Disentangling direct and indirect effects of extreme events on coastal wetland communities.

One of the primary ways in which climate change will impact coastal freshwater wetlands is through changes in the frequency, intensity, timing and distribution of extreme weather events. Disentangling the direct and indirect mechanisms of population- and community-level responses to extreme events is vital to predicting how species composition of coastal wetlands will change under future conditions. We extended static structural equation modelling approaches to incorporate system dynamics in a multi-year multispecies occupancy model to quantify the effects of extreme weather events on a coastal freshwater wetland system. We used data from an 8-year study (2009-2016) on St. Marks National Wildlife Refuge in Florida, USA, to quantify species-specific and community-level changes in amphibian and fish occupancy associated with two flooding events in 2012 and 2013. We examine how physical changes to the landscape, including potential changes in salinity and increased wetland connectivity, may have contributed to or exacerbated the effects of these extreme weather events on the biota of isolated coastal wetlands. We provide evidence that the primary effects of flooding on the amphibian community were through indirect mechanisms via changes in the composition of the sympatric fish community that may have had lethal (i.e. through direct predation) or non-lethal (i.e. through direct or indirect competitive interactions) effects. In addition, we have shown that amphibian species differed in their sensitivity to direct flooding effects and indirect changes in the fish community and wetland-specific conductance, which led to variable responses across the community. These effects led to the overall decline in amphibian species richness from 2009 to 2016, suggesting that wetland-breeding amphibian communities on St. Marks National Wildlife Refuge may not be resilient to predicted changes in coastal disturbance regimes because of climate change. Understanding both direct and indirect effects, as well as species interactions, is important for predicting the effects of a changing climate on individual species, communities and ecosystems.

Species interactions and the effects of climate variability on a wetland amphibian metacommunity.

Disentangling the role that multiple interacting factors have on species responses to shifting climate poses a significant challenge. However, our ability to do so is of utmost importance to predict the effects of climate change on species distributions. We examined how populations of three species of wetland-breeding amphibians, which varied in life history requirements, responded to a six-year period of extremely variable precipitation. This interval was punctuated by both extensive drought and heavy precipitation and flooding, providing a natural experiment to measure community responses to environmental perturbations. We estimated occurrence dynamics using a discrete hidden Markov modeling approach that incorporated information regarding habitat state and predator-prey interactions. This approach allowed us to measure how metapopulation dynamics of each amphibian species was affected by interactions among weather, wetland hydroperiod, and co-occurrence with fish predators. The pig frog, a generalist, proved most resistant to perturbations, with both colonization and persistence being unaffected by seasonal variation in precipitation or co-occurrence with fishes. The ornate chorus frog, an ephemeral wetland specialist, responded positively to periods of drought owing to increased persistence and colonization rates during periods of low-rainfall. Low probabilities of occurrence of the ornate chorus frog in long-duration wetlands were driven by interactions with predators due to low colonization rates when fishes were present. The mole salamander was most sensitive to shifts in water availability. In our study area, this species never occurred in short-duration wetlands and persistence probabilities decreased during periods of drought. At the same time, negative effects occurred with extreme precipitation because flooding facilitated colonization of fishes to isolated wetlands and mole salamanders did not colonize wetlands once fishes were present. We demonstrate that the effects of changes in water availability depend on interactions with predators and wetland type and are influenced by the life history of each of our species. The dynamic species occurrence modeling approach we used offers promise for other systems when the goal is to disentangle the complex interactions that determine species responses to environmental variability.

Life history plasticity does not confer resilience to environmental change in the mole salamander (Ambystoma talpoideum).

Plasticity in life history strategies can be advantageous for species that occupy spatially or temporally variable environments. We examined how phenotypic plasticity influences responses of the mole salamander, Ambystoma talpoideum, to disturbance events at the St. Marks National Wildlife Refuge (SMNWR), FL, USA from 2009 to 2014. We observed periods of extensive drought early in the study, in contrast to high rainfall and expansive flooding events in later years. Flooding facilitated colonization of predatory fishes to isolated wetlands across the refuge. We employed multistate occupancy models to determine how this natural experiment influenced the occurrence of aquatic larvae and paedomorphic adults and what implications this may have for the population. We found that, in terms of occurrence, responses to environmental variation differed between larvae and paedomorphs, but plasticity (i.e. the ability to metamorphose rather than remain in aquatic environment) was not sufficient to buffer populations from declining as a result of environmental perturbations. Drought and fish presence negatively influenced occurrence dynamics of larval and paedomorphic mole salamanders and, consequently, contributed to observed short-term declines of this species. Overall occurrence of larval salamanders decreased from 0.611 in 2009 to 0.075 in 2014 and paedomorph occurrence decreased from 0.311 in 2009 to 0.121 in 2014. Although variation in selection pressures has likely maintained this polyphenism previously, our results suggest that continued changes in environmental variability and the persistence of fish in isolated wetlands could lead to a loss of paedomorphosis in the SMNWR population and, ultimately, impact regional persistence in the future.

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.

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.

Seeking shelter from the storm: Conservation and management of imperiled species in a changing climate.

Climate change is anticipated to exacerbate the extinction risk of species whose persistence is already compromised by habitat loss, invasive species, disease, or other stressors. In coastal areas of the southeastern United States (USA), many imperiled vertebrates are vulnerable to hurricanes, which climate models predict to become more severe in the 21st century. Despite this escalating threat, explicit adaptation strategies that address hurricane threats, in particular, and climate change more generally, are largely underrepresented in recovery planning and implementation. We provide a basis for stronger emphasis on strategic planning for imperiled species facing the increasing threat of catastrophic hurricanes. Our reasoning comes from observations of short-term environmental and biological impacts of Hurricane Michael, which impacted the Gulf Coast of the southeastern USA in October 2018. During this storm, St. Marks National Wildlife Refuge, located along the northern Gulf of Mexico's coast in the panhandle region of Florida, received storm surge that was 3.0-3.6 m (NAVD88) above sea level. Storm surge pushed sea water into some ephemeral freshwater ponds used for breeding by the federally threatened frosted flatwoods salamander (Ambystoma cingulatum). After the storm, specific conductance across all ponds measured varied from 80 to 23,100 µS/cm, compared to 75 to 445 µS/cm in spring 2018. For 17 overwashed wetlands that were measured in both spring and fall 2018, posthurricane conductance observations were, on average, more than 90 times higher than in the previous spring, setting the stage for varying population responses across this coastal landscape. Importantly, we found live individual flatwoods salamanders at both overwashed and non-overwashed sites, although we cannot yet assess the demographic consequences of this storm. We outline actions that could be incorporated into climate adaptation strategies and recovery planning for imperiled species, like A. cingulatum, that are associated with freshwater coastal wetlands in hurricane-prone regions.

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.

Pathogenic lineage of Perkinsea associated with mass mortality of frogs across the United States.

Emerging infectious diseases such as chytridiomycosis and ranavirus infections are important contributors to the worldwide decline of amphibian populations. We reviewed data on 247 anuran mortality events in 43 States of the United States from 1999-2015. Our findings suggest that a severe infectious disease of tadpoles caused by a protist belonging to the phylum Perkinsea might represent the third most common infectious disease of anurans after ranavirus infections and chytridiomycosis. Severe Perkinsea infections (SPI) were systemic and led to multiorganic failure and death. The SPI mortality events affected numerous anuran species and occurred over a broad geographic area, from boreal to subtropical habitats. Livers from all PCR-tested SPI-tadpoles (n = 19) were positive for the Novel Alveolate Group 01 (NAG01) of Perkinsea, while only 2.5% histologically normal tadpole livers tested positive (2/81), suggesting that subclinical infections are uncommon. Phylogenetic analysis demonstrated that SPI is associated with a phylogenetically distinct clade of NAG01 Perkinsea. These data suggest that this virulent Perkinsea clade is an important pathogen of frogs in the United States. Given its association with mortality events and tendency to be overlooked, the potential role of this emerging pathogen in amphibian declines on a broad geographic scale warrants further investigation.

Drought, deluge and declines: the impact of precipitation extremes on amphibians in a changing climate.

The Class Amphibia is one of the most severely impacted taxa in an on-going global biodiversity crisis. Because amphibian reproduction is tightly associated with the presence of water, climatic changes that affect water availability pose a particularly menacing threat to both aquatic and terrestrial-breeding amphibians. We explore the impacts that one facet of climate change-that of extreme variation in precipitation-may have on amphibians. This variation is manifested principally as increases in the incidence and severity of both drought and major storm events. We stress the need to consider not only total precipitation amounts but also the pattern and timing of rainfall events. Such rainfall "pulses" are likely to become increasingly more influential on amphibians, especially in relation to seasonal reproduction. Changes in reproductive phenology can strongly influence the outcome of competitive and predatory interactions, thus potentially altering community dynamics in assemblages of co-existing species. We present a conceptual model to illustrate possible landscape and metapopulation consequences of alternative climate change scenarios for pond-breeding amphibians, using the Mole Salamander, Ambystoma talpoideum, as an example. Although amphibians have evolved a variety of life history strategies that enable them to cope with environmental uncertainty, it is unclear whether adaptations can keep pace with the escalating rate of climate change. Climate change, especially in combination with other stressors, is a daunting challenge for the persistence of amphibians and, thus, the conservation of global biodiversity.