- The University of Western Australia, School of Animal Biology, Faculty Memberadd
- I am a zoologist.edit
Research Interests: Demography, Climate Change, Conservation Biology, Biology, Ecology, and 15 morePhenology, Endangered Species, Medicine, Biological Sciences, Colonization, Environmental Sciences, Reptiles, Animals, New Zealand, Translocation, Introduced species, Threatened Species, Genetic variation, Conservation of Natural Resources, and Socioeconomic Factors
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Ex situ (‘off‐site’) management refers to keeping species in artificial conditions away from their natural habitat and includes captive breeding facilities, botanical gardens and seed banks. There is scope for ex situ programmes to be... more
Ex situ (‘off‐site’) management refers to keeping species in artificial conditions away from their natural habitat and includes captive breeding facilities, botanical gardens and seed banks. There is scope for ex situ programmes to be more commonly used for supplementing or establishing wild populations. However, undertaking ex situ management comes with risks, costs and uncertainties, which must be assessed in the context of available in situ (‘on‐site’) management options. The PACES (Planning and Assessment for Conservation through Ex situ management) tool tailors the principles of structured decision‐making to the specific problem of assessing and comparing ex situ and in situ management options. We applied the PACES tool to the mahogany glider (Petaurus gracilis), a threatened arboreal marsupial endemic to north Queensland, Australia. Through an expert elicitation process, we predicted the likely benefits of an ex situ and two in situ management options, as compared to a baselin...
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In the face of the current global extinction crisis, it is critical we give conservation management strategies the best chance of success. Australia is not exempt from global trends with currently the world’s greatest mammal extinction... more
In the face of the current global extinction crisis, it is critical we give conservation management strategies the best chance of success. Australia is not exempt from global trends with currently the world’s greatest mammal extinction rate (~ 1 per 8 years). Many more are threatened including the dibbler (Parantechinus apicalis) whose remnant range has been restricted to Western Australia at just one mainland site and two small offshore islands—Whitlock Island (5 ha) and Boullanger Island (35 ha). Here, we used 14 microsatellite markers to quantify genetic variation in the remaining island populations from 2013 to 2018 and incorporated these data into population viability analysis (PVA) models, used to assess factors important to dibbler survival and to provide guidance for translocations. Remnant population genetic diversity was low (< 0.3), and populations were highly divergent from each other (pairwise FSTs 0.29–0.52). Comparison of empirical data to an earlier study is consi...
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Additional file 4. ROSES checklist.
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Until recently, the reptile fauna of Christmas Island in the Indian Ocean comprised five endemic species (two skinks, two geckos, and one snake) and one native, non‐endemic skink. Four of these species were common and widespread until at... more
Until recently, the reptile fauna of Christmas Island in the Indian Ocean comprised five endemic species (two skinks, two geckos, and one snake) and one native, non‐endemic skink. Four of these species were common and widespread until at least 1979, but by 2012 had disappeared from the wild. During the years of decline, little research was undertaken to examine why the species were disappearing. Here, we use a retrospective expert elicitation to rank potential factors that contributed to the loss of Christmas Island's reptiles and to assess the likelihood of re‐establishing populations of two species now listed as Extinct in the Wild. We additionally considered why one endemic lizard, the Christmas Island giant gecko (Cyrtodactylus sadleiri), and three introduced lizards remain common. Experts considered that the introduced common wolf snake (Lycodon capucinus) was the most likely cause of decline, as its temporal and spatial spread across the island closely matched patterns of ...
Research Interests: Geography, Ecology, Fauna, Squamata, Extinction, and 3 moreChristmas Island, Lizard, and Expert Elicitation
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Quantifying organismal sensitivity to heat stress provides one means for predicting vulnerability to climate change. Birds are ideal for investigating this approach, as they display quantifiable fitness consequences associated with... more
Quantifying organismal sensitivity to heat stress provides one means for predicting vulnerability to climate change. Birds are ideal for investigating this approach, as they display quantifiable fitness consequences associated with behavioural and physiological responses to heat stress. We used a recently developed method that examines correlations between readily‐observable behaviours and air temperature (Tair) to investigate interspecific variation in avian responses to heat stress in seasonally hot, arid regions on three continents: the southwestern United States, the Kalahari Desert of southern Africa and the Gascoyne region of western Australia. We found substantial interspecific variation in heat dissipation behaviours (wing‐drooping, panting, activity‐reduction, shade‐seeking) across all three regions. However, pooling the data revealed that little of this interspecific variation was systematically explained by organismal traits (foraging guild, diet, drinking dependency, bod...
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Terrestrial‐breeding amphibians are likely to be vulnerable to warming and drying climates, as their embryos require consistent moisture for successful development. Adaptation to environmental change will depend on sufficient genetic... more
Terrestrial‐breeding amphibians are likely to be vulnerable to warming and drying climates, as their embryos require consistent moisture for successful development. Adaptation to environmental change will depend on sufficient genetic variation existing within or between connected populations. Here, we use Single Nucleotide Polymorphism (SNP) data to investigate genome‐wide patterns in genetic diversity, gene flow and local adaptation in a terrestrial‐breeding frog (Pseudophryne guentheri) subject to a rapidly drying climate and recent habitat fragmentation. The species was sampled across 12 central and range‐edge populations (192 samples), and strong genetic structure was apparent, as were high inbreeding coefficients. Populations showed differences in genetic diversity, and one population lost significant genetic diversity in a decade. More than 500 SNP loci were putatively under directional selection, and 413 of these loci were correlated with environmental variables such as tempe...
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Reptile populations are in decline globally, with total reptile abundance halving in the past half century, and approximately a fifth of species currently threatened with extinction. Research on reptile distributions, population trends,... more
Reptile populations are in decline globally, with total reptile abundance halving in the past half century, and approximately a fifth of species currently threatened with extinction. Research on reptile distributions, population trends, and trophic interactions can greatly improve the accuracy of conservation listings and planning for species recovery, but data deficiency is an impediment for many species. Environmental DNA (eDNA) can detect species and measure community diversity at diverse spatio‐temporal scales, and is especially useful for detection of elusive, cryptic, or rare species, making it potentially very valuable in herpetology. We aim to summarize the utility of eDNA as a tool for informing reptile conservation and management and discuss the benefits and limitations of this approach. A literature review was conducted to collect all studies that used eDNA and focus on reptile ecology, conservation, or management. Results of the literature search are summarized into key discussion points, and the review also draws on eDNA studies from other taxa to highlight methodological challenges and to identify future research directions. eDNA has had limited application to reptiles, relative to other vertebrate groups, and little use in regions with high species richness. eDNA techniques have been more successfully applied to aquatic reptiles than to terrestrial reptiles, and most (64%) of studies focused on aquatic habitats. Two of the four reptilian orders dominate the existing eDNA studies (56% Testudines, 49% Squamata, 5% Crocodilia, 0% Rhynchocephalia). Our review provides direction for the application of eDNA as an emerging tool in reptile ecology and conservation, especially when it can be paired with traditional monitoring approaches. Technologies associated with eDNA are rapidly advancing, and as techniques become more sensitive and accessible, we expect eDNA will be increasingly valuable for addressing key knowledge gaps for reptiles.
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The value of assisted colonisation as a response to climate change can only be realised if focal species are well suited to their new habitats. For ectotherms, new habitats must offer microclimates that promote crucial behaviours such as... more
The value of assisted colonisation as a response to climate change can only be realised if focal species are well suited to their new habitats. For ectotherms, new habitats must offer microclimates that promote crucial behaviours such as thermoregulation and foraging. The Western swamp turtle Pseudemydura umbrina, a Critically Endangered species from south‐western Australia, serves as a global case‐study of assisted colonisation in action. Initial trials where juvenile P. umbrina were released into wetter and cooler climates found that individuals spent considerable time at body temperatures that apparently limited their growth. Using high‐resolution biologging data (temperature and depth), here we tested if turtle activity is thermally constrained in cooler latitudes by releasing 48 juveniles into seasonal swamps at three sites. One site was core natural habitat, and the other sites were wetlands 380 km apart that offered either warmer or cooler microclimates. Generalised additive ...
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Comprehensive assessments of species’ extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and... more
Comprehensive assessments of species’ extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction3. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods4–7. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs6. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened—confirming a previous extrapolation8 and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods—agriculture, logging, urban development and invasive species—although the threat posed by climate change remains uncertain. Re...
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Many Australian mammal species are highly susceptible to predation by introduced cats (Felis catus) and European red foxes (Vulpes vulpes). At least 34 Australian endemic mammal species have been made extinct since 1788, about 10% of... more
Many Australian mammal species are highly susceptible to predation by introduced cats (Felis catus) and European red foxes (Vulpes vulpes). At least 34 Australian endemic mammal species have been made extinct since 1788, about 10% of Australia’s terrestrial mammal. Predation by introduced cats and foxes was a major contributor to most of those extinctions. The Australian mammal extinctions make up about one-third of all global mammal extinctions over the last ca. 500 years. Cats and foxes have also driven large distributional and population declines for many more surviving species. Cats now occur across the entire Australian mainland and Tasmania, and are present on many of the larger islands.
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Background Mammals, globally, are facing population declines. Strategies increasingly employed to recover threatened mammal populations include protecting populations inside predator-free havens, and translocating animals from one site to... more
Background Mammals, globally, are facing population declines. Strategies increasingly employed to recover threatened mammal populations include protecting populations inside predator-free havens, and translocating animals from one site to another, or from a captive breeding program. These approaches can expose predator-naïve animals to predators they have never encountered and as a result, many conservation projects have failed due to the predation of individuals that lacked appropriate anti-predator responses. Hence robust ways to measure anti-predator responses are urgently needed to help identify naïve populations at risk, to select appropriate animals for translocation, and to monitor managed populations for trait change. Here, we outline a protocol for a systematic review that collates existing behavioural assays developed for the purpose of quantifying anti-predator responses, and identifies assay types and predator cues that provoke the greatest behavioural responses. Methods...
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Drier and hotter conditions caused by climate change threaten species that exist close to their physiological limits, as well as those with limited ability to move. Habitat specialists may also be particularly vulnerable if they have... more
Drier and hotter conditions caused by climate change threaten species that exist close to their physiological limits, as well as those with limited ability to move. Habitat specialists may also be particularly vulnerable if they have specific abiotic requirements. Here we assess whether thermal and hydric constraints can explain the highly restricted and declining distributions of the critically endangered terrestrial-breeding frog, Geocrinia alba. We also evaluate the species’ vulnerability to climate change based on the similarity of current microclimatic conditions to their physiological limits. We found that G. alba had low thresholds of thermal and desiccation tolerance relative to other anuran species. The estimated thermal optimum (Topt) and critical thermal maxima (CTmax) were 23.3°C and 29.6°C, respectively, and adult frogs had an absorption threshold (AT, the lowest water potential at which water can be absorbed from a substrate) of −50 kPa, the lowest recorded for an amph...
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Defining species habitat requirements is essential for effective conservation management through revealing agents of population decline and identifying critical habitat for conservation actions, such as translocations. Here we studied the... more
Defining species habitat requirements is essential for effective conservation management through revealing agents of population decline and identifying critical habitat for conservation actions, such as translocations. Here we studied the habitat-associations of two threatened terrestrial-breeding frog species from southwestern Australia, Geocrinia alba and Geocrinia vitellina, to investigate if fine-scale habitat variables explain why populations occur in discrete patches, why G. alba is declining, and why translocation attempts have had mixed outcomes. We compared habitat variables at sites where the species are present, to variables at immediately adjacent sites where frogs are absent, and at sites where G. alba is locally extinct. Dry season soil moisture was the most important predictor of frog abundance for both species, and explained why G. alba had become extinct from some areas. Sites where G. alba were present were also positively associated with moss cover, and negatively...
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More than a third of the world’s amphibian species are listed as Threatened or Extinct, with a recent assessment identifying 45 Australian frogs (18.4% of the currently recognised species) as ‘Threatened’ based on IUCN criteria. We... more
More than a third of the world’s amphibian species are listed as Threatened or Extinct, with a recent assessment identifying 45 Australian frogs (18.4% of the currently recognised species) as ‘Threatened’ based on IUCN criteria. We applied structured expert elicitation to 26 frogs assessed as Critically Endangered and Endangered to estimate their probability of extinction by 2040. We also investigated whether participant experience (measured as a self-assigned categorical score, i.e. ‘expert’ or ‘non-expert’) influenced the estimates. Collation and analysis of participant opinion indicated that eight species are at high risk (>50% chance) of becoming extinct by 2040, with the disease chytridiomycosis identified as the primary threat. A further five species are at moderate–high risk (30–50% chance), primarily due to climate change. Fourteen of the 26 frog species are endemic to Queensland, with many species restricted to small geographic ranges that are susceptible to stochastic e...
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Australia hosts approximately 10% of the world’s reptile species, the largest number of any country. Despite this and evidence of widespread decline, the first comprehensive assessment of the conservation status of Australian terrestrial... more
Australia hosts approximately 10% of the world’s reptile species, the largest number of any country. Despite this and evidence of widespread decline, the first comprehensive assessment of the conservation status of Australian terrestrial squamates (snakes and lizards) was undertaken only recently. Here we apply structured expert elicitation to the 60 species assessed to be in the highest IUCN threat categories to estimate their probability of extinction by 2040. We also assessed the probability of successful reintroduction for two Extinct in the Wild (EW) Christmas Island species with trial reintroductions underway. Collation and analysis of expert opinion indicated that six species are at high risk (>50%) of becoming extinct within the next 20 years, and up to 11 species could be lost within this timeframe unless management improves. The consensus among experts was that neither of the EW species were likely to persist outside of small fenced areas without a significant increase ...
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Distributions of Earth's species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural... more
Distributions of Earth's species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation's Sustainable Development Goals.
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Abstract The embryos of many egg-laying species develop under the environmental conditions selected by one or both parents, and these conditions may cease to be optimal under a changed climate. Assisted colonization is an emerging option... more
Abstract The embryos of many egg-laying species develop under the environmental conditions selected by one or both parents, and these conditions may cease to be optimal under a changed climate. Assisted colonization is an emerging option to relocate species that are threatened by unfavourable changes in the local climate, but the incubation requirements of embryos are rarely considered in conservation translocations despite suggestions that relocation of early life stages could be more effective than relocating older animals. Here we review examples and outcomes of relocations of reptile eggs, and the decision tools currently available for guiding translocation decisions from an embryonic perspective. We then demonstrate a mechanistic approach, using the modelling framework NicheMapR, for assessing the optimal translocation range for the Western Swamp Turtle ( Pseudemydura umbrina ), a Critically Endangered reptile with an extremely restricted natural distribution. We determine thermal reaction norms and critical thermal limits for embryonic development based on laboratory and field data, and model soil temperatures at typical nest depths, simulate embryonic development at these depths, and map the probability of survival of P. umbrina embryos within the major bioregions of south-western Australia. The same model forced by future climates for 2050–70 demonstrates a southerly shift in the regions where embryos would be viable. However, if P. umbrina is to be translocated in the near future to regions 300–400 km south of its natural range, females will need to nest in relatively unshaded sites to achieve temperatures that are high enough to promote hatchling success.
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Contemporary declines of marine turtle populations are expected to be exacerbated through a number of processes associated with anthropogenic climate change. A rapid increase in ambient temperatures will adversely impact all life history... more
Contemporary declines of marine turtle populations are expected to be exacerbated through a number of processes associated with anthropogenic climate change. A rapid increase in ambient temperatures will adversely impact all life history stages of marine turtles, with the embryonic stage being the most vulnerable due to narrow physiological thresholds and their inability to avoid excess heat during incubation. Incubation temperatures now often occur close to the upper thermal limits of the embryo. Further, incubation temperatures are important drivers of population demography, as marine turtles have a temperature-dependent mechanism of sex determination (TSD), where females are produced at warmer temperatures and males are produced at cooler temperatures (type-MF TSD). As a consequence, increasing temperatures have been predicted to lead to rookery feminization and increased embryonic mortality, and this is already being observed at many marine turtle rookeries within and outside of...
Supplementary Methods and Figures;Data file
The file contains Single Nucleotide Polymorphism (SNP) data for each individual from the sympatric species (Pseudophryne occidentalis) and the novel species studied
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Ejaculate traits vary extensively among individuals and species, but little is known about their variation among populations of the same species. Here, we investigated patterns of intraspecific variation in male reproductive investment in... more
Ejaculate traits vary extensively among individuals and species, but little is known about their variation among populations of the same species. Here, we investigated patterns of intraspecific variation in male reproductive investment in the terrestrial-breeding frog Pseudophryne guentheri . Like most anurans, breeding activity in P. guentheri is cued by precipitation, and therefore the timing and duration of breeding seasons differ among geographically separated populations, potentially leading to differences in the level of sperm competition. We, therefore, anticipated local adaptation in sperm traits that reflect these phenological differences among populations. Our analysis of six natural populations across a rainfall gradient revealed significant divergence in testes and ejaculate traits that correspond with annual rainfall and rainfall seasonality; males from the northern and drier edge of the species range had significantly smaller testes containing fewer, smaller and less m...
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ABSTRACTIntra-specific variation in the ability of individuals to tolerate environmental perturbations is often neglected when considering the impacts of climate change. Yet this information is potentially crucial for mitigating any... more
ABSTRACTIntra-specific variation in the ability of individuals to tolerate environmental perturbations is often neglected when considering the impacts of climate change. Yet this information is potentially crucial for mitigating any deleterious effects of climate change on threatened species. Here we assessed patterns of intra-specific variation in desiccation tolerance in the frogPseudophryne guentheri, a terrestrial-breeding species experiencing a drying climate. Adult frogs were collected from six populations across a rainfall gradient and their dehydration and rehydration rates were assessed. We also compared desiccation tolerance of embryos and hatchlings originating from within-population parental crosses from four of the six populations, where selection on desiccation tolerance should be especially strong given that embryos cannot move to escape unfavourable microclimates. Embryos were reared on soil at three soil-water potentials, ranging from wet to dry (ψ = −10, −100 & −40...
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Assisted colonisation - the translocation of organisms with release in areas outside their indigenous range in response to threats such as climate change - was presented in the scientific literature only a few years ago as a new tool for... more
Assisted colonisation - the translocation of organisms with release in areas outside their indigenous range in response to threats such as climate change - was presented in the scientific literature only a few years ago as a new tool for species conservation. The idea of planned introductions for conservation is a controversial issue, prompting vigorous, and sometimes ill-informed, debate in the scientific literature. The broad consensus wa that this represented a bold new direction that had merit but carried great risk. Unacknowledged by most commentators, assisted colonisation (by other names) was already taking place, and in Australia and New Zealand was even a long-accepted part of the conservation management tool kit. In 2013, the IUCN recognised assisted colonisation as a legitimate, if inherently risky conservation translocation, and set out a comprehensive set of guidelines for its application. We review the history of assisted colonisalion, with a focus on Australia and New...
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The thermal environment of sea turtle embryos has marked effects on many aspects of their development and energetics and has consequences for posthatching stages. Here we incubated Chelonia mydas embryos from Ningaloo Reef in Western... more
The thermal environment of sea turtle embryos has marked effects on many aspects of their development and energetics and has consequences for posthatching stages. Here we incubated Chelonia mydas embryos from Ningaloo Reef in Western Australia at a range of temperatures (27°, 29°, 30°, 31°, 32°, and 30° ± 5°C) to determine development rates and the pivotal temperature for sex determination. We also measured embryonic growth, oxygen consumption, and carbon dioxide production throughout development at 27° and 31°C. Metabolic rates were higher at 31°C than at 27°C, but total energy expenditure was greater at 27°C, with 2,281 mL of oxygen consumed compared with 1,992 mL at 31°C. Respiration at both temperatures showed a pattern typical of sea turtle embryos, with peak rates occurring at approximately 85% of development and then declining toward hatching. Hatchlings produced at higher incubation temperatures developed faster, were smaller, and had larger residual yolk masses than hatchlings produced at lower temperatures. The pivotal temperature that produced an equal sex ratio was 29.2°C, with mixed sexes produced between 27.9° and 30.4°C. Our results showed that the Ningaloo population of C. mydas has somewhat different thermal sensitivities than other C. mydas populations and justified why is it necessary to collect population-specific data to accurately project the impacts of global warming on focal populations.
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The conservation of highly mobile species presents challenges to managers for assessment of threats to survival, given the difficulties in locating and observing such species. Here we evaluate satellite telemetry, DNA faecal metabarcoding... more
The conservation of highly mobile species presents challenges to managers for assessment of threats to survival, given the difficulties in locating and observing such species. Here we evaluate satellite telemetry, DNA faecal metabarcoding and traditional field observations as three complementary techniques to acquire critical management information for an endangered species, Carnaby's Cockatoo Calyptorhynchus latirostris. Satellite telemetry of 23 birds resulted in 6026 location fixes accurate to within 500 m, and combined with extensive field observations and DNA faecal metabarcoding resulted in a more detailed understanding of how this species survives in an urbanised landscape. We identified 168 night roosts, 75% of which were previously unknown, which will contribute towards a more accurate population size estimate based on annual counts of roosting birds. We also determined the scale of daily movements (morning 5.4 ± 3.4 km from roost, afternoon 5.5 ± 3.3 km to roost; maximum distance between consecutive roosts 69.7 km) and the size of foraging areas around roosts (range 17 to 276 km2), and identified dependence on a variety of native and exotic food sources. Field observations identified 11 food-plant families, but combined with DNA faecal metabarcoding this was extended to 21 food-plant families. The three techniques were compared to assess their individual and collective values. By combining spatial ecology information from satellite telemetry with ecological knowledge from field observation and DNA faecal analysis, we gained deeper insights into the ecology of the species than would have been possible from any one technique alone. This information will lead to more strategic conservation planning to allow this species to persist within a rapidly expanding urban environment
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Nest microclimates influence embryonic development and survival in many lineages, including reptiles with temperature-dependent sex determination. These microclimates are dependent on physical drivers and biological processes, such as... more
Nest microclimates influence embryonic development and survival in many lineages, including reptiles with temperature-dependent sex determination. These microclimates are dependent on physical drivers and biological processes, such as embryonic metabolism, that generate heat. The flatback turtle (Natator depressus) has among the largest hatchlings of the seven extant sea turtle species, making it an excellent candidate for quantifying the contribution of embryonic metabolism to the nest microclimate. Consequently, we measured embryonic metabolic rates, development rates, and the relationship between temperature and sex determination for a N. depressus population nesting at Cemetery Beach in Western Australia, a mainland beach characterized by high sand temperatures. Total oxygen consumed at 29.5°C during an average 52-d incubation period was 2,622 mL, total carbon dioxide produced was 1,886 mL, and estimated embryonic heat production reached 38 mW at 90% of development. Adjustment of metabolic rates to 32°C and 34°C increased peak heat production by 18% and 27%, respectively. The pivotal temperature (TPIV) producing an equal sex ratio was 30.3°C, mixed sexes were produced between 29.3°C and 31.2°C, and only females were produced above 31.2°C. The TPIV was similar (within 0.2°C) to that of an island rookery within the same genetic stock (North West Shelf), but the peak development rate (2.5% d−1) was estimated to be achieved at a temperature ~2.5°C higher (34.7°C) than the island rookery. Our results add to a growing consensus that thermal thresholds vary among sea turtle populations, even within the same genetic stock. Furthermore, we show that metabolic heat will have an appreciable impact on the nest microclimate, which has implications for embryonic survival and fitness under a future climate with warmer sand temperatures.