Peter H. Dutton

Global Conservation Priorities for Marine Turtles

Where conservation resources are limited and conservation targets are diverse, robust yet flexible priority-setting frameworks are vital. Priority-setting is especially important for geographically widespread species with distinct populations subject to multiple threats that operate on different spatial and temporal scales. Marine turtles are widely distributed and exhibit intra-specific variations in population sizes and trends, as well as reproduction and morphology. However, current global extinction risk assessment frameworks do not assess conservation status of spatially and biologically distinct marine turtle Regional Management Units (RMUs), and thus do not capture variations in population trends, impacts of threats, or necessary conservation actions across individual populations. To address this issue, we developed a new assessment framework that allowed us to evaluate, compare and organize marine turtle RMUs according to status and threats criteria. Because conservation priorities can vary widely (i.e. from avoiding imminent extinction to maintaining long-term monitoring efforts) we developed a “conservation priorities portfolio” system using categories of paired risk and threats scores for all RMUs (n = 58). We performed these assessments and rankings globally, by species, by ocean basin, and by recognized geopolitical bodies to identify patterns in risk, threats, and data gaps at different scales. This process resulted in characterization of risk and threats to all marine turtle RMUs, including identification of the worlds 11 most endangered marine turtle RMUs based on highest risk and threats scores. This system also highlighted important gaps in available information that is crucial for accurate conservation assessments. Overall, this priority-setting framework can provide guidance for research and conservation priorities at multiple relevant scales, and should serve as a model for conservation status assessments and priority-setting for widespread, long-lived taxa.

Regional Management Units for Marine Turtles: A Novel Framework for Prioritizing Conservation and Research across Multiple Scales

Background Resolving threats to widely distributed marine megafauna requires definition of the geographic distributions of both the threats as well as the population unit(s) of interest. In turn, because individual threats can operate on varying spatial scales, their impacts can affect different segments of a population of the same species. Therefore, integration of multiple tools and techniques — including site-based monitoring, genetic analyses, mark-recapture studies and telemetry — can facilitate robust definitions of population segments at multiple biological and spatial scales to address different management and research challenges. Methodology/Principal Findings To address these issues for marine turtles, we collated all available studies on marine turtle biogeography, including nesting sites, population abundances and trends, population genetics, and satellite telemetry. We georeferenced this information to generate separate layers for nesting sites, genetic stocks, and core distributions of population segments of all marine turtle species. We then spatially integrated this information from fine- to coarse-spatial scales to develop nested envelope models, or Regional Management Units (RMUs), for marine turtles globally. Conclusions/Significance The RMU framework is a solution to the challenge of how to organize marine turtles into units of protection above the level of nesting populations, but below the level of species, within regional entities that might be on independent evolutionary trajectories. Among many potential applications, RMUs provide a framework for identifying data gaps, assessing high diversity areas for multiple species and genetic stocks, and evaluating conservation status of marine turtles. Furthermore, RMUs allow for identification of geographic barriers to gene flow, and can provide valuable guidance to marine spatial planning initiatives that integrate spatial distributions of protected species and human activities. In addition, the RMU framework — including maps and supporting metadata — will be an iterative, user-driven tool made publicly available in an online application for comments, improvements, download and analysis.

Natal homing in juvenile loggerhead turtles (Caretta caretta)

Juvenile loggerhead turtles (Caretta caretta) from West Atlantic nesting beaches occupy oceanic (pelagic) habitats in the eastern Atlantic and Mediterranean, whereas larger juvenile turtles occupy shallow (neritic) habitats along the continental coastline of North America. Hence the switch from oceanic to neritic stage can involve a trans‐oceanic migration. Several researchers have suggested that at the end of the oceanic phase, juveniles are homing to feeding habitats in the vicinity of their natal rookery. To test the hypothesis of juvenile homing behaviour, we surveyed 10 juvenile feeding zones across the eastern USA with mitochondrial DNA control region sequences (N = 1437) and compared these samples to potential source (nesting) populations in the Atlantic Ocean and Mediterranean Sea (N = 465). The results indicated a shallow, but significant, population structure of neritic juveniles (ΦST = 0.0088, P = 0.016), and haplotype frequency differences were significantly correlated between coastal feeding populations and adjacent nesting populations (Mantel test R2 = 0.52, P = 0.001). Mixed stock analyses (using a Bayesian algorithm) indicated that juveniles occurred at elevated frequency in the vicinity of their natal rookery. Hence, all lines of evidence supported the hypothesis of juvenile homing in loggerhead turtles. While not as precise as the homing of breeding adults, this behaviour nonetheless places juvenile turtles in the vicinity of their natal nesting colonies. Some of the coastal hazards that affect declining nesting populations may also affect the next generation of turtles feeding in nearby habitats.

Cumulative human impacts on marine predators

Stressors associated with human activities interact in complex ways to affect marine ecosystems, yet we lack spatially explicit assessments of cumulative impacts on ecologically and economically key components such as marine predators. Here we develop a metric of cumulative utilization and impact (CUI) on marine predators by combining electronic tracking data of eight protected predator species (n=685 individuals) in the California Current Ecosystem with data on 24 anthropogenic stressors. We show significant variation in CUI with some of the highest impacts within US National Marine Sanctuaries. High variation in underlying species and cumulative impact distributions means that neither alone is sufficient for effective spatial management. Instead, comprehensive management approaches accounting for both cumulative human impacts and trade-offs among multiple stressors must be applied in planning the use of marine resources.

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 δ15N values of bulk skin, with distinct “low δ15N” and “high δ15N” groups. δ15N 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 δ15N 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.

Large‐scale movements and high‐use areas of western Pacific leatherback turtles, Dermochelys coriacea

The western Pacific leatherback turtle (Dermochelys coriacea), one of three genetically distinct stocks in the Indo-Pacific region, has declined markedly during past decades. This metapopulation nests year-round at beaches of several western Pacific island nations and has been documented through genetic analysis and telemetry studies to occur in multiple regions of the Pacific Ocean. To provide a large-scale perspective of their movements, high-use areas, and habitat associations, we report and synthesize results of 126 satellite telemetry deployments conducted on leatherbacks at western Pacific nesting beaches and at one eastern Pacific foraging ground during 2000-2007. A Bayesian switching state-space model was applied to raw Argos-acquired surface locations to estimate daily positions and behavioral mode (either transiting or area-restricted search) for each turtle. Monthly areas of high use were identified for post- nesting periods using kernel density estimation. There was a clear separation of migratory destinations for boreal summer vs. boreal winter nesters. Leatherbacks that nested during boreal summer moved into Large Marine Ecosystems (LMEs) of the temperate North Pacific Ocean or into tropical waters of the South China Sea. Turtles that nested during boreal winter moved into temperate and tropical LMEs of the southern hemisphere. Area-restricted search occurred in temperate and tropical waters at diverse pelagic and coastal regions exhibiting a wide range of oceanographic features, including mesoscale eddies, coastal retention areas, current boundaries, or stationary fronts, all of which are known mechanisms for aggregating leatherback prey. Use of the most distant and temperate foraging ground, the California Current LME, required a 10-12 month trans-Pacific migration and commonly involved multiple years of migrating between high-latitude summer foraging grounds and low-latitude eastern tropical Pacific wintering areas without returning to western Pacific nesting beaches. In contrast, tropical foraging destinations were reached within 5-7 months and appeared to support year-round foraging, potentially allowing a more rapid return to nesting beaches. Based on these observations, we hypothesize that demographic differences are likely among nesting females using different LMEs of the Indo-Pacific. The differences in movements and foraging strategies underscore the importance of and the need for ecosystem-based management and coordinated Pacific-wide conservation efforts.

Population Status and Internesting Movement of Leatherback Turtles, Dermochelys coriacea, Nesting on the Northwest Coast of Papua, Indonesia

ABSTRACT The northwest coast of the province of Papua in Indonesia is thought to host the largest remaining leatherback nesting population in the Pacific Ocean. We conducted a census of nesting activity at Jamursba-Medi from 2001 through 2004 and of Wermon from 2002 to 2004, and tracked internesting movements of female leatherbacks by using satellite telemetry during the nesting season in 2003. We recorded 1865–3601 nests each season at Jamursba-Medi and 1788–2881 nests at Wermon. Nesting occurred year-round, with a peak in activity between May and September at Jamursba-Medi, and between October and March at Wermon. Comparing these data with previous records of nesting activity from 1981 to 2001 indicates that, although there are indications of a long-term decline, this population has not been depleted to the extent found at other major rookeries in the Pacific. Satellite telemetry indicates that nesters frequent waters around the Raja Ampat Islands and coastal waters to the west of Jamursba-Medi, and may also nest outside the monitored area. We recommend establishing a marine protected area to ensure protection of this population in these critical nearshore marine habitats and implementation of conservation measures in partnership with local communities at these nesting beaches before this population becomes depleted.

Targeted multiplex next-generation sequencing: advances in techniques of mitochondrial and nuclear DNA sequencing for population genomics

Next‐generation sequencing (NGS) is emerging as an efficient and cost‐effective tool in population genomic analyses of nonmodel organisms, allowing simultaneous resequencing of many regions of multi‐genomic DNA from multiplexed samples. Here, we detail our synthesis of protocols for targeted resequencing of mitochondrial and nuclear loci by generating indexed genomic libraries for multiplexing up to 100 individuals in a single sequencing pool, and then enriching the pooled library using custom DNA capture arrays. Our use of DNA sequence from one species to capture and enrich the sequencing libraries of another species (i.e. cross‐species DNA capture) indicates that efficient enrichment occurs when sequences are up to about 12% divergent, allowing us to take advantage of genomic information in one species to sequence orthologous regions in related species. In addition to a complete mitochondrial genome on each array, we have included between 43 and 118 nuclear loci for low‐coverage sequencing of between 18 kb and 87 kb of DNA sequence per individual for single nucleotide polymorphisms discovery from 50 to 100 individuals in a single sequencing lane. Using this method, we have generated a total of over 500 whole mitochondrial genomes from seven cetacean species and green sea turtles. The greater variation detected in mitogenomes relative to short mtDNA sequences is helping to resolve genetic structure ranging from geographic to species‐level differences. These NGS and analysis techniques have allowed for simultaneous population genomic studies of mtDNA and nDNA with greater genomic coverage and phylogeographic resolution than has previously been possible in marine mammals and turtles.

Interactions Between Leatherback Turtles and Peruvian Artisanal Fisheries

ABSTRACT From 1985 to 1999, data were gathered opportunistically on the bycatch of 33 leatherback turtles in coastal Peru, and from 2000 to 2003, a dockside observer program provided data on an additional 133 leatherbacks caught in the coastal gillnet and longline fisheries targeting mahi mahi, sharks, and rays. These data stress the need for programs to monitor bycatch in artisanal fisheries, enforce regulations prohibiting sea turtle capture, and increase the environmental awareness of fishermen.

Post-Nesting Migrations of Leatherback Turtles (Dermochelys coriacea) from Jamursba-Medi, Bird's Head Peninsula, Indonesia

ABSTRACT Nine leatherback turtles (Dermochelys coriacea) were tracked for 111–695 days via satellite telemetry from one of the largest remaining western Pacific leatherback turtle nesting beaches, Jamursba-Medi, Papua, Indonesia. The turtles moved into tropical waters of the Philippines and Malaysia, into the Sea of Japan, and across the equatorial Pacific to temperate waters off North America. This study provides the first record of a trans-Pacific migration by a leatherback turtle.