Glyptemys Insculpta Research Articles

Improving herpetological surveys in eastern North America using the environmental DNA method.

Among vertebrates, herpetofauna has the highest proportion of declining species. Detection of environmental DNA (eDNA) is a promising method towards significantly increasing large-scale herpetological conservation efforts. However, the integration of eDNA results within a management framework requires an evaluation of the efficiency of the method in large natural environments and the calibration of eDNA surveys with the quantitative monitoring tools currently used by conservation biologists. Towards this end, we first developed species-specific primers to detect the wood turtle (Glyptemys insculpta) a species at risk in Canada, by quantitative PCR (qPCR). The rate of eDNA detection obtained by qPCR was also compared to the relative abundance of this species in nine rivers obtained by standardized visual surveys in the Province of Québec (Canada). Second, we developed multi-species primers to detect North American amphibian and reptile species using eDNA metabarcoding analysis. An occurrence index based on the distribution range and habitat type was compared with the eDNA metabarcoding dataset from samples collected in seven lakes and five rivers. Our results empirically support the effectiveness of eDNA metabarcoding to characterize herpetological species distributions. Moreover, detection rates provided similar results to standardized visual surveys currently used to develop conservation strategies for the wood turtle. We conclude that eDNA detection rates may provide an effective semiquantitative survey tool, provided that assay calibration and standardization is performed.

Convergent Evolution Provides Evidence of Similar Radiations in Shell Shape in the Turtle Families Emydidae and Geoemydidae

Abstract: We investigated phenotypic diversification in the species-rich and ecologically diverse turtle families Emydidae and Geoemydidae. In particular, we were interested in whether these groups, with many ecologically and morphologically similar species, show similar patterns of evolutionary radiation. We focused on directions of evolution and evolutionary allometry; we also quantitatively investigated whether two supposed morphological analogs shared within the two groups (e.g., “Box Turtles” and “Wood Turtles”) show evidence of convergence. A set of 53 three-dimensional landmarks were digitized on 1029 turtle shells representing 50 emydid species and 62 geoemydid species. These data were analyzed using standard geometric morphometric techniques. Evolutionary patterns were assessed using tests for phylogenetic signal, and the relationship between size and shell shape was determined via phylogenetic regression. Tests for phylogenetic signal in shell shape and for allometry both yielded significant re...

Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles.

Most turtle species possess temperature-dependent sex determination (TSD), but genotypic sex determination (GSD) has evolved multiple times independently from the TSD ancestral condition. GSD in animals typically involves sex chromosomes, yet the sex chromosome system of only 9 out of 18 known GSD turtles has been characterized. Here, we combine comparative genome hybridization (CGH) and BAC clone fluorescent in situ hybridization (BAC FISH) to identify a macro-chromosome XX/XY system in the GSD wood turtle Glyptemys insculpta (GIN), the youngest known sex chromosomes in chelonians (8-20My old). Comparative analyses show that GIN-X/Y is homologous to chromosome 4 of Chrysemys picta (CPI) painted turtles, chromosome 5 of Gallus gallus chicken, and thus to the X/Y sex chromosomes of Siebenrockiella crassicollis black marsh turtles. We tentatively assign the gene content of the mapped BACs from CPI chromosome 4 (CPI-4) to GIN-X/Y. Chromosomal rearrangements were detected in G. insculpta sex chromosome pair that co-localize with the male-specific region of GIN-Y and encompass a gene involved in sexual development (Wt1-a putative master gene in TSD turtles). Such inversions may have mediated the divergence of G. insculpta sex chromosome pair and facilitated GSD evolution in this turtle. Our results illuminate the structure, origin, and evolution of sex chromosomes in G. insculpta and reveal the first case of convergent co-option of an autosomal pair as sex chromosomes within chelonians.

The Ecology of the Wood Turtle (Glyptemys insculpta) in the Eastern Panhandle of West Virginia

Glyptemys insculpta (Wood Turtle) is listed as imperiled in West Virginia and designated as endangered under the IUCN Red List. We studied a population of Wood Turtles in the Eastern Panhandle of West Virginia from May 2010 to July 2011. We captured 25 turtles at 2 sites: 12 males, 9 females, 3 juveniles, and 1 hatchling. We fitted 10 adults with radio transmitters, 9 of which also received temperature-data loggers. Our 249 total observations include the 10 initial captures of the equipped turtles with 218 subsequent radio locations, and 15 unequipped turtles that were captured, and then recaptured 6 times. Morphometrics of Wood Turtles at the study location were similar to those reported for another West Virginia population. The home range for both males and females was approximately 6 ha; there were no significant intersexual differences. Turtles entered hibernacula in late October when temperatures were approximately 10 °C and remained inactive until mid-March when temperatures were approximately 5 °C. Our study provides a baseline assessment of the Wood Turtle in an unstudied upper-elevation Eastern Panhandle location.

Three novel herpesviruses of endangered Clemmys and Glyptemys turtles.

The rich diversity of the world’s reptiles is at risk due to significant population declines of broad taxonomic and geographic scope. Significant factors attributed to these declines include habitat loss, pollution, unsustainable collection and infectious disease. To investigate the presence and significance of a potential pathogen on populations of critically endangered bog turtles (Glyptemys muhlenbergii) as well sympatric endangered wood (G. insculpta) and endangered spotted (Clemmys guttata) turtles in the northeastern United States, choanal and cloacal swabs collected from 230 turtles from 19 sites in 5 states were screened for herpesvirus by polymerase chain reaction. We found a high incidence of herpesvirus infection in bog turtles (51.5%; 105/204) and smaller numbers of positive wood (5) and spotted (1) turtles. Sequence and phylogenetic analysis revealed three previously uncharacterized alphaherpesviruses. Glyptemys herpesvirus 1 was the predominant herpesvirus detected and was found exclusively in bog turtles in all states sampled. Glyptemys herpesvirus 2 was found only in wood turtles. Emydid herpesvirus 2 was found in a small number of bog turtles and a single spotted turtle from one state. Based on these findings, Glyptemys herpesvirus 1 appears to be a common infection in the study population, whereas Glyptemys herpesvirus 2 and Emydid herpesvirus 2 were not as frequently detected. Emydid herpesvirus 2 was the only virus detected in more than one species. Herpesviruses are most often associated with subclinical or mild infections in their natural hosts, and no sampled turtles showed overt signs of disease at sampling. However, infection of host-adapted viruses in closely related species can result in significant disease. The pathogenic potential of these viruses, particularly Emydid herpesvirus 2, in sympatric chelonians warrants additional study in order to better understand the relationship of these viruses with their endangered hosts.

Draft Genome Sequence of Robinsoniella peoriensis Strain WTD, Isolated from the Fecal Material of a Wood Turtle.

Here, we report the draft genome of Robinsoniella peoriensis strain WTD, which was isolated from the fecal material of a wood turtle. The genome size was 7,391,415 bp with 41.1 mol% G+C.

A Mycoplasma species of Emydidae turtles in the northeastern USA.

Mycoplasma infections can cause significant morbidity and mortality in captive and wild chelonians. As part of a health assessment of endangered bog turtles (Glyptemys muhlenbergii) in the northeastern US, choanal and cloacal swabs from these and other sympatric species, including spotted turtles (Clemmys guttata), eastern box turtles (Terrapene carolina carolina), wood turtles (Glyptemys insculpta), and common snapping turtles (Chelydra serpentina) from 10 sampling sites in the states (US) of Delaware, New Jersey, and Pennsylvania, were tested by PCR for Mycoplasma. Of 108 turtles tested, 63 (58.3%) were PCR positive for Mycoplasma including 58 of 83 bog turtles (70%), three of three (100%) eastern box turtles, and two of 11 (18%) spotted turtles; all snapping turtles (n = 7) and wood turtles (n = 4) were negative. Sequence analysis of portions of the 16S-23S intergenic spacer region and the 16S ribosomal RNA gene revealed a single, unclassified species of Mycoplasma that has been previously reported in eastern box turtles, ornate box turtles (Terrapene ornata ornata), western pond turtles (Emys marmorata), and red-eared sliders (Trachemys scripta elegans). We document a high incidence of Mycoplasma, in the absence of clinical disease, in wild emydid turtles. These findings, along with wide distribution of the identified Mycoplasma sp. across a broad geographic region, suggest this bacterium is likely a commensal inhabitant of bog turtles, and possibly other species of emydid turtles, in the northeastern US.

Effects of body size, habitat selection and exposure on hatchling turtle survival

AbstractIteroparous species invest little energy into annual reproduction and tend to experience low and variable survivorship in young life stages. However, juveniles with traits that increase survival will have a fitness advantage over conspecifics, and usually bigger is better for juvenile vertebrates. Understanding behavioural and morphological characteristics that increase fitness is important for our understanding of the evolution of life‐history strategies. We outfitted naturally emerging hatchlings of two species of turtles (Blanding's turtles Emydoidea blandingii and wood turtles Glyptemys insculpta) with radio transmitters to test five hypotheses related to survival from nests to overwintering sites using logistic regression models. In contrast to the widely supported hypothesis that bigger is better for survival of juveniles, we found that smaller hatchlings of both species were more likely to survive from emergence to overwintering. In E. blandingii, hatchlings that emerged later in the year, which reduced exposure time to predators and environmental risks, and spent less time in upland open habitat, were also more likely to survive. Our results demonstrate that bigger is not always better in juvenile ectotherms. Assuming bigger is better without observations of survival can lead to erroneous conclusions related to fitness proxies and the ontogeny of body size in populations. The observed relationship between habitat selection and survival in E. blandingii indicates a direct link between behaviour (habitat selection) and fitness through mortality caused by predators and environmental stressors.

A 21-Year Study of Seasonal and Interspecific Variation of Hatchling Emergence in a Nearctic Freshwater Turtle Community: To Overwinter or Not To Overwinter?

Abstract: Hatchling emergence patterns were studied in a community of six species of freshwater turtles in Lancaster County, Pennsylvania, USA, including: Chelydra serpentina, Chrysemys picta, Clemmys guttata, Glyptemys insculpta, Glyptemys muhlenbergii, and Sternotherus odoratus. Data were collected every year from 1965–1985 on estimated date of emergence, carapace length, April–May precipitation, August–September precipitation, annual precipitation, and low temperature and occurrence of precipitation during the 24 h prior to the time of each hatchling detection (n = 806). Chelydra serpentina, Ch. picta, and Cl. guttata hatchlings have a facultative delayed emergence strategy. The other species (G. insculpta, G. muhlenbergii, and S. odoratus) appear to be obligate early emergers, with the exception of one hatchling G. muhlenbergii that delayed emergence. Early emergence occurred in some species every year. However, the majority of hatchlings delayed emergence until the year following oviposition, excep...

Survey methodology for the detection of Wood Turtles (<em>Glyptemys insculpta</em>)

Wood Turtles (Glyptemys insculpta) are difficult to survey because their use of aquatic and terrestrial environments varies spatio-temporally. Existing survey methodology is highly variable and typically involves searching for Wood Turtles within water and on land 0 to >20 m from the shoreline from spring to autumn. The mobility of Wood Turtles suggests that detection is likely influenced by distance surveyed from water and the amount of vegetation, which varies by season. To determine an ideal survey methodology for the Wood Turtle, we recorded distances from a waterway of 31 radio-tagged turtles at Canadian Forces Base, Gagetown, New Brunswick, in 2003 and 2004. Ordinal logistic regression was used to determine the probability of finding male or female Wood Turtles with increasing distance from water at different times of day or season. Sex and time of day were not significant factors in detecting Wood Turtles. Season was a significant factor, with highest probability (69%) of finding Wood Turtles at a distance of 0–10 m of a waterway up to July 1 (corresponding to pre-nesting and nesting periods), compared to probabilities of <10% for any 10-m distance between 10 m and 50 m from a waterway. After July 1, the highest detection probability (50%) was at distances greater than 50 m from a waterway. We recommend that Wood Turtle surveys for environmental impact assessments and population monitoring be conducted on warm days (i.e., 10–25°C) within 10 m of waterways up to July 1.

Impacts of Hydrologic Change on Sandbar Nesting Availability for Riverine Turtles in Eastern Minnesota, USA

There have been significant increases in stream flow in many rivers of the Upper Midwestern United States since 1980. Increased summer flows may negatively impact ecological processes, including aquatic organisms’ life cycles. The smooth softshell (Apalone mutica) and wood turtle (Glyptemys insculpta) are threatened by alteration of stream flow regime and other changes to river ecosystems in the Upper Midwest. We hypothesized that prolonged duration of high summer flows would reduce time available for nesting. We assessed hydrologic change using the Indicators of Hydrologic Alteration program and stream gauge data, characterized physical properties of sandbars, surveyed turtle nesting sites and assessed historical channel change using aerial photos in GIS on five Upper Midwest rivers. A river stage-sandbar area relationship was developed to determine the effect of prolonged summer flow duration on turtle nesting opportunity for the 1940–2009 time period. Suitable water levels have declined since 1980 in the agricultural watersheds of southern Minnesota likely delaying hatching and reducing survival, particularly for aquatic turtles such as A. mutica. In contrast to the agricultural watersheds, there was no significant change in the northern forested rivers’ stream flow and sandbar availability during the nesting season. Management to reduce summer stream flow in agricultural watersheds and protection of known nest sites could benefit threatened aquatic turtle populations.

Population Decline in a Long-Lived Species: The Wood Turtle in Michigan

Abstract: Populations of Wood Turtles, Glyptemys insculpta, have steadily decreased over the past 30 yr because of habitat destruction and degradation. We sampled Wood Turtles from three areas in Michigan, USA, to characterize populations, quantify demographic trends, and measure the effect of declining population size on genetic diversity. Wood Turtle samples (n = 68) were collected from three rivers in the Lower Peninsula of Michigan and analyzed at nine microsatellite loci. Bayesian clustering programs identified two populations that split the three sampling sites into North and South populations. In both populations, analysis of genealogies estimated r < 0, indicating population decline. However, no evidence of a bottleneck was detected (P = 0.30 North, P = 0.29 South), and little evidence of inbreeding was observed (average North FIS = 0.25, average South FIS = 0.23), relative to other Emydidae populations. The high genetic diversity observed in the North and South populations is likely due to immigr...

Widespread reproductive variation in North American turtles: temperature, egg size and optimality

Theory predicts the existence of an optimal offspring size that balances the trade-off between offspring fitness and offspring number. However, in wild populations of many species, egg size can still vary from year to year for unknown reasons. Here, we hypothesize that among-year variation in population mean egg size of freshwater turtles is partly a consequence of their gonadal sensitivity to seasonal temperatures, a physiological mechanism which principally functions to synchronize reproduction with a favorable time of year. As part of this process, among-year variation in seasonal temperatures modifies the extent of egg follicle development, and this may translate into variation in mean egg size among years (both at the individual and population level). To test this hypothesis, we applied an information-theoretic approach to model relationships between mean egg mass and the temperatures experienced during discrete periods of follicular development in wild populations of three turtle species (Chrysemys picta, Chelydra serpentina, Glyptemys insculpta) over 12 consecutive years. Because follicular development occurs in the fall for C. serpentina and G. insculpta, whereas it occurs both in the fall and spring for C. picta, we expected only fall temperatures would explain egg size variation in C. serpentina and G. insculpta, whereas both fall and spring temperatures would correlate with egg size variation in C. picta. These predictions were upheld. We then compared among-year variation in within-female egg and clutch sizes of each species in order to evaluate whether such variation might still be consistent with some tenets of optimal egg size theory. In all three species, we found that clutch sizes vary more than egg sizes in spite of temperature-induced egg size variation, and this pattern of relatively high clutch-size variation matches theoretical predictions. Future work should explore the roles of direct and indirect (i.e., nutritional) influences of temperature on egg size in natural settings.

Revealing a cryptic life-history stage: differences in habitat selection and survivorship between hatchlings of two turtle species at risk (Glyptemys insculpta and Emydoidea blandingii)

Context Turtles are one of the most imperilled taxonomic groups worldwide and information about population ecology is essential to species recovery. Although the spatial ecology and demography of adults of several turtle species have been well studied, little is known about early life stages. The small size, soft shell, and limited mobility of hatchling turtles may cause differences in survivorship and habitat selection compared with adults. Aims We tested the hypothesis that hatchling turtles select habitat as they move away from nests, so as to reduce the risk of predation and desiccation. Methods We examined survivorship, behaviour and habitat selection at two spatial scales in hatchling Blanding’s turtles (Emydoidea blandingii) and wood turtles (Glyptemys insculpta) in 2009 and 2010, using radio-telemetry in Algonquin Provincial Park, Ontario, Canada. In addition, temperatures of sites used by hatchlings during winter were compared with those at haphazard stations in various habitats. Key results The mortality rate was high, with 42% of E. blandingii and 11% of G. insculpta hatchlings surviving to winter; most mortality was caused by predation. Most behavioural observations for both species were of individuals hiding under cover. Both species showed evidence of macrohabitat and microhabitat selection as they dispersed from nests towards overwintering sites, and important variables in the models differed between species. Likewise, the adult stages of these two species differ in their macrohabitat specialisation. There was also evidence that hatchlings chose overwintering sites on the basis of temperature. Conclusions Despite significant differences in survivorship between hatchlings and adults, resource selection was similar between these two demographic stages, and conservation plans based on adult habitat use should simultaneously protect hatchlings. Implications Understanding habitat selection by juveniles is important for testing hypotheses about ontogenetic shifts in resource selection and for protecting habitat for species at risk.

Can Turtle Mortality be Reduced in Managed Fields?

Abstract Early-successional habitats, including agricultural fields, appear to provide important foraging and nesting resource areas for Glyptemys insculpta (Wood Turtle) and Terrapene Carolina Carolina (Eastern Box Turtle) in the northeastern US. Mowing and agricultural activities can elevate turtle mortality rates. We performed two experiments to evaluate the risk of turtle mortality associated with 1) style of mower, 2) mower blade height, and 3) tractor tires. Mower blade height did not affect mortality rates when set to ≤15 cm. Different types of mowers appear to exert differential effects on mortality, with sickle bar mowers resulting in 50% lower mortality rates than rotary mowers and other models. However, mortality due to crushing by tractor tires may be as high as 46%, independent of blade type and height.

Use of an Artificial Nesting Mound by Wood Turtles (Glyptemys insculpta): A Tool for Turtle Conservation

Abstract We constructed an artificial nesting mound for Glyptemys insculpta (Wood Turtle) in the Great Swamp National Wildlife Refuge, NL The original nesting site was impacted by development and invasive plants. The new nesting mound was constructed from similar soil and was 100 m distant from the original site. The new mound was 50 m from stream habitat and in an old field where it received full sun for the entire day. The mound was 18 m long, 8 m wide, and had a maximum height of 1.5 m, with gently sloping sides. We encountered nest-searching female Wood Turtles on the impacted site during late May to early June for four years, 2007–2010. We carefully hand-carried females to the new nesting area and allowed them to choose whether or not to nest on the mound. We protected all nests from predators. Seventeen of 18 nests that were deposited and left on the nesting mound produced live hatchlings. Six clutches had 100% hatching success, with only one failing completely. At least nine different female Wood T...

Competing generic concepts for Blanding’s, Pacific and European pond turtles (Emydoidea, Actinemys and Emys)—Which is best?

We review competing taxonomic classifications and hypotheses for the phylogeny of emydine turtles. The formerly recognized genus Clemmys sensu lato clearly is paraphyletic. Two of its former species, now Glyptemys insculpta and G. muhlenbergii, constitute a well-supported basal clade within the Emydinae. However, the phylogenetic position of the other two species traditionally placed in Clemmys remains controversial. Mitochondrial data suggest a clade embracing Actinemys (formerly Clemmys) marmorata, Emydoidea and Emys and as its sister either another clade (Clemmys guttata + Terrapene) or Terrapene alone. In contrast, nuclear genomic data yield conflicting results, depending on which genes are used. Either Clemmys guttata is revealed as sister to ((Emydoidea + Emys) + Actinemys) + Terrapene or Clemmys guttata is sister to Actinemys marmorata and these two species together are the sister group of (Emydoidea + Emys); Terrapene appears then as sister to (Actinemys marmorata + Clemmys guttata) + (Emydoidea + Emys). The contradictory branching patterns depending from the selected loci are suggestive of lineage sorting problems. Ignoring the unclear phylogenetic position of Actinemys marmorata, one recently proposed classification scheme placed Actinemys marmorata, Emydoidea blandingii, Emys orbicularis, and Emys trinacris in one genus (Emys), while another classification scheme treats Actinemys, Emydoidea, and Emys as distinct genera. The inclusion of Actinemys in the same taxon as Emydoidea + Emys is unacceptable under a phylogenetic classification framework because there is evidence for the non-monophyly of this clade. Moreover, Actinemys, Emydoidea, and Emys are morphologically highly distinct. Their morphological divergence exceeds by far the differences that typically occur among species of the same genus, so that a continued usage of the distinct genera Actinemys, Emydoidea and Emys is recommended.

Nematode Parasites of Five Species of Turtles from the Area de Conservación Guanacaste, Costa Rica, with Description of a New Species of Falcaustra

Abstract Twenty-three turtles representing 3 families (5 species)—Chelydridae: common snapping turtle, Chelydra serpentina; Emydidae: brown wood turtle, Rhinoclemmys annulata; painted wood turtle, Rhinoclemmys pulcherrima; Kinosternidae: white-lipped mud turtle, Kinosternon leucostomum; scorpion mud turtle, Kinosternon scorpioides—collected in the Area de Conservacion Guanacaste, Costa Rica, were subjected to postmortem examination. Gravid nematodes representing 10 species, 9 previously described—Atractis costaricaensis, Cosmocercoides variabilis, Dracunculus globocephalus, Falcaustra chelydrae, Falcaustra tikasinghi, Klossinemella caballeroi, Sauricola sauricola, Serpinema magathi, Spiroxys figueiredoi—were found. Eight new host records and 7 new locality records are reported. A new species of Falcaustra inhabiting Rhinoclemmys annulata is described; it is the only known member of the genus lacking a pseudosucker, but having a toothed chamber separating the vestibule and the pharynx. Only Falcaustra kins...

Conservation genetics of a peripherally isolated population of the wood turtle (Glyptemys insculpta) in Iowa

The North American wood turtle, Glyptemys insculpta, is a semi-aquatic species that is considered rare, threatened, or endangered over much of its range. In this study, a particularly vulnerable peripheral isolate population in Iowa has been monitored over a period of 7 years. Population census size, estimated from mark-recapture data, and age structure determined from morphology are compared with genetic variation assessed using microsatellites. For reference, the genetics and demographics of this peripheral isolate are compared to data from a more dense population nearer the core of the species range in West Virginia. Geneflow between the Iowa population and a nearby population in Minnesota also is assessed. Genetic data indicate that the Iowa population is isolated, unique, and diverse. Although the Iowa population has lower allelic richness, lower heterozygosity, and smaller genetic effective population size than does the West Virginia population, the difference is not dramatic despite its lower population size, position at the periphery of the species range, and biogeographic history. The Iowa population is not inbred, and there is no genetic signature of a recent population bottleneck. However, interpretations of recent population dynamics based on genetic data may be unduly encouraging in long-lived species such as G. insculpta. Field data suggest a nearly complete lack of recruitment in Iowa. A number of environmental and anthropogenic factors, including recent increases in summer flooding during egg incubation, may have a more negative impact on the Iowa population than on the West Virginia population.

Intra-specific niche partitioning obscures the importance of fine-scale habitat data in species distribution models

Geographic information systems (GIS) allow researchers to make cost-effective, spatially explicit predictions of species’ distributions across broad geographic areas. However, there has been little research on whether using fine-scale habitat data collected in the field could produce more robust models of species’ distributions. Here we used radio-telemetry data collected on a declining species, the North American wood turtle (Glyptemys insculpta), to test whether fine-scale habitat variables were better predictors of occurrence than land-cover and topography variables measured in a GIS. Patterns of male and female occurrence were similar in the spring; however, females used a much wider array of land-cover types and topographic positions in the summer and early fall, making it difficult for GIS-based models to accurately predict female occurrence at this time of year. Males on the other hand consistently selected flat, low-elevation, riparian areas throughout the year, and this consistency in turn led to the development of a strong GIS-based model. These results demonstrate the importance of taking a more sex-specific and temporally dynamic view of the environmental niche.