Contributions to Zoology. 71 (4) 147-158 (2002)

SPB Academic Publishing bv, The Hague

Oligochaetes from underground waters of Oman with descriptions of two new of Antarctodrilus arabicus n. and species (): sp.

Phreodrilus stocki n. sp.

Stygofauna of Oman, 7*

¹, ³ Martínez-Ansemil Narcisse Giani ² & Beatrice Enrique ¹, Sambugar

1 Bioloxia Bioloxia Departamento de , Vexetal e Ecoloxia, Facultade de Ciencias, Universidade da

2 Coruna, Campus da Zapateira s/n, E-15071 A Coruna, Spain, [email protected]; Centre d’Ecologie des

Systemes Aquatiques Continentaux, UMR C5576 CNRS, Universite Paul Sabatier, 118 route de Narhonne,

3 F-31062 Toulouse Cedex, France, [email protected]; Museo Civico di Storia Naturale, Lungadige Porta

Vittoria 9, 1-37126 Verona, Italy, [email protected]

Keywords: Groundwater oligochaetes, Phreodrilidae, new species, Oman, biogeography

Abstract driloidinae), previously known from Puerto Rico and Belize in

the Atlantic western Ocean, represents a large extension ofits

known distribution area. The study oftwenty-nineoligochaete samples collected in 1996 by J. H. Stock and J. J. Vermeulen (University ofAmsterdam), in the of allowed draw in- Sultanate Oman, us to up an initial

of the Arabian ventory of the freshwater oligochaete fauna pe- Contents ninsula, a fauna totally unknown until now. The 147 specimens examined belong to nine species offour families: Phreodrilidae, Introduction 147 , Tubificidae and Enchytraeidae. The Phreodrilidae(2 Material and methods 148 whilst species) represent more than half ofthe total specimens; Systematic account 148 the rest belong mainly to the Naididae. Faunistic remarks 155 arabicus Two new species ofPhreodrilidae(Antarctodrilus Acknowledgements 157 described. Both n. sp. and Phreodrilus stocki n. sp.) are belong References to 157 the subfamily Phreodrilinae,untilnow not reported from north ofthe tropic ofCapricorn. Otheridentifiedspecies include Dero

Allonais and Doliodrilus (Dero) zeylanica, paraguayensis puer-

recorded subterranean toricensis, which are for the first time in Introduction habitats.

the of the of These studies confirm hypothesis presence Marine oligochaetes of the Arabian Gulf have been Phreodrilidae in the Arabian peninsula as relict taxa inhabiting studied refuges in hyporheic/groundwater habitats. by Erseus( 1985, 1986a, 1986b, 1988, 1989)

marine The of an fauna with phyletic presence oligochaete but the freshwater oligochaete fauna of the Ara- affinities in underground waters already highlighted in Europe bian peninsula was totally unknown until now. We now equally applies to the Arabian peninsula with the discov- had the of of the tubificid and in the opportunity studying twenty-nine oligo- ery genera Doliodrilus chaete from underground habitats ofOman. As these genera already are well samples this part of the world forwarded known from littoral marine or brackish water with a wide the to one of us (BS) by R. Vonk of the University of range of salinity, we have additional evidence that the migra- Amsterdam. The material was collected by J. H. tion of interstitialmarine meiobenthic tubificid species through Stock and J. J. Vermeulen of the of water of be the University decreasing salinity may a way of colonising subterranean freshwaters. Amsterdam in 1996, during an expedition in the

The Doliodrilus arid present record of puertoricensis (Limno- Sultanate of Oman, an country situated along

Stygofauna Oman 7. issue, nr. is published & in Muss. Nat. of nr. The previous 6, by Ruffo Holsinger Boll. Civ. Stor. Verona -

Botanica, Zoologia, vol. 27 (2003)

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- The the south-eastern margin of the Arabian peninsula. Remarks. branchial fossa displays one pair

They sampled several different subterranean habi- of parallel palps and three pairs of gills. The meas-

tats in which oligochaetes were found. The habi- urements for the anterior ventral setae are 50-70

the tats include the interstitial coarse sediments of dry pm, for posterior ventral setae 44-60 pm, for

beds and the needle 34-48 and for the hair stream (wadis), wells, springs, one cave. setae pm setae

This paper presents the results of the identifica- 120-180pm. These setal lengths are within the range

tion of this material including the description of recorded for African (Grimm, 1987) and Caribbean

two new species of Phreodrilidae, a family largely specimens (Dumnicka, 1986a; Chagne & Giani,

distributed in the southern and but lie the lower end of The hemisphere reported 1998), they at range.

twice from the northern from Sri Lanka 1914 only one: Dero (A.) africana Michaelsen, has much larger

intermedi- (Stephenson, 1913) and Morocco (Giani et al., 1995). setae (Grimm, 1985). The presence of

ate teeth in the needle setae was noted in the new

material, a feature already reported for Dero (Aulo- Material and methods phorus) furcata (Sambugar, 1986; Grimm, 1987).

The specimens were collected in wells using a Cvetkov closing

Distribution and habitat. - Known vertical in the of and the Cosmopolitan. net, and hyporheon wadis, springs to inhabit lentic and lotic habitats of surface ofthe Bou-Rouch from the wa- cave by means pump. Samples cave

with in the As and some springs were collected in superficial waters a ters, mainly intertropical region. regards

handnet. subterraneanwaters it was previously foundin wells labora- The formalin preserved samples were sorted in the of West Indian Islands (Dumnicka, 1986a) and in tory under a dissecting microscope andtransferred to 70 % etha- Morocco (Giani, unpublished data). nol. In the field, some physical-chemical parameters were directly

the electrical in mS/ measured, e.g., conductivity (eC pS/cm or

cm) and the water temperature.

The geographical position of the sampling stations is given Dero (Dero) zeylanica Stephenson, 1913 by UTM coordinates. Every site has its code in relation to a

station list provided by the University of Amsterdam.

Examined material. - Eight immature specimens from a well at All specimens were mounted in Canada balsam, most ofthem Dibab (96/23), UTM 0700988/2553839,eC 400 pS/cm, 25 March as whole mounted worms. Mature specimens were previously 1996,Legit: J. H. Stock. stained with Harris haematoxylin and some were dissected un-

der a stereo-microscope. Drawings were made by means ofa

- in camera lucida. Remarks. The material collected Oman is mor-

of is stored in the The type material the new species collec- phologically in accordance with the literature data tions of the Zoological Museum of Amsterdam (ZMA). Other (Sperber, 1948; Brinkhurst & Jamieson, 1971). reference specimens are in the authors’ own collections.

Distribution and habitat. - Previously known only

from Southern India and Sri Lanka. Not Systematic account previously

found in subterranean waters.

Family: NAID1DAE

Subfamily: Naidinae Allonais Dero (Aulophorus) furcata (Muller, 1773) paraguayensis (Michaelsen, 1905)

Examined material.-Twelveimmaturespecimens: 1 from inter- Examined material. - Thirty-five immaturespecimens, all col-

stitial waters of a spring formed in 1995 in Bait Qura lected by J.H. Stock: 10 from a well at Majaz Al Sugra (96/65), Rustaq, (96/69), UTM 0443405/2587376,eC 818 pS/cm, I April 1996, onplantation, UTM 0483567/2679077,eC 1004 pS/cm, 30 March

J. H. Stock; 3 from a well in South Dahariz UTM 1996; 2 from interstitial waters of a spring formed in 1995 in Legit: (96/99),

Rustaq, Bait Qura (96/69), UTM 0443405/2587376,eC 818 pS/ 0196965/1883319,eC 4210 pS/cm, 5 April 1996, Legit: ,1. H.

1996; from 0254392/ Stock; 1 from a well in the A’Muotazah area (Salalah cm, 1 April 5 a well at Marbat (96/84), UTM Centre) (96/100),UTM 189032/1882511,eC3490 5 1996, 1879929, eC 2.35 pS/cm, 4 April 1996; 1 from a well at Dahariz pS/cm, April

South (96/99), UTM 0196965/1883319,eC 4210 pS/cm, 5 April Legit: J. H. Stock; 3 from surface waters of the spring head of

Wadi Darbat catchment 1996; 17 from a well at Auwqad South (96/101), UTM 0184857/ the (96/103), UTM 0230717/1897256,

1881731, eC 4010 pS/cm, 5 April 1996. eC 754 pS/cm, 5 April 1996, Legit: J. H, Stock; 2 from surface

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waters ofthe Ain Hamran spring (Salah UTM region) (96/106), lip associated with circular muscle. Cutaneous glands 0210592/1892363, eC 576 gS/cm, 6 April 1996, Legit: J. H. in more or less arranged parallel rows, particularly Stock; 2 from the interstitial waters ofWadi Nakhal (96/126), setal each numerous at level of segment. Clitellum UTM 0584918/2592170, eC 1210 pS/cm, 9 April 1996, Legit: XII-X1II J. J. Vermeulen. extending over with glandular cells ar-

in ranged more or less parallel rows.

- Ventral from 11 1 Each bundle Remarks. The material from Oman is morpho- setae (Fig. A). of of consisting a pair dissimilar one logically in accordance with the literature data (e.g. setae; single and thin Sperbcr, 1948; Brinkhurst & Jamieson, 1971). The pointed (1.5-1.8 pm wide), without nodu-

needle setae in lus, the other bifid, thicker (2-2.8 and begin segment VI, bifid, with very pm wide) nodulus reduced distal teeth. with distinct at about 1/3 from distal end.

Distal ends of setae of anterior bundles strongly

curved. teethof bifid setae of II and III minute Distribution and habitat. - Known from Asia, Af- Upper

and difficult to but about halfthe rica, N. and S. America. Not previously known to see, reaching length of lower teeth in middle inhabit subterranean habitats. region of body. Setal length

from 64-80 in ranging pm segment II to 80-100

pm in middle region of body. Except for anterior

bundles, the thinner, single pointed setae seem to Family: PHREODRILIDAE be than bifid but latter longer setae, extending more Subfamily: Phreodrilinae

into coelomic Ventral setae absent Antarctodrilus arabicus deeply cavity. n. sp. (Fig. 1) from XII and present but not modified on XIII (the

Examined - spcrmathecal segment). material. Ilolotype. Mature specimen, dissected,

stained in Harris Dorsal setae from III 1 each bundle haematoxylin and mounted on a slide. Slide n. (Fig. A),

1 2: V.01.9338, ZMA. with (sometimes one longer and one shorter

and thinner) smooth (non-serrated) hair, Hanked

Type locality. - Wadi Taww, S ofHalban 0604748/ (96/50), UTM 2 about by «support» setae, 40 pm long, which do 2606459, eC 568 pS/cm, 28 March 1996, Legit: J. H. Stock. not project from setal sacs; support setae, however,

difficult to observe. Length of long hair setae ranging Paratypes.-Four mature specimens: 1 dissected, stained in Harris from 115-210 pm in anterior to 220-330 haematoxylin, slide n. V.01.9341,ZMA, and 3 whole-mounted segments in middle of specimens: 1 stained, slide n. V.O1.9340, ZMA; 2 unstained, pm region body.

slide n. V.OI.9339, Small ZMA. Locality and collection data as for pharyngeal glands in IV-V1. Large phar- holotype. with ynx cversible roof. Numerous thin dorsal and

ventral retractor muscles attaching pharynx to - body Additional material examined. 70 specimens from the type wall. locality (28 March 96, 27 mature and 38 immature; 1 April 96, Male in line with ventral 3 mature and 2 immature); I immature specimen from Wadi pores paired, setae, somewhat anterior Taww near Halban (96/01), UTM 0712319/2606459,23 March opening to middle of segment

96; 1 from Tiwi mature specimen cave (or “Deep hole”), north XII. Spermathecal vestibulae paired, opening lat- of Ferns (96/19), UTM 0712319/2549008,25 March 96. erally at the intersegmental furrow 12/13.

Genital in organs paired usual position (Fig. 1

- The name of the is derived Etymology. species Testes XL B, C). antero-ventral in Sperm sac ex- from “Arabia”, the Latin name of the region to which tending anteriorly to Vll or VIII. Prostate glands Oman belongs. absent. Atria confined to XII, tubular to club-shaped,

bent, horizontal towards and directed anterior septum

Description. - Small-sized more than 6.4 species: of Atrial 286-364 maxi- segment. ampullae pm long, mm and 32 long segments (no 70-120 Atria with complete specimens mally pm wide. a layer of tall observed); width at II 0.14-0.19 width at XII ram, glandular cells around a distinct lumen, enveloped

(clitellum) 0.22-0.26 mm (slide-mounted speci- by a thin layer of circular muscular tissue. Basal mens). Proboscis absent. Conical 71- prostomium, part of atria narrowing gradually into short ejacu- 102 pm long, 111- 132 wide, with round in pm tip. latory ducts, ending true pendant penes located Mouth and large, circular, surrounded a lobed in folds of wall by deep body (penes sacs 175-210pm

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I. view of Fig. Antarctodrilus arabicus n. sp. A, Setae; B, Longitudinal genital segments; C, Spermatheca (paratype). a, atrium; c,

circular dorsal setae ed, hair seta lu, lumen; cuticularpenis sheath; cm, muscles; ds, (hair broken); ejaculatory duct; hs, (broken); mf, male sd, duct; funnel; p, penis; ps, penis sac; s, sperm; sa, spermathecal ampulla; spermathecal ss, support setae; sv, spermathecal

ventral of of II. vestibule; vd, vas deferens; vs, setae; vsm, ventral setae the middle region; vsll, ventral setae segment

in loose deep). Penes large, 111-148 pm long, 40-58 pm segment XV. Sperm masses, not filling

with between inner and walls. Entire 627- wide, spaces outer spermathecal ampullae. spermathecae

Distinct cuticular sheaths fun- 740 penis present. Sperm pm long. nels small, located in ventral part of septum 11/12. Ovaries attached ventrally to anterior septum of

Vasa deferentia about 6 atrial thin, pm wide, joining XII. Egg sac protruding posteriorly to 14/15. Fe- atrial lumen ampullae medially but opening into male funnels at intersegment 12/13. basally.

ducts in Spermathecal ending large, globular, Remarks. - The lateral location of the spermathecal

78- muscular vestibulae (148-177 pm indicates that Antarctodrilus arabicus n. strongly long, pores sp.

100 pm wide) in segment XIII. Ducts 350-590 pm belongs to the subfamily Phreodrilinae Brinkhurst, long, 16-32 pm wide, with narrow lumen, extend- 1991, following Pinder & Brinkhurst (1997). Also

XIII and XIV. ing through segments Spermathecal according to Brinkhurst (1991), the presence among

to ovoid, with thin outer the of characterizes the ampullae spherical lining, phreodrilines pendant penes 100-180 pm long, 64-140 pm wide and Antarctodrilus 1991. occupying genus Brinkhurst,

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che material examined. - Among eight species previously included in Additional Six mature specimens. Local-

ity and collection data for this genus (Finder & Brinkhurst, 1997), A. probo- as holotype.

scidea (Brinkhurst & Fulton, 1979) and A. acan-

thaseta Finder 1997 Etymology. - The species is named in honour of & Brinkhurst, can be easily the late Professor J. H. for his distinguished from Antarctodrilus arabicus by the Stock, great contri-

bution to the of subterranean invertebrates. presence of a well developed proboscis, serrated study hair setae and accessory glands associated with the - Small-sized than 5 penis sacs (glands to be confirmed for A. acan- Description. species: more mm

24 thuseta). long and segments (no complete specimens ob-

width All the remaining species, except A. niger (Bed- served); at II 0.13-0.20 mm, width at XII

dard, 1894) and A. africanus (Goddard & Malan, (clitellum) 0.20-0.27 mm (slide-mounted speci-

1913), have setal characteristics not found in the mens). Proboscis absent. Conical prostomium, 78-

92 new all ventral 96-140 species: setae are bifid in A. palustris pm long, pm wide, with round tip. Mouth

& A. micros & circular, and (Brinkhurst Fulton, 1979), Finder large, surrounded by a lobed lip asso-

1997 and A. Finder & Brink- ciated with circular muscle. Brinkhurst, spinosus Cutaneous glands ar-

hurst, 1997; A. uniseta has in more or less (Brinkhurst, 1982) only ranged parallel rows, particularly

one seta in each each dorsal bundle, resembling the ventral numerous at setal level of segment. Clitellum

A. ones; horwitzi Finder & Brinkhurst, 1997 and extending over 1/4 XII-XIII with glandular cells

A. characterized hair setae. in spinosus are by numerous arranged more or less parallel rows.

Antarctodrilus arabicus is similar A. Ventral n. sp. to setae from II (Fig. 2 A), each bundle

niger, but it can be from the latter with a pair of dissimilar distinguished setae; one single-pointed by the the and thin larger spermathecal vestibulae, larger (1.5-2 pm wide), without nodulus, and one

atrial lumina, the of distinct thicker presence ejaculatory bifid, (2.2-3 pm wide), with a distinct nodulus

the size of the and the shorter ducts, larger penes, at about 1/3 from distal end. Distal tooth of bifid

deferentia. A. vasa Moreover, arabicus n. sp. is seta minute in II, but segment increasing up to about in unique the in having cuticular penis sheaths. half the of genus length proximal tooth in middle region the such sheaths were of Among Phreodrilidae, pre- of body. Length the two setae similar but 80-90

viously known only in Insulodrilus tanganyikae in II and pm segment 100-115 pm in middle region Brinkhurst, 1970. of body. Except for anteriormost bundles, thinner Antarctodrilus africanus, for which information single pointed setae seem to be longer than bifid is could Brinkhurst poor, be, according to (1965), setae, but this is only because latter extend more a ofA. this synonym niger. Consequently, dubious into coelomic deeply cavity. Ventral setae absent has been taken into in the dis- species not account from XII and present but not modified on XIII (the cussion above. spermathecal segment).

Dorsal setae from 111 (Fig. 2 A), each bundle Distribution and habitat. - Known to inhabit only with 1 2 or (one longer and one shorter and thinner) groundwaters of Oman. smooth hairs, accompanied by paired, thin and

straight «support» setae (up to 60 pm long), not Phreodrilus stacki n. (Fig. 2) sp. and projecting from setal sacs difficult to see. Length

of long hair setae ranging from 100-200 in Examined pm material. - Holotype. Mature specimen, dissected, anterior to 200-335 in middle stained in Harris segments pm region haematoxylin and mounted on a slide. Slide n. of V.01.9342, ZMA. body.

Small pharyngeal glands in lll-VI. Large phar-

Type locality. - Wadi Ahin at Sohar (96/60), UTM 0454903/ ynx with eversible roof. Numerous thin dorsal and 2660684, eC 678 pS/cm, 30 March 1996, Legit: J. H. Stock. ventral retractor muscles attaching pharynx to body

wall. - Paratype. Mature specimen, dissected, stained in Harris haema- Male with toxylin and mounted on a slide. pores in line ventral Locality and collection data as paired, setae, for holotype. Slide n. ZMA. V.01.9343, slightly posterior to middle ofsegment XII. Spcrma-

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2. stocki view of Male Fig. Phreodrilus n. sp. A, Setae; B, Longitudinal genital segments; C, apparatus (paratype); D, Spermatheca

circular dorsal eversible (paratype). a, atrium; cm, muscles; ds, setae (hair broken); ed, ejaculatory duct; ep, pseudopenis; ff, female

hair male funnel;hs, seta (broken); lu, lumen; mf, funnel; ms, muscular sac of pseudopenis; ps, penis sac; rm, retractor muscles; sa,

ventral spermathecal ampulla; sd, spermathecal duct; ss, support setae; sv, spermathecal vestibule; vd, vas deferens; vs, setae; vsm, ventral setae of the middle region.

thecal vestibulae paired, opening dorso-laterally in gree. Each atrium communicates, through narrow intersegmental furrow 12/13, in line with dorsal and curved ejaculatory duct, with distal tip of a setae. well set-off sphaerical muscular pseudopenial sac

in usual muscular Genital organs paired segmental posi- (70-100 pm wide; layer 2-5 pm thick),

XI. tion (Fig. 2 B, C, D). Testes antcro-ventral in inside which a long and tightly coiled eversible

IV. Prostate is enclosed. Sperm sac long, extending to glands pseudopenis (8-12 pm wide) Pseudo- absent. Atria confined to XII, tubular to reniform penis everting through a folded muscular penis sac

of of 82-145 depending on its degree of contraction, horizontal (inversion body wall XII), pm long,

wide. and directed towards anterior septum of segment. 45-60 pm In one specimen, one pseudopenis

Atrial 200-360 40- about 250 from male ampullae pin long, maximally everted, extending pm pore.

105 wide. Atria with 3-8 thick of cir- Numerous muscular fibers ectal of pm pm layer attaching parts cular muscles and thick, glandular inner epithelial atria and pseudopenial sacs to body wall. Sperm

funnels ventral of lining surrounding distinct lumina; latter up to 70 broad, located on part septum pm wide, but varying according to contraction de- 11/12. Vasa deferentia short, thin (6-8 pm), join-

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atrial but into atrial of P. ing ampullae medially opening the vasa deferentia diemenensis are clearly

lumen basally. longer and the muscular sacs of the pseudopenes

Spermathecal ducts ending in large muscular are quite different (ovoid apically, narrowing ba-

vestibulae, attached to dorsal and ventral body wall sally and attached to the atria in P. diemenensis',

XIII fine of segment by muscular strands. The vesti- sphaeric and clearly separate from the atria in P. bular form varying from folded globular (up to 105 stock!). pm wide, 150 pm long) to long tubular (up to 60

290 its habitat. - pm wide, pm long), depending on contrac- Distribution and Only known to inhabit

tion degree. Spermathecal ducts well set off from groundwaters of Oman.

vestibulae, very long (525-800 pm, reaching seg-

thin ment XV) and (12-35 pm). Spermathecal am-

thin-walled pullae long, (375-650 pm long, 85-125 Family: TUBIF1C1DAE pm wide), reaching segments XVII orXVIIl. Sperm Subfamily: Tubificinae

in loose but distinct bundles. Entire Limnodrilus elongated sper- hoffmeisteri Claparede, 1862

1.2 1.5 mathecae to mm long.

Ovaries attached ventrally to anterior septum of Examined material. - One mature and 3 immature specimens from the Ain Hamran spring (Salah region) (96/106), UTM XII. Egg sac protruding posteriorly to 14/15. Fe- 0210592/1892363, eC 576 pS/cm, 6 April 1996, Legit: J. H. male funnels at intersegment 12/13. Stock. The sample was taken in the spring itself.

Remarks. - The dorso-lateral location ofthe sperma- Remarks. -The material fromOman is morphologi- thecal pores indicates that the new species belongs cally in accordance with the literature data (e.g. to the subfamily Phreodrilinae Brinkhurst, 1991, Brinkhurst & Jamieson, 1971). Finder & Brinkhurst The following (1997). pres-

ence ofeversible pseudopenes is a diagnostic char- Distribution and habitat. - Cosmopolitan. All types acter of the genus Phreodrilus Beddard, 1891 (Finder of lentic and lotic freshwater habitats.

& Brinkhurst, 1997). Among the 20 species cur-

included in this P. stocki be- rently genus, n. sp.

longs to the group also consisting of P. subterraneus Subfamily: Limnodriloidinae (Beddard, 1891), P. mauienensis Brinkhurst, 1971, Doliodriluspuertoricensis Erseus & Milligan, 1988 and P. diemenensis Finder & Brinkhurst, 1997; all

four characterized coiled species are by highly pseu- - Examined material. One mature and 2 immature specimens P. stocki n. is in this group dopenes. sp. unique from Tiwi cave (or Deep Hole), N of Fens, huge karstic col- because the pseudopenial sacs are clearly separate lapse cave, some 700 m from marine littoral (96/19C), handnet

in cave lake, UTM 0712319/2549008,eC 36 mS/cm, from the atria. Moreover the vasa deferentiaof the day light,

salinity 15 %o, 25 March 1996; 1 mature and 6 immaturespeci- new species are short, attached to the basal half of from the mens same cave, but a large lagoon behind sand and the atria and communicating with the atrial lumina gravel bar, eC 39.3 mS/cm, 25 March 1996; at both sites Legit; at the ectal ends, instead of long, coiled and enter- J. H. Stock. One mature and 3 immature specimens from wadi

ing pseudopenial sacs or at the junctions between Taww, Halban area (96/33), UTM 0604750/2606459,eC 601

28 March H. Stock. the atrium and the later, as in the other species of pS/cm, 1996, Legit: J.

this The atria of P. subterraneus group. very long

Remarks. - The examined be- and P. mauienensis, the great body size ofthe former specimens clearly the Doliodrilus 50 and the of long to genus as defined by Erseus species (up to mm), presence an ac- (1984) and emended by Erseus (1985) and Erseus cessory gland attached to each muscular pseudo-

in & (1988). This little - three penial sac the latter, are other reliable differences Milligan genus only - identified until now is D. diver- between these two species and P. stocki. Phreodrilus species peculiar as

" ticulatus diemenensis to be the closest relative Erseus, 1985 has an unpaired oesopha- appears to P. geal diverticulum in IX, while in the other stocki. The setae, the length of the atria and the segment two species (including the the general shape of the spermathecae are similar, but present specimens),

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oesophagus in IX is modified into a peculiar bar- Distribution and habitat. - Oman (present report),

rel-shaped part covered with a blood plexus as west coast of Puerto Rico (Erseus & Milligan, 1988),

described by Gustavsson & Erseus (1999). As far and Belize (Erseus, 1990b). The present record, far

as setal characteristics and genital apparatus are from the localities previously known, represents a

fit with the extension of the distribution concerned, our specimens very origi- large area of the spe-

nal description of D. puertoricensis. So, despite the cies (Fig. 3). This can be explained by the fact that

fact that this known exclu- the Doliodrilus is still known. species was previously genus poorly

little sively from the Caribbean area, there is doubt The three species of the genus occur in brackish

that the specimens from Oman belong to this spe- water with widely fluctuating salinity. D. puertori-

cies. censis has been collected in an enclosed brackish

The Doliodrilus found in in genus was previously lagoon (Erseus & Milligan 1988) and subtidal

the coastal region of the Arabian Gulf of Saudi muds from Belize (Erseus 1990b), all subject to

Arabia (Erseus, 1985), here represented by Dolio- fluctuating salinities. The specimens examined by drilus diverticulatus. This species was later recorded us were collected in an anchyhaline cave with a

in the Northern ofAustralia Territory (Erseus 1997). salinity of 15 %o and in the hyporheon of the wadi

A third in the D. tener Erseus, 1984 species genus, Taww, with a conductivity of 601 pS/cm. These has been identified in China Erseus (Erseus, 1990a; data confirm the euryhalinity of the species.

et al., 1990).

Fig. 3. ofthe known distribution of Map Doliodrilus (Oman, present record).

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Phallodrilinae Subfamily: on investigations of the fauna of different under- Aktedrilus sp. habitats: a total of 127 ground samples were collected

and among them, only 27 include oligochaetes. The - Examined material. One mature specimen from a well in the frequency of the occurrence of Oligochaeta in all

A’Muotazah area (Salalah Centre) (96/100), UTM 189032/ of the collected samples (about 20%) is not high, 1882511, eC 3490 pS/cm, 5 April 1996, Legit: J. H. Stock. but it compares with the frequency (39%) found

by an Amsterdam expedition in the subterranean Remarks. - The only phallodriline in the Oman the waters of Caribbean West Indian Islands (Dum- material belongs to a group of Aktedrilus devoid nicka, 1986b). The 147examined specimens belong of sheaths and with penis provided a spermatheca to 9 species of 4 families: Phreodrilidae, Naididae, whose ampulla is well set-off from the duct. The Tubificidae, Enchytraeidae. The first family, with duct of spermathccal Aktedrilus sp. is cylindrical 83 found in 12 specimens samples, represents more and thick-walled; the ampulla is spheric, thin-walled than half of the total fauna; the remaining speci- and filled with a random of mass sperm. The atria mens (64) belong mainly to the family Naididae coiled. are The specimen appears to be different (54). from the six species of the identified genus already The most important biogeographic data are the in the Arabian Gulf coast (see Erseus, 1989). The presence oftwo new species of Phreodrilidae which vasa deferentia and the attachment of the posterior represent the first record of the family in the Ara- prostate glands were not observed in detail, so we bian Antarctodrilus arabicus peninsula: n. sp. and make cannot a final conclusion about the specific Phreodrilus stocki n. sp.. The former, with 77 speci- identity of our sepecimen. It seems to be close to mens collected, is the most abundant species in the A. sinensis Erseus, 1984, a species only reported material examined. The second species, with 6 speci- from southern China. We note that out of about is less abundant. mens, Remarkably, every species thirty species of Aktedrilus already known, only of Phreodrilidae was always alone (no other oligo- A. two, argatxae Giani & Rodriguez, 1988 and A. chaete species present) in the collected samples at ruffoi Sambugar, Giani & Martinez-Ansemil, 1999 our disposal. have been found in freshwaters. Information on the subterranean oligochaete fauna

is rather scarce, and for the intertropical region, in

& in particular. Juget Dumnicka (1986) a review Family: ENCHYTRAEIDAE of subterranean a total of waters, reported 65 spe- Subfamily: Enchytraeinae cies of stygobiont Oligochaeta of which 56 have Enchytraeus sp. been identified from the only paleartic area. Giani

al. et (2001) have added 32 new species described - Examined material. One mature specimen from interstitial from 1986 to 2000, bringing the total number of of formedin waters a spring 1995 in Rustaq, Bait Qura (96/69),

stygobiont all over the world to 97. UTM 0443405/2587376,eC 818 pS/cm, 1 April 1996, Legit: .1. species Among H. 15 Stock. them, only species are not paleartic, possible that the suggesting non-paleartic fauna lacks ex-

Remarks. - Unfortunately, the state of conserva- tensive research. It is noteworthy that in the last 14 tion of the does allow specimen not a specific iden- years only 3 species (Astacopsidrilus naceri, Giani, tification. Martin & Juget, 1995 from Morocco, Haplotaxis

villiersi Omodeo, 1987 and Villiersa guanivora

Omodeo, 1987 from Guinea) were described from Faunistic remarks outside the paleartic region. The two new species

of Antarctodrilus arabicus Phreodrilidae, n. sp and This work is the first faunistic inventory of fresh- Phreodrilus stocki n. be added sp., can to the non water oligochaetes in Oman, completely unknown' -paleartic subterranean oligochaete fauna. The first until now. The research, headed by J. H. Stock of one was found in interstitial waters of wadi Taww the of University Amsterdam in 1996, was based and of the anchihaline Tiwi cave. The second spe-

Downloaded from Brill.com10/05/2021 05:43:57PM via free access - 156 E. Martinez-Ansemil, N. Giani & B. Samhugar Oligochaetes from underground waters of Oman

found in the of the Arabian Moreover the cies was interstitial waters wadi peninsula. presence of

Ahin.Among the other identified species, D. (Dero) Phreodrilidae only in underground waters of Mo-

the zeylanica, Allonais paraguayensis and D. puerto- rocco lead them to assume that nothernmost

in ricensis are for the first time mentioned sub- taxa are relict inhabiting environments that can be

terranean habitats. The absence in the samples of considered as refuges (groundwaters or ancient lakes

representatives ofthe genera Pristina and Pristinella of Africa). The presence of the family in subterra-

is worthy of note because they are the dominating nean waters of the Arabian peninsula supports all

with in the conclusions. It’s mention stygophilous genera, together Dero, previous noteworthy to

subterranean fauna of Caribbean West Indian Is- that the Phreodrilidae in Oman were found only in

lands (Dumnicka, 1986b) and in the intertropical interstitial habitats and they are completely absent

freshwaters of Africa (Grimm, 1987). The Phreo- in the superficial habitats sampled (two springs)

in the Tiwi We drilidae are a family of great biogeographical in- and lake inside the cave. stress that

terest for its probable Gondwanianorigin and high Antarctodrilus arabicus n. sp. was found in the

endemicity at species level (Finder & Brinkhurst, interstitial water ofthis cave. Findings of preodrilids

in from 1997). They were found in running and stand- north-west (arid) Australia are groundwater

ing cool waters of Tasmania, New Zealand, south- bores and springs (see Pinder, 2001).

We eastern and south-western parts of Australia and know very little about the ecology and biol-

several oceanic islands of the southern hemisphere ogy of subterranean Phreodrilidae (as well as for

below the latitude of45°. Moreover they were found those of surface waters). Juget & Yacoubi-Khebiza

in below latitude 39° S in S. America, a high alti- (1997) have shown that Astacopsidrilus naceri is

in tude lake in Andes and south African lowland a stygobiont species, with a preference for the hy-

from in rivers and upland streams. The findings equa- porheic environment; as it is very rare the wells

torial areas in ancient African rift valley lakes, and found along the watersheds of the various wadis

from hyporheic waters in Morocco are few. The examined. They conclude that the hyporheon of

Sri Lankan record is from stream all alluvial be considered for an upland (for plains can a refuge super-

& data sec Finder Brinkurst, 1997). Of the eight ficial species subjected to hydrogeological pertur-

bations genera of the family, only two (Astacopsidrilus and and high temperatures. Very little is known

Nesodrilus) come from the northern hemisphere; of the three other species known for the subterra-

our data increases this number to 4. nean environment: Phreodrilus subterraneus Bed-

The two species Antarctodrilus arabicus n. sp. dard, 1891 and P. beddardi Benham, 1904, collected

and Phreodrilus stocki n. sp. belong to the subfamily in New Zealand and Astacopsidrilus novus Jackson,

Phreodrilinae until now restricted to the area south 1931 in Australia.

of the tropic of Capricorn. In fact most species of As regards temperature, our data demonstrate that

the Antarctodrilus are from Australia, the of Phreodrilidae for cool waters is genus onp preference

- - A. which species niger (Beddard, 1894) is from S. not exclusive: the temperature at our spe-

Africa number cies from to America, S. and a of subantartic were found ranges 24.9° 29°C. The

- islands, another species A. africanus (Goddard & colonization of groundwaters is probably due to

is from S. Africa. The Phreo- their from environments such Malan, 1913)- genus escape inhospitable

drilus is known only in Australia and New Zealand as warmer surface waters. Pinder & Brinkhurst

with the exception of one species, P. branchiatus (1997) reported an apparent wider tolerance to

Beddard, 1894, present in Australia and Chile. temperature for two other species (based on their

and Antarc- So the two new records enlarge the so far known distributions): Phreodrilus branchiatus

distribution for and confirm the todrilus & area every genera proboscidea (Brinkhurst Fulton, 1979). presence of Phreodrilidae in the northern hemi- As regards water mineralization, the species seem

surmised Giani al. A. arabicus which sphere, as already by et (1995). highly tolerant, especially n. sp.

In this found in the work the authors, on the basis of new data, was interstitial water of the anchyaline

shed new light on the hypothesis of the Gondwanian cave at 22 %o of salinity. It is worth noting that

origin of the family and predicted its presence in only three other phrcodrilid species Astacopsidrilus

Downloaded from Brill.com10/05/2021 05:43:57PM via free access Contributions to 71 - 2002 Zoology, (4) 157

campbellianus (Benham, 1909), A. ostiensis Finder Brinkhurst RO, Jamieson BGM. 1971. Aquatic Oligochaeta & 2000 Erseus, and Insulodrilus litoralis (Michael- of the world. Oliver & Boyd, Edinburgh.

Chagne P, Giani N. 1998. sen, 1924)- have been recorded in highly mineral- Taxinomie et faunistique des Oligochetes de ised aquatiques la Martinique. Bull. Soc. Hist. Nat., waters (intertidal or estuarine habitats) (Finder Toulouse 134; 21-32. & Erseus, 2000). Dumnicka E. 1986a. Naididae (Oligochaeta) from subterra- The LhnnodriloidinaeDoliodrilus puertoricensis neanwaters ofWest Indian — Islands Distribution, taxonomic was in previously identified the west coast of Puerto remarks and of description a new species. Bijd. Dierk. 56 Rico and Belize. The record (2): 267-281. present represents a

Dumnicka E. 1986b. from large extension of its known distribution Oligochaeta subterranean waters of area, and West Indian Islands. Fauna could aquatica. 4° Congreso Inter- a tethydian distribution be suggested for the nacional de Espeleologia. Barcelona, 95-98. Doliodrilus. genus Nevertheless, Wang & Erseus Erseus C. 1984. The marine Tubificidae (Oligochaeta) ofHong (submitted) discovered new eight species of Dolio- and Southern China. Asian Kong mar. Biol. 1: 135-175.

drilus from southern Erseus C. China, suggesting that this 1985. Annelida of Saudi Arabia. Marine Tubificidae

is of the Arabian genus likely to be Indo-Pacific, and the Caribbean (Oligochaeta) Gulf coast of Saudi Arabia.

Fauna Saudi Arabia 6 of D. (1984): 130-154. occurrence puertoricensis could be a recent Erseus C. 1986a. Marine Tubificidae introduction (Oligochaeta) ofthe Ara- (Erseus, pers. comm.) bian Gulf ofSaudi Arabia coast (Part 2). Fauna Saudi Ara- It is worth the in the noting presence underground bia 7 (1985): 59-65.

waters of Oman of two tubificids Erseus C. 1986b. taxa belonging MarineTubificidae(Oligochaeta) ofthe Ara-

the bian Gulf coast ofSaudi Arabia to marine subfamilies Limnodriloidinae (Dolio- (Part 3). Fauna Saudi Ara- bia 8: 3-5. drilus puertoricensis) and (Aktedrilus C. 1988. Marine Erseus Tubificidae (Oligochaeta) of the Ara- sp). The presence in underground habitats of Eu- bian Gulf coast of Saudi Arabia (Part 4). Fauna Saudi Ara- of an fauna with marine rope oligochaete phyletic bia 9: 19-22.

affinities Erseus C. was already highlighted by us (Sambugar 1989. Marine Tubificidae (Oligochaeta) ofthe Ara-

bian of et al., 1999); the Oman Gulf coast Saudi Arabia (Part 5). Fauna Saudi Ara- records strengthen the hy- bia 10: 11-19. pothesis as far as the Arabian peninsula is concerned. Erseus C. 1990a. Marine Oligochaeta ofHong Kong. In: Morton The and generaAktedrilus Doliodrilus are currently B ed. Proceedings of the Second InternationalMarine Bio- found in the littoral marine or brackish water within The Marine Flora and logical Workshop: Fauna ofHongKong a of and large range salinity. The migration of intersti- Southern China, HongKong 1(1986): 259-335. Erseus C. 1990b. The tial marine marine Tubificidae (Oligochaeta) of meiobenthic tubificid species through the reef barrier ecosystems at Carrie Bow Cay, Belize, and other water of decreasing salinity could be how they ofthe Caribbean Sea,with parts descriptions of twenty-seven colonized subterranean freshwaters. new species and revision ofHeterodrilus, Thalassodrilides

and Smithsonidrilus.Zool. Scr 19 (3): 243-303.

Erseus C. 1997. The marine Tubificidae (Oligochaeta) of Dar-

win Acknowledgements Harbour, Northern Territory, Australia, with descriptions

offifteen new species. In: Hanley RH, Caswell G, Megirian

D and Larson HK eds. Proceedingsofthe Sixth International We are indebted to Ronald Vonk of (University Amsterdam) Marine The Biological Workshop. marine flora andfauna of for with providing us the material of the Oligochaeta expedi- Darwin Harbour, Northern Territory, Australia. Darwin, tion of J. H. Stock and J. J. Vermeulen in the Sultanate ofOman. Australia, 99-132. We also thank C. Erseus and A.M. Pinder for their critical re- Erseus MR. 1988. C, Milligan Limnodriloidesfaxatus and view ofthe manuscript. Doliodrilus puertoricensis, new Limnodriloidinae (Oligo-

chaeta: from Puerto Rico. Tubificidae) Proc. Biol. Soc Wash

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