COVID-19 disruption reveals mass-tourism pressure on nearshore sea turtle distributions and access to optimal breeding habitat.

Quantifying the extent to which animals detect and respond to human presence allows us to identify pressure (disturbance) and inform conservation management objectively; however, obtaining baselines against which to compare human impact is hindered in areas where human activities are already well established. For example, Zakynthos Island (Greece, Mediterranean) receives around 850,000 visitors each summer, while supporting an important loggerhead sea turtle rookery (~300 individuals/season). The coronavirus (COVID-19)-driven absence of tourism in May-June 2020 provided an opportunity to evaluate the distribution dynamics of this population in the absence (2020) vs. presence (2018 and 2019) of visitors using programmed unmanned aerial system (UAS) surveys. Ambient sea temperature transitioned from suboptimal for breeding in May to optimal in late June, with turtle distribution appearing to shift from shallow (to benefit from waters 3-5°C above ambient) to deeper waters in 2018 and 2019, but not 2020. The 2020 data set demonstrated that increased tourism pressure, not temperature, drives turtles offshore. Specifically, >50% of turtles remained within 100 m of shore at densities of 25-50 visitors/km, even when sea temperature rose, with 2018 and 2019 data supporting this trend. Reduced access to warmer, nearshore waters by tourism could delay the onset of nesting and increase the length of the egg maturation period between nesting events (internesting interval) at this site. A coastal refuge zone could be delimited in May-June where touristic infrastructure is minimal, but also where turtles frequently aggregate. In conclusion, sea turtles appear capable of perceiving changes in the level of human pressure at fine spatial and temporal scales and adjusting their distribution accordingly.

Long-term photo-id and satellite tracking reveal sex-biased survival linked to movements in an endangered species.

Sex-biased survival linked to anthropogenic threats places populations at risk. We show the utility of long-term multidecadal photo-identification (photo-id) combined with long-term high-resolution (Fastloc-GPS) satellite telemetry to investigate the links between mortality rates and patterns of movement for a wide-ranging, endangered marine vertebrate. Using a photo-identification database of 947 loggerhead turtles (Caretta caretta) compiled over 18 yr, we estimated greater annual survival rates of females (0.89; 95% confidence interval [CI] 0.87-0.90) compared to males (0.73; 95% CI 0.67-0.78). For males satellite-tracked across multiple breeding seasons, 100% (26 of 26) returned to the same breeding site, suggesting the calculated lower male survival rate was likely not due to emigration to breed elsewhere. 10,111 and 2,524 tracking days for males (n = 39 individuals) and females (n = 18 individuals), respectively, revealed different habitat-use patterns outside the breeding season: males tended to occupy foraging sites closer to shore and closer to breeding sites but, due to their generally annual breeding, compared to biennial breeding for females, males migrated further per year on average. These differences in movement patterns likely contribute to higher mortality in males through increased interaction with anthropogenic threats. Long-term identification coupled with tracking offers great promise for estimating the survival rates of other wide-ranging species.

The complete mitochondrial genome of the loggerhead turtle Caretta caretta (Testudines: Cheloniidae): genome description and phylogenetic considerations.

The marine turtle Caretta caretta is a widely distributed species that is facing critical population decline, especially in the Mediterranean rookeries. Molecular markers, such as mitochondrial DNA (mtDNA) sequences, are of great importance for the description and monitoring of turtle migratory populations. The complete sequence of the C. caretta mitochondrial genome is presented here. The genome comprises 16,440 base pairs, containing 37 genes (13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes), and a control region, all organized similar to the majority of vertebrate mitogenomes. MtDNA length polymorphism and heteroplasmy were observed among, and within, individuals due to the variable size of a microsatellite repeat residing at the 3' end of the control region. The use of the above repeat as a marker for individual fingerprinting is discussed. Furthermore, phylogenetic analyses among Testudines based on complete mitogenomes, as well as among marine turtles based on partial mtDNA sequences, are considered.

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.

Microhabitat selection by sea turtles in a dynamic thermal marine environment.

1. Reproductive fitness is often compromised at the margins of a species' range due to sub-optimal conditions. 2. Set 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. 3. We 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. 4. As 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. 5. Active selection of warm waters may allow turtles to initiate nesting at an earlier date.