Elusor Research Articles

Saving the endangered Mary River turtle: Enhancing conservation outcomes through community engagement

AbstractAustralian biodiversity is facing an extinction crisis; yet, government spending on conservation is wholly inadequate. The involvement of local communities in fundraising, direct actions, and habitat restoration is becoming vital in the fate of threatened species. Here, we review the research outputs and impact generated from 22 years of conservation‐driven collaboration between researchers and a local community focused on saving the endangered Mary River turtle (Elusor macrurus). The study found that this collaboration generated a significant body of research that advanced the ecological knowledge of the species and ensured the findings were being applied towards the conservation of the turtle, locally and nationally. While the national listing status of E. macrurus as endangered has not changed over the past 22 years, the knowledge gained about the turtle's biology and its use to better advise development and water resources in the catchment suggests that the species' future is brighter than when it was first discovered in 1994. This review demonstrates the potential of local communities in driving and supporting conservation initiatives and provides a blueprint for scientific endeavours that inform adaptive community conservation programmes for threatened species.

Quantifying movement of multiple threatened species to inform adaptive management of environmental flows

There is a growing need for water managers to refine and optimise environmental flow strategies (e-flows) to balance water requirements for humans and nature. With increasing demands for freshwater and consequent declines in biodiversity, managers are faced with the problem of how to adaptively manage e-flows for multiple stakeholders and species whose flow requirements may overlap or vary. This study assessed the effectiveness of a regulated e-flow release strategy from a dam, aimed at providing movement opportunities and facilitating reproductive processes for multiple threatened species. Movements of 24 Mary River cod (Maccullochella mariensis), 20 Australian lungfish (Neoceratodus forsteri) and 13 Mary River turtle (Elusor macrurus) were quantified using acoustic telemetry over a three-year period. The influence of regulated e-flow releases, season, river depth, water temperature and rainfall on animal movements was assessed using Generalised linear mixed models (GLMMs). Models showed that hydraulic connectivity provided by both natural flows and regulated e-flow releases facilitated movement of all three species between pool habitats, throughout the year. Mary River turtles made extensive use of regulated e-flow releases when moving between habitats, whereas Mary River cod and Australian lungfish required additional natural rises in river height above the regulated e-flows to trigger movements. Significant movement activity was also recorded for cod and turtles during the dry season (winter and spring), broadly coinciding with breeding periods for these species. The effectiveness of, and potential improvements to, current e-flow strategies to sustain key life-history requirements of these species is discussed. Findings suggest a revised e-flow strategy with relatively minor increases in the magnitude of e-flow releases throughout winter and spring, would be effective in providing movement opportunities and supporting reproductive success for all three species. This study demonstrates that by quantifying movement behaviour in an e-flow context, ecological risk assessment frameworks can then be used to assess and provide for critical life-history requirements of multiple species within the context of a highly regulated system under increasing water use demands.

The efficacy of protecting turtle nests as a conservation strategy to reverse population decline

A common strategy used to conserve turtles is to increase the number of hatchlings entering the population by protecting the nests. Typically, nest protection programs require regular and systematic abundance surveys conducted over lengthy periods between oviposition and sexual maturity (20+ years) to assess if this conservation strategy is effective in recovering the population. Here, we describe a methodology that dramatically reduced the monitoring period (3 years) required to assess the impact of nest protection upon a threatened freshwater turtle (Elusor macrurus). An age-at-length curve was developed to define the size of turtles produced within the nest protection program period (15 years) and mark-recapture models were used to compare population demographics between areas with and without a nest protection program. Unexpectedly, the study revealed substantially fewer turtles younger than 15-years of age in areas with nest protection compared to areas where no nest protection program existed. The reason for the lack of recovery was due to a significantly lower number of nesting females and a much lower rate of survival from hatching through to the sub-adult stage within the area of the nest protection. Consequently, for E. macrurus, the nest protection program did not result in localised population recovery and in-stream mortality may be an equal if not greater threat to E. macrurus in this part of their geographical range. The study presents a relatively rapid methodology to assess the effectiveness of turtle nest protection programs and diagnose the reason for ongoing population declines.

Biogeographies: Transcending anthropocentrism in the Anthropocene

Biogeographies: Transcending anthropocentrism in the Anthropocene

Nesting behaviour of the endangered Mary River turtle: monitoring and modelling to inform e-flow strategies

The Mary River turtle (Elusor macrurus) is an endemic, monotypic species with multiple impacts across its life-history, including overharvesting of eggs, nest predation and habitat degradation. Long-term recruitment failure has led to protection measures established under state, federal and international authority. Previous research has demonstrated that E. macrurus lives instream but nests on river banks, requiring specific habitat for breeding, nesting and recruitment. Ecohydrological rules represent the critical water requirements contributing to a species’ life history and can be used to develop and assess environmental flow strategies for species affected by water resource development. This study investigated the nesting behaviour of E. macrurus, including the environmental drivers that affect nest inundation. Monitoring showed that nesting by E. macrurus peaked in October and November, driven by rainfall events (>10 mm), with potential impacts from flow events (20% of nests established <2.5 m above water level at time of nesting). These ecohydrological rules were modelled against 109 years of simulated natural flow and rainfall data. The ‘potential nesting and nest inundation’ (PNNI) indicator revealed that nesting for E. macrurus was assured in a majority of years under the natural flow scenario. The results of this study will inform the development and assessment of e-flow strategies for nesting by E. macrurus in terms of current, and future water resource development, along with climate change impacts.

Conservation genetics of the Mary River turtle (Elusor macrurus) in natural and captive populations

Abstract Many thousands of Mary River turtle eggs were harvested for the pet trade in the 1960s and 1970s before it was recognized as a new species in a unique genus. Pet turtles and their descendants still survive in captive collections. Elusor macrurus is now an endangered species after suffering dramatic population declines along the single Australian river that constitutes its entire range. A conservation genetic assessment was conducted to evaluate population subdivision within the remaining wild population of the Mary River turtle; to compare diversity of the wild population with a captive sample derived from the pet trade; and to establish a baseline estimate of effective population size (Ne) to assist with future monitoring and recovery. Microsatellite analysis indicated panmixia throughout most of the Mary River catchment with the exception of one downstream tributary –Tinana Creek (pop. Specific FST = 0.154). Subdivision between Tinana Creek and Mary River is a feature common to multiple co‐distributed freshwater taxa including the threatened Australian lungfish and Mary River cod. Microsatellite diversity of the wild adult population was low (average HS = 0.554) and not significantly different from that of a sample of captive turtles from the pet trade – indicating genetic diversity may be well represented in captive stocks. Mitochondrial DNA diversity was extremely limited, with only two haplotypes found in the wild and a single shared haplotype in captive turtles. Estimates of Ne applicable to the entire species in the wild were ~136 and ~158 using two independent methods. A reasonable management objective should be retention of Ne levels >100 during recovery of the species. Additional recommendations include that Mary River turtles be listed as Critically Endangered, and that a recovery plan be developed that considers ‘headstarting’ – using captive bred stocks to supplement the wild population.

Identifying critical habitat for freshwater turtles: integrating long-term monitoring tools to enhance conservation and management

The effective conservation and management of threatened species requires comprehensive knowledge about resource utilisation. Here we integrated tissue stable isotope analysis and biotelemetry to identify the predominant dietary resources of two sympatric species of freshwater turtle, and locate where those items were acquired. We deployed an array of underwater acoustic telemetry receivers to autonomously, simultaneously, and continuously, monitor the movements of the threatened Elseya albagula and Elusor macrurus, over a 12-month period. Stable isotope (SI) values (δ13C and δ15N) were measured within the carapace of each species, and compared with SI values within potential food items. The integration of movement information and carapace SI data revealed that whilst these species had overlapping home ranges, there was less than 5% probability of inter-species dietary niche overlap. E. macrurus acquired food items consisting of bivalves, gastropods and aquatic insects within rocky riffles whilst E. albagula fed on filamentous algae and crustaceans foraged from the muddy and vegetated shallow margins of deep water pools. Our findings differ from stomach content analysis and mark-recapture studies, which reported these species to have similar habitat and resource requirements. We argue that the observed disparity is because our methods provided a weighted measure of an individual’s dietary preference and habitat utilisation over a broad time-scale, whilst stomach content analysis and mark-recapture studies offer only a single observation of an individual’s dietary preference. The research demonstrates the utility of integrating passive acoustic telemetry and carapace stable isotope analysis for identifying critical habitat for freshwater turtles.

Complete mitochondrial genome of the endangered Mary River turtle (Elusor macrurus) and low mtDNA variation across the species' range

Elusor macrurus is an endangered short-necked turtle restricted to the Mary River catchment in south-eastern Queensland. Shotgun sequencing of genomic DNA was used to generate a complete mitochondrial genome sequence for E. macrurus using the Illumina MiSeq platform. The mitogenome is 16 499 base pairs (bp) long with 37 genes arranged in the typical vertebrate order and a relatively short 918-bp control region, which does not feature extensive tandem repeats as observed in some turtles. Primers were designed to amplify a 1270-bp region that includes 81% of the typically hypervariable control region. Two haplotypes were detected in a sample of 22 wild-caught individuals from eight sites across its natural range. The Mary River turtle is a species with low mtDNA nucleotide variability relative to other Chelidae. The combination of a very restricted distribution and dramatic reduction in population size due to exploitation for the pet trade are the conditions likely to have led to very low mtDNA variability in this endangered species.

Selectivity and Repeated Use of Nesting Sites in a Freshwater Turtle

Abstract: Understanding why turtles select specific localities to nest over others is important for management and conservation. For some species of freshwater turtle, the same localities are selected year upon year, but it is uncertain whether these localities are selected due to favored environmental conditions, or natal-site homing. The Mary River Turtle (Elusor macrurus) is an endangered freshwater species from Australia, and nesting data gathered between 2004 and 2011 demonstrated that female E. macrurus select to nest in specific localities along the Mary River. Here, we used time-lapse infrared photography and image-identification analysis to assess whether the same individuals returned to the same nesting banks over three consecutive years (nest-site fidelity), and we compared the physical and soil characteristics of nesting areas against other localities along the river where the turtles were not recorded to nest. The photography study illustrated that some females returned to nest at the same l...

Integrating telemetry with a predictive model to assess habitat preferences and juvenile survival in an endangered freshwater turtle

Summary The introduction of predators and habitat destruction is leading to a worldwide decline in freshwater turtles. Here, we assessed the preferred habitat and the predation rates for juveniles of the endangered Mary River turtle (Elusor macrurus). Juvenile turtles were fitted with miniaturised transmitters and located accurately over a 21‐day period. Water depth and velocity were measured at each locality, and the data used to populate a predictive distribution model (ecological niche factor analysis – ENFA – with Mahalanobis distances). The model showed that the juvenile turtles preferred areas of shallow, slow‐flowing water near riffles. Extrapolation of the model throughout the entire river trunk identified a further 49 discrete locations that possessed the environmental characteristics preferred by the juvenile turtles. A further 12 juveniles were released with long‐life (9 months) acoustic transmitters, and static underwater receivers were deployed to continuously record the presence and absence of turtles. The passive telemetry results supported the ENFA model and also suggested a 50% predation rate of the juvenile turtles over 9 months. Half of the predated turtles were probably taken by fish, whilst the other half were taken by a bird or mammal predator (inferred by changes in the movement of the attached transmitters). Combining telemetry with a predictive distribution model showed where juvenile E. macrurus are likely to be found and the riverine features that require preservation to conserve the species.

The influence of daily temperature fluctuations during incubation upon the phenotype of a freshwater turtle

AbstractIncubation temperature influences the phenotype of the hatchling turtles. The aims of the present study were to investigate the daily fluctuations in temperature to which eggs of the freshwater turtle Elusor macrurus are exposed to in the wild and examine how these fluctuations may affect the phenotype and performance of the hatchlings. Eggs in the wild experienced an overall mean daily fluctuation of 5.7°C throughout the incubation period, but on particular days, the variation was as low as 2°C and as high as 22°C. Fifty‐four eggs were collected from the wild and incubated in the laboratory at one constant (28°C) and two fluctuating (28 ± 3 and 28 ± 6°C) thermal regimes. Egg mass, incubation length and hatching success (89%) were similar for the 28 and 28 ± 3°C groups, whereas the 28 ± 6°C group only had a 5% hatching success, and the incubation length was 10 days longer. Upon hatching, there was no significant difference in body mass or straight carapace length between the 28 and 28 ± 3°C groups, and within the first 8 weeks of hatching, there was no significant difference in growth rate, self‐righting time, crawling speed and swimming performance. A single survivor from the 28 ± 6°C group had a body mass that was 27% less compared with the other two groups and it did considerably poorer in all the performance tests. The study findings illustrated that daily fluctuations in incubation temperature up to 6°C had no effect upon hatchling E. macrurus phenotype, but there was a limit (12°C) by which the extent and recurrence of these fluctuations became detrimental. These thermal regimes are not yet apparent in the wild but will occur within the geographical range of this species according to climate change predictions.

Staying cool, keeping strong: incubation temperature affects performance in a freshwater turtle

AbstractIt is unclear how predicted rises in ambient temperature associated with climate change will impact upon the survivorship of oviparous reptiles. Given that the incubation temperature can influence hatchling phenotype, understanding how elevated temperatures during development can affect the ability of hatchlings to undertake routine behaviours is important, especially for threatened species. Here we tested if raising mean incubation temperature above natural levels altered the physiology of hatchlings to an extent that behavioural function was impaired. Firstly, incubation temperatures were recorded from nests of the freshwater turtle (Elusor macrurus) in the wild, and the observed thermal range (26–31 °C) used to define the experimental protocol. Then, freshly laid E. macrurus eggs were collected and incubated at three constant temperatures (26, 29 and 32 °C). Embryos incubated at 32 °C had the lowest hatching success. Those that did hatch were smaller than the other groups and had a reduced post‐hatch growth rate. On land, the ability of hatchling turtles to right themselves is critical, and the turtles incubated at 32 °C took 30‐times longer to do this than those incubated at 26 °C. Once in the water, hatchling turtles must be able to swim effectively to evade predation and obtain food items. During swimming trials the 32 °C group exhibited a lower mean stroke force (10.5±0.3 mN) and spent less time swimming (133.7±17.7 s) compared with hatchlings incubated at 29 °C (13.4±0.4 mN, 281.3±25.7 s) and 26 °C (15.7±0.5 mN, 270.8±28.5 s). The results of the present study illustrate that even slight rises in the mean incubation temperature, over that observed in the wild, can impact upon a hatchling's performance.

Twenty-nine microsatellite markers for two Australian freshwater turtles, Elseya albagula and Emydura macquarii krefftii: development from 454-sequence data and utility in related taxa

454 shotgun sequencing was used to identify thousands of in silico microsatellite loci from two Australian freshwater turtle species (Pleurodira, Chelidae), Elseya albagula and Emydura macquarii krefftii. Twenty-nine polymorphic microsatellites were subsequently developed and tested as markers, 15 for E. m. krefftii and 14 for E. albagula. The former marker set showed greater allelic richness (mean N A = 7.7, range 3–15) than the latter (mean N A = 4.4, range 2–8). Levels of expected heterozygosity were high for both marker suites (mean H E = 0.718, range 0.177–0.875; and mean H E = 0.567, range 0.317–0.827, respectively), indicating both are suitable for studies of population genetic structure, connectivity and mating systems in these taxa. Cross-species amplification in 12 other short-necked freshwater turtle taxa highlighted the potential utility of these markers in other species, notably Emydura spp., Rheodytes leukops and Elusor macrurus.

Implications of river damming: the influence of aquatic hypoxia on the diving physiology and behaviour of the endangered Mary River turtle

AbstractRiver impoundments are characterized by low oxygen levels as a result of reduced water velocity and increased water depth. Bimodally respiring turtle species are likely to be highly sensitive to changes in aquatic PO2 with decreases in oxygen levels impacting upon their diving ability. The acute and long‐term effects of aquatic hypoxia on dive duration, oxygen consumption and blood respiratory properties were examined in hatchlings of the endangered Mary River turtle Elusor macrurus. It was hypothesized that acute exposure to aquatic hypoxia would cause a decrease in dive duration as a consequence of a decrease in reliance on aquatic respiration. With long‐term exposure to hypoxia, we predicted that Elu. macrurus would have the capacity to compensate for the acute effect of hypoxia and that dive duration would increase due to an increase in aquatic respiration, haemoglobin concentration and oxygen affinity (P50). When exposed to hypoxic conditions, aquatic respiration in Elu. macrurus was substantially reduced resulting in a 51% decrease in dive duration. Contrary to our predictions, Elu. macrurus hatchlings did not acclimate, and long‐term exposure to hypoxic conditions caused Elu. macrurus to lose significantly more oxygen to the hypoxic water than the normoxic acclimated turtles. The exacerbation of long‐term hypoxia on the respiratory physiology and diving ecology of Elu. macrurus raises concerns about the impacts of long‐term environmental change as a result of habitat alteration on the survival of freshwater turtle populations.

Diving behaviour, aquatic respiration and blood respiratory properties: a comparison of hatchling and juvenile Australian turtles

AbstractAustralia has a number of bimodally respiring freshwater turtle species that use aquatic respiration to extend their aerobic dive limit. While species variations in reliance on aquatic respiration are reflected in the diving behaviour and ecology of adults, it is unknown whether these relationships also occur in hatchling and juvenile turtles. This study compared the diving behaviour, aquatic respiration and blood respiratory properties of hatchling and juveniles from five species of Australian freshwater turtles: Rheodytes leukops, Elusor macrurus, Elseya albagula, Elseya latisternum and Emydura signata. Both diving behaviour and physiology differed significantly between species as well as age classes. Dive duration in R. leukops was 17 times longer than the other species, with two hatchlings remaining submerged for the entire 72 h recording period. The long dive duration recorded for R. leukops was supported by a high reliance on aquatic respiration (63–73%) and high blood oxygen affinity (P50=17.24 mmHg). A correlation between dive duration, aquatic respiration and blood respiratory properties was not observed in the remaining turtle species where, despite the longer dive duration of Els. albagula and Elu. macrurus compared with Em. signata and Els. latisternum, there was no difference observed in per cent aquatic respiration or blood oxygen affinity between these species. When compared with adult individuals (data from previous studies), dive duration was positively correlated with body size in Em. signata, Els. albagula and R. leukops, but a negative relationship occurred in Els. latisternum and Elu. macrurus.

Thermal Plasticity of Diving Behavior, Aquatic Respiration, and Locomotor Performance in the Mary River TurtleElusor macrurus

Locomotion is a common measure of performance used in studies of thermal acclimation because of its correlation with predator escape and prey capture. However, for sedentary animals such as freshwater turtles, we propose that diving behavior may be a more ecologically relevant measure of performance. Increasing dive duration in hatchling turtles reduces predator exposure and therefore functions as an ecological benefit. Diving behavior is thermally dependent, and in some species of freshwater turtles, it is also reliant on aquatic respiration. This study examined the influence of thermal acclimation on diving behavior, aquatic respiration, and locomotor performance in the endangered, bimodally respiring Mary River turtle Elusor macrurus. Diving behavior was found to partially acclimate at 17 degrees C, with turtles acclimated to a cold temperature (17 degrees C) having a significantly longer dive duration than hatchlings acclimated to a warm temperature (28 degrees C). This increase in dive duration at 17 degrees C was not a result of physiological alterations in metabolic rate but was due instead to an increase in aquatic oxygen consumption. Increasing aquatic oxygen consumption permitted cold-acclimated hatchlings to remain submerged for significantly longer periods, with one turtle undertaking a dive of over 2.5 d. When burst-swimming speed was used as the measure of performance, thermal acclimation was not detected. Overall, E. macrurus demonstrated a partial ability to acclimate to changes in environmental temperature.

Temperature Fails to Influence Hatchling Sex in Another Genus and Species of Chelid Turtle, Elusor macrurus

Temperature Fails to Influence Hatchling Sex in Another Genus and Species of Chelid Turtle, Elusor macrurus