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1.  Multiple Distant Origins for Green Sea Turtles Aggregating off Gorgona Island in the Colombian Eastern Pacific 
PLoS ONE  2012;7(2):e31486.
Mitochondrial DNA analyses have been useful for resolving maternal lineages and migratory behavior to foraging grounds (FG) in sea turtles. However, little is known about source rookeries and haplotype composition of foraging green turtle aggregations in the southeastern Pacific. We used mitochondrial DNA control region sequences to identify the haplotype composition of 55 green turtles, Chelonia mydas, captured in foraging grounds of Gorgona National Park in the Colombian Pacific. Amplified fragments of the control region (457 bp) revealed the presence of seven haplotypes, with haplotype (h) and nucleotide (π) diversities of h = 0.300±0.080 and π = 0.009±0.005 respectively. The most common haplotype was CMP4 observed in 83% of individuals, followed by CMP22 (5%). The genetic composition of the Gorgona foraging population primarily comprised haplotypes that have been found at eastern Pacific rookeries including Mexico and the Galapagos, as well as haplotypes of unknown stock origin that likely originated from more distant western Pacific rookeries. Mixed stock analysis suggests that the Gorgona FG population is comprised mostly of animals from the Galapagos rookery (80%). Lagrangian drifter data showed that movement of turtles along the eastern Pacific coast and eastward from distant western and central Pacific sites was possible through passive drift. Our results highlight the importance of this protected area for conservation management of green turtles recruited from distant sites along the eastern Pacific Ocean.
doi:10.1371/journal.pone.0031486
PMCID: PMC3271101  PMID: 22319635
2.  Island-finding ability of marine turtles. 
Green turtles (Chelonia mydas) swim from foraging grounds along the Brazilian coast to Ascension Island to nest, over 2200 km distant in the middle of the equatorial Atlantic. To test the hypothesis that turtles use wind-borne cues to locate Ascension Island we found turtles that had just completed nesting and then moved three individuals 50 km northwest (downwind) of the island and three individuals 50 km southeast (upwind). Their subsequent movements were tracked by satellite. Turtles released downwind returned to Ascension Island within 1, 2 and 4 days, respectively. By contrast, those released upwind had far more difficulty in relocating Ascension Island, two eventually returning after 10 and 27 days and the third heading back to Brazil after failing to find its way back to the island. These findings strongly support the hypothesis that wind-borne cues are used by turtles to locate Ascension Island.
doi:10.1098/rsbl.2003.0022
PMCID: PMC1698032  PMID: 12952621
3.  A Comparison of the Seasonal Movements of Tiger Sharks and Green Turtles Provides Insight into Their Predator-Prey Relationship 
PLoS ONE  2012;7(12):e51927.
During the reproductive season, sea turtles use a restricted area in the vicinity of their nesting beaches, making them vulnerable to predation. At Raine Island (Australia), the highest density green turtle Chelonia mydas rookery in the world, tiger sharks Galeocerdo cuvier have been observed to feed on green turtles, and it has been suggested that they may specialise on such air-breathing prey. However there is little information with which to examine this hypothesis. We compared the spatial and temporal components of movement behaviour of these two potentially interacting species in order to provide insight into the predator-prey relationship. Specifically, we tested the hypothesis that tiger shark movements are more concentrated at Raine Island during the green turtle nesting season than outside the turtle nesting season when turtles are not concentrated at Raine Island. Turtles showed area-restricted search behaviour around Raine Island for ∼3–4 months during the nesting period (November–February). This was followed by direct movement (transit) to putative foraging grounds mostly in the Torres Straight where they switched to area-restricted search mode again, and remained resident for the remainder of the deployment (53–304 days). In contrast, tiger sharks displayed high spatial and temporal variation in movement behaviour which was not closely linked to the movement behaviour of green turtles or recognised turtle foraging grounds. On average, tiger sharks were concentrated around Raine Island throughout the year. While information on diet is required to determine whether tiger sharks are turtle specialists our results support the hypothesis that they target this predictable and plentiful prey during turtle nesting season, but they might not focus on this less predictable food source outside the nesting season.
doi:10.1371/journal.pone.0051927
PMCID: PMC3526478  PMID: 23284819
4.  Multinational Tagging Efforts Illustrate Regional Scale of Distribution and Threats for East Pacific Green Turtles (Chelonia mydas agassizii) 
PLoS ONE  2015;10(2):e0116225.
To further describe movement patterns and distribution of East Pacific green turtles (Chelonia mydas agassizii) and to determine threat levels for this species within the Eastern Pacific. In order to do this we combined published data from existing flipper tagging and early satellite tracking studies with data from an additional 12 satellite tracked green turtles (1996-2006). Three of these were tracked from their foraging grounds in the Gulf of California along the east coast of the Baja California peninsula to their breeding grounds in Michoacán (1337-2928 km). In addition, three post-nesting females were satellite tracked from Colola beach, Michoacán to their foraging grounds in southern Mexico and Central America (941.3-3020 km). A further six turtles were tracked in the Gulf of California within their foraging grounds giving insights into the scale of ranging behaviour. Turtles undertaking long-distance migrations showed a tendency to follow the coastline. Turtles tracked within foraging grounds showed that foraging individuals typically ranged up to 691.6 km (maximum) from release site location. Additionally, we carried out threat analysis (using the cumulative global human impact in the Eastern Pacific) clustering pre-existing satellite tracking studies from Galapagos, Costa Rica, and data obtained from this study; this indicated that turtles foraging and nesting in Central American waters are subject to the highest anthropogenic impact. Considering that turtles from all three rookeries were found to migrate towards Central America, it is highly important to implement conservation plans in Central American coastal areas to ensure the survival of the remaining green turtles in the Eastern Pacific. Finally, by combining satellite tracking data from this and previous studies, and data of tag returns we created the best available distributional patterns for this particular sea turtle species, which emphasized that conservation measures in key areas may have positive consequences on a regional scale.
doi:10.1371/journal.pone.0116225
PMCID: PMC4315605  PMID: 25646803
5.  The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry. 
Previous tagging studies of the movements of green turtles (Chelonia mydas) nesting at Ascension Island have shown that they shuttle between this remote target in the Atlantic Ocean and their feeding grounds on the Brazilian coast, a distance of 2300 km or more. Since a knowledge of sea turtle migration routes might allow inferences on the still unknown navigational mechanisms of marine animals, we tracked the postnesting migration of six green turtle females from Ascension Island to Brazil. Five of them reached the proximity of the easternmost stretch of the Brazilian coast, covering 1777-2342 km in 33-47 days. Their courses were impressively similar for the first 1000 km, with three turtles tracked over different dates following indistinguishable paths for the first 300 km. Only the sixth turtle made some relatively short trips in different directions around Ascension. The tracks show that turtles (i) are able to maintain straight courses over long distances in the open sea; (ii) may perform exploratory movements in different directions; (iii) appropriately correct their course during the journey according to external information; and (iv) initially keep the same direction as the west-south-westerly flowing current, possibly guided by chemical cues.
PMCID: PMC1689527  PMID: 9881473
6.  Population structure and phylogeography reveal pathways of colonization by a migratory marine reptile (Chelonia mydas) in the central and eastern Pacific 
Ecology and Evolution  2014;4(22):4317-4331.
Climate, behavior, ecology, and oceanography shape patterns of biodiversity in marine faunas in the absence of obvious geographic barriers. Marine turtles are an example of highly migratory creatures with deep evolutionary lineages and complex life histories that span both terrestrial and marine environments. Previous studies have focused on the deep isolation of evolutionary lineages (>3 mya) through vicariance; however, little attention has been given to the pathways of colonization of the eastern Pacific and the processes that have shaped diversity within the most recent evolutionary time. We sequenced 770 bp of the mtDNA control region to examine the stock structure and phylogeography of 545 green turtles from eight different rookeries in the central and eastern Pacific. We found significant differentiation between the geographically separated nesting populations and identified five distinct stocks (FST = 0.08–0.44, P < 0.005). Central and eastern Pacific Chelonia mydas form a monophyletic group containing 3 subclades, with Hawaii more closely related to the eastern Pacific than western Pacific populations. The split between sampled central/eastern and western Pacific haplotypes was estimated at around 0.34 mya, suggesting that the Pacific region west of Hawaii has been a more formidable barrier to gene flow in C. mydas than the East Pacific Barrier. Our results suggest that the eastern Pacific was colonized from the western Pacific via the Central North Pacific and that the Revillagigedos Islands provided a stepping-stone for radiation of green turtles from the Hawaiian Archipelago to the eastern Pacific. Our results fit with a broader paradigm that has been described for marine biodiversity, where oceanic islands, such as Hawaii and Revillagigedo, rather than being peripheral evolutionary “graveyards”, serve as sources and recipients of diversity and provide a mechanism for further radiation.
doi:10.1002/ece3.1269
PMCID: PMC4267870  PMID: 25540693
Chelonia mydas; genetic stock structure; marine turtles; mtDNA; phylogeography
7.  Migrations of Green Turtles (Chelonia mydas) between Nesting and Foraging Grounds across the Coral Sea 
PLoS ONE  2014;9(6):e100083.
Marine megafauna tend to migrate vast distances, often crossing national borders and pose a significant challenge to managers. This challenge is particularly acute in the Pacific, which contains numerous small island nations and thousands of kilometers of continental margins. The green sea turtle, Chelonia mydas, is one such megafauna that is endangered in Pacific waters due to the overexploitation of eggs and adults for human consumption. Data from long-term tagging programs in Queensland (Australia) and New Caledonia were analysed to investigate the migrations by C. mydas across the Coral Sea between their nesting site and their feeding grounds. A review of data collected over the last 50 years by different projects identified multiple migrations of C. mydas to and from New Caledonia (n = 97) and indicate that turtles foraging in New Caledonia nest in the Great Barrier Reef (Australia) and vice versa. Several explanations exist for turtles exhibiting this energetically costly movement pattern from breeding to distant foraging grounds (1200–2680 km away) despite viable foraging habitat being available in the local vicinity. These include hatchling drift, oceanic movements and food abundance predictability. Most of the tag recoveries in New Caledonia belonged to females from the south Great Barrier Reef genetic stock. Some females (n = 2) even showed fidelity to foraging sites located 1200 km away from the nesting site located in New Caledonia. This study also reveals previously unknown migrations pathways of turtles within the Coral Sea.
doi:10.1371/journal.pone.0100083
PMCID: PMC4062437  PMID: 24940598
8.  Finding the ‘lost years’ in green turtles: insights from ocean circulation models and genetic analysis 
Organismal movement is an essential component of ecological processes and connectivity among ecosystems. However, estimating connectivity and identifying corridors of movement are challenging in oceanic organisms such as young turtles that disperse into the open sea and remain largely unobserved during a period known as ‘the lost years’. Using predictions of transport within an ocean circulation model and data from published genetic analysis, we present to our knowledge, the first basin-scale hypothesis of distribution and connectivity among major rookeries and foraging grounds (FGs) of green turtles (Chelonia mydas) during their ‘lost years’. Simulations indicate that transatlantic dispersal is likely to be common and that recurrent connectivity between the southwestern Indian Ocean and the South Atlantic is possible. The predicted distribution of pelagic juvenile turtles suggests that many ‘lost years hotspots’ are presently unstudied and located outside protected areas. These models, therefore, provide new information on possible dispersal pathways that link nesting beaches with FGs. These pathways may be of exceptional conservation concern owing to their importance for sea turtles during a critical developmental period.
doi:10.1098/rspb.2013.1468
PMCID: PMC3757977  PMID: 23945687
dispersal; distribution; marine turtles; Chelonia mydas; ocean currents; population structure
9.  Artisanal Green Turtle, Chelonia mydas, Fishery of Caribbean Nicaragua: I. Catch Rates and Trends, 1991–2011 
PLoS ONE  2014;9(4):e94667.
This is the first assessment of catch rates for the legal, artisanal green turtle, Chelonia mydas, fishery in Caribbean Nicaragua. Data were collected by community members, monitoring up to 14 landing sites from 1991 to 2011. We examined take levels, and temporal and spatial variability in catch rates for the overall fishery, by region, and community using General Additive Mixed Models (GAMMs). More than 171,556 green turtles were killed during the period, with a mean estimated minimum 8,169±2,182 annually. There was a statistically significant decline in catch rates overall. Catch rates peaked in 1997 and 2002, followed by a downward trend, particularly from mid-2008 to the end of the study period. Similar downward trends were evident in both study regions. Community specific catch rate trends also indicated declines with decreases ranging from 21% to 90%. Decrease in catch rates in Nicaragua is cause for concern even though the principal source rookery at Tortuguero, Costa Rica, shows an increase in nesting activity. Explanations for the apparent discrepancy between the increasing trend at Tortuguero and decreasing catch rate trends in Nicaragua include: i) an increase in reproductive output, ii) insufficient time has passed to observe the impact of the fishery on the rookery due to a time lag, iii) changes in other segments of the population have not been detected since only nesting activity is monitored, iv) the expansive northern Nicaragua foraging ground may provide a refuge for a sufficient portion of the Tortuguero rookery, and/or v) a larger than expected contribution of non-Tortuguero rookeries occurring in Nicaragua turtle fishing areas. Our results highlight the need for close monitoring of rookeries and in-water aggregations in the Caribbean. Where consumptive use still occurs, nations sharing this resource should implement scientifically based limits on exploitation to ensure sustainability and mitigate impacts to regional population diversity.
doi:10.1371/journal.pone.0094667
PMCID: PMC3989241  PMID: 24740258
10.  Fidelity and over-wintering of sea turtles 
While fidelity to breeding sites is well demonstrated in marine turtles, emerging knowledge of migratory routes and key foraging sites is of limited conservation value unless levels of fidelity can be established. We tracked green (Chelonia mydas, n=10) and loggerhead (Caretta caretta, n=10) turtles during their post-nesting migration from the island of Cyprus to their foraging grounds. After intervals of 2–5 years, five of these females were recaptured at the nesting beach and tracked for a second migration. All five used highly similar migratory routes to return to the same foraging and over-wintering areas. None of the females visited other foraging habitats over the study period (units lasted on average 305 days; maximum, 1356 days), moving only to deeper waters during the winter months where they demonstrated extremely long resting dives of up to 10.2 h (the longest breath-holding dive recorded for a marine vertebrate). High levels of fidelity and the relatively discrete nature of the home ranges demonstrate that protection of key migratory pathways, foraging and over-wintering sites can serve as an important tool for the future conservation of marine turtles.
doi:10.1098/rspb.2007.0211
PMCID: PMC2176160  PMID: 17456456
migration; fidelity; foraging; over-wintering; Chelonia mydas; Caretta caretta
11.  Contextualising the Last Survivors: Population Structure of Marine Turtles in the Dominican Republic 
PLoS ONE  2013;8(6):e66037.
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 740bp 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.
doi:10.1371/journal.pone.0066037
PMCID: PMC3686877  PMID: 23840394
12.  Nesting Phenology of Marine Turtles: Insights from a Regional Comparative Analysis on Green Turtle (Chelonia mydas) 
PLoS ONE  2012;7(10):e46920.
Changes in phenology, the timing of seasonal activities, are among the most frequently observed responses to environmental disturbances and in marine species are known to occur in response to climate changes that directly affects ocean temperature, biogeochemical composition and sea level. We examined nesting seasonality data from long-term studies at 8 green turtle (Chelonia mydas) rookeries that include 21 specific nesting sites in the South-West Indian Ocean (SWIO). We demonstrated that temperature drives patterns of nesting seasonality at the regional scale. We found a significant correlation between mean annual Sea Surface Temperature (SST) and dates of peak nesting with rookeries exposed to higher SST having a delayed nesting peak. This supports the hypothesis that temperature is the main factor determining peak nesting dates. We also demonstrated a spatial synchrony in nesting activity amongst multiple rookeries in the northern part of the SWIO (Aldabra, Glorieuses, Mohéli, Mayotte) but not with the eastern and southern rookeries (Europa, Tromelin), differences which could be attributed to females with sharply different adult foraging conditions. However, we did not detect a temporal trend in the nesting peak date over the study period or an inter-annual relation between nesting peak date and SST. The findings of our study provide a better understanding of the processes that drive marine species phenology. The findings will also help to predict their ability to cope with climate change and other environmental perturbations. Despite demonstrating this spatial shift in nesting phenology, no trend in the alteration of nesting dates over more than 20 years was found.
doi:10.1371/journal.pone.0046920
PMCID: PMC3467270  PMID: 23056527
13.  Genetic Structure and Natal Origins of Immature Hawksbill Turtles (Eretmochelys imbricata) in Brazilian Waters 
PLoS ONE  2014;9(2):e88746.
Understanding the connections between sea turtle populations is fundamental for their effective conservation. Brazil hosts important hawksbill feeding areas, but few studies have focused on how they connect with nesting populations in the Atlantic. Here, we (1) characterized mitochondrial DNA control region haplotypes of immature hawksbills feeding along the coast of Brazil (five areas ranging from equatorial to temperate latitudes, 157 skin samples), (2) analyzed genetic structure among Atlantic hawksbill feeding populations, and (3) inferred natal origins of hawksbills in Brazilian waters using genetic, oceanographic, and population size information. We report ten haplotypes for the sampled Brazilian sites, most of which were previously observed at other Atlantic feeding grounds and rookeries. Genetic profiles of Brazilian feeding areas were significantly different from those in other regions (Caribbean and Africa), and a significant structure was observed between Brazilian feeding grounds grouped into areas influenced by the South Equatorial/North Brazil Current and those influenced by the Brazil Current. Our genetic analysis estimates that the studied Brazilian feeding aggregations are mostly composed of animals originating from the domestic rookeries Bahia and Pipa, but some contributions from African and Caribbean rookeries were also observed. Oceanographic data corroborated the local origins, but showed higher connection with West Africa and none with the Caribbean. High correlation was observed between origins estimated through genetics/rookery size and oceanographic/rookery size data, demonstrating that ocean currents and population sizes influence haplotype distribution of Brazil's hawksbill populations. The information presented here highlights the importance of national conservation strategies and international cooperation for the recovery of endangered hawksbill turtle populations.
doi:10.1371/journal.pone.0088746
PMCID: PMC3928279  PMID: 24558419
14.  Genomic Variation of the Fibropapilloma-Associated Marine Turtle Herpesvirus across Seven Geographic Areas and Three Host Species†  
Journal of Virology  2005;79(2):1125-1132.
Fibropapillomatosis (FP) of marine turtles is an emerging neoplastic disease associated with infection by a novel turtle herpesvirus, fibropapilloma-associated turtle herpesvirus (FPTHV). This report presents 23 kb of the genome of an FPTHV infecting a Hawaiian green turtle (Chelonia mydas). By sequence homology, the open reading frames in this contig correspond to herpes simplex virus genes UL23 through UL36. The order, orientation, and homology of these putative genes indicate that FPTHV is a member of the Alphaherpesvirinae. The UL27-, UL30-, and UL34-homologous open reading frames from FPTHVs infecting nine FP-affected marine turtles from seven geographic areas and three turtle species (C. mydas, Caretta caretta, and Lepidochelys olivacea) were compared. A high degree of nucleotide sequence conservation was found among these virus variants. However, geographic variations were also found: the FPTHVs examined here form four groups, corresponding to the Atlantic Ocean, West pacific, mid-Pacific, and east Pacific. Our results indicate that FPTHV was established in marine turtle populations prior to the emergence of FP as it is currently known.
doi:10.1128/JVI.79.2.1125-1132.2005
PMCID: PMC538570  PMID: 15613340
15.  Blood Gases, Biochemistry, and Hematology of Galapagos Green Turtles (Chelonia Mydas) 
PLoS ONE  2014;9(5):e96487.
The green turtle, Chelonia mydas, is an endangered marine chelonian with a circum-global distribution. Reference blood parameter intervals have been published for some chelonian species, but baseline hematology, biochemical, and blood gas values are lacking from the Galapagos sea turtles. Analyses were done on blood samples drawn from 28 green turtles captured in two foraging locations on San Cristóbal Island (14 from each site). Of these turtles, 20 were immature and of unknown sex; the other eight were males (five mature, three immature). A portable blood analyzer (iSTAT) was used to obtain near immediate field results for pH, lactate, pO2, pCO2, HCO3−, Hct, Hb, Na, K, iCa, and Glu. Parameter values affected by temperature were corrected in two ways: (1) with standard formulas; and (2) with auto-corrections made by the iSTAT. The two methods yielded clinically equivalent results. Standard laboratory hematology techniques were employed for the red and white blood cell counts and the hematocrit determination, which was also compared to the hematocrit values generated by the iSTAT. Of all blood analytes, only lactate concentrations were positively correlated with body size. All other values showed no significant difference between the two sample locations nor were they correlated with body size or internal temperature. For hematocrit count, the iSTAT blood analyzer yielded results indistinguishable from those obtained with high-speed centrifugation. The values reported in this study provide baseline data that may be useful in comparisons among populations and in detecting changes in health status among Galapagos sea turtles. The findings might also be helpful in future efforts to demonstrate associations between specific biochemical parameters and disease.
doi:10.1371/journal.pone.0096487
PMCID: PMC4019482  PMID: 24824065
16.  Global Analysis of Anthropogenic Debris Ingestion by Sea Turtles 
Conservation Biology  2013;28(1):129-139.
Ingestion of marine debris can have lethal and sublethal effects on sea turtles and other wildlife. Although researchers have reported on ingestion of anthropogenic debris by marine turtles and implied incidences of debris ingestion have increased over time, there has not been a global synthesis of the phenomenon since 1985. Thus, we analyzed 37 studies published from 1985 to 2012 that report on data collected from before 1900 through 2011. Specifically, we investigated whether ingestion prevalence has changed over time, what types of debris are most commonly ingested, the geographic distribution of debris ingestion by marine turtles relative to global debris distribution, and which species and life-history stages are most likely to ingest debris. The probability of green (Chelonia mydas) and leatherback turtles (Dermochelys coriacea) ingesting debris increased significantly over time, and plastic was the most commonly ingested debris. Turtles in nearly all regions studied ingest debris, but the probability of ingestion was not related to modeled debris densities. Furthermore, smaller, oceanic-stage turtles were more likely to ingest debris than coastal foragers, whereas carnivorous species were less likely to ingest debris than herbivores or gelatinovores. Our results indicate oceanic leatherback turtles and green turtles are at the greatest risk of both lethal and sublethal effects from ingested marine debris. To reduce this risk, anthropogenic debris must be managed at a global level.
Análisis Global de la Ingesta de Residuos Antropogénicos por Tortugas Marinas
La ingesta de residuos marinos puede tener efectos letales y subletales sobre las tortugas marinas y otros animales. Aunque hay investigadores que han reportado la ingesta de residuos antropogénicos por tortugas marinas y la incidencia de la ingesta de residuos ha incrementado con el tiempo, no ha habido una síntesis global del fenómeno desde 1985. Por esto analizamos 37 estudios publicados, desde 1985 hasta 2012, que reportan datos colectados desde antes de 1900 y a lo largo del 2011. Investigamos específicamente si el predominio de la ingesta ha cambiado con el tiempo, qué tipos de residuos se ingieren comúnmente, la distribución geográfica de la ingesta de residuos por tortugas marinas en relación a la distribución global de residuos y cuáles especies y etapas de vida tienen más probabilidad de ingerir residuos. La probabilidad de que las tortugas verdes (Chelonia mydas) y laúd (Dermochelys coriacea) ingieran escombros incrementa significativamente con el tiempo; plástico fue el residuo que más se ingirió. Las tortugas en casi todas las regiones estudiadas ingieren residuos, pero la probabilidad de ingesta no estuvo relacionada con las densidades modeladas de residuos. Además de esto, tortugas más pequeñas, en etapa oceánica de vida, tuvieron una mayor probabilidad de ingerir residuos que las tortugas forrajeras terrestres, mientras que las especies carnívoras tuvieron menos probabilidad de ingerir residuos que las herbívoras o las gelatinívoras. Nuestros resultados indican que las tortugas verdes y laúd tienen el mayor riesgo de efectos letales y subletales de la ingesta de residuos marinos. Para reducir el riesgo, los residuos antropogénicos deben manejarse en un nivel global.
doi:10.1111/cobi.12126
PMCID: PMC4204513  PMID: 23914794
Caretta caretta; Dermochelys coriacea; Eretmochelys imbricata; garbage; Lepidochelys kempii; litter; rubbish; trash; basura; Caretta caretta; Dermochelys coriacea; escombros; Eretmochelys imbricata; Lepidochelys kempii; residuos
17.  Geographic Patterns of Genetic Variation in a Broadly Distributed Marine Vertebrate: New Insights into Loggerhead Turtle Stock Structure from Expanded Mitochondrial DNA Sequences 
PLoS ONE  2014;9(1):e85956.
Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology.
doi:10.1371/journal.pone.0085956
PMCID: PMC3900438  PMID: 24465810
18.  Land Use, Macroalgae, and a Tumor-Forming Disease in Marine Turtles 
PLoS ONE  2010;5(9):e12900.
Wildlife diseases are an increasing concern for endangered species conservation, but their occurrence, causes, and human influences are often unknown. We analyzed 3,939 records of stranded Hawaiian green sea turtles (Chelonia mydas) over 28 years to understand fibropapillomatosis, a tumor-forming disease linked to a herpesvirus. Turtle size is a consistent risk factor and size-standardized models revealed considerable spatial and temporal variability. The disease peaked in some areas in the 1990s, in some regions rates remained constant, and elsewhere rates increased. Land use, onshore of where the turtles feed, may play a role. Elevated disease rates were clustered in watersheds with high nitrogen-footprints; an index of natural and anthropogenic factors that affect coastal eutrophication. Further analysis shows strong epidemiological links between disease rates, nitrogen-footprints, and invasive macroalgae and points to foraging ecology. These turtles now forage on invasive macroalgae, which can dominate nutrient rich waters and sequester environmental N in the amino acid arginine. Arginine is known to regulate immune activity, promote herpesviruses, and contribute to tumor formation. Our results have implications for understanding diseases in aquatic organisms, eutrophication, herpesviruses, and tumor formation.
doi:10.1371/journal.pone.0012900
PMCID: PMC2947502  PMID: 20927370
19.  Eutrophication and the dietary promotion of sea turtle tumors 
PeerJ  2014;2:e602.
The tumor-forming disease fibropapillomatosis (FP) has afflicted sea turtle populations for decades with no clear cause. A lineage of α-herpesviruses associated with these tumors has existed for millennia, suggesting environmental factors are responsible for its recent epidemiology. In previous work, we described how herpesviruses could cause FP tumors through a metabolic influx of arginine. We demonstrated the disease prevails in chronically eutrophied coastal waters, and that turtles foraging in these sites might consume arginine-enriched macroalgae. Here, we test the idea using High-Performance Liquid Chromatography (HPLC) to describe the amino acid profiles of green turtle (Chelonia mydas) tumors and five common forage species of macroalgae from a range of eutrophic states. Tumors were notably elevated in glycine, proline, alanine, arginine, and serine and depleted in lysine when compared to baseline samples. All macroalgae from eutrophic locations had elevated arginine, and all species preferentially stored environmental nitrogen as arginine even at oligotrophic sites. From these results, we estimate adult turtles foraging at eutrophied sites increase their arginine intake 17–26 g daily, up to 14 times the background level. Arginine nitrogen increased with total macroalgae nitrogen and watershed nitrogen, and the invasive rhodophyte Hypnea musciformis significantly outperformed all other species in this respect. Our results confirm that eutrophication substantially increases the arginine content of macroalgae, which may metabolically promote latent herpesviruses and cause FP tumors in green turtles.
doi:10.7717/peerj.602
PMCID: PMC4184234  PMID: 25289187
Superweeds; Luxury consumption; Invasive species; Wastewater; Coastal ecology; Ecosystem based management; Nutrient pollution; Chelonia mydas; Firbropapillomatosis
20.  Global distribution of Chelonid fibropapilloma-associated herpesvirus among clinically healthy sea turtles 
BMC Evolutionary Biology  2014;14(1):206.
Background
Fibropapillomatosis (FP) is a neoplastic disease characterized by cutaneous tumours that has been documented to infect all sea turtle species. Chelonid fibropapilloma-associated herpesvirus (CFPHV) is believed to be the aetiological agent of FP, based principally on consistent PCR-based detection of herpesvirus DNA sequences from FP tumours. We used a recently described PCR-based assay that targets 3 conserved CFPHV genes, to survey 208 green turtles (Chelonia mydas). This included both FP tumour exhibiting and clinically healthy individuals. An additional 129 globally distributed clinically healthy individual sea turtles; representing four other species were also screened.
Results
CFPHV DNA sequences were obtained from 37/37 (100%) FP exhibiting green turtles, and 45/300 (15%) clinically healthy animals spanning all five species. Although the frequency of infected individuals per turtle population varied considerably, most global populations contained at least one CFPHV positive individual, with the exception of various turtle species from the Arabian Gulf, Northern Indian Ocean and Puerto Rico.
Haplotype analysis of the different gene markers clustered the CFPHV DNA sequences for two of the markers (UL18 and UL22) in turtles from Turks and Caicos separate to all others, regardless of host species or geographic origin.
Conclusion
Presence of CFPHV DNA within globally distributed samples for all five species of sea turtle was confirmed. While 100% of the FP exhibiting green turtles yielded CFPHV sequences, surprisingly, so did 15% of the clinically healthy turtles. We hypothesize that turtle populations with zero (0%) CFPHV frequency may be attributed to possible environmental differences, diet and/or genetic resistance in these individuals. Our results provide first data on the prevalence of CFPHV among seemingly healthy turtles; a factor that may not be directly correlated to the disease incidence, but may suggest of a long-term co-evolutionary latent infection interaction between CFPHV and its turtle-host across species. Finally, computational analysis of amino acid variants within the Turks and Caicos samples suggest potential functional importance in a substitution for marker UL18 that encodes the major capsid protein gene, which potentially could explain differences in pathogenicity. Nevertheless, such a theory remains to be validated by further research.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-014-0206-z) contains supplementary material, which is available to authorized users.
doi:10.1186/s12862-014-0206-z
PMCID: PMC4219010  PMID: 25342462
Co-evolution; Sea turtles; Herpesvirus; Fibropapillomatosis; Tumours; Latency; CFPHV
21.  The Role of Geomagnetic Cues in Green Turtle Open Sea Navigation 
PLoS ONE  2011;6(10):e26672.
Background
Laboratory and field experiments have provided evidence that sea turtles use geomagnetic cues to navigate in the open sea. For instance, green turtles (Chelonia mydas) displaced 100 km away from their nesting site were impaired in returning home when carrying a strong magnet glued on the head. However, the actual role of geomagnetic cues remains unclear, since magnetically treated green turtles can perform large scale (>2000 km) post-nesting migrations no differently from controls.
Methodology/Principal Findings
In the present homing experiment, 24 green turtles were displaced 200 km away from their nesting site on an oceanic island, and tracked, for the first time in this type of experiment, with Global Positioning System (GPS), which is able to provide much more frequent and accurate locations than previously used tracking methods. Eight turtles were magnetically treated for 24–48 h on the nesting beach prior to displacement, and another eight turtles had a magnet glued on the head at the release site. The last eight turtles were used as controls. Detailed analyses of water masses-related (i.e., current-corrected) homing paths showed that magnetically treated turtles were able to navigate toward their nesting site as efficiently as controls, but those carrying magnets were significantly impaired once they arrived within 50 km of home.
Conclusions/Significance
While green turtles do not seem to need geomagnetic cues to navigate far from the goal, these cues become necessary when turtles get closer to home. As the very last part of the homing trip (within a few kilometers of home) likely depends on non-magnetic cues, our results suggest that magnetic cues play a key role in sea turtle navigation at an intermediate scale by bridging the gap between large and small scale navigational processes, which both appear to depend on non-magnetic cues.
doi:10.1371/journal.pone.0026672
PMCID: PMC3202557  PMID: 22046329
22.  Chemical Contamination of Green Turtle (Chelonia mydas) Eggs in Peninsular Malaysia: Implications for Conservation and Public Health 
Environmental Health Perspectives  2009;117(9):1397-1401.
Background
Persistent organic pollutants (POPs)—such as organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs)—and heavy metals have been reported in sea turtles at various stages of their life cycle. These chemicals can disrupt development and function of wildlife. Furthermore, in areas such as Peninsular Malaysia, where the human consumption of sea turtle eggs is prevalent, egg contamination may also have public health implications.
Objective
In the present study we investigated conservation and human health risks associated with the chemical contamination of green turtle (Chelonia mydas) eggs in Peninsular Malaysia.
Methods
Fifty-five C. mydas eggs were collected from markets in Peninsular Malaysia and analyzed for POPs and heavy metals. We conducted screening risk assessments (SRAs) and calculated the percent of acceptable daily intake (ADI) for POPs and metals to assess conservation and human health risks associated with egg contamination.
Results
C. mydas eggs were available in 9 of the 33 markets visited. These eggs came from seven nesting areas from as far away as Borneo Malaysia. SRAs indicated a significant risk to embryonic development associated with the observed arsenic concentrations. Furthermore, the concentrations of coplanar PCBs represented 3 300 times the ADI values set by the World Health Organization.
Conclusions
The concentrations of POPs and heavy metals reported in C. mydas eggs from markets in Peninsular Malaysia pose considerable risks to sea turtle conservation and human health.
doi:10.1289/ehp.0900813
PMCID: PMC2737016  PMID: 19750104
C. mydas; heavy metals; human health; persistent organic pollutants; risk assessments
23.  The Distribution and Conservation Status of Green Turtles (Chelonia mydas) and Olive Ridley Turtles (Lepidochelys olivacea) on Pulau Pinang beaches (Malaysia), 1995–2009 
The Green Turtle (Chelonia mydas) and Olive Ridley Turtle (Lepidochelys olivacea) are the only sea turtles with recorded landings in the Pulau Pinang coastal area. The Green Turtle has been the most abundant and widely distributed sea turtle in this area since it was first surveyed in 1995. Statistical analysis by the Pulau Pinang Department of Fisheries on the distribution of sea turtles from 2001 through 2009 has identified Pantai Kerachut and Telok Kampi as the most strongly preferred beaches for Green Turtle landings, with records for almost every month in every year. Green Turtle tracks and nests have also been found along the coast of Pulau Pinang at Batu Ferringhi, Tanjong Bungah, Pantai Medan, Pantai Belanda, Telok Kumbar, Gertak Sanggul, Moonlight Beach, Telok Duyung, Telok Aling, Telok Bahang and Telok Katapang. The Olive Ridley Turtle is present in smaller numbers; landing and nesting have only been recorded on a few beaches. There are no previous records of Olive Ridley landings at Pantai Kerachut and Telok Kampi, but tracks and nests have been found at Telok Kumbar, Tanjong Bungah, Pantai Medan, Telok Duyung and Gertak Sanggul. A Turtle Conservation Centre has been established at Pantai Kerachut to protect these species from extinction in Pulau Pinang. This paper presents details of the records and distribution of sea turtles in Pulau Pinang from 1995 through 2009.
PMCID: PMC3799394  PMID: 24575226
Green Turtle; Pantai Kerachut; Telok Kampi; Distribution; Merambong Tree; Peak Season
24.  Turtle mating patterns buffer against disruptive effects of climate change 
For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2–4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.
doi:10.1098/rspb.2011.2285
PMCID: PMC3321698  PMID: 22279164
marine turtle; temperature-dependent sex determination; climate change; sex ratio; mating patterns; Chelonia mydas
25.  Inferring Foraging Areas of Nesting Loggerhead Turtles Using Satellite Telemetry and Stable Isotopes 
PLoS ONE  2012;7(9):e45335.
In recent years, the use of intrinsic markers such as stable isotopes to link breeding and foraging grounds of migratory species has increased. Nevertheless, several assumptions still must be tested to interpret isotopic patterns found in the marine realm. We used a combination of satellite telemetry and stable isotope analysis to (i) identify key foraging grounds used by female loggerheads nesting in Florida and (ii) examine the relationship between stable isotope ratios and post-nesting migration destinations. We collected tissue samples for stable isotope analysis from 14 females equipped with satellite tags and an additional 57 untracked nesting females. Telemetry identified three post-nesting migratory pathways and associated non-breeding foraging grounds: (1) a seasonal continental shelf–constrained migratory pattern along the northeast U.S. coastline, (2) a non-breeding residency in southern foraging areas and (3) a residency in the waters adjacent to the breeding area. Isotopic variability in both δ13C and δ15N among individuals allowed identification of three distinct foraging aggregations. We used discriminant function analysis to examine how well δ13C and δ15N predict female post-nesting migration destination. The discriminant analysis classified correctly the foraging ground used for all but one individual and was used to predict putative feeding areas of untracked turtles. We provide the first documentation that the continental shelf of the Mid- and South Atlantic Bights are prime foraging areas for a large number (61%) of adult female loggerheads from the largest loggerhead nesting population in the western hemisphere and the second largest in the world. Our findings offer insights for future management efforts and suggest that this technique can be used to infer foraging strategies and residence areas in lieu of more expensive satellite telemetry, enabling sample sizes that are more representative at the population level.
doi:10.1371/journal.pone.0045335
PMCID: PMC3447946  PMID: 23028943

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