Remote submerged banks and mesophotic ecosystems can provide key habitat for endangered marine megafauna.

The importance of some ecosystems remains poorly understood. We showed that mesophotic ecosystems (30 to 150 m) are a key habitat for a critically endangered species, with strong evidence that a globally important population of adult hawksbill turtles (Eretmochelys imbricata) almost exclusively foraged at these depths on remote submerged banks. This discovery highlights the need for such areas to be included in conservation planning, for example, as part of the United Nations High Seas Treaty. We equipped nesting turtles with Fastloc-GPS (Global Positioning System) satellite tags at an Indian Ocean breeding area and they all traveled to deep foraging sites (6765 days of tracking data across 22 individuals including 183,921 dive-depth measurements) rather than shallow coral reef sites. Both chart depths and depth data relayed from the tags indicated that turtles foraged at mesophotic depths, the modal dive depths being between 35 and 40 m. We calculate that 55,554 km2 of the western Indian Ocean alone consists of submerged banks between 30 and 60 m.

Travel routes to remote ocean targets reveal the map sense resolution for a marine migrant.

How animals navigate across the ocean to isolated targets remains perplexing greater than 150 years since this question was considered by Charles Darwin. To help solve this long-standing enigma, we considered the likely resolution of any map sense used in migration, based on the navigational performance across different scales (tens to thousands of kilometres). We assessed navigational performance using a unique high-resolution Fastloc-GPS tracking dataset for post-breeding hawksbill turtles (Eretmochelys imbricata) migrating relatively short distances to remote, isolated targets on submerged banks in the Indian Ocean. Individuals often followed circuitous paths (mean straightness index = 0.54, range 0.14-0.93, s.d. = 0.23, n = 22), when migrating short distances (mean beeline distance to target = 106 km, range 68.7-178.2 km). For example, one turtle travelled 1306.2 km when the beeline distance to the target was only 176.4 km. When off the beeline to their target, turtles sometimes corrected their course both in the open ocean and when encountering shallow water. Our results provide compelling evidence that hawksbill turtles only have a relatively crude map sense in the open ocean. The existence of widespread foraging and breeding areas on isolated oceanic sites points to target searching in the final stages of migration being common in sea turtles.

Reef benthos of Seychelles - A field guide.

BACKGROUND: During the 2019 First Descent: Seychelles Expedition, shallow and deep reef ecosystems of the Seychelles Outer Islands were studied by deploying a variety of underwater technologies to survey their benthic flora and fauna. Submersibles, remotely operated vehicles (ROVs) and SCUBA diving teams used stereo-video camera systems to record benthic communities during transect surveys conducted at 10 m, 30 m, 60 m, 120 m, 250 m and 350 m depths. In total, ~ 45 h of video footage was collected during benthic transect surveys, which was subsequently processed using annotation software in order to assess reef biodiversity and community composition. Here, we present a photographic guide for the visual identification of the marine macrophytes, corals, sponges and other common invertebrates that inhabit Seychelles' reefs. It is hoped that the resulting guide will aid marine biologists, conservationists, managers, divers and naturalists with the coarse identification of organisms as seen in underwater footage or live in the field. NEW INFORMATION: A total of 184 morphotypes (= morphologically similar individuals) were identified belonging to Octocorallia (47), Porifera (35), Scleractinia (32), Asteroidea (19), Echinoidea (10), Actiniaria (9), Chlorophyta (8), Antipatharia (6), Hydrozoa (6), Holothuroidea (5), Mollusca (2), Rhodophyta (2), Tracheophyta (2), Annelida (1), Crinoidea (1), Ctenophora (1), Ochrophyta (1) and Zoantharia (1). Out of these, we identified one to phylum level, eight to class, 14 to order, 27 to family, 110 to genus and 24 to species. This represents the first attempt to catalogue the benthic diversity from shallow reefs and up to 350 m depth in Seychelles.

High accuracy tracking reveals how small conservation areas can protect marine megafauna.

Space use estimates can inform conservation management but relaying high-accuracy locations is often not straightforward. We used Fastloc-GPS Argos satellite tags with the innovation of additional data relay via a ground station (termed a "Mote") to record high volumes (typically >20 locations per individual per day) of high accuracy tracking data. Tags were attached in the Chagos Archipelago (Indian Ocean) in 2018-2019 to 23 immature turtles of two species for which there have been long-standing conservation concerns: 21 hawksbill turtles (Eretmochelys imbricata) and two green turtles (Chelonia mydas). Over long tracking durations (mean 227.6 d per individual), most turtles moved very little. For example, 17 of 21 hawksbill turtles remained continuously in the lagoon where they were equipped, with 95% and 50% utilization distributions (UDs) averaging only 1.03 and 0.18 km2 , respectively. Many individuals, and both species, could use the same small spaces, i.e., individuals did not maintain unique home ranges. However, three hawksbill turtles travelled hundreds of kilometers from the tagging site. Our results show that, for some large marine vertebrates, even small protected areas of only a few square kilometers can encompass the movements of a large proportion of individuals over long periods. High accuracy tracking may likewise reveal the details of space use for many other animals that move little and/or use important focal areas and where previous low-accuracy tracking techniques have tended to overestimate space use.

Seascape Genetics and the Spatial Ecology of Juvenile Green Turtles.

Understanding how ocean currents impact the distribution and connectivity of marine species, provides vital information for the effective conservation management of migratory marine animals. Here, we used a combination of molecular genetics and ocean drift simulations to investigate the spatial ecology of juvenile green turtle (Chelonia mydas) developmental habitats, and assess the role of ocean currents in driving the dispersal of green turtle hatchlings. We analyzed mitochondrial (mt)DNA sequenced from 358 juvenile green turtles, and from eight developmental areas located throughout the Southwest Indian Ocean (SWIO). A mixed stock analysis (MSA) was applied to estimate the level of connectivity between developmental sites and published genetic data from 38 known genetic stocks. The MSA showed that the juvenile turtles at all sites originated almost exclusively from the three known SWIO stocks, with a clear shift in stock contributions between sites in the South and Central Areas. The results from the genetic analysis could largely be explained by regional current patterns, as shown by the results of passive numerical drift simulations linking breeding sites to developmental areas utilized by juvenile green turtles. Integrating genetic and oceanographic data helps researchers to better understand how marine species interact with ocean currents at different stages of their lifecycle, and provides the scientific basis for effective conservation management.

How numbers of nesting sea turtles can be overestimated by nearly a factor of two.

Estimating the absolute number of individuals in populations and their fecundity is central to understanding the ecosystem role of species and their population dynamics as well as allowing informed conservation management for endangered species. Estimates of abundance and fecundity are often difficult to obtain for rare or cryptic species. Yet, in addition, here we show for a charismatic group, sea turtles, that are neither cryptic nor rare and whose nesting is easy to observe, that the traditional approach of direct observations of nesting has likely led to a gross overestimation of the number of individuals in populations and underestimation of their fecundity. We use high-resolution GPS satellite tags to track female green turtles throughout their nesting season in the Chagos Archipelago (Indian Ocean) and assess when and where they nested. For individual turtles, nest locations were often spread over several tens of kilometres of coastline. Assessed by satellite observations, a mean of 6.0 clutches (range 2-9, s.d. = 2.2) was laid by individuals, about twice as many as previously assumed, a finding also reported in other species and ocean basins. Taken together, these findings suggest that the actual number of nesting turtles may be almost 50% less than previously assumed.

Male hatchling production in sea turtles from one of the world's largest marine protected areas, the Chagos Archipelago.

Sand temperatures at nest depths and implications for hatchling sex ratios of hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) nesting in the Chagos Archipelago, Indian Ocean are reported and compared to similar measurements at rookeries in the Atlantic and Caribbean. During 2012-2014, temperature loggers were buried at depths and in beach zones representative of turtle nesting sites. Data collected for 12,546 days revealed seasonal and spatial patterns of sand temperature. Depth effects were minimal, perhaps modulated by shade from vegetation. Coolest and warmest temperatures were recorded in the sites heavily shaded in vegetation during the austral winter and in sites partially shaded in vegetation during summer respectively. Overall, sand temperatures were relatively cool during the nesting seasons of both species which would likely produce fairly balanced hatchling sex ratios of 53% and 63% male hatchlings, respectively, for hawksbill and green turtles. This result contrasts with the predominantly high female skew reported for offspring at most rookeries around the globe and highlights how local beach characteristics can drive incubation temperatures. Our evidence suggests that sites characterized by heavy shade associated with intact natural vegetation are likely to provide conditions suitable for male hatchling production in a warming world.

Phylogeography, Genetic Diversity, and Management Units of Hawksbill Turtles in the Indo-Pacific.

Hawksbill turtle (Eretmochelys imbricata) populations have experienced global decline because of a history of intense commercial exploitation for shell and stuffed taxidermied whole animals, and harvest for eggs and meat. Improved understanding of genetic diversity and phylogeography is needed to aid conservation. In this study, we analyzed the most geographically comprehensive sample of hawksbill turtles from the Indo-Pacific Ocean, sequencing 766 bp of the mitochondrial control region from 13 locations (plus Aldabra, n = 4) spanning over 13500 km. Our analysis of 492 samples revealed 52 haplotypes distributed in 5 divergent clades. Diversification times differed between the Indo-Pacific and Atlantic lineages and appear to be related to the sea-level changes that occurred during the Last Glacial Maximum. We found signals of demographic expansion only for turtles from the Persian Gulf region, which can be tied to a more recent colonization event. Our analyses revealed evidence of transoceanic migration, including connections between feeding grounds from the Atlantic Ocean and Indo-Pacific rookeries. Hawksbill turtles appear to have a complex pattern of phylogeography, showing a weak isolation by distance and evidence of multiple colonization events. Our novel dataset will allow mixed-stock analyses of hawksbill turtle feeding grounds in the Indo-Pacific by providing baseline data needed for conservation efforts in the region. Eight management units are proposed in our study for the Indo-Pacific region that can be incorporated in conservation plans of this critically endangered species.

Use of long-distance migration patterns of an endangered species to inform conservation planning for the world's largest marine protected area.

Large marine protected areas (MPAs), each hundreds of thousands of square kilometers, have been set up by governments around the world over the last decade as part of efforts to reduce ocean biodiversity declines, yet their efficacy is hotly debated. The Chagos Archipelago MPA (640,000 km(2) ) (Indian Ocean) lies at the heart of this debate. We conducted the first satellite tracking of a migratory species, the green turtle (Chelonia mydas), within the MPA and assessed the species' use of protected versus unprotected areas. We developed an approach to estimate length of residence within the MPA that may have utility across migratory taxa including tuna and sharks. We recorded the longest ever published migration for an adult cheloniid turtle (3979 km). Seven of 8 tracked individuals migrated to distant foraging grounds, often ≥1000 km outside the MPA. One turtle traveled to foraging grounds within the MPA. Thus, networks of small MPAs, developed synergistically with larger MPAs, may increase the amount of time migrating species spend within protected areas. The MPA will protect turtles during the breeding season and will protect some turtles on their foraging grounds within the MPA and others during the first part of their long-distance postbreeding oceanic migrations. International cooperation will be needed to develop the network of small MPAs needed to supplement the Chagos Archipelago MPA.

Nesting phenology of marine turtles: insights from a regional comparative analysis on green turtle (Chelonia mydas).

Changes in phenology, the timing of seasonal activities, are among the most frequently observed responses to environmental disturbances and in marine species are known to occur in response to climate changes that directly affects ocean temperature, biogeochemical composition and sea level. We examined nesting seasonality data from long-term studies at 8 green turtle (Chelonia mydas) rookeries that include 21 specific nesting sites in the South-West Indian Ocean (SWIO). We demonstrated that temperature drives patterns of nesting seasonality at the regional scale. We found a significant correlation between mean annual Sea Surface Temperature (SST) and dates of peak nesting with rookeries exposed to higher SST having a delayed nesting peak. This supports the hypothesis that temperature is the main factor determining peak nesting dates. We also demonstrated a spatial synchrony in nesting activity amongst multiple rookeries in the northern part of the SWIO (Aldabra, Glorieuses, Mohéli, Mayotte) but not with the eastern and southern rookeries (Europa, Tromelin), differences which could be attributed to females with sharply different adult foraging conditions. However, we did not detect a temporal trend in the nesting peak date over the study period or an inter-annual relation between nesting peak date and SST. The findings of our study provide a better understanding of the processes that drive marine species phenology. The findings will also help to predict their ability to cope with climate change and other environmental perturbations. Despite demonstrating this spatial shift in nesting phenology, no trend in the alteration of nesting dates over more than 20 years was found.

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 world's 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.

Whose turtles are they, anyway?

The hawksbill turtle (Eretmochelys imbricata), listed since 1996 by the IUCN as Critically Endangered and by the Convention on International Trade in Endangered Species (CITES) as an Appendix I species, has been the subject of attention and controversy during the past 10 years due to the efforts of some nations to re-open banned international trade. The most recent debate has centred on whether it is appropriate for Cuba to harvest hawksbills from shared foraging aggregations within her national waters. In this issue of Molecular Ecology, Bowen et al. have used molecular genetic data to show that such harvests are likely to have deleterious effects on the health of hawksbill populations throughout the Caribbean.