Behavioral inference of diving metabolic rate in free-ranging leatherback turtles

Good estimates of metabolic rate in free‐ranging animals are essential for understanding behavior, distribution, and abundance. For the critically endangered leatherback turtle (Dermochelys coriacea), one of the world’s largest reptiles, there has been a long‐standing debate over whether this species demonstrates any metabolic endothermy. In short, do leatherbacks have a purely ectothermic reptilian metabolic rate or one that is elevated as a result of regional endothermy? Recent measurements have provided the first estimates of field metabolic rate (FMR) in leatherback turtles using doubly labeled water; however, the technique is prohibitively expensive and logistically difficult and produces estimates that are highly variable across individuals in this species. We therefore examined dive duration and depth data collected for nine free‐swimming leatherback turtles over long periods (up to 431 d) to infer aerobic dive limits (ADLs) based on the asymptotic increase in maximum dive duration with depth. From this index of ADL and the known mass‐specific oxygen storage capacity (To2) of leatherbacks, we inferred diving metabolic rate (DMR) as . We predicted that if leatherbacks conform to the purely ectothermic reptilian model of oxygen consumption, these inferred estimates of DMR should fall between predicted and measured values of reptilian resting and field metabolic rates, as well as being substantially lower than the FMR predicted for an endotherm of equivalent mass. Indeed, our behaviorally derived DMR estimates ( mL O2 min−1 kg−1) were times the resting metabolic rate measured in unrestrained leatherbacks and times the average FMR for a reptile of equivalent mass. These DMRs were also nearly one order of magnitude lower than the FMR predicted for an endotherm of equivalent mass. Thus, our findings lend support to the notion that diving leatherback turtles are indeed ectothermic and do not demonstrate elevated metabolic rates that might be expected due to regional endothermy. Their capacity to have a warm body core even in cold water therefore seems to derive from their large size, heat exchangers, thermal inertia, and insulating fat layers and not from an elevated metabolic rate.

Genetic composition of the Ascension Island green turtle rookery based on mitochondrial DNA : implications for sampling and diversity

In species of conservation concern it is often difficult to be certain that population diversity and structure have been adequately characterised by genetic sampling. Since practical and financial constraints tend to be associated with increasing sample sizes in many conservation genetic studies, it is important to consider the potential for sampling error and bias due to inadequate samples or spatio-temporal structure within populations. We analysed sequence data from the mitochondrial DNA control region in a large sample (n = 245) of green sea turtles Chelonia mydas collected at the globally important rookery of Ascension Island, South Atlantic. We examined genetic diversity and structure among 10 sampling sites, 4 beach clusters and 4 nesting seasons, and evaluated the genetic composition of Ascension against other Atlantic nesting populations, including the well-studied rookery at Tortuguero (Costa Rica). Finally, we used rarefaction and GENESAMP analyses to assess the ability of different sample sizes to provide acceptable genetic representations of a population, using Ascension and Tortuguero as models. On Ascension, we found 13 haplotypes, of which only 3 had been previously observed in the rookery, and 5 previously undescribed. We detected no differentiation among beach clusters or sampling seasons, and only weak differentiation among the 3 primary nesting sites. The increased sample size for Ascension provided higher resolution and statistical power in describing genetic structure among all other known Atlantic rookeries. Our extrapolations showed that a maximum of 18 and 6 haplotypes are expected to occur in Ascension and Tortuguero, respectively, and that current sample sizes are sufficient to describe most of the variation. We recommend using rarefaction and GENESAMP analyses on a rookery-by-rookery basis to evaluate whether a sample set adequately describes mitochondrial DNA diversity, thus strengthening subsequent phylogeographic and mixed stock analyses, and management recommendations for conservation.

Vertical movements of North Sea Cod

Various air-breathing marine vertebrates such as seals, turtles and seabirds show distinct patterns of diving behaviour. For fish, the distinction between different vertical behaviours is often less clear-cut, as there are no surface intervals to differentiate between dives. Using data from acoustic tags (n = 23) and archival depth recorders attached to cod Gadus morhua (n = 92) in the southern North Sea, we developed a quantitative method of classifying vertical movements in order to facilitate an objective comparison of the behaviour of different individuals. This method expands the utilisation of data from data storage tags, with the potential for a better understanding of fish behaviour and enhanced individual based behaviour for improved ecosystem modelling. We found that cod were closely associated with the seabed for 90% of the time, although they showed distinct seasonal and spatial patterns in behaviour. For example, cod tagged in the southern North Sea exhibited high rates of vertical movement in spring and autumn that were probably associated with migration, while the vertical movements of resident cod in other areas were much less extensive and were probably related to foraging or spawning behaviours. The full reasons underlying spatial and temporal behavioural plasticity by cod in the North Sea warrant further investigation.

Satellite tracking reveals unusual diving characteristics for a marine reptile, the olive ridley turtle : Lepidochelys olivacea

The movements, diving behaviour and thermal environment occupied by 4 adult female olive ridley turtles Lepidochelys olivacea in northern Australia were determined through satellite telemetry. Patterns of behaviour recorded were rather unusual compared to other sea turtles in that dives were mainly deep, largely benthic and exceptionally long (>2 h) in some cases, characteristics typical of over-wintering turtles in colder environments. One individual occupied shallow coastal foraging zones, while the others foraged far from land (probably on the seabed) in relatively deep water (>100 m). Individuals performed long dives (frequently >100 min), but from the short post-dive intervals we suggest that these dives were mainly aerobic. Maximum dive depth recorded was 200 ± 20 m (mean maximum depths ranged from 20.1 to 46.7 m across individuals; n = 17328 dives in total; depths ≥3 m were considered ‘dives’) and the maximum duration was 200 ± 20 min (mean durations ranged from 24.5 to 48.0 min across individuals). Temperature profiles indicate that turtles experienced temperatures ranging from 23 to 29°C at the surface, with the lowest temperature recorded (18.7°C) at a depth of 98 m. Only 6.9% of the dives were in water <20°C. From time-allocation at depth (TAD) scores, we demonstrated that many dives reaching the known or inferred sea bottom were U-shaped, but there was no apparent diel signal in dive depth. This suggests that many benthic dives were not associated exclusively with resting behaviour and likely had a foraging component as well. The ability to perform long benthic dives allows this species to exploit deeper benthic environments in addition to the shallow coastal areas more generally occupied by adult hard-shelled sea turtles (e.g. green and hawksbill turtles). Deep benthic dives also occur in certain marine mammals (e.g. narwhals) and sea birds (e.g. rockhopper penguins) and therefore seem to be a general foraging strategy exploited by animals that can perform long dives.

Do leatherback turtles Dermochelys coriacea forage during the breeding season? A combination of data-logging devices provide new insights

Animals which undertake migrations from foraging grounds to suitable breeding areas must adopt strategies in these new conditions in order to minimise the rate at which body condition deteriorates (which will occur due to oogenesis or provisioning for young). For some animals this involves continuing foraging, whereas for others the optimal strategy is to fast during the breeding season. The leatherback turtle undertakes long-distance migrations from temperate zones to tropical breeding areas, and in some of these areas it has been shown to exhibit diving behaviour indicative of foraging. We used conventional time–depth recorders and a single novel mouth-opening sensor to investigate the foraging behaviour of leatherback turtles in the southern Caribbean. Diving behaviour suggested attempted foraging on vertically migrating prey with significantly more diving to a more consistent depth occurring during the night. No obvious prey manipulation was detected by the mouth sensor, but rhythmic mouth opening did occur during specific phases of dives, suggesting that the turtle was relying on gustatory cues to sense its immediate environment. Patterns of diving in conjunction with these mouth-opening activities imply that leatherbacks are attempting to forage during the breeding season and that gustatory cues are important to leatherbacks.

A review of migratory behaviour of sea turtles off southeastern Africa

The survival of sea turtles is threatened by modern fishing methods, exploitation of eggs and habitat destruction. Forming keystone species in the ocean, their extinction would disrupt the marine food chain in ways as yet unknown. The Indian Ocean has many breeding areas for sea turtles, the southernmost ones being on the Maputaland coast of KwaZulu-Natal, where loggerhead and leatherback turtles nest in large numbers thanks to long-lasting protection programmes. For the leatherback this is the only known nesting site in the entire western Indian Ocean. At the end of the reproductive season, both loggerheads and leatherbacks undertake migrations towards disparate feeding areas. To contribute to their conservation, the migratory behaviour of these animals needs to be understood. Here we review 10 years studying this behaviour using transmitters that telemeter data via satellite. It emerges that these species frequent widely dispersed areas ranging from the Atlantic Ocean to the Mozambique Channel. The migratory behaviour of leatherback and loggerhead turtles is, however, very different, probably due to their differing food requirements. While loggerhead postnesting movements have a truly migratory nature, the large-scale wanderings of leatherbacks are better described as prolonged sojourns in extended feeding areas.

Flexible foraging movements of Leatherback turtles across the North Atlantic Ocean

Some marine species have been shown to target foraging at particular hotspots of high prey abundance. However, we show here that in the year after a nesting season, female leatherback turtles (Dermochelys coriacea) in the Atlantic generally spend relatively little time in fixed hotspots, especially those with a surface signature revealed in satellite imagery, but rather tend to have a pattern of near continuous traveling. Associated with this traveling, distinct changes in dive behavior indicate that turtles constantly fine tune their foraging behavior and diel activity patterns in association with local conditions. Switches between nocturnal vs. diurnal activity are rare in the animal kingdom but may be essential for survival on a diet of gelatinous zooplankton where patches of high prey availability are rare. These results indicate that in their first year after nesting, leatherback turtles do not fit the general model of migration where responses to resources are suppressed during transit. However, their behavior may be different in their sabbatical years away from nesting beaches. Our results highlight the importance of whole-ocean fishing gear regulations to minimize turtle bycatch.

Genetic patterns in recovered specimens of Caretta caretta from the Adriatic Sea

The Adriatic Sea is considered a feeding and developmental area for Mediterranean loggerhead turtles, but this area is severely threatened by human impacts. In the Adriatic Sea loggerhead turtles are often found stranded or floating, but they are also recovered as by-catch from fishing activities. Nevertheless, information about population structuring and origin of individuals found in the Adriatic Sea are still limited. Cooperation with fishermen and a good network of voluntary collaborators are essential for understanding their distribution, ecology and for developing conservation strategies in the Adriatic Sea. In this study, a comparative analysis of biometric data and DNA sequence polymorphism of the long fragment of the mitochondrial control region was carried out on ninety-three loggerheads recovered from three feeding areas in the Adriatic Sea: North-western, North-eastern and South Adriatic. Differences in turtles body sizes (e.g. Straight Carapace Length) among the three recovery areas and relationship between SCL and the type of recovery were investigated. The origin of turtles from Mediterranean rookeries and the use of the Adriatic feeding habitats by loggerheads in different life-stages were assessed to understand the migratory pathway of the species. The analysis of biometric data revealed a significant difference in turtle sizes between the Southern and the Northern Adriatic. Moreover, size of captured turtles resulted significantly different from the size of stranded and floating individuals. Actually, neritic sub-adults and adults are more affected by incidental captures than juveniles because of their feeding behavior. The Bayesian mixed-stock analysis showed a strong genetic relationship between the Adriatic aggregates and Mediterranean rookeries, while a low pro¬portion of individuals of Atlantic origin were detected in the Adriatic feeding grounds. The presence of migratory pathways towards the Adriatic Sea due to the surface current system was reinforced by the finding of individuals bearing haplotypes endemic to the nesting populations of Libya, Greece and Israel. A relatively high contribution from Turkey and Cyprus to the Northwest and South Adriatic populations was identified when the three sampled areas were analyzed independently. These results have to be taken in account in a conservative perspective, since coastal hazards, affecting the population of turtles feeding in the Adriatic Sea may also affect the nesting populations of the Eastern Mediterranean with a unique genetic pattern.

Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian Archipelago

The somatic growth dynamics of green turtles ( Chelonia mydas) resident in five separate foraging grounds within the Hawaiian Archipelago were assessed using a robust non-parametric regression modelling approach. The foraging grounds range from coral reef habitats at the north-western end of the archipelago, to coastal habitats around the main islands at the southeastern end of the archipelago. Pelagic juveniles recruit to these neritic foraging grounds from ca. 35 cm SCL or 5 kg ( similar to 6 years of age), but grow at foraging-ground-specific rates, which results in quite different size- and age-specific growth rate functions. Growth rates were estimated for the five populations as change in straight carapace length ( cm SCL year) 1) and, for two of the populations, also as change in body mass ( kg year) 1). Expected growth rates varied from ca. 0 - 2.5 cm SCL year) 1, depending on the foraging-ground population, which is indicative of slow growth and decades to sexual maturity, since expected size of first-time nesters is greater than or equal to 80 cm SCL. The expected size- specific growth rate functions for four populations sampled in the southeastern archipelago displayed a non-monotonic function, with an immature growth spurt at ca. 50 - 53 cm SCL ( similar to 18 - 23 kg) or ca. 13 - 19 years of age. The growth spurt for the Midway atoll population in the northwestern archipelago occurs at a much larger size ( ca. 65 cm SCL or 36 kg), because of slower immature growth rates that might be due to a limited food stock and cooler sea surface temperature. Expected age-at-maturity was estimated to be ca. 35 - 40 years for the four populations sampled at the south-eastern end of the archipelago, but it might well be > 50 years for the Midway population. The Hawaiian stock comprises mainly the same mtDNA haplotype, with no differences in mtDNA stock composition between foraging-ground populations, so that the geographic variability in somatic growth rates within the archipelago is more likely due to local environmental factors rather than genetic factors. Significant temporal variability was also evident, with expected growth rates declining over the last 10 - 20 years, while green turtle abundance within the archipelago has increased significantly since the mid-1970s. This inverse relationship between somatic growth rates and population abundance suggests a density-dependent effect on somatic growth dynamics that has also been reported recently for a Caribbean green turtle stock. The Hawaiian green turtle stock is characterised by slow growth rates displaying significant spatial and temporal variation and an immature growth spurt. This is consistent with similar findings for a Great Barrier Reef green turtle stock that also comprises many foraging-ground populations spanning a wide geographic range.

Modelling the effect of fibropapilloma disease on the somatic growth dynamics of Hawaiian green sea turtles

The effect of the tumour-forming disease, fibropapillomatosis, on the somatic growth dynamics of green turtles resident in the Pala'au foraging grounds (Moloka'i, Hawai'i) was evaluated using a Bayesian generalised additive mixed modelling approach. This regression model enabled us to account for fixed effects (fibropapilloma tumour severity), nonlinear covariate functional form (carapace size, sampling year) as well as random effects due to individual heterogeneity and correlation between repeated growth measurements on some turtles. Somatic growth rates were found to be nonlinear functions of carapace size and sampling year but were not a function of low-to-moderate tumour severity. On the other hand, growth rates were significantly lower for turtles with advanced fibropapillomatosis, which suggests a limited or threshold-specific disease effect. However, tumour severity was an increasing function of carapace size-larger turtles tended to have higher tumour severity scores, presumably due to longer exposure of larger (older) turtles to the factors that cause the disease. Hence turtles with advanced fibropapillomatosis tended to be the larger turtles, which confounds size and tumour severity in this study. But somatic growth rates for the Pala'au population have also declined since the mid-1980s (sampling year effect) while disease prevalence and severity increased from the mid-1980s before levelling off by the mid-1990s. It is unlikely that this decline was related to the increasing tumour severity because growth rates have also declined over the last 10-20 years for other green turtle populations resident in Hawaiian waters that have low or no disease prevalence. The declining somatic growth rate trends evident in the Hawaiian stock are more likely a density-dependent effect caused by a dramatic increase in abundance by this once-seriously-depleted stock since the mid-1980s. So despite increasing fibropapillomatosis risk over the last 20 years, only a limited effect on somatic growth dynamics was apparent and the Hawaiian green turtle stock continues to increase in abundance.

Response of heart rate and cloacal ventilation in the bimodally respiring freshwater turtle, Rheodytes leukops to experimental changes in aquatic PO2

Changes in heart rate (f(H)) and cloacal ventilation frequency (f(C)) were investigated in the Fitzroy turtle, Rheodytes leukops, under normoxic (17.85 kPa) and hypoxic (3.79 kPa) conditions at 25 degrees C. Given R. leukops' high reliance on aquatic respiration via the cloacal bursae, the objective Of this Study was to examine the effect of varying aquatic PO2 levels upon the expression of a bradycardia in a freely diving, bimodally respiring turtle. In normoxia, mean diving f(H) and f(C) for R. leukops remained constant with increasing submergence length, indicating that a bradycardia failed to develop during extended dives of up to 3 days. Alternatively, exposure to aquatic hypoxia resulted in the expression of a bradycardia as recorded by a decreasing mean diving f(H) with increasing dive duration. The observed bradycardia is attributed to a hypoxic-induced metabolic depression, possibly facilitated by a concurrent decrease in f(C). Results suggest that R. leukops alters its strategy from aquatic O-2 extraction via cloacal respiration in normoxia to O-2 conservation when exposed to aquatic hypoxia for the purpose of extending dive duration. Upon surfacing, a significant tachycardia was observed for R. leukops regardless of aquatic PO2, presumably functioning to rapidly equilibrate blood and tissue gas tensions with alveolar gas to reduce surfacing duration.

A bloom of Lyngbya majuscula in Shoalwater Bay, Queensland, Australia: An important feeding ground for the green turtle (Chelonia mydas)

Lyngbya majuscula, a toxic cyanobacterium, was observed blooming during June-July (winter) 2002 in Shoalwater Bay, Queensland, Australia, an important feeding area for a large population of green turtles (Chelonia mydas). The bloom was mapped and extensive mats of L majuscula were observed overgrowing seagrass beds along at least 18 km of coast, and covering a surface area of more than I I km(2). Higher than average rainfall preceded the bloom and high water temperatures in the preceding summer may have contributed to the bloom. In bloom samples, lyngbyatoxin A (LA) was found to be present in low concentration (26 mu g kg(-1) (dry weight)), but debromoaplysiatoxin (DAT) was not detected. The diet of 46 green turtles was assessed during the bloom and L. majuscula was found in 51% of the samples, however, overall it contributed only 2% of the animals' diets. L. majuscula contribution to turtle diet was found to increase as the availability of the cyanobacterium increased. The bloom appeared to have no immediate impact on turtle body condition, however, the presence of a greater proportion of damaged seagrass leaves in diet in conjunction with decreases in plasma concentrations of sodium and glucose could suggest that the turtles may have been exposed to a Substandard diet as a result of the bloom. This is the first confirmed report of L. majuscula blooming in winter in Shoalwater Bay, Queensland, Australia and demonstrates that turtles consume the toxic cyanobacterium in the wild, and that they are potentially exposed to tumour promoting compounds produced by this organism. (c) 2005 Elsevier B.V. All rights reserved.

The international importance of the archipelago of Cape Verde for marine turtles, in particular the loggerhead turtle Caretta caretta

[ES] The shores of Cape Verde hosts one of the most important nesting populations of the loggerhead turtle Caretta caretta in the world, as well as important feeding grounds for hawksbill Eretmochelys imbricata and green turtles Chelonia mydas. In the past few years, a number of scientific studies have demonstrated the relevance of the waters and beaches of this archipelago for the conservation of these endangered marine megavertebrates. This article aims to bring together the most relevant scientific information published on the subject so far. In addition, we will provide an overview of the current situation of sea turtles in Cape Verde, their conservation status and their importance in an international context.

Male hatchling production in sea turtles from one of the world's largest marine protected areas, the Chagos Archipelago

Sand temperatures at nest depths and implications for hatchling sex ratios of hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) nesting in the Chagos Archipelago, Indian Ocean are reported and compared to similar measurements at rookeries in the Atlantic and Caribbean. During 2012-2014, temperature loggers were buried at depths and in beach zones representative of turtle nesting sites. Data collected for 12,546 days revealed seasonal and spatial patterns of sand temperature. Depth effects were minimal, perhaps modulated by shade from vegetation. Coolest and warmest temperatures were recorded in the sites heavily shaded in vegetation during the austral winter and in sites partially shaded in vegetation during summer respectively. Overall, sand temperatures were relatively cool during the nesting seasons of both species which would likely produce fairly balanced hatchling sex ratios of 53% and 63% male hatchlings, respectively, for hawksbill and green turtles. This result contrasts with the predominantly high female skew reported for offspring at most rookeries around the globe and highlights how local beach characteristics can drive incubation temperatures. Our evidence suggests that sites characterized by heavy shade associated with intact natural vegetation are likely to provide conditions suitable for male hatchling production in a warming world.