Lost at sea: genetic, oceanographic and meteorological evidence for storm-forced dispersal

For many species, there is broad-scale dispersal of juvenile stages and/or long-distance migration of individuals and hence the processes that drive these various wide-ranging movements have important life-history consequences. Sea turtles are one of these paradigmatic long-distance travellers, with hatchlings thought to be dispersed by ocean currents and adults often shuttling between distant breeding and foraging grounds. Here, we use multi-disciplinary oceanographic, atmospheric and genetic mixed stock analyses to show that juvenile turtles are encountered ‘downstream’ at sites predicted by currents. However, in some cases, unusual occurrences of juveniles are more readily explained by storm events and we show that juvenile turtles may be displaced thousands of kilometres from their expected dispersal based on prevailing ocean currents. As such, storms may be a route by which unexpected areas are encountered by juveniles which may in turn shape adult migrations. Increased stormy weather predicted under climate change scenarios suggests an increasing role of storms in dispersal of sea turtles and other marine groups with life-stages near the ocean surface.

Detecting female precise natal philopatry in green turtles using assignment methods

It is well established that sea turtles return to natal rookeries to mate and lay their eggs, and that individual females are faithful to particular nesting sites within the rookery. Less certain is whether females are precisely returning to their natal beach. Attempts to demonstrate such precise natal philopatry with genetic data have had mixed success. Here we focused on the green turtles of three nesting sites in the Ascension Island rookery, separated by 5–15 km. Our approach differed from previous work in two key areas. First, we used male microsatellite data (five loci) reconstructed from samples collected from their offspring (N = 17) in addition to data for samples taken directly from females (N = 139). Second, we employed assignment methods in addition to the more traditional F-statistics. No significant genetic structure could be demonstrated with FST. However, when average assignment probabilities of females were examined, those for nesting populations in which they were sampled were indeed significantly higher than their probabilities for other populations (Mann–Whitney U-test: P < 0.001). Further evidence was provided by a significant result for the mAIC test (P < 0.001), supporting greater natal philopatry for females compared with males. The results suggest that female natal site fidelity was not sufficient for significant genetic differentiation among the nesting populations within the rookery, but detectable with assignment tests.

The importance of sand albedo for the thermal conditions on sea turtle nesting beaches

At Ascension Island and Cyprus, major nesting areas for green turtles (Chelonia mydas) in the Atlantic and Mediterranean, respectively, visual inspection shows some beaches are light in colour while others are darker. We objectively measured the albedo of the sand on different beaches, i.e. the percentage of the incident solar radiation that was reflected from the sand surface. At sites where albedo was recorded, we also measured the temperature of the sand at nest depths. At both rookeries, the sand temperature was markedly higher on darker beaches due to greater absorption of the incident solar radiation over the diurnal cycle. Temperature loggers buried at nest depths revealed seasonal changes in temperature on both islands, but showed that the lowest temperatures found on the darker beaches rarely dropped below the highest temperatures on the lighter beaches. Sea turtles exhibit temperature-dependent sex determination. Since sand albedo is a major avenue for the production of a range of incubation temperatures on both islands, it will also have profound implications for hatchling sex ratios. In comparison with both Ascension Island and Cyprus, for samples collected from sea turtle rookeries around the world there was an even greater range in sand albedo values. This suggests that sand albedo, a factor that has previously received little consideration, will have profound implications for nest temperatures, and hence hatchling sex ratios, for other populations and species.

Satellite telemetry suggests high levels of fishing-induced mortality in marine turtles

Long-term records of nesting numbers, or proxies to nesting numbers, show a precipitous decline in the size of many sea turtle populations. Population declines are most frequently attributed to fisheries bycatch, although direct quantification of this level of mortality is rare. We used satellite-tracking records for turtles in the Mediterranean Sea and Pacific, Atlantic and Indian Oceans to identify when turtles had been captured. Evidence for capture came from a combination of an increase in good quality locations from transmitters, transmitters moving inland to coastal towns and villages, and on-board submergence data, showing that transmitters had come out of the water. A high level of mortality was calculated, confirming current concerns regarding the outlook for sea turtles.

A review of long-distance movements by marine turtles, and the possible role of ocean currents

Sea turtle movements often occur in open-sea unsheltered areas, and are therefore likely to be influenced by major oceanographic processes. Only recently has work started to examine the possible relationships of these movements with dynamic oceanic features, and consequently a clear picture of such interaction is only available in a few cases. Newborn sea turtles are thought to rely on oceanic currents to reach their pelagic nursery habitats. The actual extent and timing of these developmental migrations are known for only a few populations, but these movements probably last several years and range over thousands of km. Large juveniles that have been tracked during their pelagic stage were found to make long-distance movements, sometimes swimming against the prevailing currents. Older juveniles of most species leave the pelagic habitat to recruit to neritic developmental habitats. This is a very poorly documented phase of the sea turtle life-cycle, and the few available indications show that turtles may have to swim actively for enormous distances to counterbalance their previous drift with the current. The course and extent of adult postnesting migrations vary greatly among different turtle species, but two main patterns are evident. Some species, like green, hawksbill and loggerhead turtles, shuttle between the nesting beach and a specific feeding area used for the entire inter-reproductive period. In these cases, individuals swim, rather than drift, to complete their journeys, with possible advection due to currents sometimes helping them to quickly reach their target, but sometimes providing navigational challenges. Other species such as the olive ridley and the leatherback turtle, leave the coastal nesting areas to reach the pelagic environment where they forage, and perform wandering movements. Major oceanographic processes (such as main currents and eddies) have been recently shown to have a remarkable influence on leatherback movements, making it questionable whether these journeys are to be considered migrations or, rather, prolonged stays in vast feeding areas.

Navigation by green turtles: which strategy do displaced adults use to find Ascension Island?

Sea turtles are known to perform long-distance, oceanic migrations between disparate feeding areas and breeding sites, some of them located on isolated oceanic islands. These migrations demonstrate impressive navigational abilities, but the sensory mechanisms used are still largely unknown. Green turtles breeding at Ascension Island perform long oceanic migrations (>2200 km) between foraging areas along the Brazilian coast and the isolated island. By performing displacement experiments of female green turtles tracked by satellite telemetry in the waters around Ascension Island we investigated which strategies most probably are used by the turtles in locating the island. In the present paper we analysed the search trajectories in relation to alternative navigation strategies including the use of global geomagnetic cues, ocean currents, celestial cues and wind. The results suggest that the turtles did not use chemical information transported with ocean currents. Neither did the results indicate that the turtles use true bi-coordinate geomagnetic navigation nor did they use indirect navigation with respect to any of the available magnetic gradients (total field intensity, horizontal field intensity, vertical field intensity, inclination and declination) or celestial cues. The female green turtles successfully locating Ascension Island seemed to use a combination of searching followed by beaconing, since they searched for sensory contact with the island until they reached positions NW and N of the Island and from there presumably used cues transported by wind to locate the island during the final stages of the search.

Habitat utilization by juvenile hawksbill turtles (Eretmochelys imbricata, Linnaeus, 1766) around a shallow water coral reef

Contemporary studies of sea turtle diving behaviour are generally based upon sophisticated techniques such as the attachment of time depth recorders. However, if the risks of misinterpretation are to be minimized, it is essential that electronic data are analysed in the light of first-hand observations. To this aim, we set out to make observations of juvenile hawksbill turtles (Eretmochelys imbricata, Linnaeus, 1766) foraging and resting in a shallow water coral reef habitat around the granitic Seychelles (4°'S, 55°'E). Data were collected from six study sites characterized by a shallow reef plateau (<5 m) and a flat sandy area at the base of the reef face (<10 m). Observation data were categorized into the following behaviours: (1) stationary foraging; (2) active foraging; (3) resting; and (4) assisted resting. Central to this investigation was the development of a technique for accurately estimating the size of sea turtles in situ based upon previously tested techniques for reef fishes. This revealed that through calibration, the curved carapace length (CCL) of marine turtles can be consistently estimated to within 10 cm of their actual size. Although rudimentary, this has advantages for assessing the residency or absence of specific life history stages from particular environments. Indeed, our data supported previous claims that following the reproductive season, adult hawksbills in the region may move away from the nesting beaches to alternative foraging grounds whilst immature turtles (following the pelagic juvenile stage) may opt to reside in areas close to their natal beaches. With regards to habitat utilization, juvenile hawksbills displayed an alternating pattern of short, shallow foraging dives followed by deeper, longer resting dives. These findings are consistent with previous electronic studies of free-range diving in this species and suggest that the maximization of resting duration may be an important factor driving this behaviour.

Change in body mass associated with long-term fasting in a marine reptile : the case of green turtles (Chelonia mydas) at Ascension Island

Female green sea turtles (Chelonia mydas) nesting at Ascension Island (7°57'S, 14°22'W) in the middle of the Atlantic Ocean had a mean body mass (post oviposition) of 166.3 kg (range 107.5–243.5 kg, n = 119). Individuals lost mass slowly during the nesting season (mean mass loss 0.22 kg·d–1, n = 14 individuals weighed more than once). Gut-content analysis and behavioural observations indicated a lack of feeding. Females of equivalent-sized pinniped species that also do not feed while reproducing (nursing pups) on islands lose mass about 17 times faster. This comparatively low rate of mass loss by green turtles probably reflects their ectothermic nature and, consequently, their low metabolic rate. We estimate that a female turtle would lose only 19% of her body mass during the 143-day, 4400-km round trip from Brazil if she did not eat, laid 3 clutches of eggs, and lost 0.22 kg·d–.

Reproductive seasonality and sexual dimorphism in green turtles

The temporal distribution of nesting and mating in green turtles Chelonia mydas at Ascension Island (7°57¹S, 14°22¹W) in the South Atlantic is described. Mathematical description of the seasonal pattern of nesting showed extreme similarity between seasons, and evidence is presented to support the hypothesis that observed patterns are driven by prevailing environmental temperature. Mating was observed to begin before nesting and follow a pattern consistent with a modelled seasonal influx of suitable females into the annual breeding population. When available data on male size are compared with that of females from the same population (n = 12 populations), a pronounced and consistent sexual dimorphism, with males being smaller than females, is highlighted in all populations. The possible mechanisms behind the evolution of such a pattern are discussed.

Changes in behaviour during the inter-nesting period and post-nesting migration for Ascension Island green turtles

Satellite transmitters were attached to green turtles Chelonia mydas while they were nesting on Ascension Island in the South Atlantic (7°57'S, 14°22'W) and individuals were subsequently monitored during the inter-nesting period and the post-nesting migration to Brazil. During the inter-nesting period, data from the transmitters suggested that turtles generally stayed within 5 km of the nesting beach on which they had originally been observed. During both the inter-nesting period and migration, turtles were submerged the vast majority (>95%) of the time, suggesting that they neither basked at the surface nor drifted passively during migration to any great extent. There was a clear dichotomy in submergence behaviour, with submergences tending to be of short duration during post-nesting migration (mean = 7.3 min, 3318 h of data from 5 individuals) and of longer duration during the inter-nesting period (mean = 22.1 min, 714 h of data from 5 different individuals). As submergence duration is generally linked to activity levels in sea turtles, this pattern suggests that turtles were comparatively inactive during the inter-nesting period and comparatively active during migration. During both the inter-nesting period and the post-nesting migration, diel submergence patterns were detected with dive duration tending to be longer at night. As the turtles migrated WSW from Ascension Island, there was a reduction in their speed of travel. A numerical model of the near-surface currents suggested that this reduction was associated with the weakening of the WSW flow of the prevailing South Atlantic Equatorial Current.

First records of dive durations for a hibernating sea turtle

The first published record, from the early 1970s, of hibernation in sea turtles is based on the reports of the indigenous Indians and fishermen from Mexico, who hunted dormant green turtles (Chelonia mydas) in the Gulf of California. However, there were no successful attempts to investigate the biology of this particular behaviour further. Hence, data such as the exact duration and energetic requirements of dormant winter submergences are lacking. We used new satellite relay data loggers to obtain the first records of up to 7 h long dives of a loggerhead turtle (Caretta caretta) overwintering in Greek waters. These represent the longest dives ever reported for a diving marine vertebrate. There is strong evidence that the dives were aerobic, because the turtle surfaced only for short intervals and before the calculated oxygen stores were depleted. This evidence suggests that the common belief that sea turtles hibernate underwater, as some freshwater turtles do, is incorrect.

Effects of rising temperature on the viability of an important sea turtle rookery

A warming world poses challenges for species with temperature-dependent sex determination, including sea turtles, for which warmer incubation temperatures produce female hatchlings. We combined in situ sand temperature measurements with air temperature records since 1850 and predicted warming scenarios from the Intergovernmental Panel on Climate Change to derive 250-year time series of incubation temperatures, hatchling sex ratios, and operational sex ratios for one of the largest sea turtles rookeries globally (Cape Verde Islands, Atlantic). We estimate that light-coloured beaches currently produce 70.10% females whereas dark-coloured beaches produce 93.46% females. Despite increasingly female skewed sex ratios, entire feminization of this population is not imminent. Rising temperatures increase the number of breeding females and hence the natural rate of population growth. Predicting climate warming impacts across hatchlings, male-female breeding ratios and nesting numbers provides a holistic approach to assessing the conservation concerns for sea turtles in a warming world. © 2014 Macmillan Publishers Limited.

Satellite tracking large numbers of individuals to infer population level dispersal and core areas for the protection of an endangered species

Aim: Tracking the dispersal patterns and habitat use of migratory species is necessary to delineate optimal areas for protection, with large sample sizes being more representative of the population. Here, we examine the dispersal patterns of a key Mediterranean loggerhead turtle (Caretta caretta) breeding population to identify priority foraging sites for protection. Location: Zakynthos Island, Greece and the wider Mediterranean. Method: We examined the dispersal patterns and foraging sites of 75 adult loggerheads (n = 38 males and 37 females) tracked from the breeding area of Zakynthos Island (Greece) from 2004 to 2011. We then combined our data with published sea turtle literature to identify key foraging sites for protection. Results: While both males and females exhibited similar dispersal patterns, about 25% males remained < 100 km of Zakynthos, whereas all females (except one) migrated > 200 km. Integration of our data with the wider literature isolated 10 core sites in proximity to existing protected areas, which could potentially protect 64% of the Zakynthos population, while five sites support individuals from at least 10 other loggerhead breeding populations. Main conclusions: Due to the widespread availability of neritic foraging grounds across the Mediterranean, sea turtles from Zakynthos exhibit disparate dispersal patterns. However, protecting only a few objectively defined important sites can encompass a large proportion of the foraging areas used and hence have considerable conservation benefit.

Oceanic long-distance navigation : do experienced migrants use the earth's magnetic field?

Albatrosses and sea turtles are known to perform extremely long-distance journeys between disparate feeding areas and breeding sites located on small, isolated, oceanic islands or at specific coastal sites. These oceanic journeys, performed mainly over or through apparently featureless mediums, indicate impressive navigational abilities, and the sensory mechanisms used are still largely unknown. This research used three different approaches to investigate whether bi-coordinate navigation based on magnetic field gradients is likely to explain the navigational performance of wandering albatrosses in the South Atlantic and Indian Oceans and of green turtles breeding on Ascension Island in the South Atlantic Ocean. The possibility that magnetic field parameters can potentially be used in a bi-coordinate magnetic map by wandering albatrosses in their foraging area was investigated by analysing satellite telemetry data published in the literature. The possibilities for using bi-coordinate magnetic navigation varied widely between different areas of the Southern Oceans, indicating that a common mechanism, based on a bi-coordinate geomagnetic map alone, was unlikely for navigation in these areas. In the second approach, satellite telemetry was used to investigate whether Ascension Island green turtles use magnetic information for navigation during migration from their breeding island to foraging areas in Brazilian coastal waters. Disturbing magnets were applied to the heads and carapaces of the turtles, but these appeared to have little effect on their ability to navigate. The only possible effect observed was that some of the turtles with magnets attached were heading for foraging areas slightly south of the control turtles along the Brazilian coast. In the third approach, breeding female green turtles were deliberately displaced in the waters around Ascension Island to investigate which cues these turtles might use to locate and return to the island; the results suggested that cues transported by wind might be involved in the final stages of navigation.

Conservation hotspots : implications of intense spatial area use by breeding male and female loggerheads at the Mediterranean’s largest rookery

The implementation of appropriate protection measures for endangered species in protected areas requires knowledge of their fine-scale habitat use. In May and June of 2006 and 2007, we used GPS loggers (some linked to the Argos system) and a conventional Argos transmitter to track male and female loggerhead turtles Caretta caretta in the vicinity of the breeding area of Laganas Bay within the National Marine Park of Zakynthos, Greece. We obtained (1) 9681 useable locations (mean: 1383 locations ind.–1; range: 519 to 2198 locations) from Tracktag GPS loggers attached to 7 females for a mean duration of 34 d (range: 17 to 52 d); (2) 1245 useable locations (mean: 311 locations ind.–1; range: 38 to 1110 locations) from 4 males fitted with Fastloc Argos tags for a mean duration of 29 d (range: 3 to 51 d) and (3) 100 locations from 1 male fitted with a conventional Argos satellite tag tracked for 128 d. GPS data indicated that before the onset of nesting, both males and females primarily used an area within 500 m of the shore along a core 9 km stretch of coastline, where existing protective legislation requires strengthening. Our observations suggest that a 76.7% female-biased operational sex ratio, measured previously from in-water surveys, may represent a realistic sex ratio estimate in the period before nesting starts. In the first month following the onset of nesting, female spatial distribution remained similar, whereas most males departed for distant areas presumably to forage. Our study provides quantitative evidence of the need to improve the management planning and conservation measures to protect sea turtles in a coastal breeding area, and new insights on male turtle migration.