Annelida, Clitellata) of High-Elevation Lakes in the Eastern Black Sea Range of Turkey

S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

Turk J Zool 2012; 36(1): 59-74 © TÜBİTAK Research Article doi:10.3906/zoo-1002-39

Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

Seray YILDIZ*, Murat ÖZBEK, Mustafa Ruşen USTAOĞLU, Haşim SÖMEK Department of Hydrobiology, Faculty of Fisheries, Ege University, 35100 Bornova, İzmir - TURKEY

Received: 11.02.2010

Abstract: Many large and small lakes of varying depths are present in the Eastern Black Sea Range of Turkey, the nation’s third most important glacial region following the Ağrı and Cilo-Sat mountain ranges. During the present study, 6 expeditions to collect aquatic oligochaetes from these lakes were conducted in July and August of 2005, 2006, and 2007; qualitative and quantitative samples were collected from 59 glacial lakes. We present and analyze the dominancy and distribution of aquatic oligochaete assemblages and their relation to environmental factors (temperature, dissolved -3 - 2+ 2+ oxygen, pH, electrical conductivity, salinity, turbidity, PO4 -P, HCO3 , organic carbon, hardness, Ca , Mg , Si, water depth, and altitude) using classifi cation and ordination techniques. Canonical correspondence analysis (CCA) was used to characterize the relationship between oligochaetes and the environmental variables. As a result, we determined the 4 most important environmental variables (elevation, water depth, dissolved oxygen, and temperature) aff ecting species distribution in general. Sampling localities were clustered into 8 groups with the unweighted pair-group method with arithmetic mean (UPGMA) based on physicochemical characteristics. Th e relationships between the total number of individuals and environmental measurements were determined by a simple analysis of variance (ANOVA) test. Th e results of our analyses suggest a signifi cant positive correlation between altitude (P < 0.05; F = 2.994) and the total number of individuals.

Key words: Oligochaeta, Clitellata, Haplotaxidae, Naididae, Enchytraeidae, Lumbriculidae, Tubifi cinae, Naidinae, Eastern Black Sea Range, Turkey, glacial lakes

Türkiye’nin Doğu Karadeniz Sıradağları üzerindeki yüksek rakımlı göllerde sucul Oligoket (Annelida, Clitellata) türlerinin dağılımı

Özet: Ağrı ve Cilo-Sat Dağları’ndan sonra Türkiye’nin 3. büyük buzul bölgesi olan Doğu Karadeniz Sıradağları’nda çeşitli derinliklerde büyüklü küçüklü bir çok göl vardır. Bu çalışma boyunca, bölgedeki sucul oligoket topluluklarının dağılım ve baskınlıkları analiz edilmiş ve sınıfl andırma sıralama (derecelendirme) teknikleri kullanılarak çevresel faktörlerle ilişkileri sunulmuştur. Oligoketlerle çevresel faktörler arasındaki ilişkiyi ortaya çıkarmak için kanonik korrespond analizi (CCA) kullanılmıştır. Türlerin dağılımını etkileyen 4 önemli çevresel faktör, önem sırasıyla rakım, su derinliği, çözünmüş oksijen ve sıcaklık olarak belirlenmiştir. Örnekleme yapılan lokalitelerde ölçülen fi ziko-kimyasal analiz sonuçlarına göre yapılan UPGMA analiz sonucunda, lokaliteler 8 gruba ayrılmıştır. Toplam birey sayıları ile çevresel faktörlerin ilişkisi basit ANOVA testi ile belirlenmiştir. Buna göre toplam birey sayısı ile rakım arasında önemli pozitif bir ilişki (P < 0.05; F = 2.994) olduğu saptanmıştır.

Anahtar sözcükler: Oligoket, Clitellata, Haplotaxidae, Naididae, Enchytraeidae, Lumbriculidae, Tubifi cinae, Naidinae, Doğu Karadeniz Sıradağları, Türkiye, buzul göller * E-mail: [email protected]

59 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

Introduction rivers rush down to the lower elevations. Locality Lakes in high mountains and on glaciers are information for the 59 lakes in the 6 drainage basins unique habitats in terms of faunal composition, studied during this project, and the characteristics because they constitute isolated environments. Our of the sampling sites on those lakes, are presented in knowledge of oligochaete fauna is still very limited Table 1 and Figure 1. in some parts of Turkey, especially in the mountain ranges. Th is study aims to explore the ecological and Materials and methods faunistic features of mountain lakes in the Eastern Black Sea Range. Sampling procedures and environmental variables Although various Oligochaeta studies have been conducted at easily accessible lowland lakes, according Due to the high elevation of these lakes, most to Arslan (2006), only a few studies have focused of the study sites are covered by ice and snow for on the oligochaete fauna associated with the high- 8- 9 months of the year, with ice-free conditions elevation glacial and tectonic lakes in the mountains usually present only during the warmest months of Turkey. Among these, a pioneering study by Yıldız of July and August. To collect aquatic oligochaetes et al. (2005) investigated macroinvertebrate fauna of from these lakes, 6 expeditions were conducted Eğrigöl in the Taurus Mountains; a second study by in July and August of 2005, 2006, and 2007. Some Yıldız et al. (2007) addressed the oligochaete fauna physicochemical features and the oligochaete fauna of 16 lakes located in the Taurus Range. Ustaoğlu of the 59 lakes (3 replicates per site) belonging to et al. (2008) investigated the limnology and fauna the basins of 6 rivers (Çoruh River, Fırtına Stream, of glacial lakes and streams on Mount Uludağ in İyidere, Kabisra Stream, Solaklı Stream, and Maçka western Anatolia. More recently, Yıldız et al. (2010) Stream) were determined for the fi rst time. Water presented the results of their study on the distribution samples were taken from the littoral zone of each of oligochaetes (Lumbriculidae and Enchytraeidae) lake, and 6 environmental variables, temperature −1 in the littoral zones of glacial and tectonic lakes in the (°C), dissolved oxygen (DO, mg L ), pH, electrical −1 −1 mountains of the Eastern Black Sea Range of Turkey. conductivity (COND, μs cm ), salinity (S, mg L ), and water transparency, were measured in situ with Th is study was part of a larger investigation a WTW pH meter (model 330), WTW oxygen meter focused primarily on: 1) the littoral, profundal, and (model 330), YSI SCT meter (model 30), and Secchi pelagic aquatic macroinvertebrate communities; -3 - disk. Other variables (PO4 -P, HCO3 , organic carbon, 2) the general limnology; and 3) the chemical and hardness, Ca2+, Mg2+, and Si) were measured in the physical parameters of high-elevation lakes occurring laboratory following the standard methods of the in 6 drainage basins in the Eastern Black Sea Range. American Public Health Association (1989). Th e objectives of this study were to determine the range of distribution of oligochaete species in the Benthos samples were collected from diff erent area and to document the relationships between the parts of the littoral zone (between 0 and 50 cm) of species and environmental variables. the lakes by hand-net (mesh size: 180 μm), disturbing the substrate for 3 min. In addition, an Ekman-Birge Study area grab was used in deeper parts of the lakes. Benthic Th e Eastern Black Sea Mountains are a range samples were fi xed on site with 4% formaldehyde. rising along the Black Sea coast in northeastern Aft er sorting the material, Oligochaeta samples Turkey. Th e highest peak is Kaçkar Mountain (3937 were preserved in 70% ethanol until identifi cation m), and the plateaus at about 3000 m above sea level to the species level. Aft er a temporary mounting of are the highest parts of the range. Th e mountains are sorted oligochaete samples on slides in Amman’s partially glaciated and alpine in character, with steep lactophenol, the worms were identifi ed using a rocky peaks and numerous mountain lakes. Extensive stereomicroscope and a binocular microscope. Th e glacial and water erosion has given these mountains reference materials were kept in the collection of the their craggy, rugged look. Powerful streams and fi rst author as permanent whole mounts on slides

60 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

Table 1. Locality information for and dates of sampling at 59 stations in high-elevation lakes in the Eastern Black Sea Range of Turkey, where surveys for aquatic oligochaetes were conducted in 2005, 2006, and 2007. Trophic scale: UO = ultraoligotrophic, O = oligotrophic, M = mesotrophic.

Station Sampling Altitude Substratum types Trophic Code Lakes Basins Coordinates numbers dates (m) scale

06.07.2005 40°38ʹ43ʺN, 1 Ç08 Adalıgöl Çoruh River 3020 hard, gravel O 19.08.2005 40°53ʹ10ʺE 40°38ʹ51ʺN, 2 Ç07 19.08.2005 Üstgöl Çoruh River 3030 hard, gravel O 40°52ʹ54ʺE 06.07.2005 40°38ʹ53ʺN, 3 Ç09 Ortagöl Çoruh River 3010 h ard, g r ave l U O 19.08.2005 40°53ʹ18ʺE 06.07.2005 40°38ʹ45ʺN, 4 Ç10 Büyükgöl Çoruh River 2980 h a rd , g r av e l U O 19.08.2005 40°53ʹ36ʺE 40°38ʹ53ʺN, 5 Ç11 19.08.2005 Altgöl Çoruh River 2950 hard, gravel UO 40°53ʹ40ʺE 08.07.2005 40°43ʹ11ʺN, 6 F08 Lake Atmeydan Fırtına Stream 2910 peat UO 21.08.2005 40°54ʹ01ʺE 08.07.2005 40°43ʹ06ʺN, 7 F10 İncegöl Fırtına Stream 2915 peat UO 21.08.2005 40°54ʹ23ʺE 08.07.2005 40°43ʹ22ʺN, 8 F09 Kumlugöl Fırtına Stream 2860 peat, ground soft UO 21.08.2005 40°54ʹ17ʺE 40°43ʹ11ʺN, 9 F12 21.08.2005 Lake Altkapılı Fırtına Stream 3000 peat O 40°54ʹ57ʺE Lake 40°43ʹ00ʺN, 10 F11 21.08.2005 Fırtına Stream 3000 hard, vegetation UO Büyük Kapılı 40°54ʹ54ʺE 09.07.2005 40°44ʹ58ʺN, 11 F03 Lake Çermeş Fırtına Stream 2780 gravel, stones UO 22.08.2005 40°52ʹ09ʺE 40°44ʹ37ʺN, 12 F02 22.08.2005 Çermeş Karagöl Fırtına Stream 2990 gravel, stones UO 40°52ʹ04ʺE 40°44ʹ25ʺN, 13 F01 22.08.2005 Lake Keçi Fırtına Stream 3070 gravel, stones UO 40°51ʹ50ʺE 11.07.2005 40°52ʹ28ʺN, 14 F16 İsimsizgöl Fırtına Stream 2890 mud, stones UO 24.08.2005 41°09ʹ46ʺE 11.07.2005 40°52ʹ09ʺN, 15 F14 Lake Büyükdeniz Fırtına Stream 2900 mud, stones O 24.08.2005 41°09ʹ42ʺE 40°51ʹ49ʺN, 16 F15 24.08.2005 Lake Meterez Fırtına Stream 2990 stones, sand M 41°09ʹ45ʺE 40°52ʹ42ʺN, 17 F17 24.08.2005 Lake Karadeniz Fırtına Stream 2770 stones O 41°10ʹ03ʺE 40°53ʹ44ʺN, 18 F18 29.07.2006 Lake Ceymakcur Fırtına Stream 2650 stones O 41°11ʹ30ʺE 40°56ʹ13ʺN, stones, in places 19 F19 30.07.2006 Büyükgöl Fırtına Stream 2670 O 41°12ʹ02ʺE sand

61 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

Table 1. Continued.

Station Sampling Altitude Substratum types Trophic Code Lakes Basins Coordinates numbers dates (m) scale

40°49ʹ24ʺN, 20 F13 31.07.2006 Lake Kıblekaya Fırtına Stream 2870 sand-mud O 41°06ʹ06ʺE 40°49ʹ21ʺN, sand-mud-gravel- 21 F06 01.08.2006 Lake Sırpal Fırtına Stream 2940 O 40°53ʹ40ʺE stones 40°49ʹ17ʺN, 22 F07 01.08.2006 Lake Çahberik Fırtına Stream 2810 sand-mud O 40°54ʹ09ʺE 40°37ʹ02ʺN, 23 Ç02 19.08.2005 Lake Dağbaşı Çoruh River 2710 hard, gravel M 40°46ʹ47ʺE 40°31ʹ19ʺN, sand-mud-gravel, in 24 İ07 02.08.2006 Lake Akçaağıl İyidere 2940 O 40°30ʹ40ʺE places stones 40°39ʹ31ʺN, sand-mud-gravel- 25 İ10 03.08.2006 Lake Çitrik İyidere 2850 O 40°46ʹ59ʺE stones 40°43ʹ28ʺN, sand-mud-gravel- 26 İ11 03.04.2006 Lake Salar İyidere 2820 O 40°52ʹ09ʺE stones 40°39ʹ13ʺN, 27 Ç03 04.08.2006 Lake Batıaksu Çoruh River 3050 sand, stones O 40°50ʹ39ʺE 40°39ʹ19ʺN, 28 Ç04 04.08.2006 Lake Kuzeyaksu Çoruh River 3070 sand, stones O 40°50ʹ57ʺE 40°39ʹ09ʺN, 29 Ç05 04.08.2006 Lake Doğuaksu Çoruh River 3120 sand, stones, rock O 40°51ʹ06ʺE 40°33ʹ28ʺN, gravel, stone, in 30 İ01 20.08.2006 Dipsizgöl İyidere 2670 O 40°28ʹ25ʺE places mud 40°33ʹ11ʺN, 31 İ04 20.08.2006 Lake Hatalan İyidere 2810 silt, mud, stones, UO 40°29ʹ24ʺE 40°33ʹ16ʺN, 32 İ03 20.08.2006 Lake Küçükhatalan İyidere 2800 silt, mud, stones, UO 40°29ʹ22ʺE 40°33ʹ39ʺN, 33 İ06 20.08.2006 Lake Sivrinin İyidere 2700 rock, silt UO 40°29ʹ52ʺE 40°33ʹ36ʺN, 34 İ05 20.08.2006 Lake Küçüksivri İyidere 2710 rock, silt UO 40°29ʹ50ʺE 40°34ʹ06ʺN, 35 İ08 21.08.2006 Lake Katreç İyidere 2700 rock, silt O 40°34ʹ51ʺE 40°34ʹ13ʺN, 36 İ09 21.08.2006 Lake Küçükkatreç İyidere 2690 rock, silt UO 40°34ʹ58ʺE 40°49ʹ07ʺN, 37 Ç12 23.08.2006 Lake Deniz Çoruh River 3370 rock, silt, stones UO 41°09ʹ39ʺE 40°50ʹ20ʺN, 38 Ç13 24.08.2006 Lake Kartal Çoruh River 2940 in places rock UO 41°18ʹ04ʺE 40°50ʹ22ʺN, 39 Ç14 24.08.2006 Lake Devise Çoruh River 2935 silt, stones UO 41°18ʹ12ʺE

62 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

Table 1. Continued.

Station Sampling Altitude Substratum types Trophic Code Lakes Basins Coordinates numbers dates (m) scale

Kabisra 41°09ʹ28ʺN, 40 K01 25.08.2006 Arhavi Karagöl 2660 rock, silt O Stream 41°24ʹ19ʺE 40°37ʹ14ʺN, 41 S01 26.08.2006 Uzungöl Solaklı Stream 1100 mud O 40°17ʹ44ʺE 40°31ʹ34ʺN, rock, stones, pieces 42 İ02 25.07.2007 Lake Koyun İyidere 3010 UO 40°28ʹ58ʺE of rock 40°38ʹ51ʺN, 43 Ç06 26.07.2007 Ortagöl Çoruh River 2960 stones, mud, sand O 40°52ʹ09ʺE 40°31ʹ39ʺN, 44 S05 27.07.2007 Lake Aygır Solaklı Stream 2710 mud, sand, stones M 40°23ʹ28ʺE 40°31ʹ54ʺN, 45 S04 27.07.2007 Lake Balık Solaklı Stream 2570 mud UO 40°23ʹ01ʺE 40°31ʹ58ʺN, 46 S09 28.07.2007 Lake Buz Solaklı Stream 3040 mud O 40°27ʹ36ʺE 40°31ʹ41ʺN, 47 S07 28.07.2007 Büyükyayla Karagöl Solaklı Stream 2930 mud UO 40°27ʹ03ʺE 40°32ʹ00ʺN, 48 S08 28.07.2007 Lake Pirömer Solaklı Stream 2870 mud UO 40°27ʹ09ʺE 40°31ʹ30ʺN, 49 S03 29.07.2007 Multat Karagöl Solaklı Stream 2800 mud UO 40°21ʹ46ʺE 40°31ʹ15ʺN, 50 S06 29.07.2007 Lake Sarıçiçek Solaklı Stream 2880 mud UO 40°24ʹ21ʺE 40°31ʹ46ʺN, 51 S02 30.07.2007 Lake Kırklarcami Solaklı Stream 2740 mud, coarse rock UO 40°20ʹ06ʺE 40°30ʹ36ʺN, 52 Ç01 30.07.2007 Göloba Çoruh River 2540 mud UO 40°19ʹ12ʺE 41°02ʹ19ʺN, 53 F20 22.08.2007 Lake Tobamızga Fırtına Stream 2620 sand-mud UO 41°15ʹ37ʺE 41°02ʹ08ʺN, 54 F21 22.08.2007 Lake Küçük Tobamızga Fırtına Stream 2630 sand-mud UO 41°15ʹ39ʺE 40°59ʹ24ʺN, sand-mud, in places 55 F22 23.08.2007 Büyük Çift egöl Fırtına Stream 2600 UO 41°15ʹ41ʺE rocks 40°59ʹ36ʺN, sand-mud, in places 56 F23 23.08.2007 Küçük Çift egöl Fırtına Stream 2550 UO 41°15ʹ49ʺE rocks 40°49ʹ28ʺN, 57 F05 25.08.2007 Lake Büyük Balıklı Fırtına Stream 2990 mud, few stones UO 40°52ʹ51ʺE 40°49ʹ17ʺN, 58 F04 25.08.2007 Lake Kayakaynak Fırtına Stream 3080 stones, mud UO 40°52ʹ43ʺE sand-mud, in places 40°34ʹ34ʺN, 59 M01 26.08.2007 Lake Çakır Maçka Stream 2530 rocks, gravel, many UO 39°41ʹ26ʺE macrophytes

63 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

Ardeşen BLACK SEA K01

Çayeli F20 F21 RİZE F23 F22

TRABZON F19

Kalkandere F18 F17 F16 F15 F14 Ç13 F06 F05 F13 Ç12 F04 F07 F03 F01 F02 F10 F11 İ11 F12 F08 F09 Ç03 Ç04 Ç07 İ10 Ç08 Ç10 Ç05 Ç11 N Ç06 Ç09 S01 Ç02 İ08 İ05İ06 İ01 İ03 İ09 M01 S07 İ04 S03 S05 S08 S09 S02 İ07 40 km S04 İ02 Ç01 S06 Figure 1. Map of 59 sampling stations associated with 6 drainage basins in the Eastern Black Sea Range in Turkey, where surveys for aquatic oligochaetes were conducted in 2005, 2006, and 2007. Ç = Çoruh River Basin, F = Fırtına Stream Basin, İ = İyidere Basin, K = Kabisra Stream Basin, S = Solaklı Stream Basin, M = Maçka Stream Basin. in CMCP 10 solution. Specimens were identifi ed Th e statistical signifi cance of the relationship between using the keys and other distributional information all species and all variables was tested with a Monte presented by Brinkhurst and Jamieson (1971), Carlo permutation test using 199 permutations. Rare Brinkhurst and Wetzel (1984), Sperber (1948, 1950), species were downweighted, and taxa encountered Nielsen and Christensen (1959), Timm (1999), and in only one sample were excluded to reduce Timm and Veldhuijzen van Zanten (2002). multicollinearity (ter Braak and Barendregt, 1986; ter Braak, 1995). A clustering analysis of the unweighted Data analyses pair-group method with arithmetic mean (UPGMA) Faunistic and environmental data were analyzed was conducted using the MultiVariate Statistical by canonical correspondence analysis (CCA) aft er Package (MVSP) version 3.1 (Kovach, 1998), in order testing the data with detrended correspondence to identify diff erent taxonomic assemblages among analyses (DCA). During the CCA progress in the the species at each sampling site. Th e relationship CANOCO program (ter Braak, 1989), we selected 59 between the total number of individuals and stations, those from which species had been collected environmental measurements was determined by a at least twice during this study. Th is method permits simple analysis of variance (ANOVA) test. the construction of theoretical variables (ordination axes) that best fi t the species data according to a Results unimodal method of ordination (ter Braak, 1987). In order to eliminate or reduce the eff ect of the Qualitative analysis skewness of the data, we log-transformed [ln (x + 1)] During the 2005, 2006, and 2007 sampling periods, all environmental variables, with the exception of pH. 8721 individuals belonging to 15 genera and 28 taxa

64 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

[19 taxa from Naididae, 9 of which are in subfamily seen in the lower right quadrant of the ordination Tubifi cinae (according to Erséus et al., 2008); 5 taxa diagram in Figure 2. from Enchytraeidae; 3 species from Lumbriculidae; According to the UPGMA analysis, the studied and 1 species from Haplotaxidae] were collected. lakes were clustered into 8 groups. Th e most A list of the 28 oligochaete taxa collected from the important ecological parameter in determining these study area is given in Table 2. Spirosperma ferox (in groups seemed to be elevation, because the montane 6 basins at 48 stations), Tubifex tubifex (in 6 basins lake was placed toward the upper side while the at 33 stations), and Stylodrilus parvus (in 6 basins alpine lakes were toward the lower side (Figure 3). at 21 stations) were the dominant species. Among these, 20 taxa were new records for the study area. According to ANOVA test results for the data In all samples, the Naididae dominated (68% of the collected during surveys of aquatic oligochaetes at 59 specimens; subfamily Naidinae, 36%, and subfamily stations, a signifi cant correlation was found between Tubifi cinae, 32%) (Table 2). the total numbers of individuals and altitude (P < 0.05; F = 2.994). Regarding the species diversity of the stations, station 44 (Lake Aygır) had the highest species richness (9 species), followed by stations 11, 20, Discussion 31, 41, and 52 (Lake Çermeş, Lake Kıblekaya, Lake Alpine lakes are among the most remote and Hatalan, Uzungöl, and Göloba, respectively), each undisturbed aquatic environments in Europe. In with 8 species. Th ere were no oligochaete species general, those at higher elevations are considered to observed at stations 2, 13, 29, or 55. be pristine, as they are less infl uenced by pollution Environmental variables from agriculture and wastewater than those at lower Some physicochemical measurements, according elevations (Füreder et al., 2006). to station, are presented in Table 3. Glacial and tectonic lakes on mountains of high Statistical analysis elevation are diffi cult to reach because of the rough In the ordination procedure, 7 environmental terrain. Consequently, the studied lakes are not yet variables were used. Variables aff ecting species exposed to anthropogenic pollution. distribution were, in order of importance according Oligochaete communities in high mountain lakes to CCA, elevation, water depth, dissolved oxygen, and ponds include species with various ecological and temperature (Figure 2). demands, both narrow and wide (Dumnicka and Th e CCA involved 7 environmental variables with Galas, 2002). Dumnicka and Galas determined 1 nominal variable (habitat type) and 6 selected taxa that oligochaete species from high mountain ponds that showed wide distribution in 59 samples (Figure and lakes can be grouped ecologically as follows: 1) 2). Accordingly, CCA was able to explain 90.6% of species known almost exclusively in high elevation the species-environment relationships with about lakes and ponds, 2) opportunistic species, 3) cold- 48.4% variance (Table 4). stenothermic species, and 4) semiaquatic species. While oligochaetes are common invertebrates in Th e fi rst ordination axis refl ected a gradient mostly high mountain streams, they are rarely the dominant related to temperature (Figure 2). Forward selection group in ponds and lakes located immediately with Monte Carlo permutation tests indicated that adjacent to these streams (Lencioni et al., 2004). elevation was the main environmental variable associated with assemblage composition (P < 0.05; Due to the high elevation and cold water F = 5.99). Th e second ordination axis indicated that temperatures of the lakes investigated during this water depth, as the second most important factor (P study, overall species diversity was low; a similar < 0.05; F = 1.84), had the next largest eff ect on the distribution pattern was observed for oligochaete occurrence of species. Th e remaining environmental communities in these lakes. Oligochaete species variables had relatively small eff ects on species found in the Eastern Black Sea Range show similarities composition. Th e species related to temperature are to those found in previous studies of other European

65 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey 21 4 4 1 51 45 62 42292 34 of aquatic oligochaete species collected from 59 stations in high-elevation lakes in the Eastern Black Sea Range of Turkey in in the Eastern Sea Turkey lakes Black of Range in high-elevation 59 stations species from collected oligochaete aquatic of 12345678910111213141516171819202122232425262728 -2 (Levinsen, 1884) 1 Claparede, 1862 Claparede, (Vejdovsky, 1878)(Vejdovsky, 1 (Gruithuisen, 1828) (Gruithuisen, (Müller, 1774)(Müller, 1 9 15 1 11 2 2 3 3 5 3 2 2 1 1 (Müller, 1774) (Müller, Claparede, 1862 Claparede, 1 1 5 (Michaelsen, 1889) (Michaelsen, 1 9 3 6 4 2 13 1 1 (Southern, 1909) (Southern, 5 10 5 (Piguet, 1906)(Piguet, 11 1 29 1 62 8 12 (Ørsted, 1842) (Ørsted, . (Hrabe & Cernosvitov, 1927) & Cernosvitov, (Hrabe 1 Kowalewski, 1914 Kowalewski, Piguet, 1906 Piguet, Kowalewski, 1919 Kowalewski, 8 13 26 (Eisen, 1879) 117 10 3 445 293 136 305 5 3 77 51 47 155 43 28 20 44 168 2 10 116 365 30 sp Michaelsen, 1908 Michaelsen, Piguet, 1906 Piguet, meisteri . (Müller, 1774) (Müller, 15 2 7 4 3 38 15 338 46 3 5 1 1 Piguet, 1906 Piguet, sp Müller, 1774Müller, 6 1 4 Piguet, 1906 Piguet, 29 12 2005, 2006, and 2007. 2005, 2006, and . . sp sp . sp Chaetogaster Chaetogaster templetoni Ilyodrilus Ophidonais serpentina serpentina Ophidonais diaphanus Chaetogaster ferox Spirosperma hoff Limnodrilus tubifex Tubifex montanus Tubifex nerthus Tubifex Tubifex Uncinais uncinata uncinata Uncinais Aulodrilus pluriseta pigueti Aulodrilus Stylodrilus parvusStylodrilus Stylodrilus heringianus variegatus Lumbriculus Cognettia sphagnetorum glandulosa Cognettia Henlea Mesenchytraeus armatus Mesenchytraeus Taxa Station Taxa simplex Nais Nais elinguis pardalis Nais Nais pseudobtusa pseudobtusa Nais Nais communis Nais Table 2. List and mean individual numbers m numbers individual mean 2. List and Table

66 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK 28 9 17 5 59 14 4 3 11 1 23 32 200 4 6 12 17 123 12 16 10 2 28 128236 114 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 (Levinsen, 1884) 1 Claparede, 1862Claparede, 2 386 (Vejdovsky, 1878)(Vejdovsky, 2 (Gruithuisen, (Gruithuisen, (Müller, 1774)(Müller, 5 11 2 2 14 2 15 60 10 12 (Müller, 1774)(Müller, 3 Claparede, 1862 Claparede, 33 5 18 6 (Hartmann, 1821) (Hartmann, (Michaelsen, 1889) (Michaelsen, 3 13 7 18 158 69 5 2 12 (Southern, 1909) (Southern, 3 15 8 (Piguet, 1906)(Piguet, 1 27 17 18 31 4 21 2 (Ørsted, 1842) (Ørsted, 3 . (Hrabe & Cernosvitov, & Cernosvitov, (Hrabe Kowalewski, 1914 Kowalewski, Piguet, 1906 Piguet, Kowalewski, 1919 Kowalewski, 13 3 1 88 12 2 2 (Eisen, 1879) 155 9 135 385 97 26 1 39 15 246 6 3 311 229 408 58 173 111 41 186 145 2 27 59 34 43 sp Michaelsen, 1908Michaelsen, 1 1 Piguet, 1906 Piguet, meisteri . (Müller, 1774) (Müller, 15 45 8 6 18 9 45 5 2 23 130 66 19 21 6 2 18 2 46 Piguet, 1906 Piguet, sp Müller, 1774Müller, 2 1 9 72 8 Piguet, 1906 Piguet, 1 3 . . sp sp . sp Henlea gordioides Haplotaxis 1828) Nais simplex simplex Nais Nais elinguis pardalis Nais pseudobtusa Nais Nais communis Nais serpentina Ophidonais diaphanus Chaetogaster Chaetogaster Uncinais uncinata uncinata Uncinais Ilyodrilus templetoni Ilyodrilus Spirosperma ferox Spirosperma hoff Limnodrilus tubifex Tubifex montanus Tubifex nerthus Tubifex Tubifex Aulodrilus pluriseta pigueti Aulodrilus Stylodrilus heringianus variegatus Lumbriculus Cognettia sphagnetorum Stylodrilus parvusStylodrilus 1927) Cognettia glandulosa Cognettia Mesenchytraeus armatus Mesenchytraeus Table 2. Contunied. Table

67 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey ) −1 (μg L

2 SiO ) −1 -P −3 4 (μg L PO ) −1 -N - 4 (μg L NH ed oxygen, nd = not detected. nd = not ed oxygen, ) −1 -N - 3 (μg L NO ) −1 -N - 2 (μg L NO )

−1 +2 Mg (mg L (mg )

−1 +2 Ca (mg L (mg ) −1 T. hard. T. (mg L (mg ) −3 −1 HCO (mg L (mg ) −1 Cond. (μs cm ) −1 L

DO (mg pH Water depth (m) (°C) Temp. 11 2.52 20.93 18.73 8.1 8.1 2.54 20.3 4.44 8.025 3 4.1 9.82 18.2 4.16 9.44 18.7 96 7.9 7.92 1.0 12.5 1.07 9.11 5.3 16.3 2.87 36.7 9.3 13.6 3.7 7.778 46 8.86 6 3.7 118 72 8.94 17.1 10.19 3 33.2 7.72 67.1 6 15 54.9 9.34 6.6 43 3 14.2 0.8 61 9.7 43 7.61 61 40 0.8 5.8 46 8.5 40 8.85 64 7.62 61 9.7 17.8 40 54.9 9.04 8.02 30 9.24 6.6 40 7.6 61 8 22.4 61 42.7 60 6.2 4.86 8 40 6.3 8.02 18.6 44 54.9 4.9 40 48.8 60 33 40 8 1.12 8.02 31 4.9 4.86 54.9 48.8 60 0.37 8 40 8.02 8 4.86 9.7 58.7 61 0.74 0.7 48.8 40 60 8 6.9 8.02 4.86 4.9 9.7 0 0.74 6.13 42.5 60 40 8.02 9.4 8 9.7 4.86 1.49 0.74 47 0.74 31.9 5.47 43.75 0.68 4.86 16 8 46.3 1.49 2.23 9.7 20.62 17.5 10.89 10 1108.11 0 34 1.09 2.6 4.9 4.9 8.76 49.37 1.86 33.35 8.1 53.8 1.09 1033.84 49.7 0.74 25.62 4.38 915 1.49 1203.2 18.38 4.38 56.9 33.3 3.28 1117.02 25.86 3.28 43.7 790.2 41.9 4.38 1604.2 47.6 5.47 861.5 3.28 1351.7 27.2 1185.35 40.2 3.28 1604.2 1330.92 9.85 8.76 1628 1841.9 903.1 1011 14.911 8.712 3.7 6.313 13.8 6.214 17.2 6.214 8.96 32.7 19.615 7.53 12.3 19.515 5.7 8.82 12.6 3.1 8.316 10.1 16.5 3.1 9.2517 6.3 15.1 16 5918 7.96 5.5 15.1 40.7 17 5.719 8.2 7.76 6.120 0.5 44 6.6 12.2 8.51 39 48.8 11.521 54.9 5.6 34 16.5 8.7 1.522 9.08 10.2 13.5 18 6.323 9.71 48.8 18.1 3.2 40 42.724 12 8.09 40 48.5 17.4 7.2 8.05 6125 0.7 7.1 48.8 51 16.1 0.5 7.84 60 9.4 15.1 8 2.9 60 8.02 8.4 54.9 54.9 79 8.12 2.5 40 29 8.14 40 8 67.1 14 8 45.4 8.74 4.86 37.6 16 4.9 7.6 60 40 6.9 48.8 8 8 8.02 73.2 33.7 7.63 5.8 60 36.6 9.7 3.35 77.5 42.7 4.9 1.12 6.8 8.02 16 82.5 60 4.86 7.8 4.9 86 42.7 60 16 2.98 40.62 60 56.5 2.23 4.86 61 40 35 4.9 49.2 2.23 8 61 1.49 16 60 48.8 4.9 16 30 0 3.35 24.4 33.1 8 80 1.49 23.1 24.4 6.87 9.7 60 4.9 60 16 1.49 60 4.9 51.25 60 4.38 49 32 4.9 24 6.90 4.38 80 8.85 2.23 16 0.74 4.9 49.40 51.7 16 1.12 2.04 16 1657.71 4.9 12.90 nd 5.47 4.38 998.2 24 3.28 38.1 4.9 23.10 88.1 nd 3.28 4.9 10.95 75.6 4.9 4.38 nd 2516.3 2251.9 95 4.9 796.17 11.6 0.74 5.47 9.5 0.37 2121.2 1336.86 40 6.8 1.49 805.1 33.1 2.23 44.2 9.85 26.9 1592.3 13.7 5.47 32.7 6.57 73.1 8.2 30.6 6.57 1666.6 20.4 44.2 1642.9 6.57 10.9 923.9 5.47 nd 1363.6 5.47 9.85 1693.4 5.47 1574.5 7.66 1925.1 1429 2281.6 1672.6 Sta. no. Sta. Table 3. Physicochemical features of stations in 2005, 2006, and 2007. Temp. = temperature, Cond. = conductivity, DO = dissolv = conductivity, Cond. = temperature, 3. Table 2007. Temp. in 2005, 2006, and stations of features Physicochemical

68 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK ) −1 (μg L

2 SiO ) −1 -P −3 4 (μg L PO ) −1 -N - 4 (μg L NH ) −1 -N - 3 (μg L NO ) −1 -N - 2 (μg L NO )

−1 +2 Mg (mg L (mg )

−1 +2 Ca (mg L (mg ) −1 T. hard. T. (mg L (mg ) −3 −1 HCO (mg L (mg ) −1 Cond. (μs cm ) −1 L

DO (mg pH Water depth (m) (°C) Temp. 2627 1728 16.729 17.930 2.5 17.8 7.531 15.932 3 15.5 8.1 2033 7.76 1434 2 7.65 13.135 4 6.95 8 7.3 12.436 0.8 7.45 11.4 1.5 7.137 6.9 6.96 12.3 38.238 1 37.2 7.14 14.3 6.5 7.339 7.34 37.2 6.8 1840 1 14.6 20.5 7.5 36.6 7.6 49 36.641 7.4 8.4 44 19.741 2.8 30.5 32 7.41 20.8 24.441 1 8.4 7.34 33 100 18.3 8.6 80 39.342 9 7.93 30.5 18.6 6.943 9 100 7,3 7.54 30.5 30.5 13.6 100 6.944 99.1 24 7.55 30.5 14.7 24 6.9 30.5 7.545 7.54 32.1 80 35.7 6.6 10 1846 36.3 7.64 32.1 30.5 80 19.4 6.1 1047 30.5 9.7 7.92 56.9 8.3 4.9 80 13.3 8048 4.9 13 7.43 19.7 16 6.3 24.4 15.1 4.5 4.9 24.449 7.73 60.7 16 6.8 80 13.8 17.2 106.6 5.2150 60 30.5 1.49 24 16 7.7 16.5 14.6 7.44 108.0 3.3551 8.01 9.7 24.4 6.4 80 2.23 16.5 17.2 121.8 7.63 8052 9.7 18.3 24 73.2 24.9 79.4 8.3 40 7.31 6.153 24.9 33.1 60 4.9 9.7 6.5 61.0 20.6 5.2 21 7.5354 0.37 40 33 7 24 73.2 105 24 18 7.4155 4.9 4.1 6.9 60 nd 27.2 80 106.9 4.9 19.1 25.4 36.6 1656 24.5 6.5 7.48 nd 140 nd 3 10.5 23.857 24.7 nd 8 7.3 4.9 3.5 140 42.7 7.96 4.9 23.1 23.8 11.5 1658 1 nd 27.5 6.57 16 48.8 6.5 1.49 16.03 26.4 13.5 4.9 6.5 42.7 60 7.6659 7.22 27.5 25.6 6.57 7.37 16.03 48.9 8.1 14 42.7 6 0.37 4.9 61.3 0.74 60 7.66 42.7 6.75 13.5 4.9 24.32 11 25.4 9.7 24.4 29.9 1601.3 7.53 5.9 60 79.4 8.02 36.6 0.37 80 2225.1 24.32 5.9 27.9 46.6 1 1785.5 49 36.6 7.59 100 6.2 10 0.37 8.02 86.2 9.85 66.9 2.60 724.9 7.1 80 9 16.03 36.8 nd 36.6 9.73 19.1 3.28 nd 19.1 8.02 26.9 2.60 80 5 6.8 7.82 2.19 24.05 42.7 7.85 18.3 9.73 60 3.28 10.9 7.5 24.05 36.6 258.5 4.86 18.12 8.8 6.3 2.23 42.7 14.59 60 2.19 24.05 2.5 701.1 18.12 7.66 50.6 36.6 39.4 9.73 6 6.7 805.1 40 8.02 2.6 36.6 nd 4.86 3.28 34.71 66.5 36.6 918 2.6 10.2 1.86 3.28 4.86 8.02 74.37 60 37.43 790.2 2.98 58.8 104 745.7 nd 80 36.6 43 9.73 8.02 5.21 80 52.5 3.28 4.38 36.6 745.7 80 4.38 9.73 57.5 4.09 11.57 52.5 8.02 466.4 6.57 8.02 45.62 24.4 7.66 100 4.86 4.84 5.47 36.6 56.87 8.02 28.58 1185.3 674.32 8.02 100 3.72 9.73 21.78 2.19 534.7 25.18 30 14.59 698.09 16.03 24.5 1758.7 80 2.6 38.12 14.59 677.3 25.86 100 14.59 5.47 16.03 23.12 2.98 9.85 14.59 3.28 362.41 1.12 23.14 16.03 7.66 36.07 1.12 8.02 31.87 14.59 1.09 2.23 493.12 49.68 1.86 79.37 591.15 13.75 629.76 9.73 1.09 19.46 1.09 341.62 18.12 33.35 1.86 350.53 24.37 2.19 39.47 21.87 63.29 1.86 442.62 1.49 64.66 2.19 353.5 14.97 25 34.03 4.38 653.53 5.47 18.75 13.75 4.38 552.53 3.28 23.14 2.19 751.56 273.29 23.14 27.22 570.35 2.19 555.5 305.97 4.38 4.38 404 626.79 380.23 Sta. no. Sta. Table 3. Table Contunied.

69 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

3 Limn hof high-mountain lakes (Dumnicka and Galas, 2002; Tubi tub Ophi ser Milbrink et al., 2002; Lencioni et al., 2004; Kownacki Lumbri v et al., 2006; Krno et al., 2006). Wdepth Elev. D.O. Temp. Using the trophic scale based on mean Spiro fe concentrations of total phosphorus (TP) measured in -2 Aulo plu -2 12 the study area (Catalan et al., 2006), 56% of the lakes (33 lakes) could be classifi ed as ultraoligotrophic (TP Figure 2. CCA diagram with selected environmental variables −1 and the dominant oligochaetes present at 59 stations < 4.7 μg L ) [see Materials and Methods; units were associated with high-elevation lakes in the Eastern for L−1], 36% oligotrophic (23 lakes) (4.7 < TP < 9.3 Black Sea Range of Turkey in 2005, 2006, and 2007. μg L−1), and 8% mesotrophic (3 lakes) (9.3 < TP < 31

Table 4. Results of canonical correspondence analysis (CCA) from data collected during surveys for aquatic oligochaetes at 59 stations in high-elevation lakes in the Eastern Black Sea Range of Turkey in 2005, 2006, and 2007.

Axes 1 2 3 4 Total inertia Eigenvalues 0.353 0.145 0.090 0.057 2.726 Species-environment correlations 0.906 0.673 0.444 0.457 Cumulative percentage variance of species data 13.0 18.3 21.6 23.7 of species-environment relations 48.4 68.2 80.5 88.4 Sum of all eigenvalues 2.726 Sum of all canonical eigenvalues 0.730

UPG MA 41 8 49 37 12 7 29 35 56 55 50 44 48 47 46 42 25 43 6 27 19 40 59 15 11 45 26 6 58 22 21 5 16 14 54 33 36 34 32 39 8 53 52 31 4 24 38 30 28 20 7 51 18 3 3 17 13 2 9 57 23 5 10 1 2 4 1 2.4 2.0 1.6 1.2 0.8 0.4 0 Euclidean Figure 3. UPGMA dendrogram illustrating the relationship of aquatic oligochaetes at 59 stations in high-elevation lakes in the Eastern Black Sea Range of Turkey, where surveys were conducted during 2005, 2006, and 2007.

70 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

μg L−1). Low values of chlorophyll-a measured in the western and northern Sweden, as well as in most of studied lakes also confi rm these fi ndings. Norway and Iceland, from lowland to high-elevation Naididae, the dominant family by number of taxa habitats (Milbrink, 1980, 1994). It is mainly known in this study, is one of the most important groups of as a species characteristic of heavily polluted waters, aquatic Oligochaeta. Most naidids are cosmopolitan where it can reach very high densities (Poddubnaya, and occur throughout the world (Martin et al., 2008). 1980). Milbrink (1983) claimed that T. tubifex Species of the subfamily Naidinae inhabit the water occurs in environments in which competition or column, submerged vegetation, and the surface of predation is weak (in Dumnicka and Galas, 2002). sediments, and they can be fairly active swimmers. Th is cosmopolitan species, although not commonly Th e tubifi coid Naididae (especially those taxa in encountered, is locally abundant in habitats of subfamily Tubifi cinae) represent the most diverse varying water quality, including pristine alpine and and widely distributed group of aquatic microdriles. subalpine lakes (Klemm, 1985); the bottoms of large, Th ey are commonly associated with sediments in unproductive, oligotrophic lakes; grossly polluted aquatic habitats. and organically enriched sites with low oxygen tensions; and aquatic habitats supporting few other Spirosperma ferox (Naididae, Tubifi cinae), species (Brinkhurst, 1996). In oligotrophic situations, present at 48 stations in 6 basins, was the dominant T. tubifex is generally a dominant species, occurring species in this study. It is a freshwater form widely together with S. ferox (Milbrink, 1980). Timm (1996) distributed throughout the Holarctic region, and also found this species in a small oligotrophic lake it is common particularly in northern cool-water in Estonia with Spirosperma ferox. Our fi ndings are bodies (Timm and Veldhuijzen van Zanten, 2002). consistent with these results. Th is species is an indicator of oligotrophy (Milbrink, Lumbriculidae is a thermophobe family of the 1987), most commonly associated with very fi ne northern temperate zone (Timm, 1980). It was sandy to silty substrates with a high organic matter represented by 3 species in this study (Lumbriculus content (Verdonschot, 2001). Dumnicka and variegatus, Stylodrilus parvus, and S. heringianus). S. Galas (2002) found this species to be dominant parvus, the third most dominant species in this study in the small high-mountain ponds in the Tatra (present at 21 stations in 6 basins), is a Palearctic Mountains of Poland. Th ese authors defi ned S. ferox species. It lives in various types of water bodies, as an opportunistic species. Th is species was also including lake bottoms, and is also common in frequently found in small, shallow lakes and in the mountain streams (Lencioni et al., 2004). In a study deep littoral areas of mountain lakes of the mountain of the oligochaete communities in mountain streams pine zone in the Western Tatras (Šporka, 1992) and of Poland, Dumnicka (1994) found that a third group other mountainous areas, including the Pyrenees of 5 streams was characterized by an oligochaete (Juget and Giani, 1974), Alps (Wagner, 1987), and fauna dominated by the Lumbriculidae. Among Rila Mountains (Uzunov and Varadinova, 2000). the determined taxa, S. parvus was the dominant According to Milbrink et al. (2002), in the profundal species along the entire length of the studied streams. zones of lakes characterized as oligotrophic, S. ferox According to Dumnicka and Galas (2002), the genus is dominant, either alone or together with Tubifex Stylodrilus, and probably also L. variegates, are cold- tubifex in about equal proportions. Th e same authors stenothermic species in the Tatra Mountains. L. noted that, in oligotrophic situations, T. tubifex is variegatus has very wide ecological valence (Timm, generally a dominant species, oft en together with S. 1970). ferox and Stylodrilus heringianus, and occasionally Stylodrilus heringianus, which was recorded as with a few additional species. Th is species community a new species for Turkey in one of the most recent is particularly common in waters at high elevations. studies (Yıldız et al., 2010), is considered to be the In this respect, the results of the present study are most reliable indicator of oligotrophic conditions similar to those of previous studies. in the Palaearctic region (Milbrink, 1980). It is Tubifex tubifex (present at 33 stations in 6 basins) a clean-water (Probst, 1987; Timm et al., 2001) is a characteristic species indicating oligotrophy in and cold-stenothermic species (Lang and Lang-

71 Distribution of aquatic oligochaetes (Annelida, Clitellata) of high-elevation lakes in the Eastern Black Sea Range of Turkey

Dobler, 1980; Dumnicka and Galas, 2002). It is negatively correlated with water depth and dissolved also an oligosaprobic species (Timm et al., 2001). oxygen. Limnodrilus hoff meisteri and Ophidonais L. variegatus and S. heringianus seem to have wider serpentina are negatively correlated with elevation ecological requirements; hence, they were also (Figure 2). encountered in other types of water bodies sampled Th e width and depth of the water body appeared in this study. to be the most important factors in the distribution Enchytraeidae is a cosmopolitan family. Th ey are of oligochaete species (Nijboer et al., 2004). Many found from the polar regions to the tropics, from researchers showed relationships between the the bottom of lakes and rivers to the bottoms of the oligochaete community and water depth (Collado oceans, in permanent ice (glaciers) or snow, and in and Schmelz, 2001; Nijboer et al., 2004). In our permafrost soils. Th ey also exist in abundance in study, multivariate analysis (CCA) showed that sewage trickle fi lter beds and pristine marine sands, the distribution patterns of oligochaete species and they occur in large numbers in water-logged assemblages are signifi cantly correlated with depth. soils and throughout the range of soil types, in all Probst (1987) and Särkkä (1987, in Peralta et al., but dry deserts (Wetzel et al., 2000). Enchytraeidae 2002) noticed that while L. hoff meisteri diminishes in was the best represented family in a recent study density with depth, T. tubifex increases in density in of the Eastern Black Sea Range (Yıldız et al., 2010). deeper water. Similarly, this family was most common in other In the UPGMA diagram (Figure 3), the percentage studies connected to high-mountain lakes (Manca of habitat similarity in environmental data from each et al., 1998; Rieradevall et al., 1998; Lencioni et al., sampling station was the highest between stations 2004). According to Dumnicka and Galas (2002), 22 and 21. Stations 58 and 16 were also found to be members of this family were considered semiaquatic similar to each other. In contrast, the oligochaete species, especially some species from the genera fauna associated with station 41 (Uzungöl) was the Mesenchytraeus, Cognettia, and Henlea. most diff erent from the other stations (Figure 3), Th ere have been very few attempts to defi ne and because the elevation of this lake is lower than the major variables aff ecting macroinvertebrate the others, it can be classifi ed as a montane lake; the distribution. Wathne et al. (1995), Fjellheim et other lakes are subalpine and alpine lakes (Oertli et al. (2000), and Boggero et al. (2005) identifi ed al., 2008). elevation as the most important factor infl uencing Th is study represents a pioneering contribution the distribution of species in remote alpine lakes to the research of oligochaete communities in the across Europe. Our fi ndings correspond very well glacial lakes of Turkey. Further research is needed, to this pattern. In addition to the eff ect of elevation, in Turkey and in other glacial regions, to address the other environmental parameters infl uenced the lack of information on the taxonomy and ecology of distribution of littoral macroinvertebrates in these this group of animals. lakes. Similar to previous studies, our study found that elevation is the most important factor infl uencing the distribution of oligochaete species in the Eastern Acknowledgements Black Sea Range (Figure 2). Th is project was supported by the Scientifi c Th e distribution of species along the fi rst axis and Technological Research Council of Turkey refl ects requirements associated with elevation and (TÜBİTAK, Project 104/Y/183). We are deeply temperature. Th e distribution of Spirosperma ferox grateful for their support. We would also like to is positively correlated with elevation and negatively thank Dr Süleyman Balık, Dr Hasan M. Sarı, Dr Cem correlated with water depth and dissolved oxygen. Aygen, Dr Ali İlhan, Dr Esat T. Topkara, and Mesut Tubifex tubifex and Lumbriculus variegatus are Kaptan for their invaluable support and help with negatively correlated with temperature and positively technical issues. We also thank Dr Mark J. Wetzel correlated with water depth (Figure 2). Aulodrilus (University of Illinois at Urbana-Champaign, Illinois, pluriseta is positively correlated with temperature and USA) for the linguistic revision of the manuscript.

72 S. YILDIZ, M. ÖZBEK, M. R. USTAOĞLU, H. SÖMEK

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