William E. Peterman

Projected Loss of a Salamander Diversity Hotspot as a Consequence of Projected Global Climate Change

Background Significant shifts in climate are considered a threat to plants and animals with significant physiological limitations and limited dispersal abilities. The southern Appalachian Mountains are a global hotspot for plethodontid salamander diversity. Plethodontids are lungless ectotherms, so their ecology is strongly governed by temperature and precipitation. Many plethodontid species in southern Appalachia exist in high elevation habitats that may be at or near their thermal maxima, and may also have limited dispersal abilities across warmer valley bottoms. Methodology/Principal Findings We used a maximum-entropy approach (program Maxent) to model the suitable climatic habitat of 41 plethodontid salamander species inhabiting the Appalachian Highlands region (33 individual species and eight species included within two species complexes). We evaluated the relative change in suitable climatic habitat for these species in the Appalachian Highlands from the current climate to the years 2020, 2050, and 2080, using both the HADCM3 and the CGCM3 models, each under low and high CO2 scenarios, and using two-model thresholds levels (relative suitability thresholds for determining suitable/unsuitable range), for a total of 8 scenarios per species. Conclusion/Significance While models differed slightly, every scenario projected significant declines in suitable habitat within the Appalachian Highlands as early as 2020. Species with more southern ranges and with smaller ranges had larger projected habitat loss. Despite significant differences in projected precipitation changes to the region, projections did not differ significantly between global circulation models. CO2 emissions scenario and model threshold had small effects on projected habitat loss by 2020, but did not affect longer-term projections. Results of this study indicate that choice of model threshold and CO2 emissions scenario affect short-term projected shifts in climatic distributions of species; however, these factors and choice of global circulation model have relatively small affects on what is significant projected loss of habitat for many salamander species that currently occupy the Appalachian Highlands.

Ecological resistance surfaces predict fine‐scale genetic differentiation in a terrestrial woodland salamander

Landscape genetics has seen tremendous advances since its introduction, but parameterization and optimization of resistance surfaces still poses significant challenges. Despite increased availability and resolution of spatial data, few studies have integrated empirical data to directly represent ecological processes as genetic resistance surfaces. In our study, we determine the landscape and ecological factors affecting gene flow in the western slimy salamander (Plethodon albagula). We used field data to derive resistance surfaces representing salamander abundance and rate of water loss through combinations of canopy cover, topographic wetness, topographic position, solar exposure and distance from ravine. These ecologically explicit composite surfaces directly represent an ecological process or physiological limitation of our organism. Using generalized linear mixed‐effects models, we optimized resistance surfaces using a nonlinear optimization algorithm to minimize model AIC. We found clear support for the resistance surface representing the rate of water loss experienced by adult salamanders in the summer. Resistance was lowest at intermediate levels of water loss and higher when the rate of water loss was predicted to be low or high. This pattern may arise from the compensatory movement behaviour of salamanders through suboptimal habitat, but also reflects the physiological limitations of salamanders and their sensitivity to extreme environmental conditions. Our study demonstrates that composite representations of ecologically explicit processes can provide novel insight and can better explain genetic differentiation than ecologically implicit landscape resistance surfaces. Additionally, our study underscores the fact that spatial estimates of habitat suitability or abundance may not serve as adequate proxies for describing gene flow, as predicted abundance was a poor predictor of genetic differentiation.

Fine-Scale Habitat Associations of a Terrestrial Salamander: The Role of Environmental Gradients and Implications for Population Dynamics

Environmental gradients are instrumental in shaping the distribution and local abundance of species because at the most fundamental level, an organism’s performance is constrained by the environment it inhabits. In topographically complex landscapes, slope, aspect, and vegetative cover interact to affect solar exposure, creating temperature-moisture gradients and unique microclimates. The significance of the interaction of abiotic gradients and biotic factors such as competition, movement, or physiology has long been recognized, but the scale at which these factors vary on the landscape has generally precluded their inclusion in spatial abundance models. We used fine-scale spatial data relating to surface-soil moisture, temperature, and canopy cover to describe the spatial distribution of abundance of a terrestrial salamander, Plethodon albagula, across the landscape. Abundance was greatest in dense-canopy ravine habitats with high moisture and low solar exposure, resulting in a patchy distribution of abundance. We hypothesize that these patterns reflect the physiological constraints of Plethodontid salamanders. Furthermore, demographic cohorts were not uniformly distributed among occupied plots on the landscape. The probability of gravid female occurrence was nearly uniform among occupied plots, but juveniles were much more likely to occur on plots with lower surface temperatures. The disconnect between reproductive effort and recruitment suggests that survival differs across the landscape and that local population dynamics vary spatially. Our study demonstrates a connection between abundance, fine-scale environmental gradients, and population dynamics, providing a foundation for future research concerning movement, population connectivity, and physiology.

Intermediate Pond Sizes Contain the Highest Density, Richness, and Diversity of Pond-Breeding Amphibians

We present data on amphibian density, species richness, and diversity from a 7140-ha area consisting of 200 ponds in the Midwestern U.S. that represents most of the possible lentic aquatic breeding habitats common in this region. Our study includes all possible breeding sites with natural and anthropogenic disturbance processes that can be missing from studies where sampling intensity is low, sample area is small, or partial disturbance gradients are sampled. We tested whether pond area was a significant predictor of density, species richness, and diversity of amphibians and if values peaked at intermediate pond areas. We found that in all cases a quadratic model fit our data significantly better than a linear model. Because small ponds have a high probability of pond drying and large ponds have a high probability of fish colonization and accumulation of invertebrate predators, drying and predation may be two mechanisms driving the peak of density and diversity towards intermediate values of pond size. We also found that not all intermediate sized ponds produced many larvae; in fact, some had low amphibian density, richness, and diversity. Further analyses of the subset of ponds represented in the peak of the area distribution showed that fish, hydroperiod, invertebrate density, and canopy are additional factors that drive density, richness and diversity of ponds up or down, when extremely small or large ponds are eliminated. Our results indicate that fishless ponds at intermediate sizes are more diverse, produce more larvae, and have greater potential to recruit juveniles into adult populations of most species sampled. Further, hylid and chorus frogs are found predictably more often in ephemeral ponds whereas bullfrogs, green frogs, and cricket frogs are found most often in permanent ponds with fish. Our data increase understanding of what factors structure and maintain amphibian diversity across large landscapes.

Spatial variation in water loss predicts terrestrial salamander distribution and population dynamics

Many patterns observed in ecology, such as species richness, life history variation, habitat use, and distribution, have physiological underpinnings. For many ectothermic organisms, temperature relationships shape these patterns, but for terrestrial amphibians, water balance may supersede temperature as the most critical physiologically limiting factor. Many amphibian species have little resistance to water loss, which restricts them to moist microhabitats, and may significantly affect foraging, dispersal, and courtship. Using plaster models as surrogates for terrestrial plethodontid salamanders (Plethodon albagula), we measured water loss under ecologically relevant field conditions to estimate the duration of surface activity time across the landscape. Surface activity time was significantly affected by topography, solar exposure, canopy cover, maximum air temperature, and time since rain. Spatially, surface activity times were highest in ravine habitats and lowest on ridges. Surface activity time was a significant predictor of salamander abundance, as well as a predictor of successful recruitment; the probability of a juvenile salamander occupying an area with high surface activity time was two times greater than an area with limited predicted surface activity. Our results suggest that survival, recruitment, or both are demographic processes that are affected by water loss and the ability of salamanders to be surface-active. Results from our study extend our understanding of plethodontid salamander ecology, emphasize the limitations imposed by their unique physiology, and highlight the importance of water loss to spatial population dynamics. These findings are timely for understanding the effects that fluctuating temperature and moisture conditions predicted for future climates will have on plethodontid salamanders.

Climate change and shrinking salamanders: alternative mechanisms for changes in plethodontid salamander body size

An increasing number of studies have demonstrated relationships between climate trends and body size change of organisms. In many cases, climate might be expected to influence body size by altering thermoregulation, energetics or food availability. However, observed body size change can result from a variety of ecological processes (e.g. growth, selection, population dynamics) or imperfect observation of biological systems. We used two extensive datasets to evaluate alternative mechanisms for recently reported changes in the observed body size of plethodontid salamanders. We found that mean adult body size of salamanders can be highly sensitive to survey conditions, particularly rainfall. This systematic bias in the detection of larger or smaller individuals could result in a signature of body size change in relation to reported climate trends when it is simply observation error. We also identify considerable variability in body size distributions among years and find that individual growth rates can be strongly influenced by weather. Finally, our study demonstrates that measures of mean adult body size can be highly variable among surveys and that large sample sizes may be required to make reliable inferences. Identifying the effects of climate change is a critical area of research in ecology and conservation. Researchers should be aware that observed changes in certain organisms can result from multiple ecological processes or systematic bias due to nonrandom sampling of populations.

Life history differences influence the impacts of drought on two pond-breeding salamanders

Drought is a strong density-independent environmental filter that contributes to population regulation and other ecological processes. Not all species respond similarly to drought, and the overall impacts can vary depending on life histories. Such differences can necessitate management strategies that incorporate information on individual species to maximize conservation success. We report the effects of a short-term drought on occupancy and reproductive success of two pond-breeding salamanders that differ in breeding phenology (fall vs. spring breeder) across an active military base landscape in Missouri, USA: We surveyed ~200 ponds for the presence of eggs, larvae, and metamorphs from 2011 to 2013. This period coincided with before, during, and after a severe drought that occurred in 2012. The two species showed contrasting responses to drought, where high reproductive failure (34% of ponds) was observed for the spring breeder during a single drought year. Alternatively, the fall breeder only showed a cumulative 8% failure over two years. The number of breeding ponds available for use in the fall decreased during the drought due to pond drying and/or a lack of re-filling. Estimates of occupancy probability declined for the fall-breeding salamander between 2012 and 2013, whereas occupancy probability estimates of the spring breeder increased post-drought. The presence of fish, hydroperiod, the amount of forest cover surrounding ponds, and canopy cover were all found to affect estimates of occupancy probabilities of each species. Pond clustering (distance to nearest pond and the number of ponds within close proximity), hydroperiod, forest cover, and canopy cover influenced both estimates of colonization and extinction probabilities. Our results show life history variation can be important in determining the relative susceptibility of a species to drought conditions, and that sympatric species experiencing the same environmental conditions can respond differently. Consideration of the spatial network and configuration of habitat patches that act as refuges under extreme environmental conditions will improve conservation efforts, such as the placement of permanent ponds for aquatic organisms. A better awareness of species-specific tolerances to environmental filters such as drought can lead to improved management recommendations to conserve and promote habitat for a greater diversity of species across landscapes of spatially connected populations.

Habitat traits and species interactions differentially affect abundance and body size in pond-breeding amphibians.

In recent studies, habitat traits have emerged as stronger predictors of species occupancy, abundance, richness and diversity than competition. However, in many cases, it remains unclear whether habitat also mediates processes more subtle than competitive exclusion, such as growth, or whether intra- and interspecific interactions among individuals of different species may be better predictors of size. To test whether habitat traits are a stronger predictor of abundance and body size than intra- and interspecific interactions, we measured the density and body size of three species of larval salamanders in 192 ponds across a landscape. We found that the density of larvae was best predicted by models that included habitat features, while models incorporating interactions among individuals of different species best explained the body size of larvae. Additionally, we found a positive relationship between focal species density and congener density, while focal species body size was negatively related to congener density. We posit that salamander larvae may not experience competitive exclusion and thus reduced densities, but instead compensate for increased competition behaviourally (e.g. reduced foraging), resulting in decreased growth. The discrepancy between larval density and body size, a strong predictor of fitness in this system, also highlights a potential shortcoming in using density or abundance as a metric of habitat quality or population health.

ResistanceGA: An R package for the optimization of resistance surfaces using genetic algorithms

First coined in 2003, landscape genetics has experienced rapid growth in both the number of studies and range of analytical methods utilized (Manel, Schwartz, Luikart, & Taberlet, 2003; Storfer, Murphy, Spear, Holderegger, & Waits, 2010). This integrative field draws on landscape ecology, spatial statistics, and population genetics to address a wide range of questions. Landscape genetic studies frequently seek to understand how landscape features affect spatial genetic structure (Manel et al., 2003; Storfer et al., 2007), often with a goal of quantifying the effective distance between sample locations as a function of the landscape matrix (McRae, 2006; Spear, Peterson, Matocq, & Storfer, 2005). In the absence of direct observation of movement or dispersal across the landscape, effective distances are often interpreted as functional connectivity (e.g. Cushman, McKelvey, Hayden, & Schwartz, 2006). However, functional connectivity and effective distance require an appropriately parameterized resistance surface. As defined by Spear, Balkenhol, Fortin, McRae, and Scribner (2010), a resistance surface is a spatial layer that assigns a value to each landscape or environmental feature, with values representing the extent to which that feature impedes or facilitates connectivity for an organism. Resistance values of surfaces have been determined using a variety of methods, including: habitat suitability models (e.g. Wang, Yang, Bridgman, & Lin, 2008), telemetry (e.g. Driezen, Adriaensen, Rondinini, Doncaster, & Matthysen, 2007) and statistical Received: 27 October 2017 | Accepted: 1 February 2018 DOI: 10.1111/2041-210X.12984

The effects of temperature and activity on intraspecific scaling of metabolic rates in a lungless salamander.

The scaling of metabolic rate with body mass holds substantial predictive power as many biological processes depend on energy. A significant body of theory has been developed based on the assumption that metabolic rate scales with body mass as a power function with an exponent of 0.75, and that this scaling relationship is independent of temperature. Here we test this hypothesis at the intraspecific level in a lungless salamander using data on both standard and maximal metabolic rates (SMR and MMR, respectively). We also address a recently proposed alternative explanation that predicts systematic variation in this mass-scaling exponent, the metabolic level boundaries hypothesis (MLB). Consistent with predictions of the metabolic theory of ecology the mass scaling of SMR and MMR were independent of temperature, however, we find evidence that the mass-scaling exponent for SMR and MMR differ significantly from 0.75. Further, our data do not provide strong support for MLB. Mass-scaling exponents for MMR generally exceed those for SMR, although these differences are rarely statistically significant.