Cultivating epizoic diatoms provides insights into the evolution and ecology of both epibionts and hosts.

Our understanding of the importance of microbiomes on large aquatic animals-such as whales, sea turtles and manatees-has advanced considerably in recent years. The latest observations indicate that epibiotic diatom communities constitute diverse, polyphyletic, and compositionally stable assemblages that include both putatively obligate epizoic and generalist species. Here, we outline a successful approach to culture putatively obligate epizoic diatoms without their hosts. That some taxa can be cultured independently from their epizoic habitat raises several questions about the nature of the interaction between these animals and their epibionts. This insight allows us to propose further applications and research avenues in this growing area of study. Analyzing the DNA sequences of these cultured strains, we found that several unique diatom taxa have evolved independently to occupy epibiotic habitats. We created a library of reference sequence data for use in metabarcoding surveys of sea turtle and manatee microbiomes that will further facilitate the use of environmental DNA for studying host specificity in epizoic diatoms and the utility of diatoms as indicators of host ecology and health. We encourage the interdisciplinary community working with marine megafauna to consider including diatom sampling and diatom analysis into their routine practices.

On Sea Turtle-associated Craspedostauros (Bacillariophyta), with Description of Three Novel Species.

The current study focuses on four species from the primarily marine diatom genus Craspedostauros that were observed growing attached to numerous sea turtles and sea turtle-associated barnacles from Croatia and South Africa. Three of the examined taxa, C. danayanus sp. nov., C. legouvelloanus sp. nov., and C. macewanii sp. nov., are described based on morphological and, whenever possible, molecular characteristics. The new taxa exhibit characters not previously observed in other members of the genus, such as the presence of more than two rows of cribrate areolae on the girdle bands, shallow perforated septa, and a complete reduction of the stauros. The fourth species, C. alatus, itself recently described from museum sea turtle specimens, is reported for the first time from loggerhead sea turtles rescued in Europe. A 3-gene phylogenetic analysis including DNA sequence data for three sea turtle-associated Craspedostauros species and other marine and epizoic diatom taxa indicated that Craspedostauros is monophyletic and sister to Achnanthes. This study, being based on a large number of samples and animal specimens analyzed and using different preservation and processing methods, provides new insights into the ecology and biogeography of the genus and sheds light on the level of intimacy and permanency in the host-epibiont interaction within the epizoic Craspedostauros species.

Managing conflicts between economic activities and threatened migratory marine species toward creating a multiobjective blue economy.

Harnessing the economic potential of the oceans is key to combating poverty, enhancing food security, and strengthening economies. But the concomitant risk of intensified resource extraction to migratory species is worrying given these species contribute to important ecological processes, often underpin alternative livelihoods, and are mostly already threatened. We thus sought to quantify the potential conflict between key economic activities (5 fisheries and hydrocarbon exploitation) and sea turtle migration corridors in a region with rapid economic development: southern and eastern Africa. We satellite tracked the movement of 20 loggerhead (Caretta caretta) and 14 leatherback (Dermochelys coriacea) turtles during their postnesting migrations. We used movement-based kernel density estimation to identify migration corridors for each species. We overlaid these corridors on maps of the distribution and intensity of economic activities, quantified the extent of overlap and threat posed by each activity on each species, and compared the effects of activities. These results were compared with annual bycatch rates in the respective fisheries. Both species' 3 corridors overlapped most with longline fishing, but the effect was worse for leatherbacks: their bycatch rates of approximately 1500/year were substantial relative to the regional population size of <100 nesting females/annum. This bycatch rate is likely slowing population growth. Artisanal fisheries may be of greater concern for loggerheads than for leatherbacks, but the population appears to be withstanding the high bycatch rates because it is increasing exponentially. The hydrocarbon industry currently has a moderately low impact on both species, but mining in key areas (e.g., Southern Mozambique) may undermine >50 years of conservation, potentially affecting >80% of loggerheads, 33% of the (critically endangered) leatherbacks, and their nesting beaches. We support establishing blue economies (i.e., generating wealth from the ocean), but oceans need to be carefully zoned and responsibly managed in both space and time to achieve economic (resource extraction), ecological (conservation, maintenance of processes), and social (maintenance of alternative livelihood opportunities, alleviate poverty) objectives.

Coastal leatherback turtles reveal conservation hotspot.

Previous studies have shown that the world's largest reptile - the leatherback turtle Dermochelys coriacea - conducts flexible foraging migrations that can cover thousands of kilometres between nesting sites and distant foraging areas. The vast distances that may be travelled by migrating leatherback turtles have greatly complicated conservation efforts for this species worldwide. However, we demonstrate, using a combination of satellite telemetry and stable isotope analysis, that approximately half of the nesting leatherbacks from an important rookery in South Africa do not migrate to distant foraging areas, but rather, forage in the coastal waters of the nearby Mozambique Channel. Moreover, this coastal cohort appears to remain resident year-round in shallow waters (<50 m depth) in a relatively fixed area. Stable isotope analyses further indicate that the Mozambique Channel also hosts large numbers of loggerhead turtles Caretta caretta. The rare presence of a resident coastal aggregation of leatherback turtles not only presents a unique opportunity for conservation, but alongside the presence of loggerhead turtles and other endangered marine megafauna in the Mozambique Channel, highlights the importance of this area as a marine biodiversity hotspot.

Epibiotic Diatoms Are Universally Present on All Sea Turtle Species.

The macro-epibiotic communities of sea turtles have been subject to growing interest in recent years, yet their micro-epibiotic counterparts are almost entirely unknown. Here, we provide the first evidence that diatoms are epibionts for all seven extant species of sea turtle. Using Scanning Electron Microscopy, we inspected superficial carapace or skin samples from a single representative of each turtle species. We distinguished 18 diatom taxa from these seven individuals, with each sea turtle species hosting at least two diatom taxa. We recommend that future research is undertaken to confirm whether diatom communities vary between sea turtle species and whether these diatom taxa are facultative or obligate commensals.

Impacts of plastic ingestion on post-hatchling loggerhead turtles off South Africa.

Twenty-four of 40 (60%) loggerhead turtle Caretta caretta post-hatchlings (carapace<9cm) that died within 2months of stranding on southern Cape beaches in April 2015 contained ingested anthropogenic debris. Plastic comprised of 99% of debris: 77% hard plastic fragments, 10% flexible packaging and 8% fibres; industrial pellets comprised only 3%, compared to ~70% in 1968-1973, when 12% of stranded post-hatchlings contained plastics. Turtles selected for white (38%) and blue (19%) items, but translucent items (23%) were under-represented compared to beach mesodebris. Ingested loads did not decrease up to 52days in captivity, indicating long retention times. Plastic killed 11 turtles by blocking their digestive tracts or bladders, and contributed to the deaths of five other turtles. Our results indicate that the amount and diversity of plastic ingested by post-hatchling loggerhead turtles off South Africa have increased over the last four decades, and now kill some turtles.

Global analysis of the effect of local climate on the hatchling output of leatherback turtles.

The most recent climate change projections show a global increase in temperatures along with precipitation changes throughout the 21(st) century. However, regional projections do not always match global projections and species with global distributions may exhibit varying regional susceptibility to climate change. Here we show the effect of local climatic conditions on the hatchling output of leatherback turtles (Dermochelys coriacea) at four nesting sites encompassing the Pacific, Atlantic and Indian Oceans. We found a heterogeneous effect of climate. Hatchling output increased with long-term precipitation in areas with dry climatic conditions (Playa Grande, Pacific Ocean and Sandy Point, Caribbean Sea), but the effect varied in areas where precipitation was high (Pacuare, Caribbean Sea) and was not detected at the temperate site (Maputaland, Indian Ocean). High air temperature reduced hatchling output only at the area experiencing seasonal droughts (Playa Grande). Climatic projections showed a drastic increase in air temperature and a mild decrease in precipitation at all sites by 2100. The most unfavorable conditions were projected for Sandy Point where hatching success has already declined over time along with precipitation levels. The heterogeneous effect of climate may lead to local extinctions of leatherback turtles in some areas but survival in others by 2100.

Metrics to assess ecological condition, change, and impacts in sandy beach ecosystems.

Complexity is increasingly the hallmark in environmental management practices of sandy shorelines. This arises primarily from meeting growing public demands (e.g., real estate, recreation) whilst reconciling economic demands with expectations of coastal users who have modern conservation ethics. Ideally, shoreline management is underpinned by empirical data, but selecting ecologically-meaningful metrics to accurately measure the condition of systems, and the ecological effects of human activities, is a complex task. Here we construct a framework for metric selection, considering six categories of issues that authorities commonly address: erosion; habitat loss; recreation; fishing; pollution (litter and chemical contaminants); and wildlife conservation. Possible metrics were scored in terms of their ability to reflect environmental change, and against criteria that are widely used for judging the performance of ecological indicators (i.e., sensitivity, practicability, costs, and public appeal). From this analysis, four types of broadly applicable metrics that also performed very well against the indicator criteria emerged: 1.) traits of bird populations and assemblages (e.g., abundance, diversity, distributions, habitat use); 2.) breeding/reproductive performance sensu lato (especially relevant for birds and turtles nesting on beaches and in dunes, but equally applicable to invertebrates and plants); 3.) population parameters and distributions of vertebrates associated primarily with dunes and the supralittoral beach zone (traditionally focused on birds and turtles, but expandable to mammals); 4.) compound measurements of the abundance/cover/biomass of biota (plants, invertebrates, vertebrates) at both the population and assemblage level. Local constraints (i.e., the absence of birds in highly degraded urban settings or lack of dunes on bluff-backed beaches) and particular issues may require alternatives. Metrics - if selected and applied correctly - provide empirical evidence of environmental condition and change, but often do not reflect deeper environmental values per se. Yet, values remain poorly articulated for many beach systems; this calls for a comprehensive identification of environmental values and the development of targeted programs to conserve these values on sandy shorelines globally.

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.

Are coastal protected areas always effective in achieving population recovery for nesting sea turtles?

Sea turtles are highly migratory and usually dispersed, but aggregate off beaches during the nesting season, rendering them vulnerable to coastal threats. Consequently, coastal Marine Protection Areas (MPAs) have been used to facilitate the recovery of turtle populations, but the effectiveness of these programs is uncertain as most have been operating for less than a single turtle generation (or<20 yr). South Africa, however, hosts one of the longest running conservation programs, protecting nesting loggerhead (Caretta caretta) and leatherback (Dermochelys coriacea) turtles since 1963 in a series of coastal MPAs. This provides a unique opportunity to evaluate the long-term effect of spatial protection on the abundance of two highly migratory turtle species with different life history characteristics. Population responses were assessed by modeling the number of nests over time in an index area (13 km) and an expanded monitoring area (53 km) with varying survey effort. Loggerhead abundance increased dramatically from∼250 to>1700 nests pa (index area) especially over the last decade, while leatherback abundance increased initially∼10 to 70 nests pa (index area), but then stabilized. Although leatherbacks have higher reproductive output per female and comparable remigration periods and hatching success to loggerheads, the leatherback population failed to expand. Our results suggest that coastal MPAs can work but do not guarantee the recovery of sea turtle populations as pressures change over time. Causes considered for the lack of population growth include factors in the MPA (expansion into unmonitored areas or incubation environment) of outside of the MPA (including carrying capacity and fishing mortality). Conservation areas for migratory species thus require careful design to account for species-specific needs, and need to be monitored to keep track of changing pressures.

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.