Refining trophic dynamics through multi-factor Bayesian mixing models: A case study of subterranean beetles

© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd Food web dynamics are vital in shaping the functional ecology of ecosystems. However, trophic ecology is still in its infancy in groundwater ecosystems due to the cryptic nature of these environments. To unravel trophic interactions between subterranean biota, we applied an interdisciplinary Bayesian mixing model design (multi-factor BMM) based on the integration of faunal C and N bulk tissue stable isotope data (d13C and d15N) with radiocarbon data (?14C), and prior information from metagenomic analyses. We further compared outcomes from multi-factor BMM with a conventional isotope double proxy mixing model (SIA BMM), triple proxy (d13C, d15N, and ?14C, multi-proxy BMM), and double proxy combined with DNA prior information (SIA + DNA BMM) designs. Three species of subterranean beetles (Paroster macrosturtensis, Paroster mesosturtensis, and Paroster microsturtensis) and their main prey items Chiltoniidae amphipods (AM1: Scutachiltonia axfordi and AM2: Yilgarniella sturtensis), cyclopoids and harpacticoids from a calcrete in Western Australia were targeted. Diet estimations from stable isotope only models (SIA BMM) indicated homogeneous patterns with modest preferences for amphipods as prey items. Multi-proxy BMM suggested increased—and species-specific—predatory pressures on amphipods coupled with high rates of scavenging/predation on sister species. SIA + DNA BMM showed marked preferences for amphipods AM1 and AM2, and reduced interspecific scavenging/predation on Paroster species. Multi-factorial BMM revealed the most precise estimations (lower overall SD and very marginal beetles' interspecific interactions), indicating consistent preferences for amphipods AM1 in all the beetles' diets. Incorporation of genetic priors allowed crucial refining of the feeding preferences, while integration of more expensive radiocarbon data as a third proxy (when combined with genetic data) produced more precise outcomes but close dietary reconstruction to that from SIA + DNA BMM. Further multidisciplinary modeling from other groundwater environments will help elucidate the potential behind these designs and bring light to the feeding ecology of one the most vital ecosystems worldwide

Time capsules of biodiversity: Future research directions for groundwater-dependent ecosystems of the Great Artesian Basin

The Great Artesian Basin of Australia represents one of the largest and deepest basins of freshwater on Earth. Thousands of springs fed by the Basin are scattered across Australia’s arid zone, often representing the sole sources of freshwater for thousands of kilometers. As “islands” in the desert, the springs support endemic fauna and flora that have undergone millions of years of evolution in almost total isolation. Here, we review the current body of knowledge surrounding Great Artesian Basin springs and their significance from ecological, evolutionary, and cultural perspectives using South Australian spring wetlands as a case study. We begin by identifying the status of these springs as critical sources of groundwater, the unique biodiversity they support, and their cultural significance to the Arabana people as Traditional Custodians of the land. We then summarize known threats to the springs and their biota, both exogenous and endogenous, and the potential impacts of such processes. Finally, considering the status of these at-risk habitats as time capsules of biodiversity, we discuss lessons that can be learnt from current conservation and management practices in South Australia. We propose key recommendations for improved biodiversity assessment and monitoring of Great Artesian Basin springs nationwide, including 1) enhanced legal protections for spring biota; 2) increased taxonomic funding and capacity; 3) improved biodiversity monitoring methods, and 4) opportunities for reciprocal knowledge-sharing with Aboriginal peoples when conducting biodiversity research.P. G. Beasley-Hall, N. P. Murphy, R. A. King, N. E. White, B. A. Hedges, S. J. B. Cooper, A. D. Austin, and M. T. Guzi

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38 °C cf. 42–46 °C), but the genetic basis of this physiological diference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35 °C), as determined by comparative transcriptomics. However, genes involved in these responses difer between species and a far greater number were diferentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only diferentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular fndings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.Perry G. Beasley-Hall, Terry Bertozzi, Tessa M. Bradford, Charles S. P. Foster, Karl Jones, Simon M.Tierney, William F. Humphreys, Andrew D.Austin, Steven J. B. Coope

eDNA in subterranean ecosystems: Applications, technical aspects, and future prospects

Monitoring of biota is pivotal for the assessment and conservation of ecosystems. Environments worldwide are being continuously and increasingly exposed to multiple adverse impacts, and the accuracy and reliability of the biomonitoring tools that can be employed shape not only the present, but more importantly, the future of entire habitats. The analysis of environmental DNA (eDNA) metabarcoding data provides a quick, affordable, and reliable molecular approach for biodiversity assessments. However, while extensively employed in aquatic and terrestrial surface environments, eDNA-based studies targeting subterranean ecosystems are still uncommon due to the lack of accessibility and the cryptic nature of these environments and their species. Recent advances in genetic and genomic analyses have established a promising framework for shedding new light on subterranean biodiversity and ecology. To address current knowledge and the future use of eDNA methods in groundwaters and caves, this review explores conceptual and technical aspects of the application and its potential in subterranean systems. We briefly introduce subterranean biota and describe the most used traditional sampling techniques. Next, eDNA characteristics, application, and limitations in the subsurface environment are outlined. Last, we provide suggestions on how to overcome caveats and delineate some of the research avenues that will likely shape this field in the near future. We advocate that eDNA analyses, when carefully conducted and ideally combined with conventional sampling techniques, will substantially increase understanding and enable crucial expansion of subterranean community characterisation. Given the importance of groundwater and cave ecosystems for nature and humans, eDNA can bring to the surface essential insights, such as study of ecosystem assemblages and rare species detection, which are critical for the preservation of life below, as well as above, the ground.Mattia Saccò, Michelle T. Guzik, Mieke van der Heyde, Paul Nevill, Steven J.B. Cooper, Andrew D. Austin, Peterson J. Coates, Morten E. Allentoft, Nicole E. Whit

Population genomic diversity and structure in the golden bandicoot: a history of isolation, extirpation, and conservation

Published online: 08 October 2023. OnlinePublUsing genetic information to develop and implement conservation programs is vital for maintaining biodiversity and ecosystem resilience. Evaluation of the genetic variability within and among remnant populations can inform management of both natural and translocated populations to maximise species' adaptive potential, mitigate negative impacts of inbreeding, and subsequently minimise risk of extinction. Here we use reduced representation sequencing to undertake a genetic assessment of the golden bandicoot (Isoodon auratus), a threatened marsupial endemic to Australia. The currently recognised taxon consists of three subspecies distributed among multiple natural and translocated populations. After confirming the genetic distinctiveness of I. auratus from two closely related taxa, I. fusciventer and I. macrourus, we identified four genetic clusters within I. auratus. These clusters exhibited substantial genetic differentiation (pairwise FST values ranging from 0.18 to 0.65, pairwise DXY ranging from 0.1 to 0.168), reflecting long-term isolation of some populations on offshore islands and the influence of genetic drift. Mainland natural populations in the Kimberley region had the highest genetic diversity and the largest contribution to overall allelic and gene diversity compared to both natural and translocated island populations. A population translocated to Guluwuru Island in the Northern Territory had the lowest genetic diversity. Our data suggest that island populations can appear genetically unique due to genetic drift and this needs to be taken into account when considering genetic diversity in conservation efforts to maintain overall genetic diversity of the species. We effectively demonstrate how genomic information can guide practical conservation planning, especially when declining species are represented by multiple isolated populations.Kate Rick, Margaret Byrne, Skye Cameron, Steve J. B. Cooper, Judy Dunlop, Brydie Hill, Cheryl Lohr, Nicola J. Mitchell, Craig Moritz, Kenny J. Travouillon, Brenton von Takach and Kym Ottewel

New genera, species and combinations in the Pseudomicrocara Armstrong group (Coleoptera: Scirtidae) based on morphology supported by mitochondrial and nuclear gene sequence data

The Australian Scirtidae genus Pseudomicrocara Armstrong, previously shown to be polyphyletic, is revised using both morphology and sequence data from the mitochondrial gene cytochrome oxidase subunit 1 and two nuclear genes, elongation factor 1-alpha and topoisomerase. Twenty-three genera, 16 of which are new, are recognised based on morphology, primarily of the mandibles and maxillary palpi, and male and female genitalia. Maximum likelihood and Bayesian phylogenetic analyses were used to examine relationships among species from 21 of the 23 recognised genera. Fifteen of the genera were recovered as distinct lineages. A further six, Accolabass Watts, Anocyphon gen. nov., Copiacyphon gen. nov., Nasutuscyphon gen. nov., Pseudomicrocara and Saprocyphon gen. nov. were considered to be genera based on both morphology and phylogenetic analysis but their species composition is uncertain and will require more work to confirm. The 17 new genera are fully described, keys are provided to all the genera in the Pseudomicrocara group, and to all the species in the genera Copiacyphon gen. nov., Spilotocyphon gen. nov., Accolabass Watts, Saltuscyphon gen. nov. and Vadumcyphon gen. nov. The male aedeagi of all new genera and species are illustrated, as are the female prehensors of some species. The following genera are described as new: Alpestriscyphon gen. nov., Anthocara gen. nov., Anocyphon gen. nov., Copiacyphon gen. nov., Furcacyphon gen. nov., Latuscara gen. nov., Pictacara gen. nov., Nasutuscyphon gen. nov., Nektriscyphon gen. nov., Pumiliocara gen. nov., Ruborcara gen. nov., Saltuscyphon gen. nov., Saprocyphon gen. nov., Sisyracyphon gen. nov., Spilotocyphon gen. nov., Tenebriocyphon gen. nov. and Vadumcyphon gen. nov. A total of 45 new combinations are proposed. The following species are described as new: Accolabass monteithi sp. nov.; Alpestriscyphon bartlefrere sp. nov., Al. spurgeon sp. nov.; Anocyphon lepus sp. nov.; Copiacyphon brindaleensis sp. nov., C. cardinalis sp. nov., C. dytikos sp. nov.; Pumiliocara peneparva sp. nov.; Ruborcara saintae sp. nov.; Saltuscyphon montanus sp. nov., Sal. teraniaensis sp. nov.; Saprocyphon bithongensis sp. nov.; Sisyracyphon brisbanensis sp. nov., S. bulburinensis sp. nov.; Spilotocyphon occidentalis sp. nov., Sp. orientalis sp. nov., Sp. zwicki sp. nov.; Vadumcyphon centralis sp. nov., V. rugosus sp. nov. A checklist of all Australian taxa in the redefined Pseudomicrocara group is included. Sequence data of the Argentinian species Pseudomicrocara antarctica (Fairmaire) is included. Phylogenetic analyses place this species as a distinct lineage within the Pseudomicrocara group.C.H.S. Watts, S.J.B. Cooper, M.L. Libonatt

A new genus, Perplexacara, and new generic placements of species of Australian marsh beetles (Coleoptera: Scirtidae) based on morphology and molecular genetic data

The Australian Scirtidae species previously identified as misplaced in the widespread genus Prionocyphon Redtenbacher are revisited as well as their possible relationship with the Australian genus Macrodascillus (Lea) using sequence data from the mitochondrial gene, cytochrome oxidase subunit 1 and two nuclear genes, elongation factor 1-alpha and Topoisomerase. The study confirmed the conclusion of Cooper et al. (2014) that the species did not belong in Prionocyphon. The study also included a species from each of three possibly related genera, Chameloscyphon Watts, Daploeuros Watts and Dasyscyphon Watts. Chameloscyphon huonensis Watts, Dasyscyphon victoriaensis Watts and Daploeuros lamingtonensis Watts were recovered as separate lineages with C. huonensis linking with Das. victoriaensis and Dap. lamingtonensis isolated. The species previously included in Prionocyphon were shown to belong in two genera, Macrodascillus and a new genus Perplexacara: Perplexacara caementum (Watts) new combination, P. latusmandibulara (Watts) new combination, P. macroflavida (Watts) new combination, Macrodascillus scalaris (Lea), M. insolitus (Watts) new combination and M. lamingtonensis (Watts) new combination.C.H.S. Watts, T.M.Bradford, S.J.B. Coope

Extreme genetic diversity among springtails (Collembola) in subterranean calcretes of arid Australia

Publication: Genome 18 June 2020The subterranean islands hypothesis for calcretes of the Yilgarn region in Western Australia applies to many stygobitic (subterranean-aquatic) species that are "trapped" evolutionarily within isolated aquifers due to their aquatic lifestyles. In contrast, little is known about the distribution of terrestrial-subterranean invertebrates associated with the calcretes. We used subterranean Collembola from the Yilgarn calcretes to test the hypothesis that troglobitic species, those inhabiting the subterranean unsaturated (non-aquatic) zone of calcretes, are also restricted in their distribution and represent reciprocally monophyletic and endemic lineages. We used the barcoding fragment of the mtDNA cytochrome c oxidase subunit 1 (COI) gene from 183 individuals to reconstruct the phylogenetic history of the genus Pseudosinella Schäffer (Collembola, Lepidocyrtidae) from 10 calcretes in the Yilgarn. These calcretes represent less than 5% of the total possible calcretes in this region, yet we show that their diversity for subterranean Collembola comprises a minimum of 25 new species. Regionally, multiple levels of diversity exist in Pseudosinella, indicative of a complex evolutionary history for this genus in the Yilgarn. These species have probably been impacted by climatic oscillations, facilitating their dispersal across the landscape. The results represent a small proportion of the undiscovered diversity in Australia's arid zone.Michelle T. Guzik, Mark I. Stevens, Steven J.B. Cooper, William F. Humphreys and Andrew D. Austi