Subterranean wetlands of arid Australia: remipedes, spelaeogriphaceans & diving beetles

William Humphreys, Chris Watts, Remko Leys and Steve Cooper

Western Australian Museum, South Australian Museum, Adelaide University Stable but dynamic Australia

Data: Wilson Emergent since Proterozoic Bradbury WH

Cretaceous inundation

Islands of freshwater ancients and shore colonisation.

Denudation: 6 km since Jurassic 12 km since Permian (Belton et al. 2004) changes geological Tainisopidea context: Christmas Island Karst areas 1000 km Current climate

Arid zone — evaporation>rainfall Anchialine systems

Circum-global distribution—tropics and subtropics mostlyEpicontinental in arid areas and oceanic anchialine systems

? Cape Range peninsula  Exmouth Bundera Sinkhole

Ningaloo The most  important biodiversity site C-28  in Australia

Cape Range — hydrological environment near the coast

Terraces

Cape Range Coastal plain Interface caves Freshwater lens Ocean Saltwater 100 m intrusion

Groundwater estuary Ocean Height Sinkhole 2000 mm height 1800 1600 1400

1200 1000 800 600 400 200 0 26 27 28 29 30 Sidereal day 1100

1000

900

800 0 400 800 1200 1600 2000 Ocean Height mm

Bundera Sinkhole C-28

Large white gliding filiamentous sulphur oxidizing bacteria (chemolithoautotrophs)

Thioploca tracking the oxic / anoxic boundary Motile filiaments (Beggiatoa spp.) on sediments and attached filaments on solid surfaces (commonly Thiotrix spp). Photo: Stefan Eberhard, Western Australia Museum Gradients: Depth profile: Bundera Sinkhole

Temperature ORP

Salinity pH

H2S N-species profiles: Bundera Sinkhole

H2 S NO 3   

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 Cascade of N-species in upper few metres equivalent to the upper few mm of anoxic muds Remiped anchialine fauna • Structure highly predictable (~ generic composition) • Characteristically with atyid shrimps, thermosbaenaceans, hadziid amphipods, cirolanid isopods, remipeds, thaumatocypridid ostracods. • Many copepods (epacteriscid, psedocyclopiid, and ridgewayiid calanoids, halicyclopine cyclopoids, speleophriid misophrioids, superornatiremid harpacticoids.) • Only known from NW Australia, Canary Is, northern Caribbean (Grand Bahamas Banks, Cuba, Quintana Roo, Yucatan) Holocene marine transgression

Holocene — rise from ~150 m drowned karst platforms, fragmented troglofauna and elevated anchialine fauna

stygobites Fauna from Cape Range and environs anchialine system

Milyeringa veritas Perciformes: Eleotridae 1of 2 stygobitic Bundera, CRP, BWI vertebrates in Oz Ophisternon Osteichthyes: 1of 2 stygobitic CRP candidum Synbranchidae vertebrates in Oz Halosbaena tulki Thermosbaenacea: New Order for SH CRP, BWI, Pilbara Halosbaenidae Stygiocaris stylifera Decapoda: Atyidae New genus, Bundera, CRP, BWI, endemic Pilbara Stygiocaris lancifera Decapoda: Atyidae CRP Haptolana pholeta : Cirolanidae New gen. for SH CRP, BWI, Pilbara Halicylops Copepoda: Cyclopoida: CRP longifurcatus Cyclopidae Phyllopodopsyllus Copepoda: New genus for Oz CRP wellsi Harpacticoida Only stygal sp in gen. Fauna from suboxic section of Bundera Sinkhole

Prionospio thalanji Polychaeta: Spionidae Only stygobite in genus Danielopolina kornickeri Ostracoda: Halocyprida: Thaumatocyprididae New Family for SH Lasionctes exleyi Remipedia: Nectiopoda: Speleonectidae New Class for SH Liagoceradocus branchialis Amphipoda: Hadziidae Bunderia misophaga Calanoida: Epacteriscidae New Family for SH Speleophria bunderae Copepoda: M isophrioida: Speleophriidae New Order for SH Stygocyclopia australis Calanoida: Pseudocyclopiidae New Family for Oz Lasionectes: Remipedia Lasionectes (Remipedia) Affinities of the anchialine fauna

Halosbaena spp. (Thermosbaenacea) Variations on this theme in:

Bunderia cf Enantronoides Epacteriscidae (Calanoida)

Ophisternon : Synbranchidae Speleophria (Misophrioida)

Danielopolina (Ostracoda: Thaumatocypridoidea) Stygocyclopia (Calanoida)

Haptolana (Isopoda: Cirolanidae) Danielopolina (Thaumatocyprididae) Danielopol et al. 2000.

Pokornyopsis feifeli Upper Jurassic marine crevicular palaeoenvironment (Aubrecht & Kozur 1995)

Anchialine Danielopolina Tethys 1 Plate positions 175 Ma Pokornyopsis feifeli

Tethys

Li and Powell v. 6.0 Pokornyopsis feifeli Atlantic opening 110Ma

Tethys Recent developments Danielopolina • Tethyan fauna on (Thaumatocypridoidea) Christmas Island, a sea mount island • Microceratina (Cytheruridae) spread through the Tethys Sea (Namiotko et al. 2004) First description of soft parts of this Miocene genus Enigmatic Western Shield Pilbara: cyclone affected arid region with episodic rainfall Western Fortescue Plain aquifer: lacustrine limestone Spelaeogriphacea

Tethys

Li and Powell v. 6.0

Spelaeogriphacea Water mites Mideopsellinae Arrenuroidea: Mideopsidae

Cave and interstitial habitats

Mideopsellides Tiramideopsis

Africa India

Australia Antarctica Data from Harvey 2001 : Hypsimetopodidae

hypogean

epigean? Nichollsia Pilbaraphreatoicus °Since Jurassic denudation processes Hyperoedesipus removed ~5 km of cover rock. Africa India Forcing a change in geological context? Australia Antarctica °Kohn,G.D.F. et al. Wilson, 2002. Australia n Journal of Earthpers. Sciences Comm.49: 697 2002-717. Groundwater calcretes

Shallow, thin (~ 10 m) carbonate deposits in arid zone associated with palaeovalleys Gascoyne palaeovalley

Photos: Remko Leys Palaeovalleys constrained landscape evolution and groundwater flow

Groundwater Calcrete

Quaternary K-T boundary

Divide of Archaean rocks Yilgarn calcrete stygofauna

• Diving beetles (Dytiscidae) • ‘Terrestrial’ isopods (Oniscidea) • Bathynellacea • Amphipoda • Ostracoda • Copepoda Groundwater calcretes are associated with salt lakes (playas) Windarra calcrete near salt lake cf. anchialine systems

0 -.5 Salin-PSS -1 Bathynellacea, Cyclopoida, Routine -1.5 Harpacticoida, Amphipoda, -2 purging of -2.5 Dytiscidae -3 bores -3.5 destroys -4 -4.5 biologically -5 important -5.5 -6 information -6.5 -7 . 10 20 30 40 50 60 70 80 90 100 110

0 .5 1 1.5 2 2.5 3 3.5 4 4.5 5 DO-mg/L -150 -100 -50 0 50 100 150 200 250 ORP-mV Subterranean waterbeetles (Coleoptera: Dytiscidae)

surface

Now Limbodessus Tjirtudessus Nirridessus Liodessus 1mm Dytiscidae L. compactus Limbodessus macrotarsus

Nirripirti arachnoides

Photo: C.H.S.Watts Summary of taxonomic data

50 species from 22 calcrete aquifers

12

8

4 frequency

0 1 2 3 4 number of species / locality Waterbeetle calcretes karstification and erosion phylogenetic tree formed of calcretes mitochondrial DNA

- two tribes - 36 subterranean lineages (in black) - 23 surface lineages (in grey)

- Average climatic conditions: blue: relatively humid Bidessini yellow: arid conditions

- subterranean lineages Hydroporini < 10 million years old

Million years ago Waterbeetle Sympatric species phylogenetic tree from different lineages/tribes mitochondrial DNA

- localities: Austin Downs Cunyu Mineral Bore Cunyu Sweetwaters Well Yuinmery Depot Springs Three Rivers Pinnacles

- multiple ancestral species colonised the same calcrete

Mya 350,000 km2 — 2/3 size France Dytiscidae Bidessoides 8 spp.

Subterranean Dytiscidae occur in Copelatinae Hydroporinae: Bedessini Hydroporini

Stygal data: Watts et al. Epigean data: C.H.S.Watts Poraster 8 spp. 1, All subterranean species are within the arid area.

2, Not all calcretes within arid area have stygobitic dytiscids.

3, Epigean species largely occur outside the arid area

4, Aridity + calcrete necessary but not complete requirement for stygal dytiscids

Stygal data: Watts et al. Epigean data: C.H.S.Watts Oniscidea • 19 species belonging to 2 genera :

• Haloniscus 17 species • Androphiloloscia 2 species 1 mm 1 mm

Haloniscus searlei Haloniscus n. sp. 12 Lake Keilambete, VIC Carnegie, Jimmys Well, WA All collection sites

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Stygobites Epigean Haloniscus n. sp. 4 Haloniscus n. sp. 12 Haloniscus n. sp. 8 4 9 11 12

Haloniscus longiantennatus Haloniscus n. sp. 13 8 Haloniscus stilifer Andricophiloscia pedisetosa Haloniscus tomentosus Haloniscus n. sp. 3 Andricophiloscia n. sp. 6 3 Haloniscus n. sp. 10 Haloniscus n. sp. 11 1 Haloniscus n. sp. 5 7 10 2 5 Haloniscus sp. Haloniscus n. sp. 9

Yilgarn Region (Western Australia) MURCHISON: 1, Old Cue; 2, Windimurra; 3, Yarrabubba. GASCOYNE: 4, Three Rivers. RAESIDE: 5, Yuinmery; 6, Lake Mason; 7, Perrinvale. CAREY: 8, Bubble Well; 9, Uramurdah; 10, Laverton Downs. CARNEGIE: 11, Jundee South; 12, Jimmys Well. (Map based on 1: 2,500,000 Hydrogeological Map of Western Australia 1989 compiled by D.P. Commander) BES 9462.1 Maximum Parsimony 89 BES 9461.1 100 BES 9461 Haloniscus n. sp. 2 85 BES 6667 BES 9458 Length=1749 BES 9465.1 79 100 Haloniscus n. sp. 6 NT BES 9467.1 61 100 BES 6685 BES 9493 Haloniscus n. sp. 1 BES 8086 Haloniscus n. sp. 7 BES 9886.1 98 BES 9891.1 BES 9887.1 100 BES 6573 Haloniscus searlei EPIGEAN BES 9892.1 100 BES 9913 BES 9912 BES 6655 Haloniscus sp. BES 8101 100 Haloniscus n. sp. 3 BES 5637 BES 6601 Haloniscus n. sp. 8 BES 10527 Haloniscus stilifer 52 BES 9888.1 Andricophiloscia stepheni BES 9890 ???? BES 6455 Haloniscus longiantennatus BES No Nr Haloniscus n. sp. 12 BES 10290 Haloniscus n. sp. 10 51 BES 10257 Haloniscus n. sp. 9 BES 10410 Andricophiloscia n. sp. A. ell. Armadilloniscus ellipticus (Detonidae) 100 BES 9924 Porcellionides pruinosus (Porcellionidae) BES 9895 BES 10201 Haloniscus anophthalmus BES 7416.1 Laevophiloscia yalgooensis (Philosciidae) BES 8956 Haloniscus n. sp. 5 BES 11448 Tylos neozelanicus (Tylidae) BES 11441 Pygolabis humphreysi (Tainisopidea) BES 9923 Deto marina (Detonidae) AY051333L. per. Ligia perkinsi (Ligiidae) 10 changes 5626 7270 Preliminary amphipod 8094M 5626.2 Paroo phylogeny: unknown 5609.2 5609 100 8094F 8096 5632 100 5596 - N = 43 amphipods from 9 calcretes 5596.2 Killara 8130 - 650 bp of CO1 gene 9310 74 100 - 1 of 2 Maximum Parsimony trees 9331.S Mt Padbury 9332 of length 1005 61 8142 Paroo 100 8698 Milgun/ outcamp 8697 86 100 8493 Savoury Ck. - strong bootstrap support 8496 8480 Ilgari Ck. for distinct mtDNA lineages 8664A in each calcrete. 8664 100 8665.4 -* evidence for distinct 89 8665.5 53 8664B Milgun/ Earrie mtDNA lineages in 8664.5 (20%) * 8664.S sympatry: K2P divergences 9336 of 8.2%-20% (~3-9 my ago) 100 9336.S 9344 - 1-2 species / calcrete? 100 9344.S Innouendy * 9349 94 100 9349.S (8.2%) 9348.S 8614B 8615 100 8608 8607 Plutonic 8614 B 8614A 0331 Pilbara 9309.S Mt Padbury 10 changes Summary

• Anchialine • Lacustrine calcrete • Groundwater calcrete • Procaridid (fresh and saline) • Remipede • ALSO • Enigma • Fractured rock • Shallow regolith • Karst • Alluvial • Characterisation of subterranean wetlands infancy Geographic factors and arid zone subterranean fauna

Spreading aridity

Tethys Eustatic changes Northern drift in 3° India

Glaciation Proterozoic Gondwana

Antarctica

Pangaea Circum-Antarctic current Eustacy Acknowledgements Stefano Taiti — Onsicidea; Joo-Lae Cho — Bathynellacea; J. Bradbury — Amphipoda; K. Saint — DNA Cave divers: Andrew Poole, Dave Warren, Stefan Eberhard, Paul Hosie, Craig Campbell

Graphics: Ken Grimes

Photography: Douglas Elford, Stefan Eberhard, Andrew Poole, Paul Hosie, Funding:Australian Biological Resources Study, Australian Field support: Darren Brooks, Julianne Research Council, Waldock, Jack Riley, Rae Young, Butler Trust, Western Australian Miranda Humphreys, Phoebe Museum, Department of Humphreys Conservation and Land Management