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.

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.

Changes in physiology and microbial diversity in larval ornate chorus frogs are associated with habitat quality.

Environmental change associated with anthropogenic disturbance can lower habitat quality, especially for sensitive species such as many amphibians. Variation in environmental quality may affect an organism's physiological health and, ultimately, survival and fitness. Using multiple health measures can aid in identifying populations at increased risk of declines. Our objective was to measure environmental variables at multiple spatial scales and their effect on three indicators of health in ornate chorus frog (Pseudacris ornata) tadpoles to identify potential correlates of population declines. To accomplish this, we measured a glucocorticoid hormone (corticosterone; CORT) profile associated with the stress response, as well as the skin mucosal immune function (combined function of skin secretions and skin bacterial community) and bacterial communities of tadpoles from multiple ponds. We found that water quality characteristics associated with environmental variation, including higher water temperature, conductivity and total dissolved solids, as well as percent developed land nearby, were associated with elevated CORT release rates. However, mucosal immune function, although highly variable, was not significantly associated with water quality or environmental factors. Finally, we examined skin bacterial diversity as it aids in immunity and is affected by environmental variation. We found that skin bacterial diversity differed between ponds and was affected by land cover type, canopy cover and pond proximity. Our results indicate that both local water quality and land cover characteristics are important determinants of population health for ornate chorus frogs. Moreover, using these proactive measures of health over time may aid in early identification of at-risk populations that could prevent further declines and aid in management decisions.

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.

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.

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.

The Significant Surface-Water Connectivity of "Geographically Isolated Wetlands".

We evaluated the current literature, coupled with our collective research expertise, on surface-water connectivity of wetlands considered to be "geographically isolated" (sensu Tiner Wetlands 23:494-516, 2003a) to critically assess the scientific foundation of grouping wetlands based on the singular condition of being surrounded by uplands. The most recent research on wetlands considered to be "geographically isolated" shows the difficulties in grouping an ecological resource that does not reliably indicate lack of surface water connectivity in order to meet legal, regulatory, or scientific needs. Additionally, the practice of identifying "geographically isolated wetlands" based on distance from a stream can result in gross overestimates of the number of wetlands lacking ecologically important surface-water connections. Our findings do not support use of the overly simplistic label of "geographically isolated wetlands". Wetlands surrounded by uplands vary in function and surface-water connections based on wetland landscape setting, context, climate, and geographic region and should be evaluated as such. We found that the "geographically isolated" grouping does not reflect our understanding of the hydrologic variability of these wetlands and hence does not benefit conservation of the Nation's diverse wetland resources. Therefore, we strongly discourage use of categorizations that provide overly simplistic views of surface-water connectivity of wetlands fully embedded in upland landscapes.

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.

Do geographically isolated wetlands influence landscape functions?

Geographically isolated wetlands (GIWs), those surrounded by uplands, exchange materials, energy, and organisms with other elements in hydrological and habitat networks, contributing to landscape functions, such as flow generation, nutrient and sediment retention, and biodiversity support. GIWs constitute most of the wetlands in many North American landscapes, provide a disproportionately large fraction of wetland edges where many functions are enhanced, and form complexes with other water bodies to create spatial and temporal heterogeneity in the timing, flow paths, and magnitude of network connectivity. These attributes signal a critical role for GIWs in sustaining a portfolio of landscape functions, but legal protections remain weak despite preferential loss from many landscapes. GIWs lack persistent surface water connections, but this condition does not imply the absence of hydrological, biogeochemical, and biological exchanges with nearby and downstream waters. Although hydrological and biogeochemical connectivity is often episodic or slow (e.g., via groundwater), hydrologic continuity and limited evaporative solute enrichment suggest both flow generation and solute and sediment retention. Similarly, whereas biological connectivity usually requires overland dispersal, numerous organisms, including many rare or threatened species, use both GIWs and downstream waters at different times or life stages, suggesting that GIWs are critical elements of landscape habitat mosaics. Indeed, weaker hydrologic connectivity with downstream waters and constrained biological connectivity with other landscape elements are precisely what enhances some GIW functions and enables others. Based on analysis of wetland geography and synthesis of wetland functions, we argue that sustaining landscape functions requires conserving the entire continuum of wetland connectivity, including GIWs.

Trends in amphibian occupancy in the United States.

Though a third of amphibian species worldwide are thought to be imperiled, existing assessments simply categorize extinction risk, providing little information on the rate of population losses. We conducted the first analysis of the rate of change in the probability that amphibians occupy ponds and other comparable habitat features across the United States. We found that overall occupancy by amphibians declined 3.7% annually from 2002 to 2011. Species that are Red-listed by the International Union for Conservation of Nature (IUCN) declined an average of 11.6% annually. All subsets of data examined had a declining trend including species in the IUCN Least Concern category. This analysis suggests that amphibian declines may be more widespread and severe than previously realized.

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.

A new parameterization for estimating co-occurrence of interacting species.

Models currently used to estimate patterns of species co-occurrence while accounting for errors in detection of species can be difficult to fit when the effects of covariates on species occurrence probabilities are included. The source of the estimation problems is the particular parameterization used to specify species co-occurrence probability. We develop a new parameterization for estimating patterns of co-occurrence of interacting species that allows the effects of covariates to be specified quite naturally without estimation problems. In our model, the occurrence of one species is assumed to depend on the occurrence of another, but the occurrence of the second species is not assumed to depend on the presence of the first species. This pattern of co-occurrence, wherein one species is dominant and the other is subordinate, can be produced by several types of ecological interactions (predator-prey, parasitism, and so on). A simulation study demonstrated that estimates of species occurrence probabilities were unbiased in samples of 50-100 locations and three surveys per location, provided species are easily detected (probability of detection > or = 0.5). Higher sample sizes (>200 locations) are needed to achieve unbiasedness when species are more difficult to detect. An analysis of data from treefrog surveys in southern Florida indicated that the occurrence of Cuban treefrogs, an invasive predator species, was highest near the point of its introduction and declined with distance from that location. Sites occupied by Cuban treefrogs were 9.0 times less likely to contain green treefrogs and 15.7 times less likely to contain squirrel treefrogs compared to sites without Cuban treefrogs. The detection probabilities of native treefrog species did not depend on the presence of Cuban treefrogs, suggesting that the native treefrog species are naive to the introduced species.

Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA.

From 1999 to 2006, we sampled > 1200 amphibians for the fungal pathogen Batrachochytrium dendrobatidis (Bd) at 30 sites in the southeastern USA. Using histological techniques or PCR assays, we detected chytrid infection in 10 species of aquatic-breeding amphibians in 6 states. The prevalence of chytrid infection was 17.8% for samples of postmetamorphic amphibians examined using skin swab-PCR assays (n = 202 samples from 12 species at 4 sites). In this subset of samples, anurans had a much higher prevalence of infection than caudates (39.2% vs. 5.5%, respectively). Mean prevalence in ranid frogs was 40.7%. The only infected salamanders were Notophthalmus viridescens at 3 sites. We found infected amphibians from late winter through late spring and in 1 autumn sample. Although we encountered moribund or dead amphibians at 9 sites, most mortality events were not attributed to Bd. Chytridiomycosis was established as the probable cause of illness or death in fewer than 10 individuals. Our observations suggest a pattern of widespread and subclinical infections. However, because most of the sites in our study were visited only once, we cannot dismiss the possibility that chytridiomycosis is adversely affecting some populations. Furthermore, although there is no evidence of chytrid-associated declines in our region, the presence of this pathogen is cause for concern given global climate change and other stressors. Although presence-absence surveys may still be needed for some taxa, such as bufonids, we recommend that future researchers focus on potential population-level effects at sites where Bd is now known to occur.

The effect of community composition on persistence of prey with their predators in an assemblage of pond-breeding amphibians.

We examined whether the species composition of a community influences the persistence of larval Ambystoma maculatum in assemblages composed of two larger intraguild predators (A. opacum and A. jeffersonianum) and an alternative prey species (tadpoles of Rana sylvatica). We predicted a priori that A. maculatum would have higher survival in more diverse communities containing alternative species of prey and top predators (A. opacum), the latter of which may lower the abundance of intermediate predators (A. jeffersonianum) via intraguild predation. In a factorial experiment, we manipulated the presence of larval A. opacum, A. jeffersonianum, and R. sylvatica in replicated artificial ponds containing larval A. maculatum. The presence of all three species significantly depressed biomass production in A. maculatum: biomass was highest in ponds lacking the other species and was zero in ponds initially containing all four species. Tadpoles severely reduced the growth of filamentous algae in the ponds. This, in turn, may have affected the abundance of some herbivorous prey of larval salamanders, although this possibility was not tested. The presence of congeneric predators severely restricted the presence in the water column of larval A. maculatum, which otherwise exhibited significant diel patterns of activity in the absence of predators. Together, the presence of tadpoles and a predator-mediated reduction in activity patterns may have limited foraging opportunities for A. maculatum, thus exacerbating the direct impact of predation on survival in this species. These results suggest that diverse assemblages consisting of these particular species may actually inhibit, rather than promote, inclusion of A. maculatum in some communities of pond-breeding amphibians.

Differential vulnerability to predation and refuge use in competing larval salamanders.

The aquatic larvae of two species of salamanders coexist as a result of differences in their competitive abilities: Ambystoma talpoideum is a superior aggressor, whereas A. maculatum is a superior forager. I examined the behavioral mechanisms that permit these species to coexist with their predatory congener, A. opacum. I asked whether the two prey species differ in their vulnerability to predation and in their use of structural and spatial refugia when under the risk of predation; such inter-specific variation may allow predation to contribute indirectly to prey coexistence. Larval A. maculatum (the superior forager) was more vulnerable to predation by A. opacum than was A. talpoideum, and only the latter species significantly increased its use of structural refugia (leaf litter) in the presence of the predator. In pond enclosures, both species of prey exhibited diel patterns of microhabitat use; significantly more larvae occupied shallow regions of enclosures during the day and migrated to deeper water (a spatial refugium) at night. However, when considered separately, neither (1) the presence of a predatory larval A. opacum nor (2) an increased density of intra- and interspecific competitors significantly altered this habitat shift for either prey species. Rather, diel microhabitat usage in A. talpoideum was significantly affected by an interaction between predator presence and competitor density. My results demonstrate the importance of refugia to coexistence in this predator-prey assemblage. Furthermore, predation by A. opacum may mediate prey competition; that is, preferential consumption of A. maculatum may reduce the competitive impact of this superior forager on A. talpoideum, thus enhancing their coexistence.

Morphological variation in a larval salamander: dietary induction of plasticity in head shape.

We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander, Ambystoma macrodactylum columbianum. Larvae in some populations of this species exhibit trophic polymorphism, with some individuals possessing exaggerated trophic features characteristic of a cannibalistic morphology in larval Ambystoma; e.g. a disproportionately broad head and hypertrophied vomerine teeth. We hypothesized that 1) head shape variation results from feeding upon different types of prey and that 2) cannibal morphs are induced by consumption of conspecifics. To induce variation, we fed three groups of larvae different diets: 1) brine shrimp nauplii only; 2) nauplii plus anuran tadpoles; 3) nauplii, tadpoles and conspecific larval salamanders. Comparisons of size (mass)-adjusted means revealed that this manipulation of diet induced significant variation in six measures of head shape, but not in the area of the vomerine tooth patch. For five of the six head traits, larvae that ate tadpoles and brine shrimp nauplii developed significantly broader, longer and deeper heads than did larvae that only ate brine shrimp nauplii. The ingestion of conspecifics, in addition to nauplii and tadpoles, significantly altered two head traits (interocular-width and head depth), compared to larvae only fed nauplii and tadpoles. Canonical discriminant function analysis detected two statistically reliable canonical variables: head depth was most highly associated with the first canonical variable, whereas three measures of head width (at the jaws, gills and eyes) and interocular width were most highly associated with the second canonical variable. Despite this diet-enhanced morphological variation, there was no indication that any of the three types of diet (including conspecific prey) induced the exaggerated trophic features of the "cannibal" morph in this species. These results illustrate that ingestion of different types of prey contributes to plasticity in head shape, but that some other proximate cue(s), either alone or in combination with diet variation, is essential to induce the extremes of trophic polymorphism in this species.