Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change

Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles (Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0.21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.

Ontogenetic development of migration : Lagrangian drift trajectories suggest a new paradigm for sea turtles

Long distance migration occurs in a wide variety of taxa including birds, insects, fishes, mammals and reptiles. Here, we provide evidence for a new paradigm for the determinants of migration destination. As adults, sea turtles show fidelity to their natal nesting areas and then at the end of the breeding season may migrate to distant foraging sites. For a major rookery in the Mediterranean, we simulated hatchling drift by releasing 288 000 numerical particles in an area close to the nesting beaches. We show that the pattern of adult dispersion from the breeding area reflects the extent of passive dispersion that would be experienced by hatchlings. Hence, the prevailing oceanography around nesting areas may be crucial to the selection of foraging sites used by adult sea turtles. This environmental forcing may allow the rapid evolution of new migration destinations if ocean currents alter with climate change.

Fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles

Aim  Resources can shape patterns of habitat utilization. Recently a broad foraging dichotomy between oceanic and coastal sites has been revealed for loggerhead sea turtles (Caretta caretta). Since oceanic and coastal foraging sites differ in prey availability, we might expect a gross difference in home-range size across these habitats. We tested this hypothesis by equipping nine adult male loggerhead sea turtles with GPS tracking devices. Location  National Marine Park of Zakynthos (NMPZ) Greece, central and eastern Mediterranean (Adriatic, Ionian and Aegean seas). Methods  In 2007, 2008 and 2009, Fastloc GPS-Argos transmitters were attached to nine male loggerheads. In addition, a Sirtrack PTT unit was attached to one male in 2007. Four of the turtles were tracked on successive years. We filtered the GPS data to ensure comparable data volumes. Route consistency between breeding and foraging sites of the four re-tracked turtles was conducted. Foraging site home range areas and within site movement patterns were investigated by the fixed kernel density method. Results  Foraging home range size ranged between circa 10 km2 at neritic habitats (coastal and open-sea on the continental shelf) to circa 1000 km2 at oceanic sites (using 90% kernel estimates), the latter most probably reflecting sparsely distributed oceanic prey. Across different years individuals did not follow exactly the same migration routes, but did show fidelity to their previous foraging sites, whether oceanic or neritic, with accurate homing in the final stages of migration. Main conclusions  The broad distribution and diverse life-history strategies of this population could complicate the identification of priority marine protected areas beyond the core breeding site.

Microhabitat selection by sea turtles in a dynamic thermal marine environment

1Reproductive fitness is often compromised at the margins of a species’ range due to sub-optimal conditions.2Set against this backdrop, the Mediterranean's largest loggerhead sea turtle (Caretta caretta) rookery at Zakynthos (Greece) presents a conundrum, being at a very high latitude for this species, yet hosting a high concentration of nesting.3We used visual surveys combined with global positioning system (GPS) tracking to show that at the start of the breeding season, individuals showed microhabitat selection, with females residing in transient patches of warm water. As the sea warmed in the summer, this selection was no longer evident.4As loggerhead turtles are ectothermic, this early season warm-water selection presumably speeds up egg maturation rates before oviposition, thereby allowing more clutches to be incubated when sand conditions are optimal during the summer.5Active selection of warm waters may allow turtles to initiate nesting at an earlier date.

Influence of ocean currents on long-distance movement of leatherback sea turtles in the Southwest Indian Ocean

Leatherback turtles Dermochelys coriacea spend most of their life in oceanic environments, whose physical and biological characteristics are primarily forged by sea current circulation. Water mass movements can mechanically act on swimming turtles, thus determining their routes, and can differentially distribute their planktonic prey. By integrating satellite tracking data with contemporaneous remote-sensing information, we analysed the post-nesting journeys of 9 leatherbacks with respect to oceanographic surface conditions. Tracked turtles showed large variations in migration routes and in final destinations, apparently without heading for specific foraging areas. Their complex tracks spread over wide regions around South Africa. Leatherbacks were greatly influenced by the currents encountered during their movements, with their trajectories displaying curves or revolutions in the presence of (and in accordance with) rotating water masses. An impressive similarity was observed between large parts of the turtle routes and those of surface drifters tracked in the same regions. Finally, leatherbacks remained associated for long periods with specific oceanographic features, which most probably offered them profitable foraging opportunities. These results agree with previous findings in showing a strong influence of oceanic currents and mesoscale features on the movements of South African leatherbacks, and additionally identify the role of current-related features in causing the observed route variability and in determining high-quality foraging hotspots for leatherbacks moving in the ocean.

Overwintering behaviour in sea turtles : dormancy is optional

Thirteen loggerhead turtles Caretta caretta were released (10 from Naples, Italy, 2 from Monastir, Tunisia, 1 from Gallipoli, South Italy) with satellite relay data loggers (SRDL) to elucidate their overwintering behaviour. Nine turtles were successfully tracked throughout the winter, while 4 SRDLs failed to transmit after short deployment periods. Of these 9, 4 remained within 80 km of the release site, 3 travelled to a distant overwintering site, and 2 continued to move and did not remain within 80 km of a specific site. Apart from these differences, all turtles stayed near the coast and dedicated most of their time to dives lasting 3 h and longer. Maximum dive durations ranged from 270 to 480 min and were highly correlated with water temperatures, which fell below the supposed 15°C threshold for sea turtle hibernation in all overwintering sites. Median dive depths were between 4 and 24 m and were, thus, well within the mixed layer, as revealed by temperature profiles, which also were relayed by the SRDLs. No evidence was found that the turtles preferred warmer temperatures to overwinter in, because the range of temperature was very narrow on both the horizontal and the vertical scale of their movements. Despite the long resting phases and the low temperatures (minimum = 11.8°C) all turtles retained activity to some degree, at least to commute between the depth of resting and the surface to breathe. While the degree of winter dormancy is certainly affected by temperature, turtles were by no means obligatory hibernators, and their ability to move and even forage during the winter may be important for their growth and maturation rates, as well as their reproductive output.

Female–female aggression : structure of interaction and outcome in loggerhead sea turtles

Aggressive behaviour between females of the same species is not widely documented, particularly in marine vertebrates. During a 3 yr in-water survey at the temperate loggerhead sea turtle Caretta caretta breeding area of Zakynthos, Greece, female–female interactions comprised 4% of all female loggerhead sighting events (n = 60 out of 1449 events). Male–female interactions comprised an additional 4% of sighting events, while 92% were of solitary females. The structure of interactions was analysed for 58 of these sighting events, each lasting an average of 3.4 min (SD ± 1) and comprising a total of 3.1 h observation time. We found that interactions involved ritualized escalation in behaviour from passive threat displays (e.g. head–tail circling) to aggressive combat (e.g. sparring). We suggest that circling individuals evaluate opponent size, sparring individuals test opponent strength, and that the positioning of the prehensile tail signals motivational intent to either escalate or abort. The presence of intruder females triggered a passive response in 100% of events involving basking and swimming turtles (n = 19); although residents resting on the seabed only responded on 69% of occasions (n = 27), their response was almost 4 times more likely to escalate to one of aggression. Our results suggest that certain sites may be preferentially sought after and defended by sea turtles.

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.

Different male vs. female breeding periodicity helps mitigate offspring sex ratio skews in sea turtles

 The implications of climate change for global biodiversity may be profound with those species with little capacity for adaptation being thought to be particularly vulnerable to warming. A classic case of groups for concern are those animals exhibiting temperature-dependent sex-determination (TSD), such as sea turtles, where climate warming may produce single sex populations and hence extinction. We show that, globally, female biased hatchling sex ratios dominate sea turtle populations (exceeding 3:1 in >50% records), which, at-a-glance, reiterates concerns for extinction. However, we also demonstrate that more frequent breeding by males, empirically shown by satellite tracking 23 individuals and supported by a generalized bio-energetic life history model, generates more balanced operational sex ratios (OSRs). Hence, concerns of increasingly skewed hatchling sex ratios and reduced population viability are less acute than previously thought for sea turtles. In fact, in some scenarios skewed hatchling sex ratios in groups with TSD may be adaptive to ensure optimum OSRs.

Sand temperatures for nesting sea turtles in the Caribbean: Implications for hatchling sex ratios in the face of climate change

A 200-year time series of incubation temperatures and primary sex ratios for green (Chelonia mydas), hawksbill (Eretmochelys imbricata) and leatherback (Dermochelys coriacea) sea turtles nesting in St. Eustatius (North East Caribbean) was created by combining sand temperature measurements with historical and current environmental data and climate projections. Rainfall and spring tides were important because they cooled the sand and lowered incubation temperatures. Mean annual sand temperatures are currently 31.0. °C (SD. =. 1.6) at the nesting beach but show seasonality, with lower temperatures (29.1-29.6. °C) during January-March and warmer temperatures (31.9-33.3. °C) in June-August. Results suggest that all three species have had female-biased hatchling production for the past decades with less than 15.5%, 36.0%, and 23.7% males produced every year for greens, hawksbills and leatherbacks respectively since the late nineteenth century. Global warming will exacerbate this female-skew. For example, projections indicate that only 2.4% of green turtle hatchlings will be males by 2030, 1.0% by 2060, and 0.4% by 2090. On the other hand, future changes to nesting phenology have the potential to mitigate the extent of feminisation. In the absence of such phenological changes, management strategies to artificially lower incubation temperatures by shading nests or relocating nest clutches to deeper depths may be the only way to prevent the localised extinction of these turtle populations.

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.

A comparison of the seasonal movements of tiger sharks and green turtles provides insight into their predator-prey relationship

During the reproductive season, sea turtles use a restricted area in the vicinity of their nesting beaches, making them vulnerable to predation. At Raine Island (Australia), the highest density green turtle Chelonia mydas rookery in the world, tiger sharks Galeocerdo cuvier have been observed to feed on green turtles, and it has been suggested that they may specialise on such air-breathing prey. However there is little information with which to examine this hypothesis. We compared the spatial and temporal components of movement behaviour of these two potentially interacting species in order to provide insight into the predator-prey relationship. Specifically, we tested the hypothesis that tiger shark movements are more concentrated at Raine Island during the green turtle nesting season than outside the turtle nesting season when turtles are not concentrated at Raine Island. Turtles showed area-restricted search behaviour around Raine Island for ~3–4 months during the nesting period (November–February). This was followed by direct movement (transit) to putative foraging grounds mostly in the Torres Straight where they switched to area-restricted search mode again, and remained resident for the remainder of the deployment (53–304 days). In contrast, tiger sharks displayed high spatial and temporal variation in movement behaviour which was not closely linked to the movement behaviour of green turtles or recognised turtle foraging grounds. On average, tiger sharks were concentrated around Raine Island throughout the year. While information on diet is required to determine whether tiger sharks are turtle specialists our results support the hypothesis that they target this predictable and plentiful prey during turtle nesting season, but they might not focus on this less predictable food source outside the nesting season.