Kelly R. Stewart

Global patterns of marine mammal, seabird, and sea turtle bycatch reveal taxa-specific and cumulative megafauna hotspots

Significance Loss of megafauna, termed trophic downgrading, has been found to affect biotic interactions, disturbance regimes, species invasions, and nutrient cycling. One recognized cause in air-breathing marine megafauna is incidental capture or bycatch by fisheries. Characterizing megafauna bycatch patterns across large ocean regions is limited by data availability but essential to direct conservation and management resources. We use empirical data to identify the global distribution and magnitude of seabird, marine mammal, and sea turtle bycatch in three widely used fishing gears. We identify taxa-specific hotspots and find evidence of cumulative impacts. This analysis provides an unprecedented global assessment of the distribution and magnitude of air-breathing megafauna bycatch, highlighting its cumulative nature and the urgent need to build on existing mitigation successes. Recent research on ocean health has found large predator abundance to be a key element of ocean condition. Fisheries can impact large predator abundance directly through targeted capture and indirectly through incidental capture of nontarget species or bycatch. However, measures of the global nature of bycatch are lacking for air-breathing megafauna. We fill this knowledge gap and present a synoptic global assessment of the distribution and intensity of bycatch of seabirds, marine mammals, and sea turtles based on empirical data from the three most commonly used types of fishing gears worldwide. We identify taxa-specific hotspots of bycatch intensity and find evidence of cumulative impacts across fishing fleets and gears. This global map of bycatch illustrates where data are particularly scarce—in coastal and small-scale fisheries and ocean regions that support developed industrial fisheries and millions of small-scale fishers—and identifies fishing areas where, given the evidence of cumulative hotspots across gear and taxa, traditional species or gear-specific bycatch management and mitigation efforts may be necessary but not sufficient. Given the global distribution of bycatch and the mitigation success achieved by some fleets, the reduction of air-breathing megafauna bycatch is both an urgent and achievable conservation priority.

Characterizing Fishing Effort and Spatial Extent of Coastal Fisheries

Biodiverse coastal zones are often areas of intense fishing pressure due to the high relative density of fishing capacity in these nearshore regions. Although overcapacity is one of the central challenges to fisheries sustainability in coastal zones, accurate estimates of fishing pressure in coastal zones are limited, hampering the assessment of the direct and collateral impacts (e.g., habitat degradation, bycatch) of fishing. We compiled a comprehensive database of fishing effort metrics and the corresponding spatial limits of fisheries and used a spatial analysis program (FEET) to map fishing effort density (measured as boat-meters per km2) in the coastal zones of six ocean regions. We also considered the utility of a number of socioeconomic variables as indicators of fishing pressure at the national level; fishing density increased as a function of population size and decreased as a function of coastline length. Our mapping exercise points to intra and interregional ‘hotspots’ of coastal fishing pressure. The significant and intuitive relationships we found between fishing density and population size and coastline length may help with coarse regional characterizations of fishing pressure. However, spatially-delimited fishing effort data are needed to accurately map fishing hotspots, i.e., areas of intense fishing activity. We suggest that estimates of fishing effort, not just target catch or yield, serve as a necessary measure of fishing activity, which is a key link to evaluating sustainability and environmental impacts of coastal fisheries.

Internesting and Postnesting Movements and Foraging Habitats of Leatherback Sea Turtles (Dermochelys coriacea) Nesting in Florida

ABSTRACT We tracked 10 leatherback turtles by satellite from 2 Florida Atlantic Coast nesting beaches for a period ranging from 38 days to more than 454 days. Movement and foraging areas were often coastal, which contrasts with other satellite telemetry studies where leatherbacks are more pelagic. Using kernel home-range estimation we identified the primary internesting residence areas as well as Atlantic foraging areas. The primary internesting habitat was centered east–southeast of Cape Canaveral, Florida, from 2 to 60 km offshore and extending 215 km along the coast. Atlantic foraging areas were located primarily on the continental shelf from 30° to 50°N, and in an offshore area centered at 42°N, 65°W, as well as off Africa in the Mauritania upwelling. Seasonally, the location of these foraging areas changed, occurring on the North American continental shelf from March through November and off the shelf from December through February. One of the tracked turtles may have been killed with 17 other leatherbacks by coastal shrimp fishing located near the Georgia–Florida border. We illustrate how using remotely sensed data could be used to prevent such mortalities.

Paternal genotype reconstruction reveals multiple paternity and sex ratios in a breeding population of leatherback turtles ( Dermochelys coriacea )

When animals are difficult to observe while breeding, insights into the mating system may be gained by using molecular techniques. Patterns of extra-pair copulation, multiple paternity and parental genotype analysis may elucidate population characteristics that help improve knowledge of life history while informing management decisions. During the course of a long-term study of leatherback turtles, we assessed the level of multiple paternity in successive clutches for 12 known females nesting at Sandy Point National Wildlife Refuge (St. Croix, U.S. Virgin Islands). We used seven polymorphic microsatellite markers to genotype the females and 1,019 hatchlings representing 38 nests (3–4 clutches from each female). Using deductive genotype reconstruction and GERUD1.0, we identified the 12 mothers and 17 different fathers that were responsible for 38 nests. We found that seven females (58.3%) showed no evidence of multiple paternity in their clutches, while five females (41.7%) had mated with two males each. There was evidence of two fathers (polyandry) in successive clutches for these five females. Multiple fathers didn’t contribute to clutches equally. For clutches laid by an individual female, the primary father was responsible for 53.7 to 85.9% of the hatchlings. We demonstrate the feasibility of using male genotype reconstruction to characterize the male component of this breeding population and to assess operational sex ratios for breeding sea turtles.

Geographic Patterns of Genetic Variation in a Broadly Distributed Marine Vertebrate: New Insights into Loggerhead Turtle Stock Structure from Expanded Mitochondrial DNA Sequences

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.

Assignment tests, telemetry and tag‐recapture data converge to identify natal origins of leatherback turtles foraging in Atlantic Canadian waters

Investigating migratory connectivity between breeding and foraging areas is critical to effective management and conservation of highly mobile marine taxa, particularly threatened, endangered, or economically important species that cross through regional, national and international boundaries. The leatherback turtle (Dermochelys coriacea, Vandelli 1761) is one such transboundary species that spends time at breeding areas at low latitudes in the northwest Atlantic during spring and summer. From there, they migrate widely throughout the North Atlantic, but many show fidelity to one region off eastern Canada, where critical foraging habitat has been proposed. Our goal was to identify nesting beach origins for turtles foraging here. Using genetics, we identified natal beaches for 288 turtles that were live-captured off the coast of Nova Scotia, Canada. Turtles were sampled (skin or blood) and genotyped using 17 polymorphic microsatellite markers. Results from three assignment testing programs (ONCOR, GeneClass2 and Structure) were compared. Our nesting population reference data set included 1417 individuals from nine Atlantic nesting assemblages. A supplementary data set for 83 foraging turtles traced to nesting beaches using flipper tags and/or PIT tags (n = 72), or inferred from satellite telemetry (n = 11), enabled ground-truthing of the assignments. We first assigned turtles using only genetic information and then used the supplementary recapture information to verify assignments. ONCOR performed best, assigning 64 of the 83 recaptured turtles to natal beaches (77·1%). Turtles assigned to Trinidad (164), French Guiana (72), Costa Rica (44), St. Croix (7), and Florida (1) reflect the relative size of those nesting populations, although none of the turtles were assigned to four other potential source nesting assemblages. Our results demonstrate the utility of genetic approaches for determining source populations of foraging marine animals and include the first identification of natal rookeries of male leatherbacks, identified through satellite telemetry and verified with genetics. This work highlights the importance of long-term monitoring and tagging programmes in nesting and high-use foraging areas. Moreover, it provides a scientific basis for evaluating stock-specific effects of fisheries on migratory marine species, thus identifying where coordinated international recovery efforts may be most effective.

Breeding sex ratios in adult leatherback turtles (Dermochelys coriacea) may compensate for female-biased hatchling sex ratios.

For vertebrates with temperature-dependent sex determination, primary (or hatchling) sex ratios are often skewed, an issue of particular relevance to concerns over effects of climate change on populations. However, the ratio of breeding males to females, or the operational sex ratio (OSR), is important to understand because it has consequences for population demographics and determines the capacity of a species to persist. The OSR also affects mating behaviors and mate choice, depending on the more abundant sex. For sea turtles, hatchling and juvenile sex ratios are generally female-biased, and with warming nesting beach temperatures, there is concern that populations may become feminized. Our purpose was to evaluate the breeding sex ratio for leatherback turtles at a nesting beach in St. Croix, USVI. In 2010, we sampled nesting females and later sampled their hatchlings as they emerged from nests. Total genomic DNA was extracted and all individuals were genotyped using 6 polymorphic microsatellite markers. We genotyped 662 hatchlings from 58 females, matching 55 females conclusively to their nests. Of the 55, 42 females mated with one male each, 9 mated with 2 males each and 4 mated with at least 3 males each, for a multiple paternity rate of 23.6%. Using GERUD1.0, we reconstructed parental genotypes, identifying 47 different males and 46 females for an estimated breeding sex ratio of 1.02 males for every female. Thus we demonstrate that there are as many actively breeding males as females in this population. Concerns about female-biased adult sex ratios may be premature, and mate choice or competition may play more of a role in sea turtle reproduction than previously thought. We recommend monitoring breeding sex ratios in the future to allow the integration of this demographic parameter in population models.

Perfluoroalkyl contaminants in plasma of five sea turtle species: Comparisons in concentration and potential health risks

The authors compared blood plasma concentrations of 13 perfluoroalkyl contaminants (PFCs) in five sea turtle species with differing trophic levels. Wild sea turtles were blood sampled from the southeastern region of the United States, and plasma was analyzed using liquid chromatography tandem mass spectrometry. Mean concentrations of perfluorooctane sulfonate (PFOS), the predominant PFC, increased with trophic level from herbivorous greens (2.41 ng/g), jellyfish-eating leatherbacks (3.95 ng/g), omnivorous loggerheads (6.47 ng/g), to crab-eating Kemps ridleys (15.7 ng/g). However, spongivorous hawksbills had surprisingly high concentrations of PFOS (11.9 ng/g) and other PFCs based on their trophic level. These baseline concentrations of biomagnifying PFCs demonstrate interesting species and geographical differences. The measured PFOS concentrations were compared with concentrations known to cause toxic effects in laboratory animals, and estimated margins of safety (EMOS) were calculated. Small EMOS (<100), suggestive of potential risk of adverse health effects, were observed for all five sea turtle species for immunosuppression. Estimated margins of safety less than 100 were also observed for liver, thyroid, and neurobehavorial effects for the more highly exposed species. These baseline concentrations and the preliminary EMOS exercise provide a better understanding of the potential health risks of PFCs for conservation managers to protect these threatened and endangered species.

Advances in the Application of Genetics in Marine Turtle Biology and Conservation

Marine turtles migrate across long distances, exhibit complex life histories, and occupy habitats that are difficult to observe. These factors present substantial challenges to understanding fundamental aspects of their biology or assessing human impacts, many of which are important for the effective conservation of these threatened and endangered species. The early development and application of genetic tools made important contributions to understanding marine turtle population and evolutionary biology, such as providing evidence of regional natal homing by breeding adults, establishing connectivity between rookeries and foraging habitats, and determining phylogeography and broad scale stock structure for most marine turtle species. Recent innovations in molecular technologies, statistical methods, and creative application of genetic tools have significantly built upon this knowledge to address key questions in marine turtle biology and conservation management. Here, we evaluate the latest major advances and potential of marine turtle genetic applications, including improved resolution and large-scale syntheses of population structure, connectivity and phylogeography, estimation of key demographic rates such as age to maturity and operational or breeding sex ratios, insight into reproductive strategies and behavior, and assessment of differential human impacts among populations. We then discuss remaining challenges and emerging capabilities, such as rapid, multiplexed genotyping and investigation of the genomic underpinnings of adaptive variation afforded by high-throughput sequencing technologies.

A Versatile Rapture (RAD-Capture) Platform for Genotyping Marine Turtles

Advances in high-throughput sequencing (HTS) technologies coupled with increased interdisciplinary collaboration is rapidly expanding capacity in the scope and scale of wildlife genetic studies. While existing HTS methods can be directly applied to address some evolutionary and ecological questions, certain research goals necessitate tailoring methods to specific study organisms, such as high-throughput genotyping of the same loci that are comparable over large spatial and temporal scales. These needs are particularly common for studies of highly mobile species of conservation concern like marine turtles, where life history traits, limited financial resources and other constraints require affordable, adaptable methods for HTS genotyping to meet a variety of study goals. Here, we present a versatile marine turtle HTS targeted enrichment platform adapted from the recently developed Rapture (RAD-Capture) method specifically designed to meet these research needs. Our results demonstrate consistent enrichment of targeted regions throughout the genome and discovery of candidate variants in all species examined for use in various conservation genetics applications. Accurate species identification confirmed the ability of our platform to genotype over 1,000 multiplexed samples, and identified areas for future methodological improvement such as optimization for low initial concentration samples. Finally, analyses within green turtles supported the ability of this platform to identify informative SNPs for stock structure, population assignment and other applications over a broad geographic range of interest to management. This platform provides an additional tool for marine turtle genetic studies and broadens capacity for future large-scale initiatives such as collaborative global marine turtle genetic databases.