nesting beach and crawl ashore at night to dig a nest in the sand. The sex of turtle offspring is ..... SWOT Scientific Advisory Board. Minimum data standards for ...
Questions of scale
COLLABORATIVE TURTLE RESEARCH ALONG THE KIMBERLEY‘S REMOTEST COASTS
Of the seven species of living sea turtles, six are found along the northern coast of Western Australia.1 Five of these Kimberley species come from the Cheloniidae family of marine turtles: the hawksbill turtle (Eretmochelys imbricata), olive ridley turtle (Lepidochelys olivacea), loggerhead turtle (Caretta caretta), green turtle (Chelonia mydas) and flatback turtle (Natator depressus). The exception is the leatherback turtle (Dermochelys coriacea), the only living species in the Dermochelyidae family. Like the flatback, the leatherback has a soft leathery carapace, or shell, instead of the hard keratinised scutes found in the other species.
Tony Tucker, Scott Whiting, Kellie Pendoley, Nancy FitzSimmons, Oliver Berry, Nicki Mitchell and Blair Bentley
Turtles have inhabited the world’s oceans for over 250 million years. The largest of fossil sea turtles, the now-extinct Archelon, measured up to 4.9 m, and lived during the late Cretaceous period. Contemporary sea turtles vary considerably in size: the smallest, the olive ridley turtle, weighs around 45 kg and has a shell 75 cm long, while the largest, the leatherback, weighs almost 500 kg and has a shell close to 2 m in length.2 Depending on the species, marine turtles take from 15 to 40 years to mature.3 In adulthood, they migrate to nesting beaches on 1 to 5 year cycles, producing 3 to 10 nests per season, with 50 to 140 eggs per nest.1 Turtles migrate between their foraging and breeding grounds, guided by Earth’s magnetic fields4, and return to the same grounds for each breeding cycle – a behaviour known as site fidelity (Fig. 1). Due to the length of time that it takes to store energy to reproduce5, turtles seldom breed in consecutive years unless the distance from the foraging ground to the rookery is relatively short or the foraging ground is very productive.6 Before the nesting season, females and males migrate independently to mating grounds – which may be near the nesting beaches or up to 1000 km away. Females may mate with more than one male in a short
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Figure 1 (opposite) An aerial image of a Cape Domett beach shows the density of turtle tracks – and a 3 m crocodile, which can dine on hatchlings or adult females. Photo: Kellie Pendoley / WAMSI
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Sea turtles are durable survivors despite natural mortality of their eggs on beaches and predation of juveniles and adults.3 However, they are vulnerable to recent changes introduced by humans: disturbance at nesting beaches; pollution and loss of their habitats; marine debris and plastics; poaching; unintentional capture by the fishing industry; harvesting of eggs and adult turtles for food; and illegal shell trading. Novel concerns emerge as global warming7,8 and rising sea levels9 affect the incubation of eggs on beaches. Of the Australian sea turtles, the International Union for Conservation of Nature Red List classifies the hawksbill as critically endangered; the green turtle as endangered; and the leatherback, loggerhead and olive ridley turtles as vulnerable.10 The Red List currently considers Australia’s endemic flatback turtles as ‘data deficient’, because many crucial population aspects are poorly known (Fig. 3). Australia’s flatback populations are believed to be stable, but only in the past decade have enough data amassed to establish any trends at their nesting beaches.11–13 Flatback turtles are unique in that the northernmost populations, from Torres Strait to the Kimberley, nest during the winter, while populations along the eastern and western Australian coasts nest in the summer.3 This summer-winter nesting shift may indicate where along the coast each population finds conditions that offer acceptable temperatures for incubation.
Figure 2 (top) Blair Bentley (PhD student, University of Western Australia) holds a hatchling while Ryan Douglas (DBCA) unearths a hatched nest to count eggshells (visible in foreground) to determine hatchling percentages from viable eggs. Photo: Tony Tucker / DBCA
With turtle populations so spread out – over years and across large areas – it can take time to detect the detrimental effects of human activities. Indeed, scientific research on turtles in general faces several particularly challenging problems of scale: the remoteness of breeding grounds and the difficulty in accessing them, the long gaps in research programs when these animals ‘disappear’ for many years, and the extended time needed to achieve significant results when studying such long-lived animals.14 Since the Kimberley is one of the least accessible of Australian coastlines, many of these concerns are recognised in the Recovery Plan for Marine Turtles in Australia.11
Figure 3 (bottom) A female flatback returns to the water after nesting. Photo: Ryan Douglas / DBCA
COLLABORATIVE RESEARCH IN THE KIMBERLEY
receptive period over the course of a week. Because females store sperm within the season and for another few years or more, eggs in a single clutch may have multiple paternities. Females journey onward to a chosen nesting beach and crawl ashore at night to dig a nest in the sand. The sex of turtle offspring is determined by the incubation temperature of the eggs: cooler temperatures produce more males and warmer temperatures produce more females. Hatchling survival to adulthood is low – estimated to be about 1 in 1000 – but adult survival is high (Fig. 2).
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Given the spatial and temporal scales spanning sea turtles’ life cycles, a mix of short- and long-term approaches is required to study them.15 For example, a boat survey might cover tens of square kilometres, while an aerial survey could scan up to tens of thousands of square kilometres. Field surveys tend to be carried out over hours, days or weeks, whereas local knowledge can extend over months, years or even centuries. In the Kimberley, it is essential that sea turtle research incorporates Indigenous perspectives and aspirations, because turtles have been part of Indigenous Australians’ culture and diet for thousands of years. The
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Figure 4 (opposite, top) Flatback turtle tracks have a more prominent and wider tail drag than other marine turtles. Photo: Tony Tucker / DBCA Figure 5 (opposite, bottom) Elizabeth Bevan (PhD student, University of AlabamaBirmingham, USA) watches the screen while her drone patrols above the Cape Domett beach to record turtle tracks. Photo: Ryan Douglas / DBCA
Turtle Project of the Western Australian Marine Science Institution (WAMSI) collaborated with 11 Indigenous groups to plan and conduct field studies on nesting turtles across the Kimberley. Indigenous rangers brought deep local knowledge to the partnership. The collaborative framework was consistent with current approaches used by the Department of Biodiversity, Conservation and Attractions (DBCA) to jointly manage marine parks and by the Commonwealth to collaborate on Indigenous Protected Areas. The WAMSI work included ranger training, longterm monitoring of population trends, and the introduction of scientific methods to traditional owners. The concurrent activities of WAMSI research, the development of the marine parks and the recently formed Indigenous Protected Areas meant that many lines of communication developed between Indigenous and non-Indigenous groups. The partners communicated informally during field trips on Country and other activities, such as marine park patrols, and formally through other WAMSI projects (such as the Kimberley Indigenous Saltwater Science Project), meetings, community feedback sessions and symposia (for example, the Australian Marine Turtle Symposium). This two-way communication enabled us to share knowledge and develop a mutual understanding of the distribution, abundance and timing of turtle movements. An effective blending of culture and science required us to place the management interests of local traditional owners in the larger context of the Kimberley’s landscape across multiple Indigenous groups. After initial consultation with local groups, our efforts to build knowledge about Kimberley sea turtles began with an inventory of the region’s beaches. By determining when and where each species nests, we could identify sites of significance.
NESTING HABITAT INVENTORY A standard method in beach surveys of breeding turtle populations is to count the tracks left behind by nesting females.16 We do so by walking along the beach, dragging a stick above the high-tide line to establish a reference line in the sand. The next morning, we count all the turtle tracks that crossed the line overnight (one up and one back). We distinguish nesting emergence from any non-nesting emergence by looking for the excavated sand that marks a nest. We can tell the turtle species by looking carefully at the tracks, especially the tail and flipper marks, their width, and how the sand was moved (Fig. 4). We repeat the process each morning to count the new tracks. A minimum of 14 days is needed to encompass the inter-nesting interval – that is, the time until females return to lay another clutch of eggs. This study duration also averages out the highs and lows in nesting numbers, which are influenced by tidal variation and weather. Not every emergence results in a nest; if a turtle encounters unfavourable conditions, such as dry
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sand, which tends to collapse a nest excavation, or if she is ‘picky’ or easily scared, she may leave the beach to try again later. Data from the 14-day surveys are extrapolated to the entire nesting season to estimate female breeding numbers. This low-tech, reliable approach can be enhanced by high-tech methods if the survey location is accessible by camera traps, drone flights or aerial surveys (Fig. 5). We conducted studies at a selection of major rookeries, including Eighty Mile Beach for summer-nesting flatbacks, Cape Domett for winter-nesting flatbacks and Lacepede Islands for summer-nesting green turtles. Cape Domett is an interesting case study because of the huge
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variation in the nest numbers each night: from as few as two to over 200 emergences a night during the two-week studies (Fig. 6). Flatbacks generally nest between sunset and sunrise, but the height of the tide, the time of high tide, and lunar illumination all exert an influence, with turtles favouring the darkest nights and highest spring tides. If high tides occur in the late afternoon or after dawn, there may be a few daytime nesters (Fig. 7). The Kimberley coast includes 2633 islands and 1375 mainland beaches across thousands of kilometres of shoreline. Acceptable nesting beaches of silica sand can vary in size from a tiny 100 m pocket beach up to Eighty Mile Beach. Before the WAMSI research, surveys were conducted by plane, helicopter or boat, or on foot, during oil and gas explorations, but these were temporally or spatially restricted to areas of industrial interest. Nevertheless, these surveys recognised that the Kimberley had winter and summer nesting seasons – although there was considerable uncertainty about where the seasons and spatial boundaries overlapped.
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The WAMSI study used aerial surveys of the entire Kimberley region as a snapshot of nesting abundance and density at the nesting midseason in both summer and winter (Fig. 8). The study offered the first complete regional inventory of the major rookeries and species in the area, albeit only within the survey time window. The aerial images were compared to ground truth surveys at selected sites (which were conducted by traditional owners, Indigenous and DBCA rangers, and scientists) to interpret the photos for species identification, nests and non-nesting emergences. This was an important verification and validation step, as aerial survey cameras at 150 m altitude could miss details that were evident to personnel at ground level.
Figure 6 (opposite, top) Cape Domett hosts a winter-nesting rookery with a high density of flatback turtles. Photo: Tony Tucker / DBCA
For eight days during midsummer and again in midwinter, we flew over nesting beaches with a downward-aimed digital camera mounted beneath the plane. The camera captured 45,000 digital geo-referenced images along approximately 91% of the entire length of Kimberley coast. Some isolated or smaller islands were missed, but the survey encompassed all the previously known major rookeries. We reviewed the images at high magnification and tallied the number of tracks. The detail obtained from aerial surveys depended on flight altitude, the timing of the most recent high tide, the angle of the sun in winter and summer, sun glare and smoke haze, pixel resolution, image overlap and camera refresh rates. In addition to observing the tracks and nests of adult turtles, we identified hatchling tracks and mature turtles, and recorded wildlife observations that included humpback whales, crocodiles, and signs of hatched or depredated nests.
Figure 8 (this page) An overhead image from the WAMSI aerial surveys documents the turtle nesting on a remote Kimberley beach. Photo: Kellie Pendoley / WAMSI
Figure 7 (opposite, bottom) A flatback female nesting by day usually coincides with a late afternoon high tide. Photo: Tony Tucker / DBCA
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From these analyses, we discovered the Dampier Peninsula to be a clear spatial boundary for flatback turtles. The aerial surveys delineated that summer-nesting flatbacks use beaches south of the peninsula, whereas winter-nesting flatbacks used beaches east of the peninsula. Summernesting green turtles were spread across the region, from Lacepede Islands eastward into the Kimberley. The aerial surveys indicated that all species of marine turtle might use almost any patch of sand on any little beach in the Kimberley, although green turtles predominated on offshore islands, with flatbacks on the mainland beaches and nearer islands. To better inform management in the Kimberley landscape, we measured track density to identify beaches that were heavily used by turtle species (Fig. 9). Beaches at the low end of the scale might be informative, but they are hard to monitor consistently. Similarly, beaches at the high end of the scale can be difficult to monitor because of overlapping tracks. However, these beaches may still be important sites to monitor if they fit the priorities of DBCA management or Healthy Country Plans. Some intermediate beaches, with medium densities of tracks, could be appropriate sites for monitoring, but the final decision also hinges on the costs of travel and personnel (which might be mitigated by volunteer efforts; Fig. 10). In the Kimberley, WAMSI conducted 44 field trips with 11 traditional owner groups to integrate valuable local knowledge about sea turtles in saltwater Country. Together, we shared new knowledge on the species, rookery locations, fidelity to nesting sites, migration, breeding season, re-migration intervals, eggs, predation on hatchlings, egg and hatching survivorship, hatchling sex ratio, genetics and track counts.
Figure 9 (top) Dambimangari ranger Jermaine Umbagai and DBCA ranger Danny Barrow take measurements of a green turtle’s nesting track. Photo: Tony Tucker / DBCA
Although our collaboration was productive, we recognised limitations in the studies and identified areas for potential improvement in future studies. WAMSI’s focus was restricted to nesting beaches, which are clearly a critical terrestrial link in sea turtle reproduction. However, what happens in the other 99% of the turtles’ life cycle in marine habitats remains poorly understood for the Kimberley and poses a different set of questions to those addressed by this project.
Figure 10 (bottom) The Cable Beach Turtle Volunteers assist in satellite tagging a flatback turtle. Photo: Tony Tucker / DBCA
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Sea turtles in Australia comprise several genetically diverse populations, which arise because of their fidelity to breeding sites. Determining how best to conserve each species and its genetic diversity relies on understanding these genetic differences and their implications.17
groups. It is now possible to identify distinct turtle populations in the region, determine how they are distributed, and thus understand what unique threats they may face.11
Researchers took small skin biopsies from turtles whenever possible at all rookeries in the Kimberley. DNA analyses of these samples indicate the extent of genetic similarity within and between rookeries and provide a means of defining groups of rookeries as populations or management
Prior to WAMSI’s research, genetic studies of flatback turtles sampled only the spatial extremes of Cape Domett and the Pilbara. The populations at these distant sites were recognised as genetically distinct, but there were too few samples from Kimberley sites in between to
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determine if other, unrecognised subpopulations existed. With many new samples now available from the WAMSI study, three new stocks of flatbacks have been discovered along the Kimberley coast. Similarly, an expanded set of Kimberley samples enabled us to distinguish the Pilbara and Kimberley as regionally distinct rookeries for green turtles in Western Australia. Major genetic boundaries between flatback populations have now been defined for the Pilbara and subregions within the west Kimberley and the north Kimberley.
CLIMATE CHANGE INVENTORY
Figure 11 (top) DBCA regional ecologist Ben Corey installs a weather station at Cape Domett to collect data for climate change models. Photo: Tony Tucker / DBCA Figure 12 (opposite) A flatback hatchling crosses the tide wash zone of Eighty Mile Beach Marine Park. Photo: Scott Whiting / DBCA
As the life history of turtles is highly dependent on their environment, climate change has the potential to severely impact turtle populations, particularly at the life stage when embryos develop on beaches.18 To understand how climate change might affect sea turtles in the Kimberley, we combined climate-change predictions, environmental data such as sand and air temperatures, and population-specific physiological thresholds for each turtle population into a mechanistic model. The physiological thresholds included the pivotal temperature at which equal proportions of male and female hatchlings are produced and the upper thermal limits that embryos can survive. As part of our research, we collected a few hundred eggs from turtles nesting at remote Kimberley rookeries. The eggs were cooled to 10 °C for safer transport of the developing embryos to an incubation lab at the University of Western Australia. The eggs were incubated at a range of temperatures and allowed to hatch, which is an ideal time to determine the sex of individuals by studying their internal reproductive organs. We used temperature loggers to record temperatures on the nesting beaches for up to one year, and we compared these data against modelled temperatures to determine the reliability of the models for predicting beach temperatures under current and future climates. We also installed temporary weather stations on key nesting beaches across the Kimberley, including Eighty Mile Beach, the Lacepede Islands, Deception Bay, Vansittart Bay, Cassini Island and Cape Domett, for periods ranging from months to years (Fig. 11). The collected data were used as inputs for models that predict the effects of climate on hatchling sex ratios and mortality over the coming century. Although our results are still preliminary, we discovered that there is a substantial difference in the pivotal temperature between summer- and winter-nesting populations of flatback turtles, with the summer-nesting turtles at Eighty Mile Beach having a higher threshold than the winternesting turtles at Cape Domett. We also found that green turtles are likely to produce more mixed-sex nests than flatback turtles. These differences, when coupled with the local variation in beach temperatures, show that populations of sea turtles will be differentially affected by the increasing
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Figure 13 (left) DBCA rangers for Eighty Mile Beach Marine Park supervise the setup of a satellite transmitter attached to a flatback turtle. Photo: Tony Tucker / DBCA Figure 14 (right) Tracking juvenile flatbacks helps to understand their developmental habitats. Photo: Scott Whiting / DBCA Figure 15 (opposite, top) Cross-sections of a turtle’s arm bone shows growth rings (denoted by yellow lines). Photo: Larisa Avens / National Marine Fisheries Service Figure 16 (opposite, bottom) A flatback hatchling is twice the size of other WA turtle hatchlings. Photo: Scott Whiting / DBCA
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temperatures associated with anthropogenic climate change. Winternesting populations of flatback turtle are particularly vulnerable to these effects, as the only way for them to respond to increasing incubation temperatures is to adjust their physiological thresholds, as they are already nesting at the coolest time of year. This contrasts with summernesting populations, which can feasibly shift their nesting to a cooler time of year – a potentially faster way to respond to climate change than physiological evolution. Perhaps most worryingly, predicted temperatures for beaches in the northern Kimberley will regularly exceed the upper thermal limits of developing embryos, so we expect to see more eggs die in their nests there.
THE KNOWN UNKNOWNS Many of the unanswered questions about Kimberley sea turtles require novel methods – developed through inventing, adapting and validating new technologies. We are currently working on several initiatives that are showing promise. To understand and manage sea turtles, it is vital to know where they are before, during and after their time at the nesting beaches.19 However, except for hatchlings and females at a nesting beach, flatback turtles are essentially invisible to humans (Fig. 12). We know little about the species’ location, activity, lifestyle or behaviour. Some of these characteristics can be studied if we track the turtles using satellite telemetry.20 Satellite transmitters are commonly epoxied to the shell of most turtles, but that doesn’t work for the flatback turtle’s soft skin covering. Instead, we attach the transmitter to a plate and strap the plate around the turtle (Fig. 13). The plate eventually falls off, hopefully after plenty of data have been received (Fig. 14).
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In addition to tracking the turtles’ movements, we are addressing questions such as how old they are at given sizes, what they feed on, and how they respond to environmental changes. The period from hatchling stage to adult maturity for flatback turtles is believed to be 20 years or more, based on studies of a flatback turtle in Queensland. To determine age more precisely, we use a method known as skeletochronology, which counts the growth layers in hard tissue. Bones such as the humerus (arm bone) reveal a reliable and consistent pattern of annual growth rings in most vertebrates.21 We collected bones from turtle specimens in the Western Australian, Northern Territory and Queensland museums and from dead stranded turtles, and sent them to a laboratory that specialises in preparing bones for microscopic examination to determine bone layer patterns (Fig. 15). These bone specimens might also tell us about the turtles’ diets, which in turn can indicate where they lived. By comparing the chemical signatures of stable isotopes (such as carbon and nitrogen ratios) in inner (younger) and outer (older) growth rings, we can find out if diets change as the turtles grow and possibly shift habitats. Levels of nitrogen isotopes can distinguish vegetarians from carnivores, while carbon isotopes can separate near-shore residents from offshore dwellers.22 We have focused our analyses on satellite-tracked turtles20, because their migrations were verified from nesting to known foraging grounds. Data on foraging grounds can then be correlated with nesting-related reproduction data, such as the body size, sex, clutch size and hatchling survival rate (Fig. 16). Understanding more about sea turtles’ reproductive behaviour and how it is affected by their environment is essential for identifying and conserving crucial turtle habitats.
A LARGE-SCALE, LONG-TERM ENDEAVOUR Research on sea turtles in the Kimberley is important not only for furthering scientific knowledge but also in planning better management of these species. We have made good progress, but much work remains. For example, local Indigenous managers and government management agencies need to foster and support ranger groups that address issues like marine debris or dingo predation at local scales. We need to establish index beaches to follow trends in nesting populations by region. We also need to continue studying turtle populations regularly – ideally each year for at least a decade at a time. Just like the sea turtles’ lifestyle, turtle monitoring is a large-scale, long-term endeavour. Welcome to life in the slow lane.
Acknowledgments
Kelly Waples and Stuart Field coordinated the Kimberley Node of WAMSI. We thank the Miriuwung-Gajerrong, Balanggarra, Wunambal Gaambera, Dambimangari, Mayala, Bardi Jawi, Nyul Nyul, Yawuru, Karajarri, Nyangumarta and Ngarla traditional owners for work approved of and conducted on their lands and for their collaboration in these efforts. Rob Ryan piloted the Kimberley flights. Key individuals who facilitated surveys included Trent Stillmann, Ben Corey, Luke Bentley, James Gallagher, Clement Maraltadj, Tom Nagle, Tom Vigilante, Robert Warren, Jeremy Kowan, Desmond Williams, Neil Waina, Darren Stephens, Danny Barrow, Adrian Lane, Jarrod Holmes, Phillip McCarthy, Daniel Oades, Kevin George, Mark Rothery, Albert Wiggan, Alan Byrne, Craig Olejnik, Leah Pearson, Andre Bobojcov, Erina Young, Craig Williams, Adrian Ferguson, Nathan Kay, Augustine Badal, Nathan Hunter, Jeffrey Brown, Stephen Brown, Rhys Swain, Ewan Noakes, Dean Mathews, Chris Nutt and Sarah Mullineux. For assistance with image photo-stitching and pre-flight planning, we thank Kathy Murray, Jai Denda, Chris Barber and Graham Loewenthal. Special recognition goes to Daryl Moncrieff for the Kimberley Science and Conservation Strategy and its resources directed to training Indigenous rangers.
Photo: Corrine Douglas / DBCA
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21. Avens L, Snover ML. Age and age estimation in sea turtles. In: Wyneken J, Lohman KJ, Musick JA, eds. The biology of sea turtles. Volume III. Boca Raton: CRC Press, 2013;97– 133. 22. Jones TT, Seminoff JA. Feeding biology: advances from field-based observations, physiological studies, and molecular techniques. In: Wyneken J, Lohman KJ, Musick JA, eds. The biology of sea turtles. Volume III. Boca Raton: CRC Press, 2013;211– 47.
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