A meiotic analysis of four species of turtles

The meiotic chromosomes of 4 species of turtles representing 3 genera (Clemmys, Mauremys and Geochelone) are described and compared. Clemmys differs from Mauremys and Geochelone in possessing one fewer bivalent in diakinesis and one fewer chromosome in prophase II. Mauremys differs from Clemmys and Geochelone in possessing a distinct heterochromatic knob on one small bivalent in late pachytene. The presence of this heterochromatic region in the batagurine turtle may be the ancestral condition and its loss may now characterize the emydines such as Clemmys and the testudinids such as Geochelone.     

Cryptic variation and the tragedy of unrecognized taxa: the case of international trade in the spiny turtle Heosemys spinosa (Testudines: Geoemydidae)

Loss of habitat and human exploitation have driven many turtle species to the brink of extinction, particularly in many parts of southern Asia. The spiny turtle (Heosemys spinosa) is a terrestrial species distributed throughout the Sundaland region of South‐East Asia. Despite international legislative protection, H. spinosa continues to be illegally collected for the food and traditional medicine markets of China. Given its widespread distribution, taxonomists have reasonably questioned whether H. spinosa truly represents a single evolutionary lineage or multiple undiagnosed species. Recently, a large and illegal shipment of rare, wild‐caught H. spinosa was confiscated in Hong Kong, China, and the turtles were eventually distributed to several zoos and academic collections. Based on analyses of these individuals, along with additional individuals from the pet trade and museum collections, we found concordant genetic and phenotypic variation, indicating that two distinct types of H. spinosa exist in this collection of turtles. Further characterization of this variation will require field surveys and the collection of additional morphological and genetic data from specimens of known geographic provenance. However, our data indicate that this highly exploited, endangered species may contain additional cryptic taxa, and emphasize the critical need for systematic evaluation of species before unrecognized variation is lost forever. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 811–824.     

A first estimate of sea turtle bycatch in the industrial trawling fishery of Gabon

Gabon hosts nesting grounds for several sea turtle species, including the world’s largest rookery for the leatherback turtle (Dermochelys coriacea), Africa’s largest rookery for the olive ridley turtle (Lepidochelys olivacea) and smaller aggregations of the hawksbill turtle (Eretmochelys imbricata) and green turtle (Chelonia mydas). To assess the level of incidental captures of turtles by the Gabonese trawl fishery, an onboard observer program was conducted in the period 2012–2013. A total of 143 turtles were captured by 15 trawlers during 271 fishing days. The olive ridley turtle was the main species captured (80% of bycaught turtles), with mostly adult-sized individuals. The remaining 20% included green turtles, hawksbill turtles, leatherback turtles and undetermined species. Bycatch per unit of effort (BPUE) of olive ridley turtles varied greatly depending on the period of the year (range of means: 0.261–2.270). Dead and comatose turtles were 6.2 and 24.6% respectively (n = 65). By applying the available fishing effort to two BPUE scenarios (excluding or considering a seasonal peak), the total annual number of captures was estimated as ranging between 1026 (CI 95% 746–1343) and 2581 (CI 95% 1641–3788) olive ridley turtles, with a mortality ranging from 63 (CI 95% 13–135) to 794 (CI 95% 415–1282) turtles per year depending on the scenario and on the fate of comatose turtles. Such a potential mortality may be reason for concern for the local breeding population of olive ridley turtles and recommendations in terms of possible conservation measures and further research are given.     

Global Distribution of Two Fungal Pathogens Threatening Endangered Sea Turtles

Nascent fungal infections are currently considered as one of the main threats for biodiversity and ecosystem health, and have driven several animal species into critical risk of extinction. Sea turtles are one of the most endangered groups of animals and only seven species have survived to date. Here, we described two pathogenic species, i.e., Fusarium falciforme and Fusarium keratoplasticum, that are globally distributed in major turtle nesting areas for six sea turtle species and that are implicated in low hatch success. These two fungi possess key biological features that are similar to emerging pathogens leading to host extinction, e.g., high virulence, and a broad host range style of life. Their optimal growth temperature overlap with the optimal incubation temperature for eggs, and they are able to kill up to 90% of the embryos. Environmental forcing, e.g., tidal inundation and clay/silt content of nests, were correlated to disease development. Thus, these Fusarium species constitute a major threat to sea turtle nests, especially to those experiencing environmental stressors. These findings have serious implications for the survival of endangered sea turtle populations and the success of conservation programs worldwide.     

Variation in reproductive output of marine turtles

Most marine turtle species are non-annual breeders and show variation in both the number of eggs laid per clutch and the number of clutches laid in a season. Large levels of inter-annual variation in the number of nesting females have been well documented in green turtle nesting populations and may be linked to environmental conditions. Other species of marine turtle exhibit less variation in nesting numbers. This inter-specific difference is thought to be linked to trophic status. To examine whether individual reproductive output is more variable in the herbivorous green turtle (Chelonia mydas Linneaeus 1758) than the carnivorous loggerhead (Caretta caretta Linneaeus 1758), we examined the nesting of both species in Cyprus over nine seasons. Green turtles showed slower annual growth rates (0.11 cm year⁻¹ curved carapace length (CCL) and 0.27 cm year⁻¹ curved carapace width (CCW)) than loggerhead turtles (0.36 cm year⁻¹ CCL, 0.51 cm year⁻¹ CCW). CCL was highly correlated to mean clutch size in both green (R²=0.51) and loggerhead turtles (R²=0.61) and maximal clutch size of green turtles (R²=0.58). Larger females did not lay a greater number of clutches or have a shorter remigration interval than smaller females of either species. On average, the size of green turtle clutches increased and that of loggerhead turtles decreased as the season progressed. Individual green turtles, however, produced more eggs per clutch through the season to a maximum in the third or fourth clutch. In loggerhead turtles, clutches 1-4 were very similar in size but the fifth clutch was 38% smaller than the first. No individuals of either species were recorded laying more than five clutches. Green turtles may not be able to achieve their maximum reproductive output with respect to clutch size throughout the season, whereas only loggerhead turtles laying five clutches (n=5) appear to become resource depleted. Green turtles nesting in years when large numbers of nests were recorded laid a greater number of clutches than females nesting in years with lower levels of nesting.     

Efficient establishment of primary fibroblast cultures from the hawksbill sea turtle (Eretmochelys imbricata)

The hawksbill sea turtle (Eretmochelys imbricata) is a critically endangered species at a risk of extinction. Preservation of the genomic and cellular information of endangered animals is important for future genetic and biological studies. Here, we report the efficient establishment of primary fibroblast cultures from skin tissue of the hawksbill sea turtle. We succeeded in establishing 19 primary cultures from 20 hawksbill sea turtle individuals (a success rate of 95%). These cells exhibited a fibroblast-like morphology and grew optimally at a temperature of 26°C, but experienced a loss of viability when cultured at 37°C. Chromosomal analysis using the primary cells derived here revealed that hawksbill sea turtles have a 2n?=?56 karyotype. Furthermore, we showed that our primary cell cultures are free of several fish-related viruses, and this finding is important for preservation purposes. To our knowledge, this report is the first to describe primary cell cultures established from normal tissues of the hawksbill sea turtle. The results will contribute to the preservation of biodiversity, especially for the sea turtles that are critically endangered owing to human activities.     

Pleistocene and Holocene rhinocerotids (Mammalia,Perissodactyla) from the Indochinese Peninsula

Rhinocerotids were abundant and diverse in southern Asia during the Pleistocene and the Holocene epochs, as shown by palaeontological and archaeological discoveries published throughout the last century, whereas the only living rhinoceros in the Indochinese Peninsula is Rhinoceros sondaicus (Cat Loc Reserve, Vietnam). The Pleistocene-Holocene Indochinese rhinocerotid record consists of the extinct species Dicerorhinus gwebinensis (Early Pleistocene, Myanmar) and representatives of the Recent Asian Species Rhinoceros unicornis (Middle-Late Pleistocene), R. sondaicus (Middle Pleistocene-Recent), and Dicerorhinus sumatrensis (Middle Pleistocene-Holocene). This fossil record is synthesized, mapped for Early/Middle/Late Pleistocene and Holocene/Recent times, and then compared with coeval rhinocerotid assemblages from the adjacent areas (South China), subregions (Indian, Sundaic, Philippine, and Wallacean), and region (Palearctic), from a biochronological and biogeographical perspective.     

Helminth communities of loggerhead turtles (Caretta caretta) from Central and Western Mediterranean Sea: The importance of host's ontogeny

We investigated the factors providing structure to the helminth communities of 182 loggerhead sea turtles, Caretta caretta, collected in 6 localities from Central and Western Mediterranean. Fifteen helminth taxa (10 digeneans, 4 nematodes and 1 acanthocephalan) were identified, of which 12 were specialist to marine turtles; very low numbers of immature individuals of 3 species typical from fish or cetaceans were also found. These observations confirm the hypothesis that phylogenetic factors restrict community composition to helminth species specific to marine turtles. There were significant community dissimilarities between turtles from different localities, the overall pattern being compatible with the hypothesis that parasite communities reflect the ontogenetic shift that juvenile loggerheads undergo from oceanic to neritic habitats. The smallest turtles at the putative oceanic, pelagic-feeding stage harboured only the 2 digenean species that were regionally the most frequent, i.e. Enodiotrema megachondrus and Calycodes anthos; the largest turtles at the putative neritic, bottom-feeding stage harboured 11 helminth taxa, including 3 nematode species that were rare or absent in turtles that fed partially on pelagic prey. Mean species richness per host was low (range: 1.60–1.89) and did not differ between localities. Variance ratio tests indicated independent colonization of each helminth species. Both features are expected in ectothermic and vagrant hosts living in the marine environment.     

The fossil bat assemblages from the Grotta dei Pipistrelli in Pantalica (southeastern Sicily,Italy): Chronological and palaeoecological implications

Bat remains are useful for palaeoecological reconstructions, they provide independent information on palaeoenvironment and are good indicators for hypogean microclimates. Nine taxa of Chiroptera divided into three families (Rhinolophidae, Vespertilionidae and Miniopteridae) and four genera (Rhinolophus, Myotis, Plecotus and Miniopterus) were discovered in three fossil assemblages from the Grotta dei Pipistrelli, in Sicily, a key region for an understanding of Quaternary climates and environments. Bat remains were deposited during three distinct timespans: one late Pleistocene, MIS 2, around the Last Glacial Maximum, and two Holocene, both referable to the Atlantic chronozone. The presence of yearlings, adult and old individuals suggests hibernating colonies, but the cave was also utilized as a nursery. The diversity of taxa indicates a composite landscape with prevailing vegetation cover and relatively warm climatic conditions. The percentage variations of the frequencies of the recognized taxa suggest a progressive increase of open spaces in the middle Holocene.     

Diversity of Middle Jurassic Turtles from the Berezovsk Quarry Locality,Krasnoyarsk Region,Russia: Morphology and Histological Study

Abstract—Morphology and histology of several fragmentary turtle specimens from the Middle Jurassic locality in the Berezovsk quarry (Krasnoyarsk Region, Russia) are described, including Testudines indet. 1 (costal VIII), Testudines indet. 2 (two ornamented shell fragments), and Testudines indet. 3 (distal part of a humerus), and also skeletal elements of Annemys sp. (Xinjiangchelyidae) represented by mass material in the same locality. It is shown that Testudines indet. 1 and 3 probably belong to one or two taxa of basal aquatic turtles, while Testudines indet. 2 is most likely an abnormal Annemys sp. The presumable presence of basal turtles in the Berezovsk Quarry Assemblage agrees with the fact that they are present in other Middle Jurassic turtle assemblages of Asia.     

Influence of sea turtle nesting on hunting behavior and movements of jaguars in the dry forest of northwest Costa Rica

Jaguars (Panthera onca) are opportunistic predators that prey on large profitable prey items, such as sea turtles at nesting beaches. Here, we use jaguar and sea turtle track-count surveys, combined with satellite telemetry of one jaguar, to evaluate whether jaguar hunting behavior and movements are influenced by seasonal sea turtle nesting in the Sector Santa Rosa of Área de Conservación Guanacaste in northwest Costa Rica. We used generalized linear models to evaluate the effect of moon phase and sea surface temperature on olive ridley (Lepidochelis olivacea) and green turtle (Chelonia mydas) nesting abundance, as well as the combination of these predictors on the frequency of jaguar predation activity (proximity to nesting beaches) and movements. For home-range size and location analyses, we calculated kernel density estimates for each season at three different temporal scales. Sea turtle nesting season influenced jaguar activity patterns, as well as sea turtle abundance was related to jaguar locations and predation events, but jaguar home-range size (88.8 km² overall) did not differ between nesting seasons or among temporal scales. Environmental conditions influenced sea turtle nesting and, as a consequence, also influenced jaguar movements and foraging activity. Our study defined the home range of a female jaguar in the tropical dry forest and its relationship to seasonally abundant turtles. Additional information related to the effect of tourism on jaguar–sea turtle interactions would improve conservation of these species at unique nesting beaches in the area.     

Long-distance dispersal, low connectivity and molecular evidence of a new cryptic species in the obligate rafter Caprella andreae Mayer, 1890 (Crustacea: Amphipoda: Caprellidae)

The amphipod Caprella andreae Mayer, 1890 was recorded for the first time in Southern Iberian Peninsula (36°44′15″N, 3°59′38″W). This species is the only obligate rafter of the suborder Caprellidea and has been reported to attach not only to floating objects such as ropes or driftwoods but also to turtle carapaces. Mitochondrial and nuclear markers were used to examine dispersal capabilities and population genetic structure of C. andreae across seven localities in the Mediterranean and Atlantic Ocean collected from floating substrata with different dispersal patterns. The strong population differentiation with no haplotypes shared between populations suggests that C. andreae is quite faithful to the substratum on which it settles. In addition, the proportionally higher genetic diversity displayed in populations living on turtles as well as the presence of highly differentiated haplotypes in the same turtle population may be indicative that these populations survive longer, which could lead C. andreae to prefer turtles instead of floating objects to settle and disperse. Therefore, rafting on floating objects may be sporadic, and ocean currents would not be the most important factor shaping patterns of connectivity and population structure in this species. Furthermore, molecular phylogenetic analyses revealed the existence of a cryptic species whose estimates of genetic divergence are higher than those estimated between C. andreae and other congeneric species (e.g. Caprella dilatata and Caprella penantis). Discovery of cryptic species among widely distributed small marine invertebrates is quite common and, in this case, prompts for a more detailed phylogenetic analysis and taxonomic revision of genus Caprella. On the other hand, this study also means the first record of the gammarids Jassa cadetta and Elasmopus brasiliensis and the caprellid Caprella hirsuta on drifting objects.     

Analysis of prey capture and food transport kinematics in two Asian box turtles,Cuora amboinensis and Cuora flavomarginata (Chelonia,Geoemydidae), with emphasis on terrestrial feeding patterns

This study examines the kinematics and morphology of the feeding apparatus of two geoemydid chelonians, the Malayan (Amboina) box turtle (Cuora amboinensis) and the yellow-margined box turtle (Cuora flavomarginata). Both species are able to feed on land as well as in water. Feeding patterns were analysed by high-speed cinematography. The main focus of the present study is on the terrestrial feeding strategies in both Asian box turtles, because feeding on land has probably evolved de novo within the ancestrally aquatic genus Cuora. During terrestrial feeding (analysed for both species), the initial food prehension is always done by the jaws, whereas intraoral food transport and pharyngeal packing actions are tongue-based. The food uptake modes in Cuoras differ considerably from those described for purely terrestrial turtles. Lingual food prehension is typical of all tortoises (Testudinidae), but is absent in C. amboinensis and C. flavomarginata. A previous study on Terrapene carolina shows that this emydid turtle protrudes the tongue during ingestion on land, but that the first contact with the food item occurs by the jaws. Both Asian box turtles investigated here have highly movable, fleshy tongues; nonetheless, the hyolingual complex remains permanently retracted during initial prey capture. In aquatic feeding (analysed for C. amboinensis only), the prey is captured by a fast forward strike of the head (ram feeding). As opposed to ingestion on land, in the underwater grasp the hyoid protracts prior to jaw opening. The head morphology of the investigated species differs. In contrast to the Malayan box turtle, C. flavomarginata exhibits a more complexly structured dorsal lingual epithelium, a considerable palatal vault, weaker jaw adductor muscles and a simplified trochlear complex. The differences in the hyolingual morphology reflect the kinematic patterns of the terrestrial feeding transport.     

Contextualising the Last Survivors: Population Structure of Marine Turtles in the Dominican Republic

Nesting by three species of marine turtles persists in the Dominican Republic, despite historic threats and long-term population decline. We conducted a genetic survey of marine turtles in the Dominican Republic in order to link them with other rookeries around the Caribbean. We sequenced a 740_bp fragment of the control region of the mitochondrial DNA of 92 samples from three marine turtle species [hawksbill (n = 48), green (n = 2) and leatherback (n = 42)], and incorporated published data from other nesting populations and foraging grounds. The leatherback turtle (Dermochelys coriacea) in the Dominican Republic appeared to be isolated from Awala-Yalimapo, Cayenne, Trinidad and St. Croix but connected with other Caribbean populations. Two distinct nesting populations of hawksbill turtles (Eremochelys imbricata) were detected in the Dominican Republic and exhibited interesting patterns of connectivity with other nesting sites and juvenile and adult male foraging aggregations. The green sea turtle (Chelonia mydas) has almost been extirpated from the Dominican Republic and limited inference could be made from our samples. Finally, results were compared with Lagrangian drifting buoys and published Lagrangian virtual particles that travelled through the Dominican Republic and Caribbean waters. Conservation implications of sink-source effects or genetic isolation derived from these complex inter-connections are discussed for each species and population.     

Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry

Measuring the metabolic of sea turtles is fundamental to understanding their ecology yet the presently available methods are limited. Accelerometry is a relatively new technique for estimating metabolic rate that has shown promise with a number of species but its utility with air-breathing divers is not yet established. The present study undertakes laboratory experiments to investigate whether rate of oxygen uptake ( o ₂) at the surface in active sub-adult green turtles Chelonia mydas and hatchling loggerhead turtles Caretta caretta correlates with overall dynamic body acceleration (ODBA), a derivative of acceleration used as a proxy for metabolic rate. Six green turtles (25–44 kg) and two loggerhead turtles (20 g) were instrumented with tri-axial acceleration logging devices and placed singly into a respirometry chamber. The green turtles were able to submerge freely within a 1.5 m deep tank and the loggerhead turtles were tethered in water 16 cm deep so that they swam at the surface. A significant prediction equation for mean o ₂ over an hour in a green turtle from measures of ODBA and mean flipper length (R² = 0.56) returned a mean estimate error across turtles of 8.0%. The range of temperatures used in the green turtle experiments (22–30°C) had only a small effect on o ₂. A o ₂-ODBA equation for the loggerhead hatchling data was also significant (R² = 0.67). Together these data indicate the potential of the accelerometry technique for estimating energy expenditure in sea turtles, which may have important applications in sea turtle diving ecology, and also in conservation such as assessing turtle survival times when trapped underwater in fishing nets.     

Non‐marine turtle plays important functional roles in Indonesian ecosystems

The Southeast Asian box turtle (Cuora amboinensis) is numerically the most important turtle exported from Indonesia. Listed as Vulnerable by the IUCN, this turtle is heavily harvested and exported for food and traditional medicine in China and for the pet trade primarily in the United States, Europe, and Japan. Despite its significance in global markets, relatively little is known about the species’ ecology or importance to ecosystems. We conducted our research in a national park in Sulawesi, Indonesia, and our objectives were to quantify trophic breadth, capacity for seed dispersal between aquatic and terrestrial ecosystems, and whether ingestion of seeds by C. amboinensis enhances germination. We obtained diet samples from 200 individual turtles and found that the species is omnivorous, exhibiting an ontogenetic shift from more carnivorous to more omnivorous. Both subadults and adults scavenged on other vertebrates. In a seed passage experiment, turtles passed seeds for 2?9 days after ingestion. Radio‐tracked turtles moved, on average, about 35 m per day, indicating that seeds from ingested fruits, given seed passage durations, could be dispersed 70?313 m from the parent tree and potentially between wetland and upland ecosystems. In a seed germination experiment, we found that ingestion of seeds by turtles enhanced germination, as compared with control seeds, for four of six plant species tested. Of these, two are common in the national park, making up a significant proportion of plant biomass in lowland swamp forest and around ephemeral pools in savanna, and are highly valued outside of the park for their lumber for construction of houses, furniture, and boats. Protection of C. amboinensis populations may be important for maintaining trophic linkages that benefit biodiversity, communities, and local economies.     

Population genetics of Blanding’s turtle (Emys blandingii) in the midwestern United States

Blanding’s turtle (Emys blandingii) has declined substantially in North America due to anthropogenic activities, leaving populations smaller and increasingly fragmented spatially. We sampled 212 turtles to evaluate variation at eight microsatellite loci within and among 18 populations of E. blandingii across its primary range in the midwestern United States (Illinois, Iowa, Minnesota, and Nebraska). All loci and populations were highly polymorphic. Our analyses also detected considerable genetic structure within and among the sampled localities, and revealed ancestral gene flow of E. blandingii in this region north and east from an ancient refugium in the central Great Plains, concordant with post-glacial recolonization timescales. The data further implied unexpected ‘links’ between geographically disparate populations in Nebraska and Illinois. Our study encourages conservation decisions to be mindful of the genetic uniqueness of populations of E. blandingii across its primary range.