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Concept: Leatherback turtle

569

Climate change affects species and ecosystems around the globe [1]. The impacts of rising temperature are particularly pertinent in species with temperature-dependent sex determination (TSD), where the sex of an individual is determined by incubation temperature during embryonic development [2]. In sea turtles, the proportion of female hatchlings increases with the incubation temperature. With average global temperature predicted to increase 2.6°C by 2100 [3], many sea turtle populations are in danger of high egg mortality and female-only offspring production. Unfortunately, determining the sex ratios of hatchlings at nesting beaches carries both logistical and ethical complications. However, sex ratio data obtained at foraging grounds provides information on the amalgamation of immature and adult turtles hatched from different nesting beaches over many years. Here, for the first time, we use genetic markers and a mixed-stock analysis (MSA), combined with sex determination through laparoscopy and endocrinology, to link male and female green turtles foraging in the Great Barrier Reef (GBR) to the nesting beach from which they hatched. Our results show a moderate female sex bias (65%-69% female) in turtles originating from the cooler southern GBR nesting beaches, while turtles originating from warmer northern GBR nesting beaches were extremely female-biased (99.1% of juvenile, 99.8% of subadult, and 86.8% of adult-sized turtles). Combining our results with temperature data show that the northern GBR green turtle rookeries have been producing primarily females for more than two decades and that the complete feminization of this population is possible in the near future.

Concepts: Male, Sex, Reptile, Great Barrier Reef, Sex ratio, Hawksbill turtle, Leatherback turtle, Sea turtle

207

Ingestion of artificial debris is considered as a significant stress for wildlife including sea turtles. To investigate how turtles react to artificial debris under natural conditions, we deployed animal-borne video cameras on loggerhead and green turtles in addition to feces and gut contents analyses from 2007 to 2015. Frequency of occurrences of artificial debris in feces and gut contents collected from loggerhead turtles were 35.7% (10/28) and 84.6% (11/13), respectively. Artificial debris appeared in all green turtles in feces (25/25) and gut contents (10/10), and green turtles ingested more debris (feces; 15.8 ± 33.4 g, gut; 39.8 ± 51.2 g) than loggerhead turtles (feces; 1.6 ± 3.7 g, gut; 9.7 ± 15.0 g). In the video records (60 and 52.5 hours from 10 loggerhead and 6 green turtles, respectively), turtles encountered 46 artificial debris and ingested 23 of them. The encounter-ingestion ratio of artificial debris in green turtles (61.8%) was significantly higher than that in loggerhead turtles (16.7%). Loggerhead turtles frequently fed on gelatinous prey (78/84), however, green turtles mainly fed marine algae (156/210), and partly consumed gelatinous prey (10/210). Turtles seemed to confuse solo drifting debris with their diet, and omnivorous green turtles were more attracted by artificial debris.

Concepts: Eating, Ingestion, Coprophagia, Camera, Leatherback turtle, Sea turtle, Loggerhead Sea Turtle, Sea turtles

183

Herbivory is widely accepted as a vital function on coral reefs. To date, the majority of studies examining herbivory in coral reef environments have focused on the roles of fishes and/or urchins, with relatively few studies considering the potential role of macroherbivores in reef processes. Here, we introduce evidence that highlights the potential role of marine turtles as herbivores on coral reefs. While conducting experimental habitat manipulations to assess the roles of herbivorous reef fishes we observed green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) showing responses that were remarkably similar to those of herbivorous fishes. Reducing the sediment load of the epilithic algal matrix on a coral reef resulted in a forty-fold increase in grazing by green turtles. Hawksbill turtles were also observed to browse transplanted thalli of the macroalga Sargassum swartzii in a coral reef environment. These responses not only show strong parallels to herbivorous reef fishes, but also highlight that marine turtles actively, and intentionally, remove algae from coral reefs. When considering the size and potential historical abundance of marine turtles we suggest that these potentially valuable herbivores may have been lost from many coral reefs before their true importance was understood.

Concepts: Algae, Coral, Coral reef, Herbivore, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle

180

The effect of climate warming on the reproductive success of ectothermic animals is currently a subject of major conservation concern. However, for many threatened species, we still know surprisingly little about the extent of naturally occurring adaptive variation in heat-tolerance. Here, we show that the thermal tolerances of green turtle (Chelonia mydas) embryos in a single, island-breeding population have diverged in response to the contrasting incubation temperatures of nesting beaches just a few kilometres apart. In natural nests and in a common-garden rearing experiment, the offspring of females nesting on a naturally hot (black sand) beach survived better and grew larger at hot incubation temperatures compared with the offspring of females nesting on a cooler (pale sand) beach nearby. These differences were owing to shallower thermal reaction norms in the hot beach population, rather than shifts in thermal optima, and could not be explained by egg-mediated maternal effects. Our results suggest that marine turtle nesting behaviour can drive adaptive differentiation at remarkably fine spatial scales, and have important implications for how we define conservation units for protection. In particular, previous studies may have underestimated the extent of adaptive structuring in marine turtle populations that may significantly affect their capacity to respond to environmental change.

Concepts: Reptile, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle, Kemp's Ridley, Turtle soup, Bycatch

174

A major interest has recently emerged in understanding how telomere shortening, mechanism triggering cell senescence, is linked to organism ageing and life history traits in wild species. However, the links between telomere length and key history traits such as reproductive performances have received little attention and remain unclear to date. The leatherback turtle Dermochelys coriacea is a long-lived species showing rapid growth at early stages of life, one of the highest reproductive outputs observed in vertebrates and a dichotomised reproductive pattern related to migrations lasting 2 or 3 years, supposedly associated with different environmental conditions. Here we tested the prediction of blood telomere shortening with age in this species and investigated the relationship between blood telomere length and reproductive performances in leatherback turtles nesting in French Guiana. We found that blood telomere length did not differ between hatchlings and adults. The absence of blood telomere shortening with age may be related to an early high telomerase activity. This telomere-restoring enzyme was formerly suggested to be involved in preventing early telomere attrition in early fast-growing and long-lived species, including squamate reptiles. We found that within one nesting cycle, adult females having performed shorter migrations prior to the considered nesting season had shorter blood telomeres and lower reproductive output. We propose that shorter blood telomeres may result from higher oxidative stress in individuals breeding more frequently (i.e., higher costs of reproduction) and/or restoring more quickly their body reserves in cooler feeding areas during preceding migration (i.e., higher foraging costs). This first study on telomeres in the giant leatherback turtle suggests that blood telomere length predicts not only survival chances, but also reproductive performances. Telomeres may therefore be a promising new tool to evaluate individual reproductive quality which could be useful in such species of conservation concern.

Concepts: Senescence, Organism, Turtle, Telomere, Costa Rica, Hawksbill turtle, Leatherback turtle, Sea turtle

172

Current understanding of the factors influencing hawksbill sea turtle (Eretmochelys imbricata) hatch success is disparate and based on relatively short-term studies or limited sample sizes. Because global populations of hawksbills are heavily depleted, evaluating the parameters that impact hatch success is important to their conservation and recovery. Here, we use data collected by the Jumby Bay Hawksbill Project (JBHP) to investigate hatch success. The JBHP implements saturation tagging protocols to study a hawksbill rookery in Antigua, West Indies. Habitat data, which reflect the varied nesting beaches, are collected at egg deposition, and nest contents are exhumed and categorized post-emergence. We analyzed hatch success using mixed-model analyses with explanatory and predictive datasets. We incorporated a random effect for turtle identity and evaluated environmental, temporal and individual-based reproductive variables. Hatch success averaged 78.6% (SD: 21.2%) during the study period. Highly supported models included multiple covariates, including distance to vegetation, deposition date, individual intra-seasonal nest number, clutch size, organic content, and sand grain size. Nests located in open sand were predicted to produce 10.4 more viable hatchlings per clutch than nests located >1.5 m into vegetation. For an individual first nesting in early July, the fourth nest of the season yielded 13.2 more viable hatchlings than the initial clutch. Generalized beach section and inter-annual variation were also supported in our explanatory dataset, suggesting that gaps remain in our understanding of hatch success. Our findings illustrate that evaluating hatch success is a complex process, involving multiple environmental and individual variables. Although distance to vegetation and hatch success were inversely related, vegetation is an important component of hawksbill nesting habitat, and a more complete assessment of the impacts of specific vegetation types on hatch success and hatchling sex ratios is needed. Future research should explore the roles of sand structure, nest moisture, and local weather conditions.

Concepts: Coral reef, Sand, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle, Kemp's Ridley, Sea turtles

171

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.

Concepts: Oceanography, Ocean, Sea surface temperature, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle, Turtle soup

169

Our understanding of global seagrass ecosystems comes largely from regions characterized by human impacts with limited data from habitats defined as notionally pristine. Seagrass assessments also largely focus on shallow-water coastal habitats with comparatively few studies on offshore deep-water seagrasses. We satellite tracked green turtles (Chelonia mydas), which are known to forage on seagrasses, to a remote, pristine deep-water environment in the Western Indian Ocean, the Great Chagos Bank, which lies in the heart of one of the world’s largest marine protected areas (MPAs). Subsequently we used in-situ SCUBA and baited video surveys to survey the day-time sites occupied by turtles and discovered extensive monospecific seagrass meadows of Thalassodendron ciliatum. At three sites that extended over 128 km, mean seagrass cover was 74% (mean range 67-88% across the 3 sites at depths to 29 m. The mean species richness of fish in seagrass meadows was 11 species per site (mean range 8-14 across the 3 sites). High fish abundance (e.g. Siganus sutor: mean MaxN.site-1 = 38.0, SD = 53.7, n = 5) and large predatory shark (Carcharhinus amblyrhynchos) (mean MaxN.site-1 = 1.5, SD = 0.4, n = 5) were recorded at all sites. Such observations of seagrass meadows with large top predators, are limited in the literature. Given that the Great Chagos Bank extends over approximately 12,500 km2and many other large deep submerged banks exist across the world’s oceans, our results suggest that deep-water seagrass may be far more abundant than previously suspected.

Concepts: Coral reef, Atlantic Ocean, Indian Ocean, Ocean, Chagos Archipelago, Leatherback turtle, Green turtle, Seagrass

167

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.

Concepts: Coral reef, Atlantic Ocean, Brazil, South America, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle

161

Terrestrial plants use an array of animals as vectors for dispersal, however little is known of biotic dispersal of marine angiosperms such as seagrasses. Our study in the Great Barrier Reef confirms for the first time that dugongs (Dugong dugon) and green sea turtles (Chelonia mydas) assist seagrass dispersal. We demonstrate that these marine mega-herbivores consume and pass in faecal matter viable seeds for at least three seagrass species (Zostera muelleri, Halodule uninervis and Halophila decipiens). One to two seagrass seeds per g DW of faecal matter were found during the peak of the seagrass reproductive season (September to December), with viability on excretion of 9.13% ± 4.61% (SE). Using population estimates for these mega-herbivores, and data on digestion time (hrs), average daily movement (km h) and numbers of viable seagrass seeds excreted (per g DW), we calculated potential seagrass seed dispersal distances. Dugongs and green sea turtle populations within this region can disperse >500,000 viable seagrass seeds daily, with a maximum dispersal distance of approximately 650 km. Biotic dispersal of tropical seagrass seeds by dugongs and green sea turtles provides a large-scale mechanism that enhances connectivity among seagrass meadows, and aids in resilience and recovery of these coastal habitats.

Concepts: Great Barrier Reef, Hawksbill turtle, Leatherback turtle, Sea turtle, Green turtle, Kemp's Ridley, Seagrass, Dugong