Temperature-Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance.

The adaptive significance of temperature-dependent sex determination (TSD) in reptiles remains unknown decades after TSD was first identified in this group. Concurrently, there is growing concern about the effect that rising temperatures may have on species with TSD, potentially producing extremely biased sex ratios or offspring of only one sex. The current state-of the-art in TSD research on sea turtles is reviewed here and, against current paradigm, it is proposed that TSD provides an advantage under warming climates. By means of coadaptation between early survival and sex ratios, sea turtles are able to maintain populations. When offspring survival declines at high temperatures, the sex that increases future fecundity (females) is produced, increasing resilience to climate warming. TSD could have helped reptiles to survive mass extinctions in the past via this model. Flaws in research on sex determination in sea turtles are also identified and it is suggested that the development of new techniques will revolutionize the field.

Are thermal barriers "higher" in deep sea turtle nests?

Thermal tolerances are affected by the range of temperatures that species encounter in their habitat. Daniel Janzen hypothesized in his "Why mountain passes are higher in the tropics" that temperature gradients were effective barriers to animal movements where climatic uniformity was high. Sea turtles bury their eggs providing some thermal stability that varies with depth. We assessed the relationship between thermal uniformity and thermal tolerance in nests of three species of sea turtles. We considered that barriers were "high" when small thermal changes had comparatively large effects and "low" when the effects were small. Mean temperature was lower and fluctuated less in species that dig deeper nests. Thermal barriers were comparatively "higher" in leatherback turtle (Dermochelys coriacea) nests, which were the deepest, as embryo mortality increased at lower "high" temperatures than in olive ridley (Lepidochelys olivacea) and green turtle (Chelonia mydas) nests. Sea turtles have temperature-dependent sex determination (TSD) and embryo mortality increased as temperature approached the upper end of the transitional range of temperatures (TRT) that produces both sexes (temperature producing 100% female offspring) in leatherback and olive ridley turtles. As thermal barriers are "higher" in some species than in others, the effects of climate warming on embryo mortality is likely to vary among sea turtles. Population resilience to climate warming may also depend on the balance between temperatures that produce female offspring and those that reduce embryo survival.

Shading and watering as a tool to mitigate the impacts of climate change in sea turtle nests.

Increasing sand temperatures resulting from climate change may negatively impact sea turtle nests by altering sex ratios and decreasing reproductive output. We analyzed the effect of nest shading and watering on sand temperatures as climate mitigation strategies in a beach hatchery at Playa Grande, Costa Rica. We set up plots and placed thermocouples at depths of 45 cm and 75 cm. Half of the plots were shaded and half were exposed to the sun. Within these exposure treatments, we applied three watering treatments over one month, replicating local climatic conditions experienced in this area. We also examined gravimetric water content of sand by collecting sand samples the day before watering began, the day after watering was complete, and one month after completion. Shading had the largest impact on sand temperature, followed by watering and depth. All watering treatments lowered sand temperature, but the effect varied with depth. Temperatures in plots that received water returned to control levels within 10 days after watering stopped. Water content increased at both depths in the two highest water treatments, and 30 days after the end of water application remained higher than plots with low water. While the impacts of watering on sand temperature dissipate rapidly after the end of application, the impacts on water content are much more lasting. Although less effective at lowering sand temperatures than shading, watering may benefit sea turtle clutches by offsetting negative impacts of low levels of rain in particularly dry areas. Prior to implementing such strategies, the natural conditions at the location of interest (e.g. clutch depth, environmental conditions, and beach characteristics) and natural hatchling sex ratios should be taken into consideration. These results provide insight into the effectiveness of nest shading and watering as climate mitigation techniques and illustrate important points of consideration in the crafting of such strategies.

Movements and diving behavior of internesting green turtles along Pacific Costa Rica.

Using satellite transmitters, we determined the internesting movements, spatial ecology and diving behavior of East Pacific green turtles (Chelonia mydas) nesting on Nombre de Jesús and Zapotillal beaches along the Pacific coast of northwestern Costa Rica. Kernel density analysis indicated that turtles spent most of their time in a particularly small area in the vicinity of the nesting beaches (50% utilization distribution was an area of 3 km(2) ). Minimum daily distance traveled during a 12 day internesting period was 4.6 ± 3.5 km. Dives were short and primarily occupied the upper 10 m of the water column. Turtles spent most of their time resting at the surface and conducting U-dives (ranging from 60 to 81% of the total tracking time involved in those activities). Turtles showed a strong diel pattern, U-dives mainly took place during the day and turtles spent a large amount of time resting at the surface at night. The lack of long-distance movements demonstrated that this area was heavily utilized by turtles during the nesting season and, therefore, was a crucial location for conservation of this highly endangered green turtle population. The unique behavior of these turtles in resting at the surface at night might make them particularly vulnerable to fishing activities near the nesting beaches.

Population assessment of the American crocodile, Crocodylus acutus (Crocodilia: Crocodylidae) on the Pacific coast of Costa Rica

The American crocodile, Crocodylus acutus, is widely distributed in the American neotropics. It is endangered throughout most of its range and is listed as vulnerable by the International Union for the Conservation of Natural Fauna and Flora (IUCN) and on Appendix I of the Convention for the International Trade in Endangered Species of Wild Flora and Fauna (CITES). Despite this listing, there are few published reports on population status throughout most of its range. We investigated the status of the C. acutus, at several locations along the Pacific coast of Costa Rica. We carried out spotlight and nesting surveys from 2007-2009 along the Costa Rican Pacific coast in four distinct areas, coastal areas of Las Baulas (N=40) and Santa Rosa (N=9) National Parks and the Osa Conservation Area (N=13), and upriver in Palo Verde National Park (N=11). We recorded crocodile locations and standard environmental data at each observation. Encounter rates, population structure, distribution within each area and data on successful nesting (presence of hatchlings, nests, etc) were determined. We attempted to capture all crocodiles to record standard morphometrics. A total of 586 crocodiles were observed along 185.8km of survey route. The majority of animals encountered (54.9%) were either hatchlings (<0.5m) or juveniles (0.5-1.25m). The average non-hatchling encounter rate per survey for the Pacific coast was 3.1 crocodiles/km, with individual encounter rates ranging from 1.2 crocodiles/km to 4.3 crocodiles/ km in Las Baulas National Park and the Osa Conservation Area respectively. Distribution of size classes within the individual locations did not differ with the exception of Santa Rosa and Las Baulas National Parks, where hatchlings were found in water with lower salinities. These were the first systematic surveys in several of the areas studied and additional work is needed to further characterize the American crocodile population in Costa Rica.

El cocodrilo americano, Crocodylus acutus, se encuentra ampliamente distribuido en el neotrópico Americano y hay pocos estudios publicados sobre el estado de sus poblaciones en la mayor parte de su rango de distribución. Investigamos el estado del Cocodylus acutus en varias ubicaciones a lo largo de la costa del Pacífico de Costa Rica. Se realizaron muestreos nocturnos y de anidación a lo largo de la Costa Pacífica de Costa Rica en cuatro áreas en particular desde 2007-2009,’áreas costeras en los Parque Nacionales de Las Baulas (N=40) y Santa Rosa (N=9), y en el Área de Conservación de la Osa (N=13) y en el curso alto del Parque Nacional de Palo Verde (N=11). Se registraron datos de la ubicación de los cocodrilos y datos ambientales estándar en cada observación. Se determinó la tasa de encuentros, estructura de la población, distribución dentro de cada área y evidencia de anidación exitosa (presencia de neonatos, nidos, etc.). Intentamos capturar todos los cocodrilos para registrar información morfométrica estándar. En total, se observaron 586 cocodrilos a lo largo de 185.8km de ruta de muestreo. La mayoría de los animales encontrados (54.9%) fueron neonatos (<0.5m) o juveniles (0.5-1.25m). La tasa promedio de encuentros por muestreo de no-neonatos en la costa del Pacífico fue de 3.1 cocodrilos/km; con rangos de encuentro de individuos de entre 1.2 a 4.3 cocodrilos/km en el Parque Nacional de Las Baulas y el Área de Conservación Osa. La distribución por clases de tamaño no varió, a excepción de los Parques Nacionales de Santa Rosa y Las Baulas, donde se encontró a los neonatos en aguas con bajas salinidades. Estos fueron los primeros muestreos sistemáticos en varias de las áreas estudiadas y son necesarios trabajos adicionales para caracterizar las poblaciones de cocodrilo Americano en Costa Rica.

Climate driven egg and hatchling mortality threatens survival of eastern Pacific leatherback turtles.

Egg-burying reptiles need relatively stable temperature and humidity in the substrate surrounding their eggs for successful development and hatchling emergence. Here we show that egg and hatchling mortality of leatherback turtles (Dermochelys coriacea) in northwest Costa Rica were affected by climatic variability (precipitation and air temperature) driven by the El Niño Southern Oscillation (ENSO). Drier and warmer conditions associated with El Niño increased egg and hatchling mortality. The fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC) projects a warming and drying in Central America and other regions of the World, under the SRES A2 development scenario. Using projections from an ensemble of global climate models contributed to the IPCC report, we project that egg and hatchling survival will rapidly decline in the region over the next 100 years by ∼50-60%, due to warming and drying in northwestern Costa Rica, threatening the survival of leatherback turtles. Warming and drying trends may also threaten the survival of sea turtles in other areas affected by similar climate changes.

On the dispersal of leatherback turtle hatchlings from Mesoamerican nesting beaches.

So little is known about the early life history of leatherback turtles (Dermochelys coriacea) from hatchling to adulthood that this period has been termed the 'lost years'. For critically endangered eastern Pacific leatherback populations, continued and rapid declines underscore the urgent need to develop conservation strategies across all life stages. We investigate leatherback hatchling dispersal from four Mesoamerican nesting beaches using passive tracer experiments within a regional ocean modelling system. The evolution of tracer distribution from each of the nesting beaches showed the strong influence of eddy transport and coastal currents. Modelled hatchlings from Playa Grande, Costa Rica, were most likely to be entrained and transported offshore by large-scale eddies coincident with the peak leatherback nesting and hatchling emergence period. These eddies potentially serve as 'hatchling highways', providing a means of rapid offshore transport away from predation and a productive refuge within which newly hatched turtles can develop. We hypothesize that the most important leatherback nesting beach remaining in the eastern Pacific (Playa Grande) has been evolutionarily selected as an optimal nesting site owing to favourable ocean currents that enhance hatchling survival.

Population assessment of the American crocodile, Crocodylus acutus (Crocodilia: Crocodylidae) on the Pacific coast of Costa Rica.

The American crocodile, Crocodylus acutus, is widely distributed in the American neotropics. It is endangered throughout most of its range and is listed as vulnerable by the International Union for the Conservation of Natural Fauna and Flora (IUCN) and on Appendix I of the Convention for the International Trade in Endangered Species of Wild Flora and Fauna (CITES). Despite this listing, there are few published reports on population status throughout most of its range. We investigated the status of the C. acutus, at several locations along the Pacific coast of Costa Rica. We carried out spotlight and nesting surveys from 2007-2009 along the Costa Rican Pacific coast in four distinct areas, coastal areas of Las Baulas (N=40) and Santa Rosa (N=9) National Parks and the Osa Conservation Area (N=13), and upriver in Palo Verde National Park (N=11). We recorded crocodile locations and standard environmental data at each observation. Encounter rates, population structure, distribution within each area and data on successful nesting (presence of hatchlings, nests, etc) were determined. We attempted to capture all crocodiles to record standard morphometrics. A total of 586 crocodiles were observed along 185.8km of survey route. The majority of animals encountered (54.9%) were either hatchlings (<0.5m) or juveniles (0.5-1.25m). The average non-hatchling encounter rate per survey for the Pacific coast was 3.1 crocodiles/km, with individual encounter rates ranging from 1.2 crocodiles/km to 4.3 crocodiles/ km in Las Baulas National Park and the Osa Conservation Area respectively. Distribution of size classes within the individual locations did not differ with the exception of Santa Rosa and Las Baulas National Parks, where hatchlings were found in water with lower salinities. These were the first systematic surveys in several of the areas studied and additional work is needed to further characterize the American crocodile population in Costa Rica.

Effects of illegal harvest of eggs on the population decline of leatherback turtles in Las Baulas Marine National Park, Costa Rica.

Within 19 years the nesting population of leatherback turtles (Dermochelys coriacea) at Parque Nacional Marino Las Baulas declined from 1500 turtles nesting per year to about 100. We analyzed the effects of fishery bycatch and illegal harvesting (poaching) of eggs on this population. We modeled the population response to different levels of egg harvest (90, 75, 50, and 25%) and the effect of eradicating poaching at different times during the population decline. We compared effects of 90% poaching with those of 20% adult mortality because both of these processes were present in the population at Las Baulas. There was a stepwise decline in number of nesting turtles at all levels of egg harvest. Extirpation times for different levels of poaching ranged from 45 to 282 years. The nesting population declined more slowly and survived longer with 20% adult mortality (146 years) than it did with 90% poaching (45 years). Time that elapsed until poaching stopped determined the average population size at which the population stabilized, ranging from 90 to 420 nesting turtles. Our model predicted that saving clutches lost naturally would restore the population when adult mortality rates were low and would contribute more to population recovery when there were short remigration intervals between nesting seasons and a large proportion of natural loss of clutches. Because the model indicated that poaching was the most important cause of the leatherback decline at Las Baulas, protecting nests on the beach and protecting the beach from development are critical for survival of this population. Nevertheless, the model predicted that current high mortality rates of adults will prevent population recovery. Therefore, protection of the beach habitat and nests must be continued and fishery bycatch must be reduced to save this population.

Persistent leatherback turtle migrations present opportunities for conservation.

Effective transboundary conservation of highly migratory marine animals requires international management cooperation as well as clear scientific information about habitat use by these species. Populations of leatherback turtles (Dermochelys coriacea) in the eastern Pacific have declined by >90% during the past two decades, primarily due to unsustainable egg harvest and fisheries bycatch mortality. While research and conservation efforts on nesting beaches are ongoing, relatively little is known about this population of leatherbacks' oceanic habitat use and migration pathways. We present the largest multi-year (2004-2005, 2005-2006, and 2007) satellite tracking dataset (12,095 cumulative satellite tracking days) collected for leatherback turtles. Forty-six females were electronically tagged during three field seasons at Playa Grande, Costa Rica, the largest extant nesting colony in the eastern Pacific. After completing nesting, the turtles headed southward, traversing the dynamic equatorial currents with rapid, directed movements. In contrast to the highly varied dispersal patterns seen in many other sea turtle populations, leatherbacks from Playa Grande traveled within a persistent migration corridor from Costa Rica, past the equator, and into the South Pacific Gyre, a vast, low-energy, low-productivity region. We describe the predictable effects of ocean currents on a leatherback migration corridor and characterize long-distance movements by the turtles in the eastern South Pacific. These data from high seas habitats will also elucidate potential areas for mitigating fisheries bycatch interactions. These findings directly inform existing multinational conservation frameworks and provide immediate regions in the migration corridor where conservation can be implemented. We identify high seas locations for focusing future conservation efforts within the leatherback dispersal zone in the South Pacific Gyre.

Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino Las Baulas, Costa Rica.

Physiology, environment and life history demands interact to influence marine turtle bioenergetics and activity. However, metabolism and diving behavior of free-swimming marine turtles have not been measured simultaneously. Using doubly labeled water, we obtained the first field metabolic rates (FMRs; 0.20-0.74 W kg(-1)) and water fluxes (16-30% TBW day(-1), where TBW=total body water) for free-ranging marine turtles and combined these data with dive information from electronic archival tags to investigate the bioenergetics and diving activity of reproductive adult female leatherback turtles Dermochelys coriacea. Mean dive durations (7.8+/-2.4 min (+/-1 s.d.), bottom times (2.7+/-0.8 min), and percentage of time spent in water temperatures (Tw) < or =24 degrees C (9.5+/-5.7%) increased with increasing mean maximum dive depths (22.6+/-7.1 m; all P< or =0.001). The FMRs increased with longer mean dive durations, bottom times and surface intervals and increased time spent in Tw< or =24 degrees C (all r2> or =0.99). This suggests that low FMRs and activity levels, combined with shuttling between different water temperatures, could allow leatherbacks to avoid overheating while in warm tropical waters. Additionally, internesting leatherback dive durations were consistently shorter than aerobic dive limits calculated from our FMRs (11.7-44.3 min). Our results indicate that internesting female leatherbacks maintained low FMRs and activity levels, thereby spending relatively little energy while active at sea. Future studies should incorporate data on metabolic rate, dive patterns, water temperatures, and body temperatures to develop further the relationship between physiological and life history demands and marine turtle bioenergetics and activity.

Biotic and abiotic factors affect the nest environment of embryonic leatherback turtles, Dermochelys coriacea.

Clutches of leatherback turtles, Dermochelys coriacea, have lower hatching success than those of other sea turtles, but causes of high embryonic mortality are unknown. We measured characteristics of clutches along with spatial and temporal changes in PO(2) and temperature during incubation to determine the extent to which they affected the developmental environment of leatherback embryos. Minimum PO(2) in nests decreased as both the total number and mass of metabolizing embryos increased. Increases in both the number and mass of metabolizing embryos caused an increase in maximum nest temperature. However, neither PO(2) nor temperature was correlated with hatching success. Our measurements of relatively high nest PO(2) (lowest 17.1 kPa or 16.9% O(2)) indicate that hypoxia apparently does not cause the low hatching success of leatherback clutches. Oxygen partial pressure increased and temperature decreased from the center toward the periphery of leatherback nests. We inferred from these measurements that positions of eggs within nests vary in quality and potentially affect overall developmental success of entire clutches. The large metabolic mass of leatherback clutches and limits to gas flux imposed by the sand create a situation in which leatherback embryos collectively affect their own environment.