Navigation and seasonal migratory orientation in juvenile sea turtles

Juvenile loggerhead and green turtles that inhabit inshore waters of North Carolina, USA undertake long seasonal migrations, after which they often return to specific feeding areas. In addition, juvenile turtles are capable of homing to specific sites after being displaced. As a first step towards investigating the navigational mechanisms that underlie these movements, juvenile turtles were captured in coastal waters of North Carolina and displaced 30-167 km along circuitous routes while deprived of visual cues. At the testing location, turtles were tethered in a circular arena and permitted to swim while their orientation was monitored. Between May and September, when juvenile loggerhead and green turtles inhabit feeding areas along the North Carolina coast, turtles oriented in directions that corresponded closely with the most direct route back to their capture locations. During October and November, however, both loggerhead and green turtles oriented southward, a direction consistent with the migratory paths of turtles beginning their autumn migration. The results demonstrate for the first time that both homing and migratory orientation can be elicited in juvenile turtles under laboratory conditions in which orientation cues can be readily manipulated. In addition, the results provide evidence that juvenile loggerheads can assess their position relative to a goal using local cues available at the test site and are therefore capable of map-based navigation

Use of multiple orientation cues by juvenile loggerhead sea turtles Caretta caretta

Although the orientation cues used by hatchling sea turtles have been studied extensively, little is known about the mechanisms of orientation and navigation that guide older turtles. To investigate the orientation cues used by juvenile loggerhead

Variability in age and size at maturation, reproductive longevity, and long-term growth dynamics for Kemp's ridley sea turtles in the Gulf of Mexico

Effective management of protected sea turtle populations requires knowledge not only of mean values for demographic and life-history parameters, but also temporal and spatial trends, variability, and underlying causes. For endangered Kemp's ridley sea turtles (Lepidochelys kempii), the need for baseline information of this type has been emphasized during attempts to understand causes underlying the recent truncation in the recovery trajectory for nesting females. To provide insight into variability in age and size at sexual maturation (ASM and SSM) and long-term growth patterns likely to influence population trends, we conducted skeletochronological analysis of humerus bones from 333 Kemp's ridleys stranded throughout the Gulf of Mexico (GOM) from 1993 to 2010. Ranges of possible ASMs (6.8 to 21.8 yr) and SSMs (53.3 to 68.3 cm straightline carapace length (SCL)) estimated using the "rapprochement" skeletal growth mark associated with maturation were broad, supporting incorporation of a maturation schedule in Kemp's ridley population models. Mean ASMs estimated from rapprochement and by fitting logistic, generalized additive mixed, and von Bertalanffy growth models to age and growth data ranged from 11 to 13 yr; confidence intervals for the logistic model predicted maturation of 95% of the population between 11.9 and 14.8 yr. Early juvenile somatic growth rates in the GOM were greater than those previously reported for the Atlantic, indicating potential for differences in maturation trajectories between regions. Finally, long-term, significant decreases in somatic growth response were found for both juveniles and adults, which could influence recruitment to the reproductive population and observed nesting population trends

Patterns of loggerhead turtle ontogenetic shifts revealed through isotopic analysis of annual skeletal growth increments

Ontogenetic changes in resource use often delimit transitions between life stages. Ecological and individual factors can cause variation in the timing and consistency of these transitions, ultimately affecting community and population dynamics through changes in growth and survival. Therefore, it is important to document and understand behavioral and life history polymorphisms, and the processes that drive intraspecific variation in them. To evaluate juvenile loggerhead sea turtle (Caretta caretta) life history variation and to detect shifts in habitat and diet that occur during an oceanic-to-neritic ontogenetic shift, we sequentially analyzed the stable isotope composition of humerus bone growth increments from turtles that stranded dead on Southeastern U.S. beaches between 1997 and 2013 (n = 84). In one-half of the sampled turtles, growth increment-specific nitrogen stable isotope (δ¹⁵N) data showed significant increases in δ¹⁵N values over each turtle's life. These data were used to provide a new line of evidence that juvenile Northwest Atlantic loggerheads exhibit two major ontogenetic shift patterns: discrete shifts (n = 24), which were completed within one year, and facultative shifts (n = 14), which were completed over multiple years (up to five). The mean difference in pre- and post-ontogenetic shift δ¹⁵N values was 4.3‰. Differences in isotopic baselines between neritic and oceanic habitats of the Northwest Atlantic Ocean make it likely these patterns are driven by a coupled change in both habitat and diet, and that facultative shifters utilize both neritic and oceanic resources within transitional growth years. Mean size and age at transition between habitats (54.2 cm straightline carapace length, SCL; 11.98 yr) was within the range of previous estimates and did not differ between discrete and facultative shifters. Our results further expand our understanding of loggerhead sea turtle life history polymorphisms and demonstrate the value of bone tissue analysis to the study of this variation. Sequential analysis of annual skeletal growth increments provides a valuable method for reconstructing long-term ontogenetic changes in foraging ecology and habitat use in long-lived, cryptic marine species

Dietary plasticity linked to divergent growth trajectories in a critically endangered sea turtle

Foraging habitat selection and diet quality are key factors that influence individual fitness and meta-population dynamics through effects on demographic rates. There is growing evidence that sea turtles exhibit regional differences in somatic growth linked to alternative dispersal patterns during the oceanic life stage. Yet, the role of habitat quality and diet in shaping somatic growth rates is poorly understood. Here, we evaluate whether diet variation is linked to regional growth variation in hawksbill sea turtles (Eretmochelys imbricata), which grow significantly slower in Texas, United States versus Florida, United States, through novel integrations of skeletal growth, gastrointestinal content (GI), and bulk tissue and amino acid (AA)-specific stable nitrogen (δ15N) and carbon (δ13C) isotope analyses. We also used AA δ15N ΣV values (heterotrophic bacterial re-synthesis index) and δ13C essential AA (δ13CEAA) fingerprinting to test assumptions about the energy sources fueling hawksbill food webs regionally. GI content analyses, framed within a global synthesis of hawksbill dietary plasticity, revealed that relatively fast-growing hawksbills stranded in Florida conformed with assumptions of extensive spongivory for this species. In contrast, relatively slow-growing hawksbills stranded in Texas consumed considerable amounts of non-sponge invertebrate prey and appear to forage higher in the food web as indicated by isotopic niche metrics and higher AA δ15N-based trophic position estimates internally indexed to baseline nitrogen isotope variation. However, regional differences in estimated trophic position may also be driven by unique isotope dynamics of sponge food webs. AA δ15N ΣV values and δ13CEAA fingerprinting indicated minimal bacterial re-synthesis of organic matter (ΣV < 2) and that eukaryotic microalgae were the primary energy source supporting hawksbill food webs. These findings run contrary to assumptions that hawksbill diets predominantly comprise high microbial abundance sponges expected to primarily derive energy from bacterial symbionts. Our findings suggest alternative foraging patterns could underlie regional variation in hawksbill growth rates, as divergence from typical sponge prey might correspond with increased energy expenditure and reduced foraging success or diet quality. As a result, differential dispersal patterns may infer substantial individual and population fitness costs and represent a previously unrecognized challenge to the persistence and recovery of this critically endangered species

Informing research priorities for immature sea turtles through expert elicitation

Although sea turtles have received substantial focus worldwide, research on the immature life stages is still relatively limited. The latter is of particular importance, given that a large proportion of sea turtle populations comprises immature individuals. We set out to identify knowledge gaps and identify the main barriers hindering research in this field. We analyzed the perceptions of sea turtle experts through an online survey which gathered their opinions on the current state of affairs on immature sea turtle research, including species and regions in need of further study, priority research questions, and barriers that have interfered with the advancement of research. Our gap analysis indicates that studies on immature leatherback Dermochelys coriacea and hawksbill Eretmochelys imbricata turtles are lacking, as are studies on all species based in the Indian, South Pacific, and South Atlantic Oceans. Experts also perceived that studies in population ecology, namely on survivorship and demography, and habitat use/behavior, are needed to advance the state of knowledge on immature sea turtles. Our survey findings indicate the need for more inter-disciplinary research, collaborative efforts (eg data-sharing, joint field activities), and improved communication among researchers, funding bodies, stakeholders, and decision-makers

Methods for sampling sequential annual bone growth layers for stable isotope analysis

1. Stable carbon (§13C) and nitrogen (§15N) isotope analysis (SIA) has proven useful in addressing fundamental questions in ecology such as reconstructing trophic interactions, habitat connections and climate regime shifts. The temporal scales over which SIA can be used to address ecological problems vary depending on the protein turnover times of the analysed tissue. Hard, inert tissues, such as teeth, bones and mollusc shells, grow in regular intervals (i.e. daily or annually), and sequential sampling of these growth layers provides a time series of isotopic patterns. As a result, SIA on these tissues is useful for elucidating behaviour and ecology of animals over time, especially those with cryptic life-history stages, such as marine turtles that retain growth layers in their humerus bones. To date, there exists no standard protocol for the sequential sampling of cortical bone samples taken from fresh, modern samples for SIA. 2. We tested two different methods,micromilling untreated bone cross sections and biopsy coring bone cross sections processed for skeletochronology, for sequentially sampling individual growth layers from marine turtle humerus bones. 3. We present a standard protocol for sequential bone growth layer sampling for SIA, facilitating direct comparison of future studies. We recommend using the micromilling sampling technique on untreated bone cross sections, as it facilitated higher precision sampling of growth layers that were not affected by chemical processing, and minimized sample handling, thereby reducing chances for contamination. 4. This is the first study to present a standardized method to sequentially sample annual bone growth layers for stable isotope analysis and facilitates direct comparison among future studies

Informing Research Priorities For Immature Sea Turtles Through Expert Elicitation

Although sea turtles have received substantial focus worldwide, research on the immature life stages is still relatively limited. The latter is of particular importance, given that a large proportion of sea turtle populations comprises immature individuals. We set out to identify knowledge gaps and identify the main barriers hindering research in this field. We analyzed the perceptions of sea turtle experts through an online survey which gathered their opinions on the current state of affairs on immature sea turtle research, including species and regions in need of further study, priority research questions, and barriers that have interfered with the advancement of research. Our gap analysis indicates that studies on immature leatherback Dermochelys coriacea and hawksbill Eretmochelys imbricata turtles are lacking, as are studies on all species based in the Indian, South Pacific, and South Atlantic Oceans. Experts also perceived that studies in population ecology, namely on survivorship and demography, and habitat use/behavior, are needed to advance the state of knowledge on immature sea turtles. Our survey findings indicate the need for more interdisciplinary research, collaborative efforts (e.g. data-sharing, joint field activities), and improved communication among researchers, funding bodies, stakeholders, and decision-makers

Use of skeletochronological analysis to estimate the age of leatherback sea turtles Dermochelys coriacea in the western North Atlantic

Although growth rate and age data are essential for leatherback management, estimates of these demographic parameters remain speculative due to the cryptic life history of this endangered species. Skeletochronological analysis of scleral ossicles obtained from 8 captive, known-age and 33 wild leatherbacks originating from the western North Atlantic was conducted to characterize the ossicles and the growth marks within them. Ages were accurately estimated for the known-age turtles, and their growth mark attributes were used to calibrate growth mark counts for the ossicles from wild specimens. Due to growth mark compaction and resorption, the number of marks visible at ossicle section tips was consistently and significantly greater than the number visible along the lateral edges, demonstrating that growth mark counts should be performed at the tips so that age is not underestimated. A correction factor protocol that incorporated the trajectory of early growth increments was used to estimate the number of missing marks in those ossicles exhibiting resorption, which was then added to the number of observed marks to obtain an age estimate for each turtle. A generalized smoothing spline model, von Bertalanffy growth curve, and size-at-age function were used to obtain estimates of age at maturity for leatherbacks in the western North Atlantic. Results of these analyses suggest that median age at maturation for leatherbacks in this part of the world may range from 24.5 to 29 yr. These age estimates are much greater than those proposed in previous studies and have significant implications for population management and recovery

Intrapopulation variability in the timing of ontogenetic habitat shifts in sea turtles revealed using δ15 N values from bone growth rings.

Determining location and timing of ontogenetic shifts in the habitat use of highly migratory species, along with possible intrapopulation variation in these shifts, is essential for understanding mechanisms driving alternate life histories and assessing overall population trends. Measuring variations in multi-year habitat-use patterns is especially difficult for remote oceanic species. To investigate the potential for differential habitat use among migratory marine vertebrates, we measured the naturally occurring stable nitrogen isotope (δ15 N) patterns that differentiate distinct ocean regions to create a 'regional isotope characterization', analysed the δ15 N values from annual bone growth layer rings from dead-stranded animals, and then combined the bone and regional isotope data to track individual animal movement patterns over multiple years. We used humeri from juvenile North Pacific loggerhead turtles (Caretta caretta), animals that undergo long migrations across the North Pacific Ocean (NPO), using multiple discrete regions as they develop to adulthood. Typical of many migratory marine species, ontogenetic changes in habitat use throughout their decades-long juvenile stage is poorly understood, but each potential habitat has unique foraging opportunities and spatially explicit natural and anthropogenic threats that could affect key life-history parameters. We found a bimodal size/age distribution in the timing that juveniles underwent an ontogenetic habitat shift from the oceanic central North Pacific (CNP) to the neritic east Pacific region near the Baja California Peninsula (BCP) (42·7 ± 7·2 vs. 68·3 ± 3·4 cm carapace length, 7·5 ± 2·7 vs. 15·6 ± 1·7 years). Important to the survival of this population, these disparate habitats differ considerably in their food availability, energy requirements and threats, and these differences can influence life-history parameters such as growth, survival and future fecundity. This is the first evidence of alternative ontogenetic shifts and habitat-use patterns for juveniles foraging in the eastern NPO. We combine two techniques, skeletochronology and stable isotope analysis, to reconstruct multi-year habitat-use patterns of a remote migratory species, linked to estimated ages and body sizes of individuals, to reveal variable ontogeny during the juvenile life stage that could drive alternate life histories and that has the potential to illuminate the migration patterns for other species with accretionary tissues