Daily, seasonal, and long-distance movements inferred from Fastloc-GPS telemetry of immature green turtles (Chelonia mydas) at a high-latitude, mid-ocean developmental site.

To characterize the movements and habitat use of juvenile green turtles (Chelonia mydas) in benthic developmental habitat, we deployed Fastloc-GPS-enabled satellite transmitters on 16 individuals captured as part of a multi-decade study of green turtles on the Bermuda Platform. We characterized residence areas, distinct use areas within them, and seasonal movements based on an average of 562 Fastloc-GPS positions and 284 tracking days per turtle. We estimated residence area sizes using traditional home range methods, e.g., 90% utilization distribution (UD) (mean 2.29 ±2.71 km2) and 50% UD (mean 0.54 ±0.69 km2). Total residence area size increased significantly over the 8-year study, from <1 km2 before 2013 to ≥3 km2 in 2018 (R2 = 0.51, F1,14 = 14.55, p = 0.0019), corresponding to a period of decline in seagrass habitat and suggesting increased foraging effort. We identified three types of distinct use areas within residence areas where tracked turtles typically exhibited behavioral fidelity: foraging, resting, and cool weather refugia. These distinct use areas were smaller than high-use areas from previous studies; e.g., seagrass meadow foraging areas averaged 0.05 km2. Most turtles made daily transits between foraging and resting sites; for some individuals, these involved crossing frequently used vessel navigation channels. Seasonal variation in behavior suggested that the overwintering strategy for green turtles on the Bermuda Platform involves "optional dormancy," during which turtles spent less time on seagrass meadows and made brief excursions to distinct deeper habitats. Four individuals made directed (mean path straightness = 0.93 ±0.02 SD) developmental migrations away from Bermuda toward known adult foraging range. Results of our study further knowledge of the green turtle life cycle at a high-latitude site; they demonstrate that green turtles show fidelity to distinct use areas within developmental habitats over many years and exhibit seasonal movements.

Ecological regime shift drives declining growth rates of sea turtles throughout the West Atlantic.

Somatic growth is an integrated, individual-based response to environmental conditions, especially in ectotherms. Growth dynamics of large, mobile animals are particularly useful as bio-indicators of environmental change at regional scales. We assembled growth rate data from throughout the West Atlantic for green turtles, Chelonia mydas, which are long-lived, highly migratory, primarily herbivorous mega-consumers that may migrate over hundreds to thousands of kilometers. Our dataset, the largest ever compiled for sea turtles, has 9690 growth increments from 30 sites from Bermuda to Uruguay from 1973 to 2015. Using generalized additive mixed models, we evaluated covariates that could affect growth rates; body size, diet, and year have significant effects on growth. Growth increases in early years until 1999, then declines by 26% to 2015. The temporal (year) effect is of particular interest because two carnivorous species of sea turtles-hawksbills, Eretmochelys imbricata, and loggerheads, Caretta caretta-exhibited similar significant declines in growth rates starting in 1997 in the West Atlantic, based on previous studies. These synchronous declines in productivity among three sea turtle species across a trophic spectrum provide strong evidence that an ecological regime shift (ERS) in the Atlantic is driving growth dynamics. The ERS resulted from a synergy of the 1997/1998 El Niño Southern Oscillation (ENSO)-the strongest on record-combined with an unprecedented warming rate over the last two to three decades. Further support is provided by the strong correlations between annualized mean growth rates of green turtles and both sea surface temperatures (SST) in the West Atlantic for years of declining growth rates (r = -.94) and the Multivariate ENSO Index (MEI) for all years (r = .74). Granger-causality analysis also supports the latter finding. We discuss multiple stressors that could reinforce and prolong the effect of the ERS. This study demonstrates the importance of region-wide collaborations.

First Assessment of the Sex Ratio for an East Pacific Green Sea Turtle Foraging Aggregation: Validation and Application of a Testosterone ELISA.

Determining sex ratios of endangered populations is important for wildlife management, particularly species subject to sex-specific threats or that exhibit temperature-dependent sex determination. Sea turtle sex is determined by incubation temperature and individuals lack external sex-based traits until sexual maturity. Previous research utilized serum/plasma testosterone radioimmunoassays (RIA) to determine sex in immature/juvenile sea turtles. However, there has been a growing application of enzyme-linked immunosorbent assay (ELISA) for wildlife endocrinology studies, but no study on sea turtles has compared the results of ELISA and RIA. This study provides the first sex ratio for a threatened East Pacific green sea turtle (Chelonia mydas) foraging aggregation, a critical step for future management of this species. Here, we validate a testosterone ELISA and compare results between RIA and ELISA of duplicate samples. The ELISA demonstrated excellent correspondence with the RIA for providing testosterone concentrations for sex determination. Neither assay proved reliable for predicting the sex of reproductively active females with increased testosterone production. We then applied ELISA to examine the sex ratio of 69 green turtles foraging in San Diego Bay, California. Of 45 immature turtles sampled, sex could not be determined for three turtles because testosterone concentrations fell between the ranges for either sex (females: 4.1-113.1 pg/mL, males: 198.4-2,613.0 pg/mL) and these turtles were not subsequently recaptured to enable sex determination; using a Bayesian model to predict probabilities of turtle sex we predicted all three 'unknowns' were female (> 0.86). Additionally, the model assigned all turtles with their correct sex (if determined at recapture) with 100% accuracy. Results indicated a female bias (2.83F:1M) among all turtles in the aggregation; when focusing only on putative immature turtles the sex ratio was 3.5F:1M. With appropriate validation, ELISA sexing could be applied to other sea turtle species, and serve as a crucial conservation tool.

Historical versus contemporary climate forcing on the annual nesting variability of loggerhead sea turtles in the Northwest Atlantic Ocean.

A recent analysis suggested that historical climate forcing on the oceanic habitat of neonate sea turtles explained two-thirds of interannual variability in contemporary loggerhead (Caretta caretta) sea turtle nest counts in Florida, where nearly 90% of all nesting by this species in the Northwest Atlantic Ocean occurs. Here, we show that associations between annual nest counts and climate conditions decades prior to nest counts and those conditions one year prior to nest counts were not significantly different. Examination of annual nest count and climate data revealed that statistical artifacts influenced the reported 31-year lag association with nest counts. The projected importance of age 31 neophytes to annual nest counts between 2020 and 2043 was modeled using observed nest counts between 1989 and 2012. Assuming consistent survival rates among cohorts for a 5% population growth trajectory and that one third of the mature female population nests annually, the 41% decline in annual nest counts observed during 1998-2007 was not projected for 2029-2038. This finding suggests that annual nest count trends are more influenced by remigrants than neophytes. Projections under the 5% population growth scenario also suggest that the Peninsular Recovery Unit could attain the demographic recovery criteria of 106,100 annual nests by 2027 if nest counts in 2019 are at least comparable to 2012. Because the first year of life represents only 4% of the time elapsed through age 31, cumulative survival at sea across decades explains most cohort variability, and thus, remigrant population size. Pursuant to the U.S. Endangered Species Act, staggered implementation of protection measures for all loggerhead life stages has taken place since the 1970s. We suggest that the 1998-2007 nesting decline represented a lagged perturbation response to historical anthropogenic impacts, and that subsequent nest count increases since 2008 reflect a potential recovery response.

GLOBAL PHYLOGEOGRAPHY OF THE LOGGERHEAD TURTLE (CARETTA CARETTA) AS INDICATED BY MITOCHONDRIAL DNA HAPLOTYPES.

Restriction-site analyses of mitochondrial DNA (mtDNA) from the loggerhead sea turtle (Caretta caretta) reveal substantial phylogeographic structure among major nesting populations in the Atlantic, Indian, and Pacific oceans and the Mediterranean sea. Based on 176 samples from eight nesting populations, most breeding colonies were distinguished from other assayed nesting locations by diagnostic and often fixed restriction-site differences, indicating a strong propensity for natal homing by nesting females. Phylogenetic analyses revealed two distinctive matrilines in the loggerhead turtle that differ by a mean estimated sequence divergence p = 0.009, a value similar in magnitude to the deepest intraspecific mtDNA node (p = 0.007) reported in a global survey of the green sea turtle Chelonia mydas. In contrast to the green turtle, where a fundamental phylogenetic split distinguished turtles in the Atlantic Ocean and the Mediterranean Sea from those in the Indian and Pacific oceans, genotypes representing the two primary loggerhead mtDNA lineages were observed in both Atlantic-Mediterranean and Indian-Pacific samples. We attribute this aspect of phylogeographic structure in Caretta caretta to recent interoceanic gene flow, probably mediated by the ability of this temperate-adapted species to utilize habitats around southern Africa. These results demonstrate how differences in the ecology and geographic ranges of marine turtle species can influence their comparative global population structures.

GLOBAL POPULATION STRUCTURE AND NATURAL HISTORY OF THE GREEN TURTLE (CHELONIA MYDAS) IN TERMS OF MATRIARCHAL PHYLOGENY.

To address aspects of the evolution and natural history of green turtles, we assayed mitochondrial (mt) DNA genotypes from 226 specimens representing 15 major rookeries around the world. Phylogenetic analyses of these data revealed (1) a comparatively low level of mtDNA variability and a slow mtDNA evolutionary rate (relative to estimates for many other vertebrates); (2) a fundamental phylogenetic split distinguishing all green turtles in the Atlantic-Mediterranean from those in the Indian-Pacific Oceans; (3) no evidence for matrilineal distinctiveness of a commonly recognized taxonomic form in the East Pacific (the black turtle C.m. agassizi or C. agassizi); (4) in opposition to published hypotheses, a recent origin for the Ascension Island rookery, and its close genetic relationship to a geographically proximate rookery in Brazil; and (5) a geographic population substructure within each ocean basin (typically involving fixed or nearly fixed genotypic differences between nesting populations) that suggests a strong propensity for natal homing by females. Overall, the global matriarchal phylogeny of Chelonia mydas appears to have been shaped by both geography (ocean basin separations) and behavior (natal homing on regional or rookery-specific scales). The shallow evolutionary population structure within ocean basins likely results from demographic turnover (extinction and colonization) of rookeries over time frames that are short by evolutionary standards but long by ecological standards.