Reproductive phenology of Dermochelys coriacea, Lepidochelys olivacea and Chelonia mydas in Suriname and French Guiana

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1 Università degli Studi di Padova Facoltà di Scienze MM.FF.NN. Laurea Magistrale in Biologia Evoluzionistica Reproductive phenology of Dermochelys coriacea, Lepidochelys olivacea and Chelonia mydas in Suriname and French Guiana Relatori: Marc Girondot, Université de Paris Sud XI, Laboratoire d'ecologie, Systématique et Evolution Lorenzo Zane, Università degli Studi di Padova, Dipartimento di Biologia A.Vallisneri Laureanda: Anna Rizzo Anno Accademico: 2010/2011

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3 Table of contents INTRODUCTION... 5 SEA TURTLES... 5 EVOLUTION AND PHYLOGENY... 5 BIOLOGY OF SEA TURTLES... 7 DISTRIBUTION AND LIFE HISTORY CONSERVATION AND THREATS FRENCH GUIANA AND SURINAME ROOKERY SEA TURTLE SPECIES NESTING IN FRENCH GUIANA AND SURINAME STATISTICAL METHODS FOR POPULATIONS ESTIMATION MARINE TURTLES AT CLIMATE CHANGE TIMING OF REPRODUCTION AIMS OF THE RESEARCH MATERIALS AND METHODS NESTING COUNTS DATA COLLECTION GIRONDOT 2010 NESTING SEASON MODEL SEASON PARAMETERS ESTIMATION DESCRIBING THE SOFTWARE NESTING COUNTS ANALYSIS BUILDING DATABASE NESTING SEASON FIT PHENOLOGY ANALYSIS SEA SURFACE TEMPERATURES (SST) NORTH ATLANTIC OSCILLATION (NAO) GENERAL LINEAR MODEL (GLM) IMPLEMENTATION IMPROVING THE MODEL PARAMETERS OPTIMIZATION RESULTS NESTING COUNTS ANALYSIS NESTING TRENDS PHENOLOGY ANALYSIS CLIMATE FACTORS DATA (SST, NAO) GLM MODELS IMPROVING THE MODEL DISCUSSION TURTLE NESTING PHENOLOGY AT GLOBAL WARMING INTRASEASONAL NESTING PERIODICITIES SUMMARY (ITALIANO) BIBLIOGRAPHY

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5 Sea turtles Evolution and Phylogeny Introduction Turtles (Class Reptilia, order Testudines) made their first appearance on fossil record some 200 million years ago, during the lower Jurassic, while fully marine forms were thought to have made their first appearance by 150 million years ago (Bowen et al. 1993b). A new first fossil sea turtle record, dating back to 220- million- years ago was reported from south western China in 2008 (Alroy et al. 2008), but it does not belong to the radiation leading to current species. The oldest fossil of this sea turtle radiation dates back to 110 million years, to the early Cretaceous (Hirayama 1998). The seven species of sea turtles present nowadays, representing the two families of Cheloniidae and Dermochelyidae grouped into the superfamily Chelonioidea, are the only living members from the marine radiation of the suborder Cryptodira, and constitute a monophyletic group. The extent Dermochelyidae only contains the leatherback turtle, Dermochelys coriacea, while Cheloniidae includes six species classified into five genera: the loggerhead (Caretta caretta), olive ridley (Lepidochelys olivacea), Kemp s ridley (Lepidochelys kempii) and hawksbill (Eretmochelys imbricata) turtle, constituting the tribe Carettini; green (Chelonia mydas) and flatback (Natator depressus) turtle, the tribe Chelonini. The existence of an eighth species, the black turtle or East Pacific green turtle (Chelonia agassizii), has been a matter of debate due to conflicting morphometric and genetic data. It is now generally accepted to be a population or a subspecies of Chelonia mydas. The phylogeny of the group rests on morphological features, fossil evidence and molecular data. Elderly molecular analysis were principally based on cytochrome b (Bowen et al. 1993b) and control region mitochondrial DNA, and ND4- LEU trna (Dutton 1995). Recently, given the recognized problems in relying solely on mtdna, both mitochondrial genes (12S and 16S) and nuclear DNA markers (BDNF, Cmos, R35, Rag1, Rag2), as well as microsatellite loci, were taken into account (Naro- Maciel et al. 2008). Hence, perspectives on several other conflicting hypotheses over general and tribal affinities, as well as species boundaries, have been given new evidence. Among them, the widely recognized distant position of Dermochelys coriacea relative to all other species, the sister- taxon relationship between flatback and green turtle, and the close affiliation between ridleys (Lepidochelys genus) and the loggerhead turtle. Regarding species boundaries, there is general agreement about grouping L. kempi and L. olivacea as a sister group, while paraphyly of the green turtle seems to be more questionable. Actually, a deep split between Atlantic and Pacific green turtle does exist, with a divergence estimated to have started about 7 million years ago, predating other vicariant events such as the formation of the Isthmus of Panama (3-3,5 mya), and following the closure of the Tethys Sea (14-5

6 18 mya), an event preventing the mixing between many tropical marine species of the Atlantic and Indo- Pacific. Moreover, the cooling of southern ocean temperatures from the mid to late Miocene (from mya to about 6 mya) could have been at the origin of a split due to cold waters blocking dispersal via southern routes at the tips of South America and South Africa. However, as microsatellite and mtdna phylogeographic studies support evidence for recent linkages between green turtles from the Atlantic, Indian, and Pacific, it is generally accepted that limited gene flows prevents Atlantic and Pacific Green turtles lineages from being considered separated species (Naro- Maciel et al. 2008). Hence, general agreement has been reached about considering black turtle as a melanistic form of C. mydas, separated only at a population level in the Pacific (Dutton 1995). A summary of phylogenetic relationships among sea turtle species is shown in Figure 1. Figure 1. Phylogenetic relationships among sea turtle species (Naro- Maciel et al. 2008). 6

7 Biology of sea turtles Figure 2. Sea turtle skeleton. Source: seaturtle.com. Like other Cryptodira, sea turtles are characterized by a peculiar closure of their jaws, obtained by contracting muscles over a cartilage on the otic chamber. Moreover, the head is retracted in a vertical plane and assumes an S- shape between the shoulder girdles (Meylan and Meylan 1999). Compared with other Cryptodira, living sea turtles have a reduced ability to retract their head in the carapace, but they are conferred additional protection by a thick and nearly complete skull roofing. Sea turtles have horny keratin beaks, highly variable shaped among species due to specific food habits: inward pointed in hawksbill, adapted to beat off pieces of sponges; serrated in green turtle, to cut sea grass; sharp both on bottom and top for leatherback, to successfully slice jellyfish; large and thick in loggerhead and ridleys, to break hard shells like the ones of clams and crabs; generalized for flatback, to feed on both soft and hard shelled animals. Marine turtles are considered highly derived morphologically, and developed several adaptations for sea life, common to all species. In comparison with other turtles, their carapace presents a reduced amount of bone, probably an adaptation to gain flexibility when subjected to high water pressure (Spotila 2004). Secondly, the paddle- shaped limbs, in which all movable articulations between the distal bony elements are lost and three or four digits of the hand are markedly elongated. An enlarged shoulder girdle with a markedly elongated coracoid serves as attachment site for the well- developed pectoral muscles that are used for swimming. They are also streamlined to various degrees, which improves their hydrodynamic efficiency. Turtles use their flipper- like limbs simultaneously sweeping front limbs through the water, with a movement quite similar to the one of birds wings. The front flippers move up and out and then 7

8 down and in together in a power stroke that provides propulsion forward and up or down depending upon how the flippers are oriented. The turtles glide forward by momentum as they start to move their flippers, and turn by changing the amount of sweep of one of the front flippers and by rudder- like actions by the hind flippers. Sea turtles are deep divers, and hence they evolved a physiology more similar to the ones of living mammals than other reptiles. A typical sea turtle spends 95 per cent of its time underwater and not more than one hour a day, cumulatively, at the surface. It normally spends minutes at a time underwater searching for food, but it can resist without breathing up to 45 minutes. Sea turtles can reach quite deep dive, with leatherbacks retaining the primate, reaching up to 1250 m depth (Houghton 2008). Sea turtles can quickly empty and refill their lungs with just one or few breaths, because their air passages are reinforced with cartilage and surrounded by smooth muscles. During deep dives their lungs collapse and the blood flow to them is restricted; air is left just in the air passages, where there are no blood vessels. Another adaptation to marine life is the presence of wide salt glands behind each eye. These are lacrimal glands remarkably enlarged and modified in order to remove excess salt from body fluids. They both produce a thick, clear, salty mucous which lubrificates the eye during nesting process on land and excrete excess salt. Moreover, sea turtles esophagus is adapted to eliminate salt water ingested with food, by expelling the excess water out of the mouth with muscular contraction. There has been much debate on whether marine turtles were hot or cold- blooded. Actually turtles, particularly leatherbacks, can withstand quite cold water temperatures. Recently it was suggested that they could be homeotherms, due to the difference between their internal temperature and that of the water, which ranges from the 1,2 4,3 C of tropical seas up to the 8,2 C of northern Atlantic waters (James and Mrosovsky 2004, Southwood et al. 2008). Currently, recent observations have shown that turtles rely on heat generated by their diving activity, retained by their thick shell with a layer of fat, with still a low metabolic rate (Bostrom et al. 2010). This partial endothermy seems to increase with the size, along with increasing body volume vs body surface ratio. This pattern would explain quite well some peculiar turtle habits, like basking on the water surface for a long time with the carapace exposed to the sun, in order to gain warmth. Moreover, turtles of northern latitudes, as the winter occurs, are often affected by what is called cold stunning : when temperatures fall to about 7-10 C, they get too cold to swim and dive, and just float on the surface. Sea turtles are oviparous reptiles. They are iteroparous, nesting on land more than once during the reproductive season, often not in consecutive years. The male developed a longer tail in which the penis is located and is inserted into female s cloaca during copulation. Females are receptive to mating only during the month before the nesting season and the twelve hours after laying their clutch of eggs. Egg maturation, and hence duration of interesting period, is highly influenced by temperature 8

9 (Sato et al. 1998, Hays et al. 2002). Sex of the offspring is determined by temperature during the middle third of embryo development (Yntema and Mrosovsky 1982, Desvages et al. 1993). Pivotal temperature defined as theoretical temperature that produces 50% of each sex - is highly variable, on both a species- specific and population- specific basin, and ranges from 28.2 and 30.5 C (Mrosovsky 1994, Chevalier et al. 1999, Godfrey and Mrosovsky 2006). 9

10 Distribution and life history Sea turtles are observed on most ocean basins, from the northern and southern limits of the Atlantic, Indian and Pacific oceans to the Tropics and into the Mediterranean Sea. While leatherbacks seem to be the most northern spread, foraging into colder and even polar waters, hawksbills are known as the most tropical ones. All the species are cosmopolitan in their distribution, except for Kemp s ridley and flatback turtles. While the former is limited to the waters between the Gulf of Mexico and the eastern United States coast, with some individuals occasionally extending as far as the United Kingdom coast and Western Europe, the flatback is endemic only on the Australian continental shelf. General distribution of sea turtle species is illustrated in Figure 3. Figure 3. Overall distribution of sea turtles on a global basin. Source: Defenders of wildlife, A generalized history model (Meylan and Meylan 1999) developed with data from the green turtle, and elaborated by other authors, provides a framework to define the life history of all the species of sea turtles. Although each species diverge from the model in significant ways, they share some common aspects, regarding the seasonal and ontogenetic shifts in diet and habitats, which explain much of the observed movements and migrations. After oviposition of clutches in large holes dug in sand beaches, young hatchlings emerge during night- time after a period which can last from 45 days with warmer sand temperatures to up to days for cooler ones (Spotila 2004). Upon leaving the nesting beach hatchlings begin a pelagic phase that lasts for several years, a period known as the lost years of sea turtles biology, whose duration widely varies among species and populations. The only exception to this pattern seems to be the flatback, which remains in coastal waters and lacks a pelagic phase (Hamann et al. 2011). 10

11 Figure 4. Green turtle hatchlings heading for the sea. Source: There are still great uncertainties on these early pelagic phase routes; we have a good knowledge about some species, like loggerhead, while there is little or no knowledge for others, like leatherback and ridleys. Research studies suggest that hatchlings spend the first days of their life swimming out to sea and feeding opportunistically on ctenophores and crustacean larval stages. They are often found in association with weed lines or drift lines existing near frontal boundaries of major currents. When they are far offshore, out of the reach of coastal fish and birds predators, they continue to head out into the open ocean and are carried by ocean currents to converging areas, where they find their foraging grounds, like drifting islands of sea weeds, where they feed upon a huge variety of plants, fish larvae, ctenophores, jellyfish, barnacles, crabs and shrimps, as well as insects from nearby land. After the initial lost years, most species of juvenile sea turtles move out of the open ocean and re- enter coastal waters. They occupy areas called developmental habitats where immature sea turtles commonly occur but where adults are rarely seen. They use mostly costal feeding grounds where they grow to adult size, entering and departing at predictable sizes. The juvenile turtles have a lower growth rate in respect to hatchlings, also due to less available food supply, and switch to their adult feeding habits. Loggerhead and Kemp s ridley begin to eat shellfish and crabs; green turtles turn to algae or seagrass, hawksbill to sponges and sea cucumbers, sea anemones and molluscs. Age of maturity occurs between 15 to 50 years or more, depending on the species and geographical area (Meylan and Meylan 1999, Stewart et al. 2007). Adult turtles spend most of their life inside foraging grounds. These can be fixed in space, like seagrass beds, or transitory, such as ocean areas with seasonal blooms of jellyfish or benthic invertebrates. Sexual maturity makes adults return to nesting grounds. During the reproductive season, both males and females swim up to waters surrounding nesting beaches, where they may remain up to several months. Males begin the migrations first, reaching the mating grounds and waiting for the females to appear. Figure 5. Green turtles mating, Malaysia. Source: 11

12 Mating occurs along the migratory corridor, at courtship or breeding stations, and in the proximity of a nesting beach, the longshore waters called internesting habitat. Reproductive habits of sea turtles are shared by different species. Females usually nest more than once during a single reproductive season, with one or more year internesting intervals which are specie- specific, during which turtles couple and forage (Fossette et al. 2008b, Casey et al. 2010). Others species- specific differences occur in parameters such as nesting habitat preferences, nesting strategy (aggregated or solitary), size at first reproduction, average clutch size, details of nest size and construction. Nesting behaviour, however, is highly conserved. Typically, solitary females enter nesting beaches during night time, providing any source of disturbance is absent. The only divergent reproductive behaviour is the one frequently observed in Kemp s and olive ridleys, called mass arrivals or arribadas. When an arribada occurs, huge aggregation of thousands of females gathers on the beach for nesting over a period of a few days. Nesting turtles crawl up the beach for a few minutes, until finding the right spot to dig the nest. After preparing the ground, clearing away any vegetation or debris and digging a body pit more- less of their body size, they start digging the nest with only the hind flippers. When a deep, flask- shaped hole is created, they drop the eggs. When they are all laid, the females start to cover the nest with hind flippers, and when the hole is filled, they continue to tamp down the sand till it is compact, and finally obscure the nest throwing and levelling sand on the whole area. This completed they head for the surf returning to interesting grounds. Figure 6. Leatherback turtle laying eggs in a nest. Source: All sea turtles exhibit migratory behaviour at different times of their lives, both for reproductive and foraging aims. Reproductive migrations between nesting and feeding grounds are the most known due to the facility of tagging females after the nesting effort. They extend over thousands of kilometres, from northern to southern areas. Migration routes obtained by recapture of tagged turtles as well as by satellite telemetry (Troëng et al. 2003, James et al. 2005, Hays et al. 2006, James et al. 2007, Fossette et al. 2010a, Fossette et al. 2010c ) integrated with molecular genetics permit the identification of the nesting beach origin of turtles captured at sea. 12

13 Conservation and threats It is known that several sea turtle populations are currently facing serious problems. Along with the spread and growth of human population all over the world, sea turtles have been exploited more and more. In addition, urbanisation and development of industrial economy has added new sources of damage, like pollutants and waste. As a result, some turtle populations have seen a conspicuous decline. Due to this, in fact all the seven species of marine turtles are considered at risk, and some populations are already locally extinguished. According to IUCN classification, hawksbill turtle, Kemp s ridley and leatherback turtle are considered Critically Endangered, loggerhead and green are classified as Endangered, and olive ridley is currently Vulnerable (IUCN 2011). For Kemp s ridley, data are deficient. Causes of decline are multiple, and involve both the action of local communities and the demand from populations of distant metropolis. First of all, the increased request for turtle meat and eggs, which from a limited and local use has turned into a worldwide market. Sea turtle eggs are sold both as a food source or an aphrodisiac. Individuals are taken for their meat, calipee (cartilage) and shell, considered a delicacy. But their bones and skin also become souvenirs, art objects and jewellery, boots, shoes and handbags, or oil. With mechanization of fishing techniques, indigenous people could exert a larger impact on populations. Even if now harvesting of adult and eggs is illegal in many countries, international concerted effort is still needed to mitigate legal collection and trade, including production of commercial substitutes, opinion pressure, education and enforcement (Hope 2002, Tomillo 2008 ). Another source of threat is still an indirect consequence of food demand, and consists of fishing by- catch. Shrimp trawling, gill netting and long- line fishing, often occurring on turtle gathering areas, are seriously threatening adult populations. Entangled in a net, a sea turtle is prevented Figure 8. "Underwater Sadness" by Ramon Dominguez. A sea turtle caught in a net in the Sea of Cortez, Mexico. Source: Figure 7. A poacher in Oaxaca, Mexico, takes eggs from a nesting leatherback. Source: form reaching the surface to breath and could be brought aboard alive, dying or dead. 13

14 Figure 9. Turtle Excluder Device (TED). Source: naturescrusaders.wordpress.com. Some solutions have been established to limit this threat. Turtle excluder devices, or TEDs, have been developed for shrimp trawls. They consist of trap doors that permit turtles to swim out, and have managed to reduce turtle mortality by about a half. Smaller nets and their hourly check also reduce mortality. Another solution is to limit trawl location and timing, and to establish protected marine reserves to allow population recovery (Hays et al. 2003, Pinedo 2003, Lewison 2006, Petersen 2008, Gilman 2009, Dias da Silvaa 2010, Dono 2010, Varghese 2010). Another menace is constituted by oil spills. Oil often congeals and forms tar that gathers along the ocean s convergence zones and drift lines, the same where converging of nutrients causes plankton blooms and constitutes a breeding area for hatchlings. Both adult and hatchlings are found dead with signs of oil ingestion. Analysing United States turtles washed up dead, this cause of mortality represents 6 % of cases (Spotila 2004). Also other types of contaminants, like heavy metal and chlorinated compounds, can accumulate in turtles tissue and eggs with toxic effects (Frías- Espericueta, Sakai 2000b, a, Lam 2006, Baribieri 2009, García- Fernández 2009, Guirlet et al. 2010, Jerez 2010, Páez- Osuna 2010). Plastic bags, however, easy to be mistaken for jellyfish, are the most common source of mortality, obstructing turtles oesophagus and stomach, or Figure 10. Juvenile sea turtle recovered from the oil spill occurred in Gulf of Mexico in Source: causing digestive trait disease (Barreiros and Barcelos 2001, Mrosovsky et al ). The increasing urbanisation of coastal areas, finally, represents an important risk for hatchling success. The first problem for sea turtles in developed areas is the presence of barriers, concrete or wooden seawalls, rock jetties and sandbag structures, which prevent females from crossing the beach and nesting. Beach nourishment, carried out by mechanically pumping new sand on the beach, alters temperature, gas exchange and water content. Streetlights, lamps and car headlights can also be dangerous for hatchlings, which will be disoriented and walk away from the sea towards artificial light, leading to mortality due to predators, desiccation, or exhaustion (Bourgeois et al. 2009). In conclusion, it seems evident that, in spite of their protected status, sea turtles still need concrete measures on a local, national and international scale. Human induced threats could be reduced by several means. Firstly, assessing capture and mortality rates by fisheries to reduce by- catch and control both legal 14

15 and illegal fisheries and their practices. Secondly, by reducing poaching of eggs and killing of adults, as well as reducing habitat damage and artificial light pollution. From a scientific perspective, in order to be updated with current population status, it also seems necessary to maintain beach monitoring and demographic studies, as well as expanding research into the effects of environmentally driven changes on reproductive parameters, like clutch frequency and remigration intervals, to improve the interpretation of nesting beach trends. Research should be focused mainly on survivorship of juveniles and subadults. According to Heppel (2000) they constitute one of the main factors driving population dynamics. As they reach maturity in not less than a couple of decades, juvenile mortality severely affects recovery capacity (Spotila 2004). However, huge numbers of juveniles produced and a negative density effect on their growth rate may in some case support a rapid recovery (Bjorndal et al. 2000). Life history of males, which is almost unknown, should be taken into account as well. In a long term perspective, moreover, effort should be made in order to raise awareness among the native human populations and tourists, as well as reinforcing regional cooperation between neighbouring countries (Fossette et al. 2008c). 15

16 French Guiana and Suriname rookery As sea turtles nesting habitats are constantly disappearing due to urbanisation and human presence, preservation of undisturbed natural rookeries seems to be a matter of greatest importance for the survival of sea turtle populations. Among them, the coast of French Guiana and Suriname, with their 600 km of seashore and 100 km wide continental shelf, currently represent one of the major nesting sites left for sea turtles of the western Atlantic Ocean (Girondot 2012, in press). Leatherback turtles register the most massive presence, but olive ridley and green turtles are also an important one, while hawksbill turtle and loggerhead turtle are only occasionally observed. French Guiana and Suriname are localized on the North East coast of Southern America, bordering on Guyana (W) and Brazil (S and E). Due to its low latitude (5-6 N), the area is characterised by equatorial climate, and the proximity of the Amazon river, as well as the local Maroni river (Figure 12), which highly affects coastal dynamics, dominated by large scale seashore erosion and accretion, with the disappearance and emergence of new beaches within single years. The seashore, heading in an almost NW- SE direction, consists of long sandy beaches distributed patchily among mangroves and/or coastal rainforests with extensive mudflats, which makes them an ideal landscape for sea turtles, as indicated by the large number of females nesting in the area (Figure 11). Figure 11. General map of Suriname and French Guiana, with nesting sites. Legend: number of females nesting, , (SWOT) , , > 1000, < 25, unquantified. Source: The State of the World s Sea Turtles There is no evidence for the presence of nesting leatherback sea turtles before In the sixties, large numbers of leatherbacks nesting on the beaches of French Guiana were reported. In the eighties, nesting aggregation moved to the beach close to the Yalimapo- Awala villages. That discovery opened the way to 16

17 the establishment of the Amana Natural Reserve, in 1998, which includes all the nesting beaches historically identified around Yalimapo- Awala, as well as 30 km of marine fringe. Figure 12. Aerial view of Maroni estuary. Source: In addition, in recent years increasing numbers of females are being recorded in other non- protected eastern nesting sites in French Guiana, such as Kourou and Cayenne, the capital city. These sites, however, are subjected to threats and conflict of interests with local politics, as they undergo increasing urbanisation. While in protected sites a remarkably long population monitoring has been carried out, in new urban nesting sites it is difficult to deal with such threats. The first expedition to locate sea turtles nesting sites in Suriname took place in Since 1964, nest counts have been carried out by the Nature Reserve management organisation. Wia Wia Nature Reserve was implemented in 1961, amended and enlarged in In 1969, after declaring Maronwinje beaches a sanctuary, the Galibi Nature Reserve was established. Given the periodic phenomenon of seashore modification, it is difficult to accurately assess population trends and implement adequate conservation measures. For a better understanding of these demographic processes, different types of estimates have taken place: from individual tagging, to directly studying population demographic parameters by Capture- Mark- Recapture (CMR) studies of gravid nesting females, as well as direct counting. 17

18 Sea turtle species nesting in French Guiana and Suriname Leatherback turtle, Dermochelys coriacea (Vandelli, 1761) Kingdom: Animalia Phylum: Chordata Subphylum: Vertebrata Class: Reptilia Order: Testudines Family: Dermochelyidae Genus: Dermochelys Species: Dermochelys coriacea Figure 13. Leatherback turtle swimming. Source: colareboenglish.wordpress.com. The leatherback turtle named for its shell, covered with skin is the largest turtle in the world and one of the largest living reptiles. Its mass ranges between 250 to 907 kg, and length spans from 132 to 178 cm, but can occasionally reach up to 213 cm (Spotila 2004). The leatherback has no visible hard shell. It is made up of bones buried into his dark brown or black white spotted skin (carapace), or white dark spotted skin (plastron), with about seven pronounced ridges in its back and five on the underside, which confers a hydrodynamic profile. In comparison with other species, they have remarkably elongated carapace and forelimbs. Hatchlings look mostly white on the underside and black on the back, with white margined flippers and white strips running along the length of their carapace. Their softer, leathery shell is probably an adaptation to great depths, as the leatherback is known to be the deepest of sea turtles divers, reaching up to 1230 m. During deep dives, its carapace compresses and the lung collapses to avoid nitrogen narcosis, leaving air in the respiratory passages (Fossette et al. 2010b). Figure 14. Leatherback turtle hatchling. Source: Besides being a poikilothermic animal, the leatherback has a limited capacity to maintain a constant body temperature. Its muscle tissue shows a high and fairly constant metabolic rate, which permits the turtle to maintain quite a constant temperature in the much cooler northern waters. Its wide body mass and thick layer of fat under its shell and its shoulder and neck maximizes insulation against heat loss. In addition, it has the capacity to control its blood flow to flippers, dilating and constricting its outer blood vessels. For those reasons, the leatherback is also the most widespread of all turtles: its spatial range goes from tropical waters were it migrates for nesting, to 18

19 temperate and even subarctic waters (Figure 15). It is found worldwide, in both hemispheres and all oceans with only the exception of Arctic and Antarctic waters. Occasionally individuals swim from the Indian Ocean into the Atlantic (Åkesson et al. 2003). However, genetic differences from populations around the Leatherback Sea Turtle Range world have been observed.. -=====- ===:::J'Miles 7/, 0 2,000 4,000 6,000 8,000 Note: Map represents approximate range of species. NMFS, Office of Protected Resources March 2009 Figure 15. Leatherback turtle distribution. Source: U.S. National Oceanic & Atmospheric Administration (NOAA). Leatherbacks make the longest migration, indeed, from the equatorial and subtropical latitudes of their nesting sites (Figure 16) up to the northern foraging areas. They forage from the surface down to great depths, feeding mainly on jellyfish, colonial siphonophores like Portuguese man- of- war, tunicates and other soft bodied animals. This specialized diet permit them to be the most fast growing turtles species the massive adult size is reached in just 7-13 years and to cover the high energy costs of both long distance migration and high reproductive output. Leatherbacks nest in extremely variable intervals, ranging from 1 to 6-7 years. The majority of females, however, are reported to nest every second year (70 %) and third year (25 %). The number of clutches laid per female in an entire reproductive season ranges from 1 to 9 in 9-10 days intervals, and it is positively related to previous migration duration (Fossette et al. 2008a). It can lead to as many as 14 nests per female during a season. Like other sea turtles, they have temperature sex determination, with pivotal temperature known to occur around 29 C (Bro et al. 1999). 19

20 Figure 16. Leatherback turtle worldwide rookeries. Legend: number of females nesting, < 25, , , , > 1000, unquantified. Source: The State of the World s Sea Turtles (SWOT). 20

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