Marc Girondot

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.

The evolution of long bone microstructure and lifestyle in lissamphibians

Abstract The compactness profile of femoral cross-sections and body size of 105 specimens of 46 species of lissamphibians was studied to assess the effect of lifestyle (aquatic, amphibious, or terrestrial). Several tests that incorporate phylogenetic information (permutational multiple linear regression incorporating phylogenetic distances, logistic regression using phylogenetic weighting, concentrated-changes tests) show that the return to a fully aquatic lifestyle is associated with an increase in the compactness of the femur and an increase in body size. However, amphibious taxa cannot be distinguished from terrestrial ones solely on the basis of size or compactness. Body size and compactness profile parameters of the femur exhibit a phylogenetic signal (i.e., closely related taxa tend to be more similar to each other than to distantly related taxa). Mathematical equations obtained from our data by using logistic regression with phylogenetic weighting are used to infer the lifestyle of four early stegocephalians. The results are generally congruent with prevailing paleontological interpretations, which suggests that this method could be applied to infer the lifestyle of early taxa whose lifestyle is poorly understood.

BONE PROFILER: A TOOL TO QUANTIFY, MODEL, AND STATISTICALLY COMPARE BONE-SECTION COMPACTNESS PROFILES

Bone cross sections show many characteristics that have been used to infer various properties of the individual or taxon from which they were prepared. Life history traits (Castanet et al., 1993), locomotor patterns (Casinos, 1996), habitat (Laurin et al., 2000), metabolism (Ricqlès, 1983), and growth rate (Rimblot-Baly et al., 1995) are some examples. However, bone microstructure is very complex, and few objective, quantitative methods (other than very simple ones, such as the cortico-diaphyseal index, or the global compactness) are available to describe bone sections in a way that enables statistical inference or comparison. Several cross-sectional properties, such as the cross-sectional area, centroid coordinates relative to reference axes, second moments of area about x and y axes, principal second moments of area and their orientation, section modulus, and polar moment of area have been obtained using SLICE (Nagurka and Hayes, 1980) by Ruff and Hayes (1983) and others, while Cubo and Casinos (1998) produced their own software for similar purposes. These parameters are especially useful for studying the stiffness, strength, or resistance of bones for animals of known weight and living in similar habitats. They do not describe how the bone tissue is organized. To model bone tissue distribution in sections, we need to reduce its complexity to a limited number of variables that can be further compared using statistical tests. Among the various characteristics of bone sections that could be analyzed, we decided to work mainly on compactness (amount of bone present on a given surface) because this characteristic has previously been suspected to provide much information about the life style of taxa (Laurin et al., 2000). Furthermore, compactness can be measured relatively easily from a bone section (because it only requires knowledge about the presence or absence of bone on a given area). In contrast, bone mineral density requires the use of quantitative micro-radiography that is technically more demanding. An additional advantage of working with compactness is that it can be measured both on extant animals and on fossils. Bone mineral density can usually not be evaluated on fossil bones because of the variable amount of permineralization and other diagenetic phenomena that affect fossil tissues.

Temperature-dependent sex determination and global change: are some species at greater risk?

In species with temperature-dependent sex determination (TSD), global climate change may result in a strong sex ratio bias that could lead to extinction. The relationship between sex ratio and egg incubation at constant temperature in TSD species is characterized by two parameters: the pivotal temperature (P) and the transitional range of temperature that produces both sexes (TRT). Here, we show that the proportion of nests producing both sexes is positively correlated to the width of the TRT by a correlative approach from sex ratio data collected in the literature and by simulations of TSD using a mechanistic model. From our analyses, we predict that species with a larger TRT should be more likely to evolve in response to new thermal conditions, thus putting them at lower risk to global change.

Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana.

In sea turtles, parental investment is limited to the nutrients and energy invested in eggs that will support embryonic development. Leatherback females have the largest clutches with the biggest eggs of the sea turtles and the highest reproductive output in reptiles. The migration between foraging sites and nesting beaches also represents high energy expenditure. The toxicokinetic of pollutants in the tissues is thus expected to vary during those periods but there is a lack of information in reptiles. Concentrations of essential (Copper, Zinc, Selenium) and non-essentials elements (Cadmium, Lead, Mercury) were determined in blood (n=78) and eggs (n=76) of 46 free-ranging leatherback females collected in French Guiana. Maternal transfer to eggs and relationships between blood and eggs concentrations during the nesting season were investigated. All trace elements were detectable in both tissues. Levels of toxic metals were lower than essential elements likely due to the high pelagic nature of leatherbacks that seems to limit exposure to toxic elements. Significant relationships between blood and egg concentrations were observed for Se and Cd. Se could have an important role in embryonic development of leatherback turtles and Cd transfer could be linked to similar carrier proteins as Se. Finally, as multiple clutches were sampled from each female, trends in trace elements were investigated along the nesting season. No change was observed in eggs but changes were recorded in blood concentrations of Cu. Cu level decreased while blood Pb levels increased through the nesting season. The high demand on the body during the breeding season seems to affect blood Cu concentrations. Calcium requirement for egg production with concomitant Pb mobilization could explain the increase in blood Pb concentrations along the nesting season.

Molecular Evolution of Amelogenin in Mammals

An evolutionary analysis of mammalian amelogenin, the major protein of forming enamel, was conducted by comparison of 26 sequences (including 14 new ones) representative of the main mammalian lineages. Amelogenin shows highly conserved residues in the hydrophilic N- and C-terminal regions. The central hydrophobic region (most of exon 6) is more variable, but it has conserved a high amount of proline and glutamine located in triplets, PXQ, indicating that these residues play an important role. This region evolves more rapidly, and is less constrained, than the other well-conserved regions, which are subjected to strong constraints. The comparison of the substitution rates in relation to the CpG richness confirmed that the highly conserved regions are subjected to strong selective pressures. The amino acids located at important sites and the residues known to lead to amelogenesis imperfecta when substituted were present in all sequences examined. Evolutionary analysis of the variable region of exon 6 points to a particular zone, rich in either amino acid insertion or deletion. We consider this region a hot spot of mutation for the mammalian amelogenin. In this region, numerous triplet repeats (PXQ) have been inserted recently and independently in five lineages, while most of the hydrophobic exon 6 region probably had its origin in several rounds of triplet insertions, early in vertebrate evolution. The putative ancestral DNA sequence of the mammalian amelogenin was calculated using a maximum likelihood approach. The putative ancestral protein was composed of 177 residues. It already contained all important amino acid positions known to date, its hydrophobic variable region was rich in proline and glutamine, and it contained triplet repeats PXQ as in the modern sequences.

Isotope analysis reveals foraging area dichotomy for atlantic leatherback turtles.

Background The leatherback turtle (Dermochelys coriacea) has undergone a dramatic decline over the last 25 years, and this is believed to be primarily the result of mortality associated with fisheries bycatch followed by egg and nesting female harvest. Atlantic leatherback turtles undertake long migrations across ocean basins from subtropical and tropical nesting beaches to productive frontal areas. Migration between two nesting seasons can last 2 or 3 years, a time period termed the remigration interval (RI). Recent satellite transmitter data revealed that Atlantic leatherbacks follow two major dispersion patterns after nesting season, through the North Gulf Stream area or more eastward across the North Equatorial Current. However, information on the whole RI is lacking, precluding the accurate identification of feeding areas where conservation measures may need to be applied. Methodology/Principal Findings Using stable isotopes as dietary tracers we determined the characteristics of feeding grounds of leatherback females nesting in French Guiana. During migration, 3-year RI females differed from 2-year RI females in their isotope values, implying differences in their choice of feeding habitats (offshore vs. more coastal) and foraging latitude (North Atlantic vs. West African coasts, respectively). Egg-yolk and blood isotope values are correlated in nesting females, indicating that egg analysis is a useful tool for assessing isotope values in these turtles, including adults when not available. Conclusions/Significance Our results complement previous data on turtle movements during the first year following the nesting season, integrating the diet consumed during the year before nesting. We suggest that the French Guiana leatherback population segregates into two distinct isotopic groupings, and highlight the urgent need to determine the feeding habitats of the turtle in the Atlantic in order to protect this species from incidental take by commercial fisheries. Our results also emphasize the use of eggs, a less-invasive sampling material than blood, to assess isotopic data and feeding habits for adult female leatherbacks.

Density-dependent nest destruction and population fluctuations of Guianan leatherback turtles

Approximately 40% of the world’s leatherback marine turtles (Dermochelys coriacea) nest in Suriname and French Guiana. Trends in nest numbers reconstructed for the last 34 years indicate several up and down events. We undertook computer simulations to determine whether a density-dependent phenomenon might be involved because the period of high-density nesting coincides with a high level of nest destruction by nesting females. The parameters of density-dependent nest destruction were calculated for the Ya:lima:po-Awa:la beach. We show that: (1) density-dependent nest destruction occurs, but (2) it promotes a density-dependent feminization of hatchling sex ratio, and consequently (3) the global production of juveniles continues to increase in relation with the increasing number of deposited nests even for the highest densities observed at that beach. Mean annual production of female hatchlings per adult female, although density dependent, is less than two juveniles even at the lowest densities of nesting females.

Maternal transfer of chlorinated contaminants in the leatherback turtles, Dermochelys coriacea, nesting in French Guiana

We examined the maternal transfer of organochlorine contaminants (OCs), pesticides (DDTS and HCHs) and polychlorinated biphenyls (PCBs), and the temporal variation of blood and eggs concentrations from 38 leatherback turtles (Dermochelys coriacea) nesting in French Guiana. PCBs were found to be the dominant OCs with respective mean concentrations of 55.14 ng g(-1) lipid-mass for egg and 1.26 ng mL(-1) wet-mass for blood. OC concentrations were lower than concentrations measured in other marine turtles which might be due to the lower trophic position (diet based on gelatinous zooplankton) and to the location of their foraging and nesting grounds. All OCs detected in leatherback blood were detected in eggs, suggesting a maternal transfer of OCs. This transfer was shown to depend on female blood concentration for SigmaDDTs and for the most prevalent PCB congeners, since significant relationships were found between paired blood-egg concentrations. During the nesting season, OC concentrations in eggs and the percentage of lipid in eggs were found to decline in successive clutches, highlighting a process of offloading from females to their eggs and a decreasing investment of lipid from females into their clutches. OCs in eggs tended to be higher in females spending 3 years in the foraging grounds between two nesting seasons than in those spending 2 years, suggesting an impact of time spacing two breeding seasons, called remigration interval, and of location of the foraging grounds.