multiple amphibian families and spatial scales, and the magnitude of the tolerance mismatch effect depends on environmental context. These findings may help explain patterns of amphibian declines driven by a global wildlife pandemic.

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.

Projecting invasion risk of non-native watersnakes (Nerodia fasciata and Nerodia sipedon) in the western United States.

Species distribution models (SDMs) are increasingly used to project the potential distribution of introduced species outside their native range. Such studies rarely explicitly evaluate potential conflicts with native species should the range of introduced species expand. Two snake species native to eastern North America, Nerodia fasciata and Nerodia sipedon, have been introduced to California where they represent a new stressor to declining native amphibians, fish, and reptiles. To project the potential distributions of these non-native watersnakes in western North America, we built ensemble SDMs using MaxEnt, Boosted Regression Trees, and Random Forests and habitat and climatic variables. We then compared the overlap between the projected distribution of invasive watersnakes and the distributions of imperiled native amphibians, fish, and reptiles that can serve as prey or competitors for the invaders, to estimate the risk to native species posed by non-native watersnakes. Large areas of western North America were projected to be climatically suitable for both species of Nerodia according to our ensemble SDMs, including much of central California. The potential distributions of both N. fasciata and N. sipedon overlap extensively with the federally threatened Giant Gartersnake, Thamnophis gigas, which inhabits a similar ecological niche. N. fasciata also poses risk to the federally threatened California Tiger Salamander, Ambystoma californiense, whereas N. sipedon poses risk to some amphibians of conservation concern, including the Foothill Yellow-legged Frog, Rana boylii. We conclude that non-native watersnakes in California can likely inhabit ranges of several native species of conservation concern that are expected to suffer as prey or competing species for these invaders. Action should be taken now to eradicate or control these invasions before detrimental impacts on native species are widespread. Our methods can be applied broadly to quantify the risk posed by incipient invasions to native biodiversity.