Species Of Plethodontid Salamanders Research Articles

Different patterns of introgression in a three species hybrid zone among European cave salamanders.

Hybrid zones occur where genetically distinct populations meet, mate and produce offspring with mixed ancestry. In Plethodontid salamanders, introgressive hybridization is a common phenomenon, where hybrids backcross with parental populations leading to the spread of new alleles into the parental genomes. Whereas many hybrid zones have been reported in American Plethodontid salamanders, only a single hybrid zone has been documented in European plethodontids so far, which is located at the Apuan Alps in the Italian Peninsula. Here, we describe a previously unreported hybrid zone in the Northern Apennines involving all the three Plethodontid salamander species inhabiting the Italian Peninsula. We found 21 new Speleomantes sites of occurrence, from a hitherto unexplored area located at the boundaries between three Speleomantes species ranges. Using mitochondrial (Cytb and ND2 genes) and nuclear markers (two diagnostic SNPs at the NCX1 gene), we revealed a three-way contact zone where all the three mainland species hybridize: S. strinatii, S. ambrosii and S. italicus. We observed a strong mitonuclear discordance, with mitochondrial markers showing a conspicuous geographic pattern, while diagnostic nuclear SNPs coexisted in both the same populations and individuals, providing evidence of hybridization in many possible combinations. The introgression is asymmetric, with S. italicus mitogenome usually associated with S. a. ambrosii and, to a lesser extent, to S. strinatii nuclear alleles. This finding confirms that Plethodontid are a group of choice to investigate hybridization mechanisms and suggests that behavioural, genetic and ecological components may concur in determining the direction and extent of introgression.

Microclimate species distribution models estimate lower levels of climate-related habitat loss for salamanders

Species distribution models (SDMs) largely rely on free-air temperatures at coarse spatial resolutions to predict habitat suitability, potentially overlooking important microhabitat. Integrating microclimate data into SDMs may improve predictions of organismal responses to climate change and support targeting of conservation assets at biologically relevant scales, especially for small, dispersal-limited species vulnerable to climate-change-induced range loss. We integrated microclimate data that account for the buffering effects of forest vegetation into SDMs at a very high spatial resolution (3 m2) for three plethodontid salamander species in Great Smoky Mountains National Park (North Carolina and Tennessee). Microclimate SDMs were used to characterize potential changes to future plethodontid habitat, including habitat suitability and habitat spatial patterns. Additionally, we evaluated spatial discrepancies between predictions of habitat suitability developed with microclimate and coarse-resolution, free-air climate data. Microclimate SDMs indicated substantial losses to plethodontid ranges and highly suitable habitat by mid-century, but at much more conservative levels than coarse-resolution models. Coarse-resolution SDMs generally estimated higher mid-century losses to plethodontid habitat compared to microclimate models and consistently undervalued areas containing highly suitable microhabitat. Furthermore, microclimate SDMs revealed potential areas of future gain in highly suitable habitat within current species’ ranges, which may serve as climatic microrefugia. Taken together, this study highlights the need to develop microclimate SDMs that account for vegetation and its biophysical effects on near-surface temperatures. As microclimate datasets become increasingly available across the world, their integration into correlative and mechanistic SDMs will be imperative for accurately estimating organismal responses to climate change and helping environmental managers tasked with spatially prioritizing conservation assets.

A new arboreal Pseudoeurycea (Caudata: Plethodontidae) from the Sierra de Zongolica, Veracruz, Mexico

We describe a new species of plethodontid salamander of the genus Pseudoeurycea from the Sierra de Zongolica, Veracruz, Mexico. The new species is distinguished from all other species in the genus by morphological and genetic features and by coloration. Based on a mtDNA phylogeny, the new species belongs to the Pseudoeurycea juarezi group and is most closely related to P. ruficauda from the Sierra Mazateca in northern Oaxaca. The newly described salamander increases the number of species of plethodontid salamanders from Veracruz to 43 and those recognized from Mexico to 140.

Aerial maneuvering by plethodontid salamanders spanning an arboreality gradient.

Wandering salamanders (Aneides vagrans) inhabit the crowns of the world's tallest trees, taking refuge in epiphytic fern mats within these complex arboreal environments. These salamanders readily jump from the canopy when disturbed and maintain stable postures while falling via fine adjustments of the limbs and tail in lieu of dedicated aerodynamic control surfaces, thus reliably carrying out non-vertical descent. Here, we examined the aerial behavior and performance of A. vagrans and three other species of plethodontid salamander across a habitat gradient of arboreality by recording salamanders falling from short heights and moving within the jet of a vertical wind tunnel. Kinematic performance of aerial behavior in plethodontid salamanders was correlated with a gradient of arboreal habitats; moreover, salamanders from arboreal niches were more effective in slowing and redirecting descent compared with other salamanders. Aneides vagrans and the closely related Aneides lugubris consistently engaged in parachuting and gliding when falling; their trajectories were very steep, but were sufficiently angled to enable contact with either the home trunk or nearby branches during falls or jumps from great heights. Aerial maneuvering in arboreal salamanders is similar to that seen in other vertebrates capable of non-vertical and controlled descent, suggesting that the long limbs and active tail of these arboreal plethodontids (often cited as adaptations for climbing) may also contribute to parachuting and gliding when falling from trees. These aerial behaviors within the redwood canopy warrant further investigations into other canopy residents that lack conspicuous surfaces for aerodynamic control.

Short‐term responses of riparian salamander populations to wildfire in the Southern Appalachians

AbstractWildfire is a natural disturbance within many forest ecosystems and is rapidly becoming more frequent and severe because of the combination of historical fire suppression and climate change. In Southern Appalachian hardwood forests, there is a limited understanding of how salamander populations respond to wildfire, despite their high diversity and abundance in forest ecosystems. We expected populations of lungless, plethodontid salamanders to respond negatively to wildfire and the drier microhabitat conditions in burned habitat. We evaluated the effect of fire on 3 plethodontid salamander species (Blue Ridge two‐lined salamander [Eurycea wilderae], Ocoee salamander [Desmognathus ocoee], red‐legged salamander [Plethodon shermani]) with different life histories from 2017–2019 following a wildfire in a Southern Appalachian riparian forest in North Carolina, USA. We estimated differences in abundance, frequency of adults in the population, and terrestrial distribution in relation to streams between burned and reference riparian forest sites. Wildfire had negative effects on the abundance of semi‐aquatic species, but temporal patterns differed by species. Abundance of the Blue Ridge two‐lined salamander was lower in burn sites than reference sites immediately after fire, followed by a gradual convergence towards reference‐site densities. Conversely, Ocoee salamanders had a time‐lagged response, where we observed significantly lower densities in burn sites relative to reference sites for only 2 years after fire. We did not observe strong responses of red‐legged salamander abundance to fire. There were no consistent patterns in how the percentage of adults in reference or burn sites differed over time, suggesting that population responses to burn vary by species. Finally, we observed adults of all species and juveniles of semi‐aquatic species farther from streams in burn sites. Our findings suggest plethodontid salamander communities may tolerate riparian wildfires, although longer‐term studies are required to understand how long it takes for patterns of population size structure and habitat use to converge with those in unburned reference sites.

The Asian plethodontid salamander preserves historical genetic imprints of recent northern expansion

The Korean Peninsula, located at the southern tip of Northeast Asia, has never been covered by ice sheets and was a temperate refugium during the Pleistocene. Karsenia koreana, the sole Asian plethodontid salamander species, occurs only on the southern half of the Korean Peninsula and is thought to have found various climatic refugia. Despite its phylogenetic and biogeographic importance, no population-level genetic analysis has been performed on this species. Here we study the population genetic structure of K. koreana using mitochondrial and microsatellite loci to understand the recent historical dispersion process that shaped its current distribution. Overall, the genetic distance between populations correlated well with the spatial distance, and the genetic structure among populations showed signs of a unilateral northward expansion from a southernmost refugium population. Given the distinct genetic structure formed among the populations, the level of historical gene flow among populations appears to have been very low. As the estimated effective population size of K. koreana was also small, these results suggest that the small, restricted populations of K. koreana are extremely vulnerable to environmental changes that may require high levels of genetic diversity to cope with. Thus, special management strategies are needed to preserve these remnant populations.

Effect of temperature on subclinical infection by Batrachochytrium dendrobatidis in three species of plethodontid salamanders

Abstract We assessed the effect of temperature on subclinical Batrachochytrium dendrobatidis (Bd) infection in three species of plethodontids. Collected individuals were tested for Bd in the field during the dry and rainy season and randomly assigned to 15° and 18°C treatments for 30 days. We collected 129 salamanders, of these nine individuals tested positive for Bd in the field. At the two temperature trials, 12 individuals that were Bd-negative in the field, tested positive for Bd. Near the end of the temperature trials, 18 of 21 Bd-positive individuals tested negative for Bd. Three individuals that were Bd positive in the field and assigned to the 18°C trial died during the experiment. Our results suggest that at 15°C the most of plethodontids present subclinical infection, whereas at higher temperatures, Bd infection can increase to detectable levels. The processes underlying plethodontids’s recovery from Bd infection warrants further study.

Batracholandros salamandrae (Oxyuroidea: Pharyngodonidae) in Endemic Salamanders (Amphibia: Plethodontidae) of the Trans-Mexican Volcanic Belt: Host Range Wide Distribution or Cryptic Species Complex?

Salamanders of the tribe Bolitoglossini Hallowell are a highly diversified group of amphibians, and their helminth parasite fauna has been scarcely studied. Some species of plethodontid salamanders distributed along the Trans-Mexican Volcanic Belt, in central Mexico, were sampled, and their helminth parasites were recovered for taxonomic identification. Specimens of a pharyngodonid nematode from 2 species of bolitoglossines of the genus Pseudoeurycea Taylor were morphologically identified as Batracholandros salamandrae (Schad, 1960) Petter and Quentin, 1976. These specimens were studied in further detail through light and scanning electron microscopy and were sequenced for 2 ribosomal genes and 1 mitochondrial gene to test the hypothesis of whether B. salamandrae is a species widely distributed in salamanders across the Nearctic biogeographic region, or if it represents a cryptic species complex. Our molecular results revealed that these specimens consisted of 2 genetic lineages in concordance with host species, although with slight morphological differences among specimens in each of them. A thorough study, including the generation of molecular data from individuals from other areas of North America, and the examination of type specimens, is required to test the reliability of these morphological differences and to corroborate the species identity of the 2 genetic lineages.

A New Species of Pseudoeurycea (Amphibia: Caudata) from the Mountains of Central Veracruz, Mexico

ABSTRACT We describe a new species of plethodontid salamander of the genus Pseudoeurycea from the mountains of central Veracruz, Mexico. This species can be distinguished from its congeners by colo...

Scaling between macro- to microscale climatic data reveals strong phylogenetic inertia in niche evolution in plethodontid salamanders.

Macroclimatic niches are indirect and potentially inadequate predictors of the realized environmental conditions that many species experience. Consequently, analyses of niche evolution based on macroclimatic data alone may incompletely represent the evolutionary dynamics of species niches. Yet, understanding how an organisms' climatic (Grinnellian) niche responds to changing macroclimatic conditions is of vital importance for predicting their potential response to global change. In this study, we integrate microclimatic and macroclimatic data across 26 species of plethodontid salamanders to portray the relationship between microclimatic niche evolution in response to changing macroclimate. We demonstrate stronger phylogenetic signal in microclimatic niche variables than at the macroclimatic scale. Even so, we find that the microclimatic niche tracks climatic changes at the macroscale, but with a phylogenetic lag at million-year timescales. We hypothesize that behavioral tracking of the microclimatic niche over space and phenology generates the lag: salamanders preferentially select microclimates similar to their ancestral conditions rather than adapting with changes in physiology. We demonstrate that macroclimatic variables are weak predictors of niche evolution and that incorporating spatial scale into analyses of niche evolution is critical for predicting responses to climate change.

Experimental evidence indicates variable responses to forest disturbance and thermal refugia by two plethodontid salamanders

Understanding how natural and anthropogenic disturbances affect sensitive species is critical to support conservation programs as land use activities and climatic conditions change. Forest management provides a range of ecosystem services to expanding human populations including production of substantial amounts of woody biomass, thereby reducing area under management and increasing opportunity for conservation designations. However, relatively little experimental information is available to describe how manipulating habitat at multiple scales may affect spatial and temporal variation in populations of climate-sensitive forest taxa. We conducted a Before-After Control-Impact experiment over seven years to evaluate responses of two species of Plethodontid salamanders in operational treatment (harvest, replanting, and herbicide application) and control units, Oregon, USA. In addition, we capitalized on existing variation in downed wood size and accounted for potential behavioral responses to evaluate the thermal refugia hypothesis. For Oregon slender salamanders (Batrachoseps wrighti), mean plot-level occupancy (90% CRI) was increased an estimated 11% (1.11; 0.62–2.1) and estimated mean abundance reduced 16% (0.84; 0.54–1.4) post-harvest. For Ensatina (Ensatina eschscholtzii), mean occupancy was reduced an estimated 80% (0.20; 0.08–0.47) and estimated mean abundance reduced 63% (0.37; 0.22–0.65) post-harvest. We found strong evidence of positive associations for both species with downed wood amount. As predicted, we found ambient temperatures to be higher in harvest than control units. Also, internal downed wood temperatures were warmer in harvested units, suggesting these structures may not have provided adequate thermal refugia. Application of an experimental framework provided evidence about both stand and structure level responses to active management. Habitat structures did not appear to buffer against substantial variation in local climate but evidence was equivocal about importance of these structures to population retention. Monitoring of recruitment and retention of downed wood through subsequent rotations can provide critical information to reduce trade-offs between wood production and conservation of climate sensitive taxa.

Jumping in arboreal salamanders: A possible tradeoff between takeoff velocity and in-air posture

Jumping performance can have important implications for an animal’s fitness by expanding its ability to evade predators and move between microhabitats. Jumping in terrestrial plethodontid salamanders is achieved through lateral bending and rapid unbending of the trunk, an action powered by axial musculature. Arboreal plethodontids, some of which are known to occupy tree crowns, tend to have more robust limbs and longer digits, which may affect their jumping kinematics and performance. We examined jumping kinematics in ten species of plethodontid salamanders, including four arboreal species of the genus Aneides, using high speed imaging and kinematic analysis. Salamanders of the genus Aneides exhibit lower takeoff velocities when compared with the terrestrial plethodontids Eurycea, Desmognathus, and Plethodon, possibly due to reduced trunk bending. Aneides also exhibit higher frequencies of two-footed takeoffs, and often orient their feet to launch from vertical surfaces when presented with the option. This suggests an alternative jumping behavior in salamanders that may reflect an arboreal lifestyle. All plethodontid species examined displayed distinctive in-air parachute postures after 45–100% of descending jumps, with Aneides showing the highest frequency of this behavior.

Representation of Threatened Biodiversity in Protected Areas and Identification of Complementary Areas for Their Conservation: Plethodontid Salamanders in Mexico

Protected areas (PAs) have been the most important conservation instrument worldwide and are reaching the coverage percentage suggested internationally (17%), but with the risk of not being ecologically representative, which is particularly concerning for threatened species. Using a database of records from museums, literature, and our fieldwork, we evaluated the representation of 132 plethodontid salamander species, a highly threatened group, in the PAs of Mexico. We assessed the importance of PAs, according to the type of governance, to represent the salamander species diversity, estimating the proportion of suitable habitat within PAs where salamanders occur and detecting potential areas to protect threatened species that are outside of PAs. Approximately 40% of plethodontid species, including threatened species, have not been recorded in PAs. A set of federal PAs harbor the greatest number of species, while state, community, and private PAs have different species composition and a high complementariness to federal areas. In 82% of PAs with plethodontid records, suitable habitat covers more than half of their extent. To protect the 36 threatened plethodontid species that have not been recorded in any PA, we detected 26 potential sites, as well as 12 close and suitable established PAs, to complement the protection of threatened species. Different types of governance of PAs are highly complementary to protect threatened species, but not all PAs seem to have the proper conditions for their survival.

Effect of chronic low body temperature on feeding and gut passage in a plethodontid salamander

Although feeding in some plethodontid salamander species, such as Dusky Salamanders (Desmognathus, family Plethodontidae), occurs at short-term (acute) low temperature below 5°C, it is unknown whether feeding, digestion, and gut passage continue to occur during periods of long-term (chronic) low temperature. We performed a controlled laboratory experiment to examine the effect of several chronic low environmental temperatures on both feeding and gut passage in semiaquatic Spotted Dusky Salamanders (D. conanti). We quantified salamander feeding and defecation for different experimental groups maintained for many weeks at a constant temperature of 4, 7, 10, or 13°C. Although feeding frequency, number of prey items consumed per feeding, and defecation frequency were significantly less for individuals at 4°C than for individuals at 10 or 13°C, salamanders continued to feed, defecate, and maintain body mass for 12 weeks at 4°C. The ratio of the number of fecal pellets produced to the number of prey items consumed each week by individuals did not significantly decrease at 4°C, which indicates gut passage was sustained at this temperature. Because both time between feeding and time between defecation were similarly affected by prolonged low temperature, the significant decrease in feeding frequency at 4°C may depend, in part, on a decrease in digestive function and an extended time for gut passage at low temperature. We conclude that most individuals of D. conanti can feed, digest, and maintain body mass for several months at constant low temperature down to 4°C. Our results support a growing body of data that indicate some plethodontid salamanders may acquire energy at environmental temperatures only a few degrees above freezing.

Life in the Slow Lane: Stress Responses in Plethodontid Salamanders

Abstract Plethodontid salamanders are specialized for a low-energy lifestyle, offering an interesting model for studying vertebrate stress responses. Furthermore, in an increasingly changing environment, it is important to understand how plethodontid salamanders respond to a variety of different stressors. Here, I review findings from my research group on the impact of various stressors on behavior and physiology in three species of plethodontid salamanders. A robust response to putative stressors was a decrease in locomotory activity, which was found after exposure to handling, predator kairomones, and acidic environments. The change in locomotory activity was not related to changes in corticosterone (CORT), a glucocorticoid hormone (GC) considered to be a hallmark of the vertebrate stress response. The uncoupling of CORT from stress-induced behavior might relate to the fact that decreased locomotory activity is not energetically costly, while CORT is a metabolic hormone that functions to mobilize glucos...

What Drives Variation in Plethodontid Salamander Species Richness over Space and Time?

Plethodontid salamanders have become model organisms for studying many fundamental questions in evolutionary biology, ecology, and behavior. Dozens of studies focused on geographic patterns of phenotypic and genetic variation have been conducted on plethodontids, such that we now have a deep understanding of how many species are in the family and where they occur. This body of work on patterns of speciation has been foundational to exploring the drivers of the major patterns of species richness in the family. Approximately 70% of the world's 696 extant species of salamanders are plethodontids. The distribution of plethodontid species diversity exhibits striking variation globally. Most plethodontids are concentrated into two hotspots of diversity, the Appalachian Highlands and the Mesoamerican Highlands. Moreover, within these montane centers of diversity more species are found in midelevation habitats than at the highest or lowest elevations. The clade has been highly successful in the New World tropics, which harbors more plethodontid species than the temperate zone. Here, I review new insights on the evolutionary and ecological causes of variation in plethodontid species richness over geographic space and evolutionary time. New hypotheses on the phylogenetic relationships of plethodonids and tools from comparative phylogenetics and biodiversity informatics have been critical to this recent progress. Threats to plethodontid diversity arising from global climate change are examined, as is the need to further study and to cross-validate forecasts of species' range dynamics with different modeling approaches and independent data.

A new species of Isthmura (Caudata: Plethodontidae) from the montane cloud forest of central Veracruz, Mexico.

We describe a new plethodontid salamander species of the genus Isthmura, known only from one locality in the mountainous region of central Veracruz, Mexico. Like its congeners, Isthmura corrugata sp. nov. has a large and robust body, but it is easily distinguished from the other species in the genus by the absence of any spot or mark on the dorsum (except by dull reddish brown coloration on eyelids) and by extremely well-marked costal grooves separated by very pronounced costal folds. Based on an mtDNA phylogeny, the new species is most closely related to the geographically distant I. boneti and I. maxima but occurs very near I. naucampatepetl and I. gigantea on the eastern slope of Cofre de Perote, Veracruz. The region where I. corrugata occurs contains a high number of plethodontid salamander species and is threatened by human activity.

Doing Without: Jump Performance After Tail Autotomy in Three Species of Plethodontid Salamanders

Abstract:  The ability of plethodontid salamanders to jump has been recognized for over 100 yr, but the mechanics of the jump are only now being elucidated. These salamanders often autotomize tails that can be as much as a third of the body mass. Tail loss alters jump performance in some lizards and therefore may also alter jump performance in the plethodontid salamanders. In this study, we used a high-speed camera to record subjects representing three species of plethodontid salamanders jumping with and without tails. The kinematic analyses indicate that take-off velocity, take-off angle, and maximum height are similar between salamanders with and without tails. Jump characteristics are highly variable within the individual for all salamanders (with or without tails) and this indicates that salamanders do not need to produce the same jump consistently to succeed in their primary task of escape. Better coordination might exist for arboreal plethodontid salamanders that use jumping for purposes other than ...

Movements of vastly different performance have similar underlying muscle physiology.

Many animals use elastic recoil mechanisms to power extreme movements, achieving levels of performance that would not be possible using muscle power alone. Contractile performance of vertebrate muscle depends strongly on temperature, but the release of energy from elastic structures is far less thermally dependent, thus elastic recoil confers thermal robustness to whole-animal performance. Here we explore the role that muscle contractile properties play in the differences in performance and thermal robustness between elastic and non-elastic systems by examining muscle from two species of plethodontid salamanders that use elastically powered tongue projection to capture prey and one that uses non-elastic tongue projection. In species with elastic mechanisms, tongue projection is characterized by higher mechanical power output and thermal robustness compared with tongue projection of closely related genera with non-elastic mechanisms. In vitro and in situ muscle experiments reveal that species differ in their muscle contractile properties, but these patterns do not predict the performance differences between elastic and non-elastic tongue projection. Overall, salamander tongue muscles are similar to other vertebrate muscles in contractile performance and thermal sensitivity. We conclude that changes in the tongue-projection mechanism, specifically the elaboration of elastic structures, are responsible for high performance and thermal robustness in species with elastic tongue projection. This suggests that the evolution of high-performance and thermally robust elastic recoil mechanisms can occur via relatively simple changes to morphology, while muscle contractile properties remain relatively unchanged.

Extreme Performance and Functional Robustness of Movement are Linked to Muscle Architecture: Comparing Elastic and Nonelastic Feeding Movements in Salamanders

Muscle-powered movements are limited by the contractile properties of muscles and are sensitive to temperature changes. Elastic-recoil mechanisms can both increase performance and mitigate the effects of temperature on performance. Here, we compare feeding movements in two species of plethodontid salamanders, Bolitoglossa franklini and Desmognathus quadramaculatus, across a range of body temperatures (5-25°C) to better understand the mechanism of elastically powered, thermally robust movements. Bolitoglossa exhibited ballistic, elastically powered tongue projection with a maximum muscle mass specific power of 4,642 W kg(-1) while Desmognathus demonstrated nonballistic, muscle-powered tongue projection with a maximum power of 359 W kg(-1) . Tongue-projection performance in Bolitoglossa was more thermally robust than that of Desmognathus, especially below 15°C. The improved performance and thermal robustness of Bolitoglossa was associated with morphological changes in the projector muscle, including elaborated collagen aponeuroses and the absence of myofibers attaching directly to the tongue skeleton. The elongated aponeuroses likely increase the capacity for elastic energy storage, and the lack of myofibers inserting on the tongue skeleton permits ballistic projection. These results suggest that relatively simple changes in myofiber architecture and the amount of connective tissue can improve the performance and functional robustness of movements in the face of environmental challenges such as variable temperature.