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Adam R. Backlin

Publications and source records attributed to Adam R. Backlin.

At least 19 recordsLinked to original sources

Longevity, age-specific survival, and mean generation time of Rana muscosa: Implications for conservation of possibly the longest lived Ranid frog

Life history strategies vary widely among species and play a vital role in extinction risk, especially in a rapidly changing environment. For many taxa, information on life history such as longevity, lifespan, and generation time is incomplete. This is especially true for amphibians, which have experienced large-scale declines in recent decades. The mountain yellow-legged frog ( Rana muscosa ) is a California endemic recognized as a state and federally endangered species. We evaluated a 23-year dataset of six wild R. muscosa populations in southern California. We calculated the average lifespan of individuals in these six populations to be approximately 9.5 years, with a mean generation time of 7.4 years. We did not detect a difference in longevity between sexes or a difference in apparent survival across various ages of adults. We also documented the longest-lived ranid frog ever recorded from a wild population: a male R. muscosa that was at least 21 years old. Our results suggest a relatively long generation time for this species, a characteristic that may benefit them because reproduction is regularly challenged by drought, fire activity, and disease. This information is important for understanding the complex life history of this endangered ranid frog and can help guide efforts to manage and recover the species.

California

Independent and interactive effects of disease and methylmercury on demographic rates across multiple amphibian populations

Disease, alone or combined with other stressors such as habitat loss and contaminants, affects wildlife populations worldwide. However, interactions among stressors and how they affect demography and populations remain poorly understood. The amphibian chytrid fungus ( Batrachochytrium dendrobatidis ; Bd) is a sometimes-lethal pathogen linked with population declines and extirpations of amphibians globally. Laboratory evidence shows ubiquitous contaminants like methylmercury (MeHg) can reduce vigor and survival of amphibians, but population-level effects remain unclear. We used non-lethal sampling to assess how Bd and MeHg affected survival of juvenile and adult amphibians in 20 populations across the USA. Survival of several species declined with increasing Bd loads, including some species previously considered resistant to Bd (e.g., eastern newt [ Notophthalmus viridescens ]). Although our sampling for MeHg was less intensive than for Bd, we found MeHg can both directly reduce survival and synergistically magnify the effects of Bd infection. For a population of foothill yellow-legged frogs ( Rana boylii ), the estimated reduction in survival from MeHg exceeded that from Bd. Although effects varied widely among populations and species, our results help clarify the potential for synergistic effects of disease and contaminants and emphasize the complexity of identifying and quantifying the population-level effects of interactions among stressors.

Scientific Reports

Biodiversity surveys of Wake Atoll—Featuring field guides for plants, arthropods, and herpetofauna

Introduction The U.S. Air Force (USAF) issued funds to the U.S. Geological Survey (USGS) to update the biosecurity plan, create a current (2019) flora and fauna species identification index, and do container evaluations for the presence of potential invasives. The current (2019) biosecurity protocols used for prevention were evaluated, and new biodiversity surveys were completed for terrestrial vegetation and arthropods and included the first formal reptile surveys. Results from field efforts add to existing knowledge and may identify new species arrivals to Wake. One goal of this project was to update and compile established species information for the atoll and create species identification guides for the three taxonomic groups surveyed. We made these flora and fauna species identification guides by compiling results of the recent (2019) and historical surveys. The guides can be used as resident desktop references, as a baseline for assessing future natural resource surveys, and to assist with guiding management actions. We refer herein to biosecurity and integrated pest management plan materials, which we created simultaneously to inform current (2019) biosecurity and to identify some of the top invasive species at Wake. This study was done in cooperation with the USAF, and surveys were performed for the 611th Civil Engineer Squadron Natural Resources Program, ACES PROJECT #YGFZ170002 under agreement number F2MUAA7116GW02 between the USAF and the USGS Western Ecological Research Center.

Open-File Report

Pan-amphibia distribution of the fungal parasite Batrachochytrium dendrobatidis varies with species and temperature

Batrachochytrium dendrobatidis (Bd) is a globally distributed fungal pathogen of amphibians that has contributed to one of the largest disease-related biodiversity losses in wildlife. Bd is regularly viewed through the lens of a global wildlife epizootic because the spread of highly virulent genetic lineages has resulted in well-documented declines and extinctions of multiple amphibian species. However, the current state of Bd occurrence, host range, host impacts, and ecological drivers remains poorly understood outside of the most negatively affected amphibian species and regions. Our objective was to describe the macroecology of Bd occurrence and infection intensity on caudates (salamanders) across the United States and to compare these patterns with better-studied anurans (frogs and toads). We collected swabs from 11,183 amphibians at 609 sites from 54 species across the United States from 2015 to 2017. We analyzed the prevalence and intensity of Bd infection jointly using a Bayesian hurdle model with covariates of site-level temperature and precipitation, as well as individual characteristics and species identification. Bd was distributed widely across sites and species sampled across the spatial extent of the conterminous United States. We found that Bd prevalence and intensity were most strongly influenced by temperature in the month preceding sampling and by differences among taxon groups. We estimated that temperature had a strong and nonlinear influence on both Bd prevalence and intensity with peak infection at intermediate temperatures and lower infection at low and high temperatures. We found Caudate hosts tended to have higher prevalence than Anuran hosts and Anuran hosts tended to have higher intensity at optimal temperatures for Bd infection. Our findings suggest that Bd has an amphibian-wide host range, temperature gradients exert a strong influence on Bd, and enzootic transmission likely encompasses a much larger spatial and species distribution than previously recognized across North America.

conterminous United States

Understanding and predicting infection dynamics for an endangered amphibian using long-term surveys of wild and translocated frogs

Amphibians are a prominent component of Earth's sixth mass extinction and the fungal pathogen Batrachochytrium dendrobatidis (Bd) is a primary driver of declines. Although Bd dynamics are well studied, the environmental drivers, exacerbating risk factors, and value of conservation interventions like translocations remain challenging to predict. Here, we present results from two decades of Bd monitoring for mountain yellow-legged frogs ( Rana muscosa) in the southern California Transverse and Peninsular mountain ranges. We describe Bd prevalence and infection intensity across sites; model how variables associated with climate, habitat, and populations relate to prevalence; and integrate Bd data from wild and translocated frogs to test whether a machine learning system can predict infection prevalence at new sites. Our findings indicate substantial spatiotemporal variation in Bd dynamics. Bd was present at all sites but prevalence and infection intensities were often low. Environmental features including temperature, precipitation, vegetation, and shortwave radiation explained significant variation in Bd prevalence, but their predictive value varied across mountain ranges. Although clear environmental predictors across populations remain elusive, we provide evidence for the importance of warmer and wetter springs and winters, with implications of increased risk under climate change predictions. We also found evidence for higher Bd prevalence among translocated than wild frogs. Although our machine learning model predicted a Bd prevalence threshold with relatively high accuracy, understanding the factors driving within- and between-population Bd dynamics is complex. Taken together, our findings provide new insights into the complicated role of Bd in amphibian declines and suggest revised management approaches.

California

Effects of temporal hydrologic shifts on the population biology of an endangered freshwater fish in a dryland river ecosystem

Species occupying dryland river ecosystems often experience “boom-and-bust” demographic cycles that coincide with shifts in habitat availability. Knowing whether declines are within natural thresholds versus those caused by acute human disturbance is critical for managing protected species. We investigated temporal shifts in abundance and habitat use of an endangered population of the threespine stickleback Gasterosteus aculeatus in southern California, where a Mediterranean climate leads to ephemeral habitat in one of the regions' least hydrologically modified rivers, the Santa Clara River. We conducted population surveys over a period of below-average rainfall in the upper watershed in Soledad Canyon, with predefined reaches surveyed multiple times per year to capture different hydrologic conditions. Abundances were stable across years but varied significantly depending on location, with some reaches remaining dry and others drying seasonally to varying degrees. Occupancy models showed that the presence of stable perennial reaches, drying regime, and other site-specific factors were important predictors of habitat use, and that certain reaches may be key to ensuring source-sink dynamics as flow dissipates over the dry season. Low occupancy in two sections was driven by different predominant mechanisms, one by diel cycles of evapotranspiration and the other by cattails ( Typha spp.), with both having greater effects during the hotter, drier parts of the year. As dryland river ecosystems are vulnerable to the effects of anthropogenic-induced climate change, this study demonstrates how temporal monitoring can delimit dry-state benchmarks for improving management interventions (i.e., translocation and habitat restoration) for protected species under conditions that are predicted to worsen in the coming years.

California

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 (R 2 ≥ 0.67), whereas total Hg in sediment was not (R 2 ≤ 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.

Environmental Science and Technology

Revisiting conservation units for the endangered mountain yellow-legged frog species complex (Rana muscosa, Rana sierrae) using multiple genomic methods

Insights from conservation genomics have dramatically improved recovery plans for numerous endangered species. However, most taxa have yet to benefit from the full application of genomic technologies. The mountain yellow-legged frog species complex, Rana muscosa and Rana sierrae, inhabits the Sierra Nevada mountains and Transverse/Peninsular Ranges of California and Nevada. Both species have declined precipitously throughout their historical distributions. Conservation management plans outline extensive ongoing recovery efforts but are still based on the genetic structure determined primarily using a single mitochondrial sequence. Our study used two different sequencing strategies – amplicon sequencing and exome capture – to refine our understanding of the population genetics of these imperiled amphibians. We used buccal swabs, museum tissue samples, and archived skin swabs to genotype frog populations across their range. Using the amplicon sequencing and exome capture datasets separately and combined, we document five major genetic clusters. Notably, we found evidence supporting previous species boundaries within Kings Canyon National Park with some exceptions at individual sites. Though we see evidence of genetic clustering, especially in the R. muscosa clade, we also found evidence of some admixture across cluster boundaries in the R. sierrae clade, suggesting a stepping-stone model of population structure. We also find that the southern R. muscosa cluster had large runs of homozygosity and the lowest overall heterozygosity of any of the clusters, consistent with previous reports of marked declines in this area. Overall, our results clarify management unit designations across the range of an endangered species and highlight the importance of sampling the entire range of a species, even when collecting genome-scale data.

California

Protocol for the reintroduction of California red-legged frogs to Santa Monica Mountains National Recreation Area

Once common and widespread in Southern California, California red-legged frogs ( Rana draytonii ) began declining sometime in the middle of the 20th century. They were listed as threatened under the Endangered Species Act in 1996. Three small and isolated populations remained in Los Angeles and Ventura Counties by the start of the 21st century. The nearest population of California red-legged frogs to Santa Monica Mountains National Recreation Area is critically small, located 15 km to the north, yet there is evidence of persistence, including successful reproduction each year it has been measured. A potential solution to alleviate small population size and isolation is to reintroduce a species back to habitable historical locations nearby. In 2011, we initiated a project to reintroduce California red-legged frogs back to the Santa Monica Mountains, where historical records showed they were once widespread. We developed a procedure to transfer partial egg masses into tadpole rearing pens located within streams determined to be suitable for the species. This translocation protocol outlines our procedure and results for the first five years of the project. It is our hope that this protocol will guide and inform similar conservation efforts for California red-legged frogs in other parts of their range as well as other amphibian conservation efforts throughout the world.

California

Genetic structure and historic demography of endangered unarmoured threespine stickleback at southern latitudes signals a potential new management approach

Habitat loss, flood control infrastructure, and drought have left most of southern California and northern Baja California's native freshwater fish near extinction, including the endangered unarmoured threespine stickleback ( Gasterosteus aculeatus williamsoni ). This subspecies, an unusual morph lacking the typical lateral bony plates of the G. aculeatus complex, occurs at arid southern latitudes in the eastern Pacific Ocean and survives in only three inland locations. Managers have lacked molecular data to answer basic questions about the ancestry and genetic distinctiveness of unarmoured populations. These data could be used to prioritize conservation efforts. We sampled G. aculeatus from 36 localities and used microsatellites and whole genome data to place unarmoured populations within the broader evolutionary context of G. aculeatus across southern California/northern Baja California. We identified three genetic groups with none consisting solely of unarmoured populations. Unlike G. aculeatus at northern latitudes, where Pleistocene glaciation has produced similar historical demographic profiles across populations, we found markedly different demographics depending on sampling location, with inland unarmoured populations showing steeper population declines and lower heterozygosity compared to low armoured populations in coastal lagoons. One exception involved the only high elevation population in the region, where the demography and alleles of unarmoured fish were similar to low armoured populations near the coast, exposing one of several cases of artificial translocation. Our results suggest that the current “management-by-phenotype” approach, based on lateral plates, is incidentally protecting the most imperilled populations; however, redirecting efforts toward evolutionary units, regardless of phenotype, may more effectively preserve adaptive potential.

Baja California, California

Taking the leap: A binational translocation effort to close the 420-km gap in the Baja California lineage of the California red-legged frog (Rana draytonii)

Conservation translocations, the human-mediated movement and release of a living organism for a conservation benefit, are increasingly recommended in species’ recovery plans as a technique for mitigating population declines or augmenting genetic diversity. However, translocation protocols for species with broad distributions may require regionally specific considerations to increase success, as environmental gradients may pose different constraints on population establishment and persistence in different parts of the range. Here we report on ongoing, genetically informed translocations of a threatened amphibian, California red-legged frog ( Rana draytonii ), from Baja California, México, to extirpated parts of the range in southern California in the United States, where contemporary stressors related to urbanization, invasive species, and aridification add to the natural environmental challenges already present for amphibians at this ‘warm edge’ of the range. We describe the collaborative binational planning required to jumpstart the effort, the fine-tuning of protocols for collection, transport, headstarting, and release of individuals, and results of multiple translocations, where time will tell whether the successes to date have reached their full potential. The steps outlined in this paper can serve as a template to inform future conservation translocations of imperiled amphibians across the U.S./México border, where the phylogenetics, historical biogeography and future habitat availability of a focal species are blind to political boundaries and critical to guiding recovery actions across the range.

Baja California, California

Range-wide persistence of the endangered arroyo toad (Anaxyrus californicus) for 20+ years following a prolonged drought

Prolonged drought due to climate change has negatively impacted amphibians in southern California, U.S.A. Due to the severity and length of the current drought, agencies and researchers had growing concern for the persistence of the arroyo toad ( Anaxyrus californicus ), an endangered endemic amphibian in this region. Range-wide surveys for this species had not been conducted for at least 20 years. In 2017–2020, we conducted collaborative surveys for arroyo toads at historical locations. We surveyed 88 of the 115 total sites having historical records and confirmed that the arroyo toad is currently extant in at least 61 of 88 sites and 20 of 25 historically occupied watersheds. We did not detect toads at almost a third of the surveyed sites but did detect toads at 18 of 19 specific sites delineated in the 1999 Recovery Plan to meet one of four downlisting criteria. Arroyo toads are estimated to live 7–8 years, making populations susceptible to prolonged drought. Drought is estimated to increase in frequency and duration with climate change. Mitigation strategies for drought impacts, invasive aquatic species, altered flow regimes, and other anthropogenic effects could be the most beneficial strategies for toad conservation and may also provide simultaneous benefits to several other native species that share the same habitat.

California

Defining relevant conservation targets for the endangered Southern California distinct population segment of the mountain yellow-legged frog (Rana muscosa)

The endangered mountain yellow-legged frog ( Rana muscosa ) has been reduced to <10 isolated populations in the wild. Due to frequent catastrophic events (floods, droughts, wildfires), the recent dynamics of these populations have been erratic, making the future of the species highly uncertain. In 2018, a recovery plan was developed to improve the species status by reducing the impacts of various threats (predation, disease, habitat destruction), as well as reinforcing wild populations through the reintroduction of captive-bred frogs. The short-term goal stated in this plan was to reach a minimum of 20 populations of 50 adults each (hereafter, the 20/50 target ), before the species can be considered for downlisting from the U.S. Endangered Species Act. However, there is no guarantee that this 20/50 target will be sufficient to ensure the species persistence in the long run. Using 19 years of mark-recapture data, we estimated populations' demographic trends and assessed the viability of R. muscosa from a starting state of 20 populations of 50 adults each (i.e., the downlisting criteria). Our results reveal that, from this 20/50 state , the species has high chances of persistence only at a short time horizon (50 years). Moreover, >80% of populations would be extinct 50 years later. Therefore, the species will not be able to persist without implementation of the reintroduction program. We found that it is more important to increase the number of suitable sites occupied by R. muscosa than to simply reinforce or augment existing populations. Expanding the current distribution by establishing new populations at suitable sites, even after the “20 populations” mark has been reached, would increase the likelihood of the species' persistence in the longer term.

California

Conservation implications of spatiotemporal variation in the terrestrial ecology of Western spadefoots

Conservation of species reliant on ephemeral resources can be especially challenging in the face of a changing climate. Western spadefoots ( Spea hammondii ) are small burrowing anurans that breed in ephemeral pools, but adults spend the majority of their lives underground in adjacent terrestrial habitat. Western spadefoots are of conservation concern throughout their range because of habitat loss, but little is known about the activity patterns and ecology of their terrestrial life stage. We conducted a radio-telemetry study of adult western spadefoots at 2 sites in southern California, USA, from December 2018 to November 2019 to characterize their survival, behavior, and movements from breeding through aestivation to refine conservation and management for the species. Western spadefoot survival varied seasonally, with risk of mortality higher in the active season than during aestivation. The probability of movement between successive observations was higher during the winter and spring and when atmospheric moisture was high and soil water content at 10-cm depth was low. The amount of rain between observations had the strongest effect on the probability of movement between observations; for every 20 mm of rainfall between observations, western spadefoots were 2.4 times more likely to move. When movements occurred, movement rates were highest when both relative humidity and soil water content at 10-cm depth were high. The conditions under which western spadefoots were likely active on the surface, likely to have moved, and moved at the highest rates are conditions that reduce the risk of desiccation of surface-active spadefoots. Western spadefoot home range areas varied between study sites and were mostly <1 ha, although 1 individual's home range area was >6 ha. Western spadefoots rapidly dispersed from the breeding pools, and asymptotic distances from the breeding pool were generally reached by June. The asymptotic distance from the breeding pool varied between sites, with the 95th percentile of the posterior predictive distribution reaching 486 m at 1 site and 187 m at the other. Western spadefoots did not select most habitat components disproportionately to their availability, but at Crystal Cove State Park, they avoided most evaluated vegetation types (graminoids, forbs, and shrubs). Spatial variation was evident in most evaluated western spadefoot behaviors; context-dependent behavior suggests that site-specific management is likely necessary for western spadefoots. Furthermore, comparison with an earlier study of western spadefoots at Crystal Cove State Park indicated substantial temporal variation in western spadefoot behavior. Therefore, basing management decisions on short-term studies might fail to meet conservation objectives. Better understanding the influences of spatial context and climatic variation on western spadefoot behavior will improve conservation efforts for this species.

California

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.

Continental United States

Mitigation ponds offer drought resiliency for western spadefoot (Spea hammondii) populations

Synergistic effects of habitat loss, drought, and climate change exacerbate amphibian declines. In southern California urbanization continues to convert natural habitat, while prolonged drought reduces surface water availability. Protection of biodiversity may be provided through mitigation; however, the long-term effectiveness of different strategies is often unreported. As a mitigation measure for building a new development within occupied Spea hammondii (western spadefoot) habitat in Orange County, California, artificial breeding pools were constructed at two off-site locations. Spea hammondii tadpoles were translocated from the pools at the development site to two off-site locations in 2005–2006. We conducted surveys a decade later (2016) to determine if S. hammondii were persisting and breeding successfully at either the original development site or the human-made pools at the two mitigation sites. We also verified hydroperiods of any existing pools at all three locations to see if any held water long enough for successful S. hammondii recruitment through metamorphosis. During our study, no pooling water was detected at two of three main sites surveyed, and no S. hammondii were observed at these locations. Twelve of the 14 pools created at only one of the two mitigation sites held water for over 30 d, and we detected successful breeding at seven of these pools. Recruitment in some mitigation ponds indicated that S. hammondii habitat can be created and maintained over 10+ yr, even during the fifth year of a catastrophic drought. Therefore, this may also serve as a conservation strategy to mitigate climate change and habitat loss.

California

Habitat preference modulates trans-oceanic dispersal in a terrestrial vertebrate

The importance of long-distance dispersal (LDD) in shaping geographical distributions has been debated since the nineteenth century. In terrestrial vertebrates, LDD events across large water bodies are considered highly improbable, but organismal traits affecting dispersal capacity are generally not taken into account. Here, we focus on a recent lizard radiation and combine a summary-coalescent species tree based on 1225 exons with a probabilistic model that links dispersal capacity to an evolving trait, to investigate whether ecological specialization has influenced the probability of trans-oceanic dispersal. Cryptoblepharus species that occur in coastal habitats have on average dispersed 13 to 14 times more frequently than non-coastal species and coastal specialization has, therefore, led to an extraordinarily widespread distribution that includes multiple continents and distant island archipelagoes. Furthermore, their presence across the Pacific substantially predates the age of human colonization and we can explicitly reject the possibility that these patterns are solely shaped by human-mediated dispersal. Overall, by combining new analytical methods with a comprehensive phylogenomic dataset, we use a quantitative framework to show how coastal specialization can influence dispersal capacity and eventually shape geographical distributions at a macroevolutionary scale.

Proceedings of the Royal Society B: Biological Sci