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Anders G.J. Rhodin, Craig B. Stanford, Peter Paul Van Dijk, Carla Eisemberg, Luca Luiselli, Russell A. Mittermeier, Rick Hudson, Brian D. Horne, Eric V. Goode, Gerald Kuchling, Andrew Walde, Ernst H.W. Baard, Kristin H. Berry, Albert Bertolero, Torsten E.G. Blanck, Roger Bour, Kurt A. Buhlmann, Linda J. Cayot, Sydney Collett, Andrea Currylow, Indraneil Das, Tomas Diagne, Joshua R. Ennen, Germán Forero-Medina, Matthew G. Frankel, Uwe Fritz, Gerardo García, J. Whitfield Gibbons, Paul M. Gibbons, Gong Shiping, Joko Guntoro, Margaretha D. Hofmeyr, John B. Iverson, A. Ross Kiester, Michael Lau, Dwight P. Lawson, Jeffrey E. Lovich, Edward O. Moll, Vivian P. Páez, Rosalinda Palomo-Ramos, Kalyar Platt, Steven G. Platt, Peter C.H. Pritchard, Hugh R. Quinn, Shahriar Caesar Rahman, Soary Tahafe Randrianjafizanaka, Jason Schaffer, Will Selman, H. Bradley Shaffer, Dionysius S.K. Sharma, Shi Haitao, Shailendra Singh, Ricky Spencer, Kahleana Stannard, Sarah Sutcliffe, Scott Thomson, Richard C. Vogt
We present a review and analysis of the conservation status and International Union for Conservation of Nature (IUCN) threat categories of all 360 currently recognized species of extant and recently extinct turtles and tortoises (Order Testudines). Our analysis is based on the 2018 IUCN Red List status of 251 listed species, augmented by provisional Red List assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group (TFTSG) of 109 currently unlisted species of tortoises and freshwater turtles, as well as re-assessments of several outdated IUCN Red List assessments. Of all recognized species of turtles and tortoises, this combined analysis indicates that 20.0% are Critically Endangered (CR), 35.3% are Critically Endangered or Endangered (CR+EN), and 51.9% are Threatened (CR+EN+Vulnerable). Adjusting for the potential threat levels of Data Deficient (DD) species indicates that 56.3% of all data-sufficient species are Threatened. We calculated percentages of imperiled species and modified Average Threat Levels (ATL; ranging from Least Concern = 1 to Extinct = 8) for various taxonomic and geographic groupings. Proportionally more species in the subfamily Geoemydinae (Asian members of the family Geoemydidae) are imperiled (74.2% CR+EN, 79.0% Threatened, 3.89 ATL) compared to other taxonomic groupings, but the families Podocnemididae, Testudinidae, and Trionychidae and the superfamily Chelonioidea (marine turtles of the families Cheloniidae and Dermochelyidae) also have high percentages of imperiled species and ATLs (42.9-50.0% CR+EN, 73.8-100.0% Threatened, 3.44-4.06 ATL). The subfamily Rhinoclemmydinae (Neotropical turtles of the family Geoemydidae) and the families Kinosternidae and Pelomedusidae have the lowest percentages of imperiled species and ATLs (0%-7.4% CR+EN, 7.4%-13.3% Threatened, 1.65-1.87 ATL). Turtles from Asia have the highest percentages of imperiled species (75.0% CR+EN, 83.0% Threatened, 3.98 ATL), significantly higher than predicted based on the regional species richness, due to much higher levels of exploitation in that geographic region. The family Testudinidae has the highest ATL (4.06) of all Testudines due to the extinction of several species of giant tortoises from Indian and Pacific Ocean islands since 1500 CE. The family Testudinidae also has an ATL higher than all other larger polytypic families (≥ 5 species) of Reptilia or Amphibia. The order Testudines is, on average, more imperiled than all other larger orders (≥ 20 species) of Reptilia, Amphibia, Mammalia, or Aves, but has percentages of CR+EN and Threatened species and an ATL (2.96) similar to those of Primates and Caudata (salamanders).
Mono- and bispecific genera are noteworthy compared with multispecies genera because they either may be evolutionarily older or would represent not-yet-diversified young lineages, and being in some cases endemic to specific islands and archipelagoes, they also are of conservation concern. Here, the distribution patterns of the mono- and bispecific genera of freshwater turtles and tortoises and the distribution patterns of island endemics are analyzed, using a database provided by the International Union for Conservation of Nature/Species Survival Commission Tortoise and Freshwater Turtle Specialist Group. The mean number of species per genus varied significantly across biogeographic regions. Twenty-eight genera are monospecific, and 18 are bispecific, accounting for 48.9% of the total genera of tortoises and freshwater turtles worldwide. The Oriental region housed the highest fraction of these genera, followed by the Neotropical and Afrotropical regions. More than 11% of the total number of chelonian species (n = 356) were island endemics, with most species being Neotropical. The majority of the endemic island species occurred in the Galapagos Islands and in Papua New Guinea. The endemism index varied remarkably among the various islands/archipelagoes, with the Philippines being the center of endemism with the minor value of the index and the Galapagos being that with the highest value of the index. Island size was correlated neither with the number of endemic species per island nor with the endemism index of each island, but it was significantly correlated with the total number of species (once the Galapagos were removed from analyses as an outlier). Species belonging to mono- and bispecific genera, as well as island endemic species, were more threatened (as a percentage; in all cases > 65%) than the overall percentage of threatened taxa in freshwater turtles and tortoises worldwide (50.3%).
Luis G. Fonseca, Pilar Santidrián Tomillo, Wilbert N. Villachica, Wagner M. Quirós, Marta Pesquero, Maike Heidemeyer, Frank Joyce, Pamela T. Plotkin, Jeffrey A. Seminoff, Eduardo R. Matarrita, Roldán A. Valverde
Here we report on a newly discovered nesting population of east Pacific green turtles (Chelonia mydas) in northwest Costa Rica at San José Island, Murcíelago Archipelago, that rivals those of Mexico and the Galápagos Islands, Ecuador. A total of 1232 individual green turtles were tagged over 4 nesting seasons (2012–2013 to 2015–2016). Mean (± SD) annual number of nests (1077 ± 414; range, 490-1698 nests) and females (306 ± 133; range, 164-466 females) was higher than those previously reported for Pacific Costa Rica. The number of deposited nests was similar to that registered on the Galápagos main beaches, but density of nests (number of nests/km) was the second highest for any green turtle beach in the eastern Pacific. Reproductive output was similar (mean clutch frequency: 4.4 ± 2.2 clutches and mean clutch size: 75.8 ± 14.6 eggs/clutch), and mean hatching success was higher (0.89 ± 0.14) than those reported at other sites in the eastern Pacific. Because the study site was located on an island within a protected area, several of the common threats that sea turtles face at more accessible mainland sites (i.e., egg poaching, tourist development, and predation by large mammals) were absent. Our data indicate that San José Island is the most important nesting site for east Pacific green turtles in Central America. The large size of this population, along with its isolated and protected status, suggest that this rookery is making a significant contribution to the conservation of east Pacific green turtles. Additional information at the country level will help determine the relative importance of Costa Rica for green turtle nesting in the broad eastern Pacific region.
Marine turtles are considered by people of several cultures to be a gift from God. This belief often leads to the use of these reptiles in the traditional and belief systems among aboriginal peoples. Certainly this is the case among Wayuú people, who are an indigenous group settled between Venezuela and Colombia, in the Guajira Peninsula. To assess the value of marine turtles to Wayuú ancestral people, especially as a medicinal resource, we carried out a comprehensive open-ended question-based survey of traditional healers and caretakers (locally known as Piaches and Oütsüs) from 4 Wayuú communities in the Venezuelan portion of the Guajira Peninsula. We documented customary practices where marine turtles' body parts are used as a key element of the remedies. Eleven marine turtle body parts were identified by respondents as remedies used by Wayuú people, with 7 different ways to administer them (drink, worn, powder, among others). Four of the 5 species of marine turtles present in Venezuelan waters were identified as being used in the traditional pharmacopoeia of Wayuú people; their traditional names are included on this article. Some considerations about the Wayuú's cosmovision, customs, traditions, and belief systems are included here. Our results are important in the context of likely future evaluation of the current Venezuelan legal framework to consider inclusion of traditional use of marine turtles in Venezuela.
Understanding the significance of a river reach to a particular species is critical for informing riverine restoration and management. Generally, the relative significance of a river reach for freshwater turtles is based upon population counts. However, capture rates can be greatly influenced by the methods employed, species behavior, localized in-stream conditions, and the operator's knowledge and skill. Here, we report on abundance shifts within freshwater turtle assemblages along a river continuum using a protocol that standardized the sampling effort. Turtle capture was undertaken at 20 study sites along the Mary River (Queensland, Australia), and repeated identically every 6 mo over a 2-yr period. A large funnel trap with a 30-m wingspan was deployed at each site and turtles were captured over a 4-d period. The turtle species assemblages significantly differed between the upper, mid, and lower catchments (multivariate analysis of variance, p < 0.05), suggesting species preference for the broad geomorphological and ecological features of each reach. The observed spatial variance in species assemblage was consistent over time and unaffected by the season, demonstrating that the assessment was repeatable and unaffected by individual species' life history patterns. We argue that trends in turtle species assemblage could be used instead of absolute species count data to alert natural resource managers to shifts in conditions and provide early warning signs of habitat degradation or management success. The technique is cheaper and easier to implement than abundance counts and ensures that capture biases remain constant under different conditions and operators.
Few studies document early growth of hatchling turtles. We fit growth models to 606 carapace length (CL) measurements of ornate box turtles (Terrapene ornata ornata) for 231 males, 226 females, and 53 individuals of undetermined sex. We used the Richards model to fit 95% confidence bands and 95% prediction bands on the best-fit curves for males and females. We also computed Spearman's rho correlation relating growth ring counts to CL and plotted change in CL for 131 recaptured individuals (45 males, 57 females, and 29 individuals of undetermined sex) for which we had two or more measurements from different years. There was a strong correlation between CL and number of growth rings. Using the properties of the derivative of Richards growth model, juvenile 1, juvenile 2, subadult, and adult stages were defined for male and female growth. Our overall growth models were similar to those for studies of ornate box turtles in Kansas and South Dakota and the desert box turtle (T. o. luteola) in New Mexico; however, our growth stages were defined by smaller turtles. Unlike a previous study in South Dakota, our adult males were larger than adult females. Prior to a CL of approximately 86 mm and 8 growth rings, the carapace grew faster than the plastron, after which the plastron grew faster than the carapace. Five hatchlings' plastra grew an average of 26% (SD = 14%) the first year and the carapace grew an average of 15% (SD = 7%). During the first 3 yrs, most individuals developed only one growth ring per year. If major growth rings approximate age, size can be used to estimate age in ornate box turtles up to 60–90 mm (about 8 growth rings). Between 8 and 12 growth rings, size and age are also correlated, but accuracy of age estimates decreases. Life-history traits such as age at reproductive maturation and size at which individuals are vulnerable to predation are important to assess long-term viability of a population; therefore, understanding environmental impacts on individual growth is important for conservation planning and management of this threatened species in Iowa.
Light pollution from beachfront hotels has the potential to impact nesting and hatching sea turtles. Education strategies could be used to alter visitor behavior and mitigate this threat. We tested the efficacy of a sea turtle–friendly education card that encouraged visitors to “protect the night, hide the light.” Cards were placed in beachfront hotel rooms at a prominent sea turtle nesting site: Jekyll Island, Georgia. We assessed visitor responses by conducting nightly observations to determine the proportion of occupied guest rooms with beach-visible lights under 2 different scenarios (cards present or cards absent). We found that less than half of all hotel guests closed room blinds to minimize artificial light on the nesting beach, and compliance rates seemed to be lower during peak visitation times. The nonpersonal educational treatment (card) had little effect on visitors' sea turtle–friendly lighting choices and behaviors, highlighting the need for other approaches to encourage responsible tourist behavior at ecologically sensitive beach destinations.
To address some of the threats facing sea turtles in St. Kitts, the St. Kitts Sea Turtle Monitoring Network (SKSTMN) has implemented a number of conservation education programs. The primary conservation education program has been an annual Sea Turtle Camp Program that was developed and initiated in 2007 with the goal of engaging and educating youth in the conservation of sea turtle species. In 2015 and 2016, the SKSTMN performed an assessment of this education program. The outcome assessment included 1) evaluation of pre- and postparticipation tests for the 2015 and 2016 participants, 2) comparison with a control group of nonparticipants who took the posttest, and 3) a survey of former participants and their parents or guardians. The pre/post exercise was performed to determine if students were gaining and retaining information during the Sea Turtle Camp Program and if participants had a stronger knowledge base than nonparticipants. The survey of former participants was performed to determine if this program had positively affected participants and their perceptions regarding sea turtles, the marine environment, and conservation; to ascertain strengths and weaknesses of the Sea Turtle Camp Program; and to identify conservation education areas that could be further developed. The results obtained for participants in the Sea Turtle Camp Program between the pre- and posttests indicated that the educational modalities used are successfully relaying the desired information and that the majority of the participants are retaining this information throughout the Sea Turtle Camp Program. Additionally, the results on the pre- and posttests for the Sea Turtle Camp Program participant group vs. the control group of nonparticipants indicate that the Program had a significant impact on participants' knowledge regarding sea turtle natural history, biology, and St. Kitts–specific sea turtle issues. Findings indicated that there were positive changes in behavior toward the marine environment and sea turtles in Sea Turtle Camp participants following participation and that there was a need for additional curriculum to be developed to accommodate former participants who were interested in continuing their participation in the program.
The reproductive cycles of turtles are linked to environmental factors, such as photoperiod and temperature. Currently, the reproductive physiology of diamondback terrapins (Malaclemys terrapin) is poorly understood, especially in Gulf of Mexico. The reproductive cycles of terrapins are thought to follow typical seasonal patterns. However, latitudinal variations in temperature regimens lead to longer-lasting warm periods, which can facilitate extended reproductive periods in some turtle species. This suggests that terrapins may show a similar change in the southern parts of their range. To elucidate aspects of the terrapin reproductive cycle, we sampled during the known reproductive season of a southern population of terrapins (May–July), as well as during the winter in late December and early January. We used enzymelinked immunosorbent assays to quantify concentrations of the plasma sex hormones estradiol and testosterone, and the egg yolk protein precursor vitellogenin. Additionally, we used radiography and ultrasonography to monitor the ovarian status and egg development in females. Follicles showed no significant difference in average diameter across sampling periods with preovulatory class follicles existing in both summer and winter. Eggs were only detected from May to July, with radiographic data showing second clutches in 4 individuals. Testosterone and estradiol showed elevated concentrations throughout the nesting season, coinciding with multiple clutches of eggs, before both showed a significant decrease in winter. Vitellogenin showed peak concentrations in June with other months showing lower but detectable concentrations. Our results suggest that in southwestern Florida, terrapins may have extended reproductive potential and continuous vitellogenic cycles given the presence of preovulatory follicles and high quantities of vitellogenin found in summer and winter. However, true continuous reproduction was not detected in this study.
Green turtles (Chelonia mydas) are observed year-round in the Sea of Jeju Island, Republic of Korea; however, there is limited information on their migration and seasonal distribution outside of Korean waters. To investigate their spatial and temporal movement, we tracked 8 green turtles (straight carapace length range, 49.7–85.9 cm; mean ± SD, 63.36 ± 10.99 cm), taken as bycatch in pound nets near Jeju Island, using satellite transmitters from August 2015 to January 2017. Turtles were mainly juveniles and were tracked for 17–314 d. Three turtles traveled more than 400 km from their release site in 2 different directions: one individual moved westward to China within 17 d of release, and 2 individuals traveled eastward to Japan. One turtle that moved to Japan had been flipper-tagged at Kagoshima, Japan, 1 mo prior to its capture at Jeju Island. The other 5 individuals remained near the coast of Jeju Island. The individual tracked for the longest period (314 d) overwintered (water temperature, 12°–14°C) in the eastern area of Jeju Island. These results indicate that green turtles from different regions, including China and Japan, may use the areas around Jeju Island for foraging, for overwintering, and/or as a migratory corridor. To fortify the conservation of green turtles in the region, international cooperation and expanded research efforts, such as genetic studies, are needed.
Many environmental variables that affect incubating turtle eggs in the nest may also affect hatchling development, following hatchling emergence. However, these effects may be subtle and are largely unexamined. In this study, we analyzed the effect of sand moisture content during incubation on the postemergence growth rates of loggerhead sea turtles (Caretta caretta) in southeastern Florida. We divided 10 clutches in halves, reburied them, and exposed them to 1 of 2 treatments. At emergence, 7 clutches met minimum criteria for inclusion in the study. One halfclutch received only ambient rainfall (“dry” treatment) while the other half-clutch received ambient rainfall plus daily watering (“wet” treatment). Data loggers were used to record incubation temperatures in both groups. Hatchlings were captured at emergence and laboratoryreared over a period of ∼ 3 mo. Mass, straight carapace length (SCL), and straight carapace width (SCW) were measured weekly to track growth. Initial measurements were larger for turtles from the wet nests in all metrics. Turtles from wet nests grew more in SCW than turtles from dry nests. Turtle growth from the 2 treatments did not differ in SCL or mass measurements. Larger initial sizes and faster SCW growth may enable the turtles to more quickly achieve a refuge size from their gape-limited predators. Moisture availability during nesting season is projected to decrease based on climate change models. If that change materializes, it could negatively affect hatchling sizes and neonate growth rates, survival, and hence the recovery of this imperiled species.
Sea turtle nest relocation is a management strategy commonly used to mitigate hatchling mortality, particularly that due to wave wash-over and tidal groundwater inundation. Relocation can alter the incubation environment, so there is concern regarding potential modifications to embryonic development. Several studies have explored the effects of relocation on nest productivity; however, these studies often only compare reproductive output and incubation environments between relocated and in situ nests without accounting for the incubating environment of the original nest location. We assessed the differences in sand temperature, inundation exposure, grain size, and moisture content between the original and final locations of relocated nests at a loggerhead (Caretta caretta) nesting beach in Fort Morgan, Alabama, as well as differences in nest productivity between in situ and relocated nests. Differences in mean sand temperature, likelihood of inundation, and sand moisture between original–relocated locations and in situ–relocated nests were not significant. Emergence success was significantly lower in relocated vs. in situ nests, and sand grain distributions were significantly different between original and relocated nest locations. Given that relocation did not improve nest productivity nor reduce the likelihood of inundation, this practice conferred minimal net benefit to sea turtle nests on dissipative-to-intermediate beach conditions typical of the northern Gulf of Mexico. To improve the justification for nest relocation under these beach conditions, a better understanding of embryonic tolerance to inundation and clarification of relocation criteria and guidelines is required.
Mammalian depredation of nests has been listed amongst the most significant threats to hatchling success in sea turtles. In 2013, at least 13% of green turtle (Chelonia mydas) and 25% of hawksbill turtle (Eretmochelys imbricata) nests were lost to domestic dog predation on Playa Norte, Costa Rica. In 2014 and 2015, plastic and bamboo protective screens were deployed to protect nests. Screens were deployed at different stages of the incubation period and the success of the nests analyzed. Predation rates increased as the seasons progressed with October and November being the peak depredation months, as well as the peak for hatchling emergences. Eggs remaining in nests that had been partially depredated had a significantly lower percentage of hatching success than eggs in undisturbed nests. There was no significant difference between timing of deployment and likelihood of a screen being breached. The likelihood of a screen being breached was highly dependent on the type of material used; bamboo screens were ca. 153% more effective than plastic and successfully prevented the complete predation of ca. 48% of nests. Bamboo screening is an inexpensive, environmentally inert, yet labor-intensive method for reducing nest depredation by domestic dogs. This screening method does not impact the hatching or emerging success of the nest.
The alligator snapping turtle (Macrochelys temminckii) is under consideration for listing as a federally endangered species. Distributional data and estimates of population sizes are needed to make a sound decision regarding listing, but this information is largely unavailable due to the immense effort required for M. temminckii trapping surveys. To alleviate difficulty in detection and to help inform subsequent field-intensive survey efforts, we developed an environmental DNA (eDNA) method capable of providing presence data even in systems with high turbidity and suspended organic material. The assay we developed utilizes probe-based quantitative polymerase chain reaction and reliably amplifies M. temminckii eDNA in both lentic and lotic systems, with no amplification observed in other nontarget, sympatric turtle species. The novel eDNA method developed, optimized, and field-tested in this study provides a promising tool for detection of alligator snapping turtles, with resultant presence data likely to prove beneficial for the management and conservation of this species.
We present a new record of freshwater turtle predation by the jaguar, Panthera onca, in addition to a current review of chelonian predation by this feline. In total, 16 species of chelonians were predated by jaguars: 3 were terrestrial, 8 freshwater, and 5 marine. Our review revealed that jaguars prey on a large number of chelonians, including heavily armored species, such as the Chelonoidis tortoises, and also small freshwater species.
Capture–mark–recapture and radiotelemetry was used in a population of the Mexican mud turtle (Kinosternon integrum) in the Pátzcuaro Basin. Calculated population size was 60 individuals. Sex ratio was skewed to females (1:4.75). Home range of the tracked females ranged from 0.08 to 2.7 ha and indicates a high fidelity with their aquatic and terrestrial microhabitats.
We used 454-sequencing to identify and characterize 32 microsatellite loci for the Western Hermann's tortoise (Testudo hermanni hermanni) for which primer sequences, characteristics, and multiplexes are provided. These markers have been tested for one continental (Var) and one insular (Corsica) French population as well as for the Eastern Hermann's tortoise (Testudo hermanni boettgeri). For these 3 populations, 24 loci were polymorphic. These microsatellite markers will be particularly useful to assess the genetic diversity and characteristics of the different Hermann's tortoise populations and will have direct applications for its protection, notably with respect to reintroduction and conservation programs.
We quantified boat traffic and measured frequency of scarring in 9 species of freshwater turtle at 5 sites in northeastern Oklahoma, and overall injury rates increased significantly with increases in boat traffic. One common species at all study sites, Graptemys ouachitensis, exhibited evidence of traumatic injury at a rate 1.5 times higher than the average among sympatric species. Across species, missing hind limbs were 2.4 times more common than missing forelimbs and carapace damage was 1.4 times more prevalent on the posterior half of the shell than the anterior half; we observed no left–to–right bias in the distribution of injuries.
We collected tissue samples from 41 nesting hawksbill turtles (Eretmochelys imbricata) at Sandy Point National Wildlife Refuge, St. Croix, US Virgin Islands, to characterize the genetic structure of this rookery in terms of mitochondrial DNA; we compared haplotype frequencies from this rookery to those from Buck Island, another hawksbill nesting beach on St. Croix. Pairwise FST comparisons showed that Sandy Point was demographically distinct from Buck Island (FST = 0.501, p < 0.001), a finding reinforced by significantly different haplotype frequencies (χ2 = 51.76, p < 0.001) and a lack of interchange of nesting females between both sites based on mark–recapture data. Our results support the delineation of the nesting populations at Sandy Point and Buck Island into separate units for the purposes of management.
During 2010–2018 we studied the relative abundance of invasive red–eared sliders (Trachemys scripta elegans) and native western pond turtles (Emys marmorata) at Clear Lake and its associated wetlands in Lake County, California, where T. s. elegans was first detected in 1968. Both species coexisted throughout the lake and its associated wetlands, but the proportion of T. s. elegans was significantly higher in the eastern arm of the lake (59% vs. 41%, n = 135) than in the northwestern arm (40% vs. 60%, n = 181) and, especially, the southeastern arm (10% vs. 90%, n = 31). Geographic differences in the proportions of the species were unrelated to the degree of urbanization and are presumably due to differences in the timing or frequency of T. s. elegans introductions in each arm of the lake.
Brian M. Shamblin, Matthew H. Godfrey, S. Michelle Pate, William P. Thompson, Hope Sutton, Jon Altman, Kristina Fair, Jeffrey McClary, Ann M. Wilson, Brooke Milligan, Edna J. Stetzar, Campbell J. Nairn
Green turtle nesting has been recorded in North Carolina, since 1980, but how these nesting females fit into the broader regional context genetically has not been determined. Genetic tagging through microsatellite genotyping of clutches laid in northern South Carolina, North Carolina, and Delaware from 2010 through 2014 identified at least 52 individual nesting females. The mitochondrial control region haplotype frequencies of these individuals were significantly different from all northern Greater Caribbean subpopulations, including those in Florida, suggesting that these northern US females represent an incipient subpopulation that warrants distinct management unit status.
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