VIEWPOINT. Is the Australian subterranean fauna uniquely diverse?

Is the Australian subterranean fauna uniquely diverse

Michelle T GuzikAG Andrew D AustinA Steven J B CooperAB Mark S HarveyCWilliam F HumphreysC Tessa BradfordA Stefan M EberhardD Rachael A KingABRemko LeysBE Kate A MuirheadA and Moya TomlinsonF

AAustralian Centre for Evolutionary Biology and Biodiversity The University of Adelaide SA 5005 AustraliaBSouth Australian Museum North Terrace Adelaide SA 5000 AustraliaCWestern Australian Museum Collections and Research Centre Locked Bag 49 Welshpool DC WA 6986Australia

DSubterranean Ecology Pty Ltd 837 Cedric St Stirling WA 6021 AustraliaESchool of Biological Sciences Flinders University SA 5042 AustraliaFDepartment of Environment and Resource Management GPO Box 2454 Brisbane Qld 4001 AustraliaGCorresponding author Email michelleguzikadelaideeduau

Abstract Australia was historically considered a poor prospect for subterranean fauna but in reality the continent holdsa great variety of subterranean habitats with associated faunas found both in karst and non-karst environments This papercritically examines the diversity of subterranean fauna in several key regions for the mostly arid western half of AustraliaWe aimed to document levels of species richness for major taxon groups and examine the degree of uniqueness of the faunaWe also wanted to compare the composition of these ecosystems and their origins with other regions of subterraneandiversityworld-wideUsing informationon thenumber of lsquodescribedrsquo and lsquoknownrsquo invertebrate species (recognisedbasedonmorphological andormolecular data)wepredict that the total subterranean fauna for thewestern half of the continent is 4140species of which ~10 is described and 9 is lsquoknownrsquo but not yet described The stygofauna water beetles ostracods andcopepods have the largest number of described species while arachnids dominate the described troglofauna Converselycopepods water beetles and isopods are the poorest known groups with less than 20 described species while hexapods(comprising mostly Collembola Coleoptera Blattodea and Hemiptera) are the least known of the troglofauna Comparedwith other regions of theworld we consider theAustralian subterranean fauna to be unique in its diversity comparedwith thenorthern hemisphere for three key reasons the range and diversity of subterranean habitats is both extensive and novel directfaunal links to ancient Pangaea and Gondwana are evident emphasising their early biogeographic history and Miocenearidification rather thanPleistocene post-ice agedrivendiversification events (as is predicted in the northern hemisphere) arelikely to have dominated Australiarsquos subterranean speciation explosion Finally we predict that the geologically youngeralthoughmorepoorly studied easternhalf of theAustralian continent is unlikely to be asdiverse as thewesternhalf except forstygofauna in porousmedia Furthermore based on similar geology palaeogeography and tectonic history to that seen in thewestern parts ofAustralia southernAfrica parts of SouthAmerica and Indiamay also yield similar subterranean biodiversityto that described here

Introduction

The subterranean fauna of Australia has recently revealednumerous higher taxa (classes orders and families) notpreviously recorded from the southern hemisphere as wellas living representatives of lineages previously known only asfossils (seeHumphreys 2008 for summary) Obligate subterraneanlineages remain trapped in situ and are consequently potentsubjects to test biogeographical and evolutionary hypothesesThis is especially the case for the numerous higher taxaof Crustacea that are found solely represented as obligatesubterranean fauna Here we present current estimates of newlydescribed or identified subterranean taxa from several keyregions in the western half of Australia particularly in the arid

zone (see Fig 1) We also make projections on possible totalsubterranean biodiversity in this area in particular to assesswhether the diversity of the Australian subterranean fauna isnotably high compared to that found elsewhere Our aim is todocument the scale of this biodiversity to encourage furtherexploration of these and other regions of the continent We alsomake predictions about other locations in the world that reflectsimilar geomorphology to that seen in Australiarsquos arid region andrepresent potential new sites for subterranean fauna

Globally the northern hemisphere dominates as a region ofsubterranean biodiversity hotspots in particular temperate mid-latitude locations (Culver et al 2006 Stoch and Galassi 2010)such as the Balkan Peninsula the USA (Culver and Sket 2000)

CSIRO 4 March 2011 101071IS10038 1445-522610050407

CSIRO PUBLISHING Viewpoint

wwwpublishcsiroaujournalsis Invertebrate Systematics 2010 24 407ndash418

Mexico (Reddell 1981) and most recently caves of south-eastAsia (Deharveng 2005) Subterranean faunal diversity isgenerally concentrated in karst and pseudokarst areas(Juberthie and Decu 1994 Culver et al 2001 Christman et al2005 Deharveng 2005) Even within this geomorphologicalconstraint (ie it is patchily distributed Fong and Culver 1994Culver et al 2004) the density of caves and the sampling intensityby generations of researchers in these regions have providedbiologists with the opportunity to efficiently document cavesand their fauna (Christman and Culver 2001 Culver et al2004 Zagmajster et al 2008) Consequently knowledge ofthese regions and their biodiversity phylogeography andfunctional ecology are well progressed (Gibert et al 1994Wilkens et al 2000 Culver and White 2004)

As recently as 16 years ago Humphreys (1994) advocated aknowledge gap of subterranean fauna in Australia especially inareas other than the lava tubes of tropical north Queenslandwhich are a noted troglofauna hotspot (Culver and Sket 2000)Considered depauperate of karstic habitat and havingwidespreadaridity historically Australia was considered a poor prospectfor subterranean fauna Australiarsquos arid Pleistocene climatichistory was deemed to lack key climate history events such as

Pleistocene glaciations (Moore 1964 Hamilton-Smith 1967Barr 1973) which were considered drivers of subterraneanbiodiversity in the northern hemisphere (Peck 1980 Boutin1994) This excludes Tasmania (Derbyshire 1972) which isrichly endowed with karst and caves and was subject toPleistocene glaciations These hypotheses coupled with apaucity of research on the southern hemisphere subterraneanbiota over the last two centuries have led to a prolongedlag in discovery of Australiarsquos obligate subterranean speciesHistorically the most sampled cave regions in Australiawere south-eastern South Australia (SA) New South Wales(NSW) Tasmania and the Nullarbor Plain (spanning parts ofSA and Western Australia (WA)) It is now appreciated thatAustralia holds a great variety of subterranean habitats withassociated invertebrate faunas found both in karst and non-karst environments (Eberhard and Humphreys 2003) Notabledifferences between Australia and other regions of the worldare the absence of urodele amphibians and stenasellid isopodsand a scarcity of carabid beetles and cave fishes

Focussed research on subterranean fauna from karst regionsin WA comprising troglobionts (Humphreys et al 1989)and stygobionts soon after (Humphreys and Adams 1991)

Fig 1 Geological and climatic regions of Australia from which we describe a subterranean faunalbiodiversity hotspot Five regions are named including the Western Shield an area that has beencontinually emergent since the Proterozoic Dashed lines delineate the (1) Kimberley (2) Pilbara and(3) Yilgarn Additionally the Gondwanan refuges that comprise soft-rock karst are the (4) Nullarbor and(5) south-east of South Australia

408 Invertebrate Systematics M T Guzik et al

substantially advanced our knowledge of subterranean fauna inAustralia Further the discovery of rich subterranean faunas innon-karstic substrates 20 years ago also led to a rapid expansionin the discovery and documentation of subterranean faunaldiversity Increasingly regulations requiring the inclusion ofsubterranean fauna during the environmental review processfor major resource projects in WA by the EnvironmentalProtection Agency (EPA) (EPA 2003) have accelerated thediscovery of new species based on either morphology orgenetic differences or both Coupled with these environmentalimpact assessments (EIA) is an increased interest in groundwaterbiology research (Humphreys 2006 2009 Boulton 2009)Government and privately funded research in the pastfive years has primarily focussed on the fauna of the Yilgarnand Pilbara regions of WA and aquifers in SA in particularutilising boreholes and drill holes installed for exploration andexploitation of water minerals and monitoring of groundwaterlevels and salinity rather than fauna This work has revealed adiverse subterranean fauna inhabiting both aquatic and terrestrialhabitats found in a wide range of substrates includingalluvium calcretes fractured rock karst in soft and hard rockpisolites and pseudokarst in lava and sandstone (Poore andHumphreys 1998 2003 Finston and Johnson 2004 Eberhardet al 2005 Harvey et al 2008 Humphreys 2008 Eberhard et al2009) Many of the resultant data are unavailable publiclyduring the EIA process but many become public after formalenvironmental approvals occur

In an era when human induced extinction rates are high(Pimm et al 1995) biodiversity estimates are a vital tool foridentifying knowledge gaps for the purpose of prioritisingresearch effort and funding resources and also developingconservation policies (Brooks et al 2006) Estimates ofinvertebrate species richness in Australia are typically centredaround terrestrial arthropods (eg Yeates et al 2003) Publishedstudies suggest Australiarsquos subterranean fauna is diverseespecially the Pilbara region with 78 described species ofstygofauna (Eberhard et al 2005) and an estimated 500ndash550undescribed species (Eberhard et al 2009) However a firmestimate of total species diversity is constrained by the generallysparse geographical coverage and the inevitable lag in taxonomicdescriptions Our position here is that historically Australiarsquossubterranean fauna have been vastly underestimated Given theshort duration of research targeting this field in Australia it isnot possible to realistically attempt an estimate of subterraneanfaunal diversity for the whole continent Rather we concentrateon several areas in the western half of the Australian continentthat are better studied we summarise the number of describedand recognised species from morphological and molecularstudies and then project based on the collective experienceof the specialists currently working on these faunas the likelyspecies richness of broad taxonomic groups The areas thatwere included and assessed in this study from north-west toeast include (1) the Kimberley and (2) Pilbara regions ofnorth-western WA (3) the Yilgarn region of WA (4) theNullarbor region and (5) SA including the Eyre PeninsulaFlinders Ranges and the south-east (Fig 1) We also notethat a diverse stygofauna has recently been identified fromalluvial aquifers in eastern Australia (Hancock and Boulton2008 Tomlinson 2009 Camacho and Hancock 2010) but this

region requires considerably more intensive surveying andtaxonomic work to obtain reliable estimates of faunal diversity

Methodology for estimating subterranean faunal diversity

The criteria employed to identify species richness in subterraneanhabitats of Australiarsquos west (see Table 1 for data) were 5-fold

(1) We surveyed the relevant literature for formallylsquodescribedrsquo species mostly from the last 10ndash20 years whichhas been themost productive time for exploration and descriptionof subterranean taxa (see references inTable 2 for a representativesummary of this literature)

(2) Extensive surveys of key regions were carried outprimarily by teams represented by three of the authors of thisstudy (SA Leys Pilbara and Nullarbor Eberhard Yilgarnand Kimberley Humphreys) The areas most comprehensivelysampled were the Western Shield a single long-emergent (sincethe Paleozoic) landmass comprising the Yilgarn and Pilbaracratons and associated orogens southern SA and the northernCarnarvon Basin These surveys were conducted using a varietyof access points mostly boreholes drilled for water extractiongroundwater monitoring and mineral exploration but alsopastoral wells and caves where present In general even in thebetter surveyed regions sampling density was low For examplein the only regional survey of the Pilbara region (Eberhard et al2009) sample density was 00022 km2 (one site every 460 km2)in an area of ~220 000 km2 In the Yilgarn sampling has largelybeen restricted to groundwater calcretes which are highlyprospective for subterranean fauna whereas other habitatshave been found to be largely devoid of subterranean fauna

(3) Identification of morphologically distinct species(morphospecies) beyond family or genus using currentdescriptions and keys was not always possible Therefore wecanvassed numbers of species from taxonomic experts (listed in

Table 1 Species richness of major subterranean invertebrate groupsfrom thewestern half of the Australian continent showing the number oflsquodescribedrsquo species the number of lsquoknownrsquo but undescribed species fromcollections and molecular studies and an estimate of the likely diversity

for each group (see text for further details)

Taxonomic group No speciesdescribed

No knownspecies

Estimatedsize of fauna

describedor known

StygofaunaColeoptera 98 3 510 198Amphipoda 28 91 560 213Isopoda 19 30 300 163Bathynellacea 17 66 270 307Ostracoda 70 4 180 411Copepoda 79 4 580 143Gastropoda 3 1 20 200Other stygofauna 10 20 260 115

TroglofaunaHexapoda 11 52 500 126Arachnida 57 44 380 266Myriapoda 7 12 80 238Crustacea 2 43 500 90

Total 403 367 4140 186

Is the Australian subterranean fauna uniquely diverse Invertebrate Systematics 409

Table 2) to identify probable new morphospecies These expertsused their prior knowledge to assign likely species

(4) Molecular data have proven a major innovation indelineation of new species both cryptic and otherwise (Juanet al 2010) Hence in situations in which it was uncertainwhether there were distinct species present genetic methodswere used to estimate lsquoknownrsquo but undescribed species fromrecent collections and molecular studies Such situations arosewhen geographically isolated populations were observed butmorphological differences were not immediately recognisableor in situations in which expertise was unavailable or samplevolumes were too large In these cases the mtDNA cytochrome coxidase subunit I gene (cox1)was primarily used for assessing thepresence of new genetic lineages

Criteria for discriminating whether genetic lineages for cox1were likely to be species here are as follows (1) Reciprocallymonophyletic lineages with gt90 posterior probabilitysupport and the position of these lineages within the broaderphylogeny were considered (2) On the basis of total evidencegeographically discrete lineages that complied with all othercriteria listed here and were also known to be spatially isolatedwere included Isolation could be geographical distanceandor barriers or geological barriers This criterion wascrucial in situations in which percentage genetic divergencemight have been low and provided insights into the possiblemechanisms for species divergences In particular it wasshown in several studies that major geographic barriers inhibitgeneflow between regions ie tributaries (Pilbara amphipodsFinston and Johnson 2004 Finston et al 2007 2009) or geologyof calcrete aquifers (Cooper et al 2007 2008 Guzik et al 2008)(3) Genetically divergent lineages were conservatively 16for pairwise distances based on a Kimura 2-parameter (Kimura1980) model (ie between lsquospeciesrsquo lineages Lefeacutebure et al2006) In some cases where genetic lineages satisfied all of theother criteria (ie genetically monophyletic and geographically

isolated) then lower divergences were considered Thejustification for allowing lower divergences is that in cases ofrecent speciation events divergences as low as 11 have beenobserved in morphologically distinct but sympatric species(Bradford et al 2010 R A King unpubl data) Thesefindings have been observed in other crustaceans particularlyamphipods and parabathynellids (Cooper et al 2007 2008Guzik et al 2008 K M Abrams unpubl data) Wherepossible evidence from a second marker was also taken intoaccount to strengthen the hypothesis of distinct species Genessuch as 16S rRNA (mtDNA) and 28S rRNA (nuclear DNA) wereused to supplement the cox1 data for parabathynellids andamphipods (R Leys unpubl data)

An example of how these criteria were implemented is asfollows Using DNA alone ~90 new crustacean lsquolineagesrsquo wereidentified frompublished studies (eg up to 21Pilbara amphipods(Finston and Johnson2004 Finston et al 2007 2009) 22Yilgarnamphipods (Cooper et al 2007) 1 anchialine shrimp (Pageet al 2008) 24 aquatic isopods (Cooper et al 2008) and 17parabathynellids (Guzik et al 2008)) Each of these studiesalso demonstrated geographic isolation for each of the lineages(as above) confirming our species concept using a combinedapproach as exemplified by Harvey et al (2008) where bothmorphological and molecular data reinforced conclusionsFinally some unpublished molecular work by Eberhard Leysand Abrams generated largely for EIA datasets were alsoassessed using the same criteria as that for published work

(5) In order to provide an estimate of the potential size of thefauna for different taxonomic groups and the percentage thatwas currently lsquodescribedrsquo or lsquoknownrsquo we extrapolated from theexisting surveys This extrapolation was carried out in differentways for different regions forwhichwe give two examples Firstin the Pilbara region it is likely thatmost of the landscape providespotential habitat for troglofauna and stygofauna and hence it isdifficult to assign sampledunsampled area estimates based on

Table 2 Subterranean groups the experts we consulted on the estimated number of species and the references we used for estimating the numberof lsquodescribedrsquo species

Taxonomic group Experts References

StygofaunaColeoptera Watts C Summary and checklist Watts and Humphreys (2009) Leys and Watts (2010)Amphipoda Bradbury J King R Bradbury and Williams (1997a 1997b) Bradbury (1999) Bradbury and Eberhard (2000)Isopoda Taiti S Wilson and Ponder (1992) Bruce and Humphreys (1993) Wilson and Johnson (1999) Wilson and Keable

(1999) Taiti and Humphreys (2001) Wilson (2001 2003 2008) Bruce (2008)Bathynellacea Cho J-L Cho (2005) Cho et al (2005 2006a 2006b) Cho and Humphreys (2010)Ostracoda Karanovic I Karanovic and Marmonier (2002 2003) Karanovic (2003a 2003b 2004 2005a 2005b 2007)Copepoda Karanovic T Pesce and De Laurentiis (1996) Pesce et al (1996a 1996b) Karanovic et al (2001) Karanovic and Pesce

(2002) Karanovic (2003 2004a 2004b 2005 2006)Gastropoda Ponder et al (1989)Other stygofauna Acari Harvey (1998) Anchialine faunas Humphreys (2001) Jaume and Humphreys (2001) Jaume et al

(2001)TroglofaunaHexapoda Stevens M Koch (2009)Arachnida Harvey M Harvey and Humphreys (1995) Harvey (2001) Harvey and Edward (2007) Harvey and Volschenk (2007)

Barranco andHarvey (2008) Edward andHarvey (2008) Harvey and Leng (2008a 2008b) Harvey et al(2008) Platnick (2008) Volschenk and Prendini (2008) Burger et al (2010)

Myriapoda Edgecombe (2005)Crustacea Poore and Humphreys (1998)


points (bores or caves) In this case extrapolation of richnessestimates was based on accumulation curves as outlined byEberhard et al (2009) Second in the Yilgarn region sincesubterranean taxa are restricted to calcretes and each sampledcalcrete was found to have a unique fauna extrapolation of thedata from sampled to unsampled calcretes was warranted Of200 major calcretes in the Yilgarn region ~50 (25) have beensurveyed allowing extrapolation based on the average number ofdescribed plus known species in different calcretes

Australiarsquos subterranean fauna a biodiversity hotspot

Here we estimate 4140 species for subterranean systems inAustraliarsquos western half (Table 1) many of which arerestricted to arid and semiarid regions Based on this figureover 80 of the likely fauna remain undiscovered a figurethat is not surprising given that large tracts of potentiallysuitable habitat remain unexplored lsquoDescribedrsquo speciesrepresent slightly more taxa (403) than those lsquoknownrsquo but notdescribed (367) In particular beetles ostracods and copepodshave the largest number of described species for the stygofaunawhile arachnids dominate the described troglofauna Thissituation largely reflects the current taxonomic effort byspecialists While other potentially diverse groups have notbeen investigated in detail either because of a lack of attentionby existing specialists or a general lack of expertise for specificgroups they are still likely to represent significant diversity Forthe 367 undescribed taxa the majority represent geographicallyisolated monophyletic lineages based on molecular studiesreflecting long-term isolated populations that are likely to beequivalent to distinct species especially for crustaceans such asparabathynellids (Guzik et al 2008) amphipods (Finston andJohnson 2004 Cooper et al 2007 Finston et al 2007) andisopods (Cooper et al 2008) Based on the data presented inTable 1 we predict for the stygofauna that copepods isopodsand beetles are the most poorly known groups with less than20 described species followed by gastropods and amphipodsand for the troglofauna hexapods (comprising mostlyCollembola Coleoptera Blattodea and Hemiptera) are theleast known relative to the number predicted The beetles areinteresting here because despite rigorous taxonomicwork on thisgroup the majority of newly discovered taxa remain undescribedor undiscovered

Much of the subterranean faunal diversity has been identifiedfrom the Yilgarn and Pilbara regions (Fig 2) largely due to thesustained research efforts of several groups over the last decadein addition to the numerous EIAs fuelled by Australiarsquos mineralexploration boom (Eberhard et al 2009) Geologically thePilbara and Yilgarn cratons of WA comprise the WesternShield an area that has been continually emergent since theProterozoic (Humphreys 1999 2001) (Fig 1) Suggestive ofan ancient and remnant fauna the aquifers of the Pilbara andYilgarn contain an extraordinarily diverse stygofauna(Humphreys 2006) that largely appear unrelated to each otherAlternatively troglofauna are better known in the Pilbara withextensive sampling of fractured rock and pisolites associatedwith mining surveys revealing high faunal diversity In theYilgarn troglofauna are comparatively poorly sampled butdiversity is expected to be high especially in karstic calcretes

It is likely that our species richness values are considerablyunderestimated in both the Yilgarn and Pilbara but weconsider it useful to provide an estimate based on the currentstateofknowledge and theoverall conclusion that thewesternhalfofAustralia represents a hotspot for subterranean faunal diversityA survey of SA aquifers (2007ndash10) by Leys revealed stygobiticspecies in more than 200 localities across the Flinders Ranges(fractured rocks springs and alluvia) EyrePeninsula (limestone)LoftyRanges (fractured rocks springs and alluvia) and the south-east (limestone) The subterranean faunal diversity in SA appearsto be lower than that ofWA however numerous taxa are yet to beworked through (eg Ostracoda Gastropoda (Hydrobiidae)Turbellaria and Oligochaeta)

Australia-wide projections

Our estimate of 4140 species in the western half of Australia is asubstantially higher figure than that postulated by Humphreys(2008) In that study 560 stygofauna specieswere estimated fromthe Western Shield and this area comprises ~50 of the areaexamined in this study thus clearly representing anunderestimateof species richness based on the data presented here Just forthe Pilbara region which represents an even smaller area ofthe Western Shield Eberhard et al (2009) estimated 500ndash550undescribed species using species accumulation curves Ourresults show that much of the subterranean taxa in the westernhalf of Australia remain undiscovered and the potential fornew species discovery is extremely high In the event ofbroader investigations of Australiarsquos subterranean regionsbesides caves and karst several specific areas of Australiawould benefit from a targeted approach In particular researchon four alluvial systems in eastern Australia has uncovered asubstantial fauna (Hancock and Boulton 2008 Tomlinson 2009Camacho and Hancock 2010) indicating that a rich stygofaunaoccurs in eastern alluvial habitats In particular different rivercatchments have revealed distinct faunas offering a tantalisinginsight into potential diversity in this region Arid regions ofthe Northern Territory and central Queensland particularly inlimestone areas are also likely to harbour rich stygofaunas similarto those of the Yilgarn in WA Additional taxa are likely to befound in SA particular in springs and alluvia of less studiedareas such as the Yorke Peninsula southern Flinders Rangesand the Lofty Ranges Temperate south-eastern Australia hasalready revealed significant diversity of subterranean faunapredominantly collected from limestone caves (Hunt 1990Eberhard et al 1991 Eberhard 1996 Thurgate et al 2001a2001b Ponder et al 2005 Rix et al 2008) suggesting thatTasmania Victoria and southern NSW would benefit fromadditional sampling effort in non-limestone terrains Inparticular the Great Dividing Range and surrounds would beof interest

The predicted origins of this diversity

Australia represents an ancient landscape and some of thesubterranean habitats that we focus on here have survivedthroughout the formation and dissolution of Pangaea and thesubsequent fragmentation of Gondwana Indeed some of theoldest known cave soils are found at Jenolan Caves NSW and


Fig 2 Examples of subterranean invertebrates from Western Australia (a) Troglobitic spider unknown genus and species (AraneaeTheridiidae) from the Pilbara (b) stygobitic parabathynellidAtopobathynella sp (Syncarida Parabathynellidae) from the Pilbara (c) stygobiticamphipod unknown genus and species (Amphipoda Paramelitidae) from the Pilbara (d) troglobitic dipluran unknown genus and species(HexapodaDiplura Parajapygidae) from the Pilbara (e) troglobitic beetle unknowngenus and species (Hexapoda ColeopteraCurculionidae)from the Pilbara ( f ) troglobitic millipede unknown genus and species (Diplopoda Doratodesmidae) from the Pilbara (g) stygobitic ostracodMeridiescandona lucerna Karanovic (Ostracoda Candonidae) from the Pilbara (h) stygobitic beetle Paroster plutonicensis (Watts andHumphreys 2003) (Hexapoda ColeopteraDytiscidae) from theYilgarn (Photos byGiulia Perina (andashg) andKateMuirhead (bndashf ) SubterraneanEcology Pty Ltd (wwwsubterraneanecologycomau) (Copyright) photo h by Chris Watts)


have been dated to the Devonian 375million years ago (MyaOsborne et al 2006) and in the Kimberley caves were formedfrom ancient Devonian reefs beneath the Permian ice sheet(Playford 2009) The full breadth of subterranean ecosystemsexists in Australia in contrast to other parts of the world whereonly one or two ecosystem types are typically found Australiahas a variety of water types including anchialine saline andfreshwater as well as better known subterranean types such askarst and pseudokarst alluvial and fractured rock Theseecosystems provide links to other global regions and reflecta vicariant relictual fauna especially the apparent lsquoTethyanconnectionsrsquo of anchialine fauna of epicontinental regions(eg the highly charismatic remipede species Lasionectesexleyi Yager and Humphreys 1996) Also providing links areisolated seamounts (Namiotko et al 2004 Humphreys 2008) andGondwanan lineages (Poore and Humphreys 1998) althoughthe Tethyan origin of some anchialine faunal elements may beuncertain (Karanovic and Eberhard 2009) As discussedelsewhere (Humphreys 2008) subterranean ecosystems maybe very persistent through geological time and many lineagesprobably have ancient origins (Cho et al 2006b Wilson 2008)

In the Yilgarn and Pilbara regions a myriad of short-rangeendemic species including both stygobitic (Taiti andHumphreys2001 Leys et al 2003 Leys and Watts 2008 Page et al 2008Guzik et al 2009 Bradford et al 2010) and troglobitic(Humphreys and Adams 2001 Harvey et al 2008) taxa havebeen identified Much of this diversity is likely to have resultedfrom vicariance associatedwith the aridification of theAustraliancontinent after the late Miocene (Byrne et al 2008) which led tobiotic isolation of calcretes and other subterranean habitats (egpisolitic iron ore mesas in the Pilbara) Colonisation of thesehabitats bymultiple unrelated surface species has also contributedto the high levels ofdiversity (Leys et al 2003Cooper et al 2008Guzik et al 2008) Further in situ speciation within aquifersis also considered a plausible source of species diversityparticularly in the Yilgarn (Guzik et al 2009 Juan et al 2010)and Pilbara (Finston et al 2009) Abiotic heterogeneity withinhabitats (ie salinity clines temperature variation andwater levelfluctuations) has been noted as possible sources of ecologicalvariation and niche partitioning

What is found in the rest of the world

Regional assessments of thediversity of subterranean faunas havepredominantly been conducted in the best studied locationsparticularly North America and Europe In the USA 973obligate subterranean species and subspecies were recorded byCulver et al (2000) comprising 673 terrestrial species and 269aquatic species More than 650 stygobitic species have beenrecorded from the longest and most intensively researchedregion the Balkan Peninsula where the first stygal animal wasdescribed in 1768 and from where 975 species of troglofaunahave been recorded (Sket et al 2004) Slovenia a key cave regionin Europe has 114 known stygobitic species (Culver and White2004) while six other European countries (Belgium FranceItaly Portugal Slovenia Spain (Malard et al 2009 Michelet al 2009)) have recorded 1059 stygobitic taxa with no morethan 80 species from any one karst region Most of thesetaxa are considered remnants of the Pleistocene during which

time cave populations were colonised during interglacialcycles and isolated during glacial periods (Peck 1984 Peckand Christiansen 1990 Culver et al 2006) However this islikely not the sole source of species origins with pre-Pleistoceneprocesses being well recognised (Hedin 1997 Buhay andCrandall 2005 Buhay et al 2007) Culver et al (2006)predicted that other regions of interest for cave fauna in thenorthern hemisphere are likely to include the Eurasiancontinent including Georgia and Kyrgyzstan Alternatively thesouthern hemisphere subterranean fauna arewell documented forNew Zealand where 102 described species are known fromgroundwater habitats particular Hydracarina (70 species) andcrustacean groups such as Amphipoda (four species) Isopoda(four species) and Syncarida (seven species) (Scarsbrook et al2003) South and Central America have also been recognisedto maintain novel cave fauna but which are under threat fromdeforestation In particular Brazil (Trajano 2000) Ecuador(Peck 1990) Mexico (Desutter-Grandcolas 1993) and severalCaribbean islands (Peck 1974 1999) have also yielded new cavefauna

Possible subterranean biodiversity hotspots elsewherein the world

Based on geology we expect that Africa and India may yieldsimilar subterranean biodiversity hotspots to those described herefor Australia There are established links with Australia for somestygal lineages from India (Phreatoicidea (Wilson 2008)Atopobathynella (Cho et al 2006b)) Africa (Phreatoicidea(Wilson and Keable 1999)) and more widely with Gondwana(Candoninae (Karanovic 2004 2005a 2005b) Spelaeogriphacea(Poore and Humphreys 1998 2003)) Further these Gondwananlinks between the major continents (eg the lsquocosmopolitanrsquoBathynellacea (Lopretto and Morrone 1998)) are likely to bean indicator of new regions of subterranean faunal significanceTo date Africa remains largely unexplored apart from theMediterranean north coast and Atlas Mountains WhileBotswana (Modisi 1983) and Namibia (Irish 1991 ChristelisandStruckmeier 2001) are considered possible locations thatmayharbour an undocumented diversity of stygofauna southernAfrica as a whole is a likely subterranean hotspot as similargeology karst and calcrete aquifers to those observed in WAexist there (Pickford et al 1999) South Africa has the endemicsubterranean amphipod family Sternophysingidae (Tasaki 2006)within the globally distributed superfamily Crangonyctoidea(Holsinger 1992) and the order Spelaeogriphacea (Sharrattet al 2000) The Spelaeogriphacea are only known from twoother locations in the world (Brazil and Australia) indicatinga shared Gondwanan distribution (Jaume 2008) In SouthAmerica the best characterised caves are in central Brazil andinclude the Serra do Ramalho karst area in Bahia state wellknown for its populations of the troglomorphic catfish Rhamdiaenfurnada Bichuette amp Trajano 2005 (eg Mattox et al 2008)and Minas Gerais state which is well known for its troglobiticinvertebrate fauna (Ferriera and Horta 2001 Souza and Ferreira2010) Futureworkwould benefit fromassessment of the geologyand current literature of these continents as indicators of possiblenew areas of rich biodiversity


Conclusion

Here we identify the western part of the Australian continent as aregion of extremely rich biodiversity for subterranean fauna witha projected 4140 stygobitic and troglobitic species a significantsubterranean fauna is also likely to occur across the eastern partof the continent but considerable survey work is required toestimate the diversity of this fauna Compared with other regionsof the world we consider the Australian subterranean fauna tobe unique in its diversity for three key reasons (1) the range anddiversity of subterranean habitats where fauna have beendiscovered are both extensive and novel compared with thenorthern hemisphere (2) direct faunal links to Gondwana arefound in Australiarsquos west emphasising its early biogeographichistory and (3) tertiary events particularly developing aridityin the late MiocenePliocene (14ndash2Mya) appear to havedominated the diversification of Australiarsquos subterraneanfauna unlike much of the northern hemisphere (Stoch andGalassi 2010) where the fauna was not greatly modifiedduring Pleistocene glaciations

Order of authorship

MTGADA SJBCMSH andWFH all contributed to writing themanuscript andcollating the taxonomic geographical and speciesrichness data The remaining authors listed in alphabetical ordercontributed data and ideas during a workshop in Darwin in 2009(see lsquoAcknowledgementsrsquo) and during the writing of themanuscript Images were kindly contributed by SME

Acknowledgements

Much of the research that underpins the data presented in this review wasfunded by the Australian Research Council (ARC) Discovery and Linkagegrants DP0663675 DP0770979 LP0669062 LP0776478 LP0669062and LP100200494 and the Australian Biological Resources Study Thediscussions that led to this review and collation of an early version of thespecies diversity data occurred at a workshop held in Darwin in September2009 funded through a Working Group on The Diversity and Evolution ofTroglobitic and Groundwater Ecosystems which is a part of the ARCResearch Network (RN0457921) Discovering the Past and Present toShape the Future Networking Environmental Sciences for Understandingand Managing Australian Biodiversity (Environmental Futures Network)Finally we would like to thank numerous colleagues for their help supportand discussions on the evolution and diversity of subterranean animalsThanks also to two anonymous reviewers and associate editor GonzaloGiribet who provided detailed comments that helped to improve an earlierversion of this article

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Harvey M S and Leng M C (2008b) The first troglomorphicpseudoscorpion of the family Olpiidae (Pseudoscorpiones) withremarks on the composition of the family Records of the WesternAustralian Museum 24 387ndash394

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Harvey M S Berry O Edward K L and Humphreys G (2008)Molecular and morphological systematics of hypogean schizomids(Schizomida Hubbardiidae) in semiarid Australia InvertebrateSystematics 22 167ndash194 doi101071IS07026

Hedin M C (1997) Speciational history in a diverse clade of habitat-specialized spiders (Araneae Nesticidae Nesticus) inferences fromgeographic-based sampling Evolution 51 1929ndash1945 doi1023072411014

Holsinger J R (1992) Sternophysingidae a new family of subterraneanamphipods (Gammaridea Crangonyctoidea) from South Africa withdescription of Sternophysinx calceola new species and comments onphylogenetic and biogeographic relationships Journal of CrustaceanBiology 12 111ndash124 doi1023071548726

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Jaume D and Humphreys W F (2001) A new genus of epacteriscidcalanoid copepod from an anchialine sinkhole in northwestern AustraliaJournal of Crustacean Biology 21 157ndash169 doi1016510278-0372(2001)021[0157ANGOEC]20CO2

Jaume D Boxshall G A and Humphreys W F (2001) New stygobiontcopepods (Calanoida Misophrioida) from Bundera sinkhole ananchialine cenote on north-western Australia Zoological Journal ofthe Linnean Society London 133 1ndash24 doi101111j1096-36422001tb00620x

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Karanovic T (2004a) Subterranean Copepoda from aridWestern AustraliaCrustaceana Monographs 3 1ndash366

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Karanovic I (2005b) A newCandoninae genus (Crustacea Ostracoda) fromsubterranean waters of Queensland with a cladistic analysis of the tribeCandonopsini Memoirs of the Queensland Museum 50 303ndash319

Karanovic T (2006) Subterranean copepods (Crustacea Copepoda) fromthePilbara region inWesternAustraliaRecordsof theWesternAustralianMuseum 70(Supplement) 1ndash239


Karanovic I (2007) Candoninae Ostracodes from the Pilbara Region inWestern Australia Crustaceana Monographs 7 1ndash432

Karanovic T and Eberhard SM (2009) Second representative of the orderMisophrioida (Crustacea Copepoda) from Australia challenges thehypothesis of the Tethyan origin of some anchialine faunas Zootaxa2059 51ndash68

Karanovic I and Marmonier P (2002) On the genus Candonopsis(Crustacea Ostracoda Candoninae) in Australia with key to the worldrecent species Annales de Limnologie 38 199ndash240 doi101051limn2002018

Karanovic I and Marmonier P (2003) Three new genera and nine newspecies of the subfamily Candoninae (Crustacea Ostracoda Podocopida)from the Pilbara Region (Western Australia) Beaufortia 53 1ndash51

Karanovic T and Pesce G L (2002) Copepods from ground waters ofWestern Australia VII Nitokra humphreysi sp nov (CrustaceaCopepoda Harpacticoida) Hydrobiologia 470 5ndash12 doi101023A1015694015451

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Leys R and Watts C H S (2008) Systematics and evolution of theAustralian subterranean hydroporine diving beetles (Dytiscidae) withnotes on Carabhydrus Invertebrate Systematics 22 217ndash225doi101071IS07034

Leys R andWatts C H S (2010)Paroster extraordinarius sp nov a newgroundwater diving beetle from the Flinders Ranges with notes on otherdiving beetles from gravels in South Australia (Coleoptera Dytiscidae)Australian Journal of Entomology 49 66ndash72 doi101111j1440-6055200900738x

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Pesce G L and De Laurentiis P (1996) Copepods from ground waters ofWesternAustralia IIIDiacyclops humphreysin sp and comments on theDiacyclops crassicaudis-complex (CopepodaCyclopidae)Crustaceana69 524ndash531 doi101163156854096X01096

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Pesce G L De Laurentiis P and Humphreys W F (1996b) Copepodsfrom ground waters of Australia II The genus Halicyclops (CrustaceaCopepoda Cyclopidae) Records of the Western Australian Museum 1877ndash85

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Poore G C B and HumphreysW F (2003) Second species ofMangkurtu(Spelaeogriphacea) from north-western AustraliaRecords of theWesternAustralian Museum 22 67ndash74

Reddell JR (1981)A reviewof the cavernicole fauna ofMexicoGuatemalaand Belize Texas Memorial Museum Bulletin 27 1ndash327

RixMGHarveyM S andRoberts J D (2008)Molecular phylogeneticsof the spider family Micropholcommatidae (Arachnida Araneae) usingnuclear rRNA genes (18S and 28S) Molecular Phylogenetics andEvolution 46 1031ndash1048 doi101016jympev200711001

Scarsbrook M R Fenwick G D Duggan I C and Haase M (2003)A guide to the groundwater invertebrates of New ZealandNIWA Scienceand Technology Series 51 59

Sharratt N J Picker M D and Samways M J (2000) The invertebratefaunaof the sandstonecavesof theCapePeninsula (SouthAfrica) patternsof endemism and conservation priorities Biodiversity and Conservation9 107ndash143 doi101023A1008968518058

Sket B Paragamian K and Trontelj P (2004) A census of the obligatesubterranean fauna of the Balkan Peninsula In lsquoBalkan Biodiversityrsquo(Ed H I Griffith) pp 309ndash322 (Kluwer Academic PublishersDordrecht)

Souza M F V R and Ferreira R L (2010) Eukoenenia (PalpigradiEukoeneniidae) in Brazilian caves with the first troglobiotic palpigradefrom South America The Journal of Arachnology 38 415ndash424doi101636Ha09-1121

Stoch S and Galassi D M P (2010) Stygobiotic crustacean speciesrichness a question of numbers a matter of scale Hydrobiologia653 217ndash234 doi101007s10750-010-0356-y

Taiti S and Humphreys W F (2001) New aquatic Oniscidea (CrustaceaIsopoda) from groundwater calcretes ofWesternAustraliaRecords of theWestern Australian Museum 64(Supplement) 63ndash83

Tasaki S (2006) The presence of stygobitic macroinvertebrates in karsticaquifers a case study in the Cradle of Humankind World Heritage SiteMaster of Science Thesis University of Johannesburg South Africa

Thurgate M E Gough J S Spate A and Eberhard S M (2001a)Subterranean biodiversity in New South Wales from rags to richesRecords of the Western Australian Museum 64(Supplement) 37ndash48

ThurgateM E Gough J S Clarke A K Serov P and Spate A (2001b)Stygofauna diversity and distribution in eastern Australian caves andkarst areas Records of the Western Australian Museum 64(Supplement)49ndash62

TomlinsonM (2009)A framework for determining the environmentalwaterrequirements of alluvial aquifer ecosystems PhD Thesis University ofNew England Armidale

Trajano E (2000) Cave faunas in the Atlantic tropical rain forestcomposition ecology and conservation Biotropica 32 882ndash893

Volschenk E S andPrendini L (2008)Aops oncodactylus gen et sp novthe first troglobitic urodacid (Urodacidae Scorpiones) with a re-assessment of cavernicolous troglobitic and troglomorphic scorpionsInvertebrate Systematics 22 235ndash257 doi101071IS06054

Watts C H S and Humphreys W F (2003) Twenty-five new Dytiscidae(Coleoptera) of the genera Tjirtudessus Watts amp Humphreys NirripirtiWatts amp Humphreys and Bidessodes Regimbart from undergroundwaters inAustraliaRecordsof theSouthAustralianMuseum36 135ndash187

Watts C H S and Humphreys W F (2009) Fourteen new Dytiscidae(Coleoptera) of the genera Limbodessus Guignot Paroster Sharp andExocelina Broun from underground waters in Australia Transactions ofthe Royal Society of South Australia 133 62ndash107

Wilkens H Culver D C andHumphreysW F (Eds) (2000) lsquoEcosystemsof the World Subterranean Ecosystemsrsquo (Elsevier Amsterdam)

Wilson G D F (2001) Australian groundwater-dependent isopodcrustaceans Records of the Western Australian Museum62(Supplement) 239ndash240

Wilson G D F (2003) A new genus of Tainisopidae fam nov (CrustaceaIsopoda) from the Pilbara Western Australia Zootaxa 245 1ndash20

Wilson G D F (2008) Gondwanan groundwater subterranean connectionsof Australian phreatoicidean isopods (Crustacea) to India and NewZealand Invertebrate Systematics 22 301ndash310 doi101071IS07030

Wilson G D F and Johnson R T (1999) Ancient endemism amongfreshwater isopods (Crustacea Phreatoicidea) In lsquoThe Other 99 TheConservation and Biodiversity of Invertebratesrsquo (Eds W Ponder andD Lunney) pp 264ndash268 (Transactions of the Royal Zoological Societyof New South Wales Mosman)

Wilson G D F and Keable S J (1999) A new genus of phreatoicideanisopod (Crustacea) from the north Kimberley region Western AustraliaZoological Journal of the Linnean Society London 126 51ndash79doi101111j1096-36421999tb00607x

Wilson G D F and Ponder W F (1992) Extraordinary new subterraneanisopods (Peracarida Crustacea) from the Kimberley region WesternAustralia Records of the Australian Museum 44 279ndash298 doi103853j0067-197544199236

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Yeates D K Harvey M S D and Austin A D (2003) New estimates forterrestrial arthropod species-richness in Australia Proceedings of theRoyal Society of South Australia 7 231ndash241

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Manuscript received 5 November 2010 accepted 8 January 2011


httpwwwpublishcsiroaujournalsis

Mexico (Reddell 1981) and most recently caves of south-eastAsia (Deharveng 2005) Subterranean faunal diversity isgenerally concentrated in karst and pseudokarst areas(Juberthie and Decu 1994 Culver et al 2001 Christman et al2005 Deharveng 2005) Even within this geomorphologicalconstraint (ie it is patchily distributed Fong and Culver 1994Culver et al 2004) the density of caves and the sampling intensityby generations of researchers in these regions have providedbiologists with the opportunity to efficiently document cavesand their fauna (Christman and Culver 2001 Culver et al2004 Zagmajster et al 2008) Consequently knowledge ofthese regions and their biodiversity phylogeography andfunctional ecology are well progressed (Gibert et al 1994Wilkens et al 2000 Culver and White 2004)

As recently as 16 years ago Humphreys (1994) advocated aknowledge gap of subterranean fauna in Australia especially inareas other than the lava tubes of tropical north Queenslandwhich are a noted troglofauna hotspot (Culver and Sket 2000)Considered depauperate of karstic habitat and havingwidespreadaridity historically Australia was considered a poor prospectfor subterranean fauna Australiarsquos arid Pleistocene climatichistory was deemed to lack key climate history events such as

Pleistocene glaciations (Moore 1964 Hamilton-Smith 1967Barr 1973) which were considered drivers of subterraneanbiodiversity in the northern hemisphere (Peck 1980 Boutin1994) This excludes Tasmania (Derbyshire 1972) which isrichly endowed with karst and caves and was subject toPleistocene glaciations These hypotheses coupled with apaucity of research on the southern hemisphere subterraneanbiota over the last two centuries have led to a prolongedlag in discovery of Australiarsquos obligate subterranean speciesHistorically the most sampled cave regions in Australiawere south-eastern South Australia (SA) New South Wales(NSW) Tasmania and the Nullarbor Plain (spanning parts ofSA and Western Australia (WA)) It is now appreciated thatAustralia holds a great variety of subterranean habitats withassociated invertebrate faunas found both in karst and non-karst environments (Eberhard and Humphreys 2003) Notabledifferences between Australia and other regions of the worldare the absence of urodele amphibians and stenasellid isopodsand a scarcity of carabid beetles and cave fishes

Focussed research on subterranean fauna from karst regionsin WA comprising troglobionts (Humphreys et al 1989)and stygobionts soon after (Humphreys and Adams 1991)

Fig 1 Geological and climatic regions of Australia from which we describe a subterranean faunalbiodiversity hotspot Five regions are named including the Western Shield an area that has beencontinually emergent since the Proterozoic Dashed lines delineate the (1) Kimberley (2) Pilbara and(3) Yilgarn Additionally the Gondwanan refuges that comprise soft-rock karst are the (4) Nullarbor and(5) south-east of South Australia













No knownspecies


describedor known



Total 403 367 4140 186





































Conclusion


Order of authorship


Acknowledgements


References














































































































































































No knownspecies


describedor known



Total 403 367 4140 186





































Conclusion


Order of authorship


Acknowledgements


References






































































































































































































Conclusion


Order of authorship


Acknowledgements


References























































































































































































Conclusion


Order of authorship


Acknowledgements


References













































































































































































Conclusion


Order of authorship


Acknowledgements


References











































































































































































Conclusion


Order of authorship


Acknowledgements


References



































































































































































Conclusion


Order of authorship


Acknowledgements


References






























































































































































































































































































































































































































































































































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VIEWPOINT. Is the Australian subterranean fauna uniquely diverse?

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