Scott D. Whiting

The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange

Ecological and genetic studies of marine turtles generally support the hypothesis of natal homing, but leave open the question of the geographical scale of genetic exchange and the capacity of turtles to shift breeding sites. Here we combine analyses of mitochondrial DNA (mtDNA) variation and recapture data to assess the geographical scale of individual breeding populations and the distribution of such populations through Australasia. We conducted multiscale assessments of mtDNA variation among 714 samples from 27 green turtle rookeries and of adult female dispersal among nesting sites in eastern Australia. Many of these rookeries are on shelves that were flooded by rising sea levels less than 10 000 years (c. 450 generations) ago. Analyses of sequence variation among the mtDNA control region revealed 25 haplotypes, and their frequency distributions indicated 17 genetically distinct breeding stocks (Management Units) consisting either of individual rookeries or groups of rookeries in general that are separated by more than 500 km. The population structure inferred from mtDNA was consistent with the scale of movements observed in long‐term mark–recapture studies of east Australian rookeries. Phylogenetic analysis of the haplotypes revealed five clades with significant partitioning of sequence diversity (Φ = 68.4) between Pacific Ocean and Southeast Asian/Indian Ocean rookeries. Isolation by distance was indicated for rookeries separated by up to 2000 km but explained only 12% of the genetic structure. The emerging general picture is one of dynamic population structure influenced by the capacity of females to relocate among proximal breeding sites, although this may be conditional on large population sizes as existed historically across this region.

Enhancing the use of Argos satellite data for home range and long distance migration studies of marine animals.

Accurately quantifying animals’ spatial utilisation is critical for conservation, but has long remained an elusive goal due to technological impediments. The Argos telemetry system has been extensively used to remotely track marine animals, however location estimates are characterised by substantial spatial error. State-space models (SSM) constitute a robust statistical approach to refine Argos tracking data by accounting for observation errors and stochasticity in animal movement. Despite their wide use in ecology, few studies have thoroughly quantified the error associated with SSM predicted locations and no research has assessed their validity for describing animal movement behaviour. We compared home ranges and migratory pathways of seven hawksbill sea turtles (Eretmochelys imbricata) estimated from (a) highly accurate Fastloc GPS data and (b) locations computed using common Argos data analytical approaches. Argos 68th percentile error was <1 km for LC 1, 2, and 3 while markedly less accurate (>4 km) for LC ≤0. Argos error structure was highly longitudinally skewed and was, for all LC, adequately modelled by a Student’s t distribution. Both habitat use and migration routes were best recreated using SSM locations post-processed by re-adding good Argos positions (LC 1, 2 and 3) and filtering terrestrial points (mean distance to migratory tracks ± SD = 2.2±2.4 km; mean home range overlap and error ratio  = 92.2% and 285.6 respectively). This parsimonious and objective statistical procedure however still markedly overestimated true home range sizes, especially for animals exhibiting restricted movements. Post-processing SSM locations nonetheless constitutes the best analytical technique for remotely sensed Argos tracking data and we therefore recommend using this approach to rework historical Argos datasets for better estimation of animal spatial utilisation for research and evidence-based conservation purposes.

Blood chemistry reference values for two ecologically distinct populations of foraging green turtles, eastern Indian Ocean

Blood chemistry reference values are important to allow the monitoring of the health of individuals and populations. Blood chemistry reference values were obtained from individuals of two ecologically distinct foraging populations of green turtles (Chelonia mydas) in the eastern Indian Ocean. Samples were taken from 51 resident green turtles from Ashmore Reef (a shelf-edge platform reef) with a predominant seagrass diet, and 59 samples were taken from green turtles from Fog Bay, an inshore coastal embayment in the Northern Territory of Australia with a predominant algal diet. Reference values were different between habitats and showed the importance of regional and habitat-specific reference values for green turtles if they are to be used as a diagnostic tool. Green turtles with a diet of seagrass showed higher levels of total protein than turtles of the same size with algal diets. Clinically sick turtles from Fog Bay had significantly higher levels of urea and AST and lower PCV values than healthy turtles from the same population. Newly recruited turtles from Fog Bay also had higher levels of urea and AST compared to other turtles from the same area. Low levels of internal parasites did not affect blood reference values in clinically healthy turtles.

SHORT TERM FORAGING RANGES OF ADULT GREEN TURTLES (CHELONIA MYDAS)

Conventional Very High Frequency (VHF) transmitters encased in a float were attached by a lanyard to ten adult green turtles foraging in Repulse Bay, central Queensland, Australia. Short term move- ments of 4-25 km and foraging ranges between 84-850 ha were recorded during attachment times of 4-29 days. Recaptures of tagged turtles in this area support radio tracking data. These are the largest movements reported by green turtles in a foraging ground and the only foraging movement data published on adult green turtles. Large foraging movements are attributed to the low-average above ground seagrass biomass in southern Repulse Bay. The seagrass community comprised Zostera capricorni, Halodule uninervis and

Insights into size, seasonality and biology of a nesting population of the Olive Ridley turtle in northern Australia

The Olive Ridley turtle (Lepidochelys olivacea), classed as endangered in Australia, is one of Australia’s least studied marine turtles and is little known in the south-east Asian region. This is the first detailed study of the nesting biology and ecology of L. olivacea in Australia or south-east Asia, which adds to the regional knowledge of the species and will aid management locally. Daytime surveys of nesting tracks at 14-day intervals in 2004 and irregular surveys in 2005 indicated that the nesting season extended from February to November with peak nesting in April and May. Daily track counts over a 14-day period in April 2004 during peak nesting showed that nesting abundance varied between nights and along the beach. Nightly numbers ranged from 2 to 59 turtles per night over the 10-km beach while, spatially, nesting densities (0.1–6.9 tracks km–1 night–1) varied between sectors. Nesting in this population was solitary, as opposed to the mass nesting behaviour of L. olivacea observed elsewhere in its range, such as in India, Mexico and Costa Rica. The size of nesting L. olivacea was normally distributed with a mean curved carapace length of 69.6 ± 2.3 (s.d.) cm (range = 65.0–75.2, n = 85). During the peak of the nesting season dingoes (Canis lupus dingo) were responsible for the highest egg mortality (over 14%), followed by varanids (Varanus spp., 4.5%) and humans (1.7%). Cyclone Ingrid caused significant egg loss in 2004. Saltwater crocodiles (Crocodylus porosus) were a significant predator of adult nesting turtles.

Increased expression of Hsp70 and Hsp90 mRNA as biomarkers of thermal stress in loggerhead turtle embryos (Caretta Caretta).

The survival and viability of sea turtle embryos is dependent upon favourable nest temperatures throughout the incubation period. Consequently, future generations of sea turtles may be at risk from increasing nest temperatures due to climate change, but little is known about how embryos respond to heat stress. Heat shock genes are likely to be important in this process because they code for proteins that prevent cellular damage in response to environmental stressors. This study provides the first evidence of an expression response in the heat shock genes of embryos of loggerhead sea turtles (Caretta caretta) exposed to realistic and near-lethal temperatures (34°C and 36°C) for 1 or 3 hours. We investigated changes in Heat shock protein 60 (Hsp60), Hsp70, and Hsp90 mRNA in heart (n=24) and brain tissue (n=29) in response to heat stress. Under the most extreme treatment (36°C, 3h), Hsp70 increased mRNA expression by a factor of 38.8 in heart tissue and 15.7 in brain tissue, while Hsp90 mRNA expression increased by a factor of 98.3 in heart tissue and 14.7 in brain tissue. Hence, both Hsp70 and Hsp90 are useful biomarkers for assessing heat stress in the late-stage embryos of sea turtles. The method we developed can be used as a platform for future studies on variation in the thermotolerance response from the clutch to population scale, and can help us anticipate the resilience of reptile embryos to extreme heating events.

Artificial light on water attracts turtle hatchlings during their near shore transit

We examined the effect of artificial light on the near shore trajectories of turtle hatchlings dispersing from natal beaches. Green turtle (Chelonia mydas) hatchlings were tagged with miniature acoustic transmitters and their movements tracked within an underwater array of 36 acoustic receivers placed in the near shore zone. A total of 40 hatchlings were tracked, 20 of which were subjected to artificial light during their transit of the array. At the same time, we measured current speed and direction, which were highly variable within and between experimental nights and treatments. Artificial lighting affected hatchling behaviour, with 88% of individual trajectories oriented towards the light and spending, on average, 23% more time in the 2.25 ha tracking array (19.5 ± 5 min) than under ambient light conditions (15.8 ± 5 min). Current speed had little to no effect on the bearing (angular direction) of the hatchling tracks when artificial light was present, but under ambient conditions it influenced the bearing of the tracks when current direction was offshore and above speeds of approximately 32.5 cm s−1. This is the first experimental evidence that wild turtle hatchlings are attracted to artificial light after entering the ocean, a behaviour that is likely to subject them to greater risk of predation. The experimental protocol described in this study can be used to assess the effect of anthropogenic (light pollution, noise, etc.) and natural (wave action, current, wind, moonlight) influences on the in-water movements of sea turtle hatchlings during the early phase of dispersal.

Heritable variation in heat shock gene expression: a potential mechanism for adaptation to thermal stress in embryos of sea turtles

The capacity of species to respond adaptively to warming temperatures will be key to their survival in the Anthropocene. The embryos of egg-laying species such as sea turtles have limited behavioural means for avoiding high nest temperatures, and responses at the physiological level may be critical to coping with predicted global temperature increases. Using the loggerhead sea turtle (Caretta caretta) as a model, we used quantitative PCR to characterise variation in the expression response of heat-shock genes (hsp60, hsp70 and hsp90; molecular chaperones involved in cellular stress response) to an acute non-lethal heat shock. We show significant variation in gene expression at the clutch and population levels for some, but not all hsp genes. Using pedigree information, we estimated heritabilities of the expression response of hsp genes to heat shock and demonstrated both maternal and additive genetic effects. This is the first evidence that the heat-shock response is heritable in sea turtles and operates at the embryonic stage in any reptile. The presence of heritable variation in the expression of key thermotolerance genes is necessary for sea turtles to adapt at a molecular level to warming incubation environments.

Phylogeography, Genetic Diversity, and Management Units of Hawksbill Turtles in the Indo-Pacific

Hawksbill turtle (Eretmochelys imbricata) populations have experienced global decline because of a history of intense commercial exploitation for shell and stuffed taxidermied whole animals, and harvest for eggs and meat. Improved understanding of genetic diversity and phylogeography is needed to aid conservation. In this study, we analyzed the most geographically comprehensive sample of hawksbill turtles from the Indo-Pacific Ocean, sequencing 766 bp of the mitochondrial control region from 13 locations (plus Aldabra, n = 4) spanning over 13500 km. Our analysis of 492 samples revealed 52 haplotypes distributed in 5 divergent clades. Diversification times differed between the Indo-Pacific and Atlantic lineages and appear to be related to the sea-level changes that occurred during the Last Glacial Maximum. We found signals of demographic expansion only for turtles from the Persian Gulf region, which can be tied to a more recent colonization event. Our analyses revealed evidence of transoceanic migration, including connections between feeding grounds from the Atlantic Ocean and Indo-Pacific rookeries. Hawksbill turtles appear to have a complex pattern of phylogeography, showing a weak isolation by distance and evidence of multiple colonization events. Our novel dataset will allow mixed-stock analyses of hawksbill turtle feeding grounds in the Indo-Pacific by providing baseline data needed for conservation efforts in the region. Eight management units are proposed in our study for the Indo-Pacific region that can be incorporated in conservation plans of this critically endangered species.

Reconstructed paternal genotypes reveal variable rates of multiple paternity at three rookeries of loggerhead sea turtles (Caretta caretta) in Western Australia

Abstract. Female sea turtles are promiscuous, with clutches of eggs often sired by multiple males and rates of multiple paternity varying greatly within and across species. We investigated levels of multiple paternity in loggerhead sea turtles (Caretta caretta) from three rookeries in Western Australia by analysing polymorphic species-specific genetic markers. We predicted that the level of multiple paternity would be related to female population size and hence the large rookery at Dirk Hartog Island would have higher rates of multiple paternity than two smaller mainland rookeries at Gnaraloo Bay and Bungelup Beach. Contrary to our prediction, we found highly variable rates of multiple paternity among the rookeries that we sampled, which was unrelated to female population size (25% at Bungelup Beach, 86% at Gnaraloo Bay, and 36% at Dirk Hartog Island). Approximately 45 different males sired 25 clutches and the average number of sires per clutch ranged from 1.2 to 2.1, depending on the rookery sampled. The variance in rates of multiple paternity among rookeries suggests that operational sex ratios are variable in Western Australia. Periodic monitoring would show whether the observed patterns of multiple paternity for these three rookeries are stable over time, and our data provide a baseline for detecting shifts in operational sex ratios.