Australian Freshwater Turtles Research Articles

Current conservation status of Australian freshwater turtles

Current conservation status of Australian freshwater turtles

Effects of temperature and exercise on metabolism of three species of Australian freshwater turtles: implications for responses to climate change

Oxygen consumption () of Chelodina expansa, C. longicollis and Emydura macquarii (Pleurodira: Chelidae) was measured at rest and during induced exercise at 8, 13, 18, 22, 26, 30 and 34°C. Resting varied significantly among species, being lowest in C. expansa, which is the most sedentary of the three species in nature, and highest in E. macquarii, which is the most energetic, but active did not differ significantly among the three species overall. For both Chelodina species, resting was appreciably lower than expected from regression of on body mass for non-marine turtles globally, a result that reinforces previous evidence of low resting metabolism in Australian chelid turtles. Active of all three species at higher temperatures was similar to reported for active freshwater cryptodires. Resting of all three species increased similarly with temperature, but active and aerobic scope did not. In C. expansa and E. macquarii, active and aerobic scope increased over the full temperature range assessed but in C. longicollis these variables reached a plateau above 22°C. Projected increases in freshwater temperatures in south-eastern Australia as a result of global warming are likely to enhance activity, feeding and growth of the three species (subject to food availability), especially in cooler seasons for C. longicollis and warmer seasons for C. expansa and E. macquarii. However, other aspects of predicted climate change, especially increased drought, are likely to be detrimental.

Identifying Critical Habitat for Australian Freshwater Turtles in a Large Regulated Floodplain: Implications for Environmental Water Management.

Freshwater turtles face many threats, including habitat loss and river regulation reducing occupancy and contributing to population decline. Limited knowledge of hydrological conditions required to maintain viable turtle populations in large floodplain wetlands hinders effective adaptive management of environmental water in regulated rivers. We surveyed three turtle species over 4 years across the Lower Murrumbidgee River floodplain, a large wetland complex with a long history of water resource development. Using site and floodplain metrics and generalized linear models, within a Bayesian Model Averaging framework, we quantified the main drivers affecting turtle abundance. We also used a hierarchical modeling approach, requiring large sample sizes, quantifying possible environmental effects while accounting for detection probabilities of the eastern long-necked turtle (Chelodina longicollis). The three species varied in their responses to hydrological conditions and connectivity to the main river channel. Broad-shelled turtles (Chelodina expansa) and Macquarie River turtles (Emydura macquarii macquarii) had restricted distributions, centered on frequently inundated wetlands close to the river, whereas the eastern long-necked turtles were more widely distributed, indicating an ability to exploit variable habitats. We conclude that turtle communities would benefit from long-term management strategies that maintain a spatiotemporal mosaic of hydrological conditions. More specifically, we identified characteristics of refuge habitats and stress the importance of maintaining their integrity during dry periods. Neighboring habitats can be targeted during increased water availability years to enhance feeding and dispersal opportunities for freshwater turtles.

Responses of an Australian freshwater turtle to drought‐flood cycles along a natural to urban gradient

AbstractUrban areas provide habitat for numerous native species, but life in towns and cities presents many challenges. The effect of climate on the ecology and the behaviour of non‐volant vertebrates inhabiting urban habitats have received little attention. In this study, we investigated demography, growth rates, movements and reproduction of a semi‐aquatic freshwater turtle, Chelodina longicollis, along a natural to urban gradient during a period of relatively high rainfall (2011–2014) and compared this to a previous study in the same system during drought (2006–2007). In addition to changes in rainfall, urbanization increased considerably over the same time period and a pest‐exclusion fence was constructed to mitigate against urban hazards encroaching on the adjacent reserve. Turtles grew at similar rates, had similar abundances and sex ratios and had similar reproductive output across the gradient from urban to non‐urban sites during the wet period. Despite increasing urbanization, recruitment occurred at all sites and survivorship estimates were similar among sites. Turtles moved among wetlands at high rates and over long distances (6 km), underscoring the importance of movements in urban landscapes. Our results contrast with those for the same system during drought, when turtles were less abundant and grew slower in the nature reserve compared with the urban environment. Our results underscore the strong influence climate can have on population dynamics and resilience of species to changes brought about by urbanization. Further monitoring is required to understand the long‐term population responses of long‐lived species to drought cycles.

Road density and wetland context alter population structure of a freshwater turtle

AbstractRoads are detrimental to wildlife populations that require contiguous networks of terrestrial and aquatic habitats. Many species of freshwater turtles are sensitive to habitat fragmentation caused by roads, and are susceptible to road mortality during overland migrations. The common long‐necked turtle (Chelodina longicollis) is anAustralian freshwater turtle that frequently moves between wetlands, and so populations may incur negative impacts from road effects. Here, we assessed the relationship betweenC. longicollisand road density and landscape variables within populations inhabiting 20 wetlands distributed throughout greaterMelbourne,Australia. The size frequency distribution ofC. longicollisat sites surrounded by high road densities was skewed towards larger individuals, but there was no difference in the frequency of juveniles between high and low road density sites. Regression modelling revealed a clear positive relationship between road density and carapace length (CL) ofC. longicollis; the meanCLat a site with the highest road density was predicted to be 23% greater than meanCLat a site surrounded by no roads. FemaleCLwas also positively related to road density. There was a clear positive relationship between wetland age andCL, although this relationship was not as strong. While there was no relationship evident between road density and the proportion of femaleC. longicollisat a site, more females were captured at smaller ephemeral sites surrounded by a high proportion of green open space and located near drainage lines. We did not find evidence of sex‐related differences in road effects. These results suggest that roads may be affectingC. longicollisin the study area, but the direct cause of any effects is difficult to identify.

Hatching behavior of eastern long-necked turtles (Chelodina longicollis): The influence of asynchronous environments on embryonic heart rate and phenotype

Variable temperatures within a nest cause asynchronous development within clutches of freshwater turtle embryos, yet synchronous hatching occurs and is thought to be an important survival strategy for hatchlings. Metabolic compensation and circadian rhythms in heart rates of embryonic turtles indicate the potential of communication between embryos in a nest. Heart rates were used to identify metabolic circadian rhythms in clutches of an Australian freshwater turtle (Chelodina longicollis) and determine whether embryos metabolically compensate and hatch synchronously when incubated in asynchronous environments. The effects of a group environment during incubation on egg development and incubation period were also investigated during the final 3weeks of development. Chelodina longicollis hatch synchronously and metabolically compensate so that less advanced embryos catch up to more advanced clutch-mates. Heart rates of embryos remained stable from week 4–7 in asynchronous (M=89bpm) and synchronous (M=92bpm) groups and declined in the final 2weeks of incubation (M=72 and 77bpm). Circadian rhythms were present throughout development and diel heart rates of embryos in asynchronous groups showed less deviation from the mean (M=−0.5bpm) than synchronous groups (M=−4bpm). Eggs incubated in groups had a significantly shorter incubation period than eggs incubated individually. Phenotypic traits including size, performance, and growth of all hatchlings were not affected. Egg position within a turtle nest is important for coordinating development throughout incubation and facilitating synchronous hatching.

Significant genetic structure despite high vagility revealed through mitochondrial phylogeography of an Australian freshwater turtle (Chelodina longicollis)

Restriction to the freshwater environment plays a dominant role in the population genetic structure of freshwater fauna. In taxa with adaptations for terrestriality, however, the restrictions on dispersal imposed by drainage divides may be overcome. We investigate the mitochondrial phylogeographic structure of the eastern long-necked turtle (Chelodina longicollis), a widespread Australian freshwater obligate with strong overland dispersa\l capacity and specific adaptations to terrestriality. We predict that such characteristics make this freshwater species a strong candidate to test how life-history traits can drive gene flow and interbasin connectivity, overriding the constraining effects imposed by hydrological boundaries. Contrary to expectations, and similar to low-vagility freshwater vertebrates, we found two ancient mitochondrial haplogroups with clear east–west geographic partitioning either side of the Great Dividing Range. Each haplogroup is characterised by complex genetic structure, demographically stable subpopulations, and signals of isolation by distance. This pattern is overlaid with signatures of recent gene flow, likely facilitated by late Pleistocene and ongoing anthropogenic landscape change. We demonstrate that the divergent effects of landscape history can overwhelm the homogenising effects of life-history traits that connect populations, even in a highly vagile species.

Reproductive investment compromises maternal health in three species of freshwater turtle.

Life-history theory predicts that a trade-off in the allocation of resources between different physiological systems exists because resources are finite. As a result, females investing heavily in reproduction may compromise their future health. We used hematology, serum biochemistry, mass, and morphometric measurements as indicators of physiological health state to investigate whether reproductive investment altered subsequent maternal health in three Australian freshwater turtles: the oblong turtle (Chelodina oblonga; n = 12), the Macquarie turtle (Emydura macquarii; n = 9), and the eastern long-necked turtle (Chelodina longicollis; n = 8). Maternal health was impaired in turtles that produced larger and heavier eggs and clutches. In C. oblonga and E. macquarii, increased reproductive investment generally resulted in negative changes to the hematology and serum biochemistry profile of maternal blood. Generally, increases in heterophil/lymphocyte ratio, aspartate transaminase, creatine kinase, calcium/phosphorus ratio, and albumin/globulin ratio were observed following reproduction, in addition to a decrease in glucose and total protein. These findings agree with the physiological constraint hypothesis and highlight the connection between life-history evolution and animal physiology by documenting, for the first time, how measures of physiological health state relate to reproductive investment in Australian freshwater turtles. Additionally, our findings suggest that body condition, a readily used morphological biomarker, is a poor predictor of health in turtles. Our results emphasize the need to investigate how maternal health is influenced by the reproductive process in different species.

Phylogeography of the Australian freshwater turtleChelodina expansareveals complex relationships among inland and coastal bioregions

We examined range-wide mitochondrial phylogeographical structure in the riverine freshwater turtle Chelodina expansa to determine whether this species exhibits deep genetic divergence between coastal and inland hydrological provinces, as seen in co-distributed freshwater taxa. We sequenced two mitochondrial loci, genealogical relationships were assessed using a network approach, and relationships among biogeographical regions were tested using analyses of molecular variance. Population history was evaluated using neutrality tests, indices of demographic expansion, and mismatch analyses. Twenty-one haplotypes were recovered across two mitochondrial haplogroups separated by approximately 4% nucleotide divergence. The haplogroups have discrete geographical boundaries but only partially support a hypothesis of deep divergence between coastal and inland bioregions. The first haplogroup comprises populations from the inland Murray-Darling Basin and from coastal catchments south of the Mary River in south-east Queensland. The second haplogroup comprises populations from coastal catchments north of the Mary River. Cryptic phylogeographical barriers separating adjacent coastal populations are congruent with those demonstrated for other freshwater taxa and may result from the combined influences of the Conondale Range and alluvial deposits at the mouth of the Mary River. The findings of the present study demonstrate that freshwater taxa commonly display genetic differentiation within a biogeographical region where no boundaries have been recognized, highlighting the need to uncover cryptic microbiogeographical regions to aid conservation of freshwater biota. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 789–805.

Ancient Phenotypes Revealed Through Present Day Species—A Morphological Analysis of Australia's Saw-Shelled Turtles Including the ThreatenedMyuchelys bellii(Testudines: Chelidae)

Understanding of evolutionary history and speciation events to inform phylogeography of extant species can be gleaned from the fossil record. However, the fossil record for Australian freshwater turtles contains many gaps and interpretation of the fossils that are known is difficult because of poor knowledge of the morphology of extant forms. There are no fossils currently assigned to short-necked turtles in the genus Myuchelys. In an alternative approach, morphological characters of the extant species Myuchelys bellii, Myuchelys georgesi, Myuchelys latisternum, and Myuchelys purvisi were mapped against their current molecular phylogeny. The cryptic species pair, M. georgesi and M. purvisi, are morphologically very similar, but distant phylogenetically, and their common ancestor includes M. latisternum and M. bellii in its decendents. This suggests that current shared morphology of M. georgesi and M. purvisi represents a suite of symplesiomorphies (shared primitive characters). These characters include presence of a cervical scute, lack of prominent neck tubercles, a relatively small head size, minor or no serrations of marginal scutes, an oval carapace, and a smooth head shield extending down the parietal arch toward the tympanum. This commonality of characters of this cryptic species pair represents a rare insight to the ancestral phenotype of the Myuchelys. The loss of the cervical scute and presence of enlarged neck tubercles, a large robust head and furrowed head shield, deep serrated shell margins, and compressed shell profile in M. bellii and M. latisternum are synapomorphies (shared derived characters). There is no morphological support for the distinction at the level of species or subspecies between discrete populations of M. bellii. A dichotomous key to species is provided.

Mitochondrial variation among Australian freshwater turtles (genus Myuchelys), with special reference to the Endangered M. bellii

Identifying species and the relationships among them remains important for assess- ing biodiversity trends and is a critical focus for reversing global biodiversity loss. The saw-shelled turtles of Australia, in the genus Myuchelys, show cryptic diversity and include species that range from Endangered (M. bellii), through those that are locally abundant but extremely limited in dis- tribution (M. georgesi and M. purvisi) to those that are common and widespread (M. latisternum). The Endangered M. bellii is restricted to 3 small isolated populations in the headwaters of the Murray-Darling basin, in the Border, Gwydir and Namoi tributaries. There is no evidence of strong differentiation among these 3 populations based on mitochondrial DNA (mtDNA) diver- gences; rather there is only a shallow genetic structure ranging from 0.1 to 0.3% divergence. The 3 restricted and small populations of the Endangered M. bellii face a number of threatening pro- cesses and require conservation management across state boundaries as a single biological spe- cies. The mtDNA phylogeny supports previous phylogenetic findings of a deep phylogenetic divergence between M. purvisi and M. georgesi (13.5% mtDNA) and the sister taxa relationship of M. latisternum and M. bellii. A notable exception was our finding that Emydura macquarii and M. georgesi are sister taxa inside the Myuchelys radiation.

Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

Incubation temperature affects developmental rates and defines many phenotypes and fitness characteristics of reptilian embryos. In turtles, eggs are deposited in layers within the nest, such that thermal gradients create independent developmental conditions for each egg. Despite differences in developmental rate, several studies have revealed unexpected synchronicity in hatching, however, the mechanisms through which synchrony are achieved may be different between species. Here, we examine the phenomenon of synchronous hatching in turtles by assessing proximate mechanisms in an Australian freshwater turtle (Emydura macquarii). We tested whether embryos hatch prematurely or developmentally compensate in response to more advanced embryos in a clutch. We established developmental asynchrony within a clutch of turtle eggs and assessed both metabolic and heart rates throughout incubation in constant and fluctuating temperatures. Turtles appeared to hatch at similar developmental stages, with less-developed embryos in experimental groups responding to the presence of more developed eggs in a clutch by increasing both metabolic and heart rates. Early hatching did not appear to reduce neuromuscular ability at hatching. These results support developmental adjustment mechanisms of the 'catch-up hypothesis' for synchronous hatching in E. macquarii and implies some level of embryo-embryo communication. The group environment of a nest strongly supports the development of adaptive communication mechanisms between siblings and the evolution of environmentally cued hatching.

Nine microsatellite markers for the Australian side-necked turtle Chelodina expansa (Chelidae) and cross species amplifications

Nine microsatellite DNA loci for the Australian broad-shelled freshwater turtle ( Chelodina expansa) are presented. Markers were tailed with 20-mer oligonucleotides for use in four-colour fluorescent multiplex PCRs. The markers show high allelic richness (mean N A = 10.9, range 2–38) and expected heretozygosity (mean H E = 0.643; range 0.161–0.963) indicating that they will be valuable for population genetics studies in C. expansa. Cross-species amplification in three Australian freshwater turtle species further highlights the potential utility of these markers, particularly in the side-neck species C. longicollis and C. rugosa.

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.

Camallanus Railliet et Henry, 1915 (Nematoda, Camallanidae) from Australian freshwater turtles with descriptions of two new species and molecular differentiation of known taxa

AbstractTwo new species of Camallanus are described from Australian freshwater turtles. Camallanus beveridgei sp. nov. is reported from Elseya dentata in Northern Territory. It differs from other species of the genus parasitic in turtles by several characters including the shape of the median ridge in the buccal capsule and the position of the anterior pair of caudal papillae in males. Camallanus sprenti sp. nov. is reported from Elseya latisternum (type host) and Emydura krefftii in northern Queensland. It is closely related to Camallanus tuckeri, and differs from the latter species in possessing a shorter oesophagus. We summarize data on morphology, distribution and specificity of 5 known Camallanus spp. from Australian turtles and provide a key for their identification. Sequence comparison of more than 500 base pairs at the 5′ end of the nuclear 28S rDNA gene confirms the status of C. sprenti and C. beveridgei as new species. Camallanus sprenti differs from the other 4 species of Camallanus from Australian turtles by 16–59 bases (3.1–11.5%) while C. beveridgei differed from the other 4 species by 23–60 bases (4.5–11.6%). Phylogenetic analysis demonstrates close interrelationships among C. tuckeri, C. sprenti and C. beveridgei, the three species with most similar buccal capsules.

The natural history of nesting in two Australian freshwater turtles

The nesting behaviour of two Australian freshwater turtles, the broad-shelled river turtle Chelodina expansa and the Brisbane river turtle Emydura signata are described.Both species nest during, or soon after rain. C. expansa nests exclusively during the day while E. signata as a preference for nesting at night but can be found nesting during the day. C. expansa nests 30-300 m from the water's edge usually after walking up a hill, while E. signata typical nests just 2-10 m from the water's edge. Both species dig their nests exclusively with their hind legs by alternative scooping movements. Nest excavation takes from 20 to 180 minutes depending on how hard the soil is compacted. Typically some water is released from the cloaca during the nesting process but the role of this behaviour remains unknown. C. expansa uses a ‘body-slamming’ behaviour to compact the nest plug at the end of nesting but this behaviour was not observed in E. signata.

Life in the suburbs: Behavior and survival of a freshwater turtle in response to drought and urbanization

Urbanization fundamentally alters the abiotic and biotic components of landscapes, presenting wildlife with serious challenges to which they must respond in order to avoid excess mortality from urban dangers. In this study, we used radio-telemetry to examine the behavior and survivorship of an Australian freshwater turtle, Chelodina longicollis, in a suburban environment compared to a control group on an adjacent nature reserve. We expected turtles in the suburbs to be less mobile, but the suburban environment did not inhibit the ability of turtles to traverse large areas and make frequent movements among several different wetlands. In fact, suburban turtles were more vagile, moving distances twice as far as those on the nature reserves. Turtles on the nature reserve responded to dropping water levels during drought by estivating for several months in sheltered woodland micro-habitats. Suburban turtles did not estivate terrestrially, in part because their water bodies experienced dampened water level fluctuations and retained water during drought, though the relative unavailability of suitable estivation sites and perceived threats could also account for their avoidance of extended forays into the terrestrial environment. Annual survival rate was 95.3% in the reserves compared to 87.6% in the suburbs, but this 7.7% decrease in survival from road mortality was not significant in our survivorship models. The continued ability of suburban turtles to remain vagile without suffering from high mortality rates is likely a product of the availability of vegetated drainage lines and under-road “box” culverts that allow turtles to travel safely throughout the suburban landscape.

Terrestrial activity, movements and spatial ecology of an Australian freshwater turtle, Chelodina longicollis, in a temporally dynamic wetland system

AbstractAnimal movements, use of space, activity patterns and habitat use are in part determined by proximal factors such as the landscapes they occupy, seasonal or environmental cues and individual attributes such as sex and body size. Using radio‐telemetry and a drift fence, we examined the contribution of these factors to variation in movements, use of space and terrestrial activity in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae), in south‐east Australia. Movements and use of space depended strongly on landscape attributes, while sex and body size were less important. Movements and use of space also varied seasonally and were partly correlated with rainfall. The high overall vagility of turtles, irrespective of sex and adult body size (13.8 ± 2.8 ha (±SE) home range, 2608 ± 305 m total distance moved, 757 ± 76 m range length), probably reflects a common need to be mobile in a landscape characterized by fluctuating resources in temporary wetlands. Use of temporary wetlands also drives C. longicollis into terrestrial habitats for movements between wetlands and extended refuge. Timing of inter‐wetland movements was associated with rainfall, but most notably for immature individuals and for those moving towards temporary wetlands. Movements of adults, evacuation of the drying wetland and periods of extended refuge (i.e. aestivation) were less dependent upon rainfall if at all. We conclude that movements about and use of the landscape by C. longicollis are under the strong influence of several interacting factors such as patch configuration, seasonal and environmental cues, and in part, body size. We argue that such behaviours are also ultimately under selection from the costs and benefits of these behaviours in the context of fluctuating resources.

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.

Epizoochory, Algae and the Australian Eastern Long-Necked Turtle Chelodina Longicollis (Shaw)

The role of animals in seed dispersal is widely acknowledged and turtles have been reported to act as vectors. All reports of turtles dispersing seeds to date have been via endozoochrony. The first evidence of turtles being epizoochronic dispersers of seeds via their carapacial algal mat is reported here. Chelodina longicollis is widespread and abundant throughout most of the eastern fringe of mainland Australia and throughout the largest inland river system, the Murray Darling Basin. They are the most terrestrially mobile of the Australian freshwater turtles and they are the most indiscriminate in habitat choice, inhabiting the entire range of water bodies from rivers to small ephemeral wetlands. Our results showed that turtles with even moderate carapacial algae can act as vectors in the dispersal of seeds associated with wetlands. However, as C. longicollis is unlikely to be unique among the freshwater turtles in this regard, we conclude that epizoochory is likely to occur in other turtle species.