Post-nesting movements and submergence patterns of loggerhead marine turtles in the Mediterranean assessed by satellite tracking

Two female loggerhead turtles (Caretta caretta) were tracked, following nesting at Alagadi Beach (35°33′N, 33°47′E), Northern Cyprus, eastern Mediterranean for 60 and 82 days, respectively. The two individuals showed marked differences in their behaviour. Individual A was tracked to Syrian coastal waters, whereas individual B travelled around the coast of Northern Cyprus to a foraging site in the waters off the east coast of Northern Cyprus. Submergence durations varied markedly during different phases of the migration, suggesting coastal foraging/resting at certain stages en route with sustained directed travelling movements during initial coastal movements and open ocean crossing. Both turtles showed fidelity to foraging grounds for the duration of transmissions (Turtle A: 36 days; Turtle B: 58 days). In both cases, locations were centred in inshore waters although the two individuals exhibited quite different submergence patterns. Individual A carried out very short dives of typical duration <10 min, whereas Individual B carried out longer dives with typical duration >20 min. Diel differences in submergence duration at the foraging grounds suggested longer dives at night/early morning for both turtles. For Turtle A, there was a general reduction in submergence duration as the period of residence increased; a pattern that may have been related to increasing temperature experienced. The total distance travelled by the two turtles (320 and 227 km) was relatively short when compared to satellite tracking studies of conspecifics following nesting in South Africa and USA and tagging studies of nesting loggerhead turtles in Greece and Australia. It is hypothesized that short migratory distance may be correlated with both the small body size and the relatively high frequency of remigration in this population.     

Fidelity and over-wintering of sea turtles

While fidelity to breeding sites is well demonstrated in marine turtles, emerging knowledge of migratory routes and key foraging sites is of limited conservation value unless levels of fidelity can be established. We tracked green (Chelonia mydas, n=10) and loggerhead (Caretta caretta, n=10) turtles during their post-nesting migration from the island of Cyprus to their foraging grounds. After intervals of 2-5 years, five of these females were recaptured at the nesting beach and tracked for a second migration. All five used highly similar migratory routes to return to the same foraging and over-wintering areas. None of the females visited other foraging habitats over the study period (units lasted on average 305 days; maximum, 1356 days), moving only to deeper waters during the winter months where they demonstrated extremely long resting dives of up to 10.2h (the longest breath-holding dive recorded for a marine vertebrate). High levels of fidelity and the relatively discrete nature of the home ranges demonstrate that protection of key migratory pathways, foraging and over-wintering sites can serve as an important tool for the future conservation of marine turtles.     

Metabolic heating in Mediterranean loggerhead sea turtle clutches

Offspring sex ratio is an important demographic parameter and, given its determination by incubation temperature in sea turtles, might be a key factor for their conservation under climate warming. An appealing approach to estimate hatchling sex ratios is to measure sand temperatures at nest depth and deduce hatchling sex ratios from a beforehand-established relationship of hatchling sex ratio and sand temperature. Such estimates will only be accurate though if metabolic heat produced by the embryos is considered. Judging whether metabolic heating has a potential effect on hatchling sex ratios without actually measuring temperature within clutches would greatly facilitate monitoring protocols. We tested for a relationship between the amount of metabolic heating and the number of developed embryos as well as clutch size in the largest known loggerhead sea turtle (Caretta caretta) population of the Mediterranean on Zakynthos (Greece). Temperatures were measured within 20 nests as well as at a reference site in the sand at nest depth. Metabolic heating was detected, but only during the last third of the incubation period did nests heat up considerably (1.6 °C on average) above the temperature of the surrounding sand. During the middle third of incubation, when sex is determined, the amount of metabolic heating was negligible. The amount of metabolic heating during the last third of the incubation duration was significantly correlated to the number of offspring developed to at least about 75% of incubation duration. This factor explained nearly 50% of variation in metabolic heating. Metabolic heating was also significantly correlated to clutch size. Given that clutch size within the Mediterranean is largest in Zakynthos loggerheads, we conclude that metabolic heating can be ignored in the estimate of hatchling sex ratios in Mediterranean loggerhead populations. These results thus provide the basis for a feasible monitoring of hatchling sex ratios in the loggerhead sea turtle in the Mediterranean.     

Responses of hatchling sea turtles to rotational displacements

After emerging from underground nests, sea turtle hatchlings migrate through the surf zone and out to the open ocean. During this migration, both waves and water currents can disrupt hatchling orientation by unpredictably rotating the turtles away from their migratory headings. In addition, waves cause turtles to roll and pitch, temporarily impeding forward swimming by forcing the hatchlings into steeply inclined positions. To maintain seaward orientation and remain upright in the water column, hatchlings must continuously compensate for such displacements. As a first step toward determining how this is achieved, we studied the responses of loggerhead (Caretta caretta L.) sea turtle hatchlings to rotational displacements involving yaw, roll, and pitch. Hatchlings responded to rotations in the horizontal plane (yaw) by extending the rear flipper on the side opposite the direction of rotation. Thus, the flipper presumably acts as a rudder to help turn the turtle back toward its original heading. Turtles responded to rotations in the roll plane with stereotypic movements of the front flippers that act to right the hatchlings with respect to gravity. Finally, hatchlings responded to rotations in the pitch plane with movements of the hind flippers that appear likely to curtail or counteract the pitching motion. Thus, the results of these experiments imply that young sea turtles emerge from their nests possessing a suite of stereotypic behavioral responses that function to counteract rotational displacements, enable the animals to maintain equilibrium, and facilitate efficient movement toward the open sea.     

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.     

The geomagnetic environment in which sea turtle eggs incubate affects subsequent magnetic navigation behaviour of hatchlings

Loggerhead sea turtle hatchlings (Caretta caretta) use regional magnetic fields as open-ocean navigational markers during trans-oceanic migrations. Little is known, however, about the ontogeny of this behaviour. As a first step towards investigating whether the magnetic environment in which hatchlings develop affects subsequent magnetic orientation behaviour, eggs deposited by nesting female loggerheads were permitted to develop in situ either in the natural ambient magnetic field or in a magnetic field distorted by magnets placed around the nest. In orientation experiments, hatchlings that developed in the normal ambient field oriented approximately south when exposed to a field that exists near the northern coast of Portugal, a direction consistent with their migratory route in the northeastern Atlantic. By contrast, hatchlings that developed in a distorted magnetic field had orientation indistinguishable from random when tested in the same north Portugal field. No differences existed between the two groups in orientation assays involving responses to orbital movements of waves or sea-finding, neither of which involves magnetic field perception. These findings, to our knowledge, demonstrate for the first time that the magnetic environment present during early development can influence the magnetic orientation behaviour of a neonatal migratory animal.     

Molecular evidence of male-biased dispersal in loggerhead turtle juveniles

Serum testosterone levels and mtDNA haplotypes were obtained from 65 juvenile loggerhead turtles (Caretta caretta, L.) incidentally caught in the central Mediterranean. The group of specimens carrying a haplotype specific for the northwest Atlantic had higher testosterone levels, and so included more males, than the other one. Since primary sex ratios of northwest Atlantic colonies are strongly skewed towards females, results indicate a male bias among Atlantic turtles entering the Mediterranean. This demonstrates for the first time a sex-biased dispersal of specimens in the pelagic phase, an important factor to be considered in conservation programs.     

Nest site fidelity and clutch frequency of loggerhead turtles are better elucidated by satellite telemetry than by nocturnal tagging efforts: Implications for stock estimation

Satellite telemetry and ground-based tagging studies are complementary methods to define the spatial and temporal patterns of nesting behavior by migratory sea turtles. Estimates of site fidelity and clutch frequencies are compared for satellite telemetry versus ground truth patrols over a 6 km stretch at a southwest Florida loggerhead (Caretta caretta) rookery. Site fidelity ranged from 1.9 km to 109.1 km for all nests deposited by a female within a season. The mean site fidelity was 28.1 km for all nests, but declined to 16.9 km if omitting the first nest. Nest frequency ranged from 2 to 8 nests per season, with a modal value of 5 nests. Satellite telemetry documented a mean nest frequency of 5.4 nests per female in comparison to 2.2 nests detected by monitoring patrols. The remigrant females had higher clutch frequency, were larger in size, and had higher site fidelity compared to newly tagged females. Satellite telemetry provided improved measurements of site fidelity and reveals a need for revised fecundity estimates. If measures of clutch frequency are representative of loggerhead assemblages nesting elsewhere within the South Florida grouping, the confidence bounds on Western Atlantic loggerhead stocks are approximately 32% lower than currently accounted for annual nesting individuals.     

The dual function of the lung in chelonian sea turtles: buoyancy control and oxygen storage

Chelonian sea turtles use their lung as a buoyancy organ and as the major oxygen store when diving, and hence, buoyancy regulation and oxygen consumption can be expected to interact. The buoyancy of seven juvenile loggerhead turtles, Caretta caretta, was determined by measuring directly their underwater weight (M_uw) while they were resting on a freely suspended weighing platform at a depth of 80 cm. Underwater weight was recorded continuously for 2 days for each turtle, followed by another 2 days measurements during which the turtles carried lead weights attached to their carapace, and finally, a last day of measurement after the weights had been removed. Total duration of resting dives (t_r), buoyancy (F_B), total resulting force acting on the resting turtle (F_res) and body volumes were derived from the M_uw data. Turtles were slightly negatively buoyant when resting (F_res=−0.2943 to −0.981 N kg⁻¹) and M_uw increased significantly throughout each apnoeic period, meaning that the turtles progressively lost buoyancy. Pulmonary gas loss was calculated from the rate at which buoyancy decreased, which was significantly slower during the first half of the dive than during the second half of the dive. Resting oxygen consumption rates (V_O2) were calculated from these data assuming that the pulmonary gas loss represents oxygen consumption from the lung. The V_O2 obtained in this way (1.69-4.86 ml O₂ min⁻¹) corresponded well with other published and V_O2 measured previously on loggerhead turtles in the same facility. Using oxygen from the lung affects buoyancy and may have impacts on the diving behaviour.     

Comparative study on the fatty acid composition of two marine vertebrates: striped dolphins and loggerhead turtles

The fatty acid composition of total lipids extracted from seven different tissues (fat, liver, cerebrum, cerebellum, lung, kidney and muscle) of 10 striped dolphins (Stenella coeruleoalba) (weight 75.7±16.2 kg) found dead or moribund during a morbillivirus epizootic, and from two tissues (fat and liver) of 54 loggerhead turtles (Caretta caretta) (18.5±10.5 kg) seized dead after illegal capture, both from the Mediterranean Sea, have been determined by high resolution chromatography techniques. When comparing both species, fatty acid composition is surprisingly similar, with a predominance of the monoenoic followed by the saturated group of fatty acids, and a very close ratio of polyunsaturates n-3/n-6. The relatively high arachidonic acid content in the liver of the two marine species is remarkable. The similar diet can play an important role in these findings, but it is suggested that probably metabolic pathways and essential fatty acid requirements between both marine vertebrates are similar, more than is expected from their earlier filogenetic evolutionary divergence.     

Natural beaches confer fitness benefits to nesting marine turtles

Coastal ecosystems provide vital linkages between aquatic and terrestrial habitats and thus support extremely high levels of biodiversity. However, coastlines also contain the highest densities of human development anywhere on the planet and are favoured destinations for tourists, creating a situation where the potential for negative effects on coastal species is extremely high. I gathered data on marine turtle reproductive output from the literature to determine whether coastal development negatively influences offspring production. Female loggerhead (Caretta caretta) and green turtles (Chelonia mydas) nesting on natural beaches (as opposed to beaches with permanent development) produce significantly more hatchling turtles per nest; all else being equal, females that successfully produce more offspring will have higher fitness than conspecifics producing fewer offspring. Thus, female marine turtles nesting on natural beaches probably have higher fitness than turtles nesting on developed beaches. Consequently, populations nesting on natural beaches may be able to recover more quickly from the historic population declines that have plagued marine turtles, and some species may recover more quickly than others.     

Establishing physiological blood parameters in the loggerhead sea turtle (Caretta caretta)

The loggerhead sea turtle (Caretta caretta), one of the three sea turtle species inhabiting the Mediterranean Sea, is an endangered species. However, although frequently treated in marine animal rescue centers, and the subject of several studies in literature, as yet, few studies have been conducted on large numbers of loggerhead sea turtles in order to establish physiological reference ranges that enable the identification of pathological values. The lack of studies on reference parameters probably depends on the fact that marine turtles treated in wildlife rescue centers are usually in a critical conditions, thus precluding the collection of data on healthy animals and compromising the reliability of any data obtained from them. The present biological study was therefore conducted in order to obtain a database from healthy animals in natural conditions. Serum biochemistry and serum protein electrophoresis were performed on blood samples obtained from 65 healthy adult loggerhead sea turtles captured and delivered to the Sea Turtle Rescue Center of Linosa (Italy); the blood samples were collected during the clinical examination of rescued animals. Laboratory analyses of serum samples were made in order to establish reference parameters, commonly required for laboratory diagnoses in mammals and diseased animals.

Tetranucleotide markers from the loggerhead sea turtle (Caretta caretta) and their cross-amplification in other marine turtle species

The loggerhead sea turtle (Caretta caretta) is a federally threatened species and listed as endangered by the World Conservation Union (IUCN). We describe primers and polymerase chain reaction (PCR) conditions to amplify 11 novel tetranucleotide microsatellite loci from the loggerhead sea turtle. We tested primers using samples from 22 females that nested at Melbourne Beach, Florida (USA). Primer pairs yielded an average of 11.2 alleles per locus (range of 4–24), an average observed heterozygosity of 0.83 (range 0.59–0.96), and an average polymorphic information content of 0.80 (range 0.62–0.94). We also demonstrate the utility of these primers, in addition to primers for 15 loci previously described, for amplifying microsatellite loci in four additional species representing the two extant marine turtle families: olive ridley (Lepidochelys olivacea), hawksbill (Eretmochelys imbricata), green turtle (Chelonia mydas), and leatherback (Dermochelys coriacea).     

Variation in reproductive output of marine turtles

Most marine turtle species are non-annual breeders and show variation in both the number of eggs laid per clutch and the number of clutches laid in a season. Large levels of inter-annual variation in the number of nesting females have been well documented in green turtle nesting populations and may be linked to environmental conditions. Other species of marine turtle exhibit less variation in nesting numbers. This inter-specific difference is thought to be linked to trophic status. To examine whether individual reproductive output is more variable in the herbivorous green turtle (Chelonia mydas Linneaeus 1758) than the carnivorous loggerhead (Caretta caretta Linneaeus 1758), we examined the nesting of both species in Cyprus over nine seasons. Green turtles showed slower annual growth rates (0.11 cm year⁻¹ curved carapace length (CCL) and 0.27 cm year⁻¹ curved carapace width (CCW)) than loggerhead turtles (0.36 cm year⁻¹ CCL, 0.51 cm year⁻¹ CCW). CCL was highly correlated to mean clutch size in both green (R²=0.51) and loggerhead turtles (R²=0.61) and maximal clutch size of green turtles (R²=0.58). Larger females did not lay a greater number of clutches or have a shorter remigration interval than smaller females of either species. On average, the size of green turtle clutches increased and that of loggerhead turtles decreased as the season progressed. Individual green turtles, however, produced more eggs per clutch through the season to a maximum in the third or fourth clutch. In loggerhead turtles, clutches 1-4 were very similar in size but the fifth clutch was 38% smaller than the first. No individuals of either species were recorded laying more than five clutches. Green turtles may not be able to achieve their maximum reproductive output with respect to clutch size throughout the season, whereas only loggerhead turtles laying five clutches (n=5) appear to become resource depleted. Green turtles nesting in years when large numbers of nests were recorded laid a greater number of clutches than females nesting in years with lower levels of nesting.     

DNA barcoding of Brazilian sea turtles (Testudines)

Five out of the seven recognized species of sea turtles (Testudines) occur on the Brazilian coast. The Barcode Initiative is an effort to undertake a molecular inventory of Earth biodiversity. Cytochrome Oxidase c subunit I (COI) molecular tags for sea turtle species have not yet been described. In this study, COI sequences for the five species of sea turtles that occur in Brazil were generated. These presented widely divergent haplotypes. All observed values were on the same range as those already described for other animal groups: the overall mean distance was 8.2%, the mean distance between families (Dermochelyidae and Cheloniidae) 11.7%, the mean intraspecific divergence 0.34%, and the mean distance within Cheloniidae 6.4%, this being 19-fold higher than the mean divergence observed within species. We obtained species-specific COI barcode tags that can be used for identifying each of the marine turtle species studied.     

Twelve new polymorphic microsatellite markers from the loggerhead sea turtle (Caretta caretta) and cross-species amplification on other marine turtle species

We describe 12 new polymorphic dinucleotide microsatellite loci and multiplex Polymerase Chain Reaction conditions from the loggerhead sea turtle Caretta caretta. Levels of polymorphism were assessed in 50 individuals from the nesting population of the Cape Verde Islands. Number of alleles ranged from 3 to 13 (average of 7.33) and the values of observed heterozygosities from 0.32 to 0.80 (average of 0.61). Cross-species amplification on three other marine turtles, Chelonia mydas, Eretmochelys imbricata and Dermochelys coriacea, revealed polymorphism and variability at eight, eleven and three loci, respectively.     

The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications

The population genetic structure of the loggerhead sea turtle (Caretta caretta) nesting in the eastern Mediterranean was assessed by sequencing a fragment of the control region of the mitochondrial DNA (n = 190) and seven microsatellites (n = 112). The two types of markers revealed genetic structuring (mtDNA: γ_st = 0.212, P < 0.001; nDNA F _st = 0.006, P < 0.001), thus indicating that both females and males are philopatric and that gene flow between populations is restricted. Mitochondrial DNA data indicate that the female populations nesting on the islands of Crete and Cyprus have suffered a recent bottleneck or colonization event. However, no bottleneck or founder effect was revealed by nuclear markers, thus indicating male-mediated gene flow from other populations that would increase nuclear genetic variability. Crete, and to a lower extent Cyprus, are thought to play a central role in such male-mediated gene flow that may reduce the negative effect of genetic drift or inbreeding on the small populations of Lebanon and Israel. This population structure indicates that assessing population relevance only on the basis of genetic variability and size would be misleading, as some populations not fulfilling those requirements may play a relevant role in genetic exchange and hence contribute to the overall genetic variability.     

Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea

Hawksbill turtles (Eretmochelys imbricata) migrate between nesting beaches and feeding habitats that are often associated with tropical reefs, but it is uncertain which nesting colonies supply which feeding habitats. To address this gap in hawksbill biology, we compile previously published and new mitochondrial DNA (mtDNA) haplotype data for 10 nesting colonies (N = 347) in the western Atlantic and compare these profiles to four feeding populations and four previously published feeding samples (N = 626). Nesting colonies differ significantly in mtDNA haplotype frequencies (Phi(ST) = 0.588, P < 0.001), corroborating earlier conclusions of nesting site fidelity and setting the stage for mixed-stock analysis. Feeding aggregations show lower but significant structure (Phi(ST) = 0.089, P < 0.001), indicating that foraging populations are not homogenous across the Caribbean Sea. Bayesian mixed-stock estimates of the origins of juveniles in foraging areas show a highly significant, but shallow, correlation with nesting population size (r = 0.378, P = 0.004), supporting the premise that larger rookeries contribute more juveniles to feeding areas. A significant correlation between the estimated contribution and geographical distance from nesting areas (r = -0.394, P = 0.003) demonstrates the influence of proximity on recruitment to feeding areas. The influence of oceanic currents is illustrated by pelagic stage juveniles stranded in Texas, which are assigned primarily (93%) to the upstream rookery in Yucatan. One juvenile had a haplotype previously identified only in the eastern Atlantic, invoking rare trans-oceanic migrations. The mixed-stock analysis demonstrates that harvests in feeding habitats will impact nesting colonies throughout the region, with the greatest detriment to nearby nesting populations.