Isolation and characterization of novel microsatellites from the critically endangered hawksbill sea turtle (Eretmochelys imbricata)

We isolated and characterized 12 microsatellite loci from the hawksbill sea turtle (Eretmochelys imbricata). The loci exhibited a variable number of alleles that ranged from three to 14 with an average observed heterozygosity of 0.70 (SD 0.18) across 40 hawksbill turtles from the Caribbean. The polymorphism exhibited individually and in combination makes them suitable for fine-scale genetic studies. In particular, the low probability of identity and high paternity exclusion of these markers makes them highly useful for parentage and relatedness studies. These new markers greatly increase the power of genetic studies directed towards the conservation of this endangered species.     

Extreme rainfall events and cooling of sea turtle clutches: Implications in the face of climate warming

Understanding how climate change impacts species and ecosystems is integral to conservation. When studying impacts of climate change, warming temperatures are a research focus, with much less attention given to extreme weather events and their impacts. Here, we show how localized, extreme rainfall events can have a major impact on a species that is endangered in many parts of its range. We report incubation temperatures from the world's largest green sea turtle rookery, during a breeding season when two extreme rainfall events occurred. Rainfall caused nest temperatures to drop suddenly and the maximum drop in temperature for each rain‐induced cooling averaged 3.6°C (n = 79 nests, min = 1.0°C, max = 7.4°C). Since green sea turtles have temperature‐dependent sex determination, with low incubation temperatures producing males, such major rainfall events may have a masculinization effect on primary sex ratios. Therefore, in some cases, extreme rainfall events may provide a “get‐out‐of‐jail‐free card” to avoid complete feminization of turtle populations as climate warming continues.     

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.     

Solomon Islands Largest Hawksbill Turtle Rookery Shows Signs of Recovery after 150 Years of Excessive Exploitation

The largest rookery for hawksbill turtles in the oceanic South Pacific is the Arnavon Islands, which are located in the Manning Strait between Isabel and Choiseul Province, Solomon Islands. The history of this rookery is one of overexploitation, conflict and violence. Throughout the 1800s Roviana headhunters from New Georgia repeatedly raided the Manning Strait to collect hawksbill shell which they traded with European whalers. By the 1970s the Arnavons hawksbill population was in severe decline and the national government intervened, declaring the Arnavons a sanctuary in 1976. But this government led initiative was short lived, with traditional owners burning down the government infrastructure and resuming intensive harvesting in 1982. In 1991 routine beach monitoring and turtle tagging commenced at the Arnavons along with extensive community consultations regarding the islands’ future, and in 1995 the Arnavon Community Marine Conservation Area (ACMCA) was established. Around the same time national legislation banning the sale of all turtle products was passed. This paper represents the first analysis of data from 4536 beach surveys and 845 individual turtle tagging histories obtained from the Arnavons between 1991-2012. Our results and the results of others, reveal that many of the hawksbill turtles that nest at the ACMCA forage in distant Australian waters, and that nesting on the Arnavons occurs throughout the year with peak nesting activity coinciding with the austral winter. Our results also provide the first known evidence of recovery for a western pacific hawksbill rookery, with the number of nests laid at the ACMCA and the remigration rates of turtles doubling since the establishment of the ACMCA in 1995. The Arnavons case study provides an example of how changes in policy, inclusive community-based management and long term commitment can turn the tide for one of the most charismatic and endangered species on our planet.     

Migration of hawksbill turtles Eretmochelys imbricata from Tortuguero, Costa Rica

The hawksbill turtle Eretmochelys imbricata is a widely distributed and critically endangered species that feeds on sponges and fills an important ecological role in the coral reef ecosystem. At Tortuguero, Costa Rica, trend analyses indicate considerable decline in nesting estimated at 77.2–94.5% between 1956 and 2003, as a result of excessive turtle fishing. We analyzed flipper tag returns, satellite telemetry and genetic samples to determine movements and habitat use of adult female Tortuguero hawksbills. Tag returns and satellite telemetry show hawksbills migrate to foraging grounds in Nicaragua and Honduras. Genetic analysis indicates the hawksbills may also migrate to Cuban, Puerto Rican, and possibly Mexican waters. We conclude hawksbills represent an internationally shared resource. There is a close correlation between tag recapture sites, hawksbill foraging grounds and coral reef distribution. Caribbean coral reef decline may reduce food availability and negatively impact hawksbill turtles. Conversely, hawksbill decline may shift the balance on coral reefs by reducing predation pressure on sponges and hence make coral reefs less resilient to natural and anthropogenic threats. Strategies aiming to conserve hawksbills and coral reefs must consider both the extensive hawksbill migrations and the close relationship between the species and the coral reef ecosystem.     

Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach

Whether a turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm temperatures produce 100% females. Therefore, global warming has the potential to drastically alter their sex ratios. Air temperatures on Antigua have increased by 0.7°C over the last 35 years. Measurements in both the sand and the clutches laid by hawksbill turtles (Eretmochelys imbricata) at Pasture Bay, Antigua, show that for important parts of the nesting season temperatures are already above the level producing 50% of each sex (pivotal level). Comparisons are made to sand temperature measurements taken on this beach in 1989 and 1990. It is estimated that fewer males were produced in 2003 than in the previous years. Recommendations are made for close monitoring of the fertility of eggs and for research on any turtles nesting at cooler times of year.     

Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata)

We present the first data collected on the genetic mating system of the hawksbill turtle Eretmochelys imbricata, the only marine turtle not studied to date. We examined paternity within 12 egg clutches from ten female hawksbill turtles from Sabah Turtle Islands, Malaysia. A total of 375 hatchlings were analysed using five microsatellite markers. Results demonstrated that clutches from two out of ten females were sired by multiple males (maximum of two). Although at a low frequency, observation of multiple paternity indicates that hawksbill turtles exhibit the same genetic mating system (polyandry) as observed for other species of marine turtles. Consistent paternity across multiple clutches laid by individual females in one breeding season supports the hypothesis that sperm are stored from mating prior to nesting and are then used to fertilize all subsequent clutches of eggs that season.     

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.     

Effects of El Niño-driven environmental variability on black turtle migration to Peruvian foraging grounds

We analyzed sea temperature as an environmental factor, in association with ENSO, affecting the migration of East Pacific black turtle, Chelonia mydas (=Chelonia agassizii Bocourt), to its foraging areas and its feeding ecology at San Andrés, Peru. A 19-year sea turtle landing database (1970–1988) was constructed to associate landing fluctuations with environmental variability represented by the Peruvian Oscillation Index. A positive correlation between them (r = 0.75, P < 0.05) indicated that exceptionally large black turtle landings occurred in San Andrés port during El Niño episodes. Warmer waters (SST 22–28°C) approached near the Peruvian coast during El Niño episodes, thus facilitating black turtle access to this area. Furthermore, during El Niño 1987, large juvenile and adult black turtles, known to be primarily herbivorous, fed mainly on the scyphozoan jellyfish Chrysaora plocamia Péron &; Lesueur, which was very abundant during this event. It is likely that black turtles exploited this resource opportunistically. Inter-annual environmental variability, driven by El Niño Southern Oscillation, has profound consequences for the ecology of the endangered black turtle, which should be considered when evaluating the effects of anthropogenic activities on its population dynamics.     

The developmental biogeography of hawksbill sea turtles in the North Pacific

High seas oceanic ecosystems are considered important habitat for juvenile sea turtles, yet much remains cryptic about this important life‐history period. Recent progress on climate and fishery impacts in these so‐called lost years is promising, but the developmental biogeography of hawksbill sea turtles (Eretmochelys imbricata) has not been widely described in the Pacific Ocean. This knowledge gap limits the effectiveness of conservation management for this globally endangered species. We address this with 30 years of stranding observations, 20 years of bycatch records, and recent simulations of natal dispersal trajectories in the Hawaiian Archipelago. We synthesize the analyses of these data in the context of direct empirical observations, anecdotal sightings, and historical commercial harvests from the insular Pacific. We find hawksbills 0–4 years of age, measuring 8–34 cm straight carapace length, are found predominantly in the coastal pelagic waters of Hawaii. Unlike other species, we find no direct evidence of a prolonged presence in oceanic habitats, yet satellite tracks of passive drifters (simulating natal dispersal) and our small sample sizes suggest that an oceanic phase for hawksbills cannot be dismissed. Importantly, despite over 600 million hooks deployed and nearly 6000 turtle interactions, longline fisheries have never recorded a single hawksbill take. We address whether the patterns we observe are due to population size and gear selectivity. Although most sea turtle species demonstrate clear patterns of oceanic development, hawksbills in the North Pacific may by contrast occupy a variety of ecosystems including coastal pelagic waters and shallow reefs in remote atolls. This focuses attention on hazards in these ecosystems – entanglement and ingestion of marine debris – and perhaps away from longline bycatch and decadal climate regimes that affect sea turtle development in oceanic regions.     

Conditions for initiating Lake Victoria haplochromine (Oreochromis esculentus) primary cell cultures from caudal fin biopsies

The global decline of freshwater fishes has created a need to cryopreserve biological materials from endangered species in an effort to conserve the biodiversity within this taxon. Since maternal gametes and embryos from fish are difficult to cryopreserve, somatic cells obtained from caudal fins have become an increasingly popular resource as they contain both maternal and paternal DNA ensuring valuable traits are not lost from the population. Somatic cells stored in cryobanks can be used to supplement endangered populations with genetically valuable offspring with the use of assisted reproductive technologies. However, initiating primary cell cultures from caudal fin biopsies of endangered species can be challenging as standardized protocols have not yet been developed. The objective of this study was to identify culture conditions, including antibiotic supplementation, biopsy size, and culture temperature, suitable for establishing primary cell cultures of ngege (Oreochromis esculentus), a critically endangered African cichlid. Six-millimeter caudal fin biopsies provided sufficient material to develop a primary cell culture when incubated at 25°C using standard fish cell culture medium containing 1× Primocin. Further investigation and application of these culture conditions for other endangered freshwater fishes is necessary.     

Comparison of functional aspects of the coagulation cascade in human and sea turtle plasmas

Functional hemostatic pathways are critical for the survival of all vertebrates and have been evolving for more than 400 million years. The overwhelming majority of studies of hemostasis in vertebrates have focused on mammals with very sparse attention paid to reptiles. There have been virtually no studies of the coagulation pathway in sea turtles whose ancestors date back to the Jurassic period. Sea turtles are often exposed to rapidly altered environmental conditions during diving periods. This may reduce their blood pH during prolonged hypoxic dives. This report demonstrates that five species of turtles possess only one branch of the mammalian coagulation pathway, the extrinsic pathway. Mixing studies of turtle plasmas with human factor-deficient plasmas indicate that the intrinsic pathway factors VIII and IX are present in turtle plasma. These two factors may play a significant role in supporting the extrinsic pathway by feedback loops. The intrinsic factors, XI and XII are not detected which would account for the inability of reagents to induce coagulation via the intrinsic pathway in vitro. The analysis of two turtle factors, factor II (prothrombin) and factor X, demonstrates that they are antigenically/functionally similar to the corresponding human factors. The turtle coagulation pathway responds differentially to both pH and temperature relative to each turtle species and relative to human samples. The coagulation time (prothrombin time) increases as the temperature decreases between 37 and 15 °C. The increased time follows a linear relationship, with similar slopes for loggerhead, Kemps ridley and hawksbill turtles as well as for human samples. Leatherback turtle samples show a dramatic nonlinear increased time below 23 °C, and green turtle sample responses were similar but less dramatic. All samples also showed increased prothrombin times as the pH decreased from 7.8 to 6.4, except for three turtle species. The prothrombin times decreased, to varying extents, in a linear fashion relative to reduced pH with the rate of change greatest in leatherbacks>greenloggerhead turtles. All studies were conducted with reagents developed for human samples which would impact on the quantitative results with the turtle samples, but are not likely to alter the qualitative results. These comparative studies of the coagulation pathway in sea turtles and humans could enhance our knowledge of structure/function relationships and evolution of coagulation factors.     

Bioko: critically important nesting habitat for sea turtles of West Africa

We evaluate the conservation status and threats faced by sea turtle nesting populations at Bioko Island, Equatorial Guinea (Central Africa). Beaches were monitored to obtain a detailed sea turtle nest census and, where possible, tagging of adult females was undertaken. Four sea turtle species were found nesting in the area: the green turtle (Chelonia mydas), the leatherback (Dermochelys coriacea), the olive ridley (Lepidochelys olivacea) and the hawksbill (Eretmochelys imbricata); with the former two species nesting in regionally important numbers. Nesting activity was concentrated between November and February, with a peak in December–January. Tagging and recapture of green turtles in two consecutive seasons suggested an estimated 560 (interquartile range: 420–1,681) and 414 (interquartile range: 190–1,255) nesting females in the area, respectively. Estimated numbers of nesting leatherbacks ranged from 123 to 215 and 243 to 293 in the first and second season, respectively. The other two species were less abundant (olive ridley: 19–29 and 28–43; hawksbill: 4–10 and 2 turtles). Data were compared with more recent surveys in the area and contextualised with information on human related threats. Despite the size of nesting stocks, ongoing permitted and illegal take of adult turtles at the nesting site constitutes a serious threat for these breeding aggregations. Additionally, tag returns from throughout the Gulf of Guinea suggest that the level of take in regional fisheries may also be a major threat.     

Relationship between tropical cyclones and the distribution of sea turtle nesting grounds

Aim This study examines the relationship between the distribution of existing sea turtle nesting sites and historical patterns of tropical cyclone events to investigate whether cyclones influence the current distribution of sea turtle nesting sites. The results, together with information on predicted cyclone activity and other key environmental variables, will help in the identification and prediction of future nesting sites for sea turtles as changes to the coastal environment continue. Location Queensland, Australia. Methods We used data on the nesting distribution of seven populations of four species of sea turtles [green (Chelonia mydas), flatback (Natator depressus), hawksbill (Eretmochelys imbricata) and loggerhead (Caretta caretta)] from the eastern Queensland coast, and tropical cyclone track data from 1969 to 2007 to explore the relationship between (1) sea turtle nesting phenology and cyclone season, and (2) sea turtle nesting sites and cyclone distribution. Furthermore, using two green turtle populations as a case study, we investigated the relationship between cyclone disturbance and sea turtle reproductive output, nesting site and season. Bootstrapping was used to explore if current sea turtle nesting sites are located in areas with lower or higher cyclone frequency than areas where turtles are currently not nesting. Results All populations of sea turtles studied here were disturbed by cyclone activity during the study period. The exposure (frequency) of tropical cyclones that crossed each nesting site varied greatly among and within the various sea turtle populations. This was mainly a result of the spatial distribution of each population’s nesting sites. Bootstrapping indicated that nesting sites generally have experienced lower cyclone activity than other areas that are available for nesting. Main conclusions Tropical cyclones might have been sufficiently detrimental to sea turtle hatching success on the eastern Queensland coast that through a natural selection process turtles in this region are now nesting in areas with lower cyclone activity. Therefore, it is important that future studies that predict climate or range shifts for sea turtle nesting distributions consider future cyclone activity as one of the variables in their model.     

Dispersal, recruitment and migratory behaviour in a hawksbill sea turtle aggregation

We investigated the dispersal, recruitment and migratory behaviour of the hawksbill sea turtle ( Eretmochelys imbricata ), among different life-history stages and demographic segments of the large hawksbill turtle aggregation at Mona Island, Puerto Rico. There were significant differences in both mitochondrial DNA (mtDNA) haplotype diversity and haplotype frequencies among the adult males, females and juveniles examined, but little evidence for temporal heterogeneity within these same groups sampled across years. Consistent with previous studies and the hypothesis of strong natal homing, there were striking mtDNA haplotype differences between nesting females on Mona Island and nesting females in other major Caribbean rookeries. Breeding males also showed strong, albeit weaker, genetic evidence of natal homing. Overall, Bayesian mixed-stock analysis suggests that Mona Island was the natal rookery for 79% (65–94%) of males in the aggregation. In contrast, the Mona Island rookery accounted for only a small subset of the new juvenile recruits to the foraging grounds or in the population of older juvenile hawksbills turtles on Mona. Instead, both new recruits and the older juvenile hawksbill turtles on Mona more likely recruited from other Caribbean rookeries, suggesting that a mechanism besides natal homing must be influencing recruitment to feeding habitats. The difference in the apparent degree of natal homing behaviour among the different life-history stages of hawksbill turtles at Mona Island underscores the complexity of the species' life-history dynamics and highlights the need for both local and regional conservation efforts.     

Reconciling Biodiversity with Fishing: A Holistic Strategy for Pacific Sea Turtle Recovery

Recovery of sea turtle populations requires addressing: multiple sources of mortality; nonmarket, diffuse benefits with costs localized on the poor; and a transboundary resource with incomplete jurisprudence, markets, and institutions. Holistic recovery strategies include: beach conservation protecting nesting females, their eggs, and critical breeding habitat to maximize hatchling production; enhanced at-sea survival of turtles on the high seas and in commercial coastal fisheries; and reduced artisanal coastal fisheries mortality of turtles. The traditional approach of focusing long-term sustained conservation efforts on the nesting beaches has by itself led to increases in several sea turtle populations. However, current conservation is inadequate to reverse declines in other cases such as the critically endangered leatherback populations in the Pacific. This article discusses policy instruments comprising a holistic recovery strategy that reconciles fishing with biodiversity conservation.     

A survey of the epibiota of Eretmochelys imbricata (Testudines: Cheloniidae) of Mona Island, Puerto Rico

Epibiotic organisms inhabiting non-nesting hawksbill sea turtles, Eretmochelys imbricata (Linnaeus, 1766), are described from Mona and Monito Islands, Puerto Rico. Epibiont samples from 105 turtles of shallow (< 40 m) water foraging habitats were collected and identified to the lowest possible taxon. This epibiotic assemblage consisting of at least 4 algal functional groups and 12 animal phyla represents the greatest phylogenetic diversity for marine turtle epibiota. Six groups are considered new reports for marine turtles. Most epibiont colonization was found on posterior marginal scutes and under overlapping scutes. Ecological attributes of epibiota and their symbiosis with E. imbricata provide a tool to understand basi and epibiont populations.     

Development of a Summarized Health Index (SHI) for Use in Predicting Survival in Sea Turtles

Veterinary care plays an influential role in sea turtle rehabilitation, especially in endangered species. Physiological characteristics, hematological and plasma biochemistry profiles, are useful references for clinical management in animals, especially when animals are during the convalescence period. In this study, these factors associated with sea turtle surviving were analyzed. The blood samples were collected when sea turtles remained alive, and then animals were followed up for surviving status. The results indicated that significantly negative correlation was found between buoyancy disorders (BD) and sea turtle surviving (p < 0.05). Furthermore, non-surviving sea turtles had significantly higher levels of aspartate aminotranspherase (AST), creatinine kinase (CK), creatinine and uric acid (UA) than surviving sea turtles (all p < 0.05). After further analysis by multiple logistic regression model, only factors of BD, creatinine and UA were included in the equation for calculating summarized health index (SHI) for each individual. Through evaluation by receiver operating characteristic (ROC) curve, the result indicated that the area under curve was 0.920 ± 0.037, and a cut-off SHI value of 2.5244 showed 80.0% sensitivity and 86.7% specificity in predicting survival. Therefore, the developed SHI could be a useful index to evaluate health status of sea turtles and to improve veterinary care at rehabilitation facilities.     

Investigating the potential impacts of climate change on a marine turtle population

Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with warmer sea surface temperature. We modelled the effects of incremental increases in mean AT of up to 7.5°C, the maximum predicted increase under modelled scenarios, which would lead to 100% female hatchling production and lethally high incubation temperatures, causing reduction in hatchling production. Populations of turtles in more southern parts of the United States are currently highly female biased and are likely to become ultra‐biased with as little as 1°C of warming and experience extreme levels of mortality if warming exceeds 3°C. The lack of a demonstrable increase in AT in North Carolina in recent decades coupled with primary sex ratios that are not highly biased means that the male offspring from North Carolina could play an increasingly important role in the future viability of the loggerhead turtle in the Western Atlantic.