Memoirs of the Museum of Victoria 56(2):5 13-51 9 (1997) 28 February 1997 https://doi.org/10.24199/j.mmv.1997.56.45 AMPHIPOD (CRUSTACEA) DIVERSITY IN UNDERGROUND WATERS IN AUSTRALIA: AN ALADDIN'S CAVE

J. H. Bradbury and W. D. Williams

Department of Zoology, University of Adelaide, Adelaide, SA 5005. Australia

Abstract

Bradbury, J.H. and Williams, W.D., 1997. Amphipod (Crustacea) diversity in underground waters in Australia: an Aladdin's cave. Memoirs ofthe Museum of Victoria 56(2): 513-519. The presently known troglobitic and troglophilic (stygobiont) species of Australian aquatic amphipods are listed and discussed, and their geographical distributions are indi- cated. The 26 species known are predominantly in crangonyctoid and hadzioid families. Further undescribed species are referred to. The diversity is high and confirms Australia as a centre of stygobiont amphipod speciation. Explanations for the diversity include the con- siderable extent of karst, the frequent occurrence and extensive areas of former marine transgressions, and palaeoclimatic fluctuations. Attention is drawn to the usefulness of sty- gobiont amphipods as biogeographical tools, and to the need for their diversity in Australia to be noted in discussions, legislation and actions to conserve Australian biodiversity.

Introduction In this paper, our immediate intentions are to summarize the present status of our knowledge Until relatively recently, our knowledge of the of the of hypogean amphipods in Aus- taxonomy of Australian freshwater amphipods tralia on the basis of described species, to pro- (Crustacea: ) was limited. Few vide some indication of the extent of diversity species had been described, the extent of diver- based on described species and undescribed sity was unrecognized, and most available material, and to offer some explanation for this species descriptions were in need of revision. diversity. Thus this paper provides a basis for Williams and Barnard (1988) began the initial discussion and should help achieve two, more revision with redescriptions of all known needed general aims, namely: species and added descriptions of a few new 1. to focus attention upon the usefulness of species. Their efforts were continued in a second hypogean amphipods as biogeographical paper (Barnard and Williams, 1995). Both tools (given the nature of their ecology and papers referred to subsurface as well as surface environments) within an Australian context, forms. and Taxonomic studies of the Australian fresh- 2. to draw attention to the significant diversity water amphipods are a long way from com- of Australian hypogean amphipods at a time pletion but the papers of Barnard and Williams when considerable discussion is taking place and other recent studies have pointed to the at a variety of levels — State, Federal and existence of much greater diversity amongst sur- international — on the conservation of face forms than had been realised. They also biodiversity. point to the existence of greater biodiversity amongst subsurface forms than had been In these discussions, the diversity of hypogean forgotten; whilst caves realised (Williams, 1986). The diversity of sub- amphipods should not be other subsurface waters do not have the surface forms is confirmed by the studies of and of course Knott (1983) and Bradbury and Williams (1995, faunal diversity of surface waters, and col- lack plants, within the groups that do 1996 a, b) and unpublished work on recent for example. Culver, 1982, and lections from caves and other underground occur there (see, Holsinger. 1985), much speciation has waters in Western Australia, New South Wales Barr and and Tasmania. This diversity amongst subsur- taken place. Holsinger (1991, 1994a) has pre- viously noted the global importance of hypogean face forms is not surprising given both the biogeographical studies, and paucity of previous studies and, more import- amphipods for Knott (1985) has noted their interest in Aus- antly, the fact that amphipods are known world- Australian speleologists have long recog- wide to be amongst the most widespread, tralia. for caves to be conserved and abundant and diverse of subsurface aquatic nized the need fauna protected on the basis of both bio- invertebrates (Holsinger, 1991). their

513 514 J.H. BRADBURY AND WD. WILLIAMS

logical and geomorphological criteria. Govern- sity is concerned worldwide, namely, the cran- ments have generally acted sympathetically to gonyctoids, the hadzioids s. I. and the bogidiel- this need for cave protection and conser- lids. vation. The geographical distribution of the species

In passing, we also mention the recent recog- listed in Table 1 is indicated in Fig. 1. An obvi- nition of much higher diversity than expected in ous point to emerge from this figure is the large other bodies of inland water in Australia that — number of stygobiont species recorded from like underground waters — have generally Western Australia. Of particular note in this received less attention from biologists than per- respect is the extraordinarily large number manent fresh waters near major metropolises. described from Barrow Island, a relatively small These waters include salt lakes, temporary offshore island. Species recorded from this streams and freshwater lakes, and other bodies island comprise those collected from boreholes of surface water in arid and semi-arid regions. (species of Nedsia and Bogadomma australis), Recent work has indicated that considerable and two species from an anchialine cave — that biodiversity occurs within such localities (e.g., is, a coastal cave under marine influence — (Lia- see Frey, 1991; Timms, 1993; Comin and goceradocus spp.). None of the Nedsia species

Williams, 1 994). Their fauna, however, does not was found co-existing with another (but note usually involve amphipods as these paucity of specimens available), and all at pres- are more or less confined to permanent, fresh ent are known only from one locality each, the waters. It does involve a comprehensive range of type locality. Apart from the facultatively sub- other invertebrate groups. terranean Austrochiltonia australis, which is also a common and widespread surface form, other species listed in the table and figured in the map Present status of the hypogean (stygobiont) are likewise recorded from either a single amphipod fauna locality or a restricted area. An absence of sym- Table 1 lists all described species recorded thus patry appears to be generally characteristic of far from either underground waters (caves, bore- stygobiont amphipods elsewhere too. holes) or springs near their source. It lists two A less obvious point shown by Fig. 1 is that the principal sorts of taxa: those which have been distributions of hypogean amphipods extend recorded from underground waters (including more to the north in Australia than do those of springs) and nowhere else (obligate stygobionts or troglobites sensu Barr and Holsinger, 1985); and those recorded from both underground and surface waters (facultative stygobionts or troglo- philes). In total, the table lists over 30 species of which half can be regarded as troglobites and half, troglophiles. All are endemic. On the basis of described species, therefore, approximately 60 per cent of the total amphipod diversity of Australian inland waters can be found in subsur- face waters. This figure is far higher than the global figure of 13 per cent given by Holsinger (1993) for the approximate fraction of all described amphipod species that are stygo- bionts. Our percentage is undoubtedly inflated by our concentration on stygobionts during recent studies. It seems likely that more bal- anced and comprehensive studies of both hypo- gean and epigean species will lead to some correction of this high figure towards a lower value. With regard to the systematic positions of the Figure I. Geographical distribution of stygobiont species listed in the table, it is immediately obvi- amphipods in Australia. 1-12, hadzioids; 13. Bogad- ous that most belong to the three groups ident- omma; 14-28, crangonyctoids. Austrochiltonia aus- ified by Holsinger as (1993) those of most tralis, Phreatochiltonia anapthalma and Pseudomoera importance so far as hypogean amphipod diver- fontana omitted. .

AMPHIPOD DIVERSITY IN UNDERGROUND WATERS IN AUSTRALIA 515

Table 1. Systematic position and geographic distribution of Australian subterranean amphipods.

The index numbers relate to Fig. 1

Taxon Distribution Habit Index no. HADZIOIDS Melitidae Nedsia straskraba Bradbury & Williams Barrow Island troglobite 1 N. fragilis Bradbury & Williams Barrow Island troglobite 2 N.humphreysi Bradbury & Williams Barrow Island troglobite 3 N.hurlberti Bradbury & Williams Barrow Island troglobite 4 N.urifimbriata Bradbury & Williams Barrow Island troglobite 5 N. macrosculptilis Bradbury & Williams Barrow Island troglobite 6 N.sculptilis Bradbury & Williams Barrow Island troglobite 7 Liagoceradocus subthalassicus Bradbury & Barrow Island anchialine troglobite 8 Williams Liagoceradocus branchialis Bradbury & North West Cape anchialine troglobite 9 Williams Nedsia douglasi Barnard & Williams North West Cape troglobite 10 Brachina invasa Barnard & Williams Flinders Ranges hyporheic interstitial 11 12 Nurinna Cave Melita like Nullabor Plain troglobite BOGIDIELLIDS Bogidiellidae 13 Bogadomma australis Bradbury & Williams Barrow Island troglobite CRANGONYCTOIDS Paramelitidae 14 Hurleya kalamundae Straskraba SW Australia troglobite Nicholls Darling Range, troglophile 15 Protocrangonyx fontinalis WA 16 Uroctena westralis (Chilton) nr Perth W A troglophile Totgammarus eximius Bradbury & Williams SW Australia troglophile 17 troglobite 18 Chillagoe thea Barnard & Williams N Queensland 19 Giniphargus pulchellus Karaman & Barnard Gippsland Vic troglobite 20 Austrogammarus species Barnard & Tasmania troglophile Karaman 24 Austrogammarus smithi Williams & Barnard Tasmania troglophile troglophile 21 Antipodeus antipodeus (G.W.Smith) Tasmania troglophile 22 Antipodeus wellingtoni (G.W.Smith) Tasmania troglophile 23 Antipodeus franklini Williams & Barnard Tasmania troglobite 25 Uronyctus longicaudus Stock & Iliffe SE South Australia Perthiidae Australia troglophile 26 Perthia acutitelson Straskraba SW Neoniphargidae Vic. possible troglophile 27 Neoniphargus obrieni Nicholls Mt Buffalo, Tasmania troglophile 28 Neoniphargus spp. Stebbing CEINIDS Ceinidae spring, SA poss troglobite 29 Phreatochiltonia anapthalma Zeidler Mound cosmopolitan troglophile 30 Austrochiltonia australis (Sayce) EUSIRIDS Eusiridae SE Australia troglophile 31 Pseudomoera fontana (Sayce) .

516 J.H. BRADBURY AND WD. WILLIAMS

any surface aquatic amphipod. Thus, those from Barrow Island in Western Australia and Chilla- goe thea in Queensland lie many hundreds of kilometres north of areas where surface amphi- pods occur. It is not difficult to provide an explanation of this; freshwater amphipods are not common in subtropical and tropical waters and only subterranean waters in these regions provide the lower temperatures and more stable environmental conditions required to support amphipod populations. It may be noted that not all northern and apparently suitable subtropical subsurface waters in Australia contain amphi- pods. The Cutta Cutta caves near Katherine, Northern Territory, for example, do not appear to be inhabited by amphipods; a recent and dili- gent search for them by one of us (WDW) failed to locate any specimens although considerable material of the atyid shrimp which do inhabit the caves was collected (Parisia spp.; see Figure 2. Marine transgressions in Williams, 1964). Perhaps the water in this cave Australia during the Cretaceous (119-114 million years ago). Redrawn system is too warm, the atyids too powerful a from Paine (1990). Areas free of inundation shaded. competitor, or there was no available ancestral surface form. No amphipods, likewise, have been collected from caves in the Kimberly The ecological nature of subsurface waters region of Western Australia (Humphreys, inhabited by species here considered as stygo- 1995). bionts covers a considerable range in type. As for geographical patterns, three are obvi- Avoiding the plethora of technical terms that ous and accord with the broad biogeographical have been applied to subsurface waters, patterns postulated by Holsinger (1994a) for all included are freshwater streams and lakes in subterranean amphipods and perhaps other inland caves in calcareous karst, coastal anchial- malacostracans. These patterns are: ine caves containing marine or brackish water, 1 that shown by stygobionts derived from old springs, mud or plant detritus on the bottom of freshwater ancestors (limnostygobionts); surface waters which are in obvious continuity 2. that shown by stygobionts derived from with the water table in unconsolidated substrata, marine ancestors, and and interstitial (hyporheic) water associated 3. that shown by stygobionts inhabiting coastal with streams. The collection of material from waters with marine affinities and clearly such a diversity of habitats itself demands diver- derived from closely allied marine ancestors sity. For example, cave forms have been col- (thalassostygobionts or 'crawl-outs'). lected from open water by sweep nets or by The process involved in pattern 3 is often baiting, forms in interstitial waters by pumping, referred to as 'stranding'. Crangonyctoid species and spring species by placing nets over surface clearly exhibit pattern 1, hadzioid species, pat- outlets for extended periods (collections of tern 2, and Liagoceradocus species, pattern 3. Brachina invasa were made by placing a collect- Other Australian stygobionts are less easily ing net over the outlet of a spring for 12 hr). assigned to a particular pattern, but Pseudo- moera fontana at least, given its marine taxo- The diversity of the hypogean amphipod fauna nomic affinities and despite its entirely fresh- water distribution, would appear exhibit to On the basis of described species alone (Table 1 ), pattern 3. Fig. 2 indicates how close the corre- it is obvious that significant diversity exists lation between distribution of stygobiont amongst amphipods found in subsurface waters amphipods derived from hadziid ancestors is in Australia. How much more diverse will this with areas of marine transgression and, con- fauna prove to be when further investigations versely, of those with crangonyctoid ancestors have taken place? We have reason to believe that and areas not inundated before or during the the answer is that it will prove to be substantially Cretaceous. more diverse. This response is based in part on AMPHIF'OD DIVERSITY IN UNDERGROUND WATERS IN AUSTRALIA 517 our possession of further undescribed material troglophiles but these do exhibit some troglo- from underground waters and including at least morphic features. Various species of Antipodeus three new species from Western Australia, two provide examples. The third step includes tro- from Queensland, and three from New South globites with clear troglomorphy. Hurleya kala- Wales (see also Eberhard et al., 1991). We mundae, Nedsia species, and Protocrangonyx believe it doubtful, however, that the number of fbntinalis are some examples. species of hypogean amphipodsin Australia will Of much greater interest are those factors ever reach the numbers found in the two most responsible for the high diversity. In this

diverse regions of the world in so far as this connection it is instructive to determine those

group is concerned, that is, the central-southern features held in common by the two regions of European — Mediterranean region and the east- greatest stygobiont amphipod diversity, the ern and southern North American — West central-southern European — circum Mediter-

Indian region. Even so, it is already clear that ranean region and the eastern and southern our increased knowledge of the diversity of North American — West Indian region. In both hypogean amphipods in Australia confirms, as regions, the following features are both held in in indicated, Holsinger's ( 1 993) view that southern common and regarded as significant Australia is a region of significant diversity for promoting the development of high diversity this group. However, unlike the genera:species (Holsinger, 1994a): a former proximity to the ratios found in the two regions of highest diver- Tethys Sea, the lack of extensive glaciation dur- sity mentioned, where the usual pattern is one of ing the Pleistocene, large areas of karst, and many species per crangonyctoid and few widespread marine transgressions in the late species per hadzioid genus, the pattern in Aus- Mesozoic and Cainozoic. To a not inconsider- tralia appears to be different, with many species able degree, thesefeatures also characterise large per genus an obvious pattern for at least some parts of the Australian continent, Over much of hadzioid genera, and few species per genus for the Mesozoic, the Tethys Sea lay west of Aus- most crangonyctoid genera. tralia; apart from the highlands ofTasmania and small areas of the highest mountains in the south-east of the mainland, the Australian con- The causes of diversity tinent was free of ice during the Pleistocene; and Two issues are involved in considering this mat- marine transgressions covered large areas of the ter. First, the factors that have led to the evol- Australian continent during the early Cre- ution of styobiont amphipods in Australia, and taceous (Fig. 2). The only difference, and one of second, those factors responsible for the high degree not kind, is the extent of karst in Aus- diversity. tralia. Karst does occur widely in Australia (Jen- continuously The first set of factors are of relatively little nings, 1985; Mathews, 1985), but interest in the present context; it may be pre- extensive areas are confined to the Nullabor sumed that the evolutionary routes followed by Plain and the lower Murray Valley, with only stygobiont amphipods in Australia are similar to relatively minor occurrences elsewhere those followed elsewhere by such organisms. (included here is the Fitzroy Basin of Western Plain, Jenolan and Wee Thus, all originated from surface forms by Australia, the Cooleman regressive evolution — irrespective of whether Jasper areas of New South Wales, the Buchan selection, the accumulation of neutral caves area of Victoria, the Mole Creek area of mutations, or genetic drift was the more import- northern Tasmania, and the Barkly Basin of ant in this process (Culver, 1982) — after iso- Queensland). depend lation from surface forms had occurred follow- The evolution of stygobionts does not karst, but there is ing sea-level change, the onset of climatic entirely upon the presence of their evolution aridity, or a given geomorphological event. A little doubt that it does promote number of evolutionary steps have been pro- and the development of diversity. In any event, posed through which populations pass as stygo- we believe that the features listed above, includ- biont species evolve. As a general rule, three ing the occurrence of karst — albeit it to an in Europe broad ones can be recognized to accommodate extent more limited than the southern North American West the evolution of stygobionts from both inland — Mediterranean and — and marine ancestors (Holsinger, 1994a). The Indian regions — have been important in pro- if ducing the observed diversity of the Australian first is inclusive of troglophiles with few any troglomorphic features. Neoniphargus obrieni stygobiont amphipod fauna. Also important, we provides an example. The second also include believe, has been both: 518 J.H. BRADBURY AND WD. WILLIAMS

1. continental drift during which Australia first Bradbury. J.H., and Williams, W.D., 1996a. Fresh- broke free from Gondwana and then passed water amphipods from Barrow Island, Western Australia. Records the Australian Museum 48: through a series of quite distinct climatic of 33-74 zones during the Cainozoic, and Bradbury J.H. and Williams, W.D., 1996b. Two new 2. palaeoclimaticfluctuations including periods species of anchialine amphipods (Crustacea, allied of aridity which, in conjunction with Hadziidae, Liagoceradocus) from Barrow Island, sea-level changes for coastal populations, Western Australia. Records of the Western would have served to isolate surface and sub- Australian Museum 17(4) in press. surface populations of a species and have led Comin, F. and Williams, W.D., 1994. Parched conti- to the development of discrete drainage nents: our common future? Pp 473-527 in: basins. Margalef, R. (ed.), Limnology now; a paradigm of A succession of favourable (wetter and colder) planetary problems. Elsevier: Amsterdam. Culver, D.C., 1982. Cave life. Evolution and ecology. and unfavourable (drier and warmer) climates Harvard University Press: Cambridge, Mass. could easily have provided mechanisms promot- Eberhard, S.M., Richardson, A.M.M. and Swain, R., ing stygobiont speciation as epigean populations 1991. The invertebrate cave fauna of Tasmania. were driven to seek subterranean refugia. It may Department of Zoology, University of Tasmania: also be that some troglomorphic forms (lacking Hobart. eyes) now found in surface waters actually Frey, D.G., 1991. A new genus of alonine chydorid represent the return to epigean conditions of cladocerans from athalassic saline waters of New hypogean forms in the absence of surface com- South Wales, Australia. Hydrobiologia 224: 11- petitors, the latter having become extinct during 48. Holsinger, J.R., 1991. What can vicariance biogeo- former unfavourable conditions. It is not poss- graphic models tell us about the distributional ible, for eyes, once lost, to be regained. history of subterranean amphipods? Hydrobio- Finally, some explanation should be offered logia 223: 43-45. for the extraordinary diversity of stygobionts on Holsinger, J.R., 1993. Biodiversity of subterranean Barrow Island. The most likely one is that after amphipod crustaceans: global patterns and zoo- stranding, ancestral populations were isolated in geographic implications. Journal of Natural a series of small and discrete subterranean History 27: 821-835 basins where genetic drift led to the evolution of Holsinger, J.R., 1 994a. Pattern and process in the bio- separate species from the original founder geography of subterranean amphipods. Hydrobio- population. logia 287: 131-145. Holsinger, J.R., 1994b. Amphipoda. Pp. 147-163 in: Juberthie, C. and Decou. V.(eds), Encyclopaedia

Acknowledgments Biospeologica 1 : Societe de Biospeologie. Humphreys, W.F., 1995. Limestone of the east Kim- Many specimens examined were made available berly, Western Australia — karst and cave fauna. by Dr W.F.Humphreys of the Western Aus- Report to the Australian Heritage Commission tralian Museum and by Mr S.M. Eberhard and to the Western Australian Heritage Com- whose particular devotion to the rigorous collec- mittee. 190+ xix.pp. Unpublished.

Jennings, J.N. , Karst tion of cave fauna deserves special recognition. 1985. geomorphology. Blackwcll: Oxford. We thank them. The work has been supported by Knott, B.. 1983. Amphipods from Nurina Cave — a grant from the Australian Biological Resources Nullabor Plain. Australian Speleological Study. Federation Newsletter 101: 3-4. Knott, B., 1985. Australian aquatic cavernicolous amphipods. Paper presented to the 1 5th biennial References conference. Australian Speleological Federation, Barnard. J.L.. and Williams. W.D.. 1995. The tax- Hobart. 1 1 pp. onomy of Amphipoda (Crustacea) from Aus- Mathews, P.G. (ed.), 1985. Australian karst index. tralian fresh waters. Part 2, Records of the Aus- Australian Speleological Federation Inc.: tralian Museum 47(2): 161-201. Melbourne. Barr, T.C., and Holsinger, J.R., 1985. Speciation in Paine. A.G.L. (ed.), 1990. Australia. Evolution of a cave faunas. Annual Review of Ecology and continent. Australian Government Publishing Systematics 16: 313-337. Service: Canberra. Bradbury, J.H., and Williams, W.D., 1995. A new Timms. B.V., 1993. Saline lakes of the Paroo, inland genus and species of erangonyctoid amphipod. New South Wales, Australia. Hydrobiologia 267: (Crustacea) from Western Australian fresh 269-289. waters. Transactions of the Royal Society ofSouth Williams, W.D., 1964. Subterranean freshwater Australia 119(2): 67-74. prawns in Australia (Crustacea: Decapoda: AMPHIPOD DIVERSITY IN UNDERGROUND WATERS IN AUSTRALIA 519

Atyidae). Australian Journal of Marine and Williams, W.D. and Barnard, J.L., 1988. The tax- Freshwater Research 15(1): 93-106. onomy of crangonyctoid Amphipoda (Crustacea) Williams, W.D., 1986. Amphipoda on land masses from Australian fresh waters: foundation studies, derived from Gondwana. Pp. 551-559 in: Boto- Records of the Australian Museum, Supplement saneanu, L. (ed.), Stygofauna Mundi. Brill and 10: 1-180. Backhuys: Leiden.