Global phylogeography of ridley sea turtles (Lepidochelys spp.): evolution, demography, connectivity, and conservation.

Globally distributed marine taxa are well suited for investigations of biogeographic impacts on genetic diversity, connectivity, and population demography. The sea turtle genus Lepidochelys includes the wide-ranging and abundant olive ridley (L. olivacea), and the geographically restricted and 'Critically Endangered' Kemp's ridley (L. kempii). To investigate their historical biogeography, we analyzed a large dataset of mitochondrial DNA (mtDNA) sequences from olive (n = 943) and Kemp's (n = 287) ridleys, and genotyped 15 nuclear microsatellite loci in a global sample of olive ridleys (n = 285). We found that the ridley species split ~ 7.5 million years ago, before the Panama Isthmus closure. The most ancient mitochondrial olive ridley lineage, located in the Indian Ocean, was dated to ~ 2.2 Mya. Both mitochondrial and nuclear markers revealed significant structure for olive ridleys between Atlantic (ATL), East Pacific (EP), and Indo-West Pacific (IWP) areas. However, the divergence of mtDNA clades was very recent (< 1 Mya) with low within- clade diversity, supporting a recurrent extinction-recolonization model for these ocean regions. All data showed that ATL and IWP groups were more closely related than those in the EP, with mtDNA data supporting recent recolonization of the ATL from the IWP. Individual olive ridley dispersal between the ATL, EP, and IN/IWP could be interpreted as more male- than female-biased, and genetic diversity was lowest in the Atlantic Ocean. All populations showed signs of recent expansion, and estimated time frames were concordant with their recent colonization history. Investigating species abundance and distribution changes over time is central to evolutionary biology, and this study provides a historical biogeographic context for marine vertebrate conservation and management. Supplementary Information: The online version contains supplementary material available at 10.1007/s10592-022-01465-3.

Multivariate analysis of biologging data reveals the environmental determinants of diving behaviour in a marine reptile.

Diving behaviour of 'surfacers' such as sea snakes, cetaceans and turtles is complex and multi-dimensional, thus may be better captured by multi-sensor biologging data. However, analysing these large multi-faceted datasets remains challenging, though a high priority. We used high-resolution multi-sensor biologging data to provide the first detailed description of the environmental influences on flatback turtle (Natator depressus) diving behaviour, during its foraging life-history stage. We developed an analytical method to investigate seasonal, diel and tidal effects on diving behaviour for 24 adult flatback turtles tagged with biologgers. We extracted 16 dive variables associated with three-dimensional and kinematic characteristics for 4128 dives. K-means and hierarchical cluster analyses failed to identify distinct dive types. Instead, principal component analysis objectively condensed the dive variables, removing collinearity and highlighting the main features of diving behaviour. Generalized additive mixed models of the main principal components identified significant seasonal, diel and tidal effects on flatback turtle diving behaviour. Flatback turtles altered their diving behaviour in response to extreme tidal and water temperature ranges, displaying thermoregulation and predator avoidance strategies while likely optimizing foraging in this challenging environment. This study demonstrates an alternative statistical technique for objectively interpreting diving behaviour from multivariate collinear data derived from biologgers.

Age-specific growth and maturity estimates for the flatback sea turtle (Natator depressus) by skeletochronology.

To address a major knowledge gap for flatback sea turtles (Natator depressus), a species endemic to Australia and considered 'Data Deficient' for IUCN Red List assessment, we present the first-ever skeletochronology-derived age and growth rate estimates for this species. Using a rare collection of bone samples gathered from across northern Australia, we applied skeletochronology and characterized the length-at-age relationship, established baseline growth rates from the hatchling to adult life stages, and produced empirical estimates of age-at- and size-at-sexual-maturation (ASM, SSM). We analyzed humeri from 74 flatback sea turtles ranging in body size from 6.0-96.0 cm curved carapace length (CCL), and recovered from Western Australia (n = 48), Eastern Australia (n = 13), central Australia (n = 8; Northern Territory n = 3, the Gulf of Carpentaria n = 5), and unknown locations (n = 5). We identified the onset of sexual maturity for 29 turtles, based on rapprochement growth patterns in the bones. Estimates for ASM ranged from 12.0 to 23.0 years (mean: 16.3 ± 0.53 SE), SSM ranged from 76.1 to 94.0 cm CCL (mean: 84.9 ± 0.90 SE), and maximum observed reproductive longevity was 31 years for a 45-year old male flatback. Growth was modeled as a smoothing spline fit to the size-at-age relationship and at the mean SSM (84.9 cm CCL) corresponded with a spline-predicted maturity age of 18 years (95% CI: 16 to 24), while mean nesting sizes reported in the literature (86.4 to 94 cm CCL) corresponded to estimated ages of 24+ years. A bootstrapped von Bertalanffy growth model was also applied and showed consistencies with the spline curve, yielding an estimated upper size limit, Linf, at 89.2 ± 0.04 cm (95% CI: 85.5 to 95.9 cm) with the intrinsic growth rate parameter, k, at 0.185 ± 0.0004 (0.16 to 0.22); at the same mean SSM (84.9 cm CCL) the estimated ASM was 16.3 ± 0.05 years (95% CI: 12.8 to 27.7 years). Lastly, four of the samples analyzed were collected from deceased adult females that had previous sizes known from on-going mark/recapture studies at nesting sites in Western Australia. The paired CCL data (measured at nesting and back-calculated) did not significantly differ (p = 0.875). This first skeletochronology study for flatback sea turtles generates valuable empirical estimates for ongoing conservation and management efforts.

Streptococcus iniae associated mass marine fish kill off Western Australia.

Streptococcus iniae causes high mortality in cultured and wild fish stocks globally. Since the first report in captive Amazon river dolphins Inia geoffrensis in 1976, it has emerged in finfish across all continents except Antarctica. In March 2016, an estimated 17000 fish were observed dead and dying along a remote 70 km stretch of the Kimberley coastline north of Broome, Western Australia. Affected species included finfish (lionfish Pterois volitans, angelfish Pomacanthus sp., stripey snapper Lutjanus carponotatus, sand bass Psammoperca waigiensis, yellowtail grunter Amniataba caudavittata, damselfish Pomacentridae sp.), flatback sea turtles Natator depressus, and olive (Aipysurus laevis) and black-ringed (Hydrelaps darwiniensis) sea snakes. Moribund fish collected during the event exhibited exophthalmia and abnormal behaviour, such as spiralling on the surface or within the water column. Subsequent histopathological examination of 2 fish species revealed bacterial septicaemia with chains of Gram-positive cocci seen in multiple organs and within brain tissue. S. iniae was isolated and identified by bacterial culture, species-specific PCR, Matrix-Assisted Laser Desorption Ionisation Time-Of-Flight (MALDI-TOF) and biochemical testing. This is the first report of S. iniae associated with a major multi-species wild marine fish kill in Australia. Extreme weather events in the region including a marked decrease in water temperatures, followed by an extended period of above-average coastal water temperatures, were implicated as stressors potentially contributing to this outbreak.

Radionuclides in sea turtles at the Montebello Islands former nuclear test sites: Current and historical dose rates for adults and embryos.

Radionuclides from 1950s weapons testing at the Montebello Islands, Western Australia, may impact sea turtle embryos incubating within eggs laid in contaminated sands or be taken up into adult body tissues where they can contribute to radiation dose over a turtles' 60+ year lifespan. We measured plutonium in all local samples including turtle skin, bones, hatchlings, eggshells, sea sediments, diet items and beach sands. The amount of Pu in developing embryos/hatchling samples was orders of magnitude lower than that in the surrounding sands. These contaminated sands caused most dose to eggs (external dose from 137Cs, 152Eu), while most of the dose to adults was from internalised radionuclides (98%). While current dose rates are relatively low, local dose rates were high for about ten years following the 1950s detonations and may have resulted in lethality or health impacts to a generation of turtles that likely carry biomarkers today.

Microclimate modelling of beach sand temperatures reveals high spatial and temporal variation at sea turtle rookeries.

The continual development of ecological models and availability of high-resolution gridded climate surfaces have stimulated studies that link climate variables to functional traits of organisms. A primary constraint of these studies is the ability to reliably predict the microclimate that an organism experiences using macroscale climate inputs. This is particularly important in regions where access to empirical information is limited. Here, we contrast correlative models based on both ambient and sea surface temperatures to mechanistic modelling approaches to predict beach sand temperatures at depths relevant to sea turtle nesting. We show that mechanistic models are congruent with correlative models at predicting sand temperatures. We used these predictions to explore thermal variation across 46 mainland and island beaches that span the geographical range of sea turtle nesting in Western Australia. Using high resolution gridded climate surfaces and site-specific soil reflectance, we predict almost 9 °C variation in average annual temperatures between beaches, and nearly 10 °C variation in average temperatures during turtle nesting seasons. Validation of models demonstrated that predictions were typically within 2 °C of observations and, although most sites had high correlations (r2 > 0.7), predictive capacity varied between sites. An advantage of the mechanistic model demonstrated here is that it can be used to explore the impacts of climate change on sea turtle nesting beach temperatures as, unlike correlative models, it can be forced with novel combinations of environmental variables.

Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

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.

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.

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 68(th) 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.

Non-migratory breeding by isolated green sea turtles (Chelonia mydas) in the Indian Ocean: biological and conservation implications.

Green sea turtles (Chelonia mydas) are renowned for their long-distance migrations but have less fame for short-distance migrations or non-migratory behavior. We present satellite telemetric evidence from Cocos (Keeling) Islands, Indian Ocean for the first predominantly non-migratory green sea turtle (C. mydas) population. The mean migration distance from the nesting beach to the foraging grounds was 35.5 km with a maximum mean transit time of 3.4 days. The behavior of this population has major implications for our general understanding of green turtle behavior and their life cycle and for conservation. Firstly, these results indicate a level of juvenile or adult non-breeding homing behavior from the open ocean to foraging grounds adjacent to their natal nesting beach. Secondly, a non-migratory breeding phase reduces the consumption of reproductive energy utilized, potentially resulting in higher fecundity for this population. Thirdly, the close proximity of the nesting and foraging habitats allows for uniformity in management and conservation strategies rarely possible for wide-ranging green turtle populations.