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Noninvasive fecal genotyping can be a useful tool for population monitoring of elusive species. We tested extraction protocols on scat samples from the threatened Mojave Desert tortoise, Gopherus agassizii, to evaluate whether scat-based mark–recapture and population genetic monitoring studies are feasible.We extracted DNA from G. agassizii scat samples collected in California and Nevada using several extraction protocols and evaluated the reliability of resulting genotypes using quality scores, maximum likelihood reliability estimates, and paired scat and blood genotypes from the same individuals. Finally, we assessed probabilities of identity and sibship, and locus amplification quality, and calculated genotyping error rates for 19 microsatellite loci to determine the best set of loci to use with G. agassizii scat extractions. We found that genotype quality depended more on the sample quality than on the extraction method, and that the Qiagen DNeasy Plant Mini extraction kit is an efficient method for extracting tortoise DNA from tortoise scat. We identified 6 G. agassizii microsatellite loci that can be used to generate a unique molecular tag for individual tortoises. We characterized the reliability of an additional 13 microsatellite loci for use in population genetic analyses where additional power at the expense of some increase in error may be advantageous. As proof of concept, with very low error rates, we matched 3 opportunistically collected scat samples to blood genotypes from animals captured during population surveys within the study area and discovered at least 3 new individuals, even after 2 yrs of extensive survey work. These results suggest that genotyping of field-collected scat can complement existing methods used in long-term demographic and movement studies of G. agassizii and other, closely related, tortoise species.
Animals are tracked using a wide range of methods. Some researchers track animals by manually recording global positioning system locations while others combine manually recorded locations with sophisticated mapping software. Individuals of the public regularly come in contact with animals and, as citizen-scientists, may represent a relatively constant source of data for researchers through written forms, web maps, or smartphone applications. We collected hawksbill (Eretmochelys imbricata) sightings from citizen-scientists using a new geographic information systems web map and smartphone application, and then calculated home ranges of individual turtles to gain insights into hawksbill movements within a marine protected area in Roatán, Honduras. We found that 3 of 4 individual turtles had home ranges of less than 1 km2 within the West Bay and West End zones of the marine protected area, whereas the fourth turtle had a home range of 1.44 km2 that extended from West Bay to Sandy Bay. We also found significantly more prey sponge in the West Bay and West End zones than in the Sandy Bay zone and suggest the small home ranges of hawksbills in our study may be due to the abundance of prey sponges within the Sandy Bay West End Marine Reserve. This study is the first to use citizenscience data collected via web-based and smartphone geographic information systems software to identify sea turtle home ranges. Our results correspond well to prior home range estimations derived using very high frequency radio telemetry. Although we analyzed small-scale home ranges for hawksbill sea turtles using citizen-based data, this method may potentially be applied around the world to any animals with home ranges.
Metabolic heating caused by physiological processes during the development of oviparous embryos can raise nest temperatures above those of the surrounding substrate and may be sufficient to increase embryonic growth rates, influence sex ratios of hatchlings with temperature-dependent sex determination, and increase hatching success in seasonal environments. In sea turtles with large clutch sizes, metabolic heating can raise nest temperatures by as much as 6°C. However, no studies have directly investigated metabolic heating in any species of freshwater turtle. We investigated whether metabolic heating occurs in nests of snapping turtles (Chelydra serpentina) from southeastern Michigan, United States. A temperature logger was placed in the center of 8 unaltered snapping turtle nests. A second temperature logger was placed at the same depth in the surrounding substrate 5 cm from the side of the nest chamber. Metabolic heating is more pronounced in nests with larger clutches, so we artificially increased the size of 2 additional nests using donor clutches of 11 and 21 eggs, respectively. Temperatures were recorded at 2-hr intervals until after the presumptive hatch date of all nests. We found that there was a significant increase both in mean nest temperature and accumulated heat units for natural and experimental treatment nests during the last third of incubation. Further, in nests with experimentally increased clutch sizes, mean nest temperature was significantly greater than substrate temperature throughout incubation, suggesting that large nests also exhibit a thermal inertia that results in positive heat balance throughout development, at least in the soils studied.
Bonnie L. Raphael, Suzanne K. Macey, Steven G. Platt, Tracie A. Seimon, Robert J. Ossiboff, Brian D. Horne, Ariana L. Gamarra, Michelle G. Barrera, Tint Lwin, Me Me Soe, Shwe Htay Aung, San San New, Lay Lay Khaing, Kalyar Platt
The once abundant Burmese star tortoise (Geochelone platynota) was functionally extirpated from Myanmar largely due to exploitation for wildlife trade markets. Geochelone platynota is endemic to the dry zone of central Myanmar, a desert-like region formed by the rain shadow of the western mountains. To prevent biological extinction, ex situ captive assurance colonies were established and a captive breeding program was initiated. Three major assurance colonies of Burmese star tortoises in Myanmar produced approximately > 14,000 individuals between 2004 and 2018. In 2013 and 2014, the Wildlife Conservation Society, Turtle Survival Alliance, and Myanmar Forestry Department performed health assessments on 539 tortoises prior to reintroduction. Tortoises were negative by polymerase chain reaction for the presence of Mycoplasma spp., ranavirus, herpesvirus, and the intranuclear coccidian parasite of Testudines. Results from hematologic assessment of all study tortoises were consistent with published data on other species of healthy tortoises. Such health assessments, including physical examination, hematologic analysis and molecular pathogen screening, are important to generate baseline information about potential circulating organisms or pathogens. Additionally, health assessments ensure the success of repatriation projects by both assuring that potential pathogens associated with disease are not inadvertently introduced into the wild, and that individuals slated for release are healthy enough to weather the rigors of reintroduction.
Urban coastal ecosystems are unique intersections of human development and biodiversity, and monitoring populations in these areas is critical to understanding ecosystem health and function. Three highly urbanized estuary systems, San Diego Bay, San Gabriel River, and Seal Beach National Wildlife Refuge (all in California), are the northernmost foraging habitats for green turtles (Chelonia mydas) in the Eastern Pacific. Here, we report blood biochemistry and morphological parameters for these Southern California green sea turtle foraging aggregations to investigate the current health status of these animals and provide baseline values for future work. Morphometric and blood biochemistry parameters for green turtles captured in this study (n = 39) were clinically reasonable and were generally consistent with previously reported parameters for green turtles.
A priority for sea turtle conservation is the identification of early biomarkers of environmental perturbation effects on the health of populations. The micronucleus (MN) assay is a noninvasive, sensitive, and economical in vivo assay for the determination of genotoxicity. It could help in ecotoxicological studies to determine if genotoxic chemicals are present in the environment and examine the chronic exposure of wildlife. The sample preparation protocol required to perform the MN assay in sea turtle peripheral blood is presented. The optimal times to fix (ethanol 80%) and stain (acridine orange) air-dried blood smears were evaluated. Acridine orange was used at a concentration of 0.01 g/100 ml in phosphate buffer (pH 7.4). MN and nuclear bud (NBUD) frequencies were determined in 1000 erythrocytes of free-ranging green sea turtles (Chelonia mydas) by using the species-specific developed protocol. The number of nuclear abnormalities in immature green turtles that inhabited 2 feeding grounds in the Mexican Caribbean was 0–17 NBUDs/1000 erythrocytes, and only 1 MN/1000 erythrocytes was detected in a single sea turtle specimen. Green turtles from the touristic and urbanized site presented a larger frequency of nuclear abnormalities (50%) than the value observed in the reference group. This protocol generates optimal results in a simple manner, and it is specific to validate and determine the frequency of spontaneous micronucleated erythrocytes in sea turtle peripheral blood. The preliminary results suggest the potential utility of the MN assay as biomarker of genotoxicity in sea turtles.
The Rio Grande cooter (Pseudemys gorzugi), the westernmost species of the genus Pseudemys, is a riverine turtle native to the lower Rio Grande River basin and its tributaries. Currently, P. gorzugi is under review by the US Fish and Wildlife Service for federal protection. However, very little is known about any aspect of this species' ecology and natural history, posing challenges to the assessment of its conservation status. To fill in these knowledge gaps, we studied female size at maturity, clutch size and mean egg size, correlation between reproductive output and female size, and reproductive seasonality of P. gorzugi from mid-May to mid-August 2018. We captured P. gorzugi on the Black River, New Mexico, using traditional hoop net traps and snorkeling. Of 155 females, 28 contained oviductal follicles and 16 contained shelled eggs. We observed a high proportion of gravid females at the end of May through mid-June, although the egg development cycle may extend into August. Our findings allow for a better understanding of this poorly studied species. Knowledge on seasonality of egg development and deposition can aid management planners in determining appropriate times for implementing protection for nesting females and nesting sites.
Mesoclemmys raniceps is a medium-sized aquatic turtle widely distributed throughout the northern Amazon Basin in South America. Little information has been published about its reproductive biology. Because there is a significant problem identifying juveniles of this species found in the wild, and a controversy concerning the taxonomic status of the Mesoclemmys nasuta group, we incubated eggs from known females from known localities at controlled and ambient temperatures. We describe the hatchlings produced. The eggs hatched after an incubation period of 249 d at 28°C. Incubation experiments found both M. raniceps and Mesoclemmys heliostemma phenotypes hatching from the same clutch of eggs, suggesting that these taxa are conspecific. Mesoclemmys wermuthi had been incorrectly synonymized with M. nasuta and later absorbed by M. raniceps when M. raniceps was elevated to species status, resulting in the confusion of M. raniceps being different from M. heliostemma. Mesolemmys wermuthi is a distinct species separate from M. raniceps; however, M. wermuthi is preceded by Hydraspis maculata, which was synonymized with M. raniceps and is available for this species as Mesoclemmys maculata.
Conserving and managing an imperiled species, such as Testudo hermanni, requires information on population status and demographic traits. To acquire this information, we surveyed Hermann's tortoises, Testudo hermanni boettgeri, in European Turkey from April to October 2014–2016. We found 283 (135 males, 102 females, 45 juveniles, and 1 unknown) T. h. boettgeri at 34 locations. Of these sites, 29% included at least 1 individual. We found that females were larger and heavier (mean straight carapace length [SCL] = 175.4 mm, body mass = 1234.1 g) than males (SCL = 153.2 mm, body mass = 849.6 g). The age frequency had a normal Gaussian distribution with 11–15 yrs being the most common. Elevation at capture sites ranged from 22 to 380 m above sea level. Illegal overharvesting for the pet trade appears to have caused no reduction in body size.
Marine turtles often conduct extensive migrations from foraging to breeding habitats. Turtles may spend several months in these breeding habitats, while periodically taking brief excursions onto terrestrial environments to nest. Identification and protection of these breeding habitats over the duration of the reproductive season is therefore vital for the conservation of sea turtles. Here, we used satellite telemetry to investigate the internesting behavior of East Pacific green turtles from 2 nesting beaches: Nombre de Jesús and Playa Cabuyal, located 50 km apart on the Pacific coast of Costa Rica. A total of 21 satellite transmitters were deployed at Nombre de Jesús (n = 8) between 2007 and 2009 and at Cabuyal (n = 13) between 2012 and 2015. We found that turtle movements and dive behaviors were notably different between the 2 beaches. Specifically, the turtles from Cabuyal engaged in deeper dives (10 ±3 m vs. 6.5 ±2 m [mean ±SD]), presumably because they had access to deeper waters, and had larger minimum convex polygon area (606.5 ± 1150.5 km2 vs. 16 ± 11 km2) than turtles from Nombre De Jesús. Turtles from Nombre de Jesús also engaged in shorter dives (6.68 ± 4.5 min), compared with Cabuyal, where a majority of dives lasted between 10 and 30 min (18.75 ± 5.6 min). Finally, turtles at Nombre de Jesús dove significantly deeper during the day compared with the night, a pattern that was not present at Cabuyal. We conclude that internesting behaviors can be different even between beaches within the same geographical area. As such, internesting habitat management plans should pay specific attention to potential site-specific variation in internesting behaviors.
Road networks threaten biodiversity and particularly herpetofauna, including common snapping turtles (Chelydra serpentina), which have an especially slow life history that prevents rapid recovery of populations subjected to road mortality. Cootes Drive is a 2.5-km 4-lane highway that bisects wetland habitat used for nesting and overwintering by snapping turtles. We hypothesized that turtle mortality from collisions with vehicles on Cootes Drive has caused a male bias and a decline in the population as turtles attempt to access habitat on both sides of the road. Capture–mark–recapture studies confirmed a dramatic decline in the turtle population from 941 individuals in 1985 to 177 individuals in 2002, a loss of 764 individuals in only 17 yrs. Using the same data, we also determined that the population has been significantly male-biased since 1985. Using 2009–2016 road mortality data obtained from the Dundas Turtle Watch (a citizen-science program), we completed a population viability analysis using the 2002 population size estimate to isolate the impact of road mortality. We found that this population is at risk of extirpation due to road mortality. The population range overlapped with the Cootes Drive and 7 of the 10 tracked turtles had individual home ranges that overlapped with the road. Our findings support the hypothesis that road mortality has contributed to the dramatic decline in the snapping turtle population in Cootes Paradise Marsh. This population is in jeopardy of extirpation; therefore, exclusion fencing must be installed for an extended distance along both sides of surrounding roads to prevent turtles from crossing the road and to promote their use of existing aquatic culverts.
Leatherback sea turtles (Dermochelys coriacea) are listed as Vulnerable globally by the International Union for Conservation of Nature. To preserve this species, we must protect them during several life stages, including protecting hatchlings emerging from nests. We studied the timing of emergence of leatherback hatchlings at Sandy Point National Wildlife Refuge, an area created for the protection of this species. We surveyed 524 nests in 2010–2014 and evaluated the time that hatchlings began emerging from the surface of the sand, the time that the last hatchling in the group finished emerging from the sand, the incubation duration of each nest (number of days between deposition and first emergence), and the number of hatchlings in the initial pulse of emergence. In situ clutches (those occurring naturally and not manipulated by location) had an incubation period of 61.4 ± 21.1 d (mean ± SD; n = 332) and emerged from 1825 to 1906 hrs. The incubation duration varied significantly from relocated clutches (those that had been moved at deposition because of erosion threats), had an incubation period of 60.0 ± 2.7 days (n = 192), and emerged from 1827 to 1903 hrs (on average, for all years combined; p < 0.0001). These nests yielded 36.6 ± 21.1 first-emergence hatchlings from in situ clutches, which was different from relocated clutches (14.9 ± 13.6 first-emergence; p < 0.0001). Other studies have found that hard-shelled sea turtles all begin emerging once the sun sets and continue emerging throughout the night. In contrast, we found that leatherback sea turtle hatchlings emerge earlier in the evening, at least at Sandy Point. During the seasons sampled, emergence often began before sunset (between 1834 and 1859 hrs) and hatchlings usually did not continue to emerge through the night. To allocate resources most effectively, beach management programs at Sandy Point National Wildlife Refuge should be maximized between 1700 and 2000 hrs, the period when most hatchlings are emerging and require the most protection from predators. This work provides important information about the timing of leatherback emergence and may be applicable to other leatherback nesting beaches where predation may be a problem. These findings can help ensure that nest protection programs maintain efficiency and protect hatchlings during their vulnerable crawl to the sea.
Edson Soares da Silva-Júnior, Daniel Solon Dias de Farias, Aline da Costa Bomfim, Augusto Carlos da Boaviagem Freire, Rafael Ângelo Revorêdo, Silmara Rossi, Eliana Reiko Matushima, José Henrique Hildebrand Grisi-Filho, Flávio José de Lima Silva, Simone Almeida Gavilan
Fibropapillomatosis is a threat to the survival of marine turtles, especially green turtles; therefore, studies on this neoplastic disease are considered a conservation priority. Our goal was to characterize the incidence and spatial–temporal distribution of fibropapillomatosis in the Potiguar Basin, Rio Grande do Norte and Ceará states, Brazil. This study was based on data obtained during daily observations by a beach monitoring program from 2012 to 2015. A total of 2688 marine turtles, comprising the 5 species that occur in the Brazilian coast, were observed; 604 of the 610 individuals that presented fibropapillomatosis tumors were green turtles (Chelonia mydas). During the study period, we identified an increase in relative fibropapillomatosis frequency from 13.16% (2012) to 35.29% (2015), with a yearly peak in strandings between October and December. Fibropapillomatosis tumors were classified according to anatomical distribution, size, and the Southwest Atlantic Fibropapillomatosis Score (e.g., mild, moderate, and severe). The total number of tumors varied from 1 to 67; most were classified as size B and mild and were located mainly on the forelimbs and neck (49.63 and 25.95%, respectively). Our study shows the need to implement mitigation measures to promote sea turtle conservation in the Potiguar Basin, an important area for marine turtles in Brazil.
We present survey data on one of the rarest turtles in the world, the Nubian flapshell turtle, Cyclanorbis elegans, on the basis of data coming from structured interviews with Bari fishermen of South Sudan and comparison of these data with those coming from our field studies. Our study documented that local ecological knowledge (LEK) data can be very useful to complement information on the natural history of rare and poorly known species and helpful to their conservation and management. We urge that any protected area focusing on C. elegans include a few of their communal nesting areas (as described by LEK) that should be carefully monitored to prevent collection of females or eggs during the reproductive period.
We conducted physical examinations of 8 green turtles (Chelonia mydas) with boat strike injuries caught repeatedly near Mabul Island (lat 4.246°N, long 118.630°E), Malaysia, where 1 adult female showed evidence of newly recorded injuries in every capture. The healing progress of boat strike injuries on this turtle and 7 other green turtles of various size classes with similar injuries was documented through repetitive captures from between August 2010 and November 2017. We provide the first report of its kind on the incidence of newly documented boat strike injuries on repeatedly captured wild green turtles at their foraging ground.
Recordings were made in nests of Eretmochelys imbricata and 107 samples of 10-min recordings revealed 575 sounds that were classified manually into 4 categories. Our results show that hawksbill turtles vocalize within the nest, especially during and after eclosion, which suggests vocalizations are important for communication among hatchlings to synchronize emergence from the nest.
Recent studies have shown that acoustic signals play an important role in turtle social behavior and reproduction. We recorded embryos and hatchlings of Lepidochelys kempii inside the nest and underwater in June 2016 in Playa Santander, Veracruz, Mexico, and detected 189 sounds that were classified into 6 types according to their aural and spectral characteristics. Our results show that acoustic communication appears to be widely used in all species of sea turtles in aquatic environments, probably because of the high efficiency of this signaling modality in water compared with air.
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