Michael G. Rix

Protecting the innocent: studying short-range endemic taxa enhances conservation outcomes

A major challenge confronting many contemporary systematists is how to integrate standard taxonomic research with conservation outcomes. With a biodiversity crisis looming and ongoing impediments to taxonomy, how can systematic research continue to document species and infer the ‘Tree of Life’, and still maintain its significance to conservation science and to protecting the very species it strives to understand? Here we advocate a systematic research program dedicated to documenting short-range endemic taxa, which are species with naturally small distributions and, by their very nature, most likely to be threatened by habitat loss, habitat degradation and climate change. This research can dovetail with the needs of industry and government to obtain high-quality data to inform the assessment of impacts of major development projects that affect landscapes and their biological heritage. We highlight how these projects are assessed using criteria mandated by Western Australian legislation and informed by guidance statements issued by the Environmental Protection Authority (Western Australia). To illustrate slightly different biological scenarios, we also provide three case studies from the Pilbara region of Western Australia, which include examples demonstrating a rapid rise in the collection and documentation of diverse and previously unknown subterranean and surface faunas, as well as how biological surveys can clarify the status of species thought to be rare or potentially threatened. We argue that ‘whole of biota’ surveys (that include all invertebrates) are rarely fundable and are logistically impossible, and that concentrated research on some of the most vulnerable elements in the landscape – short-range endemics, including troglofauna and stygofauna – can help to enhance conservation and research outcomes.

Phylogeny and historical biogeography of ancient assassin spiders (Araneae: Archaeidae) in the Australian mesic zone: Evidence for Miocene speciation within Tertiary refugia

The rainforests, wet sclerophyll forests and temperate heathlands of the Australian mesic zone are home to a diverse and highly endemic biota, including numerous old endemic lineages restricted to refugial, mesic biomes. A growing number of phylogeographic studies have attempted to explain the origins and diversification of the Australian mesic zone biota, in order to test and better understand the mode and tempo of historical speciation within Australia. Assassin spiders (family Archaeidae) are a lineage of iconic araneomorph spiders, characterised by their antiquity, remarkable morphology and relictual biogeography on the southern continents. The Australian assassin spider fauna is characterised by a high diversity of allopatric species, many of which are restricted to individual mountains or montane systems, and all of which are closely tied to mesic and/or refugial habitats in the east and extreme south-west of mainland Australia. We tested the phylogeny and vicariant biogeography of the Australian Archaeidae (genus Austrarchaea Forster & Platnick), using a multi-locus molecular approach. Fragments from six mitochondrial genes (COI, COII, tRNA-K, tRNA-D, ATP8, ATP6) and one nuclear protein-coding gene (Histone H3) were used to infer phylogenetic relationships and to explore the phylogeographic origins of the diverse Australian fauna. Bayesian analyses of the complete molecular dataset, along with differentially-partitioned Bayesian and parsimony analyses of a smaller concatenated dataset, revealed the presence of three major Australian lineages, each with non-overlapping distributions in north-eastern Queensland, mid-eastern Australia and southern Australia, respectively. Divergence date estimation using mitochondrial data and a rate-calibrated relaxed molecular clock revealed that major lineages diverged in the early Tertiary period, prior to the final rifting of Australia from East Antarctica. Subsequent speciation occurred during the Miocene (23-5.3 million years ago), with tropical and subtropical taxa diverging in the early-mid Miocene, prior to southern and temperate taxa in the mid-late Miocene. Area cladograms reconciled with Bayesian chronograms for all known Archaeidae in southern and south-eastern Australia revealed seven potentially vicariant biogeographic barriers in eastern Queensland, New South Wales and southern Australia, each proposed and discussed in relation to other mesic zone taxa. Five of these barriers were inferred as being of early Miocene age, and implicated in the initial vicariant separation of endemic regional clades. Phylogeographic results for Australian Archaeidae are congruent with a model of sequential allopatric speciation in Tertiary refugia, as driven by the contraction and fragmentation of Australias mesic biomes during the Miocene. Assassin spiders clearly offer great potential for further testing historical biogeographic processes in temperate and eastern Australia, and are a useful group for better understanding the biology and biogeography of the Australian mesic zone.

Biogeography and speciation of terrestrial fauna in the south-western Australian biodiversity hotspot

The south‐western land division of Western Australia (SWWA), bordering the temperate Southern and Indian Oceans, is the only global biodiversity hotspot recognised in Australia. Renowned for its extraordinary diversity of endemic plants, and for some of the largest and most botanically significant temperate heathlands and woodlands on Earth, SWWA has long fascinated biogeographers. Its flat, highly weathered topography and the apparent absence of major geographic factors usually implicated in biotic diversification have challenged attempts to explain patterns of biogeography and mechanisms of speciation in the region. Botanical studies have always been central to understanding the biodiversity values of SWWA, although surprisingly few quantitative botanical analyses have allowed for an understanding of historical biogeographic processes in both space and time. Faunistic studies, by contrast, have played little or no role in defining hotspot concepts, despite several decades of accumulating quantitative research on the phylogeny and phylogeography of multiple lineages. In this review we critically analyse datasets with explicit supporting phylogenetic data and estimates of the time since divergence for all available elements of the terrestrial fauna, and compare these datasets to those available for plants. In situ speciation has played more of a role in shaping the south‐western Australian fauna than has long been supposed, and has occurred in numerous endemic lineages of freshwater fish, frogs, reptiles, snails and less‐vagile arthropods. By contrast, relatively low levels of endemism are found in birds, mammals and highly dispersive insects, and in situ speciation has played a negligible role in generating local endemism in birds and mammals. Quantitative studies provide evidence for at least four mechanisms driving patterns of endemism in south‐western Australian animals, including: (i) relictualism of ancient Gondwanan or Pangaean taxa in the High Rainfall Province; (ii) vicariant isolation of lineages west of the Nullarbor divide; (iii) in situ speciation; and (iv) recent population subdivision. From dated quantitative studies we derive four testable models of historical biogeography for animal taxa in SWWA, each explicit in providing a spatial, temporal and topological perspective on patterns of speciation or divergence. For each model we also propose candidate lineages that may be worthy of further study, given what we know of their taxonomy, distributions or relationships. These models formalise four of the strongest patterns seen in many animal taxa from SWWA, although other models are clearly required to explain particular, idiosyncratic patterns. Generating numerous new datasets for suites of co‐occurring lineages in SWWA will help refine our understanding of the historical biogeography of the region, highlight gaps in our knowledge, and allow us to derive general postulates from quantitative (rather than qualitative) results. For animals, this process has now begun in earnest, as has the process of taxonomically documenting many of the more diverse invertebrate lineages. The latter remains central to any attempt to appreciate holistically biogeographic patterns and processes in SWWA, and molecular phylogenetic studies should – where possible – also lead to tangible taxonomic outcomes.

Barcoding of mygalomorph spiders (Araneae : Mygalomorphae) in the Pilbara bioregion of Western Australia reveals a highly diverse biota

Abstract. The Pilbara bioregion of Western Australia is an area that contains vast mineral deposits and unique ecosystems. To ensure that mineral deposits are mined with minimal impact on the natural environment, impact assessment surveys are required to determine what fauna and flora species are located within proposed development areas, in particular, by determining the distributions of short-range endemic species (SREs). One infraorder of Arachnida, the Mygalomorphae (trapdoor spiders and their kin), are frequently identified as SREs. These identifications are traditionally performed using morphological techniques; however, only males can be reliably identified to species. Furthermore, the majority of species have not been formally described and males comprise only ∼5% of specimens collected. To assess mygalomorph diversity and the distribution of species in the Pilbara, we employed a molecular barcoding approach. Sequence data from the mitochondrial DNA cytochrome c oxidase subunit I (COI) gene were obtained from 1134 specimens, and analysed using Bayesian methods. Only a fraction of the total mygalomorph fauna of the Pilbara has been documented, and using a species boundary cut-off of 9.5% sequence divergence, we report an increase in species richness of 191%. Barcoding provides a rapid, objective method to help quantify mygalomorph species identifications and their distributions, and these data, in turn, provide crucial information that regulatory authorities can use to assess the environmental impacts of large-scale developments.

Australian Assassins, Part II: A review of the new assassin spider genus Zephyrarchaea (Araneae, Archaeidae) from southern Australia

Abstract The Assassin Spiders of the family Archaeidae from southern Australia are revised, with a new genus (Zephyrarchaea gen. n.) and nine new species described from temperate, mesic habitats in southern Victoria, South Australia and south-western Western Australia: Zephyrarchaea austini sp. n., Zephyrarchaea barrettae sp. n., Zephyrarchaea grayi sp. n., Zephyrarchaea janineae sp. n., Zephyrarchaea marae sp. n., Zephyrarchaea marki sp. n., Zephyrarchaea melindae sp. n., Zephyrarchaea porchi sp. n. and Zephyrarchaea vichickmani sp. n. Specimens of the type species, Zephyrarchaea mainae (Platnick, 1991), comb. n., are redescribed from the Albany region of Western Australia, along with the holotype female of Zephyrarchaea robinsi (Harvey, 2002) comb. n. from the Stirling Range National Park. The previously described species Archaea hickmani Butler, 1929 from Victoria is here recognised as a nomen dubium. A key to species and multi-locus molecular phylogeny complement the species-level taxonomy, with maps, habitat photos, natural history information and conservation assessments provided for all species.

Australian Assassins, Part I: A review of the Assassin Spiders (Araneae: Archaeidae) of mid-eastern Australia

Abstract The Assassin Spiders of the family Archaeidae are an ancient and iconic lineage of basal araneomorph spiders, characterised by a specialised araneophagic ecology and unique, ‘pelican-like’ cephalic morphology. Found throughout the rainforests, wet sclerophyll forests and mesic heathlands of south-western, south-eastern and north-eastern Australia, the genus Austrarchaea Forster & Platnick, 1984 includes a diverse assemblage of relictual, largely short-range endemic species. With recent dedicated field surveys and significant advances in our understanding of archaeid biology and ecology, numerous new species of assassin spiders have been discovered in the montane sub-tropical and warm-temperate closed forests of mid-eastern Australia, including several rare or enigmatic taxa and species of conservation concern. This fauna is revised and 17 new species are described from south-eastern Queensland and eastern New South Wales: Austrarchaea alani sp. n., Austrarchaea aleenae sp. n., Austrarchaea binfordae sp. n., Austrarchaea christopheri sp. n., Austrarchaea clyneae sp. n., Austrarchaea cunninghami sp. n., Austrarchaea dianneae sp. n., Austrarchaea harmsi sp. n., Austrarchaea helenae sp. n., Austrarchaea judyae sp. n., Austrarchaea mascordi sp. n., Austrarchaea mcguiganae sp. n., Austrarchaea milledgei sp. n., Austrarchaea monteithi sp. n., Austrarchaea platnickorum sp. n., Austrarchaea raveni sp. n. and Austrarchaea smithae sp. n. Adult specimens of the type species, Austrarchaea nodosa (Forster, 1956) are redescribed from the Lamington Plateau, south-eastern Queensland, and distinguished from the sympatric species Austrarchaea dianneae sp. n. A key to species and a molecular phylogenetic analysis of COI and COII mtDNA sequences complement the species-level taxonomy, with maps, habitat photos, natural history information and conservation assessments provided for all species.

A revision of the textricellin spider genus Raveniella (Araneae : Araneoidea : Micropholcommatidae): exploring patterns of phylogeny and biogeography in an Australian biodiversity hotspot

South-western Western Australia is a biodiversity hotspot, with high levels of local endemism and a rich but largely undescribed terrestrial invertebrate fauna. Very few phylogeographic studies have been undertaken on south-western Australian invertebrate taxa, and almost nothing is known about historical biogeographic or cladogenic processes, particularly on the relatively young, speciose Quaternary sand dune habitats of the Swan Coastal Plain. Phylogeographic and taxonomic patterns were studied in textricellin micropholcommatid spiders belonging to the genus Raveniella Rix & Harvey. The Micropholcommatidae is a family of small spiders with a widespread distribution in southern Western Australia, and most species are spatially restricted to refugial microhabitats. In total, 340 specimens of Raveniella were collected from 36 surveyed localities on the Swan Coastal Plain and 17 non-Swan Coastal Plain reference localities in south-western Western Australia. Fragments from three nuclear rRNA genes (5.8S, 18S and ITS2), and one mitochondrial protein-coding gene (COI) were used to infer the phylogeny of the genus Raveniella, and to examine phylogeographic patterns on the Swan Coastal Plain. Five new species of Raveniella are described from Western Australia (R. arenacea, sp. nov., R. cirrata, sp. nov., R. janineae, sp. nov., R. mucronata, sp. nov. and R. subcirrata, sp. nov.), along with a single new species from south-eastern Australia (R. apopsis, sp. nov.). Four species of Raveniella were found on the Swan Coastal Plain: two with broader distributions in the High Rainfall and Transitional Rainfall Zones (R. peckorum Rix & Harvey, R. cirrata); and two endemic to the Swan Coastal Plain, found only on the western-most Quindalup dunes (R. arenacea, R. subcirrata). Two coastally restricted species (R. subcirrata, R. janineae) were found to be morphologically cryptic but genetically highly distinct, with female specimens morphologically indistinguishable from their respective sister-taxa (R. cirrata and R. peckorum). The greater Perth region is an important biogeographic overlap zone for all four Swan Coastal Plain species, where the ranges of two endemic coastal species join the northern and south-western limits of the ranges of R. peckorum and R. cirrata, respectively. Most species of Raveniella were found to occupy long, highly autapomorphic molecular branches exhibiting little intraspecific variation, and an analysis of ITS2 rRNA secondary structures among different species of Raveniella revealed the presence of an extraordinary hypervariable helix, ranging from 31 to over 400 nucleotides in length.

Where have all the spiders gone? The decline of a poorly known invertebrate fauna in the agricultural and arid zones of southern Australia

Earth is currently experiencing the sixth mass extinction of complex multi‐cellular life, the first at the hands of a single species. The documented extinctions of iconic (mostly vertebrate and plant) taxa dominate the discourse, while poorly known invertebrate species are disappearing ‘silently’, sometimes without having ever been described. Here, we highlight the decline of elements of the trapdoor spider (Mygalomorphae: Idiopidae) fauna of southern Australia – a taxonomically poorly documented yet diverse assemblage of long‐lived fossorial predators. We show that a number of trapdoor spider species may be threatened after a century of intensive land clearing and stocking, and that remaining populations in some areas may be experiencing serious contemporary population declines. So, how do we conserve this fauna? We suggest that baseline systematic studies are crucial, and that follow‐up surveys, including integrative citizen science solutions, should be used to assess where remnant populations still exist, and whether they can persist into the future. Detailed population genetic research on a handful of carefully chosen taxa could be broadly informative, and ongoing natural history studies remain invaluable. Although solutions may be limited in the face of ongoing habitat degradation and other threats, urgently quantifying declines has implications not just for spiders but for mitigating against the mass extinction of poorly known invertebrate taxa across the globe.

Refugia within refugia: in situ speciation and conservation of threatened Bertmainius (Araneae : Migidae), a new genus of relictual trapdoor spiders endemic to the mesic zone of south-western Australia

Abstract. The trapdoor spider family Migidae has a classical Gondwanan distribution and is found on all southern continents except the Indian region. The Australian fauna consists of three genera including Moggridgea O. P. Cambridge from south-western Australia and Kangaroo Island, South Australia; Moggridgea is otherwise widespread throughout Africa. The sole named species of Moggridgea from Western Australia, M. tingle Main, and its unnamed relatives are the subject of the present paper, which was stimulated by concern for the long-term persistence of populations, and the discovery of deep genetic divergences between populations. A phylogeny of the Western Australian species relative to African and South Australian Moggridgea was generated using molecular COI and ITS rDNA data, and based on both molecular and morphological criteria we conclude that the Western Australian taxa should be removed from Moggridgea and transferred to a new genus, Bertmainius. The seven species are delimited using both morphological and molecular criteria: B. tingle (Main) (the type species), and six new species, B. colonus, B. monachus, B. mysticus, B. opimus, B. pandus and B. tumidus. All seven species are considered to be threatened using IUCN criteria, with the major threatening processes being inappropriate fire regimes and climate change.

Australian Assassins, Part III: A review of the Assassin Spiders (Araneae, Archaeidae) of tropical north-eastern Queensland

Abstract The assassin spiders of the family Archaeidae from tropical north-eastern Queensland are revised, with eight new species described from rainforest habitats of the Wet Tropics bioregion and Mackay-Whitsundays Hinterland: Austrarchaea griswoldi sp. n., Austrarchaea hoskini sp. n., Austrarchaea karenae sp. n., Austrarchaea tealei sp. n., Austrarchaea thompsoni sp. n., Austrarchaea wallacei sp. n., Austrarchaea westi sp. n. and Austrarchaea woodae sp. n. Specimens of the only previously described species, Austrarchaea daviesae Forster & Platnick, 1984, are redescribed from the southern Atherton Tableland. The rainforests of tropical eastern Queensland are found to be a potential hotspot of archaeid diversity and endemism, with the region likely to be home to numerous additional short-range endemic taxa. A key to species complements the taxonomy, with maps, natural history information and conservation assessments provided for all species.