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Clare, E. L.

Publications and source records attributed to Clare, E. L..

11 recordsLinked to original sources

Contrasted effects of human pressure on biodiversity in the UK: a multi-taxonomic assessment using airborne environmental DNA

Human activities have significantly modified habitats, resulting in a global biodiversity crisis. Here, we leveraged the first national-scale biodiversity survey based on airborne environmental DNA, comparing the effects of three human pressure indices increasing in complexity and scope across diverse vertebrates, insects, plants and fungi. While most taxa exhibited higher diversity in urban areas compared to rural ones, we uncovered more complex patterns using the landscape-pollution and human footprint indices, including dual diversity peaks at both high and moderate levels of human pressure. We also show an effect of human pressure on community composition even when local species richness remained stable: regardless of the human pressure index, anthropogenic sites were mostly characterized by synanthropic and invasive species. Overall, our results underscore the complex interactions among anthropogenic pressures, taxon diversity and community composition, demonstrating the value of multi-taxon analyses and multiple indices to better understand biodiversity patterns at large scales.

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First national survey of terrestrial biodiversity using airborne eDNA

Near real-time data across taxa are necessary for quantifying biodiversity at regional to continental scales and evaluating conservation measures. Yet, standardized methods and globally distributed infrastructure are still lacking. In this study, we conducted the first national survey of terrestrial biodiversity using a metabarcoding approach on airborne environmental DNA collected by a national ambient air quality monitoring network. Our goal was to perform a multi-taxonomic biodiversity assessment at a national scale, compare detections with those of another large-scale monitoring approach (citizen sciences) and estimate a tentative minimum eDNA transportation distance. We identified over 1,100 taxa, including vertebrates, invertebrates, protists, fungi and plants covering a wide range of life history traits and ecological niches. Citizen science and eDNA detections were complementary, with eDNA better mapping less charismatic and difficult to spot taxa, demonstrating its potential to align with global conservation goals. Airborne eDNA signals were relatively local, likely due to the deposition of the larger particles from the air over shorter distances and limited wind transportation at near ground level. Overall, our results show that molecular protocols integrated into existing air quality monitoring networks can provide standardized, biodiversity monitoring at relatively low field cost, with potential for broad scalability.

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Variable responses of individual species to tropical forest degradation

The functional stability of ecosystems depends greatly on interspecific differences in responses to environmental perturbation. However, responses to perturbation are not necessarily invariant among populations of the same species, so intraspecific variation in responses might also contribute. Such inter-population response diversity has recently been shown to occur spatially across species ranges, but we lack estimates of the extent to which individual populations across an entire community might have perturbation responses that vary through time. We assess this using 524 taxa that have been repeatedly surveyed for the effects of tropical forest logging at a focal landscape in Sabah, Malaysia. Just 39 % of taxa - all with non-significant responses to forest degradation - had invariant responses. All other taxa (61 %) showed significantly different responses to the same forest degradation gradient across surveys, with 6 % of taxa responding to forest degradation in opposite directions across multiple surveys. Individual surveys had low power (< 80 %) to determine the correct direction of response to forest degradation for one-fifth of all taxa. Recurrent rounds of logging disturbance increased the prevalence of intra-population response diversity, while uncontrollable environmental variation and/or turnover of intraspecific phenotypes generated variable responses in at least 44 % of taxa. Our results show that the responses of individual species to local environmental perturbations are remarkably flexible, likely providing an unrealised boost to the stability of disturbed habitats such as logged tropical forests.

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Logging alters tropical forest structure, while conversion reduces biodiversity and functioning

The impacts of degradation and deforestation on tropical forests are poorly understood, particularly at landscape scales. We present an extensive ecosystem analysis of the impacts of logging and conversion of tropical forest to oil palm from a large-scale study in Borneo, synthesizing responses from 82 variables categorized into four ecological levels spanning a broad suite of ecosystem properties: 1) structure and environment, 2) species traits, 3) biodiversity, and 4) ecosystem functions. Responses were highly heterogeneous and often complex and non-linear. Variables that were directly impacted by the physical process of timber extraction, such as soil structure, were sensitive to even moderate amounts of logging, whereas measures of biodiversity and ecosystem functioning were generally resilient to logging but more affected by conversion to oil palm plantation. One-Sentence SummaryLogging tropical forest mostly impacts structure while biodiversity and functions are more vulnerable to habitat conversion.

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Out of thin air: surveying tropical bat roosts through air sampling of eDNA

Understanding roosting behaviour is essential to bat conservation and biomonitoring, often providing the most accurate methods of assessing population size and health. However, roosts can be challenging to survey. Roosts can be physically impossible to access or present risks for researchers and disturbance during monitoring can disrupt natural bat behaviour and present material risks to the population e.g. disrupting hibernation cycles. One solution to this is the use of non-invasive monitoring approaches. Environmental (e)DNA has proven especially effective at detecting rare and elusive species particularly in hard-to-reach locations. It has recently been demonstrated that eDNA is carried in air and, when collected in semi-confined spaces can provide remarkably accurate profiles of biodiversity, even in complex tropical communities. In this study we deploy novel airborne eDNA collection for air for the first time in a natural setting and use this approach to survey difficult to access potential roosts in the neotropics. Using airborne eDNA we confirmed the presence of bats in 9 out of 12 roosts. The identified species matched previous historical records of roost use obtained from photographic and live capture methods demonstrating the utility of this approach. We also detected the presence of the white-winged vampire bat (Diaemus youngi) which had never been confirmed in the area but was long suspected. In addition to the bats, we also detected several non-bat vertebrates, including the big-eared climbing rat (Ototylomys phyllotis), which has previously been observed in and around bat roosts. We also detected eDNA from other local species known to be in the vicinity. Using airborne eDNA to detect new roosts and monitor known populations, particularly when species turnover is rapid, could maximize efficiency for surveyors while minimizing disturbance to the animals. This study presents the first applied use of airborne eDNA collection for ecological analysis and demonstrates a clear utility for this technology in the wild.

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Selective logging shows no impact on the dietary breadth of the fawn leaf-nosed bat (Hipposideros cervinus)

Logging activities degrade forest habitats across large areas of the tropics, but the impacts on trophic interactions that underpin forest ecosystems are poorly understood. DNA metabarcoding provides an invaluable tool to investigate such interactions, allowing analysis at a far greater scale and resolution than has previously been possible. We analysed the diet of the insectivorous fawn leaf-nosed bat Hipposideros cervinus across a forest disturbance gradient in Borneo, using a dataset of ecological interactions from an unprecedented number of bat-derived faecal samples. Bats predominantly consumed insects from the orders Lepidoptera, Blattodea, Diptera and Coleoptera, and the taxonomic composition of their diet remained relatively consistent across sites regardless of logging disturbance. There was little difference in the richness of prey consumed in each logging treatment, indicating potential resilience of this species to habitat degradation. In fact, bats consumed a high richness of prey items, and intensive sampling is needed to reliably compare feeding ecology over multiple sites regardless of the bioinformatic procedures used.

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Measuring biodiversity from DNA in the air

Impacts of the biodiversity crisis far exceed our ability to monitor changes in terrestrial ecosystems. Environmental DNA has revolutionized aquatic biomonitoring, permitting remote population and diversity assessments. Here we demonstrate that DNA from terrestrial animals can now be collected from the air under natural conditions, a ground-breaking advance for terrestrial biomonitoring. Using air samples from a zoological park, where species are spatially confined and unique compared to native fauna, we show that DNA in air can be used to identify the captive species and their potential interactions with local taxa. Air samples contained DNA from 25 species of mammal and bird including 17 known (and distinct) terrestrial zoo species. We also identified food items from air sampled in enclosures and detected four taxa native to the local area, including the Eurasian hedgehog, endangered in the UK, and the muntjac deer, a locally established invasive species. Our data provide evidence that airDNA is concentrated around recently inhabited areas (e.g., indoor enclosures) but that there is dispersal away from the source suggesting an ecology to airDNA movement which highlights the potential for airDNA sampling at distance. Our data clearly demonstrate the profound potential of air as a source of DNA for global terrestrial biomonitoring and ecological analysis. Significance StatementThe global decline in biodiversity requires rapid non-invasive biomonitoring tools applicable at a global scale. In this study we collect environmental DNA from mammals and birds from air samples collected in a natural setting. Using only air, we identified 25 species of mammal and bird known to be in the area. Our dataset detected species at risk of local extinction and several confirmed predator-prey interactions. This approach will revolutionize terrestrial biodiversity surveys.

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Dung beetles as vertebrate samplers: a test of high throughput analysis of dung beetle iDNA

The application of environmental DNA (eDNA) sampling in biodiversity surveys has gained widespread acceptance, especially in aquatic systems where free eDNA can be readily collected by filtering water. In terrestrial systems, eDNA-based approaches for assaying vertebrate biodiversity have tended to rely on blood-feeding invertebrates, including leeches and mosquitoes (termed invertebrate-derived DNA or iDNA). However, a key limitation of using blood-feeding taxa as samplers is that they are difficult to trap, and, in the case of leeches, are highly restricted to humid forest ecosystems. Dung beetles (superfamily Scarabaeoidea) feed on the faecal matter of terrestrial vertebrates and offer several potential benefits over blood-feeding invertebrates as samplers of vertebrate DNA. Importantly, these beetles can be easily captured in large numbers using simple, inexpensive baited traps; are globally distributed; and also occur in a wide range of biomes, allowing mammal diversity to be compared across habitats. In this exploratory study, we test the potential utility of dung beetles as vertebrate samplers by sequencing the mammal DNA contained within their guts. First, using a controlled feeding experiment, we show that mammalian DNA can be retrieved from the guts of large dung beetles (Catharsius renaudpauliani) for up to 10 hours after feeding. Second, by combining high-throughput sequencing of a multi-species assemblage of dung beetles with PCR replicates, we show that multiple mammal taxa can be identified with high confidence. By providing preliminary evidence that dung beetles can be used as a source of mammal DNA, our study highlights the potential for this widespread group to be used in future biodiversity monitoring surveys.

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Altered structure and stability of bat-prey interaction networks in logged tropical forests revealed by metabarcoding

O_LIHabitat degradation is pervasive across the tropics and is particularly acute in Southeast Asia, with major implications for biodiversity. Much research has addressed the impact of degradation on species diversity; however, little is known about how ecological interactions are altered, including those that constitute important ecosystem functions such as pest consumption. C_LIO_LIWe examined how rainforest degradation alters trophic interaction networks linking insectivorous bats and their prey. We used DNA metabarcoding to study the diets of forest-dwelling insectivorous bat species, and compared bat-prey interaction networks between old growth forest and forest degraded by logging in Sabah, Borneo. C_LIO_LIWe predicted that rainforest degradation would cause measurable reductions in the numbers of prey consumed by individual bats, and that this degradation would yield networks in logged forest with lower functional complementarity, modularity and nestedness than those in old growth forest. C_LIO_LICompared to bats in old growth rainforest, bats in logged sites consumed a lower diversity of prey. Their interaction networks were less nested and had a more modular structure in which bat species had lower closeness centrality scores than in old growth forest. These network structures were associated with reduced network redundancy and thus increased vulnerability to perturbations in logged forests. C_LIO_LIOur results show how ecological interactions change between old growth and logged forests, with potentially negative implications for ecosystem function and network stability. We also highlight the potential importance of insectivorous bats in consuming invertebrate pests. C_LI Malay abstractO_LIDegradasi habitat merupakan suatu fenomena yang berleluasa dikawasan tropika, terutamanya di Asia Tenggara dengan implikasi yang besar ke atas biodiversiti. Banyak kajian telahpun meneliti impak degradasi habitat atas kepelbagaian spesis. Walau bagaimanapun, dari segi mana interaksi ekologi diubah suai kurang diselidik, termasuk interaksi yang membentuk fungsi ekosistem yang penting seperti pemakanan binatang perosak. C_LIO_LIKami telah memeriksa bagaimana degradasi hutan hujan tropika dapat mengubah suai interaksi antara tahap trofik yang menghubungkan kelawar yang memakan serangga dan mangsa mereka. Kami telah menggunakan "DNA metabarcoding" untuk mengenal pasti kandungan artropod dalam sampel najis kelawar and membandingkan jaringan interaksi kelawar dan mangsa mereka diantara hutan dara dan hutan yang telah dibalak di Sabah, Borneo. C_LIO_LIKami meramalkan bahawa degradasi hutan hujan akan menyebabkan kekurangan dalam bilangan nod mangsa yang dimakan oleh setiap individu kelawar yang dapat diukur. Degradasi ini pula boleh menghasilkan jaringan yang mempunyai fungsi saling melengkapi dan modulariti yang rendah, dan lebih berkelompok atau "mempunyai "nestedness" yang lebih tinggi di hutan yang dibalak berbanding hutan dara. C_LIO_LIKelawar di kawasan hutan yang dibalak memakan diversiti mangsa yang lebih rendah dengan kelawar di habitat hutan hujan dara. Jaringan-jaringan interaksi mereka kurang berkelompok dan mempunyai stuktur yang lebih modular dimana spesis kelawar mempunyai pemarkahan kerapatan berpusat yang lebih rendah daripada sepesis kelawar di hutan dara. Struktur-struktur jaringan ini berkait dengan lebihan jaringan atau "network redundancy" yang lebih rendah and ini membawa kepada kerentantan yang meningkat terhadap gangguan luar di hutan yang telah dibalak. C_LIO_LIKeputusan kami menunjukkan bagaimana interaksi ekologi berubah diantara hutan dara dan hutan yang dibalak, dengan potensi implikasi negatif untuk fungsi ekosistem dan kestabilan jaringan. Kami juga telah menunjukkan potensi kepentingan kelawar yang memakan serangga dalam fungsi mereka untuk makan perosak invertebrat. C_LI Data Accessibility StatementData are currently archived at the Centre for Ecology and Hydrology Environmental Information Data Centre (https://doi.org/10.5285/8b106445-d8e0-482c-b517-5a372a09dc91) and will be released from embargo following publication. Specific analysis scripts are available on GitHub with links given in the manuscript and will be archived on Zenodo prior to publication. Statement of authorshipSR, EC, DHB, MS and OTL conceived the project, DHB, VK and JB undertook field collections and laboratory work, DHB analysed the data with input from EC, and DHB wrote the manuscript with input from all authors.

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Assessing the impact of taxon resolution on network structure, with implication for comparative ecology

Constructing networks has become an indispensable approach in understanding how different taxa interact. However, methodologies vary widely among studies, potentially limiting our ability to meaningfully compare results. In particular, how network architecture is influenced by the extent to which nodes are resolved to either taxa or taxonomic units is poorly understood. To address this, here we collate nine datasets of ecological interactions, from both observations and DNA metabarcoding, and construct networks under a range of commonly-used node resolutions. We demonstrate that small changes in node resolution can cause wide variation in almost all key metric values, including robustness and nestedness. Moreover, relative values of metrics such as robustness were seen to fluctuate continuously with node resolution, thereby potentially confounding comparisons of networks, as well as interpretations concerning their constituent ecological interactions. These findings highlight the need for care when comparing networks, especially where these differ with respect to node resolution.\n\nStatement of authorshipDRHB, SJR and ELC conceived of the project, DRHB facilitated fieldwork in Malaysia, DRHB, HFMO and ELC undertook field collections, DRHB, SCLC and HFMO analysed the data, and DRHB wrote the manuscript with input from all authors.\n\nData Accessibility StatementAll data used in this analysis will be archived in Dryad and made available by DOI. Specific analysis scripts are available on GitHub with links given in the manuscript.

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Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data?

Advances in DNA sequencing technology have revolutionised the field of molecular analysis of trophic interactions and it is now possible to recover counts of food DNA barcode sequences from a wide range of dietary samples. But what do these counts mean? To obtain an accurate estimate of a consumers diet should we work strictly with datasets summarising the frequency of occurrence of different food taxa, or is it possible to use the relative number of sequences? Both approaches are applied in the dietary metabarcoding literature, but occurrence data is often promoted as a more conservative and reliable option due to taxa-specific biases in recovery of sequences. Here, we point out that diet summaries based on occurrence data overestimate the importance of food consumed in small quantities (potentially including low-level contaminants) and are sensitive to the count threshold used to define an occurrence. Our simulations indicate that even with recovery biases incorporated, using relative read abundance (RRA) information can provide a more accurate view of population-level diet in many scenarios. The ideas presented here highlight the need to consider all sources of bias and to justify the methods used to interpret count data in dietary metabarcoding studies. We encourage researchers to continue to addressing methodological challenges, and acknowledge unanswered questions to help spur future investigations in this rapidly developing area of research.

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