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Descriptionsof the developmental stages of embryonic marine turtles are presented in the form of a dichotomous key supported by drawings to facilitate identifying stages of development in the field. The key emphasizes the sequential appearance or loss of external morphological structures that can be seen either with the unaided eye or with a ×10 hand lens and a handheld light. Stages are placed in the context of normal beach temperatures to facilitate estimation of laying date, emergence date, and events that cause embryonic mortality. Measurements of embryos are presented to assist determining stage.
The giant South American river turtle (Podocnemis expansa) is the largest extant member of the suborder Pleurodira and the largest freshwater chelonian in South America. Owing to its size, its meat is sought for consumption and trade in the Amazon region. The aim of the present study was to investigate the reproductive behavior of 2 different populations of P. expansa. Allelic frequency variation was studied in 6 DNA microsatellite loci of recently hatched offspring from 8 nests on a beach in the municipality of Oriximiná in the state of Pará, Brazil. Multiple paternity was identified in all nests studied. Between 5 and 10 fathers contributed to each nest. Compared with previous studies, a greater frequency of multiple paternity and a greater number of fathers contributing to each nest were found in the present investigation. The results suggest that populations from different locations may exhibit different paternity patterns due to ecological or biological differences. By comparison with previous studies, we suggest that the differences in the number of nests, proportion of offspring per nest, and number of loci analyzed in each study may influence the frequency of multiple paternity detected.
Maria das Neves S. Viana, Jessica dos Anjos Oliveira, Maria Augusta Paes Agostini, José Erickson, Giovanne Matias de Morais, Luiz Alberto dos Santos Monjeló, Paulo César M. Andrade, Daniely Félix-Silva, Waldesse Piragé de Oliveira Júnior, Jack W. Sites,, Richard C. Vogt, Tomas Hrbek, Izeni Pires Farias
Podocnemis sextuberculata (Pleurodira: Podocnemididae) is widely distributed throughout the Amazon drainage basin in Brazil, Colombia, and Peru. Telemetry and previous molecular data suggest that P. sextuberculata lacks population structure in the central Amazon basin of Brazil. Generalization of these results, however, requires much-broader sampling across a range of habitats of this broadly distributed species. For this reason, we tested the hypothesis of panmixia in P. sextuberculata, analyzing a total of 319 specimens sequenced for the mitochondrial control region. Our sampling included localities from 16 areas in the Amazon basin from rivers characteristic of the Amazon basin (whitewater), clearwater rivers of the Guiana shield (Branco, Trombetas, and Nhamundá rivers), and the Brazilian shield (Xingu River). The hypothesis of panmixia was rejected because the results of analysis of molecular variance, pairwise ФST, and Bayesian analysis of population structure indicated population structure in the group of individuals from the locality of Xingu which was not correlated to a pattern of isolation by distance. We suggest that the populations of P. sextuberculata of the Brazilian Amazon basin are composed of 2 management units, one represented by populations restricted to the Xingu River and the other represented by all other populations. The population of the Xingu should be viewed with attention and concern, especially considering the direct and indirect impacts of damming the Xingu River.
Connie Ka Yan Ng, Peter H. Dutton, He Xiang Gu, Tsung Hsien Li, Ming Bin Ye, Zhong Rong Xia, Fei Yan Zhang, Jin Xia Duan, Chung Kang Hsu, George H. Balazs, Margaret B. Murphy
Sea turtles are globally endangered and face anthropogenic threats, such as direct harvest, bycatch, and habitat degradation. Genetic studies help identify connectivity between nesting and foraging grounds for conservation and management. However, information on genetic stock composition of green turtles (Chelonia mydas) in the South China Region (including Hong Kong, Guangdong Province, and Taiwan) is severely limited. In this study, mixed stock analysis based on the 760-bp mitochondrial DNA (mtDNA) control region of green turtles (n = 110) revealed that the primary source rookeries in the Pacific contributing to foraging green turtle aggregations in the South China Region were Peninsular Malaysia, Yap in the Federated States of Micronesia, Aru of Indonesia, Sulu Sea, northeastern Borneo, Republic of Marshall Islands, Wan-an of Taiwan, and the central Ryukyu and Yaeyama of Japan. This study is the first to investigate and report the source nesting populations of a relatively large number of foraging green turtles in the region. The genetic results also indicate possible use of coastal Guangdong, the Taiwan Strait, and the East China Sea as habitat by pelagic-phase green turtles hatched from nesting beaches in Taiwan and mainland China. As a precautionary approach for effective sea turtle conservation, conservation and management of each distinct green turtle source rookery as well as foraging aggregations sourced from multiple natal origins in the South China Region is needed to preserve genetic diversity for the species. Anthropogenic threats to nesting and foraging habitats and migratory pathways, such as direct take for trade and fishery impacts, should be thoroughly assessed and effectively mitigated by regional collaboration to sustain these populations.
Cheloniamydas in temperate areas exhibits behavioral changes for adapting to sea temperature fluctuations; however, prolonged exposure to cold temperatures can lead to hypothermia and thus hypothermic stunning events. Here we report an unusual stranding event of 90 green turtles recorded in a 12-d period in July 2012 in southeastern Uruguay, analyzing the event in an oceanographic and meteorological context. Monitoring such events provides a unique opportunity to understand the impact of hypothermic stunning on juvenile green turtle stocks that spend the entire year in this temperate region of the southwestern Atlantic Ocean.
Knowledge of species-specific patterns of energy use is important for understanding the evolution of life histories as well as for determining how species might respond to alterations in environmental conditions. We measured standard metabolic rates (SMRs) in 59 Eastern Box Turtles (mass range = 106−510 g) and determined how differences in body mass and body temperature (20°C vs. 30°C) influenced SMRs. Rates of standard metabolism were significantly influenced by body mass at body temperatures of 20°C and 30°C and SMR was significantly higher at 30°C (Q10 = 3.04). There was significant among-individual variation in SMR and individuals with higher metabolism at 20°C also tended to have higher metabolism at 30°C.
Understanding reproductive biology and embryonic development is vital to guide conservation programs for endangered species. The Red-footed Tortoise, Chelonoidis carbonarius, is a vulnerable species for which the sex determination mechanism and the transitional temperatures range are unknown. In an attempt to obtain this information, we incubated 145 eggs (38 nests) at 3 constant temperatures: 29°C, 31°C, and 33°C. All embryos incubated at 33°C (n = 49) died during the first third of the incubation period. Of the eggs incubated at 31°C (n = 47), only 10.6% hatched, and 2.12% of the embryos showed malformations of the carapace, head, or legs. Of the eggs incubated at 29°C (n = 49), 52% hatched successfully with 10.2% exhibiting body malformations. From the 30 neonates obtained, we were able to sex 20 individuals by laparoscopies, 2 by gonads histology, 1 was impossible to identify because of the small sizes of the gonads at the time of death, and the remaining were released back to their tortoise origin of collection without being sexed. These results suggest that C. carbonarius exhibits a temperature-dependent sex determination mechanism with females produced at, or above, 29°C. Our incidental findings of embryo malformations, asynchronous hatching, and incomplete yolk absorption suggest that this species may be able to arrest embryonic development via embryonic diapause, aestivation, or both. Future studies should focus on the developmental biology of this species including confirmation of the production of males at temperatures below 29°C.
Ectothermic species are strongly affected by thermal changes. To assess the viability of these species under climate change constraints, we need to quantify the sensitivity of their life history traits to temperature. The loggerhead marine turtle (Caretta caretta) nests regularly in the Oriental Basin of the Mediterranean Sea. The different populations are separated because of time (< 12,000 yrs) and very different thermal habitats; it is hotter on the southern coast (Libya) than on the northern ones (Cyprus, Greece, and Turkey). Patterns of embryo growth response to incubation temperatures have been searched for these 2 populations. We found that both populations have similar thermal reaction norms for embryonic growth rate. This highlights that 12,000 yrs is not enough time for this species to adapt to specific thermal habitats and raises the question of the persistence of these populations in the context of rapid climate change.
We studied the sexual dimorphism in body size and shape of Beal's eyed turtle, Sacalia bealei, by measuring 15 morphological characteristics of 68 adult individuals (40 females, 28 males) collected from Fujian Province, China. Females were slightly larger than males in carapace length with a sexual dimorphism index of 0.09. This translated into greater absolute values of females for all the traits we measured except for tail length, preanal tail length, and analia to supracaudal junction length. Comparisons between the sexes of size-corrected morphological traits indicated that females exhibited a longer plastron and higher carapace relative to carapace length, thereby providing a larger internal volume. Females also exhibited relatively wider heads. In males, the plastron was smaller and more indented than in females and the openings between the plastron and the carapace were also more developed. Overall, females were larger in size and displayed a more voluminous shell than did males while males had longer tails and larger spaces available to move the legs, head, and tail.
Many marine organisms (invertebrates, fishes) produce large numbers of small offspring (larvae) that differ in appearance and behavior from adults. That outcome occurs because larvae as they grow occupy one or more ontogenetic niches that select for phenotypes that differ from those that promote adult survival. Our purpose in this study was to determine whether similar associations also occur in marine turtles. To find out, we examined relationships between juvenile appearance (body shape) and the ontogenetic niches occupied by 3 species of marine turtles: leatherbacks (Dermochelys coriacea) and 2 cheloniids (green turtles, Chelonia mydas; loggerheads, Caretta caretta). Our measurements indicate that juvenile body shape differs the least from adult body shape in leatherbacks and the most from adults in the 2 cheloniid species. We present evidence from other studies showing that juvenile leatherbacks occupy ontogenetic niches that resemble adult niches, whereas during their ontogeny, both juvenile green turtles and loggerheads make radical niche shifts as they transition between oceanic and neritic habitats. These results are thus consistent with the hypothesis that many morphological and behavioral characteristics expressed by juvenile marine turtles, like those of other larval forms, are best understood as evolved responses shaped by the characteristics of their ontogenetic niches.
Nest-site selection by most turtles affects the survival of females and their offspring. Although bog turtles (Glyptemys muhlenbergii) do not typically leave their wetlands for nesting, nest-site selection can impact hatching success and hatchling survival. Between 1974 and 2012, we monitored the fates of 258 bog turtle eggs incubated in the field and 91 eggs incubated under laboratory conditions from 11 different bogs, fens, or wetland complexes in New Jersey and Pennsylvania. Laboratory-incubated eggs exhibited the greatest hatching success (81%), but we did not detect a significant difference in hatching success between nests protected with predator excluder cages (43%) and unprotected nests (33%). However, we found significantly lower predation rates in protected nests, suggesting that while predator excluder cages successfully reduced predation, other environmental factors persisted to reduce egg survival in the field. Natural hatching success was potentially reduced by poor weather conditions, which may have resulted in embryo developmental problems, dehydration, or embryos drowning in the egg. Our results suggest that egg depredation, coupled with embryo developmental problems and infertility, are limiting factors to hatching success in our study populations. Using predator excluder cages to protect bog turtle eggs in the field, or incubating eggs in the laboratory and releasing hatchlings at original nesting areas, may be an effective conservation tool for recovering populations of this federally threatened species.
Characterizing variation in reproductive output is foundational to understanding the demography of a population and determining management strategies. Doing so is paramount when the species of interest is threatened with extinction. The red-crowned roofed turtle (Batagur kachuga) and the three-striped roofed turtle (Batagur dhongoka) are severely threatened by overharvesting and habitat loss. Despite their imperiled status, there are very few published studies on species ecology and life history to enable effective conservation; the 3 published studies that are available were completed nearly 3 decades ago. We herein provide information on variation in reproductive output for these turtles in the Chambal River of North India. Generalized linear models and analyses of variance were fitted to data on nesting density, fecundity, and egg volume. The number of nests showed an overall decline across 3 seasons (2007, 2008, and 2010) over a 4-yr duration with the highest number of nests observed in the middle of each nesting season. Peak nesting activity potentially occurs at lowest river depth or maximum availability of nesting habitat. The observed decline in the number of nests could be related to a decline in the nesting cohort or a geographic shift in suitable nesting habitat or changes in food resource availability and/or acquisition, leading to fewer females nesting. The number of nests in B. kachuga were significantly negatively correlated with total precipitation in the immediately preceding year. Presumably, total precipitation may affect the amount of nesting habitat available or availability of some other limiting resource. Reproductive output in both species varied as a function of fecundity rather than egg volume, implying that maturity occurs at larger body sizes for egg volume to be unconstrained, which would require relatively long generation times. Variation in clutch size could be tied to variable resource acquisition patterns, although total precipitation was not found to be an appropriate proxy. Potential variation in fecundity as a function of body size was not accounted for in the study. The study corroborated previous findings that B. kachuga lays larger and fewer eggs than B. dhongoka. These results contribute to understanding the life history of these poorly documented turtle species and toward informing conservation actions. Future studies over a larger spatial extent need to characterize nesting sites and nest-site fidelity and incorporate data from individual females.
KEYWORDS: Reptilia, Testudines, Emydidae, Graptemys oculifera, population sizes, trapping success, basking counts, sex ratios, survivorship, longevity, realized population growth, Pearl River, Mississippi
Effective management of long-lived species requires demographic and life-history data that are best acquired from long-term studies. The ringed sawback (Graptemys oculifera), endemic to the Pearl River watershed of Mississippi and Louisiana, is a species of management concern at both the state and federal levels. Population sizes, trapping success, basking counts, sex ratios, survivorship, and growth of this species were investigated at 5 sites on the Pearl River in Mississippi over a 25-yr period. Estimates of age at maturity were 4.6 yrs for males and 9.1 yrs for females. Mean annual survivorship estimates for males, females, and juveniles were 0.88, 0.93, and 0.69, respectively. Maximum longevity estimates were 48.8 yrs for males and 76.4 yrs for females. Average longevity estimates were 8.5 yrs for males and 13.9 yrs for females. The sex ratio of captured turtles was male-biased before 2000 but unbiased after 2000. Realized population growth estimates indicated that 4 populations were stable over the 25-yr period and 1 population had declined. Population estimates and basking counts trended downward through time at most sites. Trapping success after 2000 for all sites combined declined by 77%, 45%, and 25% for juveniles, males, and females, respectively. Taken together, these data indicate that 1 population of G. oculifera has declined, 3 appear to be in the initial stages of decline, and 1 is relatively stable. Additional monitoring of these populations will be necessary to determine if these trends continue into the future.
Turtles are highly susceptible to the negative effects of commercial harvesting. In October 2007, the Maryland Department of Natural Resources convened a Working Group to discuss the snapping turtle (Chelydra serpentina) fishery in Maryland and to make recommendations considered necessary to maintain a sustainable fishery. We collected information on population structure and the collecting techniques used by local harvesters in the field. An increase in the minimum legal size limit from 9.5 inches (24.1 cm) in 2008 to 11 inches (27.9 cm) in 2009 resulted in more females being protected from harvesting yet significantly decreased catch per unit effort, forcing harvesters to increase collecting effort to maintain catch levels.
The present study is the first to report the diet of 2 sympatric turtle species, Cuora mouhotii and Cuora galbinifrons. In Diaoluoshan Natural Reserve in Hainan Province, China, both species were observed to have an omnivorous diet; however, the composition of the diets was different between the species. The diet of C. mouhotii consisted of fungi, plants, earthworms, land snails, and insects, whereas the diet of C. galbinifrons included fungi, plants, earthworms, and lepidopterous larvae.
Recently, 2 studies almost simultaneously described the same previously unrecognized species of semiaquatic Southeast Asian snail-eating turtle (Testudines: Geoemydidae: MalayemysLindholm 1931): Malayemys khoratensisIhlow et al. 2016 and M. isanSumontha et al. 2016. In order to determine the valid name for the species in question, we performed a comprehensive bibliographical analysis of both underlying publications. We come to the conclusion that M. khoratensis is the older available name that fulfills all requirements of being published for the purpose of nomenclature. The name was made available in full agreement with the requirements of the International Code of Zoological Nomenclature in an electronic publication of the journal PLoS ONE on 6 April 2016. The earliest date a printed copy of Volume 8(1) of the journal Taprobanica (which contains the description of M. isan and constitutes the nomenclaturally relevant edition of this publication outlet) can be shown to have been in existence, via actual printing records, is 13 April 2016. However, 13 April, in fact, dates after we placed a request to purchase a printed copy and after we asked several questions about the journal's publication procedures. By definition, our finding unveils Taprobanica 8(1) as being published under a print-on-demand model, a violation of Article 8.1 in that such print-on-demand publications do not constitute a published work under the Code. In agreement with Article 9.12, Volume 8(1) of Taprobanica cannot be considered published for the purpose of nomenclature and thus, following Article 11.1, M. isan cannot be considered an available name in zoological nomenclature. The valid name for the recently described species of Malayemys consequently is M. khoratensis: the Khorat snail-eating turtle.
After a control program for feral foxes was instigated, the monitor lizard Varanus panoptes has become the most common predator of loggerhead turtle nests at the Wreck Rock beach nesting aggregation adjacent to Deepwater National Park in southeastern Queensland. We empirically tested the efficacy of aluminum mesh cages, plastic mesh sheets, red flags, and hot chili powder in protecting loggerhead turtle nests from monitor lizard predation across 2 nesting seasons (2014–2015 and 2015–2016). Our study indicated that plastic mesh, when applied correctly, is a relatively inexpensive and effective way to prevent monitor lizard nest predation at sea turtle nesting beaches.
Here we describe the effects of beach morphological features on loggerhead (Caretta caretta) nesting behavior on the barrier islands of the north-central Gulf of Mexico. Our results show that loggerhead crawl length decreases as beach slope increases, and our data comparing nest crawls (resulting in egg laying) versus false crawls (emergence onto the beach without laying eggs) suggest that beach slope and crawl length differ between the crawl types but elevation does not. We infer that loggerheads cue in to beach slope to reach a perceived elevation with reduced risk of inundation, crawling longer distances on flatter slopes compared with shorter distances on steep slopes, but that after this elevation is reached, other environmental variables may ultimately factor into the decision to lay eggs.
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