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

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 Mya. The genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined 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 the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of noncollinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared with other reptiles, and harbor a higher genetic load compared with green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.

Species and population specific gene expression in blood transcriptomes of marine turtles.

BACKGROUND: Transcriptomic data has demonstrated utility to advance the study of physiological diversity and organisms' responses to environmental stressors. However, a lack of genomic resources and challenges associated with collecting high-quality RNA can limit its application for many wild populations. Minimally invasive blood sampling combined with de novo transcriptomic approaches has great potential to alleviate these barriers. Here, we advance these goals for marine turtles by generating high quality de novo blood transcriptome assemblies to characterize functional diversity and compare global transcriptional profiles between tissues, species, and foraging aggregations. RESULTS: We generated high quality blood transcriptome assemblies for hawksbill (Eretmochelys imbricata), loggerhead (Caretta caretta), green (Chelonia mydas), and leatherback (Dermochelys coriacea) turtles. The functional diversity in assembled blood transcriptomes was comparable to those from more traditionally sampled tissues. A total of 31.3% of orthogroups identified were present in all four species, representing a core set of conserved genes expressed in blood and shared across marine turtle species. We observed strong species-specific expression of these genes, as well as distinct transcriptomic profiles between green turtle foraging aggregations that inhabit areas of greater or lesser anthropogenic disturbance. CONCLUSIONS: Obtaining global gene expression data through non-lethal, minimally invasive sampling can greatly expand the applications of RNA-sequencing in protected long-lived species such as marine turtles. The distinct differences in gene expression signatures between species and foraging aggregations provide insight into the functional genomics underlying the diversity in this ancient vertebrate lineage. The transcriptomic resources generated here can be used in further studies examining the evolutionary ecology and anthropogenic impacts on marine turtles.

VALIDATION OF ULTRASOUND AS A NONINVASIVE TOOL TO MEASURE SUBCUTANEOUS FAT DEPTH IN LEATHERBACK SEA TURTLES (DERMOCHELYS CORIACEA).

Leatherback turtles (Dermochelys coriacea) undergo substantial cyclical changes in body condition between foraging and nesting. Ultrasonography has been used to measure subcutaneous fat as an indicator of body condition in many species but has not been applied in sea turtles. To validate this technique in leatherback turtles, ultrasound images were obtained from 36 live-captured and dead-stranded immature and adult turtles from foraging and nesting areas in the Pacific and Atlantic oceans. Ultrasound measurements were compared with direct measurements from surgical biopsy or necropsy. Tissue architecture was confirmed histologically in a subset of turtles. The dorsal shoulder region provided the best site for differentiation of tissues. Maximum fat depth values with the front flipper in a neutral (45-90°) position demonstrated good correlation with direct measurements. Ultrasound-derived fat measurements may be used in the future for quantitative assessment of body condition as an index of health in this critically endangered species.

Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean.

Fisheries bycatch is a critical source of mortality for rapidly declining populations of leatherback turtles, Dermochelys coriacea. We integrated use-intensity distributions for 135 satellite-tracked adult turtles with longline fishing effort to estimate predicted bycatch risk over space and time in the Pacific Ocean. Areas of predicted bycatch risk did not overlap for eastern and western Pacific nesting populations, warranting their consideration as distinct management units with respect to fisheries bycatch. For western Pacific nesting populations, we identified several areas of high risk in the north and central Pacific, but greatest risk was adjacent to primary nesting beaches in tropical seas of Indo-Pacific islands, largely confined to several exclusive economic zones under the jurisdiction of national authorities. For eastern Pacific nesting populations, we identified moderate risk associated with migrations to nesting beaches, but the greatest risk was in the South Pacific Gyre, a broad pelagic zone outside national waters where management is currently lacking and may prove difficult to implement. Efforts should focus on these predicted hotspots to develop more targeted management approaches to alleviate leatherback bycatch.

Impacts of marine heatwaves on top predator distributions are variable but predictable.

Marine heatwaves cause widespread environmental, biological, and socio-economic impacts, placing them at the forefront of 21st-century management challenges. However, heatwaves vary in intensity and evolution, and a paucity of information on how this variability impacts marine species limits our ability to proactively manage for these extreme events. Here, we model the effects of four recent heatwaves (2014, 2015, 2019, 2020) in the Northeastern Pacific on the distributions of 14 top predator species of ecological, cultural, and commercial importance. Predicted responses were highly variable across species and heatwaves, ranging from near total loss of habitat to a two-fold increase. Heatwaves rapidly altered political bio-geographies, with up to 10% of predicted habitat across all species shifting jurisdictions during individual heatwaves. The variability in predicted responses across species and heatwaves portends the need for novel management solutions that can rapidly respond to extreme climate events. As proof-of-concept, we developed an operational dynamic ocean management tool that predicts predator distributions and responses to extreme conditions in near real-time.

Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions.

Interactions with fisheries are believed to be a major cause of mortality for adult leatherback turtles (Dermochelys coriacea), which is of particular concern in the Pacific Ocean, where they have been rapidly declining. In order to identify where these interactions are occurring and how they may be reduced, it is essential first to understand the movements and behavior of leatherback turtles. There are two regional nesting populations in the East Pacific (EP) and West Pacific (WP), comprising multiple nesting sites. We synthesized tracking data from the two populations and compared their movement patterns. A switching state-space model was applied to 135 Argos satellite tracks to account for observation error, and to distinguish between migratory and area-restricted search behaviors. The tracking data, from the largest leatherback data set ever assembled, indicated that there was a high degree of spatial segregation between EP and WP leatherbacks. Area-restricted search behavior mainly occurred in the southeast Pacific for the EP leatherbacks, whereas the WP leatherbacks had several different search areas in the California Current, central North Pacific, South China Sea, off eastern Indonesia, and off southeastern Australia. We also extracted remotely sensed oceanographic data and applied a generalized linear mixed model to determine if leatherbacks exhibited different behavior in relation to environmental variables. For the WP population, the probability of area-restricted search behavior was positively correlated with chlorophyll-a concentration. This response was less strong in the EP population, but these turtles had a higher probability of search behavior where there was greater Ekman upwelling, which may increase the transport of nutrients and consequently prey availability. These divergent responses to oceanographic conditions have implications for leatherback vulnerability to fisheries interactions and to the effects of climate change. The occurrence of leatherback turtles within both coastal and pelagic areas means they have a high risk of exposure to many different fisheries, which may be very distant from their nesting sites. The EP leatherbacks have more limited foraging grounds than the WP leatherbacks, which could make them more susceptible to any temperature or prey changes that occur in response to climate change.

A dynamic ocean management tool to reduce bycatch and support sustainable fisheries.

Seafood is an essential source of protein for more than 3 billion people worldwide, yet bycatch of threatened species in capture fisheries remains a major impediment to fisheries sustainability. Management measures designed to reduce bycatch often result in significant economic losses and even fisheries closures. Static spatial management approaches can also be rendered ineffective by environmental variability and climate change, as productive habitats shift and introduce new interactions between human activities and protected species. We introduce a new multispecies and dynamic approach that uses daily satellite data to track ocean features and aligns scales of management, species movement, and fisheries. To accomplish this, we create species distribution models for one target species and three bycatch-sensitive species using both satellite telemetry and fisheries observer data. We then integrate species-specific probabilities of occurrence into a single predictive surface, weighing the contribution of each species by management concern. We find that dynamic closures could be 2 to 10 times smaller than existing static closures while still providing adequate protection of endangered nontarget species. Our results highlight the opportunity to implement near real-time management strategies that would both support economically viable fisheries and meet mandated conservation objectives in the face of changing ocean conditions. With recent advances in eco-informatics, dynamic management provides a new climate-ready approach to support sustainable fisheries.

The political biogeography of migratory marine predators.

During their migrations, marine predators experience varying levels of protection and face many threats as they travel through multiple countries' jurisdictions and across ocean basins. Some populations are declining rapidly. Contributing to such declines is a failure of some international agreements to ensure effective cooperation by the stakeholders responsible for managing species throughout their ranges, including in the high seas, a global commons. Here we use biologging data from marine predators to provide quantitative measures with great potential to inform local, national and international management efforts in the Pacific Ocean. We synthesized a large tracking data set to show how the movements and migratory phenology of 1,648 individuals representing 14 species-from leatherback turtles to white sharks-relate to the geopolitical boundaries of the Pacific Ocean throughout species' annual cycles. Cumulatively, these species visited 86% of Pacific Ocean countries and some spent three-quarters of their annual cycles in the high seas. With our results, we offer answers to questions posed when designing international strategies for managing migratory species.

Estimating Limit Reference Points for Western Pacific Leatherback Turtles (Dermochelys coriacea) in the U.S. West Coast EEZ.

Biological limit reference points (LRPs) for fisheries catch represent upper bounds that avoid undesirable population states. LRPs can support consistent management evaluation among species and regions, and can advance ecosystem-based fisheries management. For transboundary species, LRPs prorated by local abundance can inform local management decisions when international coordination is lacking. We estimated LRPs for western Pacific leatherbacks in the U.S. West Coast Exclusive Economic Zone (WCEEZ) using three approaches with different types of information on local abundance. For the current application, the best-informed LRP used a local abundance estimate derived from nest counts, vital rate information, satellite tag data, and fishery observer data, and was calculated with a Potential Biological Removal estimator. Management strategy evaluation was used to set tuning parameters of the LRP estimators to satisfy risk tolerances for falling below population thresholds, and to evaluate sensitivity of population outcomes to bias in key inputs. We estimated local LRPs consistent with three hypothetical management objectives: allowing the population to rebuild to its maximum net productivity level (4.7 turtles per five years), limiting delay of population rebuilding (0.8 turtles per five years), or only preventing further decline (7.7 turtles per five years). These LRPs pertain to all human-caused removals and represent the WCEEZ contribution to meeting population management objectives within a broader international cooperative framework. We present multi-year estimates, because at low LRP values, annual assessments are prone to substantial error that can lead to volatile and costly management without providing further conservation benefit. The novel approach and the performance criteria used here are not a direct expression of the "jeopardy" standard of the U.S. Endangered Species Act, but they provide useful assessment information and could help guide international management frameworks. Given the range of abundance data scenarios addressed, LRPs should be estimable for many other areas, populations, and taxa.

Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids.

Effective conservation strategies for highly migratory species must incorporate information about long-distance movements and locations of high-use foraging areas. However, the inherent challenges of directly monitoring these factors call for creative research approaches and innovative application of existing tools. Highly migratory marine species, such as marine turtles, regularly travel hundreds or thousands of kilometers between breeding and feeding areas, but identification of migratory routes and habitat use patterns remains elusive. Here we use satellite telemetry in combination with compound-specific isotope analysis of amino acids to confirm that insights from bulk tissue stable isotope analysis can reveal divergent migratory strategies and within-population segregation of foraging groups of critically endangered leatherback sea turtles (Dermochelys coriacea) across the Pacific Ocean. Among the 78 turtles studied, we found a distinct dichotomy in δ(15)N values of bulk skin, with distinct "low δ(15)N" and "high δ(15)N" groups. δ(15)N analysis of amino acids confirmed that this disparity resulted from isotopic differences at the base of the food chain and not from differences in trophic position between the two groups. Satellite tracking of 13 individuals indicated that their bulk skin δ(15)N value was linked to the particular foraging region of each turtle. These findings confirm that prevailing marine isoscapes of foraging areas can be reflected in the isotopic compositions of marine turtle body tissues sampled at nesting beaches. We use a Bayesian mixture model to show that between 82 and 100% of the 78 skin-sampled turtles could be assigned with confidence to either the eastern Pacific or western Pacific, with 33 to 66% of all turtles foraging in the eastern Pacific. Our forensic approach validates the use of stable isotopes to depict leatherback turtle movements over broad spatial ranges and is timely for establishing wise conservation efforts in light of this species' imminent risk of extinction in the Pacific.

Comparative health assessment of Western Pacific leatherback turtles (Dermochelys coriacea) foraging off the coast of California, 2005-2007.

Leatherback turtles (Dermochelys coriacea) are critically endangered, primarily threatened by the overharvesting of eggs, fisheries entanglement, and coastal development. The Pacific leatherback population has experienced a catastrophic decline over the past two decades. Leatherbacks foraging off the coast of California are part of a distinct Western Pacific breeding stock that nests on beaches in Indonesia, Papua New Guinea, and the Solomon Islands. Although it has been proposed that the rapid decline of Pacific leatherback turtles is due to increased adult mortality, little is known about the health of this population. Health assessments in leatherbacks have examined females on nesting beaches, which provides valuable biological information, but might have limited applicability to the population as a whole. During September 2005 and 2007, we conducted physical examinations on 19 foraging Pacific leatherback turtles and measured normal physiologic parameters, baseline hematologic and plasma biochemistry values, and exposure to heavy metals (cadmium, lead, and mercury), organochlorine contaminants, and domoic acid. We compared hematologic values of foraging Pacific leatherbacks with their nesting counterparts in Papua New Guinea (n=11) and with other nesting populations in the Eastern Pacific in Costa Rica (n=8) and in the Atlantic in St. Croix (n=12). This study provides the most comprehensive assessment to date of the health status of leatherbacks in the Pacific. We found significant differences in blood values between foraging and nesting leatherbacks, which suggests that health assessment studies conducted only on nesting females might not accurately represent the whole population. The establishment of baseline physiologic data and blood values for healthy foraging leatherback turtles, including males, provides valuable data for long-term health monitoring and comparative studies of this endangered population.

Practice parameter for the assessment and treatment of children and adolescents with posttraumatic stress disorder.

This Practice Parameter reviews the evidence from research and clinical experience and highlights significant advances in the assessment and treatment of posttraumatic stress disorder since the previous Parameter was published in 1998. It highlights the importance of early identification of posttraumatic stress disorder, the importance of gathering information from parents and children, and the assessment and treatment of comorbid disorders. It presents evidence to support trauma-focused psychotherapy, medications, and a combination of interventions in a multimodal approach.