Phaeognathus Research Articles

No remnants of nasolacrimal ducts in any Desmognathini salamanders indicates loss early in their evolutionary history

Abstract Previous studies demonstrated that nasolacrimal ducts were present in the ancestral plethodontid lineage. Two lineages within Plethodontidae contain individuals that do not possess nasolacrimal ducts: Desmognathus and Eurycea. Earlier works examined only two species of Desmognathus, D. fuscus and D. monticola. We obtained every Desmognathini (Phaeognathus + Desmognathus) species possible from novel collections and museum collections and assessed presence or absence of nasolacrimal ducts using contrast-enhanced computed tomography and routine histological procedures. The goal was to test the hypothesis that nasolacrimal ducts were lost on the evolutionary branch leading to Desmognathus. We rejected our hypothesis by finding that nasolacrimal ducts were absent in all Desmognathus that we examined and Phaeognathus hubrichti; thus, we recovered the absence of nasolacrimal ducts on the evolutionary branch leading to Desmognathini.

Decision analysis for habitat conservation of an endangered, range‐limited salamander

AbstractMany species of conservation concern are habitat limited and often a major focus of management for these species is habitat acquisition and/or restoration. Deciding the location of habitat restoration or acquisition to best benefit a protected species can be a complicated subject with competing management objectives, ecological uncertainties and stochasticity. Structured decision making (SDM) could be a useful approach for explicitly incorporating those complexities while still working toward species conservation and/or recovery. We applied an SDM approach to Red Hills salamander Phaeognathus hubrichti habitat conservation decision making. Phaeognathus hubrichti is a severely range‐limited endemic species in south central Alabama and has highly specific habitat requirements. Many known populations live on private lands and the primary mode of habitat protection is habitat conservation planning, but such plans are non‐binding and not permanent. Working with stakeholders, we developed an objectives hierarchy linking land acquisition or protection actions to fundamental objectives. We built a model to assess and compare the quality of the habitat in the known range of P. hubrichti. Our model evaluated key habitat attributes of 5814 pixels of 1 km2 each and ranked the pixels from best to worst with respect to P. hubrichti habitat requirements. Our results are a spatially explicit valuation of each pixel, with respect to its probable benefit to P. hubrichti populations. The results of this effort will be used to rank pixels from most to least beneficial, then identify land owners in the most useful areas for salamanders who are willing to sell or enter into a permanent easement agreement.

Effects of Buffering Key Habitat for Terrestrial Salamanders: Implications for the Management of the Federally Threatened Red Hills Salamander (Phaeognathus hubrichti) and Other Imperiled Plethodontids

Forestry practices are placing ever increasing emphasis on sustainability and the maintenance of ecological processes, biodiversity, and endangered species or populations. Balancing timber harvest and the management of imperiled species presents a particularly difficult challenge during this shift, as we often know very little about these species’ natural history and how and why silviculture practices affect their populations. Accordingly, investigation of and improvement on current management practices for threatened species is imperative. We investigated the effectiveness of habitat buffers as a management technique for the imperiled Red Hills salamander (Phaeognathus hubrichti) by combining genetic, transect, and body-condition data. We found that populations where habitat buffers have been employed have higher genetic diversity and higher population densities, and individuals have better overall body condition. These results indicate that buffering the habitat of imperiled species can be an effective management tool for terrestrial salamanders. Additionally, they provide further evidence that leaving the habitat of imperiled salamanders unbuffered can have both immediate and long-term negative impacts on populations.

Informing management of endemic habitat specialists: Multiscale habitat selection by the Red Hills salamander

Rare species with highly specific habitat requirements present challenges for land managers. The primarily fossorial Red Hills salamander (Phaeognathus hubrichti) is endemic to a small area in south-central Alabama and restricted to a unique coastal plain slope and ravine habitat. Both the current distribution and population demography of the species are thought to be influenced by past and current land use. We quantified habitat use and selection of P. hubrichti at 6 scales: 3 of which were designed to identify habitat attributes at the landscape scale, the remaining were designed to identify habitat attributes at the microhabitat scale. We documented habitat selection at all 6 spatial scales. Because the data best explained habitat selection at the smallest spatial scale that we evaluated, we advocate for an approach to P. hubrichti habitat management and restoration that begins at a fine spatial scale but incorporates management goals at multiple and larger scales. The framework we use for quantifying habitat selection of P. hubrichti may be useful for other rare species with narrow ranges and specific habitat requirements. © 2014 The Wildlife Society.

Tail Length and Sexual Size Dimorphism (SSD) in Desmognathan Salamanders

Tails serve multiple functions in salamanders: energy storage, courtship, antipredator defense, and respiration. Differences in life history strategies between males and females may generate sexual size dimorphism (SSD) in tail length. However, the contribution of tail length to SSD is relatively unstudied. Because the basal member of the desmognathan salamander Phaeognathus hubrichti shows SSD in tail dimensions (females have long, thin tails compared to the shorter, thicker tails of males), we hypothesized that other desmognathans may follow the same pattern. We took standard morphological measurements, aged, and sexed 342 Desmognathus quadramaculatus (the largest species of Desmognathus) and 244 Desmognathus aeneus (one of the smallest species) to determine whether SSD in tail length followed the same pattern as in P. hubrichti. Neither Desmognathus species showed SSD in tail length and the trends were in opposite directions. Males of both species had significantly wider tail diameters than the females. Females had a significantly longer distance between limbs than did males. We also found that all three species differ in resource allocation to different body parts as they mature. This suggests that life history traits, and behavioral and ecological requirements, have a stronger influence on body size than does phylogeny in this group of salamanders.

Population structure and gene flow in a heavily disturbed habitat: implications for the management of the imperilled Red Hills salamander (Phaeognathus hubrichti)

Estimating levels of gene flow and assessing levels of population connectivity are of critical importance to the field of conservation genetics, especially for imperiled species. Many factors can influence dispersal and therefore gene-flow patterns across a natural landscape. These patterns can be substantially altered by the impacts of habitat modification by humans or natural phenomena. Landscape-genetic studies that address both historical and contemporary influences on gene flow can be critical to demonstrating whether isolated populations with low levels of genetic variation are typical of the species or a result of strong negative effects of such modification. We used 10 microsatellite markers to investigate the spatial genetic patterns of the Red Hills salamander (Phaeognathus hubrichti), a federally listed species. Bayesian clustering revealed five well-supported demes within the range of P. hubrichti. Gene-flow analysis suggested that overall migration levels for P. hubrichti are low, but coalescent methods indicate that migration levels were significantly higher before habitat modification by humans. By accounting for history and species characteristics, our results suggest that loss and fragmentation of habitat have strongly negatively affected P. hubrichti by reducing migration, increasing bottlenecks, and promoting high levels of inbreeding.

Development and characterization of twelve polymorphic microsatellite loci in the threatened Red Hills salamander, Phaeognathus hubrichti

We isolated and characterized 12 microsatellite loci from the endangered Red Hills salamander, Phaeognathus hubrichti. Loci were screened in 24 individuals of P. hubrichti. The number of alleles per locus ranged from 2 to 16, observed heterozygosity ranged from 0.130 to 0.750, and the probability of identity values ranged from 0.012 to 0.778. These new loci provide tools for examining the population genetics of this federally threatened salamander.

Antipredator Behaviors of the Red Hills Salamander, Phaeognathus hubrichti

The antipredator behaviors of Phaeognathus hubrichti (Red Hills Salamander), a large fossorial plethodontid, and the basal member of the desmognathine salamanders, are unknown. The responses of P. hubrichti to tongue-flicks from hand-held snakes, tapping with a rod and pinching with a forceps were recorded with a videocamera. When contacted by a snake tongue- flick, P. hubrichti exhibited several antipredator behaviors including immobility, gape, walk, run, head flatten, head elevation, flip, bite, and flinch. One other antipredator behavior—writhe—was observed in the field. The antipredator be- haviors of P. hubrichti are more similar to those species in its sister taxon, Desmognathus, than to those of other less closely related fossorial salamanders. Gape, a threat display, is nearly identical to that of Desmognathus quadramaculatus. Gape, bite, and writhe are proposed to be ancestral behaviors in this group.

Sexual Size Dimorphism in the Red Hills Salamander, Phaeognathus hubrichti (Caudata: Plethodontidae: Desmognathinae)

Body size is an important variable used in life-history and sexual selection theory to predict reproductive, behavioral, and ecological traits. Except for the presence of special skin glands in males, sexual dimorphism has not been reported in the Red Hills Salamander (Phaeognathus hubrichti), the basal member of the Desmognathinae. These data provide insight into the evolution of SSD (sexual size dimorphism) in the entire subfamily. We conducted multivariate and univariate tests on eight morphological measurements of 92 preserved P. hubrichti. We also examined specimens for broken tails and U-shaped scars, which may indicate bites from conspecifics. Male salamanders were larger than females in all measurements except tail length and had more scars than either females or juveniles. This species exhibited male-biased SSD in shape and size: males were broad and bulky, females were long and thin. Regression analysis showed differences in resource allocation between male and female salamanders. Differences in life-history strategies and sexual selection in the form of male-male combat may explain these differences in body size.

Notes on the Reproductive Biology of the Alabama Red Hills Salamander (Phaeognathus hubrichti )

Living Amphibia exhibit two major life history modes, possession of an aquatic larval stage or direct development, with the latter assumed to be the derived evolutionary condition (Duellman and Trueb 1986, Wake 1989). A small group (n = 20 species) of plethodontid salamanders, the subfamily Desmognathinae, is of great interest because its members display both developmental modes (Marks 1995). For decades the prevailing phylogenetic hypothesis for the group, based upon morphology and habitat, was a monophyletic sequence from the larger, more aquatic species that possessed the longest larval lives to two dwarf terrestrial species with direct development Dunn (1926). This “aquatic to terrestrial” hypothesis remained unchallenged even with the discovery of a new, giant, fossorial species, the Alabama Red Hills Salamander (Phaeognathus hubrichti), that was thought to be a third species with direct development (Highton 1961).Recently, analysis of mtDNA sequences revealed that the terrestrial desmognathines form the three deepest branches in desmognathine phylogeny, compelling the authors to advance an alternative phylogenetic hypothesis that absence of an aquatic larval stage may be ancestral for desmognathines (Titus and Larsen 1996). Their hypothesis rested, however, on details of the developing embryo and hatchlings in the three species with direct development, but critical data on the eggs, hatchlings, and whether larvae exist in P. hubrichti are unavailable.Aspects of the reproductive biology of the rare and secretive Phaeognathus hubrichti are difficult to observe in the field because the species is a burrower. One clutch laid by a female kept in captivity for six years apparently was unfertilized because the eggs failed to develop (Brandon and Moruska 1982). The large size and small number of ripe ovarian oocytes observed in preserved specimens, coupled with the unusual terrestrial burrowing behavior of the species, suggest the absence of an aquatic larval stage (Brandon 1965).On several visits to one ravine in Butler Co., Alabama (31°32’N, 86°45’W) during the spring and summer of 2002, I repeatedly observed a 105 mm SVL gravid female, discovered her eggs, kept them in captivity until they hatched, then returned the female and her clutch alive back into the field. Here I describe the field observations, eggs, embryos, and hatchlings.

Activity Patterns of Red Hills Salamanders (Phaeognathus hubrichti) at Their Burrow Entrances

The Red Hills salamander (Phaeognathus hubrichti), a large fossorial plethodontid endemic to south-central Alabama, was listed as federally threatened in 1976. To determine the seasonal and daily activity patterns of this species, I counted the number of salamanders present at burrow entrances, recorded the amount of time individual salamanders spent at entrances, and measured five abiotic variables to determine how they correlated with the number of salamanders at burrow entrances. Red Hills salamanders were present at burrow entrances all months of the year, displayed a unimodal daily activity pattern, and spent a mean of 12.3 continuous hours at an entrance each day. Regardless of season, time spent at an entrance remained relatively constant. Air temperature had the highest correlation with the number of salamanders present at entrances. Burrow entrances play a prominent role in the lives of these salamanders. When estimating population size for conservation efforts, surveys should be conducted at night and at multiple times and dates during the warmer months of the year because not all salamanders are present at entrances at any one time.

Diet of the Red Hills Salamander Phaeognathus hubrichti

brichti) is a unique species found only in the Red Hills physiographic region of southern Alabama (Schwaner and Mount, 1970). Red Hills salamanders inhabit burrow systems on steep, moist, hardwood-dominated slopes shaded by a full canopy (Dodd, 1991). Information on life-history characteristics, including foraging behavior, of P hubrichti is limited due to their fossorial habits. Red Hills salamanders may feed on prey items found within their burrows and on prey captured on the surface. During burrow excavations, Jordan (1975) found numerous invertebrates that could serve as prey for the Red Hills salamander, including camel crickets, millipedes, spiders, and snails. Red Hills salamanders often sit at the entrance to

Longevity and Abandonment of Burrows Used by the Red Hills Salamander (Phaeognathus hubrichti)

Longevity and Abandonment of Burrows Used by the Red Hills Salamander (Phaeognathus hubrichti)

Molecular Phylogenetics of Desmognathine Salamanders (Caudata: Plethodontidae): A Reevaluation of Evolution in Ecology, Life History, and Morphology

1 - 2 4 Abstract.—Phylogenetic relationships were reconstructed for salamanders of the plethodontid sub- family Desmognathinae to examine evolution of morphology, ecology, and life history. Mitochon- drial DNA sequences encoding 12S and 16S ribosomal RNA and the valine transfer RNA provided 259 phylogenetically informative sites from approximately 1,200 nucleotide positions for 21 spec- imens representing 15 species and subspecies. These data were analyzed in conjunction with 13 morphological and reproductive characters to generate phylogenetic hypotheses. The directly de- veloping terrestrial desmognathines Phaeognathus hubrichti and Desmognathus wrighti represent, respectively, the first and second phylogenetic branching events within the subfamily, and the remaining terrestrial lineage, D. aeneus, also branches near the base of the phylogenetic tree. These results challenge earlier hypotheses that within Desmognathus the small nonmetamorphosing spe- cies, D. aeneus and D. wrighti, represent the end of a graded phylogenetic decrease in size and decrease in use of aquatic habitats. In contrast to previous hypotheses, our results suggest that desmognathine evolution includes transformations in the direction of larger body sizes, lengthened larval periods, and greater use of aquatic habitats. (Desmognathinae; ecology; life history; mito- chondrial DNA; molecular phylogenetics; ribosomal DNA; salamanders.)

The status of the Red Hills salamander Phaeognathus hubrichti, Alabama, USA, 1976–1988

A total of 144 sites in the Red Hills Physiographic Province in south-central Alabama, USA, were surveyed in 1988 for burrows of the Red Hills salamander Phaeognathus hubrichti. Of 92 sites surveyed in 1976, no change occurred in the habitat at 54 sites, conditions improved at 19 sites and deteriorated at 18 sites following selective or clear cutting. An additional 14 of 52 sites not surveyed in 1976 were adversely affected by logging. Burrows were most often found on high (x̄ = 17 m), steep (x̄ = 50°), uncut slopes containing a high soil moisture content (x̄ = 57%) and full tree canopy. Slope angle and soil pH did not affect burrow abundance. Burrow openings averaged 10·9 mm high × 15·3 mm wide. Burrow angle was negatively correlated with burrow width and slope angle but low r2 values indicate that little of the variation was explained by these variables. Burrows were most often found on the upper two-thirds of slopes; burrows on slopes affected by cutting were found in the middle of the slope where they were less prone to disturbance and desiccation. Although most timber companies claim to no longer cut steep slopes in order to protect salamanders, detrimental forestry practices are still occuring. In some instances, Red Hills salamanders survive selective and clear cutting, but the persistence and viability of affected populations remain unknown. Suggestions are made to reduce impacts from forestry operations. Acquisition of 25 sites containing viable salamander populations and retention as a threatened species under United States federal law are recommended.

Notes on the Distribution, Habits, and Ecology of the Salamander Phaeognathus hubrichti Highton

Notes on the Distribution, Habits, and Ecology of the Salamander Phaeognathus hubrichti Highton

Morphological Variation and Ecology of the Salamander Phaeognathus hubrichti

A new locality for the species in Conecuh County, Alabama, is recorded. Specimens collected ranged from 31 to 120 mm snout to vent. Sexual maturity apparently occurs at about 100 mm body length in females, and near 80 mm in males. Mature males have no melanophores on the testis and no mental gland. Number of lobes of testes increases with increasing body length. The presence of a few large ovarian ova in 2 females suggests that there is probably no free-living, aquatic larva. Phaeognathus hubrichti seems able to start its own burrows only in loosely packed soil, but can enlarge and use previously formed cavities and tunnels. Gut contents of P. hubrichti and Plethodon glutinosus are similar, and differ from those of Desmognathus monticola. P. hubrichti feeds at the burrow entrance on surface-dwelling food. All specimens of P. hubrichti examined were infested with intestinal flukes and colic roundworms.

The Middle Ear of Holbrookia maculata maculata, the Northern Earless Lizard

A plethodontid salamander from Butler County, Alabama, represents a new genus and species, described herein as Phaeognathus hubrichti. The new genus is related to Desmognathus and Leurognathus, which it resembles in possessing similar head musculature, stalked occipital condyles, and probably also opisthocoelous vertebrae. It differs from the other two genera of the subfamily Desmognathinae in possessing seven more body vertebrae, reduced limbs and a greater size. Acknowledgements.-The writer wishes to thank Mr. Hubricht and Dr. Cochran for permission to describe this form and the National Science Foundation for financial support of this research. Mr. Robert Kanazawa kindly took the radiograph. Misses Anne Moskos and Hannah Segal made a special trip to the type locality in an unsuccessful attempt to obtain additional material. la a a is Des ognathus LITERATURE CITED