Bijdragen tot de Dierkunde, 60 (3/4) 145-150 (1990)

SPB Academie Publishingbv, The Hague

Aspects of the evolution and biogeography of stygobiontic

(Crustacea: )

Johann-Wolfgang Wägele

Fachbereich 7, Universität Oldenburg, D-2900 Oldenburg, W. Germany

Keywords: Crustacea, Isopoda, evolution, stygofauna, biogeography

Abstract Introduction

The the and The evolution of the stygobiontic isopods is discussed corre- increasing knowledge on

lating the phylogenetic with biogeography. All stygobi- system distribution of stygobiontic isopods allows some

ontic isopods probably are derived from remote marine ances- general observations on their phylogeny and bio- tors. The colonization of subterranean aquatic biotopes geography. The "Amsterdam Expeditions to the occurred in two ways: (1)via the coastal groundwaterin the case West Indian Islands" and other expeditions of the of the Microparasellidae, Gnathostenetroididae, Stenetriidae,

and in Cyathura (Stygocyathura), (2) in most families, however, group of Prof. Dr. Jan H. Stock proved that many

via epigean freshwater ancestors. Ancient freshwater isopods hypogean genera have a wide distribution, not only

that must have existed before the Cretaceous and whose already in the both sides peri-Caribbean area, but also on stygobiontic phylogenetic lines partly must have existed before of the Atlantic, some even reaching into the Indo- the opening of the Atlantic are the Aselloidea, Calabozoida, Pacific Botosaneanu et 1986; Botosanea- Phreatoicidea, and probably also the Protojaniridae. In the (e.g. al.,

course of Cretaceous and Tertiary regressions other, more apo- nu, 1987; Notenboom, 1984; Stock, 1977; 1985).

morphic taxa “stranded” and adapted to stygobionticbiotopes, These stygobionts are of high scientific interest, as

such as the “Monolistrini” (). some of them obviously are relicts, without close

relatives in marine biotas (e.g. Calabozoa, Curas-

Zusammenfassung santhura), stimulating research and speculation be-

cause of their distribution and phylogenetic age. Die Evolution der stygobiontischen Isopoden wird in einem Ver- Evolutionand biogeography cannot be separated in gleich des phylogenetischen Systems mit der geographischen any effort to understand the origin of the aquatic Verbreitung der Taxa diskutiert. Alle stygobionte Isopoden

haben wahrscheinlich marine Vorfahren gehabt. Die Besiedlung hypogean species.

limnischer,unterirdischer Biotopeerfolgt auf zwei Wegen: Über

das Küstengrundwasser im Fall der Microparaselliden, Gna-

thostenetroididae, Stenetriidae, und bei Cyathura (Stygo- Monophyly and biogeography cyathura), bei den meisten Familien jedoch über epigäische

Süßwasserformen. Alte Süßwasserisopoden, die schon vor der

Kreide gelebt haben müssen und deren hypogäische Linien z.T. A summary of hitherto accumulated knowledge on schon zum Zeitpunkt der Öffnung des Atlantiks existierten, sind the evolution of the has been Isopoda recently pre- die Aselloidea, Calabozoida,Phreatoicidea und wahrscheinlich pared (Wägele, 1989). A simplified scheme of the auch die Protojaniridae.Im Verlauf von Regressionen während results all those taxa and containing groups of Kreide und Tertiär sind andere, “modernere” Taxa “gestran- that is in 1. det” und ins Süßwasser und Grundwasser gelangt, wie die genera are stygobiontic represented Fig.

“Monolistrini” (Sphaeromatidae). Aquatic hypogean biotopes were conquered several 146 J.-W. Wagele - Aspects of the evolution and biogeography of stygobiontic Isopoda

Fig. 1. Dendrogramfor the phylogenetic system of the Isopoda (after Wägele, 1989), representing the taxa that belong to the stygofauna.

Note that most groups evolved via epigean freshwater ancestors. Question marks indicate that it is not known if such epigean ancestors could have existed. Black circles without names represent single taxa or groups of taxa.

if took times by members of nearly all isopod suborders, expected or several parallel invasions place with the of Oniscidea within In the first exception the (which have a genus or a family. case a genus some cave-dwelling species) and the Valvifera. occurring for example at both sides of the Atlantic

Nearly always some marine sister-group is known must have a common stygobiont ancestor and be at and there is no doubt about the marine origin of least as old as the central AtlanticOcean. In the sec-

ond of marine most families. To understand the mechanisms lead- case populations a ancestor species

it is find of wide distribution could in ing to present-day distribution necessary to adapt independently out whether within a phylogenetic line crossing the remote areas to the coastal or estuarine interstitial border marine benthos/aquatic stygofauna only a or other hypogean biotas. Monophyly of the adapt-

vicari- single event (adaptation to hypogean biotas) is to be ed group of species can be an indication of Bijdragen tot de Dierkunde 60 (3/4) - 1990 147

continental other mechanisms known how the of this are related anee by drift, being not genera family

less probable. to each other; some may belong to monophyletic

subterranean groups. Neither is known, if hypo-

Eurasia have Phreatoicidea gean species of North America and a

common stygobiontic ancestor.

The Phreatoicidea is the oldest known isopod The remaining families of the aselloid line

suborder (300 million years: Schram, 1970). Pres- evolved in a different way: arising from an

line ent-day species live exclusively in fresh water of unknown common aselloid ancestor this

Gondwana fragments (New Zealand, Australia, evolved completely in subterranean fresh water.

Tasmania, India, South Africa). The Nichollsidae, The Stenasellidaestill have the size of epigean asel-

a subterranean family known only from India, lids and have a wide distribution in southern Eu-

most probably evolved on this subcontinent in- rope, Africa, Central America, and Asia (summary

in The last ancestor dependently of other subterranean groups. Other Henry et al., 1986). common

have lived in Laurasia and will not closely related hypogean species are known for must descendents

have this continent before the forma- the Amphisopidae (Hypsimetopinae), obviously spread over

representing several separate invasions of the un- tion of the Atlantic. Gondwana was probably also

less derived of the sister- derground (Knott, 1986); the species in question oc- populated. The species

dwarfish Atlantasellidae and Microcer- cur in Australia and Tasmania. In the third family group, the

in southern Africa (Phreatoicidae) hypogean species are known from beridae, occur partly (Protocer-

Bermuda New Zealand and Tasmania. The Nichollsidae are berus, Afrocerberus), partly on (Atlan-

the only monophyletic hypogean family; the tasellus). Likewise, this line of dwarfish forms was

in existence before the Atlantic phylogeny of the other hypogean groupsof species already was

is not known. formed. Atlantasellus has an intermediate mor-

phology between stenasellids and microcerberids,

Calabozoida sharing some synapomorphies with the microcer-

berids (Wägele, 1983), suggesting that some con-

According to Wägele (1989) the Calabozoida are nection between the present-day Bermuda Island the sister-group of the Asellota, the close relation- and older continental fragments must have existed.

ship having been noted already by Van Lieshout While the most primitive Microcerberidae live in

is for (1983). Only one species known (from Venezue- fresh water, the more apomorphic species occur

la): Calabozoa pellucida (Van Lieshout, 1983). It the most part in the brackish or marine coastal seems to be a relict; no close marine relatives are mesopsammal. They must have means for dispersal

have found known. over ocean basins, as they been e.g. on

the Maldives and Laccadives, and on many Carib-

Asellota bean islands (summary in Coineau, 1986a). Some

freshwater species with the more apomorphic

be of marine Most species of asellotes are marine. The more "coastal" morphology may aproduct

familes live in shallow coastal while Mexicerberus primitive areas, regressions (e.g. troglodytes Schultz, a large number of specialized genera and families 1979, Microcerberus plesai Chappuis & Delamare, radiated in the deep-sea. A separate phylogenetic 1958, and M. remyi Chappuis, 1954). line evolved in fresh water, namely the Aselloidea. Further stygobiontic species are known in those

Withinthis line the less specialized family Asellidae of the remaining asellote families, which probably has epigean as well as hypogean species. It is very evolved in shallow marine habitats. Interestingly,

line obvious that hypogean species of this family the more primitive genera in the janiroid (Wil- evolved not have to interstitialconditions very often in independent, closely re- son, 1987) an affinity lated groups. In Asellus aquaticus (Linné, 1758) (Caecostenetroides, Neostenetroides, Anneckella, epigean as well as hypogean populations exist. It is Enckella, Protojanira). Species of these genera are 148 J.-W. Wdgele - Aspects of the evolution and biogeography of stygobiontic Isopoda

rare and must be survivors derived from ancient tions that "stranded" during Miocene regression.

stocks which were displaced by the more advanced The Australian freshwater species ofAngeliera is of

Stock Janiroidea. Africa (Gondwana) and the areas adja- enigmatic origin (Stock, 1985); suggests that

be the where could have stranded late Ter- cent to the Tethys Sea seem to regions, populations during

Gnathostenetroidoidea in Australia. The these genera radiated. The tiary uplift Microparasellidae

have oculatedand blind species; they evolved in the then could have been a coastal interstitial family

marine interstitial. The Protojaniroidea are exclu- widely distributed in the Cretaceous Tethys, of

which sively freshwater stygobionts (Sket, 1982; Henry et single populations stranded during regres-

al., 1986). This superfamily is morphologically in- sions and evolved to inland species.

termediate between the Gnathostenetroidoideaand

the higher evolved Janiroidea/Pseudojaniroidea Anthuridea

(Wilson, 1987; Wägele, 1989). The distribution

(South Africa, Sri Lanka) suggests that the Pro- The Anthuridea are worm-like marine isopods,

rather old than 130 shelf tojaniroidea are (more My?) mostly living on the of warmer seas. Only

and of Gondwana three have The origin. genera stygobiontic species. subge-

Within the Janiroidea the less derived, non- nus Cyathura (Stygocyathura) evolved frommarine

monophyletic "family" Janiridae contains several ancestors, adapting to the coastal mesopsammal

lines of marine origin which most probably radiat- and to brackish and fresh water (Wägele et al.,

ed independent of each other in fresh water. The 1987). The wide Tethys distribution, ranging from genera Heterias, Protocharon, and Mackinia are the Caribbean to Borneo, New Caledonia, and closely related; only Mackinia is subterranean, Melanesia, suggests a radiation and speciation on

known from East Asia and Japan (summary in the shores of the former Tethys Sea. Their absence

Coineau, 1986b). A second group, for which the in the peri-Mediterranean area and occurrence on

in phylogenetic system is not known detail, con- Easter Island and Pitcairn (Botosaneanu, 1987) are tains the genera Microjanira, Caecianiropsis, and enigmatic. Parallel evolutionin the development of

Microjaera. These are coastal mesopsammic, with- the "interstitial habitus" in different populations is out major speciation and dispersion. not very probable because of the nearly identical

"Monophyly or polyphyly?" is the question not morphology of the species, which indicates mono-

solved in of definitely the case the Microparaselli- phyly. Species of Curassanthura, the most primi- dae All (Wägele, 1989). genera are represented by tive of the stinging-sucking paranthurids, obviously interstitial coastal in relicts species, mostly mesopsammic are (Wägele, 1985; Wägele & Brandt, 1985).

Angeliera, Paracharon, partly in Microcharon, They are only known from the Caribbeanand from while Microparasellus has been found in caves and the Canary Islands; the amphi-Atlantic distribution wells (eastern Europe and Lebanon). The phyloge- suggests for the genus an age of at least 50 My. netic of not relationships the species are known. Cruregens is an endemic monotypic genus of New

The coastal could have mesopsammic groups Zealand, occurring on the Southern and on the evolved and spread similarly to Microcerberus, as Northern Island; it evolved from specialized tropi- many populations occur in marine or brackish cal shallow-water ancestors (sister-group: Colan- water (Coineau, 1986b). In the case of Microcha- thura, Califanthura) (Wägele, 1982, 1989).

known from marine coastal ron, a genus waters and from fresh water in Europe, Mediterraneanislands, Sphaeromatidea

North Africa, Iran, Russia, Polynesia, New

Caledonia, and Bonaire, it is not known whether its The suborder Sphaeromatidea is composed for the

is in fresh in origin water or the marine interstitial. most part of exclusively marine families (Wägele,

Stock (1977) has shown that most localities lie near 1989). Only within the Sphaeromatidae some the Oligocene shore-lines of the Tethys Sea. Inland genera are adapted to tolerate brackish and even

therefore be of fresh in species might offsprings popula- water. Hypogean species are only present - 149 Bijdragen tot de Dierkunde 60 (3/4) 1990

in those areas of A model, as the "active colonization specialized genera occurring history. single

Rouch southern Europe, which had been covered by the model" of & Danielopol (1987) can not ex-

northern all such the of sea during Tertiary periods (Yugoslavia, plain known phenomena, as presence

in All relict of local of Italy, southernFrance; summary Sket, 1986). primitive taxa, "stranding", a

radiation within these genera (, Caecosphaeroma, large a stygobiontic monophylum.

related and In main can be discerned: Microlistra) are closely (Wägele, 1989) isopods two processes (1)

in fresh followed possibly evolved from an ancestor species that preadaptation epigean water, by

karst into tolerated brackish or fresh water and "stranded" penetration into systems (caves etc.), or

during regressions. phreatic or hyporheic habitats, and (2) colonization

via the coastal mesopsammal. The latter case can be

Cymothoida observed in Cyathura (Stygocyathura) and in the

families Gnathostenetroididae, Stenetriidae, Mi-

In the suborder Cymothoida only the family croparasellidae, and possibly in some Cirolanidae.

direct freshwater Cirolanidae has stygobiontic species. A first survey But most generaseem to have an-

be found: of the phylogeny on generic level (Wägele, 1989) cestors. Here two different groups can

has shown that at least two monophyletic lines and (a) Old freshwater groups, whose transition from

further single species invaded the hypogean world. marine to inland waters probably happened before

Phreatoi- In some epigean genera (Annina, Anopsilana) the Cretaceous; to this group belong the

also the Calabozoida with an affinity to fresh water, hypogean species cidea, the Aselloidea, possibly

and These are found (summary in Botosaneanu et al., 1986). Protojaniroidea. isopods are more prim-

of Bahalana, itive than in the remaining subord- A large group genera (including representatives

coastal Arubolana, Antrolana, Typhlocirolana, Skotobae- ers. It is interesting that the mesopsammal

inland na, etc.) is a monophyletic group of stygobionts, was also conquered by an group (Microcer-

localities in the distributedover several Caribbean, beridae) (see Wägele, 1983).

Mexico, Texas, and Virginia in the West, and in (b) Groups of freshwater genera, originating from

North Africa, Somalia, Ethiopia, and peri-Medi- Cretaceous/Tertiary ancestors that "stranded"

viz. "Monolistrini"and cirola- terranean areas in the East. This points to a during regressions,

of the “Bahalana” Tethyan origin of these genera. It even seems that nids, especially amphi-Atlantic subgroups of hypogean genera already existed be- group and related genera.

fore the opening of the Atlantic: the western genera Local (regional) speciation of the stygobiontic

took all times and is considered in Antrolana, Mexilana, and Cirolanidesare probably taxa place at not

this related with the eastern genera Typhlocirolana and paper.

Turcolana; the western genus Sphaerolana may be a close relative of the eastern Faucheria and

Skotobaena. All these genera belong to the same References monophylum (group E of the Cirolanidae in

A second related Han- 1987. A Wägele, 1989). line, to Botosaneanu, L., new thalassostygobiont species of

(Isopoda: Anthuridea) from the South-East Pacif- senolana and Anopsilana, is known from the Cyathura ic. Stygologia, 3: 296-304. is im- Caribbean (Creaseriella, Haptolana). It very Botosaneanu, L., N. Bruce & J. Notenboom, 1986. Isopoda: probable that within these monophyletic groups Cirolanidae. In: L. Botosaneanu (ed.), Stygofauna mundi: evolved of each stygobiontic species independently 412-422 (Brill-Backhuys, Leiden). other in localities of the Old and the New World. Coineau, N., 1986a. Isopoda: Microcerberidae. In: L. Boto-

saneanu (ed.), Stygofauna mundi: 473-479 (Brill-Backhuys,

Leiden).

Conclusions Henry, J.-P., J.J. Lewis & G. Magniez, 1986. Isopoda: Asello-

ta: Aselloidea, Gnathostenetroidoidea, Stenetrioidea. In: L. The colonizationof the subterraneanenvironment Botosaneanu (ed.), Stygofauna mundi: 434-464 (Brill- is different very complex, as every single case has a Backhuys, Leiden). 150 J.-W. Wagele - Aspects of the evolution and biogeography of stygobiontic Isopoda

In: L. Botosaneanu Knott, B., 1986. Isopoda: Phreatoicidea. marks on their morphology and adaptations. Bijdr. Dierk.,

(ed.), Stygofaunamundi: 486-492 (Brill-Backhuys, Leiden). 52: 49-59.

Lieshout, S.E.N, van, 1983. Calabozoidea, a new suborder of Wägele, J.W., 1983. On the origin of the Microcerberidae

stygobiont Isopoda, discovered in Venezuela. Bijdr. Dierk., (Crustacea: Isopoda). Z. zool. Syst. Evolut. -forsch., 21:

53: 165-177. 249-262.

Notenboom, J., 1984. Arubolana parvioculata n. sp. (Isopoda, Wägele, J.W., 1985. On the tethyan originof the stygobiont An-

Cirolanidae) from the interstitial of an intermittent river in thuridea Curassanthura and Cyathura (Stygocyathura), with

Jamaica, with notes onA. imula Botosaneanu & Stock and A. description of Curassanthura canariensis n. sp. from Lan-

aruboides (Bowman & Iliffe). Bijdr. Dierk., 54: 51—65. zarote (Crustacea, Isopoda). Stygologia, 1: 258-269.

Rouch, R. & D.L. Danielopol, 1987. L'origine de la faune aqua- Wägele, J.W., 1989. Evolution und phylogenetisches System der

tique souterraine, entre le paradigme du refuge et le modèle Isopoda. Stand der Forschung und neue Erkenntnisse.

de la colonisation active. Stygologia, 3(4): 345-372. Zoologica (Stuttgart), 140: 1-262.

Schram, F.R., 1970. Isopod from the Pennsylvanian ofIllinois. Wägele, J.W. & A. Brandt, 1985. New West Atlantic localities

Science, 169: 854-855. for the stygobiont paranthurid Curassanthura (Crustacea,

Sket, B., 1982. New Protojaniridae(Isopoda, Asellota) from Sri Isopoda, Anthuridea) with description of Curassanthura ber-

Lanka and some corrections of the of the mudensis 55: 324-330. taxonomy family. n. sp. Bijdr. Dierk.,

Biol. Vestnik, 39: 127-142. Wägele, J.W., O. Coleman & U. Hosse, 1987. Two new

Sket, B., 1986. Isopoda: Sphaeromatidae. In: L. Botosaneanu hypogean species of Cyathura from Melanesia (Crustacea:

(ed.), Stygofaunamundi: 423-427 (Brill-Backhuys, Leiden). Isopoda: Anthuridea): further Tethyan relicts? Stygologia, 3:

Stock, J.H., 1977. Microparasellidae (Isopoda: Asellota) from 89-106.

Bonaire, with notes on the origin ofthe family. Stud. Fauna Wilson, G.D.F., 1987. The road to the Janiroidea: comparative

Curaçao, 51: 69-91. morphology and evolution of the asellote isopod .

Stock, J.H., 1985. Discovery ofinterstitial Isopoda ofthe fami- Z. zool. Syst. Evolut.-forsch., 25: 257-280.

ly Microparasellidae in inland waters of Australia. Stygolo-

gia, 1: 93-100.

Wägele, J.W., 1982. The hypogean Paranthuridae Cruregens Received: 12 October 1989

and Curassanthura Kensley (Crustacea, Isopoda), with re- Revised: 25 July 1990