School of BioSciences - Research Publications

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    Defining and evaluating predictions of joint species distribution models
    Wilkinson, DP ; Golding, N ; Guillera-Arroita, G ; Tingley, R ; McCarthy, MA ; Freckleton, R (WILEY, 2021-03)
    Abstract Joint species distribution models (JSDMs) simultaneously model the distributions of multiple species, while accounting for residual co‐occurrence patterns. Despite increasing adoption of JSDMs in the literature, the question of how to define and evaluate JSDM predictions has only begun to be explored. We define four different JSDM prediction types that correspond to different aspects of species distribution and community assemblage processes. Marginal predictions are environment‐only predictions akin to predictions from single‐species models; joint predictions simultaneously predict entire community assemblages; and conditional marginal and conditional joint predictions are made at the species or assemblage level, conditional on the known occurrence state of one or more species at a site. We define five different classes of metrics that can be used to evaluate these types of predictions: threshold‐dependent, threshold‐independent, community dissimilarity, species richness and likelihood metrics. We illustrate different prediction types and evaluation metrics using a case study in which we fit a JSDM to a frog occurrence dataset collected in Melbourne, Australia. Joint species distribution models present opportunities to investigate the facets of species distribution and community assemblage processes that are not possible to explore with single‐species models. We show that there are a variety of different metrics available to evaluate JSDM predictions, and that choice of prediction type and evaluation metric should closely match the questions being investigated.
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    Correlates of extinction risk in Australian squamate reptiles
    Senior, AF ; Böhm, M ; Johnstone, CP ; McGee, MD ; Meiri, S ; Chapple, DG ; Tingley, R (Wiley, 2021-09-01)
    Abstract Aim Identification of particular traits that predispose species to elevated extinction risk is an important component of proactive conservation. We capitalise on a recent strategic extinction risk assessment of all Australian squamate reptiles to identify intrinsic life history traits and extrinsic threats that correlate with extinction risk. We further assess whether extinction risk correlates differ between species impacted by different threatening processes (habitat loss vs. invasive species). Location Australia. Taxon Squamate reptiles. Methods We used the IUCN Red List data for Australian squamates, and publicly available datasets for 14 intrinsic and extrinsic traits. We used phylogenetically controlled Bayesian inference to test hypotheses regarding relationships between extinction risk and species traits, environment, and threat measures. Results We found that intrinsic characteristics (habitat specialisation, small range size and large body size), as well as extrinsic factors (high human footprint, accessibility from human population centres, cold temperatures and high rainfall), predispose a species to extinction. Similar predictors were important in threat‐specific analyses, although relationships were generally more uncertain. Conclusions Our results largely accord with those of global and regional studies of extinction risk in reptiles and of terrestrial vertebrates more broadly. Our findings illustrate that there is no single pathway to extinction among Australian squamates.
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    Environmental correlates of morphological diversity in Australian geckos
    Norris, J ; Tingley, R ; Meiri, S ; Chapple, DG ; Sandel, B (Wiley, 2021-05-01)
    Abstract Aim Climatic variation has long been regarded as a primary source of morphological variation. However, there is mixed support for the adherence of reptiles to ecogeographical hypotheses, such as Bergmann’s rule (body size decreases with temperature) and Allen’s rule (limb length increases with temperature). We quantified body and limb morphology among the diverse Australian gecko fauna (4 families, 30 genera, 226 of the 231 described species) to investigate environmental correlates of morphological variation in this radiation. Location Australia. Major taxa studied Geckos (Squamata: Gekkota; the families Gekkonidae, Carphodactylidae, Diplodactylidae and Pygopodidae). Methods We measured 20 external features of ethanol‐preserved museum specimens. We investigated whether principal component axes of morphology were correlated with three key environmental variables, and the microhabitat occupied by each species. Results Morphology varied greatly among Australian gecko families and genera, although there was a strong phylogenetic signal in morphology. After accounting for phylogeny, morphology was correlated with a species’ microhabitat use. Saxicolous species and species with variable microhabitat requirements (i.e., generalists) had larger body dimensions than terrestrial species. Saxicolous species also had longer proportional forelimbs and hindlimbs than terrestrial species. Main conclusions Our results highlight the importance of phylogeny and microhabitat use in shaping the morphology of Australian geckos. We find little evidence that Australian geckos adhere to Bergmann’s rule or Allen’s rule, suggesting that these ecogeographical hypotheses provide limited insight into the adaptive potential of lizard species to altered environmental conditions.
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    Conservation status of the world's skinks (Scincidae): Taxonomic and geographic patterns in extinction risk
    Chapple, DG ; Roll, U ; Boehm, M ; Aguilar, R ; Amey, AP ; Austin, CC ; Baling, M ; Barley, AJ ; Bates, MF ; Bauer, AM ; Blackburn, DG ; Bowles, P ; Brown, RM ; Chandramouli, SR ; Chirio, L ; Cogger, H ; Colli, GR ; Conradie, W ; Couper, PJ ; Cowan, MA ; Craig, MD ; Das, I ; Datta-Roy, A ; Dickman, CR ; Ellis, RJ ; Fenner, AL ; Ford, S ; Ganesh, SR ; Gardner, MG ; Geissler, P ; Gillespie, GR ; Glaw, F ; Greenlees, MJ ; Griffith, OW ; Grismer, LL ; Haines, ML ; Harris, DJ ; Hedges, SB ; Hitchmough, RA ; Hoskin, CJ ; Hutchinson, MN ; Ineich, I ; Janssen, J ; Johnston, GR ; Karin, BR ; Keogh, JS ; Kraus, F ; LeBreton, M ; Lymberakis, P ; Masroor, R ; McDonald, PJ ; Mecke, S ; Melville, J ; Melzer, S ; Michael, DR ; Miralles, A ; Mitchell, NJ ; Nelson, NJ ; Nguyen, TQ ; Nogueira, CDC ; Ota, H ; Pafilis, P ; Pauwels, OSG ; Perera, A ; Pincheira-Donoso, D ; Reed, RN ; Ribeiro-Junior, MA ; Riley, JL ; Rocha, S ; Rutherford, PL ; Sadlier, RA ; Shacham, B ; Shea, GM ; Shine, R ; Slavenko, A ; Stow, A ; Sumner, J ; Tallowin, OJS ; Teale, R ; Torres-Carvajal, O ; Trape, J-F ; Uetz, P ; Ukuwela, KDB ; Valentine, L ; Dyke, JUV ; van Winkel, D ; Vasconcelos, R ; Vences, M ; Wagner, P ; Wapstra, E ; While, GM ; Whiting, MJ ; Whittington, CM ; Wilson, S ; Ziegler, T ; Tingley, R ; Meiri, S (ELSEVIER SCI LTD, 2021-05)
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    A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis
    Melville, J ; Chapple, DG ; Keogh, JS ; Sumner, J ; Amey, A ; Bowles, P ; Brennan, IG ; Couper, P ; Donnellan, SC ; Doughty, P ; Edwards, DL ; Ellis, RJ ; Esquerre, D ; Fenker, J ; Gardner, MG ; Georges, A ; Haines, ML ; Hoskin, CJ ; Hutchinson, M ; Moritz, C ; Nankivell, J ; Oliver, P ; Pavon-Vazquez, CJ ; Pepper, M ; Rabosky, DL ; Sanders, K ; Shea, G ; Singhal, S ; Wilmer, JW ; Tingley, R ; Dobson, AP (PUBLIC LIBRARY SCIENCE, 2021-06)
    Global biodiversity loss is a profound consequence of human activity. Disturbingly, biodiversity loss is greater than realized because of the unknown number of undocumented species. Conservation fundamentally relies on taxonomic recognition of species, but only a fraction of biodiversity is described. Here, we provide a new quantitative approach for prioritizing rigorous taxonomic research for conservation. We implement this approach in a highly diverse vertebrate group-Australian lizards and snakes. Of 870 species assessed, we identified 282 (32.4%) with taxonomic uncertainty, of which 17.6% likely comprise undescribed species of conservation concern. We identify 24 species in need of immediate taxonomic attention to facilitate conservation. Using a broadly applicable return-on-investment framework, we demonstrate the importance of prioritizing the fundamental work of identifying species before they are lost.
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    Niche shifts and environmental non-equilibrium undermine the usefulness of ecological niche models for invasion risk assessments.
    Pili, AN ; Tingley, R ; Sy, EY ; Diesmos, MLL ; Diesmos, AC (Springer Science and Business Media LLC, 2020-05-14)
    Niche shifts and environmental non-equilibrium in invading alien species undermine niche-based predictions of alien species' potential distributions and, consequently, their usefulness for invasion risk assessments. Here, we compared the realized climatic niches of four alien amphibian species (Hylarana erythraea, Rhinella marina, Hoplobatrachus rugulosus, and Kaloula pulchra) in their native and Philippine-invaded ranges to investigate niche changes that have unfolded during their invasion and, with this, assessed the extent of niche conservatism and environmental equilibrium. We investigated how niche changes affected reciprocal transferability of ecological niche models (ENMs) calibrated using data from the species' native and Philippine-invaded ranges, and both ranges combined. We found varying levels of niche change across the species' realized climatic niches in the Philippines: climatic niche shift for H. rugulosus; niche conservatism for R. marina and K. pulchra; environmental non-equilibrium in the Philippine-invaded range for all species; and environmental non-equilibrium in the native range or adaptive changes post-introduction for all species except H. erythraea. Niche changes undermined the reciprocal transferability of ENMs calibrated using native and Philippine-invaded range data. Our paper highlights the difficulty of predicting potential distributions given niche shifts and environmental non-equilibrium; we suggest calibrating ENMs with data from species' combined native and invaded ranges, and to regularly reassess niche changes and recalibrate ENMs as species' invasions progress.
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    steps: Software for spatially and temporally explicit population simulations
    Visintin, C ; Briscoe, NJ ; Woolley, SNC ; Lentini, PE ; Tingley, R ; Wintle, BA ; Golding, N ; Graham, L (WILEY, 2020-04)
    Abstract Species population dynamics are driven by spatial and temporal changes in the environment, anthropogenic activities and conservation management actions. Understanding how populations will change in response to these drivers is fundamental to a wide range of ecological applications, but there are few open‐source software options accessible to researchers and managers that allow them to predict these changes in a flexible and transparent way. We introduce an open‐source, multi‐platform r package, steps, that models spatial changes in species populations as a function of drivers of distribution and abundance, such as climate, disturbance, landscape dynamics and species ecological and physiological requirements. To illustrate the functionality of steps, we model the population dynamics of the greater glider Petauroides volans, an arboreal Australian mammal. We demonstrate how steps can be used to simulate population responses of the glider to forest dynamics and management with the types of data commonly used in ecological analyses. steps expands on the features found in existing software packages, can easily incorporate a range of spatial layers (e.g. habitat suitability, vegetation dynamics and disturbances), facilitates integrated and transparent analyses within a single platform and produces interpretable outputs of changes in species' populations through space and time. Further, steps offers both ready‐to‐use, built‐in functionality, as well as the ability for advanced users to define their own modules for custom analyses. Thus, we anticipate that steps will be of significant value to environment and wildlife managers and researchers from a broad range of disciplines.
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    Accounting for false positive detections in occupancy studies based on environmental DNA: A case study of a threatened freshwater fish (Galaxiella pusilla)
    Tingley, R ; Coleman, R ; Gecse, N ; van Rooyen, A ; R. Weeks, A (Wiley, 2021-03-01)
    Abstract Environmental DNA (eDNA) sampling is a promising method for surveying aquatic fauna. Recent eDNA studies have investigated the likelihood of false negative errors in the laboratory and in the field, but the likelihood of false positives remains poorly studied. We investigated the likelihood of both types of errors in eDNA surveys of an Australian threatened freshwater fish (Galaxiella pusilla) using laboratory experiments, field surveys, and recent advances in hierarchical site occupancy‐detection modeling. Laboratory experiments revealed high primer/probe specificity; absence of sample contamination in extraction and qPCR blanks; and rapid accumulation and deterioration of eDNA in aquaria. Hierarchical site occupancy‐detection models fitted to pilot data collected at 13 wetlands revealed that two water samples, each with two qPCRs, would be required to achieve a cumulative detection probability >.95. A more comprehensive survey, in which we simultaneously used dip netting and eDNA sampling at 29 wetlands, revealed similar mean detection probabilities of the two sampling methods (trapping: 0.74 vs. eDNA: 0.68), and low probabilities of false positive errors at the water sample level (0.0080) and at the qPCR level (0.0039) for eDNA sampling. Collectively, our results illustrate that eDNA sampling can be a sensitive and specific method for monitoring the occurrence of freshwater fauna. Detection probabilities of eDNA sampling were comparable to those of a traditional sampling method, and probabilities of laboratory‐induced false positives were low. Future studies employing eDNA sampling should estimate, and properly account for, false positive errors in addition to false negatives.
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    Multispecies models reveal that eDNA metabarcoding is more sensitive than backpack electrofishing for conducting fish surveys in freshwater streams
    McColl-Gausden, EF ; Weeks, AR ; Coleman, RA ; Robinson, KL ; Song, S ; Raadik, TA ; Tingley, R (WILEY, 2021-07)
    Environmental DNA (eDNA) sampling can provide accurate, cost-effective, landscape-level data on species distributions. Previous studies have compared the sensitivity of eDNA sampling to traditional sampling methods for single species, but similar comparative studies on multispecies eDNA metabarcoding are rare. Using hierarchical site occupancy detection models, we examined whether key choices associated with eDNA metabarcoding (primer selection, low-abundance read filtering and the number of positive water samples used to classify a species as present at a site) affect the sensitivity of metabarcoding, relative to backpack electrofishing for fish in freshwater streams. Under all scenarios (teleostei and vertebrate primers; 0%, 0.1% and 1% read filtering thresholds; one or two positive samples required to classify species as present), we found that eDNA metabarcoding is, on average, more sensitive than electrofishing. Combining vertebrate and teleostei markers resulted in higher detection probabilities relative to the use of either marker in isolation. Increasing the threshold used to filter low-abundance reads decreased species detection probabilities but did not change our overall finding that eDNA metabarcoding was more sensitive than electrofishing. Using a threshold of two positive water samples (out of five) to classify a species as present typically had negligible effects on detection probabilities compared to using one positive water sample. Our findings demonstrate that eDNA metabarcoding is generally more sensitive than electrofishing for conducting fish surveys in freshwater streams, and that this outcome is not sensitive to methodological decisions associated with metabarcoding.
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    The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients
    Enriquez-Urzelai, U ; Tingley, R ; Kearney, MR ; Sacco, M ; Palacio, AS ; Tejedo, M ; Nicieza, AG ; Marske, K (WILEY, 2020-07)
    The vulnerability of species to climate change is jointly influenced by geographic phenotypic variation, acclimation and behavioural thermoregulation. The importance of interactions between these factors, however, remains poorly understood. We demonstrate how advances in mechanistic niche modelling can be used to integrate and assess the influence of these sources of uncertainty in forecasts of climate change impacts. We explored geographic variation in thermal tolerance (i.e. maximum and minimum thermal limits) and its potential for acclimation in juvenile European common frogs Rana temporaria along elevational gradients. Furthermore, we employed a mechanistic niche model (NicheMapR) to assess the relative contributions of phenotypic variation, acclimation and thermoregulation in determining the impacts of climate change on thermal safety margins and activity windows. Our analyses revealed that high-elevation populations had slightly wider tolerance ranges driven by increases in heat tolerance but lower potential for acclimation. Plausibly, wider thermal fluctuations at high elevations favour more tolerant but less plastic phenotypes, thus reducing the risk of encountering stressful temperatures during unpredictable extreme events. Biophysical models of thermal exposure indicated that observed phenotypic and plastic differences provide limited protection from changing climates. Indeed, the risk of reaching body temperatures beyond the species' thermal tolerance range was similar across elevations. In contrast, the ability to seek cooler retreat sites through behavioural adjustments played an essential role in buffering populations from thermal extremes predicted under climate change. Predicted climate change also altered current activity windows, but high-elevation populations were predicted to remain more temporally constrained than lowland populations. Our results demonstrate that elevational variation in thermal tolerances and acclimation capacity might be insufficient to buffer temperate amphibians from predicted climate change; instead, behavioural thermoregulation may be the only effective mechanism to avoid thermal stress under future climates.