Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community.

Climate change has had a significant impact globally on the timing of ecological events such as reproduction and migration in many species. Here, we examined the phenology of reproductive migrations in 10 amphibian species at a wetland in South Carolina, USA using a 30 year dataset. We show for the first time that two autumn-breeding amphibians are breeding increasingly later in recent years, coincident with an estimated 1.2°C increase in local overnight air temperatures during the September through February pre-breeding and breeding periods. Additionally, two winter-breeding species in the same community are breeding increasingly earlier. Four of the 10 species studied have shifted their reproductive timing an estimated 15.3 to 76.4 days in the past 30 years. This has resulted in rates of phenological change that range from 5.9 to 37.2 days per decade, providing examples of some of the greatest rates of changing phenology in ecological events reported to date. Owing to the opposing direction of the shifts in reproductive timing, our results suggest an alteration in the degree of temporal niche overlap experienced by amphibian larvae in this community. Reproductive timing can drive community dynamics in larval amphibians and our results identify an important pathway by which climate change may affect amphibian communities.

Mercury contamination in turtles and implications for human health.

Mercury contamination threatens many ecosystems worldwide. Methylmercury bioaccumulates at each trophic level, and biomagnifies within individuals over time. Long-lived turtles often occupy high trophic positions and are likely to accumulate mercury in contaminated habitats. Millions of turtles worldwide are sold in Asia for human consumption, and consumers may be at risk if turtles contain high levels of mercury. The authors dissected 71 turtles from 14 food trade species and analyzed their tissues (liver, kidneys, muscle, claws, and scutes) for total mercury content. Mercury was generally highest in carnivores, and lowest in herbivores. Liver and scutes had the highest concentrations. The authors compared mercury concentrations with consumption limits developed by the U.S. Environmental Protection Agency and Food and Drug Administration to evaluate mercury in fish tissue. Several samples exceeded the recommended 1,900 parts per billion (ppb) consumption threshold, indicating that consumers who eat certain turtle species frequently may be at risk for mercury-related health problems.

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.

Perfluoroalkyl substances in diamondback terrapins (Malaclemys terrapin) in coastal South Carolina.

This study focused on an estuarine wildlife species exhibiting high site fidelity and ubiquitous distribution in coastal environments along the Atlantic and Gulf coasts of the United States to monitor per- and polyfluoroalkyl substances (PFAS). A total of 75 diamondback terrapin (Malaclemys terrapin) plasma samples were collected from five creeks associated with Kiawah (Oyster Creek, Fiddler Creek, Sandy Creek, Gnat Creek) and Edisto (Townsend Creek) islands in Charleston County, South Carolina and investigated for 15 legacy PFAS. Of those, PFHxS was the only PFAS found in all terrapin plasma samples. Four additional PFAS were routinely detected (greater than 90% of the samples) and were included in statistical analyses: PFOS, PFNA, PFDA, and PFUnA. Sex-differences were observed for two creeks with male plasma containing higher PFAS than female plasma (PFHxS at Townsend Creek, PFOS at Oyster Creek). Sex-specific site differences in PFAS concentrations were observed primarily for males, suggesting male terrapins may be more sensitive indicators of localized contaminant profiles than females. Three PFAS were observed to have negative correlations with body mass: PFOS in males (p = 0.045, tau = -0.220), PFNA in males (p = 0.016, tau = -0.269), and PFHxS in both males (p = 0.007, tau = -0.302) and females (p = 0.001, tau = -0.379). No relationships for body mass and PFDA and PFUnA were observed.

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.

Using multiscale spatial models to assess potential surrogate habitat for an imperiled reptile.

UNLABELLED: In evaluating conservation and management options for species, practitioners might consider surrogate habitats at multiple scales when estimating available habitat or modeling species' potential distributions based on suitable habitats, especially when native environments are rare. Species' dependence on surrogates likely increases as optimal habitat is degraded and lost due to anthropogenic landscape change, and thus surrogate habitats may be vital for an imperiled species' survival in highly modified landscapes. We used spatial habitat models to examine a potential surrogate habitat for an imperiled ambush predator (eastern diamondback rattlesnake, Crotalus adamanteus; EDB) at two scales. The EDB is an apex predator indigenous to imperiled longleaf pine ecosystems (Pinus palustris) of the southeastern United States. Loss of native open-canopy pine savannas and woodlands has been suggested as the principal cause of the species' extensive decline. We examined EDB habitat selection in the Coastal Plain tidewater region to evaluate the role of marsh as a potential surrogate habitat and to further quantify the species' habitat requirements at two scales: home range (HR) and within the home range (WHR). We studied EDBs using radiotelemetry and employed an information-theoretic approach and logistic regression to model habitat selection as use vs. AVAILABILITY: We failed to detect a positive association with marsh as a surrogate habitat at the HR scale; rather, EDBs exhibited significantly negative associations with all landscape patches except pine savanna. Within home range selection was characterized by a negative association with forest and a positive association with ground cover, which suggests that EDBs may use surrogate habitats of similar structure, including marsh, within their home ranges. While our HR analysis did not support tidal marsh as a surrogate habitat, marsh may still provide resources for EDBs at smaller scales.

Fish predation in size-structured populations of treefrog tadpoles.

The effects of tadpole body size, tadpole sibship, and fish body size on predation of gray treefrog tadpoles, Hyla chrysoscelis, were studied in laboratory and artificial pond experiments. Tadpole body size had a significantly positive effect on the survival of tadpoles in all experiments. The relationship between tadpole biomass eaten and biomass available suggested that fish were not satiated when consuming the largest tadpoles. Large tadpoles were probably better able to evade predators. A difference in survival among full sib families of tadpoles was only present in one family, suggesting that genetic differences in predator avoidance behavior or palatability were probably secondarily important to body size per se. Fish body size had a significantly negative effect on the survival of tadpoles. Larger fish consumed a larger number and proportion of tadpoles as well as greater biomass. These results indicate that environmental factors affecting the growth rate of tadpoles cand dramatically alter their vulnerability to gape-limited predators.

Catastrophic reproductive failure, terrestrial survival, and persistence of the marbled salamander.

Wide variation in reproductive success is common among amphibians that breed in seasonal ponds, but persistence of adults can buffer against these fluctuations, particularly for long-lived species. We hypothesized that the frequent episodes of catastrophic failure of the marbled salamander (Ambystoma opacum) enhance the importance of high terrestrial survival. At Rainbow Bay in South Carolina reproductive success was poor (< 1 metamorph/breeding female) in nearly half of the 22 years that the species bred. Complete failure occurred in 6 of 22 years. To study catastrophic failure, we adapted an age-structured, individual-based model with density-dependent growth and survival of larvae. The model was based on extensive data from local field studies and experiments. With consistently good survival in the pond stages, the simulated population required survival probabilities in the upland stages (juveniles and adults) near 0.5/year to persist and near 0.8/year to achieve the increases observed. Catastrophic failure, occurring randomly with probability 0.5/year created additional fluctuations in the population, raised the thresholds of survival required for persistence, and caused extinction under conditions that were otherwise favorable. The marbled salamander at Rainbow Bay is not at great risk of extinction because of catastrophic failure, but the risk increases dramatically if life span is decreased or frequency of failure is increased. Any reduction in terrestrial survival will have deleterious consequences by reducing the breeding populations at equilibrium, even if it does not jeopardize persistence. Our model provides assessments of risk that can be applied to poorly studied species with similar life histories, such as the endangered flatwoods salamander (A. cingulatum).

Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought-induced aestivation.

1. Capital breeding is an ideal reproductive strategy for many ectotherms because it provides a disassociation between feeding and reproduction, a necessary requirement for animals that become anorexic during pregnancy. Among ectotherms, some viviparous snakes (e.g. Viperidae) exemplify the capital breeding strategy because many species (i) do not feed during pregnancy due to behavioural conflicts between reproduction and foraging, and (ii) take more than one season to accumulate sufficient energetic stores for reproduction. 2. Isolated wetlands often exhibit extreme annual fluctuations in environmental conditions with prolonged droughts periodically leaving wetlands completely dry and devoid of prey. Following droughts, however, wetlands can be extremely productive, rendering prey resources virtually unlimited for some species. 3. This study examines drought survival strategy and reproductive ecology of a small aquatic snake Seminatrix pygaea (Cope) in an isolated wetland. Seminatrix pygaea are atypical from most sympatric snake species in that (i) their small body size, reliance on aquatic prey, and high rates of evaporative water loss make them ill-suited to overland movement, and (ii) they may not be subject to costs typically associated with feeding during pregnancy. 4. We hypothesized that S. pygaea would survive periodic multiyear droughts by aestivating within the dried wetland, a survival strategy heretofore undocumented in snakes. Further, we hypothesized that if S. pygaea rely on 'typical' snake reproductive strategies of 'adaptive anorexia' and capital breeding, reproductive output would be reduced in the first wet year following drought. 5. By encircling a 10-ha wetland with a continuous drift fence before it refilled we were able to demonstrate that S. pygaea were present within the dried wetland prior to the onset of spring rains that refilled the wetland in 2003. Our results suggest that S. pygaea are capable of surviving multiyear droughts by aestivating within the dried wetland. 6. Despite having presumably depleted energy reserves during the drought, S. pygaea reproduced with the same frequency and fecundity during the first season following refilling of the wetland as in pre-drought years. 7. The ability of S. pygaea to rebound rapidly from the stresses of prolonged drought is due in part to their reproductive ecology. Seminatrix pygaea readily feed throughout pregnancy and consequently can rapidly translate high prey abundances into reproductive output through income breeding.

Remarkable amphibian biomass and abundance in an isolated wetland: implications for wetland conservation.

Despite the continuing loss of wetland habitats and associated declines in amphibian populations, attempts to translate wetland losses into measurable losses to ecosystems have been lacking. We estimated the potential productivity from the amphibian community that would be compromised by the loss of a single isolated wetland that has been protected from most industrial, agricultural, and urban impacts for the past 54 years. We used a continuous drift fence at Ellenton Bay, a 10-ha freshwater wetland on the Savannah River Site, near Aiken, South Carolina (U.S.A.), to sample all amphibians for 1 year following a prolonged drought. Despite intensive agricultural use of the land surrounding Ellenton Bay prior to 1951, we documented 24 species and remarkably high numbers and biomass of juvenile amphibians (>360,000 individuals; >1,400 kg) produced during one breeding season. Anurans (17 species) were more abundant than salamanders (7 species), comprising 96.4% of individual captures. Most (95.9%) of the amphibian biomass came from 232095 individuals of a single species of anuran (southern leopard frog[Rana sphenocephala]). Our results revealed the resilience of an amphibian community to natural stressors and historical habitat alteration and the potential magnitude of biomass and energy transfer from isolated wetlands to surrounding terrestrial habitat. We attributed the postdrought success of amphibians to a combination of adult longevity (often >5 years), a reduction in predator abundance, and an abundance of larval food resources. Likewise, the increase of forest cover around Ellenton Bay from <20% in 1951 to >60% in 2001 probably contributed to the long-term persistence of amphibians at this site. Our findings provide an optimistic counterpoint to the issue of the global decline of biological diversity by demonstrating that conservation efforts can mitigate historical habitat degradation.

PHYLOGEOGRAPHIC PATTERNS IN MITOCHONDRIAL DNA OF THE DESERT TORTOISE (XEROBATES AGASSIZI), AND EVOLUTIONARY RELATIONSHIPS AMONG THE NORTH AMERICAN GOPHER TORTOISES.

Restriction-fragment polymorphisms in mitochondrial DNA (mtDNA) were used to evaluate population-genetic structure in the desert tortoise Xerobates agassizi and to clarify evolutionary affinities among species of the gopher tortoise complex. Fourteen informative endonucleases were employed to assay mtDNAs from 56 X. agassizi representing 22 locations throughout the species' range. The mtDNA genotypes observed were readily partitioned into three major phylogenetic assemblages, each with striking geographic orientation. Overall, the X. agassizi mtDNA genotypes typify a common phylogeographic pattern, in which broad genetic uniformity of populations is interrupted by geographic features that presumably have functioned as dispersal barriers. The geologic history of the Colorado River area, which includes extensive marine incursions, may account for the marked mtDNA divergence between eastern and western X. agassizi assemblages. In mtDNA comparisons among the four species of the gopher tortoise complex, both UPGMA and Wagner parsimony analysis strongly support the recognition of two distinct species groups previously suggested by traditional systematic approaches. Furthermore, the mtDNA data identify the eastern X. agassizi assemblage as the probable inceptive lineage of X. berlandieri. Results from both intra- and interspecific comparisons illustrate how clues to historical events may be present in the geographic structure of mtDNA phylogenies.