Karen A. Bjorndal

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.

Nutrition and grazing behavior of the green turtle Chelonia mydas.

The apparent digestibility coefficients for 4 size classes of the green turtle Chelonia mydas feeding on the seagrass Thalassia testudinum were measured in Union Creek, Great Inagua, Bahamas, from September 1975 to August 1976. The values ranged from 32.6 to 73.9% for organic matter; from 21.5 to 70.7% for energy; from 71.5 to 93.7% for cellulose; from 40.3 to 90.8% for hemicellulose; and from 14.4 to 56.6% for protein. Digestive efficiency increased with increases in water temperature and body size. There was no seasonal variation in the nutrient composition of T. testudinum blades. Grazing on T. testudinum may be limited by its low quality as a forage, a result of its high fiber content and possible low protein availability. Turtles did not graze at random over the extensive beds of T. testudinum, but maintained “grazing plots” of young leaves by consistent recropping. They thus consumed a more digestible forage-higher in protein and lower in lignin-than the ungrazed, older leaves of T. testudinum. The selectivity of green turtles for either a seagrass or algal diet may reflect the specificity of their intestinal microflora.

Role of larger herbivores in seagrass communities

The nutritional ecology of macroherbivores in seagrass meadows and the roles of grazing by urchins, fishes and green turtles in tropical systems and waterfowl in temperate systems are discussed in this review. Only a few species of animals graze on living seagrasses, and apparently only a small portion of the energy and nutrients in seagrasses is usually channeled through these herbivores. The general paucity of direct seagrass grazers may be a function of several factors in the composition of seagrasses, including availability of nitrogen compounds, presence of relatively high amounts of structural cell walls, and presence of toxic or inhibitory substances. The macroherbivores, however, can have a profound effect on the seagrass plants, on other grazers and fauna associated with the meadow, and on chemical and decompositional processes occurring within the meadow. Grazing can alter the nutrient content and digestibility of the plant, as well as its productivity. Removal of leaf material can influence interrelations among permanent and transient faunal residents. Grazing also interrupts the detritus cycle. Possible consequences of this disruption, either through acceleration or through decreased source input, and the enhancement of intersystem coupling by increased export and offsite fecal production, are discussed. The extent and magnitude of these effects and their ecological significance in the overall functioning of seagrass meadows only can be speculated, and probably are not uniform or of similar importance in both tropical and temperate seagrass systems. However, areas grazed by large herbivores provide natural experiments in which to test hypotheses on many functional relations in seagrass meadows.

GREEN TURTLE SOMATIC GROWTH MODEL: EVIDENCE FOR DENSITY DEPENDENCE

The green turtle, Chelonia mydas, is a circumglobal species and a primary herbivore in marine ecosystems. Overexploitation as a food resource for human populations has resulted in drastic declines or extinction of green turtle populations in the Greater Caribbean. Attempts to manage the remaining populations on a sustainable basis are ham- pered by insufficient knowledge of demographic parameters. In particular, compensatory responses resulting from density-dependent effects have not been evaluated for any sea turtle population and thus have not been explicitly included in any population models. Growth rates of immature green turtles were measured during an 18-yr study in Union Creek, a wildlife reserve in the southern Bahamas. We have evaluated the growth data for both straight carapace length (SCL) and body mass with nonparametric regression models that had one response variable (absolute growth rate) and five potential covariates: sex, site, year, mean size, and recapture interval. The SCL model of size-specific growth rates was a good fit to the data and accounted for 59% of the variance. The body-mass model was not a good fit to the data, accounting for only 26% of the variance. In the SCL model, sex, site, year, and mean size all had significant effects, whereas recapture interval did not. We used results of the SCL model to evaluate a density-dependent effect on somatic growth rates. Over the 18 yr of our study, relative population density underwent a sixfold increase followed by a threefold decrease in Union Creek as a result of natural immigration and emigration. Three lines of evidence support a density-dependent effect. First, there is a significant inverse correlation between population density and mean annual growth rate. Second, the condition index (mass/(SCL)3) of green turtles in Union Creek is positively correlated with mean annual growth rates and was negatively correlated with population density, indicating that the green turtles were nutrient limited during periods of low growth and high population densities. Third, the population in Union Creek fluctuated around carrying capacity during our study and thus was at levels likely to experience density- dependent effects that could be measured. We estimate the carrying capacity of pastures of the seagrass Thalassia testudinum, the major diet plant of the green turtle, as a range from 122 to 4439 kg green turtles/ha or 16- 586 million 50-kg green turtles in the Caribbean. Because green turtle populations are probably regulated by food limitation under natural conditions, carrying capacity can serve as a baseline to estimate changes in green turtle populations in the Caribbean since pre- Columbian times and to set a goal for recovery for these depleted populations. Finally, we compare the growth functions for green turtle populations in the Atlantic and Pacific oceans. Not only does the form of the size-specific growth functions differ between the two regions (monotonic declining in the Atlantic and nonmonotonic in the Pacific), but also small juvenile green turtles in the Atlantic have substantially higher growth rates than those in the Pacific. Research is needed to evaluate the causes of these differences, but our results indicate that demographic parameters between ocean basins should only be extrapolated with great caution.

TRANSATLANTIC DEVELOPMENTAL MIGRATIONS OF LOGGERHEAD SEA TURTLES DEMONSTRATED BY mtDNA SEQUENCE ANALYSIS

Molecular markers based on mitochondrial (mt) DNA control region sequences were used to test the hypothesis that juvenile loggerhead sea turtles (Caretta caretta) in pelagic habitats of the eastern Atlantic are derived from nesting populations in the western Atlantic. We compared mtDNA haplotypes from 131 pelagic juvenile turtles (79 from the Azores and 52 from Madeira) to mtDNA haplotypes observed in major nesting colonies of the Atlantic Ocean and Mediterranean Sea. A subset of 121 pelagic samples (92%) contained haplotypes that match mtDNA sequences observed in nesting colonies. Maximum likelihood analyses (UCON, SHADRACQ) estimate that 100% of these pelagic juveniles are from the nesting populations in the southeastern United States and adjacent Yucatan Peninsula, Mexico. Estimated contributions from nesting populations in south Florida (0.71, 0.72), northern Florida to North Carolina (0.19, 0.17), and Quintana Roo, Mexico (0.11, 0.10) are consistent with the relative size of these nesting aggregates....

The 'lost years' of green turtles: using stable isotopes to study cryptic lifestages

Ignorance of the location or inaccessible locations of lifestages can impede the study and management of species. We used stable isotopes of carbon and nitrogen to identify the habitats and diets and to estimate the duration of a ‘missing’ lifestage: the early juvenile stage of the green turtle, Chelonia mydas. Stable isotopes in scute from young herbivorous green turtles in shallow-water habitats revealed that they spend 3–5 years as carnivores in oceanic habitats before making a rapid ontogenetic shift in diet and habitat. Stable isotopes in persistent and continuously growing tissues, such as some fish scales, bird bills and claws and mammal hair and claws, can be used to evaluate the ecology of inaccessible lifestages.

Ingestion of marine debris by juvenile sea turtles in coastal Florida habitats

Digestive tracts from 51 sea turtle carcasses that washed ashore on the east and west coasts of Florida were examined for the presence of anthropogenic debris. Debris was found in 24 of 43 green turtles (Chelonia mydas), 0 of 7 Kemps ridleys (Lepidochelys kempi), and 1 of 1 loggerhead (Caretta caretta). Ingested debris included plastic, monofilament line, fish hooks, rubber, aluminium foil, and tar. For green turtles, ingestion of debris was not significantly affected by location of stranding, season, or body size. Debris ingestion was significantly affected by sex of the turtle. Frequency of occurrence of debris was significantly higher in females, but differences in the mass or volume of ingested debris were not significantly different between the sexes. Although frequency of occurrence of debris was high in green turtles (56%), the mass and volume of the debris were small—mean 0.52% of wet mass of gut contents and mean 0.72% of the volume of gut contents, respectively. However, small quantities of debris can kill sea turtles; the death of at least two turtles in this study resulted from debris ingestion. The debris in the two turtles represented 4.6% and 5.8% of wet mass and 3.2% and 9.8% of volume of the gut contents, respectively. In both turtles, the debris represented inflated percentages because the turtles had not been feeding normally prior to death because the debris affected gut function. Sublethal effects of debris ingestion (e.g. absorption of toxins) has an unknown—but potentially great—negative effect on the demography of sea turtles.

Nutritional Ecology of Sea Turtles

Analysis of the nutritional ecology of sea turtles, that is, how nutrition influences their biology and determines their interactions with the environment, is necessarily restricted to the green turtle, Chelonia mydas. Our knowledge of the nutrition of the other species of sea turtles is limited to information on diet from gut content studies and a few reports on the anatomy and histology of the digestive tract. The literature on diet and gut anatomy and histology are summarized in the first two sections of this review. The remainder of this review is a discussion of the nutrition of Caribbean green turtles: their digestive efficiencies, adaptations to their major food plant Thalassia testudinum, and the effect the diet has, through nutrient limitation, on their productivity. Although Thalassia is a very abundant food source which is fairly constant in productivity and nutrient quality, few herbivores graze on it. Green turtles have two adaptations that enable them to utilize Thalassia more efficiently. First, they maintain grazing plots where, by cropping the young regrowth, they obtain blades of much higher quality because of lower lignin and higher nitrogen concentrations. Secondly, they have a hindgut microbial fermentation that digests the fiber in Thalassia and yields both an important energy source to the green turtle, in the form of volatile fatty acids, and gives the green turtle access to the highly digestible cell contents. In spite of the advantages of these adaptations-grazing plots and hindgut fermentation-they are not sufficient to prevent nutrient limitation and the resulting slow growth rates, delayed sexual maturity, and reduced reproductive output. Comparison with green turtles on high-quality, pelleted diets shows that the productivity of wild populations is well below their genetic potential. Ironically, nutrient limitation acting through delayed sexual maturity may benefit green turtles during periods of intense exploitation by man.

Relation of Temperature, Moisture, Salinity, and Slope to Nest Site Selection in Loggerhead Sea Turtles

Abstract Nest site selection in reptiles can affect the fitness of the parents through the survival of their offspring because environmental factors influence embryo survivorship, hatchling quality, and sex ratio. In sea turtles, nest site selection is influenced by selective forces that drive nest placement inland and those that drive nest placement seaward. Nests deposited close to the ocean have a greater likelihood of inundation and egg loss to erosion whereas nest placement farther inland results in greater likelihood of desiccation, hatchling misorientation, and predation on nesting females, eggs, and hatchlings. To evaluate the role of microhabitat cues in nest site selection in Loggerhead Sea Turtles (Caretta caretta), we assessed temperature, moisture, salinity (conductivity), and slope along the tracks of 45 female loggerheads during their beach ascent from the ocean to nest sites in the Archie Carr National Wildlife Refuge in Florida on the beach with the greatest density of loggerhead nesting in the Atlantic. Of the four environmental factors evaluated (slope, temperature, moisture, and salinity), slope appears to have the greatest influence on nest site selection, perhaps because it is associated with nest elevation. Our results refute the current hypothesis that an abrupt increase in temperature is used by loggerheads as a cue for excavating a nest. Moisture content and salinity of surface sand are potential cues but may not be reliable for nest site selection because they can vary substantially and rapidly in response to rainfall and changes in the water table. Sea turtles may use multiple cues for nest site selection either in series with a threshold that must be reached for each environmental factor before the turtle initiates nest excavation or integrated as specific patterns of associations.