Ongoing declines for the world's amphibians in the face of emerging threats.

Systematic assessments of species extinction risk at regular intervals are necessary for informing conservation action1,2. Ongoing developments in taxonomy, threatening processes and research further underscore the need for reassessment3,4. Here we report the findings of the second Global Amphibian Assessment, evaluating 8,011 species for the International Union for Conservation of Nature Red List of Threatened Species. We find that amphibians are the most threatened vertebrate class (40.7% of species are globally threatened). The updated Red List Index shows that the status of amphibians is deteriorating globally, particularly for salamanders and in the Neotropics. Disease and habitat loss drove 91% of status deteriorations between 1980 and 2004. Ongoing and projected climate change effects are now of increasing concern, driving 39% of status deteriorations since 2004, followed by habitat loss (37%). Although signs of species recoveries incentivize immediate conservation action, scaled-up investment is urgently needed to reverse the current trends.

Populating a Continent: Phylogenomics Reveal the Timing of Australian Frog Diversification.

The Australian continent's size and isolation make it an ideal place for studying the accumulation and evolution of biodiversity. Long separated from the ancient supercontinent Gondwana, most of Australia's plants and animals are unique and endemic, including the continent's frogs. Australian frogs comprise a remarkable ecological and morphological diversity categorized into a small number of distantly related radiations. We present a phylogenomic hypothesis based on an exon-capture dataset that spans the main clades of Australian myobatrachoid, pelodryadid hyloid, and microhylid frogs. Our time-calibrated phylogenomic-scale phylogeny identifies great disparity in the relative ages of these groups which vary from Gondwanan relics to recent immigrants from Asia and include arguably the continent's oldest living vertebrate radiation. This age stratification provides insight into the colonization of⁠, and diversification on, the Australian continent through deep time, during periods of dramatic climatic and community changes. Contemporary Australian frog diversity highlights the adaptive capacity of anurans, particularly in response to heat and aridity, and explains why they are one of the continent's most visible faunas.

A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis.

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.

Initiation of speciation across multiple dimensions in a rock-restricted, tropical lizard.

Population isolation and concomitant genetic divergence, resulting in strong phylogeographical structure, is a core aspect of speciation initiation. If and how speciation then proceeds and ultimately completes depends on multiple factors that mediate reproductive isolation, including divergence in genomes, ecology and mating traits. Here we explored these multiple dimensions in two young (Plio-Pleistocene) species complexes of gekkonid lizards (Heteronotia) from the Kimberley-Victoria River regions of tropical Australia. Using mitochondrial DNA screening and exon capture phylogenomics, we show that the rock-restricted Heteronotia planiceps exhibits exceptional fine-scale phylogeographical structure compared to the codistributed habitat generalist Heteronotia binoei. This indicates pervasive population isolation and persistence in the rock-specialist, and thus a high rate of speciation initiation across this geographically complex region, with levels of genomic divergence spanning the "grey zone" of speciation. Proximal lineages of H. planiceps were often separated by different rock substrates, suggesting a potential role for ecological isolation; however, phylogenetic incongruence and historical introgression were inferred between one such pair. Ecomorphological divergence among lineages within both H. planiceps and H. binoei was limited, except that limestone-restricted lineages of H. planiceps tended to be larger than rock-generalists. By contrast, among-lineage divergence in the chemical composition of epidermal pore secretions (putative mating trait) exceeded ecomorphology in both complexes, but with less trait overlap among lineages in H. planiceps. This system-particularly the rock-specialist H. planiceps-highlights the role of multidimensional divergence during incipient speciation, with divergence in genomes, ecomorphology and chemical signals all at play at very fine spatial scales.

The first linkage map for Australo-Papuan Treefrogs (family: Pelodryadidae) reveals the sex-determination system of the Green-eyed Treefrog (Litoria serrata).

Amphibians represent a useful taxon to study the evolution of sex determination because of their highly variable sex-determination systems. However, the sex-determination system for many amphibian families remains unknown, in part because of a lack of genomic resources. Here, using an F1 family of Green-eyed Treefrogs (Litoria serrata), we produce the first genetic linkage map for any Australo-Papuan Treefrogs (family: Pelodryadidae). The resulting linkage map contains 8662 SNPs across 13 linkage groups. Using an independent set of sexed adults, we identify a small region in linkage group 6 matching an XY sex-determination system. These results suggest Litoria serrata possesses a male heterogametic system, with a candidate sex-determination locus on linkage group 6. Furthermore, this linkage map represents the first genomic resource for Australo-Papuan Treefrogs, an ecologically diverse family of over 220 species.

Linking physiology and climate to infer species distributions in Australian skinks.

Climate has a key impact on animal physiology, which in turn can have a profound influence on geographic distributions. Yet, the mechanisms linking climate, physiology and distribution are not fully resolved. Using an integrative framework, we tested the predictions of the climatic variability hypothesis (CVH), which states that species with broader distributions have broader physiological tolerance than range-restricted species, in a group of Lampropholis skinks (8 species, 196 individuals) along a latitudinal gradient in eastern Australia. We investigated several physiological aspects including metabolism, water balance, thermal physiology, thermoregulatory behaviour and ecological performance. Additionally, to test whether organismal information (e.g. behaviour and physiology) can enhance distribution models, hence providing evidence that physiology and climate interact to shape range sizes, we tested whether species distribution models incorporating physiology better predict the range sizes than models using solely climatic layers. In agreement with the CVH, our results confirm that widespread species can tolerate and perform better at broader temperature ranges than range-restricted species. We also found differences in field body temperatures, but not thermal preference, between widespread and range-restricted species. However, metabolism and water balance did not correlate with range size. Biophysical modelling revealed that the incorporation of physiological and behavioural data improves predictions of Lampropholis distributions compared with models based solely on macroclimatic inputs, but mainly for range-restricted species. By integrating several aspects of the physiology and niche modelling of a group of ectothermic animals, our study provides evidence that physiology correlates with species distributions. Physiological responses to climate are central in establishing geographic ranges of skinks, and the incorporation of processes occurring at local scales (e.g. behaviour) can improve species distribution models.

Composition of a chemical signalling trait varies with phylogeny and precipitation across an Australian lizard radiation.

The environment presents challenges to the transmission and detection of animal signalling systems, resulting in selective pressures that can drive signal divergence amongst populations in disparate environments. For chemical signals, climate is a potentially important selective force because factors such as temperature and moisture influence the persistence and detection of chemicals. We investigated an Australian lizard radiation (Heteronotia) to explore relationships between a sexually dimorphic chemical signalling trait (epidermal pore secretions) and two key climate variables: temperature and precipitation. We reconstructed the phylogeny of Heteronotia with exon capture phylogenomics, estimated phylogenetic signal in amongst-lineage chemical variation and assessed how chemical composition relates to temperature and precipitation using multivariate phylogenetic regressions. High estimates of phylogenetic signal indicate that the composition of epidermal pore secretions varies amongst lineages in a manner consistent with Brownian motion, although there are deviations to this, with stark divergences coinciding with two phylogenetic splits. Accounting for phylogenetic non-independence, we found that amongst-lineage chemical variation is associated with geographic variation in precipitation but not temperature. This contrasts somewhat with previous lizard studies, which have generally found an association between temperature and chemical composition. Our results suggest that geographic variation in precipitation can affect the evolution of chemical signalling traits, possibly influencing patterns of divergence amongst lineages and species.

Are Pheromones Key to Unlocking Cryptic Lizard Diversity?

Animals use mating traits to compete for, attract, and choose mates. Because mating traits influence mate choice, the divergence of mating traits between populations can result in reproductive isolation. This can occur without associated morphological divergence, producing reproductively isolated cryptic species that are visually indistinguishable. Thus, identifying the mating traits in morphologically conservative groups is key to resolving diversity and speciation processes. Lizards contain many such groups, with phylogeographic studies often revealing highly divergent but morphologically cryptic lineages within species. Considering that cryptic lizard species can be sympatric but morphologically indistinguishable, we hypothesize that candidate species will exhibit divergent pheromones and that pheromones will have typically diverged more than morphology. To test this, we used gas chromatography to characterize pheromones (epidermal pore secretions) from 10 genetically divergent lineages of the Bynoe's gecko (Heteronotia binoei) species complex in northern Australia. Multivariate analyses of pheromone blends and morphology indicate that pheromones are lineage specific and have diverged relatively more than morphology. Such specificity suggests that pheromones influence behavioral isolation in this morphologically conservative lizard radiation. These results suggest that pheromone data may unlock the tremendous cryptic diversity currently being uncovered in many lizard groups.

A Framework for Resolving Cryptic Species: A Case Study from the Lizards of the Australian Wet Tropics.

As we collect range-wide genetic data for morphologically-defined species, we increasingly unearth evidence for cryptic diversity. Delimiting this cryptic diversity is challenging, both because the divergences span a continuum and because the lack of overt morphological differentiation suggests divergence has proceeded heterogeneously. Herein, we address these challenges as we diagnose and describe species in three co-occurring species groups of Australian lizards. By integrating genomic and morphological data with data on hybridization and introgression from contact zones, we explore several approaches-and their relative benefits and weaknesses-for testing the validity of cryptic lineages. More generally, we advocate that genetic delimitations of cryptic diversity must consider whether these lineages are likely to be durable and persistent through evolutionary time.

Beyond the model: expert knowledge improves predictions of species' fates under climate change.

The need to proactively manage landscapes and species to aid their adaptation to climate change is widely acknowledged. Current approaches to prioritizing investment in species conservation generally rely on correlative models, which predict the likely fate of species under different climate change scenarios. Yet, while model statistics can be improved by refining modeling techniques, gaps remain in understanding the relationship between model performance and ecological reality. To investigate this, we compared standard correlative species distribution models to highly accurate, fine-scale, distribution models. We critically assessed the ecological realism of each species' model, using expert knowledge of the geography and habitat in the study area and the biology of the study species. Using interactive software and an iterative vetting with experts, we identified seven general principles that explain why the distribution modeling under- or overestimated habitat suitability, under both current and predicted future climates. Importantly, we found that, while temperature estimates can be dramatically improved through better climate downscaling, many models still inaccurately reflected moisture availability. Furthermore, the correlative models did not account for biotic factors, such as disease or competitor species, and were unable to account for the likely presence of micro refugia. Under-performing current models resulted in widely divergent future projections of species' distributions. Expert vetting identified regions that were likely to contain micro refugia, even where the fine-scale future projections of species distributions predicted population losses. Based on the results, we identify four priority conservation actions required for more effective climate change adaptation responses. This approach to improving the ecological realism of correlative models to understand climate change impacts on species can be applied broadly to improve the evidence base underpinning management responses.

Phylogenomics of a rapid radiation: the Australian rainbow skinks.

BACKGROUND: The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such as the multispecies coalescent (MSC) model. However, the MSC makes strong assumptions about divergence history and population structure, and when using the full Bayesian implementation, current computational limits mean that relatively few loci and samples can be analysed for even modest sized radiations. We explore these issues through analyses of an extensive (> 1000 loci) dataset for the Australian rainbow skinks. This group consists of 3 genera and 41 described species, which likely diversified rapidly in Australia during the mid-late Miocene to occupy rainforest, woodland, and rocky habitats with corresponding diversity of morphology and breeding colouration. Previous phylogenetic analyses of this group have revealed short inter-nodes and high discordance among loci, limiting the resolution of inferred trees. A further complication is that many species have deep phylogeographic structure - this poses the question of how to sample individuals within species for analyses using the MSC. RESULTS: Phylogenies obtained using concatenation and summary coalescent species tree approaches to the full dataset are well resolved with generally consistent topology, including for previously intractable relationships near the base of the clade. As expected, branch lengths at the tips are substantially overestimated using concatenation. Comparisons of different strategies for sampling haplotypes for full Bayesian MSC analyses (for one clade and using smaller sets of loci) revealed, unexpectedly, that combining haplotypes across divergent phylogeographic lineages yielded consistent species trees. CONCLUSIONS: This study of more than 1000 loci provides a strongly-supported estimate of the phylogeny of the Australian rainbow skinks, which will inform future research on the evolution and taxonomy of this group. Our analyses suggest that species tree estimation with the MSC can be quite robust to violation of the assumption that the individuals representing a taxon are sampled from a panmictic population.

The impact of parasites during range expansion of an invasive gecko.

Host-parasite dynamics can play a fundamental role in both the establishment success of invasive species and their impact on native wildlife. The net impact of parasites depends on their capacity to switch effectively between native and invasive hosts. Here we explore host-switching, spatial patterns and simple fitness measures in a slow-expanding invasion: the invasion of Asian house geckos (Hemidactylus frenatus) from urban areas into bushland in Northeast Australia. In bushland close to urban edges, H. frenatus co-occurs with, and at many sites now greatly out-numbers, native geckos. We measured prevalence and intensity of Geckobia mites (introduced with H. frenatus), and Waddycephalus (a native pentastome). We recorded a new invasive mite species, and several new host associations for native mites and geckos, but we found no evidence of mite transmission between native and invasive geckos. In contrast, native Waddycephalus nymphs were commonly present in H. frenatus, demonstrating this parasite's capacity to utilize H. frenatus as a novel host. Prevalence of mites on H. frenatus decreased with distance from the urban edge, suggesting parasite release towards the invasion front; however, we found no evidence that mites affect H. frenatus body condition or lifespan. Waddycephalus was present at low prevalence in bushland sites and, although its presence did not affect host body condition, our data suggest that it may reduce host survival. The high relative density of H. frenatus at our sites, and their capacity to harbour Waddycephalus, suggests that there may be impacts on native geckos and snakes through parasite spillback.

Extinction debt from climate change for frogs in the wet tropics.

The effect of twenty-first-century climate change on biodiversity is commonly forecast based on modelled shifts in species ranges, linked to habitat suitability. These projections have been coupled with species-area relationships (SAR) to infer extinction rates indirectly as a result of the loss of climatically suitable areas and associated habitat. This approach does not model population dynamics explicitly, and so accepts that extinctions might occur after substantial (but unknown) delays-an extinction debt. Here we explicitly couple bioclimatic envelope models of climate and habitat suitability with generic life-history models for 24 species of frogs found in the Australian Wet Tropics (AWT). We show that (i) as many as four species of frogs face imminent extinction by 2080, due primarily to climate change; (ii) three frogs face delayed extinctions; and (iii) this extinction debt will take at least a century to be realized in full. Furthermore, we find congruence between forecast rates of extinction using SARs, and demographic models with an extinction lag of 120 years. We conclude that SAR approaches can provide useful advice to conservation on climate change impacts, provided there is a good understanding of the time lags over which delayed extinctions are likely to occur.

A portable Raspberry Pi-based camera set-up to record behaviours of frogs and other small animals under artificial or natural shelters in remote locations.

We describe a Raspberry Pi-based camera system that is portable, robust and weatherproof, with a close-up focus (2.5 cm). We show that this camera system can be used in remote locations with high rainfall and humidity. The camera has an Infrared LED light to film in dark places and can continuously record up to 21 days (504 h). We also describe how to make concrete artificial shelters to mount the camera in. One of the great strengths of this shelter/camera set-up is that the animals choose to take up residence and can then be filmed for extended periods with no disturbance. Furthermore, we give examples of how shelters and cameras could be used to film a range of behaviours in not only many small cryptic amphibian species but also other small vertebrates and invertebrates globally.

A new frog species (Microhylidae:Cophixalus) from boulder-pile habitat of Cape Melville, north-east Australia.

In Australia, microhylid frogs are found almost exclusively in the tropical north-east, but in this region diversity is high. Sixteen species occur in the Wet Tropics region and a further six species are found further north on Cape York Peninsula. Most Australian microhylid species belong to the genus Cophixalus (18 species). The majority of these have highly localized distributions, with two-thirds being found on single mountain ranges. While most Cophixalus are small (10-29 mm snout to vent length) rainforest species, four differ dramatically in morphology and ecology, being large (30-53 mm) species that inhabit isolated areas ofjumbled boulder-pile habitat. Here I describe a new species of Cophixalus from boulder-pile habitat in the Melville Range on Cape Melville, north-east Cape York Peninsula. Cophixalus petrophilus sp. nov. is highly distinct from all congeners in morphology, colour pattern and mating call. This species is restricted to deeply piled granite boulder habitat that is largely devoid of vegetation. As for the other four boulder-pile Cophixalus, C. petrophilus sp. nov. is large and shows other similar morphological adaptations to this unique habitat (e.g., long limbs, large finger discs). However, it is notable in that it is the smallest of the boulder-pile species (26-32 mm) and it has particularly large eyes. I speculate that the latter trait is an adaptation to dimly lit conditions deep within the boulder-field. Cophixalus petrophilus sp. nov. was only found in exposed boulder habitat, whereas the co-occurring boulder species, C. zweifeli, was found using forested areas on and adjacent to the boulder-fields at night. Cape Melville is the only boulder-field with two co-occurring boulder Cophixalus and it appears that there is habitat partitioning between them. Cophixalus petrophilus sp. nov. has a highly localised distribution but appears common within this and is probably secure.

A new skink (Scincidae: Saproscincus) from rocky rainforest habitat on Cape Melville, north-east Australia.

Saproscincus skinks are restricted to wet forest habitats of eastern Australia. Eleven species have previously been described, with most having small distributions in disjunct areas of subtropical and tropical rainforest. The localized distributions and specific habitat requirements of Saproscincus have made them a key group for understanding the biogeographic history of Australia's rainforests. Here I describe a new species of Saproscincus from the Melville Range on Cape Melville, north-east Australia. The Melville Range is composed of boulder-fields and areas of rainforest in the uplands, and is highly isolated from other areas of elevated rainforest. All individuals of the new species were found on a moist ridgeline, active on boulders under a rainforest canopy or on boulder-field immediately adjacent to rainforest. Saproscincus saltus sp. nov. is highly distinct in morphology and colour pattern. Of particular interest are its long limbs and digits compared to congeners, which in conjunction with the observed ecology, suggest a long history of association with rock. The discovery of S. saltus sp. nov. extends the distribution of the genus over 100 km north from the nearest congeners in the Wet Tropics region. This species brings the number of vertebrates known to be endemic to the Melville Range to six, which is remarkable for such a small area.

A spectacular new leaf-tailed gecko (Carphodactylidae: Saltuarius) from the Melville Range, north-east Australia.

Leaf-tailed geckos are a distinctive group of carphodactyline geckos of rainforests and rocky habitats of eastern Australia. Three genera are recognized: Phyllurus (9 species), Saltuarius (6 species) and Orraya (1 species). Leaf-tailed geckos have been the subject of much survey and taxonomic work because they are large, impressive geckos and generally have highly localized distributions. The six species comprising Saltuarius are distributed in rock outcrops and rainforests along the ranges from northern New South Wales to the Wet Tropics region of north-east Queensland. Here we report the discovery of a new Saltuarius species at Cape Melville, a rainforest outlier on Cape York Peninsula in north-east Queensland. The new species is assigned to Saltuarius based on morphological and genetic data. Saltuarius eximius sp. nov. is highly distinct from all congeners in many aspects of morphology. It has a very long slender form, with relatively longer limbs, lon- ger body, narrower body and narrower neck than all congeners. It also has a highly distinct head that is relatively smaller than that of all other Saltuarius, with very large eyes that are grey rather than patterned. The tail is large but with a relatively short attenuated tip. Saltuarius eximius sp. nov. appears to be highly localized to upland rainforest associated with boulder habitat in the Cape Melville Range. The unusual elongate form and large eyes of S. eximius sp. nov. likely reflect adaptation to deep boulder habitat. Two other new vertebrate species (a skink and a frog) were discovered in the rainforest and boulder-fields of Cape Melville during recent surveys, bringing the number of vertebrates known to be endemic to the Cape Melville Range to six (three frogs, two skinks and one gecko).

Two new subspecies of the leaf-tailed gecko Phyllurus ossa (Lacertilia: Carphodactylidae) from mid-eastern Queensland, Australia.

Following the discovery of a new population of Phyllurus ossa on Whitsunday Island in the Cumberland Island Group, eastern Queensland, we conducted both genetic and morphological analyses to assess differences between all known populations. The analyses revealed three genetically distinct, morphologically diagnosable, geographical units. The differences are such that we recognise these as subspecies: Phyllurus ossa ossa restricted to the Mt Ossa/Mt Pelion/ Mt Charlton/ St Helens Gap area; P. ossa hobsoni subsp. nov. on Mt Dryander and in the Conway Range and P. ossa tamoya subsp. nov. currently only known from Whitsunday Island. There are now 11 recognised taxa in Phyllurus. The three P. ossa subspecies are narrowly distributed and closely associated with exposed rock in low to mid-elevation vine forests. Their current distributions are shaped by past climate change that progressively contracted and fragmented the distribution of rainforests in eastern Australia. The recognition of these subspecies has land management/conservation implications.

A new treefrog (Hylidae: Litoria) from Kroombit Tops, east Australia, and an assessment of conservation status.

The Litoria phyllochroa species-group are small hylid frogs that occur in wet forests of south-east Australia. This group has had a long history of taxonomic confusion and has received little attention in the last decade. A population of this species-group at Kroombit Tops, several hundred kilometers north of all other populations, has been recognised for some time as being genetically highly distinct. Here we describe this population as a new species, L. kroombitensis sp. nov. This species is most similar to L. barringtonensis and L. pearsoniana but is readily distinguished based on differences in morphology, colour pattern, mating call and genetics. Litoria kroombitensis sp. nov. is restricted to Kroombit Tops, an isolated area of wet forest in south-east Queensland. The species inhabits slow and intermittently flowing streams in rainforest and adjoining wet sclerophyll forest. The tadpole of L. kroombitensis sp. nov., described herein, is similar in morphology and behaviour to the tadpoles of other species within the Litoria phyllochroa species-group, in particular L. pearsoniana. Li toria kroombitensis sp. nov. has a very small distribution, with all records coming from the headwaters of five streams, Extensive surveys since the mid-1990s have revealed population declines, attributable to amphibian chytrid fungus (Batrachochytrium dendrobatidis). Other threats include degradation of riparian habitat due to invasive weeds, feral pigs and livestock, and fire. Further, the extent of wet forest habitats at Kroombit Tops is likely to be reduced by climate change impacts. Litoria kroombitensis sp. nov. meets IUCN Red List criteria for critically endangered CR B lab (i-v) due to its small geographic range, naturally fragmented distribution, and observed and projected decline in populations. In this paper we also assess the validity of the names L. barringtonensis, L. pearsoniana and L. piperata. We conclude that the names L. barringtonensis and L. pearsoniana are valid but the validity of L. piperata requires further investigation.