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.

Turtles and Tortoises Are in Trouble.

Turtles and tortoises (chelonians) have been integral components of global ecosystems for about 220 million years and have played important roles in human culture for at least 400,000 years. The chelonian shell is a remarkable evolutionary adaptation, facilitating success in terrestrial, freshwater and marine ecosystems. Today, more than half of the 360 living species and 482 total taxa (species and subspecies combined) are threatened with extinction. This places chelonians among the groups with the highest extinction risk of any sizeable vertebrate group. Turtle populations are declining rapidly due to habitat loss, consumption by humans for food and traditional medicines and collection for the international pet trade. Many taxa could become extinct in this century. Here, we examine survival threats to turtles and tortoises and discuss the interventions that will be needed to prevent widespread extinction in this group in coming decades.

Altered spring phenology of North American freshwater turtles and the importance of representative populations.

Globally, populations of diverse taxa have altered phenology in response to climate change. However, most research has focused on a single population of a given taxon, which may be unrepresentative for comparative analyses, and few long-term studies of phenology in ectothermic amniotes have been published. We test for climate-altered phenology using long-term studies (10-36 years) of nesting behavior in 14 populations representing six genera of freshwater turtles (Chelydra, Chrysemys, Kinosternon, Malaclemys, Sternotherus, and Trachemys). Nesting season initiation occurs earlier in more recent years, with 11 of the populations advancing phenology. The onset of nesting for nearly all populations correlated well with temperatures during the month preceding nesting. Still, certain populations of some species have not advanced phenology as might be expected from global patterns of climate change. This collection of findings suggests a proximate link between local climate and reproduction that is potentially caused by variation in spring emergence from hibernation, ability to process food, and thermoregulatory opportunities prior to nesting. However, even though all species had populations with at least some evidence of phenological advancement, geographic variation in phenology within and among turtle species underscores the critical importance of representative data for accurate comprehensive assessments of the biotic impacts of climate change.

Turtle soup, Prohibition, and the population genetic structure of Diamondback Terrapins (Malaclemys terrapin).

Diamondback terrapins (Malaclemys terrapin) were a popular food item in early twentieth century America, and were consumed in soup with sherry. Intense market demand for terrapin meat resulted in population declines, notably along the Atlantic seaboard. Efforts to supply terrapins to markets resulted in translocation events, as individuals were moved about to stock terrapin farms. However, in 1920 the market for turtle soup buckled with the enactment of the eighteenth amendment to the United States' Constitution-which initiated the prohibition of alcoholic drinks-and many terrapin fisheries dumped their stocks into local waters. We used microsatellite data to show that patterns of genetic diversity along the terrapin's coastal range are consistent with historical accounts of translocation and cultivation activities. We identified possible instances of human-mediated dispersal by estimating gene flow over historical and contemporary timescales, Bayesian model testing, and bottleneck tests. We recovered six genotypic clusters along the Gulf and Atlantic coasts with varying degrees of admixture, including increased contemporary gene flow from Texas to South Carolina, from North Carolina to Maryland, and from North Carolina to New York. In addition, Bayesian models incorporating translocation events outperformed stepping-stone models. Finally, we were unable to detect population bottlenecks, possibly due to translocation reintroducing genetic diversity into bottlenecked populations. Our data suggest that current patterns of genetic diversity in the terrapin were altered by the demand for turtle soup followed by the enactment of alcohol prohibition. In addition, our study shows that population genetic tools can elucidate metapopulation dynamics in taxa with complex genetic histories impacted by anthropogenic activities.

Spatiotemporal analysis of gene flow in Chesapeake Bay Diamondback Terrapins (Malaclemys terrapin).

There is widespread concern regarding the impacts of anthropogenic activities on connectivity among populations of plants and animals, and understanding how contemporary and historical processes shape metapopulation dynamics is crucial for setting appropriate conservation targets. We used genetic data to identify population clusters and quantify gene flow over historical and contemporary time frames in the Diamondback Terrapin (Malaclemys terrapin). This species has a long and complicated history with humans, including commercial overharvesting and subsequent translocation events during the early twentieth century. Today, terrapins face threats from habitat loss and mortality in fisheries bycatch. To evaluate population structure and gene flow among Diamondback Terrapin populations in the Chesapeake Bay region, we sampled 617 individuals from 15 localities and screened individuals at 12 polymorphic microsatellite loci. Our goals were to demarcate metapopulation structure, quantify genetic diversity, estimate effective population sizes, and document temporal changes in gene flow. We found that terrapins in the Chesapeake Bay region harbour high levels of genetic diversity and form four populations. Effective population sizes were variable. Among most population comparisons, estimates of historical and contemporary terrapin gene flow were generally low (m ≈ 0.01). However, we detected a substantial increase in contemporary gene flow into Chesapeake Bay from populations outside the bay, as well as between two populations within Chesapeake Bay, possibly as a consequence of translocations during the early twentieth century. Our study shows that inferences across multiple time scales are needed to evaluate population connectivity, especially as recent changes may identify threats to population persistence.

Spatial variation in the littoral vertebrate community of a reservoir relative to physical and biological gradients.

Reservoirs possess gradients in conditions and resources along their long (deep-shallow) axis, but the response of littoral vertebrates (fish and turtles) to these gradients is poorly understood. We have quantified the littoral vertebrate communities throughout a small reservoir in Southeastern Ohio during July and August using traps, and related community composition to environmental variables using NMDS ordination. Ordination revealed that fish and turtles were broadly separated in ordination space, and three distinctly different environmental gradients were significantly associated with the underlying observed species abundances. Observed turtle abundance was explained by measurements of bathymetry, turbidity, and benthic resources, but none of these environmental variables were a reliable predictor of observed fish abundance. Temperature was a poor predictor of observed abundance for both fish and turtles independently, but when fish and turtles were considered together, it became apparent that there were cold areas of the reservoir where observed fish and turtle abundances were different than in other areas of the reservoir. These results suggest that the predictor (environmental) variables we used were appropriate for investigating turtle ecology in reservoirs, but that observed fish abundance is mediated by factors that were not modeled. The efficacy of using traps, the ecological implications of considering fish and turtles together as sympatric and potentially competing species, and directions for future study are discussed.

Applying a reservoir functional-zone paradigm to littoral bluegills: differences in length and catch frequency?

Reservoirs exhibit gradients in conditions and resources along the transition from lotic to lentic habitat that may be important to bluegill ecology. The lotic-lentic gradient can be partitioned into three functional zones: the riverine, transitional, and lacustrine zones. We measured catch frequency and length of bluegills (Lepomis macrochirus) captured along the periphery of these areas (i.e., in the littoral zone of each functional zone) for four small reservoirs in Southeastern Ohio during the summer months of three years. Catch frequency differed between zones for two reservoirs, but these differences were not observed in other years. There was no relationship between reservoir zone and either standard length or catch frequency when the data for all reservoirs were pooled, but we did observe a bimodal length distribution in all reservoirs. A combination of ecological factors including inter and intraspecific competition, predation intensity, management practices, limnology, and assemblage complexity may be mitigating bluegill distribution and abundance in reservoirs. Therefore, a functional zone (categorical) approach to understanding bluegill ecology in reservoirs may not be appropriate.

Geographic variation in egg size and lipid provisioning in the diamondback terrapin Malaclemys terrapin.

Understanding phenotypic differentiation among populations of wide-ranging species remains at the core of life-history research, because adaptation to local environmental conditions is expected. For example, when energy resources influence offspring fitness (as in oviparous ectotherms), the egg and hatchling environments are expected to influence selection by acting on the amount of energy allocated to offspring. Here we identify population variation in egg mass, length, width, and volume from diamondback terrapin Malaclemys terrapin eggs collected in Rhode Island (RI), Maryland (MD), and South Carolina (SC). Egg size (mean volume: 7.6, 8.1, and 9.1 cc in RI, MD, and SC, respectively) and clutch size (mean no. eggs: 16.1, 12.2, and 6.0 in RI, MD, and SC, respectively) differed among populations, which indicated that females produce larger clutches with smaller eggs at high latitudes and smaller clutches of larger eggs at lower latitudes. Lipid analyses indicated that eggs from SC contained yolks with a higher proportion of nonpolar lipids than did eggs from MD or RI (mean percentage of nonpolar lipids: 22.3%, 22.5%, and 31.8% in RI, MD, and SC, respectively). Thus, female terrapins in SC are laying larger eggs with increased lipid content to provide more energy for the developing embryo. Interestingly, total triacylglycerol (energetic lipid) was greater in southern populations but occurred in higher proportions in northern populations (total triacylglycerol: 88.0%, 85.4%, and 81.9% in RI, MD, and SC, respectively). This variation in triacylglycerol levels demonstrates the necessity for quantifying each lipid component. These data indicate a difference in reproductive strategy by which females in northern populations invest in higher fecundity with less energetic resources per offspring, whereas females in southern populations invest in larger eggs with considerably greater energy reserves.

Impacts of multiple stressors on growth and metabolic rate of Malaclemys terrapin.

Coastal species encounter numerous physiological stressors ranging from daily fluctuations in salinity and temperature to anthropogenic contaminants, yet the effects of such stressor combinations on aquatic organisms remain largely unknown. Exposure to environmental contaminants, such as polychlorinated biphenyls (PCBs), can disrupt physiological processes, and while physiological responses to salinity change are well understood, the combined effects of salinity change and contaminants on these processes are unknown. Marine and brackish water turtles are often simultaneously exposed to both stressors. We exposed male, eight-month-old diamondback terrapins to one of four salinity treatments (0, 10, 20, and 30 parts per thousand) in the presence and absence of the anthropogenic stressor 3,3',4,4',5-pentachlorobiphenyl (PCB 126, 20 microg/g via intraperitoneal injection) and monitored growth (carapace length and mass) and metabolic rate for six months. Exposure to PCB 126 significantly reduced growth (p < 0.0001), lowered standard metabolic rates (SMRs; p < 0.0001), and altered respiratory pattern (p < 0.0001). Salinity stress reduced growth (p < 0.0001) and altered the respiratory pattern (p < 0.0001) but had no overall effect on metabolic rate (p = 0.33). No interactive effects of PCBs and salinity were seen on either growth or metabolic rate. Our data indicate terrapins may be able to cope with some effects of salinity change through physiological adjustments but are less able to cope with PCBs. We show that PCB 126 disrupts the ecophysiological mechanisms that affect life history traits and thus ultimately could alter population structure and dynamics. The present study enriches our understanding of the environmental toxicology of reptiles and aids in the interpretation of health conditions documented in field-collected turtles contaminated with PCBs.