Aquatic Oligochaeta (Annelida) of Balıkdamı wetland (Turkey), with description of two new species of Phallodrilinae

Biologia, Bratislava, 62/3: 323—334, 2007Section ZoologyDOI: 10.2478/s11756-007-0055-y

Aquatic Oligochaeta (Annelida) of Balıkdamı wetland (Turkey),with description of two new species of Phallodrilinae

Naime Arslan1, Tarmo Timm2 & Christer Erséus3

1Eskisehir Osmangazi University, Faculty of Arts and Science, Department of Biology, 26480 Eskisehir, Turkey; e-mail:[email protected] University of Life Science, Institute of Agricultural and Environmental Sciences, EE61101 Rannu, Tartumaa,Estonia; e-mail: [email protected] of Zoology, Goteborg University, Box 463, SE-40530 Goteborg, Sweden; e-mail: [email protected]

Abstract: The Balıkdamı Wetland, an impoundment of the upper course of the Sakarya River located near Sivrihisar(Eskisehir, Central Anatolia), is one of the most important bird conservation areas in Turkey. This area also encompassesthe mouth of the torrential Goksu Stream, which is partly hyporheic. During this study (2001–2003), 1,471 specimensrepresenting 34 taxa of aquatic Oligochaeta were collected from the Balıkdamı Wetland. All the species identified are newrecords for Balıkdamı. Two species, Coralliodrilus amissus sp. n. and Gianius anatolicus sp. n., are new to science, andfive species, Stylodrilus parvus (Hrabě et Černosvitov, 1927), Chaetogaster diastrophus (Gruithuisen, 1828), Peipsidriluslibanus (Giani et al., 1982), Tubifex acuticularis Martinez-Ansemil et Giani, 1983, and Epirodrilus moubayedi Giani etMartinez-Ansemil, 1983, are new records for Turkey. Two other species, Peipsidrilus libanus and Tubifex acuticularis, arere-described. The oligochaete fauna of the wetland was dominated by widely distributed tubificid taxa. The lumbriculidStylodrilus parvus was the most abundant species in the Goksu stream. The two new phallodriline species are remarkablesince most representatives of this subfamily live in the marine environment. Due to the species richness and diversity ofOligochaeta, as well as of several other animal groups, the Balıkdamı wetland area deserves conservation.

Key words: Oligochaeta; taxonomy; new species; conservation; biodiversity; wetland; Turkey

Introduction

The Ramsar Convention (Anonymous 2002) definedwetlands as “areas of marsh, fen, peat-land or wa-ter, whether natural or artificial, permanent or tempo-rary, with water that is static or flowing, fresh, brack-ish or salty, including areas of marine water the depthof which at low tide does not exceed six meters”. Wet-lands have values and functions that cannot be com-pared with other ecosystems. Turkey has been recog-nized as one of the most important countries of bothEurope and the Middle East referring to wetlands. Theprimary reason is the presence of rich and widespreadwetland habitats with different ecological conditions.Seventy-one wetlands of international importance havebeen determined in Turkey (Magnin & Yarar 1997) ac-cording to Ramsar’s fish and waterfowl criteria to date,and this number is likely to increase. Second, the geo-graphical characteristics unique to Turkey are such thatthe two most important migratory flyways for birds inthe western Palaearctic region (Magnin et al. 2000) oc-cur here.Turkey encompasses an area of 779,452 km2 and

has 97 Important Bird Areas (IBAs) covering a totalof 29,978 km2 or 4% of the total land area (Magnin et

al. 2000). Among them Balıkdamı is one of the few re-maining wetlands along the Sakarya River, the secondlongest river in Turkey. Turkey is rich in areas impor-tant for wetland birds of the Palaearctic (Magnin &Yarar 1997). However, along with those in the otherCircum-Mediterranean countries, many Turkish wet-lands and lakes are under increasing human impact (wa-ter abstraction, pollution) and the increasing effects ofclimatic aridity (Altınsaclı & Griffiths 2001). Signifi-cant changes in the Balıkdamı Wetland are now occur-ring because of water allocations or water removal fromthe system for irrigation, degeneration of water qualityfrom agricultural pollution, sediment transport and un-controlled reed cutting.Aquatic Oligochaeta are benthic animals living ei-

ther on or within the substrates of streams and wet-lands, although a few species are nektobenthic. Theyare often used for passive and active biomonitoring, aswell as in hazard and risk assessments (e.g., Brinkhurst& Jamieson 1971; Rosenberg & Resh 1993; Lang 1998).Aside from early, occasional faunistic and taxonomicworks (Sperber 1958; Geldiay & Tareen 1972; Sahin& Baysal 1972; Pop 1974), there has been little re-search directed towards the aquatic oligochaete faunaof Turkey. In recent years, however, some studies have

c©2007 Institute of Zoology, Slovak Academy of Sciences

324 N. Arslan et al.

Fig. 1. Geographical location of the Balıkdamı Wetland and sampling stations in west-central Turkey. The Important Bird Area (IBA)part of Balıkdamı is delineated by a thick line.

focused on the freshwater Oligochaeta of the Turkishlakes (e.g., Ustaoglu 1980; Kırgız 1988; Balık et al. 2000,2001) and rivers (e.g., Kazancı & Girgin 1998; Balıket al. 1999; Polatdemir Arslan & Sahin 2003; Arslan& Sahin 2003, 2006). Unfortunately, along with thosein other circum-Mediterranean xeric habitats, manyTurkish wetland sites are under increasing pressure –through anthropogenic impacts (water abstraction, pol-lution) coupled with the (possibly increasing) effects ofclimatic aridity (Altınsaclı & Griffiths 2001). The entirearea of Balıkdamı was declared a Natural Monument in1988 and a Permanent Wildlife Reserve in 1994.The objective of the present study was to exam-

ine both the taxonomic composition and distributionof Oligochaeta in the Balıkdamı Wetland as a meansto evaluate the contribution of this component to thediversity of an important Turkish wetland fauna.

Study sites

The Balıkdamı Wetland lies on the Sakarya River in thesouthern Eskisehir Province, West-Central Anatolia, Turkey(about 799 m a.s.l.), and has a surface area of 1,470 hectares(Fig. 1). The International Bird Area includes two partshere: the eastern portion commonly known as Balıkdamı,comprising 503 hectare of extensive reed beds (Phragmitesaustralis) with an area of temporary open water (duringwinter and spring) and mudflats; and the western part, 967hectare, consisting of marsh and grassland of the villages ofKurtseyh and Ahiler (Magnin and Yarar 1997).

Material and methods

During the present study, 1,471 specimens of aquaticOligochaeta were collected in Balıkdamı from October 2001through June 2003 (October 2001, April 2002, June 2002,November 2002, May 2003 and June 2003). The sampleswere collected with a dip net or an Ekman grab sampler.After the samples were processed in the field using a se-ries of sieves with decreasing mesh sizes, specimens were

extracted from raw samples in lab, under a dissecting mi-croscope, and transferred to 70% ethyl alcohol. Specimenswere prepared for study by mounting them on microscopeslides under cover slips, either in glycerin, polyvinyl lac-tophenol, or (after dehydration with alcohol) Canada bal-sam. Some tubificid and lumbriculid specimens were studiedas serial sections stained after Hauser (1969). Holotypes ofboth newly described species and voucher specimens of thespecies new for the fauna of Turkey are deposited in theEskisehir Osmangazi University, Museum of HydrobiologyDepartment, Turkey (ESOGU); paratypes of the newly de-scribed species are deposited in ESOGU and in the Centrefor Limnology, Rannu, Estonia (CL), and other material inCL.

Hereinafter, segment range numbers are marked withRoman numerals (e.g., X, XI) and the respective interseg-mental furrows or dissepiments with Arabic numerals (e.g.,10/11). All measurements and observations were made onpreserved specimens.

Faunistic results

During this study, a total of 34 oligochaete taxa rep-resenting 22 genera were identified; these include 29tubificids (13 of which are naidines), two lumbriculids,one haplotaxid, one enchytraeid, and one lumbricid(Table 1). All taxa collected during the study arenew records for Balıkdamı. Two species, Coralliodrilusamissus sp. n. and Gianius anatolicus sp. n., are newto science, and likely associated with sites influencedby groundwater discharge; they are probably associ-ated with groundwater but closely related to marinetaxa (see systematic part below). Several other speciescollected during the study (Chaetogaster diastrophus,Stylodrilus parvus, Epirodrilus moubayedi, Peipsidriluslibanus, and Tubifex acuticularis) are recorded fromTurkey for the first time. The genera Trichodrilus andAchaeta are also new to the Turkish fauna. Rhya-codrilus coccineus (Vejdovský, 1875) was recently re-ported for the first time from Gumus stream (Mardin)

Aquatic Oligochaeta of Balıkdamı wetland in Turkey 325

Table 1. Sampling site details and species composition of Oligochaeta and number of collected specimens in Balıkdamı Wetland, Turkey(Stations 1 and 5 are the Goksu stream sampling sites).

Sampling stations1 2 3 4 5 6 7

Hydrogen ion concentration (as pH)(min–max)

7–7.5 7.7–8 7.5–7.9 7.4–7.9 7.2–7.8 7.1–7.7 6.8–7.3

Dissolved oxygen (mg L −1) (min–max) 4.8–6 6–7.4 6.7–8 7.8–9 6.1–6.5 5.9–6.4 6.1–8Depth (m) (min–max) 1–1.2 1–2 1.5 1 0.4–0.8 0.6–1 1Temperature (◦C) in autumn, spring andsummer (min–max)

17–19 9–20 11–21 10–20 17–18 9–19 7–18

Substrate s, m m m, p m s, p m, p m, pVegetation a, sa r – r a, sa r r

Tubificidae (without Naidinae)1 Tubifex tubifex (Muller, 1774) – – – – – 20 –2 Tubifex acuticularis Martinez-Ansemil et

Giani, 198340 – – – 17 – –

3 Tubifex ignotus (Štolc, 1886) – – – 5 – – –4 Limnodrilus hoffmeisteri Claparede, 1862 – 5 166 32 12 18 115 Spirosperma velutinus (Grube, 1879) – – – 2 – – –6 Haber speciosus (Hrabě, 1931) – 10 – – – – –7 Peipsidrilus libanus (Giani et al., 1982) 45 – – – 14 – –8 Tubificinae gen. sp. 1 1 – – – – –9 Potamothrix hammoniensis (Michaelsen,

1901)– 5 6 3 – 18 21

10 Potamothrix bavaricus (Oschmann, 1913) – – 4 – – – 3Potamothrix spp. juv. – 1 407 49 – – –

11 Psammoryctides moravicus (Hrabě, 1934) 1 – – – 7 – –12 Psammoryctides albicola (Michaelsen,

1901)– 1 – – – – –

13 Rhyacodrilus coccineus (Vejdovský, 1876) – – – 10 – – –14 Epirodrilus moubayedi Giani et Martínez-

Ansemil, 198349 – 1 – 2 – –

15 Coralliodrilus amissus sp. n. 18 – – – – – –16 Gianius anatolicus sp. n. 3 – – – – – –

Naidinae17 Chaetogaster diastrophus (Gruithuisen,

1828)– 12 – – – – –

18 Paranais frici Hrabě, 1941 – 3 – – – – –19 Stylaria lacustris (L., 1767) – 5 – – – – –20 Nais elinguis Muller, 1773 8 – – 1 – – –21 Nais communis Piguet, 1906 – 18 – – – 10 –22 Nais variabilis Piguet, 1906 – 2 – – – – –23 Nais pardalis Piguet, 1906 – 13 – – – 5 –24 Nais simplex Piguet, 1906 – 2 – – – – –25 Nais pseudobtusa Piguet, 1906 1 13 – – – – –26 Pristina aequiseta Bourne, 1891 3 – – – – – –27 Pristina jenkinae Stephenson, 1931 3 – – – – – –28 Pristina sp. – – 1 3 – – –29 Dero (Aulophorus) furcatus (Muller,

1773)– – 1 3 – – –

Haplotaxidae30 Haplotaxis gordioides (Hartmann, 1821) – – 1 – – – –

Lumbriculidae31 Stylodrilus parvus (Hrabě et Černosvitov,

1927)192 – – – 113 – –

32 Trichodrilus sp. 4 – 2 – 1 – –Lumbricidae

33 Eiseniella tetraedra (Savigny, 1826) 1 – – – – – –Enchytraeidae

34 Achaeta sp. 2 – – – – – –

Mineral substrate: m – mud; s – sand; p – stones. Vegetation: a – algae; sa – small aquatic plants; r – reed.

in Turkey (Onturk & Arslan 2003). Three other taxa re-mained unidentifiable beyond the subfamily or genericlevel (Tubificinae gen. sp., Trichodrilus sp., andAchaetasp.).

Systematics and taxonomy

Descriptions of two new phallodriline species, as wellas re-descriptions of two rare tubificid species basedon new material – both new records for Turkey – are

326 N. Arslan et al.

Fig. 2. Peipsidrilus libanus: A – anterior end of body; B – anterior bundle of dorsal chaetae; C – anterior bundle of ventral chaetae;D – penial sheaths. Scales 200 µm (Fig. A), 20 µm (Figs B–D).

presented here. In addition, morphological observationsand preliminary descriptions for some other taxa col-lected during this study are given.

Peipsidrilus libanus (Giani et al., 1982) (Fig. 2)

Description. 59 specimens, many of them sexually ma-ture.Length 2–7 mm; diameter of mature specimens

0.15–0.25 mm anteriorly and posteriorly, but 0.25–0.40 mm in genital segments; segment number 22–60,most often 50–60. Prostomium mostly blunt and con-ical, sometimes rounded or prolonged. Body smoothand transparent. No secondary rings but body surfacefinely annulated (Fig. 2A). Dorsal bundles consist of 1–2 smooth hair chaetae, and 2–4(5), in midbody mostly3, pectinate chaetae. Hair chaetae 150–325 µm long inpreclitellar region, becoming shorter and gradually dis-appearing in midbody and posterior segments. Pecti-nates 40–85 µm long, with about equal main teeth, andseveral fine intermediate teeth (Fig. 2B); replaced withordinary bifid crotchets posteriorly. Ventral crotchetsin anterior segments 3–5(6) per bundle, 50–85 µm long,with teeth of equal length but upper tooth thinner thanlower (Fig. 2C). Little change observed in the number[2–4(5) per bundle], length (50–70 µm), or shape of

the bifid chaetae, neither in posterior dorsal nor ven-tral bundles. No modified genital chaetae; ventral bun-dles of XI either absent, or represented by 1–2 shorter(about 50 µm) bifid crotchets. Coelomocytes not ob-served. Chloragogen tissue from VI on, sparse. Intesti-nal dilation smooth. Large pharyngeal glands (chro-mophilous cells) present both on pharynx in III andin body cavity of IV–V. Dorsal blood vessel thin in an-terior segments (I–VII), but thicker from VIII; locatedlaterally from X on in some specimens.Clitellum in XI–XII (sometimes also extending

slightly to neighboring segments), thin, with obscurelimits. Spermathecal pores slightly above (sometimesalso anterior to) ventral bundles of X. Male pores atventral bundles of XI, or in place of the lacking bun-dles. Testes in X, anterior sperm sac reaching VII, VIII,or IX in some specimens, but lacking in others; poste-rior sperm sac can reach at least XIV. Ovaries in XI,mature eggs observed in XI–XIII.Male funnels in X, at ventral part of 10/11, at least

35 µm long and 30 µm wide; mouth of funnels dilatingup to 42 µm, directed upwards, and bearing large tuftsof spermatozoa. Vasa deferentia longer than atria, inter-nally ringed (consisting of transversally oriented cells),usually 16 µm wide for most of their course but 12 µmwhen piercing 10/11, and, in some specimens, dilating

Aquatic Oligochaeta of Balıkdamı wetland in Turkey 327

up to 19–21 µm in their distal half. Vas deferens mak-ing several small coils in anterior half of XI, then anarc over atrium, joining posterior side of latter. Atriaerect, oval or sacculate, sometimes concave posteriorly,mostly 90–110 µm long and 65–75 µm wide. Muscu-lar layer of atrial wall thin (usually 2–3 µm), partiallyextending onto the penial sac, but with parts of it con-nected directly with body wall. Atrial epithelium 5–16µm thick, with nuclei in periphery while the inner por-tion looks pale and honeycomb-like. Sparse, long bun-dles of spermatozoa in the atrial lumen. A compact,flat prostate gland lies between 11/12 and the poste-rior wall of atrium, attached to latter near entrance ofvas deferens.Penial sacs spacious, like truncated cones in XI,

50–75 µm high, about 60 µm wide, in their flat upperportion tightly pressed against atrium. Inner wall of up-per portion of penial sacs folded. Penes, cylindrical ordumbbell-shaped, much smaller than penial sacs. Eachpenis covered with thick but elastic cuticle visible as apenial sheath in whole mounts. These sheaths (Fig. 2D)usually 20–30 µm long, 16–19 µm wide in their narrow-est, middle portion, while proximal “collar” (33–47 µmwide) extending to walls of penial sac. However, in onespecimen one of the sheaths was stretched, 77 µm long,with its collar 34 µm wide.Spermathecae in anterior portion of X, sometimes

partially pressed into neighboring segments. Rounded,oval, or irregularly shaped ampulla, 80–170 µm in di-ameter, with wall 3–7 µm thick, and containing bundlesof free, long spermatozoa. Spermathecal duct clearlydistinguished, about 90 µm long, proximally 30–42 µmwide but narrowing to 26 µm in its distal end; withmuscular and epithelial layer equally thick, and withnarrow lumen.

Remarks. The taxon fits well with the Peipsidriluslibanus, first described as Neoaulodrilus libanus by Gia-ni et al. (1982), but later transferred to Peipsidrilus byGiani et al. (1984). Slightly smaller size of the atria andpenes, and more variable shape of the penial sheaths(usually displaying a narrow midpart, in our material)are the only differences, in comparison with the origi-nal description. The lack of spermatozeugmata in sper-mathecae distinguishes this genus and other membersof the former subfamily Aulodrilinae [invalidated byGiani et al. (1984)] from the typical Tubificinae. Thischaracter, together with the small body size and simi-lar exterior appearance, can easily cause confusion withsome small Rhyacodrilinae. However, the lack of coelo-mocytes, the presence of penial sheaths, and the ab-sence of modified penial chaetae in mature specimensenable this species to be distinguished from the rhya-codrilines. The penial sheaths resemble those of Peip-sidrilus pusillus Timm, 1977 but they are more delicate[compare with Fig. 1.4 in Timm (1977)].Peipsidrilus libanus was found only in Goksu

Stream within our study area (Table 1) (October 2001,June and November 2002) but it has been documentedfrom several sites in Lebanon (Giani et al. 1982). We

now believe that Peipsidrilus libanus may have a widerdistribution in the Near East.

Tubifex acuticularis Martinez-Ansemil et Giani,1983 (Fig. 3)

Description. 57 specimens studied, many of them sex-ually mature or maturing.Length 6–11.5 mm; diameter 0.25–0.40 mm but

at rear end only 0.15–0.20 mm; segment number 44–64. Prostomium semi-spherical, conical, or oval. Bodysmooth, sometimes finely ringed, transparent. Inter-segmental furrows distinct; no secondary annulation.Genital segments not distinctly wider than the rest(Fig. 3A).Anterior dorsal bundles composed of 1–3 (mostly

1), smooth, 160–300 µm long hair chaetae and 2–4pectinates, 65–100 µm long, with equal straight teeth,and fine short intermediate denticles (Fig. 3B). Hairchaetae in mid-body single, small, and gradually disap-pearing in caudal segments. Anterior ventral crotchets(2)3–4 per bundle, 70–110 µm long, but shorter, 50–70µm, in II and in genital and postclitellar segments; up-per tooth thinner than lower, in anteriormost segmentsoccasionally slightly longer (Fig. 3C). In posterior seg-ments, 2(3) similar bifid crotchets in both dorsal andventral bundles. No modified genital chaetae; ordinaryventral crotchets present in X and XI.Small brain in 0–I; ventral nerve cord thin, in some

specimens beginning already in I–II. Roof of pharynxthick, covered with a layer of glands; chromophilousgland cells surrounding oesophagus in IV–VI. Chlor-agogen tissue from VI on. Intestine dilating abruptly inVIII. Free dorsal and ventral vessels distinctly visibleeven in anterior segments. Upper portion of transversalvessels dilated as “hearts” in VIII. No coelomocytes.Clitellum in XI–XII, thin; genital pores not ele-

vated above the body surface. Testes in X, ovaries inXII. Both sperm and egg sacs posteriorly reaching upto XVII. No anterior sperm sac.Male funnels at 10/11 large, of irregular shape.

Vasa deferentia long, forming several loops in XII, in-ternally ringed in their whole length. Proximal end ofvas deferens narrower (14–20 µm) than distal end (upto 33 µm), entering apical end of atrium. The atria andpenes were not studied in all details. Atria appearingclub-shaped (120–133 µm long, 40–49 µm wide in opti-cal section), each with prostate gland attached to oneside of the proximal, wider portion. Atrial wall about13 µm thick, with external muscular layer 2–3 µm. Noejaculatory duct. Soft penes 35 µm wide, in large pe-nial sacs, without any sheath. External male pores nearventral chaetae in XI.Spermathecae very large; usually one of them di-

rected anteriorly into IX–X, the other posteriorly to XI–XIII and dilating only behind clitellum. Ampulla sac-culate and long; up to 200–250 µm wide in its roundedinner end, the posterior ampulla yet extending as anarrow tube through several segments. Its epithelialwall 5–9 µm thick in stretched portions, but 23–28 µm

328 N. Arslan et al.

Fig. 3. Tubifex acuticularis: A – anterior end of body; B – dorsal chaetal bundle (midbody); C – ventral chaeta (midbody). Scales 200µm (Fig. A), 20 µm (Figs B, C).

thick and with finely papillate internal surface in re-laxed portions. Several long, nematode-shaped sperma-tozeugmata per ampulla, their diameter reaching 28–37µm. Spermathecal pores dorsolateral, between ventraland dorsal bundles of X.

Remarks. The new material differs from the originaldescription in smaller segment number, variable shapeof prostomium, and smaller size of atria and penes.Unfortunately, the exact length of penes was not es-tablished in our material. The other characters, par-ticularly the large spermathecae extended in differentdirections and containing very long spermatozeugmata,fit well.Tubifex acuticularis was originally described by

Martinez-Ansemil & Giani (1983), and like Peipsidriluslibanus, was previously known from only a few sitesin Lebanon. Our present findings document the occur-rence of T. acuticularis in the Near East also outside ofLebanon. In Balıkdamı Wetland, the species was foundonly in the Goksu Stream (Table 1) (October 2001,June and November 2002) like P. libanus.

Epirodrilus moubayedi Giani et Martinez-Ansemil,1983

At least 52 specimens, from three stations both in thewetland and stream (see Table 1) (October 2001, June2002), have been tentatively identified as E. moubayedi.

Some of the immature individuals may actually belongto different species.Description. Up to 4.5 mm long, with 49 segments(but most specimens studied were broken). Similar toPeipsidrilus libanus in external somatic characters: 1–2 hair chaetae, 160–205 µm long, and 2–4 pectinates,40–65 µm long, in anterior dorsal bundles; anterior ven-tral bundles with 3–4 bifids, 45–70 µm long, with uppertooth thinner than lower. However, mature individualsreveal typical rhyacodriline penial bundles in XI, with3–4 chaetae, 55–90 µm long; simple, thin and curveddistal tips of penial chaetae converged in each bundle.Coelomocytes were observed in most specimens. Intes-tine slightly dilated, beginning varies from VII to XIII.Internal reproductive organs not clearly seen, but

in general are similar to those presented in the orig-inal description. Atria in XI elongate, up to 140 µmlong and 37–60 µm in diameter, with thick epitheliumand narrow lumen. Prostatic cover apparently lackingin one specimen but not exactly established in the oth-ers. Unpaired copulatory sac present in one specimenwhile separate pseudopenes were observed in another.Spermathecae in X consisting of a roundish or saccu-late ampulla, either empty or with amorphous mass ofsperm, and short and thick, muscular duct. The pro-portions between muscular and epithelial layers of theampulla were different in separate specimens.E. moubayedi has been known so far from Lebanon

(Giani & Martínez-Ansemil 1983) and Tunis (Boumaiza

Aquatic Oligochaeta of Balıkdamı wetland in Turkey 329

Fig. 4. Coralliodrilus amissus sp. n.: A – anterior end of body; B – anterior bundle of locomotory chaetae; C – bundle of penial chaetae(in XI). Scales 200 µm (Fig. A), 20 µm (Figs B, C).

et al. 1986).

Coralliodrilus amissus sp. n. (Figs 4, 5)

Description. A tiny species (only 2.5–3.5 mm long),with 39–53 segments (Fig. 4A). All somatic chaetae bi-fid, with very short upper tooth (Fig. 4B); their numberis 3–7 per bundle, and length 33–81 µm (the longestones in dorsal bundles of midbody). In mature indi-viduals, penial bundles in XI, consisting of 4–7 paral-lel straight chaetae, 60–80 µm long, with very distalnodulus and with simple obtuse, curved tip (Figs 4C,5). Clitellum weakly developed. No coelomocytes. Be-ginning of wider midgut varies from XII to XVI, inseparate individuals. Dorsal blood vessel observed inpreclitellar segments, sometimes reaching XII. Anteriorsperm sac reaching VIII or IX (Fig. 4A); the posteriorone, if present, extending into XII only. Large spermbundles indicating position of sperm funnels at 10/11.Genitalia paired, here described on the basis of holo-type only (Fig. 5). Vasa deferentia short, about 10 µmwide, leading to bipartitate atria in XI. Proximal part ofatrium oval, about 30 µm long, 18 µm wide, with gran-ulated inner epithelium and thin outer layer of muscles.

Distal portion of atrium tubular, about 40 µm long, 10µm wide, opening on small protuberance on flat under-side of XI, laterally of penial chaetae. Prostate glandsabsent. Ripe eggs observed in XII and XIII. Spermath-ecae with lateral pores in X, each with short, indistinct,conical duct, and oval ampulla, about 50 µm long, 25µm wide; latter with longitudinally arranged sperma-tozoa.

Holotype. ESOGU, Oligochaeta (B) No 1, whole-mountedsexually mature specimen (October 2001).Type locality. Goksu Stream, Station 1 (Fig. 1, Table 1).Paratypes. CL, Oligochaeta, No 28, fourteen whole-mountedspecimens on different stages of maturity, on a commonslide, all from the type locality (October 2001 and June2002).Other material. CL, three sectioned specimens from thetype locality.

Etymology. The species epithet amissus (Latin for“lost”) alludes to the fact that this freshwater speciesis so far away from the marine habitats known for allother members of Coralliodrilus Erséus, 1979.

330 N. Arslan et al.

Fig. 5. Coralliodrilus amissus sp. n., lateral view of spermathecaand male genitalia in segments X–XI. aa – atrial ampulla; ad –atrial duct; pc – penial chaetae; s – spermatheca; sb – spermbundle; vd – vas deferens. Scale 100 µm.

Remarks. Coralliodrilus Erséus, 1979 is a genus ofphallodriline Tubificidae characterized by the completelack of prostate glands outside the atrial ampullae. Itcontains 22 marine species, most of which are from shal-low waters in warmer seas (Erséus 1979, 1992, 1993,1997a; Erséus & Milligan 1992). Coralliodrilus amissussp. n. is thus the first member of this taxon from afreshwater habitat.More than half of the previously known Corallio-

drilus species have atria that are more or less bipartite(i.e., each atrium consists of a proximal ampulla fol-lowed by a demarcated distal duct leading to the malepore). This condition was seen also in C. amissus. Thelatter is morphologically most similar to (but not nec-essarily most closely related to) C. mirus Erséus, 1990,from south-western Australia (Erséus 1990; Erséus &Wang 2005). Coralliodrilus mirus also has (1) a highnumber of bifid somatic chaetae (up to 6 per bundle),(2) multiple straight penial chaetae with pointed, some-what curved tips, (3) spermathecal pores near the lat-eral lines, (4) small, bipartite, atria, and (5) spermath-ecae that are often oval (but variable, sometimes pear-or club-shaped). Coralliodrilus amissus, however, haslonger penial chaetae than C. mirus; in the latter thesechaetae are only 25–55 µm long. Moreover, none of thecongeners with genitalia similar to those of C. amis-sus has prolonged chaetae in the dorsal bundles of the

midbody, which is a striking feature of our new species.Among the freshwater tubificids, the new species

can be easily confused with Aulodrilus limnobiusBretscher, 1899, due to somewhat similar set of loco-motory chaetae.

Gianius anatolicus sp. n. (Figs 6, 7)

Description. Length 3–3.5 mm, segment number 48–67 (Fig. 6A). Somatic chaetae of three kinds. In anteriorpart of body, bifid crotchets 2–3 per bundle (Fig. 6C),31–58 µm long in dorsal bundles, and somewhat shorter28–47 µm, in ventral bundles, about 2 µm thick. In mid-and posterior of body, paired simple-pointed chaetae inall bundles (Figs 6E, F). Those simple-pointed chaetaeonly 26–33 µm long, 1 µm thick, in ventral bundles(Fig. 6E), but much larger (58–75 µm long, 3 µm thick)in dorsal ones (Fig. 6F). Ventral bundles of XI in holo-type, 4–5 parallel penial chaetae, 25 µm long, sigmoid,with thin simple tip (Fig. 6D). Genitalia paired (Fig. 7).Large sperm bundles indicating position of sperm fun-nels at 10/11. Vasa deferentia not observed (probablyhidden inside anterior prostate glands). Atria curved,cylindrical, 65 µm long, 12 µm wide, with granulated in-ner epithelium and thin outer layer of muscles. Distally,atria opening as simple pores on underside of XI, moreor less in line with penial chaetae. Two pairs of prostateglands: anterior pair large, apparently attached to prox-imal ends of atrium; posterior pair much smaller, lo-cated close to distal ends of atria, near 11/12. Sper-mathecae opening in line with ventral chaetae, in ante-rior portion of X, each with short, indistinct duct, andelongated pear-shaped, thin-walled, ampulla; sperm asrandom mass filling wider distal part of each spermath-eca (Fig. 7).

Holotype. ESOGU, Oligochaeta (B) No 2, whole-mountedsexually mature specimen (June 2002).Type locality. Goksu Stream, Station 1 (Fig. 1).Paratypes. ESOGU, Oligochaeta (B) No 2, two whole-mounted juvenile specimens, from the type locality, (June2002) mounted on the same slide with holotype.

Etymology. Named for Anatolia, the Asian part ofTurkey where the type locality of this species is located.

Remarks. Gianius Erséus, 1992 is another genus ofphallodriline Tubificidae, to date with eight describedspecies (Erséus 1992, 1997b) – all with curved elon-gated atria each bearing two prostate glands. However,as noted by Erséus (1992), the monophyly of taxonis weakly supported (based only on the shape of theatria). Gianius contains marine as well as freshwaterspecies, and G. anatolicus appears most closely relatedto G. riparius (Giani et Martinez-Ansemil, 1981) – aspecies presently known only from subterranean watersin Spain and France (Giani & Martínez-Ansemil 1981;Giani et al. 2001). These two taxa have virtually iden-tical penial chaetae, male ducts and spermathecae. Thenew Anatolian species, however, has a unique chaetal

Aquatic Oligochaeta of Balıkdamı wetland in Turkey 331

Fig. 6. Gianius anatolicus sp. n.: A – lateral view of the whole body; B – ventral view of the genital region; C – anterior bundle oflocomotory chaetae; D – bundle of penial chaetae; E – posterior ventral and F – posterior dorsal bundle of locomotory chaetae. Scales200 µm (Fig. A), 20 µm (Figs B–F).

pattern; none of its congeners has three kinds of somaticchaetae as described for G. anatolicus, above.

Pristina sp.

Four immature specimens, tentatively identified in thegenus Pristina, were collected from two wetland sam-ples (Table 1) (October 2001, June 2002 and 2003).Without proboscis. Differing from Pristina jenkinae inthat they have needle chaetae with very long teeth. Inaddition, the blood plexus occurs in II–VI, and largersimple transversal vessels begin in VII. Stomach inIX.

Trichodrilus sp.

Incomplete specimens of this genus found at three sta-tions, both in the wetland and Goksu Stream (Table 1)(June 2002 and May 2003) were too badly preserved foridentification to the species level. Paired simple-pointedchaetae, lack of lateral vessels in postclitellar segments,male funnels in IX and X, pyriform atria in X, andspermathecae in XI and XII, were observed.

Achaeta sp.

Two small, immature enchytraeids of the genus Achaeta(without any chaetae) were also collected during this

332 N. Arslan et al.

Fig. 7. Gianius anatolicus sp. n., horizontal view of spermathecae and male genitalia in segments X–XI. a – atrium; pc – penial chaetae;pr1 – anterior prostate gland; pr2 – posterior prostate gland; s – spermatheca; sb – sperm bundle. Scale 100 µm.

study (Table 1) (October 2001 And April 2002), butbecause of their complete lack of reproductive organs,could not be identified to species.

Discussion

Balıkdamı can be divided into two major areas usingthe distribution of identified taxa documented duringthis study. The fauna of the Goksu stream was conspic-uously different from that occurring in the other sam-pling stations. Stylodrilus parvus was the most abun-dant species here, accompanied by Peipsidrilus libanus,Tubifex acuticularis, Epirodrilus moubayedi, Corallio-drilus amissus sp. n., Gianius anatolicus sp. n., and sev-eral others. We assume that P. libanus, T. acuticularisand E. moubayedi, previously known from Lebanon(Giani et al. 1982; Martinez-Ansemil & Giani 1983,respectively), may be widely distributed elsewhere inthe Near East, what has been remained poorly stud-ied to date. The oligochaete fauna of the marshlandand reeds was dominated by widely distributed tubi-ficine and naidine tubificids. The former family of Nai-didae is treated here as a subfamily of Tubificidae, fol-lowing Erséus et al. (2002) and Erséus & Gustavsson(2002). Most of the Naidinae found in Balıkdamı – Sty-laria lacustris, Nais elinguis, N. communis, N. vari-abilis, N. pardalis, N. simplex, N. pseudobtusa, Pristinaaequiseta, P. jenkinae [formerly Pristinella jenkinae,before the genus Pristinella was suppressed by Col-lado & Schmelz (2000)], and Dero (Aulophorus) fur-cata – had been recorded previously from the Sakarya

River (Arslan 1999; Polatdemir Arslan & Sahin 2003).Of these, N. pardalis and P. jenkinae were the mostwidely distributed, while P. aequiseta has the most lim-ited distribution (Polatdemir Arslan & Sahin 2003). Inour Balıkdamı, both Pristina jenkinae and P. aequi-seta were met only at a single station (Tab. 1). Themost common species of Tubificinae in our researcharea were the cosmopolitan Limnodrilus hoffmeisteriand the Palaearctic Potamothrix hammoniensis. Bothspecies have also been repeatedly recorded from otherregions of Turkey (e.g., Kırgız 1988; Balık et al. 2000,2001, 2004).Prior to the present study, only two taxa of Lum-

briculidae had been recorded from Turkey: the Holarc-tic Lumbriculus variegatusMuller, 1773, from Isıklı lake(Balık et al. 2000), and Lumbriculus sp. from Golcuklake (Geldiay & Tareen 1972). Species belonging to Sty-lodrilus Claparede, 1862, and Trichodrilus Claparede,1862, had never been recorded from Turkey prior tothis study, although they are common in a variety ofHolarctic subterranean freshwater habitats (caves, hy-porheic and phreatic waters, wells, and springs), and,particularly, in similar habitats in the Palaearctic region(Giani & Rodriguez 1994; Rodriguez & Coates 1996).Thus, the marshy wetland area of Balıkdamı was inhab-ited primarily by common, widely distributed species,while several rare taxa were concentrated mainly in theGoksu Stream.Among the rare species, Coralliodrilus amissus and

Gianius anatolicus belong to the subfamily Phallodrili-nae most characteristic of marine habitats. However,

Aquatic Oligochaeta of Balıkdamı wetland in Turkey 333

several phallodrilines adapted to fresh water have beendiscovered in underground sites. As belonging to dif-ferent, principally marine genera, they must be re-garded as comparatively recent invaders in the conti-nental groundwater. The problem has been discussedby Sambugar et al. (1999).Wetlands are under heavy pressure with the in-

tensification of human activities and environmentalchanges. In Turkey, a large area of natural wetlands hasbeen lost, degraded or transformed in recent decades.Some of them disappeared completely due to reclama-tion for agriculture and expansion of towns; others weredegraded in quality due to environmental pollution; andyet others were changed into artificial wetlands such aspaddy fields, aquacultural ponds, reservoirs and irri-gation canals. Loss of natural wetlands worldwide inrecent years has resulted in the construction of artifi-cial wetlands, which are the only choice for water birdcommunities in the regions where natural wetlands areunavailable (Magnin et al. 2000). DSI (State WaterWorks) currently plans to irrigate the entire area alongthe upper reaches of the Sakarya River. One of the DSIprojects, the second phase of the “Upper Sakarya Ir-rigation Scheme”, envisages the irrigation of 4736 haarea west and east of Balıkdamı. Water required bythis project will be provided by four pumping stationson the Sakarya River and from the Goksu springs (im-mediately south of the IBA), where it will be stored in asmall reservoir. The stone barrier will be replaced witha regulator, maintaining a higher water level through-out the year and creating a permanent lake of ca 500ha in the eastern part of the IBA. In addition to theloss of valuable natural habitat in the western part, thecreation of a permanent lake in the east will result inthe loss of virtually all the sensitive and ecologicallyimportant marsh and mudflat areas.Our results indicate that species richness and di-

versity of Oligochaeta fauna of Balıkdamı wetland arehigh, including two new species. In terms of biologi-cal values or functions, wetlands serve as habitat forrare, endangered or endemic or relic species. Apart fromOligochaeta, other invertebrate groups also may includerare, new or endemic species even among vertebrates(particularly fish). Therefore, the Balıkdamı wetlandarea, with its yet poorly studied freshwater fauna, ex-hibits nature values that clearly serve as arguments forthe conservation of this area.

Acknowledgements

The Research Foundation of Eskisehir Osmangazi Univer-sity financed this study under the project No. 200219041.The studies by the second author were partly supported bythe Core Grant No. 0362482s03 “Formation and changes ofthe biological diversity under the human impact in differentlake types (Estonia-Denmark-Netherlands)” of the EstonianMinistry of Education and Research. The third author’s con-tribution was supported by the Swedish Research Council(Grant No. 621-2004-2397). The authors also thank Mark J.Wetzel (Illinois Natural History Survey) and two anonymous

reviewers, for their useful suggestions incorporated into thispaper.

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Received June 1, 2006Accepted November 15, 2006