Effects of diving and swimming behavior on body temperatures of pacific leatherback turtles in tropical seas

Mathematical models and recordings of cloacal temperature suggest that leatherback turtles (Dermochelys coriacea) maintain core body temperature higher than ambient water temperature (T(W)) while freely swimming at sea. We investigated the thermoregulatory capabilities of free-ranging leatherbacks and, specifically, the effect that changes in diving patterns and ambient temperatures have on leatherback body temperatures (T(B)). Data loggers were used to record subcarapace and gastrointestinal tract temperatures (T(SC) and T(GT), respectively), T(W), swim speed, dive depth, and dive times of female leatherback turtles during internesting intervals off the coast of Guanacaste, Costa Rica. Mean T(SC) (28.7 degrees -29.0 degrees C) was significantly higher than mean T(W) (25.0 degrees -27.5 degrees C). There was a significant positive relationship between T(SC) and T(W) and a significant negative correlation between T(SC) and dive depth and T(GT) and dive depth. Rapid fluctuations in T(GT) occurred during the first several days of the internesting interval, which suggests that turtles were ingesting prey or water during this time. Turtles spent 79%-91% of the time at sea swimming at speeds greater than 0.2 m s(-1), and the average swim speed was 0.7 +/- 0.2 m s(-1). Results from this study show that alterations in diving behavior and T(W) affect T(B) of leatherback turtles in the tropics. Body temperatures of free-ranging leatherback turtles correspond well with values for T(B) predicted by mathematical models for tropical conditions.     

Locomotion in hatchling leatherback turtles Dermochelys coriacea

Hatchling leatherback turtles can only swim forwards, and employ synchronized beating of the forelimbs whether swimming slowly or quickly. The hind limbs make no contribution to propulsion. Effectively, the hatchlings have two swimming speeds; subsurface and fast (30 cm s^-1) or surfaced and slow (8 cm s^-1). Intermediate velocities are transitory; the hatchlings were never seen to rest without movement, nor did they exhibit gliding of the type seen in green turtles. During fast ('vigorous') swimming, power is developed on both the upstroke and downstroke of the limb cycle. During slow swimming, power is only developed during the upstroke—a consequence of the orientation of the axis of limb beat which is opposite in direction to that of cheloniid sea turtles. Terrestrial locomotion is laboured and features an unstable gait which involves simultaneous movement of all four limbs and forward overbalancing during each limb cycle.     

Migration cues and timing in leatherback sea turtles

Atlantic leatherback sea turtles migrate annually from foraginggrounds off eastern Canada and the northeastern United Statesto southern foraging and breeding areas. Using Cox's proportionalhazards model, we investigated the individual timing of thesouthward migrations of 27 turtles equipped with satellite-linkedtransmitters off Nova Scotia compared with turtle characteristicsand satellite-measured ocean variables. Latitude, longitude,1-week lagged average sea surface temperature, and 1-week laggedaverage chlorophyll-a concentration appear to influence theprobability of departure. Higher temperature and, in the northernrange of the study, higher chlorophyll concentration increaseddeparture rates, perhaps due to the acceleration of the lifecycle of the leatherback's gelatinous prey and/or increasedfeeding efficiency in these areas. This study highlights theopportunity to use satellite telemetry and environmental datato examine the cues for and timing of animal migrations andexpands the study of migration timing to include a new speciesand environment.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

Navigational challenges in the oceanic migrations of leatherback sea turtles

The open-sea movements of marine animals are affected by the drifting action of currents that, if not compensated for, can produce non-negligible deviations from the correct route towards a given target. Marine turtles are paradigmatic skilful oceanic navigators that are able to reach remote goals at the end of long-distance migrations, apparently overcoming current drift effects. Particularly relevant is the case of leatherback turtles (Dermochelys coriacea), which spend entire years in the ocean, wandering in search of planktonic prey. Recent analyses have revealed how the movements of satellite-tracked leatherbacks in the Indian, Atlantic and Pacific Oceans are strongly dependent on the oceanic currents, up to the point that turtles are often passively transported over long distances. However, leatherbacks are known to return to specific areas to breed every 2–3 years, thus finding their way back home after long periods in the oceanic environment. Here we examine the navigational consequences of the leatherbacks'' close association with currents and discuss how the combined reliance on mechanisms of map-based navigation and local orientation cues close to the target may allow leatherbacks to accomplish the difficult task of returning to specific sites after years spent wandering in a moving medium.     

Behaviour and physiology: the thermal strategy of leatherback turtles

Background

Adult leatherback turtles (Dermochelys coriacea) exhibit thermal gradients between their bodies and the environment of ≥8°C in sub-polar waters and ≤4°C in the tropics. There has been no direct evidence for thermoregulation in leatherbacks although modelling and morphological studies have given an indication of how thermoregulation may be achieved.

Methodology/Principal Findings

We show for the first time that leatherbacks are indeed capable of thermoregulation from studies on juvenile leatherbacks of 16 and 37 kg. In cold water (< 25°C), flipper stroke frequency increased, heat loss through the plastron, carapace and flippers was minimized, and a positive thermal gradient of up to 2.3°C was maintained between body and environment. In warm water (25 – 31°C), turtles were inactive and heat loss through their plastron, carapace and flippers increased. The thermal gradient was minimized (0.5°C). Using a scaling model, we estimate that a 300 kg adult leatherback is able to maintain a maximum thermal gradient of 18.2°C in cold sub-polar waters.

Conclusions/Significance

In juvenile leatherbacks, heat gain is controlled behaviourally by increasing activity while heat flux is regulated physiologically, presumably by regulation of blood flow distribution. Hence, harnessing physiology and behaviour allows leatherbacks to keep warm while foraging in cold sub-polar waters and to prevent overheating in a tropical environment.     

Long-term monitoring of leatherback turtle diving behaviour during oceanic movements

The diving behaviour of four leatherback turtles (Dermochelys coriacea) was recorded for periods of 0.5-8.1 months during their postnesting movements in the Indian and Atlantic Oceans, when they covered 1569-18,994 km. Dive data were obtained using satellite-linked transmitters which also provided information on the dive depths and profiles of the turtles. Turtles mainly dove to depths < 200 m, with maximum dive durations under 30-40 min and exhibited diel variations in their diving activity for most part of the routes, with dives being usually longer at night. Diurnal dives were in general quite short, but cases of very deep (> 900 m) and prolonged (> 70 min) dives were however recorded only during daytime. The three turtles that were tracked for the longest time showed a marked change in behaviour during the tracking, decreasing their dive durations and ceasing to dive deeply. Moreover, diel variations disappeared, with nocturnal dives becoming short and numerous. This change in turtle diving activity appeared to be related to water temperature, suggesting an influence of seasonal prey availability on their diving behaviour. The turtle diving activity was independent on the shape of their routes, with no changes between linear movements in the core of main currents or looping segments in presence of oceanic eddies.     

Renal oxalosis in free-ranging green turtles Chelonia mydas

Eighteen green turtles Chelonia mydas recovered from the Atlantic and Gulf coasts of Florida and Tortuguero National Park, Costa Rica, were diagnosed with renal oxalosis by histopathological examination. Affected sea turtles included 14 adults and 4 immature animals, which comprised 26% (18/69) of green turtle necropsy cases available for review. Calcium oxalate deposition ranged from small to moderate amounts and was associated with granuloma formation and destruction of renal tubules. All affected turtles died from traumatic events or health problems unrelated to renal oxalosis; however, 1 immature turtle had notable associated renal injury. Crystal composition was confirmed by infrared and scanning electron microscopy and energy dispersive X-ray analysis. The source of calcium oxalate is unknown and is presumed to be of dietary origin.     

Egg components, egg size, and hatchling size in leatherback turtles

Relationships between egg size, egg components, and neonate size have been investigated across a wide range of oviparous taxa. Differences in egg traits among taxa reflect not only phylogenetic differences, but also interactions between biotic (i.e., maternal resource allocation) and abiotic (i.e. nest environment conditions) factors. We examined relationships between egg mass, egg composition, and hatchling size in leatherback turtles (Dermochelys coriacea) because of the unique egg and reproductive characteristics of this species and of sea turtles in general. Albumen comprised 63.0%+/-2.8% (mean+/-S.D.) of egg mass and explained most of the variation in egg mass, whereas yolk comprised only 33.0%+/-2.7%. Additionally, leatherback albumen dry mass was approximately 16% of albumen wet mass. Whereas hatchling mass increased significantly with egg mass (n = 218 clutches), hatchling mass increased by only approximately 2 g for each 10 g increase in egg mass and was approximately 10-20 g greater than yolk mass. Taken together, our results indicate that albumen might play a particularly significant role in leatherback embryonic development, and that leatherback eggs are both capable of water uptake from the nest substrate and also possess a large reservoir of water in the albumen. Relationships between egg mass and egg components, such as variation in egg mass being largely explained by variation in albumen mass and egg mass containing a relatively high proportion of albumen solids, are more similar to bird eggs than to eggs of other non-avian reptiles. However, hatchling mass correlates more with yolk mass than with albumen mass, unlike patterns observed in bird eggs of similar composition.     

Current transport of leatherback sea turtles (Dermochelys coriacea) in the ocean

While the long-distance movements of pelagic vertebrates are becoming known thanks to satellite telemetry, the factors determining their courses have hardly been investigated. We have analysed the effects of oceanographic factors on the post-nesting movements of three satellite-tracked leatherback turtles (Dermochelys coriacea) moving in the southwest Indian Ocean. By superimposing the turtle tracks on contemporaneous images of sea-surface temperatures and sea height anomalies, we show that currentrelated features dominate the shape of the reconstructed routes. After an initial offshore movement, turtles moved along straight routes when in the core of the current, or executed loops within eddies. Large parts of the routes were strikingly similar to those of surface drifters tracked in the same region. These findings document that long-lasting oceanic movements of marine turtles may be shaped by oceanic currents.     

Nest site fidelity of leatherback turtles at Playa Grande, Costa Rica

The possibility of nest site fidelity of leatherback turtles, Dermochelys coriacea, raises concerns about the merit of translocating poorly located clutches to a safe hatchery. Specifically, if some females habitually nest in areas where the probability of egg survival is low because of tidal inundation, nest relocation may inadvertently select for turtles that make poor nest site selections. We investigate the nest site fidelity of leatherbacks by studying consecutive nest site selections by leatherbacks at Playa Grande, Costa Rica, from 1993 to 2001. Along the ocean-to-vegetation axis, consecutive nest placements were independent (G₄²=4.737, P=0.315). Regardless of previous zone choices, leatherbacks typically nested in the open beach above the high tide line and away from vegetation. Thus, concerns about translocation of poorly located nests are unfounded. Along the coastal axis, however, an independence model was rejected (G₃₆²=145.179, P<0.001). The log-linear model-based analysis we developed and applied indicated that the pattern of dependence in nest site locations is more consistent with a hypothesis of spatial proximity in which leatherbacks simply nest close to the site of the previous nest than it is with a hypothesis of intrinsic fidelity to a specific location on the beach. Our model-based approach is suitable for other settings where longitudinal nesting data are available.     

Topsy-turvy: turning the counter-current heat exchange of leatherback turtles upside down

Counter-current heat exchangers associated with appendages of endotherms feature bundles of closely applied arteriovenous vessels. The accepted paradigm is that heat from warm arterial blood travelling into the appendage crosses into cool venous blood returning to the body. High core temperature is maintained, but the appendage functions at low temperature. Leatherback turtles have elevated core temperatures in cold seawater and arteriovenous plexuses at the roots of all four limbs. We demonstrate that plexuses of the hindlimbs are situated wholly within the hip musculature, and that, at the distal ends of the plexuses, most blood vessels supply or drain the hip muscles, with little distal vascular supply to, or drainage from the limb blades. Venous blood entering a plexus will therefore be drained from active locomotory muscles that are overlaid by thick blubber when the adults are foraging in cold temperate waters. Plexuses maintain high limb muscle temperature and avoid excessive loss of heat to the core, the reverse of the accepted paradigm. Plexuses protect the core from overheating generated by muscular thermogenesis during nesting.     

Bacteraemia in free-ranging Hawaiian green turtles Chelonia mydas with fibropapillomatosis

Past studies of free-ranging green turtles Chelonia mydas with fibropapillomatosis (FP) in Hawaii have shown that animals become immunosuppressed with increasing severity of this disease. Additionally, preliminary clinical examination of moribund turtles with FP revealed that some animals were also bacteraemic. We tested the hypothesis that bacteraemia in sea turtles is associated with the severity of FP. We captured free-ranging green turtles from areas in Hawaii where FP is absent, and areas where FP has been endemic since the late 1950s. Each turtle was given an FP severity score ranging from 0 (no tumours) to 3 (severely affected). A fifth category included turtles that were stranded ashore and moribund with FP. We found that the percentage of turtles with bacteraemia increased with the severity of FP, and that the majority of bacteria cultured were Vibrio spp. Turtles with severe FP were more susceptible to bactaeremia, probably in part due to immunosuppression. The pattern of bacteraemia in relation to severity of disease strengthens the hypothesis that immunosuppression is a sequel to FP.     

Orientation behaviour of leatherback sea turtles within the North Atlantic subtropical gyre

Leatherback sea turtles (Dermochelys coriacea) travel thousands of kilometres between temperate feeding and tropical breeding/over-wintering grounds, with adult turtles able to pinpoint specific nesting beaches after multi-year absences. Their extensive migrations often occur in oceanic habitat where limited known sensory information is available to aid in orientation. Here, we examined the migratory orientation of adult male, adult female and subadult leatherbacks during their open-ocean movements within the North Atlantic subtropical gyre by analysing satellite-derived tracks from fifteen individuals over a 2-year period. To determine the turtles'' true headings, we corrected the reconstructed tracks for current drift and found negligible differences between current-corrected and observed tracks within the gyre. Individual leatherback headings were remarkably consistent throughout the subtropical gyre, with turtles significantly oriented to the south-southeast. Adult leatherbacks of both sexes maintained similar mean headings and showed greater orientation precision overall. The consistent headings maintained by adult and subadult leatherbacks within the gyre suggest use of a common compass sense.     

The diving behaviour of green turtles at Ascension Island

For six green turtles, Chelonia mydas, that had nested on Ascension Island in the South Atlantic, we used time-depth recorders to examine their diving behaviour during the subsequent internesting interval (10-12 days). All the turtles performed dives where they remained at a fixed depth for a long period, surfaced briefly and then dived to the same depth again. It is generally believed these dive profiles are caused by the turtles resting on the sea bed. The maximum depth that turtles routinely reached on these resting dives was between 18 and 20 m, with resting dives deeper than 20 m being extremely rare. Resting dive duration increased significantly with deeper dives. From this relationship, and assuming that turtles with fully inflated lungs at the surface need to dive to 19 m to achieve negative buoyancy, we estimated for two turtles that the oxygen consumption during resting dives was 0.016 and 0.020 litres O(2)/kg per h, respectively. This is similar to the value predicted from the allometric scaling relationship for the minimal oxygen consumption of turtles. We calculated that the energy conserved by resting during the internesting period may appreciably increase the reproductive output of females. Copyright 2000 The Association for the Study of Animal Behaviour.     

Robust hierarchical state-space models reveal diel variation in travel rates of migrating leatherback turtles

1. Biological and statistical complexity are features common to most ecological data that hinder our ability to extract meaningful patterns using conventional tools. Recent work on implementing modern statistical methods for analysis of such ecological data has focused primarily on population dynamics but other types of data, such as animal movement pathways obtained from satellite telemetry, can also benefit from the application of modern statistical tools. 2. We develop a robust hierarchical state-space approach for analysis of multiple satellite telemetry pathways obtained via the Argos system. State-space models are time-series methods that allow unobserved states and biological parameters to be estimated from data observed with error. We show that the approach can reveal important patterns in complex, noisy data where conventional methods cannot. 3. Using the largest Atlantic satellite telemetry data set for critically endangered leatherback turtles, we show that the diel pattern in travel rates of these turtles changes over different phases of their migratory cycle. While foraging in northern waters the turtles show similar travel rates during day and night, but on their southward migration to tropical waters travel rates are markedly faster during the day. These patterns are generally consistent with diving data, and may be related to changes in foraging behaviour. Interestingly, individuals that migrate southward to breed generally show higher daytime travel rates than individuals that migrate southward in a non-breeding year. 4. Our approach is extremely flexible and can be applied to many ecological analyses that use complex, sequential data.     

Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean

Fisheries bycatch is a critical source of mortality for rapidly declining populations of leatherback turtles, Dermochelys coriacea. We integrated use-intensity distributions for 135 satellite-tracked adult turtles with longline fishing effort to estimate predicted bycatch risk over space and time in the Pacific Ocean. Areas of predicted bycatch risk did not overlap for eastern and western Pacific nesting populations, warranting their consideration as distinct management units with respect to fisheries bycatch. For western Pacific nesting populations, we identified several areas of high risk in the north and central Pacific, but greatest risk was adjacent to primary nesting beaches in tropical seas of Indo-Pacific islands, largely confined to several exclusive economic zones under the jurisdiction of national authorities. For eastern Pacific nesting populations, we identified moderate risk associated with migrations to nesting beaches, but the greatest risk was in the South Pacific Gyre, a broad pelagic zone outside national waters where management is currently lacking and may prove difficult to implement. Efforts should focus on these predicted hotspots to develop more targeted management approaches to alleviate leatherback bycatch.     

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 Ni?o Southern Oscillation (ENSO). Drier and warmer conditions associated with El Ni?o 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.