Unusual gut contents in a Cretaceous ichthyosaur

Despite ichthyosaurs being one of the most extensively studied Mesozoic marine reptile groups, there is little documented direct evidence of dietary habits in most taxa. Here, we report the discovery of hatchling-sized marine protostegid turtle remains and an enantiornithine bird (in association with actinopterygian fish and phosphatic nodules) within the body cavity of a gravid female ichthyosaur (Platypterygius longmani) from the Lower Cretaceous of Australia; this is the first evidence, to our knowledge, of feeding by ichthyosaurs upon both turtles and birds. The exceptionally preserved gut contents show little evidence of digestion, suggesting consumption shortly before the ichthyosaur's death. Poor swimming ability may have made hatchling turtles easy prey that could have been either swallowed whole or processed by shake feeding. Ingestion of bird remains probably occurred through scavenging. Opportunistic feeding on vertebrates is at odds with existing interpretations of dietary habits in Cretaceous ichthyosaurs, which favour predation primarily upon cephalopods. Such specialization is considered a contributing factor in the group's ultimate extinction. However, the evidence here that at least some forms were able to use a wide range of available food types suggests that the decline of ichthyosaurs in the mid-Cretaceous may be linked to other factors such as competition with ecologically analogous pursuit predators.     

First records of dive durations for a hibernating sea turtle

The first published record, from the early 1970s, of hibernation in sea turtles is based on the reports of the indigenous Indians and fishermen from Mexico, who hunted dormant green turtles (Chelonia mydas) in the Gulf of California. However, there were no successful attempts to investigate the biology of this particular behaviour further. Hence, data such as the exact duration and energetic requirements of dormant winter submergences are lacking. We used new satellite relay data loggers to obtain the first records of up to 7h long dives of a loggerhead turtle (Caretta caretta) overwintering in Greek waters. These represent the longest dives ever reported for a diving marine vertebrate. There is strong evidence that the dives were aerobic, because the turtle surfaced only for short intervals and before the calculated oxygen stores were depleted. This evidence suggests that the common belief that sea turtles hibernate underwater, as some freshwater turtles do, is incorrect.     

First records of flipper beat frequency during sea turtle diving

Depth and flipper movements were simultaneously measured during 23 dives for a free-swimming green turtle (Chelonia mydas) at Ascension Island. A few characteristic dive profiles that have been widely reported in hard-shelled turtles were recorded. Flipper movements revealed that, on dives to midwater, there was generally active swimming, compared to long periods of inactivity on dives to the seafloor. During all dives, there were clear changes in the flipper beat frequency during the descent. On leaving the surface, flippers beats occurred quickly (typically 30-40 beats min⁻¹) and then as the descent continued the frequency declined (typically to about 10-14 beats min⁻¹). These observations match the general pattern reported for other air-breathing divers for increased effort at the start of the descent to overcome initial positive buoyancy.     

Fungal infection of sea turtle eggs in the sea turtle hatcheries in Peninsular Malaysia

Fungal infection in sea turtle nests has become a potential threat to sea turtle embryos. We screened the hatchery nest sand, eggshells of failed eggs, and stillbirths of green turtles and hawksbills collected from hatcheries in Malacca, Pahang, Perak and Terengganu for the presence of fungi. The DNA sequence of the ITS region of the three highest occurring isolated fungi confirmed that these species were Pseudallescheria ellipsoidea (35.4%), Scedosporium aurantiacum (27.2%), and Fusarium solani (22.0%). Morphological characteristics of these fungi were recorded. Although the total fungi abundance had no significant effect on hatching success (p > 0.05), the abundance of P. ellipsoidea significantly increased mortality in the nests (r = 0.70, p < 0.05). Future research should focus on understanding the biological aspects of this species to establish a more effective mitigation technique for the prevention of fungal infection of sea turtle eggs and hatchery employees.     

Reproductive synchrony in a recovering bottlenecked sea turtle population

1. The assessment of species extinction risk has been well established for some time now. Assessing the potential for recovery in endangered species is however much more challenging, because complementary approaches are required to detect reliable signals of positive trends. 2. This study combines genetics, demography and behavioural data at three different time-scales to assess historical and recent population changes and evidence of reproductive synchrony in a small population of olive ridley sea turtle Lepidochelys olivacea. Lepidochelys is considered as the most extraordinary example of reproductive synchrony in reptiles, yet to date, it has only been reported in large populations. 3. Using Bayesian coalescent-based models on microsatellite nuclear DNA variability, we demonstrate that effective population size in olive ridleys nesting in French Guiana has dramatically declined by 99% over the last 20 centuries. This low current population size is further illustrated by the absence of genetic mitochondrial DNA diversity in the present nesting population. Yet, monitoring of nesting sites in French Guiana suggests a possible recovery of the population over the last decade. 4. Satellite telemetry shows that over the first 14 days of their 28-days inter-nesting interval, i.e. when eggs maturation is likely to occur, gravid females disperse over the continental shelf. They then gather together with a striking spatiotemporal consistency close to the nesting site, where they later emerge for their second nesting event. 5. Our results therefore suggest that reproductive synchrony also occurs in small populations. Olive ridleys may ensure this synchrony by adjusting the duration of the second half of their inter-nesting interval prior to landing, possibly through social mediation. 6. Such reproductive synchrony may be related to the maintenance of some species-specific strategy despite former collapse and may contribute to the present population recovery. The gregarious behaviour of reproductive individuals close to shore where human-induced perturbations occur is however a cause for conservation concern for this still poorly known species.     

Energetics of swimming of a sea turtle.

Young (mean mass 735 g) green turtles (Chelonia mydas) were able to swim in a water channel at sustained speeds between 0-14 and 0-35 m.s-1. Oxygen consumption at rest was was 0-07 l.kg-1.h-1; at maximum swimming speed oxygen consumption was 3-4 times greater than at rest for a given individual. In comparison with other animals of the same body mass the cost of transport for the green turtle (0.186lO2.kg-1.km-1) is less than that for flying birds but greater than that for fish. From drag measurements it was calculated that the aerobic efficiency of swimming was between 1 and 10%; the higher efficiencies were found at the higher swimming speeds. Based upon the drag calculations for young turtles, it is estimated that adult turtles making the round-trip breeding migration between Brazil and Ascension Island (4800 km) would require the equivalent of about 21% of their body mass in fat stores to account for the energetic cost of swimming.     

Oxygen transport in the green sea turtle

Summary Green sea turtles (Chelonia mydas) are well known as endurance swimmers and divers. Physiological correlates of these traits were studied in 9 adult sea turtles (mean body mass=87 kg) at a body temperature of 25°C. The respiratory properties of the blood were similar to those of other turtles except for a higher oxygen affinity (P ₅₀=18.2 Torr, pH 7.6), which may be an allometric function. Resting, systemic blood flow, calculated from the Fick principle was 21.5 ml·kg⁻¹. min⁻¹, similar to values reported for other turtles. Pulmonary blood flow, measured by mass spectrometry of acetylene uptake in the lungs was 24.0 ml·kg⁻¹·min⁻¹, not significantly different from the calculated systemic flow. Other evidence of a small (net) intracardiac shunt is the high arterial saturation (ca. 90%) of arterial blood. This distinctive feature of O₂ transport inC. mydas provides an content difference of 4.1 ml· dl⁻¹. This results in a relatively low blood convection requirement at rest =24.4 mlbtps·mlstpd ⁻¹), similar to that for many mammals. This would favor a high maximum O₂ uptake, as measured by others in this species. The relatively high O₂ affinity of blood in this species could be adaptive to “loading” O₂ during intermittent breathing while swimming and to utilizing the lung O₂ store during the progressive hypoxia of diving.     

Forecasting the viability of sea turtle eggs in a warming world

Animals living in tropical regions may be at increased risk from climate change because current temperatures at these locations already approach critical physiological thresholds. Relatively small temperature increases could cause animals to exceed these thresholds more often, resulting in substantial fitness costs or even death. Oviparous species could be especially vulnerable because the maximum thermal tolerances of incubating embryos is often lower than adult counterparts, and in many species mothers abandon the eggs after oviposition, rendering them immobile and thus unable to avoid extreme temperatures. As a consequence, the effects of climate change might become evident earlier and be more devastating for hatchling production in the tropics. Loggerhead sea turtles (Caretta caretta) have the widest nesting range of any living reptile, spanning temperate to tropical latitudes in both hemispheres. Currently, loggerhead sea turtle populations in the tropics produce nearly 30% fewer hatchlings per nest than temperate populations. Strong correlations between empirical hatching success and habitat quality allowed global predictions of the spatiotemporal impacts of climate change on this fitness trait. Under climate change, many sea turtle populations nesting in tropical environments are predicted to experience severe reductions in hatchling production, whereas hatching success in many temperate populations could remain unchanged or even increase with rising temperatures. Some populations could show very complex responses to climate change, with higher relative hatchling production as temperatures begin to increase, followed by declines as critical physiological thresholds are exceeded more frequently. Predicting when, where, and how climate change could impact the reproductive output of local populations is crucial for anticipating how a warming world will influence population size, growth, and stability.     

Time in tortoiseshell: a bomb radiocarbon-validated chronology in sea turtle scutes

Some of the most basic questions of sea turtle life history are also the most elusive. Many uncertainties surround lifespan, growth rates, maturity and spatial structure, yet these are critical factors in assessing population status. Here we examine the keratinized hard tissues of the hawksbill (Eretmochelys imbricata) carapace and use bomb radiocarbon dating to estimate growth and maturity. Scutes have an established dietary record, yet the large keratin deposits of hawksbills evoke a reliable chronology. We sectioned, polished and imaged posterior marginal scutes from 36 individual hawksbills representing all life stages, several Pacific populations and spanning eight decades. We counted the apparent growth lines, microsampled along growth contours and calibrated Δ¹⁴C values to reference coral series. We fit von Bertalanffy growth function (VBGF) models to the results, producing a range of age estimates for each turtle. We find Hawaii hawksbills deposit eight growth lines annually (range 5–14), with model ensembles producing a somatic growth parameter (k) of 0.13 (range 0.1–0.2) and first breeding at 29 years (range 23–36). Recent bomb radiocarbon values also suggest declining trophic status. Together, our results may reflect long-term changes in the benthic community structure of Hawaii reefs, and possibly shed light on the critical population status for Hawaii hawksbills.     

Long-term climate forcing in loggerhead sea turtle nesting

The long-term variability of marine turtle populations remains poorly understood, limiting science and management. Here we use basin-scale climate indices and regional surface temperatures to estimate loggerhead sea turtle (Caretta caretta) nesting at a variety of spatial and temporal scales. Borrowing from fisheries research, our models investigate how oceanographic processes influence juvenile recruitment and regulate population dynamics. This novel approach finds local populations in the North Pacific and Northwest Atlantic are regionally synchronized and strongly correlated to ocean conditions--such that climate models alone explain up to 88% of the observed changes over the past several decades. In addition to its performance, climate-based modeling also provides mechanistic forecasts of historical and future population changes. Hindcasts in both regions indicate climatic conditions may have been a factor in recent declines, but future forecasts are mixed. Available climatic data suggests the Pacific population will be significantly reduced by 2040, but indicates the Atlantic population may increase substantially. These results do not exonerate anthropogenic impacts, but highlight the significance of bottom-up oceanographic processes to marine organisms. Future studies should consider environmental baselines in assessments of marine turtle population variability and persistence.     

Metabolic heating in Mediterranean loggerhead sea turtle clutches

Offspring sex ratio is an important demographic parameter and, given its determination by incubation temperature in sea turtles, might be a key factor for their conservation under climate warming. An appealing approach to estimate hatchling sex ratios is to measure sand temperatures at nest depth and deduce hatchling sex ratios from a beforehand-established relationship of hatchling sex ratio and sand temperature. Such estimates will only be accurate though if metabolic heat produced by the embryos is considered. Judging whether metabolic heating has a potential effect on hatchling sex ratios without actually measuring temperature within clutches would greatly facilitate monitoring protocols. We tested for a relationship between the amount of metabolic heating and the number of developed embryos as well as clutch size in the largest known loggerhead sea turtle (Caretta caretta) population of the Mediterranean on Zakynthos (Greece). Temperatures were measured within 20 nests as well as at a reference site in the sand at nest depth. Metabolic heating was detected, but only during the last third of the incubation period did nests heat up considerably (1.6 °C on average) above the temperature of the surrounding sand. During the middle third of incubation, when sex is determined, the amount of metabolic heating was negligible. The amount of metabolic heating during the last third of the incubation duration was significantly correlated to the number of offspring developed to at least about 75% of incubation duration. This factor explained nearly 50% of variation in metabolic heating. Metabolic heating was also significantly correlated to clutch size. Given that clutch size within the Mediterranean is largest in Zakynthos loggerheads, we conclude that metabolic heating can be ignored in the estimate of hatchling sex ratios in Mediterranean loggerhead populations. These results thus provide the basis for a feasible monitoring of hatchling sex ratios in the loggerhead sea turtle in the Mediterranean.     

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.     

The First Jurassic turtle from India

A primitive cryptodiran turtle, Indochelys spatulata gen. et sp. nov., is described from the Early Jurassic Kota Formation, a member of the Upper Gondwana Group in the Pranhita-Godavari Valley, Deccan, India. The shell morphology of Indochelys differs substantially from that of the Triassic Proganochelys of Germany but is significantly similar to the oldest known Early Jurassic cryptodire, Kayentachelys , from the Kayenta Formation of Arizona. Indochelys also shares many shell characters with the Late Jurassic North American turtles, in particular Dinochelys . The new family Indochelyidae is proposed, which probably has the same phyletic status as that of Kayentachelyidae, with both evolving simultaneously in different regions.     

Effects of hybridization on sea turtle fitness

Sea turtle hybridization is a common phenomenon in Brazil between loggerheads (Caretta caretta) and hawksbills (Eretmochelys imbricata) as well as between loggerheads and olive ridleys (Lepidochelys olivacea). In a previous study we showed that the reproductive output of loggerhead/hawksbill hybrids is similar to that of parental species, suggesting no negative effect of hybridization at this life stage. In this study, we used pooled amplicon sequencing to assign species identity to dams and their progeny, and to investigate the fitness consequences of hybridization, using hatchling viability as a proxy for fitness. We genotyped 4829 hatchlings from egg clutches laid by 78 loggerheads, 13 hawksbills, seven loggerhead/hawksbill hybrids, and three loggerhead/olive ridley hybrids. The proportion of viable hybrid (heterozygous) hatchlings was similar to that of homozygous hatchlings (based on data at two loci), independent of the dam’s genotype. Multiple species paternity was observed in 35.7% of the nests. Both hybrid males and females were fertile and produced viable offspring, and we found no evidence for hybrid breakdown. We suggest a genome-wide study of the hybrids and parental species to better characterize hybrids, as well as studies on additional demographic and ecological parameters to further assess the effects of hybridization and its consequences for sea turtles and their environment.     

The 'lost year' of the sea turtle

The extent to which the vagaries of the history of biology have influenced subsequent developments is often surprising. In particular, the early dichotomies between individual fields of enquiry have sometimes led to the disregard of important biological phenomena. The development of biological oceanography over the last 100 years provides an interesting example.     

Ammonite morphotypes as indicators of oxygenation in a Cretaceous epicontinental sea

An examination of ammonite morphotypes through stratigraphic sections of the Greenhorn Cyclothem of the Cretaceous Western Interior suggests that they may be useful indicators of oxygenation within ancient epicontinental seas. Because some morphotypes appear to reflect a nektobenthic and others a pelagic habitat, the presence of specific morphotypes may be used to indicate benthic and water-column oxygenation, respectively. At the same time, their absence may provide a valuable indicator of dysaerobic to anaerobic conditions that may have promoted the development of petroleum source rocks. □ Ammonites, anoxia, Cretaceous, Greenhorn Cyclothem, western Interior.     

Climate change resilience of a globally important sea turtle nesting population

Few studies have looked into climate change resilience of populations of wild animals. We use a model higher vertebrate, the green sea turtle, as its life history is fundamentally affected by climatic conditions, including temperature‐dependent sex determination and obligate use of beaches subject to sea level rise (SLR). We use empirical data from a globally important population in West Africa to assess resistance to climate change within a quantitative framework. We project 200 years of primary sex ratios (1900–2100) and create a digital elevation model of the nesting beach to estimate impacts of projected SLR. Primary sex ratio is currently almost balanced, with 52% of hatchlings produced being female. Under IPCC models, we predict: (a) an increase in the proportion of females by 2100 to 76%–93%, but cooler temperatures, both at the end of the nesting season and in shaded areas, will guarantee male hatchling production; (b) IPCC SLR scenarios will lead to 33.4%–43.0% loss of the current nesting area; (c) climate change will contribute to population growth through population feminization, with 32%–64% more nesting females expected by 2120; (d) as incubation temperatures approach lethal levels, however, the population will cease growing and start to decline. Taken together with other factors (degree of foraging plasticity, rookery size and trajectory, and prevailing threats), this nesting population should resist climate change until 2100, and the availability of spatial and temporal microrefugia indicates potential for resilience to predicted impacts, through the evolution of nest site selection or changes in nesting phenology. This represents the most comprehensive assessment to date of climate change resilience of a marine reptile using the most up‐to‐date IPCC models, appraising the impacts of temperature and SLR, integrated with additional ecological and demographic parameters. We suggest this as a framework for other populations, species and taxa.