Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Marine turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remain largely unknown. Additionally, many populations have declined drastically due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for green (Chelonia mydas) and leatherback (Dermochelys coriacea) turtles, representing the two extant marine turtle families (MRCA ~60 MYA). Generally, these genomes are highly syntenic and homologous. Non-collinearity was associated with higher copy numbers of immune, zinc-finger, or olfactory receptor (OR) genes in green turtles. Gene family analyses suggested that ORs related to waterborne odorants have expanded in green turtles and contracted in leatherbacks, which may underlie immunological and sensory adaptations assisting navigation and occupancy of neritic versus pelagic environments, and diet specialization. Microchromosomes showed reduced collinearity, and greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, demographic history and diversity analyses showed stark contrasts between species, indicating that leatherback turtles have had a low yet stable effective population size, extremely low diversity when compared to other reptiles, and a higher proportion of deleterious variants, reinforcing concern over the persistence of this species under future climate scenarios. These highly contiguous genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.

Time-Varying Stock-Recruitment Model For Estimating Population Characteristics of Green Turtles

The stock-recruitment relationship (SR), customarily used in fisheries assessment, can be used to analyze demographic data of sea turtles to infer changes in hatchling production (R) as a function of nester abundance (S), recruitment rates and the influence of environmental conditions on these population features. The SR Cushing model (R=aS^b), where a and b are the model parameters) is well-suited for representing the dynamics of recovering populations, such as the green turtle (Chelonia mydas) in Campeche, Mexico. This study aimed to explore the SR Cushing model using a time series of the abundance of nesters and hatchlings (1984–2020). By applying local regressions (9-yr moving windows), we found that the time series of parameter b (the change in R as a function of S) and the recruitment rate (hatchlings per nester) were inversely correlated with a 26-yr cycle of the Atlantic Multidecadal Oscillation –sea surface temperature (SST), over the Atlantic– (r^2=0.83) and (r^2=0.64), respectively, at a 3-yr lag). Model diagnostics using the time-dependent Cushing model substantiated that the log-normal distribution of hatchlings of C. mydas in Campeche depends on the abundance of nesting females and on a low frequency SST signal (r^2=0.98). The positive trend in nester numbers of green turtles in Campeche during the past 44 years may be the result of persistent conservation efforts, while the drastic and sporadic changes in the growth rate of annual arrivals and hatchling production are suggestive of population dynamics driven by low frequency, basin-wide environmental signals.

Inter-Nesting Movements, Migratory Pathways, and Resident Foraging Areas of Green Sea Turtles (Chelonia mydas) Satellite-Tagged in Southwest Florida

Globally, sea turtle research and conservation efforts are underway to identify important high-use areas where these imperiled individuals may be resident for weeks to months to years. In the southeastern Gulf of Mexico, recent telemetry studies highlighted post-nesting foraging sites for federally endangered green turtles (Chelonia mydas) around the Florida Keys. In order to delineate additional areas that may serve as inter-nesting, migratory, and foraging hotspots for reproductively active females nesting in peninsular southwest Florida, we satellite-tagged 14 green turtles that nested at two sites along the southeast Gulf of Mexico coastline between 2017 and 2019: Sanibel and Keewaydin Islands. Prior to this study, green turtles nesting in southwest Florida had not previously been tracked and their movements were unknown. We used switching state space modeling to show that an area off Cape Sable (Everglades), Florida Bay, and the Marquesas Keys are important foraging areas that support individuals that nest on southwest Florida mainland beaches. Turtles were tracked for 39–383 days, migrated for a mean of 4 days, and arrived at their respective foraging grounds in the months of July through September. Turtles remained resident in their respective foraging sites until tags failed, typically after several months, where they established mean home ranges (50% kernel density estimate) of 296 km2. Centroid locations for turtles at common foraging sites were 1.2–36.5 km apart. The area off southwest Florida Everglades appears to be a hotspot for these turtles during both inter-nesting and foraging; this location was also used by turtles that were previously satellite tagged in the Dry Tortugas after nesting. Further evaluation of this important habitat is warranted. Understanding where and when imperiled yet recovering green turtles forage and remain resident is key information for designing surveys of foraging resources and developing additional protection strategies intended to enhance population recovery trajectories.

eDNA metabarcoding for diet analyses of green sea turtles (Chelonia mydas)

Understanding sea turtle diets can help conservation planning, but their trophic ecology is complex due to life history characteristics such as ontogenetic shifts and large foraging ranges. Studying sea turtle diet is challenging, particularly where ecological foraging observations are not possible. Here, we test a new minimally invasive method for the identification of diet items in sea turtles. We fingerprinted diet content using DNA from esophageal and cloacal swab samples by metabarcoding the 18S rRNA gene. This approach was tested on samples collected from green turtles (Chelonia mydas) from a juvenile foraging aggregation in the Bijagós archipelago in Guinea-Bissau. Esophagus samples (n = 6) exhibited a higher dietary richness (11 ± 5 amplicon sequence variants (ASVs) per sample; average ± SD) than cloacal ones (n = 5; 8 ± 2 ASVs). Overall, the diet was dominated by red macroalgae (Rhodophyta; 48.2 ± 16.3% of all ASVs), with the main food item in the esophagus and cloaca being a red alga belonging to the Rhodymeniophycidae subclass (35.1 ± 27.2%), followed by diatoms (Bacillariophyceae; 7.5 ± 7.3%), which were presumably consumed incidentally. Seagrass and some invertebrates were also present. Feeding on red algae was corroborated by field observations and barcoding of food items available in the benthic habitat, validating the approach for identifying diet content. We conclude that identification of food items using metabarcoding of esophageal swabs is useful for a better understanding of the relationships between the feeding behavior of sea turtles and their environment.

Evidence for Host Selectivity and Specialization by Epizoic Chelonibia Barnacles Between Hawksbill and Green Sea Turtles

Epibionts are organisms that utilize the exterior of other organisms as a living substratum. Many affiliate opportunistically with hosts of different species, but others specialize on particular hosts as obligate associates. We investigated a case of apparent host specificity between two barnacles that are epizoites of sea turtles and illuminate some ecological considerations that may shape their host relationships. The barnacles Chelonibia testudinaria and Chelonibia caretta, though roughly similar in appearance, are separable by distinctions in morphology, genotype, and lifestyle. However, though each is known to colonize both green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) sea turtles, C. testudinaria is >5 times more common on greens, while C. caretta is >300 times more common on hawksbills. Two competing explanations for this asymmetry in barnacle incidence are either that the species’ larvae are spatially segregated in mutually exclusive host-encounter zones or their distributions overlap and the larvae behaviorally select their hosts from a common pool. We indirectly tested the latter by documenting the occurrence of adults of both barnacle species in two locations (SE Florida and Nose Be, Madagascar) where both turtle species co-mingle. For green and hawksbill turtles in both locations (Florida: n = 32 and n = 275, respectively; Madagascar: n = 32 and n = 125, respectively), we found that C. testudinaria occurred on green turtles only (percent occurrence – FL: 38.1%; MD: 6.3%), whereas the barnacle C. caretta was exclusively found on hawksbill turtles (FL: 82.2%; MD: 27.5%). These results support the hypothesis that the larvae of these barnacles differentially select host species from a shared supply. Physio-biochemical differences in host shell material, conspecific chemical cues, external microbial biofilms, and other surface signals may be salient factors in larval selectivity. Alternatively, barnacle presence may vary by host micro-environment. Dissimilarities in scute structure and shell growth between hawksbill and green turtles may promote critical differences in attachment modes observed between these barnacles. In understanding the co-evolution of barnacles and hosts it is key to consider the ecologies of both hosts and epibionts in interpreting associations of chance, choice, and dependence. Further studies are necessary to investigate the population status and settlement spectrum of barnacles inhabiting sea turtles.

Strandings of sea turtles on beaches around the oil capital in Brazil

The south-western region of the Atlantic Ocean has feeding and nesting areas for the five species of sea turtles registered in Brazil, which are in different degrees of extinction threat, mainly due to anthropogenic factors. Fishing and the ingestion of solid waste, were identified as causing stranding and the mortality of sea turtles. In this work, data from the monitoring of beaches in the Municipalities of Macaé and Rio das Ostras, important oil zone in Brazil, in the north-central region of the State of Rio de Janeiro, were used in order to analyse the effects of seasonality on the sea turtle stranding. The monitoring was carried out daily from September 2017 to June 2019, in a study area covering 23.8 km long beach. Stranding data were obtained from active (n = 126) and passive (n = 66) monitoring of beaches and included the records of Chelonia mydas (n = 151), Caretta caretta (n = 23), Lepidochelys olivacea (n = 14), Dermochelys coriacea (n = 2) and Eretmochelys imbricata (n = 1). The largest stranding record occurred in the summer (n = 61) and spring (n = 60), a period compatible with the reproductive season of the species. The results obtained in this study emphasise the importance of the analysis of strandings of sea turtles, which provide relevant data on the biology of the group, the intra and interspecific dynamics and the state of conservation of these animals.