Chelydra Serpentina Research Articles

TURTLE ASSEMBLAGE IN A HIGHLY ALTERED SPRING SYSTEM: COMAL SPRINGS, TEXAS

Comal Springs in New Braunfels, Texas, is the largest freshwater spring west of the Mississippi. The spring is within the Edwards Plateau Savanna Ecoregion of the Southeastern United States Turtle Priority Area. Comal Springs is an environmentally sensitive spring run situated in an urbanized area visited by >1,000,000 people each year and thus may be impacted by recreational use. We assessed baseline population levels for the turtle assemblage residing in Comal Springs. We captured 4,238 turtles from February 2012 to February 2015 across 12 separate sampling sessions. Captures and individually marked turtles (in parentheses) included 2,322 (1,715) Sternotherus odoratus, 1,558 (793) Pseudemys texana, 329 (141) Trachemys scripta, and 29 (19) Chelydra serpentina serpentina. We report population densities of 1,690/ha (S. odoratus), 230/ha (P. texana), 43/ha (T. scripta), and 5/ha (C. s. serpentina). We estimated biomass for each species and sex, resulting in a total biomass estimate of 5,309.6 kg or 632.1 kg/ha. Sex ratios for P. texana and T. scripta were 1:1, whereas the sex ratio for S. odoratus was 2.26:1, male biased. Our results suggest that a robust turtle assemblage inhabits Comal Springs, similar in richness to the more well-studied freshwater spring habitats in Florida. Future studies or management actions can use our data as a benchmark as the results of few turtle surveys in Texas have been published.

Incubation temperature and satiety influence general locomotor and exploratory behaviors in the common snapping turtle (Chelydra serpentina)

Temperature during embryogenesis determines sex and has been shown to influence other physiological traits in reptiles. The common snapping turtle (Chelydra serpentina) is an ideal model for testing how temperature impacts behavior in species that display temperature-dependent sex determination. Behavioral assays are crucial to understanding how a changing climate may affect whole organism function in the snapping turtle. Currently, there are few behavioral assays for semi-aquatic vertebrates like turtles. In this study, we used digital cameras to record behavior of fed and fasted hatchling turtles from different incubation temperatures in an open field setting for 20 min in 2018 and repeated the experiment in 2019. Open fields were circular tanks filled with water to a depth of 3.5 cm. Each field was split into four quadrants and two zones (inner and outer). The amount of time turtles spent actively moving, total distance travelled, and several other measures were collected and summarized automatically from videos with open source image analysis software (ImageJ). Satiety and incubation temperature had significant effects on total distance moved, time spent moving, and time moving in the outer zone. These findings indicate that temperature during embryogenesis has a long-lasting effect on neural mechanisms underlying exploratory or general locomotor behavior in turtles.

The Effects of Common Snapping Turtles on a Freshwater Food Web

While organisms are typically considered permanent residents of a community, many transient organisms occupy a community for only brief periods. Despite the duration, the effects of a short visit by a top predator may remain long after departure. To test hypotheses on the impacts of a short-term visit by a top predator on pond communities, we used artificial ponds and constructed food web treatments that varied in trophic structure (Control Food Web = no predators present, Bluegill Food Web = only intermediate predators present, and Full Food Web = top and intermediate predators present). The constructed food webs were replicated five times and contained two prey species (frog tadpoles), an intermediate predator (fish), and one top predator (freshwater turtle). The Full Food Web simulated a four-day visit by Chelydra serpentina (Common Snapping Turtle). Predation by Lepomis macrochirus (Bluegill) reduced mean tadpole survival for Hyla chrysoscelis (Cope's Gray Tree Frog) in all food webs, including the Full Food Web with C. serpentina, compared to the Control Food Web. Although C. serpentina had no effects on tadpoles of H. chrysoscelis, the top predator reduced mean survival and increased mean mass of Rana sphenocephala (Southern Leopard Frog) when compared to the Bluegill Food Web. Therefore, our results suggest that brief visits from transient organisms, especially top predators, can alter community structure and initiate cascading effects.

Abnormal persistence of the chorioallantoic membrane is associated with severe developmental abnormalities in freshwater turtles

Development in oviparous reptiles requires the correct formation and function of extra-embryonic membranes in the egg. In 2017, we incubated 2583 eggs from five species of freshwater turtle during a long-term ecological study and opened eggs that failed to hatch. We described a previously unreported developmental anomaly: the retention of an extra-embryonic membrane around 7 turtles (1 Spiny Softshell Turtle (Apalone spinifera (Le Sueur, 1827)), 1 Snapping Turtle (Chelydra serpentina (Linnaeus, 1758)), and 5 Northern Map Turtles (Graptemys geographica (Le Sueur, 1817))) that were alive but unhatched >14 days after their clutch mates had emerged. We investigated the association between retention of this membrane and the exhibition of other developmental deformities of varying severity, and we tested whether this novel abnormality was associated with reduced fertility or hatching success in affected clutches. Consultation of ∼150 years of literature suggests that we observed persistence of the chorioallantoic membrane (CAM; also called the chorioallantois). Our data suggest that clutches where at least one turtle exhibits a persistent CAM may also exhibit slightly reduced fertility or hatch success in the rest of the clutch compared with conspecific clutches that do not contain this anomaly. Future research should investigate the factors predicting CAM retention and other developmental abnormalities.

Distribution and Diversity of Glossiphoniid Leeches on Three Common Species of Freshwater Turtles from Texas, U.S.A.

Spiny softshell turtles (Apalone spinifera), common snapping turtles (Chelydra serpentina), and red-eared sliders (Trachemys scripta elegans) were surveyed for leeches at 16 sites across Texas, U.S.A., from March to December of 2017. Five species of leeches were found (3 from 15 A. spinifera sampled, 4 from 9 C. serpentina sampled, and 3 from 55 T. scripta elegans), representing 3 new host records and 1 new locality record. Leech abundance was also compared to water parameters (ammonia, carbon dioxide, chloride, dissolved oxygen, hardness, nitrite, nitrate, pH, salinity, temperature, and turbidity) and qualitative environmental variables (vegetation, sediment, latitude, longitude, season, and water body) through principle components analysis, stepwise regression, and model selection. We found significant effects of sediment composition and seasonality on leech abundance. This study adds novel data on leech–host associations, distributions, and diversity in Texas.

New record of the non-native snapping turtle Chelydra serpentina (Linnaeus, 1758) in the wild of the Republic of Korea

New record of the non-native snapping turtle Chelydra serpentina (Linnaeus, 1758) in the wild of the Republic of Korea

First Evidence of Metabolic Heating in a Freshwater Turtle (Chelydra serpentina)

Abstract Metabolic heating caused by physiological processes during the development of oviparous embryos can raise nest temperatures above those of the surrounding substrate and may be sufficient t...

Decades of Road Mortality Cause Severe Decline in a Common Snapping Turtle (Chelydra serpentina) Population from an Urbanized Wetland

Road networks threaten biodiversity and particularly herpetofauna, including common snapping turtles (Chelydra serpentina), which have an especially slow life history that prevents rapid recovery of populations subjected to road mortality. Cootes Drive is a 2.5-km 4-lane highway that bisects wetland habitat used for nesting and overwintering by snapping turtles. We hypothesized that turtle mortality from collisions with vehicles on Cootes Drive has caused a male bias and a decline in the population as turtles attempt to access habitat on both sides of the road. Capture–mark–recapture studies confirmed a dramatic decline in the turtle population from 941 individuals in 1985 to 177 individuals in 2002, a loss of 764 individuals in only 17 yrs. Using the same data, we also determined that the population has been significantly male-biased since 1985. Using 2009–2016 road mortality data obtained from the Dundas Turtle Watch (a citizen-science program), we completed a population viability analysis using the 2002 population size estimate to isolate the impact of road mortality. We found that this population is at risk of extirpation due to road mortality. The population range overlapped with the Cootes Drive and 7 of the 10 tracked turtles had individual home ranges that overlapped with the road. Our findings support the hypothesis that road mortality has contributed to the dramatic decline in the snapping turtle population in Cootes Paradise Marsh. This population is in jeopardy of extirpation; therefore, exclusion fencing must be installed for an extended distance along both sides of surrounding roads to prevent turtles from crossing the road and to promote their use of existing aquatic culverts.

New size record for Snapping Turtle (<i>Chelydra serpentina</i>) in southern Quebec, Canada

We report a new size record for a Snapping Turtle (Chelydra serpentina) in Quebec, Canada. We captured an adult male in good general condition in the Rivière du Sud in the southern Montérégie region. Its straight midline carapace length was 43.2 cm (maximum carapace length 45.1 cm), and it weighed 19.8 kg. This record contributes to our understanding of the maximum size of this species at the northeastern part of its range. More intensive effort will be necessary to document the Snapping Turtle population structure in Quebec to allow for sound comparisons with other populations, as well as a better understanding of the effects of elevation, latitude, and local habitat on Snapping Turtle growth and size.

Different mechanisms of serum complement activation in the plasma of common (Chelydra serpentina) and alligator (Macrochelys temminckii) snapping turtles.

Reptiles are declining worldwide yet our understanding of their immune function lags far behind other taxa. The innate immune system is the primary mode of defense in reptiles, and the serum complement cascade is its major component. We assessed serum complement activity of plasma in two closely related aquatic turtle species, the common snapping turtle (CST; Chelydra serpentina) and alligator snapping turtle (AST; Macrochelys temminckii). We used a sheep red blood cell (SRBC) hemolysis assay to assess serum complement activity. Although the antibacterial activities of the plasma of these turtle species are similar, the hemolytic activity was much stronger in CST than AST. Treatment with inhibitors of the serum complement cascade indicated differences in the mechanisms of complement activation between the turtle species. We subjected plasma from both turtle species to mannan affinity chromatography and analyzed the eluate with SDS-PAGE, which revealed that plasma from the CSTs contained only small amounts of one C-type lectin protein while the AST plasma contained high concentrations of two C-type lectins (31.0 and 35.9 kDa). Edman degradation analyses confirmed that the two AST proteins contained identical N-terminal sequences. Thus, the CST appears to rely more heavily on the alternative mechanism of serum complement activation, while the AST appears to rely more on the lectin-mediated pathway, which is a pattern recognition response to prokaryotes not activated by the SRBCs. These results are unique in that the use of serum complement pathways are generally assumed to be conserved within clades.

How do embryonic turtles process yolk? Evidence from the Snapping Turtle,Chelydra serpentina(Chelydridae)

Compared with amphibians, oviparous reptiles and birds lay large eggs that contain abundant yolk. Because the yolk is extracellular, it must be taken up by cells of the yolk sac and metabolized so that products of yolk digestion can be transported to the embryo to fuel development. In birds, the yolk is processed by cells that line the inside of the yolk sac. A very different developmental pattern recently has been demonstrated in lizards and snakes in which the yolk sac cavity is converted to a compact mass of blood vessels lined by endodermal cells. In this study, we used scanning electron microscopy to determine which of these developmental patterns (if either) occurs in a representative chelonian, the North American Snapping Turtle (Chelydra serpentina (Linnaeus, 1758)). Our observations reveal that yolk-filled endodermal cells progressively fill the yolk sac cavity. These cells become organized around anastomosing blood vessels, forming elongated strands that are morphologically well suited for yolk digestion and vascular transport of nutrients. This developmental pattern shares features with that of squamates, but it differs markedly from that of birds. These observations indicate that mechanisms of yolk processing in lizards and snakes have an evolutionary history that pre-dates the squamate clade.

Role for androgens in determination of ovarian fate in the common snapping turtle, Chelydra serpentina

Sex steroids are involved in sex determination in almost all vertebrates, including species with temperature-dependent sex determination (TSD). It is well established that aromatase and estrogens are involved in ovary determination in TSD species. In contrast, the role of non-aromatizable androgens in TSD is less clear. In this study, we used dihydrotestosterone (DHT) and an antagonist of the mammalian androgen receptor (flutamide) to examine the impact of androgens on sex determination in the snapping turtle. We incubated eggs at a male-producing temperature and treated embryos with drug delivery vehicle (5 L ethanol), DHT in vehicle, or flutamide in vehicle during the sex-determining period. We then measured expression of markers for ovarian and testicular development and genes involved in steroidogenesis. A subset of embryos and hatchlings were collected for histological analysis of gonad differentiation and sex determination. DHT and flutamide both induced ovarian development: 100% of vehicle-treated hatchlings had testes, while 60% of DHT-treated and 32% flutamide-treated hatchlings had ovaries. DHT and flutamide treatments also had feminizing effects on gene expression patterns and the structure of embryonic gonads. DHT treatment increased expression of FoxL2, androgen receptor, aromatase and several steroidogenic genes. Flutamide produced a similar, but weaker, pattern of gene expression. Genes involved in testis development (Sox9 and Amh) were influenced by flutamide treatment. Our findings support the hypothesis that androgens and the androgen receptor are involved in ovary determination in the common snapping turtle.

Revisiting the hypothesis of sex-biased turtle road mortality

Road mortality poses a major threat to turtle populations. Several studies have suggested that the terrestrial movements associated with nesting increase this risk for females. The Ontario Turtle Conservation Centre (OTCC) is home to the Kawartha Turtle Trauma Centre, which admits 900 or more turtles a year, with road injuries the primary cause of admission. We tested the hypothesis that road mortality in turtles is female-biased using data from injured Midland Painted Turtles (Chrysemys picta marginata), Snapping Turtles (Chelydra serpentina), Blanding’s Turtles (Emydoidea blandingii), and Northern Map Turtles (Graptemys geographica) collected over about 126 000 km2 and admitted to OTCC’s hospital from January 2013 to October 2017. There was no difference in the number of male and female admissions of Midland Painted, Blanding’s, or Snapping Turtles (P > 0.05); however, more female Northern Map Turtles than males were admitted (P < 0.001). Admission of female turtles peaked in June during the nesting season, but male admissions were more evenly distributed throughout the season. Our admissions data provide a temporally unbiased and geographically broad snapshot of turtle–vehicle interactions that can directly inform conservation and management policies. Although our data are not equivalent to mortality rates, these results demonstrate that vehicle strikes can have a substantial impact on both female and male turtles.

Anthropogenic nest sites provide warmer incubation environments than natural nest sites in a population of oviparous reptiles near their northern range limit.

Oviposition site choice affects a host of offspring phenotypes and directly impacts maternal fitness. Recent evidence suggests that oviparous reptiles often select nest sites where the landscape has been altered by anthropogenic activity, whereas natural nest sites are less often used. We leverage a long-term study of snapping turtle (Chelydra serpentina) to identify natural nest sites and anthropogenic nest sites and to compare habitat variables among nest site types. Natural and anthropogenic nest sites did not differ in average canopy closure, distance to nearest water, substrate composition, or aspect. However, anthropogenic nest sites had less ground-level vegetation and greater soil brightness, and were 3.3°C warmer than natural nests during incubation. We used the Schoolfield model of poikilotherm development to assess differences in development rate between natural and anthropogenic nests. Because of the difference in temperature, embryos in anthropogenic nests were predicted to have undergone nearly twice as much development as embryos in natural nests during incubation. We outline why the evolution of fast embryonic development rate cannot compensate indefinitely for the low temperature incubation regimes that become increasingly prevalent at northern range margins, thereby underlining why maternal nest site choice of relatively warm anthropogenic sites may help oviparous reptiles persist in thermally constrained environments. Future research should aim to quantify both the thermal benefits of anthropogenic nest sites, as well as associated fitness costs (e.g., increased adult mortality) to elucidate whether anthropogenic disturbance of the landscape can be an ecological trap or serve a net benefit to some reptiles in northern environments.

SURGICAL ANATOMY OF CELIOTOMY APPROACHES TO THE STOMACH IN THE COMMON SNAPPING TURTLE (CHELYDRA SERPENTINA)

Entanglement in or ingestion of fishing gear is a common cause of morbidity and mortality in chelonians. Commercial and recreational fishing activities exert bycatch pressures sufficient to cause population declines in the common snapping turtle (Chelydra serpentina) and the alligator snapping turtle (Macrochelys spp.). Gastrotomy for the removal of fish hook foreign bodies from the stomach of freshwater turtles typically requires a plastron osteotomy but in sea turtles has been successfully accomplished via soft tissue approaches. This study compared the anatomy and feasibility of soft tissue surgical approaches to the stomach in the common snapping turtle in both the prefemoral and the axillary regions. Anatomical dissections were performed on cadavers of five adult common snapping turtles, and the surgical anatomy of the left axillary and left prefemoral regions was characterized. The left axillary approach required extensive transection of musculature and provided poor exposure of the coelomic cavity and stomach. In contrast, the left prefemoral approach was simple to perform and provided sufficient access to the stomach for gastrotomy. The prefemoral celiotomy has significant advantages over the axillary celiotomy in the common snapping turtle and should be considered the surgical approach of choice for gastrotomy in this species.

Assessment of critical habitat for common snapping turtles (Chelydra serpentina) in an urbanized coastal wetland

Critical habitats such as nesting areas and overwintering sites are specific areas used by organisms to carry out important life functions. In many urbanized centers, critical habitats of at-risk species have often become degraded and/or fragmented because of human activities. Such is the case for the population of common snapping turtles (Chelydra serpentina) in Cootes Paradise Marsh, a highly urbanized ecosystem located at the western tip of Lake Ontario. In addition to these threats, mortality from collisions with cars on a four-lane highway at the western end of the marsh has greatly reduced wildlife populations. Here, we examine long-term changes in critical habitat distribution that has accompanied urbanization of Cootes Paradise Marsh from 1934 to 2010. We delineated potential nesting habitat for snapping turtles in 7 digitized aerial photos, using literature information and 2017 nesting surveys as guides. Between 1934 and 2010, total area of potential nesting habitat decreased by almost 50%. Nesting surveys confirmed that snapping turtles were disproportionately using created nesting mounds and this suggests that availability of natural nesting habitat is limited. We also radio tracked 11 snapping turtles to identify use of overwintering habitat. Temperature loggers monitored in-situ water temperatures at each turtle’s location and other unconfirmed habitats. The snapping turtle population overwintered in a wide range of upland terrestrial habitats and we found consistent characteristics regarding water temperature across both confirmed and unconfirmed sites, therefore suggesting overwintering habitat may not be limiting within the marsh.

Influence of Hoop-Net Trap Diameter on Capture Success and Size Distribution of Comparatively Large and Small Freshwater Turtles

We investigated the influence of hoop-net trap size on number and size of captures for comparatively large (Chelydra serpentina [Snapping Turtle]) and small (Chrysemys picta [Painted Turtle]) freshwater turtle species. We trapped turtles at 32 ponds throughout West Virginia in the summers of 2016 and 2017, with each pond sampled for 5 consecutive days using five 0.91-m–diameter and five 0.76-m–diameter baited hoop-net traps. We captured a total of 98 and 283 unique Snapping Turtles and Painted Turtles, respectively. Larger-diameter traps captured more Snapping Turtles and smallerdiameter traps captured more Painted Turtles. Mean carapace length was greater for both species in larger-diameter traps, but this result was possibly influenced by the ability of the smallest Painted Turtles to escape through the mesh of the larger traps. Our results indicate that hoop-net–trap diameter can substantially influence both number and size distribution of captures, and thus, trap size is an important sampling design consideration for freshwater turtle research and monitoring using hoop-net traps.

Positive or negative? The shell alters the relationship among behavioral defense strategy, energy metabolic levels and antioxidant capacity in freshwater turtles

BackgroundThe relationships among energy metabolic levels, behavioral and other physiological traits help to determine the trade-off of energy allocation between different traits and the evolution of life-history driven by natural selection. However, these relationships may be distinctive in selected animal taxa because of their unique traits. In the present study, the relationships among energy metabolic levels, behavioral defense strategies, and antioxidant capacity were explored in three freshwater turtle species with different shell morphologies, by assessing responses to attack, righting time, shell morphology, whole-organism metabolic rates, tissue metabolic enzyme activities and antioxidant levels.ResultsThe Chinese three-keeled pond turtles, Chinemys reevesii, showed a passive defense strategy, relatively larger shells, a higher resting metabolic rate (RMR) and higher antioxidant levels compared to the snapping turtle, Chelydra serpentina, or the Chinese soft-shelled turtle, Pelodiscus sinensis. These latter two species both showed an active defense strategy, a higher factorial aerobic scope and better muscle anaerobic metabolic capacity but relatively smaller shells, lower RMR and antioxidant capacity.ConclusionOur results indicate a negative relationship between RMR and activity levels in behavioral defense strategies along small-big shell continuum among the three turtle species. We also found a positive relationship between antioxidant capacity and energy metabolism but a negative one between antioxidant capacity and activity levels in defense strategies. The present study indicated a role of turtle shell in forming unique relationship between energy metabolic levels and behaviors in freshwater turtle taxa and a possible trade-off between the maintenance of physiological homeostasis and activity levels in energy allocation.

The herpetofauna of Wallops Island, Accomack County, Virginia: A case study of a vulnerable community

abstractBarrier islands are valuable models for evolutionary and conservation biology studies. Since 2010, we have investigated the herpetofauna of Wallops Island, Virginia, 25 years after a seminal study. We used combinations of taxon-specific field techniques to maximize accuracy. A total of four species of amphibians and seven species of reptiles were identified. The most abundant amphibian and reptile were Fowler’s toad (Anaxyrus fowleri) and the North American racer (Coluber constrictor), respectively. We report three previously undetected amphibians and the likely prior misidentification of another. We also identified a new snake species. The diamond-backed terrapin (Malaclemys terrapin) is only seasonally abundant on the island, in contrast to the year-round well-established Eastern mud turtle (Kinosternon subrubrum), while only a few juveniles of the common snapping turtle (Chelydra serpentina) were detected. No lizards were found in the island. These limited yet interesting herpetofauna face momentous environmental challenges derived from global climate change and rising sea level.

First report of ranavirus mortality in a common snapping turtle Chelydra serpentina.

An adult male snapping turtle with marked palpebral edema and multifocal skin ulceration was found alive in a marsh in southern Ontario in summer 2017. The turtle was transported to a rehabilitation facility and died 4 d after arrival. The carcass was submitted to the Canadian Wildlife Health Cooperative for post-mortem examination. Gross lesions included ulcerative conjunctivitis, necrotizing stomatitis, and splenomegaly. Microscopically, this corresponded to multisystemic fibrinonecrotizing vasculitis and severe fibrinous splenic necrosis. Liver tissue tested positive for frog virus 3-like ranavirus and negative for herpesvirus via polymerase chain reaction. The gross and microscopic lesions were consistent with previous reports of ranavirus infection in turtles and were severe enough to have been the cause of death in this case. This is the first report of morbidity and mortality in a common snapping turtle with a ranavirus infection, and the first reported case of ranavirus infection in a reptile in Canada. Ranaviruses are considered to be an emerging infectious disease in chelonians as they are increasing in distribution, prevalence, and host range.