Malaclemys Research Articles

The effects of commercial diets on the growth of diamondback terrapins Malaclemys terrapin in head-start programmes

Populations of diamondback terrapins Malaclemys terrapin are declining. Consequently, head-start programmes, in which hatchling terrapins are reared in captivity for 6–9 months and then released into their natural habitat, are needed to help stabilise wild populations. As a contribution to the development of optimal husbandry conditions for future generations of diamondback terrapins in head-start programmes, we examined the effects of two widely available commercial turtle foods (Reptomin® and Mazuri®) on the growth of juvenile terrapins over a period of 12 weeks. While terrapins did well on both diets, we show that terrapins consuming the Mazuri® diet had a significantly greater increase in mass and carapace length compared to terrapins on the Reptomin® diet.

Chromosome-level genome of diamondback terrapin provides insight into the genetic basis of salinity adaptation.

Diamondback terrapins (Malaclemys terrapin centrata) exhibit strong environmental adaptability and live in both freshwater and saltwater. However, the genetic basis of this adaptability has not been the focus of research. In this study, we successfully constructed a ∼2.21-Gb chromosome-level genome assembly for M. t. centrata using high-coverage and high-depth genomic sequencing data generated on multiple platforms. The M. t. centrata genome contains 25 chromosomes and the scaffold N50 of ∼143.75 Mb, demonstrating high continuity and accuracy. In total, 53.82% of the genome assembly was composed of repetitive sequences, and 22435 protein-coding genes were predicted. Our phylogenetic analysis indicated that M. t. centrata was closely related to the red-eared slider turtle (Trachemys scripta elegans), with divergence approximately ∼23.6 million years ago (Mya) during the early Neogene period of the Cenozoic era. The population size of M. t. centrata decreased significantly over the past ∼14 Mya during the Cenozoic era. Comparative genomic analysis indicated that 36 gene families related to ion transport were expanded and several genes (AQP3, solute carrier subfamily, and potassium channel genes) underwent specific amino acid site mutations in the M. t. centrata genome. Changes to these ion transport-related genes may have contributed to the remarkable salinity adaptability of diamondback terrapin. The results of this study not only provide a high-quality reference genome for M. t. centrata but also elucidate the possible genetic basis for salinity adaptation in this species.

Demographics of a Previously Undocumented Diamondback Terrapin (Malaclemys terrapin) Population

Demographics of a Previously Undocumented Diamondback Terrapin (Malaclemys terrapin) Population

The characterization of the mitochondrial genome of Graptemys ouachitensis

Graptemys ouachitensis (CAGLE, 1953) belongs to the Graptemys genus, the Emydidae family, and the Testudines order. This study involved sequencing the complete mitochondrial genome (mitogenome) of G. ouachitensis using next-generation sequencing, and analyzing the essential characteristics, and phylogenetic relationship. The results revealed that the G. ouachitensis mitogenome was 16,674 bp in length (A: 34.1%, C: 26.0%, G: 13.0%, T: 26.9%) and included 22 tRNAs, 13 protein-coding genes, two ribosomal RNA genes, and a non-coding control region (GenBank accession: NC071766). The genome composition of G. ouachitensis presented a slight A + T bias (61.0%) and exhibited a positive AT skew (0.118) and a negative GC skew (–0.333). A phylogenetic analysis based on the complete mitogenome indicated that the G. ouachitensis was more closely associated with Malaclemys terrapin than the other eight known Emydidae species. Thus, our findings present a novel mitogenome at the species level. This study introduces the first complete mitogenome of G. ouachitensis, providing valuable molecular information for phylogenetic and conservation genetics analyses of G. ouachitensis.

Salinity preferences of Diamondback Terrapin (<i>Malaclemys terrapin</i>) headstarts: A laboratory study

Salt marshes along the eastern coast of the USA are challenging environments due to their tidal nature,which causes constant fluctuations in the salinity levels of their brackish water. Diamondback Terrapins (Malaclemysterrapin) can inhabit these salt marshes due to their ability to tolerate highly saline water. The physiological mechanismsunderlying this ability are well known in adults, but have not been thoroughly explored in hatchlings and juveniles,which cannot grow when exposed to high salinity. We examined salinity preferences of hatchlings and juveniles in thelaboratory and concluded that hatchlings do not exhibit salinity preferences and develop this trait as juveniles.

Multiple horizontal transfer events of a DNA transposon into turtles, fishes, and a frog

Horizontal transfer of transposable elements (HTT) has been reported across many species and the impact of such events on genome structure and function has been well described. However, few studies have focused on reptilian genomes, especially HTT events in Testudines (turtles). Here, as a consequence of investigating the repetitive content of Malaclemys terrapin terrapin (Diamondback turtle) we found a high similarity DNA transposon, annotated in RepBase as hAT-6_XT, shared between other turtle species, ray-finned fishes, and a frog. hAT-6_XT was notably absent in reptilian taxa closely related to turtles, such as crocodiles and birds. Successful invasion of DNA transposons into new genomes requires the conservation of specific residues in the encoded transposase, and through structural analysis, these residues were identified indicating some retention of functional transposition activity. We document six recent independent HTT events of a DNA transposon in turtles, which are known to have a low genomic evolutionary rate and ancient repeats.

Presumptive Stenotrophomonas maltophilia–Associated Multisystemic Granulomatous Disease in Aquatic Turtles

Abstract Stenotrophomonas maltophilia is a gram-negative bacterium that can be routinely identified in the aquatic environment, and has become an emergent, multi-drug resistant life-threatening organism in some circumstances. This bacterium was identified as a presumptive causative agent in cases of polysystemic granulomatous disease in one diamondback terrapin (Malaclemys terrapin) and one mata mata (Chelus fimbriata). Both chelonians presented with lethargy, hyporexia, and multifocal subcutaneous masses diagnosed by physical examination and in one individual on computed tomography (CT). The primary hematologic finding was moderate to severe heterophilic leukocytosis, and both turtles were treated with a combination of supportive care, systemic antibiotics, and/or surgical resection of subcutaneous masses. Medical and surgical management were unsuccessful, and one patient was euthanized and the other found deceased. Necropsies revealed multisystemic granulomas, and cultures identified growth of Stenotrophomonas maltophilia. A post-mortem investigation into possible risk factors identified co-morbidities including shell disease, repeated administration of injectable antibiotics, low environmental temperature, and aquatic pH changes as possible contributing factors. This bacterium appears to be an emerging organism of concern and should be considered as a potential cause of granulomas in aquatic chelonians.

An easily implemented single-visit survey method for intermittently available and imperfectly detectable wildlife applied to the Florida east coast diamondback terrapin (Malaclemys terrapin tequesta).

Single-visit surveys of plots are often used for estimating the abundance of species of conservation concern. Less-than-perfect availability and detection of individuals can bias estimates if not properly accounted for. We developed field methods and a Bayesian model that accounts for availability and detection bias during single-visit visual plot surveys. We used simulated data to test the accuracy of the method under a realistic range of generating parameters and applied the method to Florida's east coast diamondback terrapin in the Indian River Lagoon system, where they were formerly common but have declined in recent decades. Simulations demonstrated that the method produces unbiased abundance estimates under a wide range of conditions that can be expected to occur in such surveys. Using terrapins as an example we show how to include covariates and random effects to improve estimates and learn about species-habitat relationships. Our method requires only counting individuals during short replicate surveys rather than keeping track of individual identity and is simple to implement in a variety of point count settings when individuals may be temporarily unavailable for observation. We provide examples in R and JAGS for implementing the model and to simulate and evaluate data to validate the application of the method under other study conditions.

Development, verification, and implementation of an eDNA detection assay for emydids with a case study on diamondback terrapins, Malaclemys terrapin, and red eared slider, Trachemys script elegans

Development, verification, and implementation of an eDNA detection assay for emydids with a case study on diamondback terrapins, Malaclemys terrapin, and red eared slider, Trachemys script elegans

Estimating Changing Marshland Habitat and Conservation Potential for Diamondback Terrapins (Malaclemys terrapin) in New Jersey under Climate Change

The diamondback terrapin (Malaclemys terrapin), a brackish water turtle species native to the eastern United States, is under “special concern” in the state of New Jersey, due to decreasing habitat from development and changing climatic conditions. Diamondback terrapins reside in saline marshes and coastal wetlands and nest in sandy substrate, primarily beaches and dunes, in June and July. New Jersey is vulnerable to sea level rise, leaving diamondback terrapin habitats and nesting areas at risk of inundation under future climate scenarios, and, as the most densely populated state, subject to continual development pressures on potentially conservable land. Changing sea levels and climatic conditions will cause accretion and migration of marshes into open grassy land, yielding new potential terrapin habitats, though changing temperatures could affect the availability of male-producing nesting sites and impact potential nesting patterns. This study spatially modeled lost, gained, and changed habitat and nesting areas under sea level rise scenarios for 2050 and 2100 in New Jersey and quantified these by municipality to offer insights into potential conservable land that may mitigate these changes for the vulnerable species. The results indicate an overall decrease in potential habitat coupled with a decrease in both overall and male-producing nesting ranges.

Satellite telemetry reveals space use of diamondback terrapins

Movement and space use information of exploited and imperiled coastal species is critical to management and conservation actions. While satellite telemetry has been successfully used to document movements of marine turtles, the large tag sizes available have limited use on smaller turtle species. We used small Argos-based satellite tags to document movement patterns of diamondback terrapins (Malaclemys terrapin), the only estuarine turtle species in North America. Movement data from ten terrapins in St. Joseph Bay, Florida were gathered between July 13, 2018 and July 22, 2021. We estimated seasonal space use using the daily locations generated from a Bayesian hierarchical state-space model to calculate minimum convex polygons (95% MCP) and kernel density estimates (50% and 95% KDE). Mean tracking duration was 125 days and mean home range size was 9.4 km2 (95% MCP) and 8.1 km2 (95% KDE). Seagrass habitat comprised 55.8% of all home ranges on average, whereas salt marsh comprised a mean of 3.0%. Mean elevation used by terrapins was − 0.13 m (95% MCP) and -0.35 m (95% KDE). Satellite telemetry provided broad-scale spatiotemporal movement and space use data; however, Argos error produced considerable noise relative to true terrapin movements given their size, speed, and behavior. Terrapin home ranges were greater than previously reported and three of the ten terrapins exhibited repeated long-distance, directed movements within the bay. Small patches of salt marsh habitat were centralized within home ranges, despite comprising only a small percentage for each terrapin. Moreover, the percentage of salt marsh present in each core use area was positively correlated with terrapin mass. Although considered an estuarine species, seagrass habitat comprised a large portion of terrapin home ranges; however, our data did not provide the detail necessary to understand how terrapins were using this habitat. As northward-expanding mangroves continue to infringe upon salt marsh habitat, there is potential for negative impacts to terrapin populations across the northern Gulf of Mexico. As salt marsh habitat continues to be infringed upon by northward-expanding mangroves impacts to terrapins across the northern Gulf of Mexico.

Evaluating uncertainty to improve a common monitoring method and guide management decisions for diamond‐backed terrapins

AbstractDesigning monitoring with adequate certainty to evaluate management actions can be challenging, especially for elusive species in relatively inaccessible habitats. The diamond‐backed terrapin (Malaclemys terrapin) is considered a high priority species for management in all states within its range. Among key threats to terrapin populations is bycatch mortality in crab pots, prompting states throughout the species' range to consider crabbing regulations and creating a need for a monitoring approach able to evaluate the success of any new crabbing regulations to benefit terrapins. Because terrapins occupy extensive and often difficult to access estuarine habitat, it is hard to collect sufficient data to estimate population responses accurately and precisely for management. To assist state managers with decisions regarding monitoring bycatch reduction regulations, we modeled 12 years of terrapin capture‐recapture data. We used estimates from those models to simulate capture‐recapture data pre‐ and post‐implementation of bycatch reduction that resulted in a 0.20 absolute increase in mean apparent survival probability. Results indicated weak reliability of a monitoring approach using only manual seining of tidal creeks to detect a real management effect, with a positive management effect detected at the 95% certainty level only 34% of the time. When we considered 85% and 75% certainty thresholds, we detected a positive effect on survival among 61% and 75% of simulations, respectively. Low within‐year recapture probability and the effect of tide amplitude on terrapin availability indicate there is low feasibility of improving monitoring precision at a single site, requiring monitoring of more sites to improve confidence in the detection of the management effect. The number of sites monitored depends on the acceptable level of certainty. We recommend that researchers and management entities that use seining assess the level of certainty they require to evaluate management actions and increase the number of sites sampled to meet that level of certainty. Additionally, the use of multiple monitoring methods and integrated models should be explored to reduce uncertainty and to allow for easier monitoring of more populations over broader spatial scales.

Bycatch reduction devices exclude diamondback terrapins and maintain blue crab catch in two Virginia tidal creeks

AbstractObjectiveThe diamondback terrapin Malaclemys terrapin is frequently caught as bycatch in both commercial and recreational blue crab Callinectes sapidus fisheries throughout its range along the Atlantic and Gulf coasts of North America. Bycatch reduction devices (BRDs) are plastic or wire rectangles mounted in the entrance funnels of crab traps, designed to exclude terrapins while still allowing crabs to enter. In this study conducted in two tidal creeks in Virginia, USA, we assessed the effectiveness of four BRD designs, including two novel oval designs, against control traps with no BRDs.MethodsWe tested four replicates of each of the five trap treatments (1.75‐inch oval BRD, 2‐inch oval BRD, 1.75‐inch rectangular BRD, 2‐inch rectangular BRD, and a control trap without a BRD) in each tidal creek, for a total of 20 traps per creek and 40 traps total. We fitted traps with wire chimneys that extended above the high tide water line to allow trapped terrapins to surface for air. For eight weeks during summer 2021, we baited traps with Atlantic Menhaden Brevoortia tyrannus each day, beginning on Monday. Tuesday–Friday, we emptied traps of any animals inside, and recorded terrapin sex, terrapin carapace length, terrapin carapace width, and terrapin shell height, as well as blue crab carapace length.ResultWe found that all four BRD designs were highly effective at excluding terrapins and maintaining crab catch when compared to control traps. We found a significant difference (p = 0.003) in catch per unit effort (CPUE) of diamondback terrapins among treatments, with the control group (those without BRDs) having the highest CPUE (0.97 ± 0.18). All traps fitted with BRDs decreased terrapin capture significantly compared to the control group. Oval BRDs excluded more terrapins than their rectangular counterparts with the same height dimension, although these differences were not significant. We found no significant difference in CPUE of blue crabs among treatments (p = 0.392), or in the size of legal crabs caught in each treatment (p = 0.216).ConclusionThis study provides evidence of the effectiveness of both rectangular and oval‐shaped BRDs to exclude terrapins and maintain crab catch in Virginia waters, where BRDs are not currently required.

HEALTH ASSESSMENT OF WILD NORTHERN DIAMOND-BACKED TERRAPINS (MALACLEMYS TERRAPIN TERRAPIN) IN NEW JERSEY, USA.

A popular species in the pet trade, and therefore in the illegal wildlife trade, the diamond-backed terrapin, Malaclemys terrapin, population has seen significant declines. Associated with the illegal wildlife trade, occasions arise in which terrapins are confiscated, and no standard operating procedures exist for repatriation into the wild. To develop such procedures, an understanding of the pathogens circulating in the wild diamond-backed terrapin population in New Jersey is needed. We sampled 30 wild female diamond-backed terrapins for herpesvirus, Mycoplasmopsis, ranavirus, and intestinal and blood parasites and performed white blood cell counts and differentials and evaluated biochemistry values. Terrapins had an average age of 10 yr (8-15 yr), and 70% were gravid at the time of sampling. Thirty-three percent of the sampled northern diamond-backed terrapins were positive for Mycoplasmopsis sp., and all were negative for ranavirus and herpesviruses. Occasional blood parasites were found, and few intestinal parasites were noted. There was no significant difference between gravid status and any of the blood parameters (P<0.05). Blood chemistry values appeared to vary according to feeding activity; no differences were noted in the values in relation to gravid status. Four terrapins had heterophil to lymphocyte (H:L) ratios above 4.5, significantly higher than the other terrapins sampled, which may indicate inflammation. Two of the four had Mycoplasmopsis, one sample was contaminated by other bacteria and was discarded, and one was negative. No significant difference was found between Mycoplasmopsis infection status and H:L ratio (P=0.926). Our findings, though conducted on a small number of female terrapins at a specific time point, provide data on the pathogens that may be circulating in this population, adding to the current body of knowledge and helping to guide decision making for the reintroduction of confiscated diamond-backed terrapins into New Jersey's wild population.

Isotopic niche of New Jersey terrapins suggests intraspecific resource partitioning, and little variability following a major hurricane

Diamondback terrapins (Malaclemys terrapin) are sexually dimorphic generalist turtles that inhabit salt marshes and estuaries along the Atlantic and Gulf coasts of the United States. On October 29th, 2012, Hurricane Sandy made landfall in New Jersey, USA, directly impacting terrapin populations inhabiting central and southern Barnegat Bay. To examine potential food web mediated impacts to the terrapin population and their foraging dynamics we examined carbon and nitrogen stable isotope values collected from terrapin tissues (2011, 2015, 2019) and resource taxa (2015, 2019) within Barnegat Bay. Isotopic analysis revealed that mature females had lower carbon and higher nitrogen values than immature females and males with almost no isotopic niche overlap, whereas males and immature females had statistically similar values with overlapping niches. Terrapins and resources collected from island habitats contained higher carbon and nitrogen values than those from mainland habitats, with little overlap in niche between habitats. There were no significant temporal variations detected in either carbon or nitrogen values from terrapins between years, or within each habitat pre- and post-Hurricane Sandy. These findings suggest long-term terrapin foraging dynamics have remained relatively stable, signifying resilience to disturbance events within the study site.

Plasma Vitellogenin and Testosterone in Diamond-backed Terrapins (Malaclemys terrapin) during the Nesting Season in Coastal New Jersey

Vitellogenesis is the process in which female oviparous vertebrates synthesize the protein vitellogenin to develop egg yolk. In some species, vitellogenin has been used to investigate reproductive status, as a biomarker of clutch size and nesting frequency, and as a biomarker of exposure to endocrine-disruptive chemicals. The Diamond-backed Terrapin (Malaclemys terrapin) is an obligate coastal species that in the northern extent of its range nests in the spring and summer months. Diamond-backed Terrapins serve as a key indicator species of coastal ecosystem health; thus, furthering our understanding of the endocrine control of reproduction may inform biologists of the health and status of coastal ecosystems. The objective of this study was to quantify baseline values of vitellogenin and testosterone in Diamond-backed Terrapins during the nesting season, in the northern part of their range. Blood samples were taken from adult female terrapins from two populations in coastal New Jersey from June–August. Enzyme-linked immunosorbent assays (ELISAs) were used to quantify vitellogenin (VTG) and testosterone (T) across the nesting season. VTG concentrations showed peak values in the earliest part of the nesting season, significantly declining through the summer before reaching basal values in August, with T showing a similar trend. This suggests that terrapins in New Jersey follow a similar reproductive cycle to other turtle species from temperate latitudes. Additionally, we found that larger females exhibited higher concentration of T and VTG than smaller females. This suggests that VTG and T are useful biomarkers of reproductive output in these animals. Lastly, we also noted that larger females tended to nest earlier in the nesting season than smaller females. We hypothesize that larger females may compete for resources more effectively and efficiently than smaller females, which may confer larger individuals a fitness advantage.

Factors affecting spatiotemporal patterns of nest site selection and abundance in diamondback terrapins.

Determining what factors influence the distribution and abundance of wildlife populations is crucial for implementing effective conservation and management actions. Yet, for species with dynamic seasonal, sex-, and age-specific spatial ecology, like the diamondback terrapin (Malaclemys terrapin; DBT), doing so can be challenging. Moreover, environmental factors that influence the distribution and abundance of DBT in their northernmost range have not been quantitatively characterized. We investigated proximity to nesting habitat as one potential driver of spatiotemporal variation in abundance in a three-step analytical approach. First, we used a scale selection resource selection function (RSF) approach based on landcover data from the National Landcover Database (NLCD) to identify the scale at which DBT are selecting for (or avoiding) landcover types to nest. Next, we used RSF to predict areas of suitable nesting habitat and created an index of nest suitability (NSI). Finally, analyzing visual count data using a generalized linear mixed model (GLMM), we investigate spatiotemporal drivers of relative abundance, with a specific focus on whether similar factors affect offshore abundance and onshore nest site selection. We found the scale of selection for developed and saltmarsh land use classes to be 550 and 600 m and open water land use classes to be 100. Selection was positive for nesting areas proximal to saltmarsh habitat and negative for developed and open water. Expected relative abundance was best explained by the interaction between NSI and day of season, where expected relative abundance was greater within high NSI areas during the nesting season (2.20 individuals, CI: 1.19-3.93) compared to areas of low NSI (1.84 individuals, CI: 1.10-3.10). Our results provide evidence that inferred spatial patterns of suitable nesting habitats explain spatiotemporal patterns of terrapin movement and abundance.

Post‐emergence movements and habitat use by hatchling diamondback terrapins

AbstractDiamondback terrapins (Malaclemys terrapin) inhabit estuarine environments, and adult females typically nest in coastal uplands. Hatchlings emerging from nests overwinter on land and in coastal salt marshes, but the proportions that use each land cover type is not well documented. From 2019 to 2021, we tracked movements and habitat use of hatchlings post‐emergence to determine the importance of upland overwintering sites to a terrapin population in Rhode Island, USA. In late summer and early fall, we attached a radio‐transmitter and passive integrated transponder (PIT) tag (n = 46) or only a PIT tag (n = 132) to carapaces of hatchlings emerging from nests. From August to June, we tracked the hatchlings via radio‐telemetry and a sweeping PIT tag antenna, successfully documenting the fates of 46.6% of them (n = 83). This group included 23 hatchlings that overwintered in the upland, 11 hatchlings that moved to the salt marsh in fall, 46 predated hatchlings, and 3 hatchlings dead from unknown causes. Upon emergence from their nests, 68% of hatchlings dispersed toward water and 32% of hatchlings dispersed away from water. In the uplands, hatchlings typically overwintered within about 2 m of habitat edges. Movement in the uplands peaked from late August to early October, then ceased until hatchlings re‐emerged in late April through early June. To protect terrapins, we recommend limiting the use of heavy equipment (e.g., mowers, tillers) in vegetated uplands near nest sites, and scheduling vegetation management for colder months (Nov–Mar in New England, USA) when hatchlings are inactive.

Loss of Mississippi Diamondback Terrapin (Malaclemys terrapin pileata) Nesting Habitat in the Northern Gulf of Mexico

Diamondback terrapins (Malaclemys terrapin) are a species of turtle that occupy coastal tidal marshes and nest on sandy areas above the high-tide line. Within the Grand Bay National Estuarine Research Reserve, Mississippi diamondback terrapin (M. t. pileata) shoreline nesting habitat at Grand Battures (also known as South Rigolets Island) has decreased from a 2.34-km length of surveyable shoreline in 2014 to a 1.45-km length of shoreline in 2021. Depredated nest surveys in 2021 detected the lowest number of nests to date at this location, with increased search effort, and this is likely due to the high rates of erosion described for this area.

PREVALENCE OF MULTIPLE REPTILIAN PATHOGENS IN THE OROPHARYNGEAL MUCOSA, CLOACAL MUCOSA, AND BLOOD OF DIAMONDBACK TERRAPIN (MALACLEMYS TERRAPIN) POPULATIONS FROM MARYLAND AND GEORGIA, USA.

The diamondback terrapin (Malaclemys terrapin) is a coastal turtle with a range from Massachusetts to Texas and is the only exclusively brackish water turtle in North America. Two populations of wild terrapins from Maryland (n=55) and Georgia (n=7) were examined and tested for potential reptile pathogens. Whole blood and a mucosal (combined oropharyngeal and cloacal) swab from each animal were evaluated by quantitative PCR for 15 potential pathogens including frog virus 3, box turtle Mycoplasmopsis, Mycoplasma agassizii, Mycoplasma testudineum, Salmonella Enteritidis, Salmonella Typhimurium, Borrelia burgdorferi, Anaplasma phagocytophilum, tortoise intranuclear coccidia, testudinid alphaherpesvirus 2, terrapene herpesvirus 1, and terrapene adenovirus. Swabs were positive for a DNA segment 100% homologous to M. testudineum in both populations, with Maryland animals 87% (48 of 55) positive and Georgia animals 86% (6 of 7) positive. Although Mycoplasmopsis spp. are important respiratory pathogens for members of the order Testudines, none of the animals in the study showed any sign of upper respiratory disease. Our data suggest that M. testudineum may survive in non-Testudinidae turtles without causing clinical sigs of disease and suggesting appropriate precautions should be taken in facilities that house multiple species of turtles simultaneously.