(Oligochaeta) and Leeches (Hirudinea) in the Ob’ River Basin

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Fauna, Spatial Distribution, and Ecological Peculiarities of Oligohaetes (Oligochaeta) and Leeches (Hirudinea) in the Ob’ River Basin

Article in Biology Bulletin · January 2020 DOI: 10.1134/S1062359019090085

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Евгения Николаевна Крылова Dmitry M. Bezmaternykh Institute for Water and Environmental Problems (IWEP) Institute for Water and Environmental Problems (IWEP)

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The user has requested enhancement of the downloaded file. ISSN 1062-3590, Biology Bulletin, 2019, Vol. 46, No. 9, pp. 1001–1011. © Pleiades Publishing, Inc., 2019. Russian Text © The Author(s), 2019, published in Zoologicheskii Zhurnal, 2019, Vol. 98, No. 6, pp. 605–615.

Fauna, Spatial Distribution, and Ecological Peculiarities of Oligohaetes (Oligochaeta) and Leeches (Hirudinea) in the Ob’ River Basin E. N. Krylovaa, * and D. M. Bezmaternykha, ** aInstitute for Water and Environmental Problems, Siberian Branch, Russian Academy of Sciences, Barnaul, 656038 Russia *e-mail: [email protected] **e-mail: [email protected] Received April 27, 2018; revised January 11, 2019; accepted January 13, 2019

Abstract—The fauna, spatial distribution, and ecological features of oligochaetes and leeches of reservoirs and watercourses of the Ob’ River basin (including Teletskoe Lake and Novosibirsk, Belovskoe, and Gile- vskoe reservoirs) have been considered. Published and original data were summarized from 1903 to 2016. Var- ious samplers were used: bottom grabs, scrapers and wash-off from the solid substrates. The assessment of the distribution of oligochaetes in the Ob’ River basin showed that oligochaeto and hirudofauna were formed mainly by eurybiont species, without significant zonal changes. The most common oligochaetes in the Ob’ River basin were Tubifex tubifex (Müller 1774), Limnodrilus hoffmeisteri Claparéde 1862, Spirosperma ferox Eisen 1879, Lumbriculus variegatus (Müller 1773), Stylaria lacustris (Linnaeus 1767), Nais variabilis Piguet. 1906, Chaetogaster diaphanus (Gruithuisen 1828), leeches, Glossiphonia complanata (Linnaeus 1758), Helob- della stagnalis (Linnaeus 1758), and Erpobdella octoculata (Linnaeus 1758). These species were the key components of benthic biocenoses of the water bodies and watercourses of the Ob’–Irtysh interfluve. The species diversity of oligochaetes and leeches in the Ob’ River basin was much less than that in the large basins of Europe (Volga River) and Eastern Siberia (Lake Baikal) and was comparable with the fauna of certain regions of Europe and the Urals. The largest number of species of oligochaetes and leeches was noted in the well- studied basins of the Upper and Middle Ob’ River.

Keywords: oligochaetes, leeches, Ob’ River, tributaries, Teletskoe Lake, Novosibirsk, Belovskoe and Gile- vskoe reservoirs, taxonomic composition, distribution, ecology DOI: 10.1134/S1062359019090085

INTRODUCTION and water bodies of the Upper Ob’ River basin are pre- The Ob’ River has a length of 4338 km. It crosses all conditioned by the significant variety of the natural of western Siberia and has about 2000 tributaries. The environment and the nature of use of its vast territory area of its basin is 2990000 km2 (Zapadnaya Sibir’, (Kirillov, 2001). 1963). Its average discharge is 12700 m3/s, and the Oligochaetes and leeches of the Ob’ River basin greatest is 42800 m3/s. In the middle reaches, the Ob’ have been studied much less than those of the basins of River has a depth of 20 m and a width of 3–4 km. This the European rivers. The first data appeared at the is a river of prolonged high water, which explains the beginning of the 20th century (Michaelsen, 1903; turbidity of the water due to suspension, leading to a Ioffe, 1947; Malevich, 1949), and the largest contribu- decrease in transparency down to 30 cm with low tion to these studies was made by an assistant professor salinity of the waters, as well as prolonged flooding of of Tomsk University, N.A. Zaloznyi (Zaloznyi, 1973, the dead arms of the river and the channels. According 1973a, 1979, 1979a, 1984, 2005, 2007; Zaloznyi and to the hydrological regime, the Ob’ River basin is Krylova, 1996; Zaloznyi and Vorob’ev, 2006). In 1996, divided into the Upper Ob’ River (down to Novosi- under his scientific supervision, studies of oligo- birsk Reservoir), the Middle Ob’ River (down to the chaetes and leeches of the Ob’ River basin began at the mouth of the Irtysh River), and the Lower Ob’ River Institute of Water and Environmental Problems, Sibe- (down to the Gulf of Ob’). The entire diversity of the rian Branch, Russian Academy of Sciences. rivers of the Ob’ River basin is subdivided into five This study aims to analyze the current state of the areas: mountain, steppe, swamp, tundra, and delta fauna (composition, spatial distribution) and the ecol- (Zhadin and Gerd, 1961). The features of the forma- ogy of oligochaetes and leeches in the water bodies and tion and functioning of the ecosystems of watercourses streams of the Ob’ River basin.

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Table 1. Volume of the material studied Years Number Publications with detailed Water bodies of sampling of samples description of the material Bol’shaya Cheremshanka River 1999 30 Bezmaternykh, 2008 Barnaulka River 1996–2000 300 Bezmaternykh, 2004 Tom’ River 2000, 2001, 2006 44 Koveshnikov and Krylova, 2002 Chumysh River 2001, 2011 30 Yanygina and Krylova, 2012 Izdrevaya River 2003 12 Bezmaternykh, 2007 Irtysh River 2001 30 Koveshnikov, 2014а Reservoir at Chernovoi Urop River 2014 9 Bezmaternykh and Krylova, 2014 Belovskoe Reservoir 2002, 2006, 2008 97 Yanygina et al., 2003; Kirillov et al., 2004 Gilevskoe Reservoir 2012 24 Bezmaternykh and Krylova, 2014, 2016 Novosibirsk Reservoir 2007, 2008 59 Krylova, 2012 Telestkoe Lake 1996–2002, 2004–2006 1512 Krylova, 2004, 2009, 2013 Tributaries of Telestkoe Lake 2006–2008 59 Koveshnikov, 2014 Bol’shoe Shchuch’e Lake 2016 28 Krylova and Koveshnikov, unpublished data Lakes and rivers of Ukok Plateau 2001 45 Krylova, 2003 Lakes and rivers of Yamal Peninsula 2015 30 Krylova and Koveshnikov, unpublished data

MATERIALS AND METHODS The basin of the Upper Ob’ River. Eighteen species of oligochaetes from four families and the worms Sampling was carried out in the tributaries of the belonging to family Enchytraeidae, which were not Ob’ River, and in the rivers, lakes, and reservoirs determined down to the species level, were identified belonging to its basin during the ice-free period. The in the zoobenthos of mountain lakes (Ukok Plateau) material for this study was original data obtained in of the Upper Ob’ River basin. The richest family of 1996–2016 (Table 1), as well as published data from Naididae comprised nine species. Among them there 1903–2018 (Michaelsen, 1903; Ioffe, 1947; Malevich, were phyto- and psammophiles (living on algae and 1949; Leshchinskaya, 1962; Chekanovskaya, 1962; sand, respectively, and eating algae and other fouling), Stal’makova, 1968, 1974; Dolgin et al., 1973; Zalo- phytophages, and predators. The other families were znyi, 1973, 1973a, 1979, 1979a, 1984, 2005, 2007; mainly represented by pelophiles and detritus feeders Timm, 1987; Popchenko, 1988; Priroda Yamala, 1995; (organisms living on silt and feeding on bacteria in the Prirodnaya Sreda Yamala, 1995; Zaloznyi and Kry- silt and detritus, respectively). Most species are tem- lova, 1996; Sharapova, 1998, 2007; Bogdanov, 2000; perature-indifferent, eurythermic, and characterized Sharapova and Abdullina, 2004; Nijboer et al., 2004; by a wide geographical range. Cold-water steno- Stepanov, 2005, 2006, 2008, 2014; Stepanova, 2009; therms, L. profundicola (Verrill 1871), Rh. altaianus Stepanova et al., 2011; Palatov and Chertoprud, 2012; Michaelsen 1935, B. lemani (Grube 1880), and H. gor- Fedorova, 2018). dioides (Hartmann 1821) have been also found; one The sampling and processing of the field data was species (Rh. altaianus) was endemic to this region. The carried out using standard hydrobiological methods largest number of species was found in the lakes of the (Rukovodstvo…, 1992). Key identifiers were used for Dzhulukul Depression (Krylova, 2003). taxonomic identification (Chekanovskaya, 1962; In the deep (323.3 m) mountain Teletskoe Lake, 21 Lukin, 1976; Opredelitel’…, 1994). species of oligochaetes have been found belonging to five families: Naididae, Tubificidae, Haplotaxidae, Lumbriculidae, and Lumbricidae (Krylova, 2009, 2013). RESULTS There were five species of leeches; the most common According to the published and original data, 76 species were G. complanata and E. octoculata. species of oligochaetes and 14 species of leeches have In Teletskoe Lake, as in the other deepest lakes been registered in the water bodies of the Ob’ River (Popchenko, 1988), the majority of oligochaetes spe- basin (Table 2). The list is not complete, since there cies, including all phytophilic Naididae, inhabited the are many unexplored reservoirs in the basin of the littoral, which was characterized by a variety of sedi- Middle and Lower Ob’ River. The Upper Ob’ River is ments and plant substrates. Single species of Naididae the most studied basin. (U. uncinata (Oersted 1842)), which were not related

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Table 2. Taxonomic composition and geographical and environmental characteristics of oligochaetes and leeches in the Ob’ River basin Taxons 1 2 3 4 5 UOMOLOINWS OLIGOCHAETA Family Aeolosomatidae Aelosoma hemprichi Ehrenberg 1828 v C Ph E zp, zb – + – – – Family Naididae Stylaria lacustris (Linnaeus 1767) v, ss HON Ph E zp, zb + + + + + Stylaria fossularis Leidy 1852 v H Ph E zp + + – – – Arcteonais lomondi (Martin 1907) v, ss, bwl, sed H PhD E zb, zp – + + + – Ripistes parasite (Schmidt 1847) v H PhD E zp, zb + + + – + Veydovskyella comata (Veydovsky 1883) ss, v H PhD E zb, zp + + – – – Veydovskyella intermedia (Bretscher 1896) ss, v H PhD E zb, zp – + – – – Vejdovskyella macrochaeta (Lastoc’kin 1921) ss, v H PhD E zb, zp – + – – – Dero obtusa d’Udekem 1855 sed, ss, v C PhD E zb, zp – + – – – Dero digitata (Müller 1773) sed, ss, v C PhD E zb, zp + + – – – Nais barbata Müller 1773 v, ss C PhD E zp, zb + + + – + Nais communis Piguet 1906 v, ss C PhD E zp, zb + + + – + Nais preudobtusa Piguet 1906 v, bwl H Ph E zp, zb + + + + + Nais variabilis Piguet 1906 v, ss C PhE zp, zb+++++ Nais bretscheri Michaelsen 1899 + + – – – Nais elinguis Müller 1773 bwl, ss C D Хс zp, zb + + – + – Nais pardalis Piguet 1906 v, ss C PhD E zp, zb + + – – – Nais behningi Michaelsen 1923 ss C PhD CWS zb – + – – – Nais sp. +–––– Ophidonais serpentina (Müller 1773) v, ss H Ph E zp, zb + + + + + Aulophorus furcatus (Müller 1773) sed C D E zb + + – – – Uncinais uncinata (Oersted 1842) v, ss P PhD E zb + + + + + Piguetiella blanci (Piguet 1906) v H Ph E zp – – + – – Specaria josinae (Veydovsky 1883) sed H D E zb – + – – – Homochaeta naidina Bretscher 1896 v, ss P Ph E zb + + + – – Paranais litoralis (Müller 1784) v C PhD E zp, zb – – + – – Paranais frici Hrabe 1941 v C PhD E zp, zb + + – – – Chaetogaster diaphanus (Gruithuisen 1828) v, sed C Pr E zp, zb + + + + + Chaetogaster diastrophus (Gruithuisen 1828) v C PhD E zp, zb + + – + – Chaetogaster langi Bretscher 1896 sed C PhD E zb + + + – + Chaetogaster setosus Svetlov 1925 sed H PhD E zb – + – – – Chaetogaster limnaei Baer 1827 sed H D, PrE zp, zb++++– Pristina aequiseta Bourne 1891 ss H PhD E zp, zb – + – – + Pristina foreli Piguet 1906 ss H PhD E zp, zb – + – – – Pristina longiseta Ehrenberg 1828 ss C PhD E zp, zb – + – – – Pristina bilobata (Bretscher 1903) v C PhD E zp, zb – + – – – Pristina sp. +–––– Slavina appendiculata (d’ Udekem 1855) v, sed C PhD E zp, zb + + – – + Amphichaeta leydigi Tauber 1879 v, sed H PhD E zp, zb – + – – – Bratislavia palmeni (Munsterhjelm 1905) ss H PhD E zp, zb – + – – –

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Table 2. (Contd.) Taxons 1 2 3 4 5 UOMOLOINWS Family Tubificidae Aulodrilus limnobius Bretscher 1899 sed H D E zb + + + – + Aulodrilus pluriseta (Piguet 1906) sed C D E zb + + + + – Rhyacodrilus coccineus (Vejdovsky 1875) sed C D E zb + + + – + Rhyacodrilus altaianus Michaelsen 1935 sed En D CWS zb + – – – – Rhyacodrilus lepnevae Malevich 1949 sed En D CWS zb + – – – – Limnodrilus profundicola (Verrill 1871) sed H D CWS zb + + + + + Limnodrilus udekemianus Claparéde 1862 sed H D E zb + + + + + Limnodrilus hoffmeisteri Claparéde 1862sed C D E zb +++++ Limnodrilus claparedianus Ratzel 1868 sed H D E zb ++++– Potamothrix hammoniensis (Michaelsen 1901) sed C D E zb + + + + – Psammoryctides albicola (Michaelsen 1901)sed H D E zb +++–– Psammoryctides barbatus (Grube 1861) sed H D E zb + + – – – Tubifex tubifex (Müller 1774) sed C D E zb + + + + + Tubifex ignotus (Štolc 1886) sed H D E zb + + + – – Spirosperma ferox Eisen 1879 sed H D E zb + + + + + Peloscolex inflatus (Michaelsen 1901) sed H D E zb – – + – – Peloscolex oregonensis Brinkhurst 1965 sed H D E zb – – + – + Ilyodrilus hammoniensis (Michaelsen 1901) sed H D E zb – + – – – Isochaetides michaelseni (Lastočkin 1936) sed H D E zb – – + – – Isochaetides sp. +–––– Alexandrovia onegaensis Hrabe 1962 sed H D E zb ––––+ Family Enchytraeidae Propappus volki Michaelsen 1915 sed H D E zb + – + + – Enchytraeus albidus Henle 1837 sed C D E zb – + – – – Enchytraeus sp. +–––– Fridericia sp. +–––– Marionina lobate (Bretscher 1899) sed H D E zb – + – – – Family Lumbriculidae Lumbriculus variegatus (Müller 1773) sed H D E zb + + + + + Stylodrilus heringianus Claparéde 1862 sed H D E zb – – + – – Rhynchelmis limosella Hoffmeister 1843sed H D E zb –++–– Rhynchelmis tetratheca Michaelsen 1920 sed H D E zb – + + – – Bythonomus lemani (Grube 1880) sed H D CWS zb + – – – – Family Lumbricidae Eiseniella tetraedra (Savigny 1826) sed H D E am + + – – – Lumbricus terrestris Linnaeus 1758 sed C D E am +* – – – – Family Haplotaxidae Haplotaxis gordioides (Hartmann 1821) sed H D CWS zb + – – – – Haplotaxis ascaridoides Michaelsen 1905 sed H D CWS zb + – – – – Pelodrilus ignatovi Michaelsen 1903 sed En D CWS zb + – – – – Total number of oligochaete species—76 – – – – – 50 56 35 20 22

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Table 2. (Contd.) Taxons 1 2 3 4 5 UOMOLOINWS HIRUDINEA Family Acanthobdellidae Acanthobdella peledina Grube 1851 bs P Par CWS – – – + + + Family Glossiphoniidae Glossiphonia complanata (Linnaeus 1758) v, ss H Pr E – + + + + + Glossiphonia heteroclita (Linnaeus 1761) v H Pr E – + + + + – Glossiphonia concolor (Apathy 1888) v, ss H Pr E – + + + – – Helobdella stagnalis (Linnaeus 1758) v, sed P Pr E – + + + + + Hemiclepsis marginata (O.F. Muller 1744) w, bs P Pr, E – ++++– Par Protoclepsis tessulata (O.F. Muller 1774) bs P Par E – + + – – – Family Ichtyobdellidae Piscicola geometra (Linnaeus 1761) v, bs P Par E – + + + + + Cystobranchus mammilatus (Malm 1863) bs P Par CWS – – + + + + Family Erpobdellidae Erpobdella octoculata (Linnaeus 1758) w P PrE – +++++ Erpobdella testacea (Savigny 1820) w, sed P Pr E – + + + + + Erpobdella nigricollis (Brandes 1899) v P Pr E – + + + – – Family Hirudinidae Hirudo medicinalis Linnaeus 1758 w, sed P, En Pr WW – +** – – – – Haemopis sanguisuga (Linnaeus 1758) w, sed P Pr E – + + – + – Total number of leech species—14 – – – – – 12 12 11 10 7 “+” Species found; “–” species not found; * sediment-dwelling species, enters into water bodies from the coastal zone; ** rare species, probably, temporary populations released by the local population for breeding in nature were found (Krasnaya kniga…, 2006). UO, Upper Ob; MO, Middle Ob; LO, Lower Ob; I, Irtysh; NWS, Northwestern Siberia; 1, biotope (v, vegetation; p, plankton; bwl, near- bottom water layer; ss, sediment surface; sed, in the sediment, bs, body surface; w, water); 2, type of distribution (C, cosmopolitan; H, Holarctic; P, Palaearctic; En, endemic; HON Holarctic–Oriental–Neotropic); 3, feeding type (Ph, phytophage; PhD, phytophage and detritus feeder; D, detritus feeder; Pr, predator; Par, parasite); 4, relation to temperature (E, eurytherm; CWS, cold-water stenotherm; WW, warm-water species); 5, ecological group (zb, zoobenthos; zp, zooperiphyton; am, amphibiont). to vegetation, penetrated into the sublittoral; there- prevailed (76%). When looking at the substrate prefer- fore, the number of species decreased sharply. Only six ences, four groups of oligochaetes were identified in species were recorded in the upper sublittoral zone Teletskoe Lake: phytophilic, psammophilic, pelo- (mainly eurytopic Tubificidae). Eight species were philic, and amphibiotic species. The phytophiles and found in the profundal with homogeneous sediments pelophiles made the main contribution to oligocha- and a low temperature: cold-water stenothermal, etocenosis (43% each). According to the food spectra, endemic, and eurybiotic (Krylova, 2004, 2013). The three groups of oligochaetes were noted: phytophages, complex T. tubifex–S. ferox–L. hoffmeisteri is charac- detritus feeders, and predators. Most of the species teristic of the lake. In different depth zones of the lake, (52%) were detritus feeders: representatives of the slight differences in the composition of the predomi- families Tubificidae, Haplotaxidae, Lumbriculidae, nant species were noted: it was S. ferox–T. tubifex in and Lumbricidae. The group of phytophages made up the littoral, T. tubifex–S. ferox–L. hoffmeisteri in the 43% of the total species number and included most of sublittoral, and T. tubifex–L. hoffmeisteri–Rh. lepne- the worms of the family Naididae, feeding on algae vae Malevich 1949 in the profundal. and protozoa from the fouling of solid substrates. The In the zoogeographical aspect, in the fauna of oli- presence of various biotopes (sand, stones, pebbles, gochaetes of Teletskoe Lake, four groups of oligo- silt, macrophytes) determined the development of the chaetes have been identified: cosmopolitan, Holarc- diverse fauna of oligochaetes in this reservoir. tic, Palearctic, and endemic. The core of the fauna was In oligochetocenoses of the Biya River basin (river formed by Holarctic (33%) and Palearctic (29%) spe- flows from Teletskoe Lake), 12 species of oligochaetes cies. Regarding the temperature, eurythermic species were found. S. lacustris, N. bretscheri Michaelsen

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1899, Ch. diaphanous were the dominant species of species; they were mainly represented by widespread Naididae; Lumbriculus variegatus (Müller 1773), of eurybiont species: L. hoffmeisteri, T. tubifex, and Lumbriculidae; T. tubifex, of Tubificidae; and Lumbri- S. lacustris. Four leech species were identified; the cus terrestris Linnaeus 1758, of Lumbricidae, which widespread eurybiont genera Erpobdella and Glossi- often penetrated into water bodies and streams from phonia were the most common (Bezmaternykh and the coastal zone. In the zoogeographical aspect, Hol- Krylova, 2014). arctic and cosmopolitan species predominated. With Fourteen species of oligochaetes from two families, regard to the temperature, they were eurytherms, and Naididae (9) and Tubificidae (5), were identified in concerning the food spectra, they were phyto- and the zoobenthos of the Novosibirsk Reservoir, the larg- detritus feeders (Koveshnikov, 2014). est in western Siberia. Most representatives of Naidi- Among the lowland tributaries of the Upper Ob’ dae were found on aquatic vegetation and the substrate River, oligochaetes and leeches of the river were stud- surface and belonged to phytophages. Tubificidae pre- ied from the Alei River (a large tributary of the Ob’ ferred soft sediments, which they fed on. Cosmopoli- River) and the Gilevskoe Reservoir, where nine spe- tan (43%) and Holarctic (36%) species prevailed. cies of oligochaetes have been identified. The most Most species (86%) were eurytherms. In the Novosi- common eurybiont and widespread species of oligo- birsk Reservoir, L. hoffmeisteri was the most common chaetes, L. hoffmeisteri and T. tubifex, and the leech species (encountered in 68–85% of the samples), fol- E. octoculata were encountered the most frequently lowed by N. variabilis (37%) and T. tubifex (26–31%). (Bezmaternykh and Krylova, 2016). More than half of the species (57%) were found singly. The Barnaulka River, flowing from the group of Previously, 13 species of oligochaetes and eight species lowland lakes and tributaries, is also inhabited by nine of leeches were found in the reservoir (Zaloznyi, 1984; species of oligochaetes and five species of leeches, Blagovidova and Zaloznyi, 1976). An increase in the among which the same eurybiontic and widespread abundance of oligochaetes from the upper parts of the species—L. hoffmeisteri, T. tubifex, and E. octoculata reservoir to the lower reaches was noted, which was (Bezmaternykh, 2008)—were found most frequently. possibly associated with a change in the sediment In the small Bol’shaya Cheremshanka River, origi- type, from sandy to silty. The same trend was observed nating in the spurs of the Biysk-Chumysh Upland, for the entire benthic community (Yanygina and Kry- and its tributaries, four species of oligochaetes and two lova, 2012). types of leeches were registered, among which the spe- The basin of the Middle Ob’ River. In the Tom’ cies that were found more often were the same as those River, 14 oligochaete species of various taxa were iden- observed in the Alei and Barnaulka rivers. In the small tified. L. hoffmeisteri and T. tubifex formed the basis of Izdrevaya River (a tributary of the Inya River, Novosi- the oligochaete community, and E. octoculata, the birsk Region), oligochaetes were not found, and the leech community. The list of species is far from com- leeches were represented by one species, E. octoculata, plete, in as much as 37 oligochaete species and 11 leech which was found on rocky substrates of the lower species were previously reported for the Tom’ River reaches (Bezmaternykh, 2007). (Zaloznyi, 1984). In the Belovskii Reservoir, 14 species of oligo- The registered species were widespread, confined chaetes and three species of leeches were identified. to a rocky littoral, rich in phyto-fouling, and belonged The highest frequency of occurrence was observed for mainly to the potamo-rheophilic ecological group oligochaetes (55%), (45%), L. hoffmeisteri T. tubifex (Koveshnikov and Krylova, 2002). and Limnodrilus claparedianus Ratzel 1868 (41%). Leeches were rare, represented mostly by Erpobdella In the Irtysh River, which is the largest tributary of nigricollis (Brandes 1899) (6%). It was found that the the Ob’ River, about 1800 km of the river (90% of its spatial distribution of the worms of the Belovskii Res- Russian part) were examined during a complex expe- ervoir was primarily influenced by the type of biotope dition performed from July 19 to August 4, 2001. The and by the addition of fish feed to the water in the area fauna of oligochaetes and leeches was represented by of the fishery enterprise, and heating of the water was seven species of oligochaetes (excluding the family a secondary factor. Enchytraeidae) and one leech species. L. hoffmeisteri In the lower reaches of the large Chumysh River, and Ophidonais serpentina (Müller 1773) were the the leech species were E. octoculata and H. stagnalis most common oligochaete species (Koveshnikov, (Bezmaternykh, 2008). In 2011, two species of oligo- 2014a). chaetes, L. hoffmeisteri and N. variabilis, were found in Based on original molecular data (DNA barcod- the middle reaches. N. variabilis dominated by fre- ing) and morphological studies (Fedorova, 2018), the quency of occurrence; L. hoffmeisteri, by biomass species diversity of the hirudofauna of the Irtysh River (Yanygina and Krylova, 2012). basin was assessed in detail. The fauna of leeches now In the reservoir located on the small Chernovoi includes 12 species, seven of which are potentially new Urop River, the species composition of oligochaetes in to science (Alboglossiphonia sp., three species of Glos- the macrozoobenthos of the lake comprised only six siphonia, and three species of Erpobdella genera).

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Table 3. The number of identified species of oligochaetes in various water bodies Number Water bodies References of species Lake Baikal 206 Semernoi, 2004 Volga River basin 133 Arkhipova, 2005 Rivers of the North Urals 85 Shubina, 2006 The water bodies of the Netherlands 76 Nijboer et al., 2004 Ob River basin 76 Original data Lake Onega 69 Ekosistema Ladozhskogo Ozera…, 1990 Lake Ladoga 45 Stal’makova, 1968; Ladozhskoe Ozero…, 1992; Barbashova, 2015 Biwa Lake 41 Ohtaka and Machiko, 1999 The water bodies of the Polar Urals 36 Baturina and Loskutova, 2010 Towada Lake 29 Ohtaka, 2001 The water bodies of northern Fennoscandia 20 Yakovlev, 2005 Khubsugul Lake 17 Semernoi, 1972; Semernoi and Akin’shina, 1980 Thingvallavatn Lake 16 Ecology of Oligotrophic…, 1992

Basin of the Lower Ob’ River. The basin of the uous range, as well as the leech Acanthobdella peledina Lower Ob’ River is characterized by frequent fluctua- Grube 1851, which was confined to the northern lati- tions in the water level and flow velocity, a low water tudes of Eurasia. temperature, and almost no macrophytes, which Thirteen species of oligochaetes and three species together cause a depletion in the species diversity of of leeches were found in the reservoirs and water- oligochaetes and leeches (35 and 11 species, respec- courses of the Yamal Peninsula in 2015. L. hoffmeisteri tively). Sandy sections of the river bed are practically dominated in the sediments, and Naididae representa- devoid of benthic organisms. Silted sandy soils of tives, in the coastal biotopes. E. octoculata was the coastal zones are populated variably and abundantly. most common leech species. Tubificidae were the main representatives of the oligochaete fauna (L. hoffmeisteri and T. tubifex); in leeches, E. octoculata and G. complanata were common (Zalo- DISCUSSION zny, 1984; Kuzikova et al., 1989). The fauna of oligochaetes of the Ob’ River basin is The water bodies of northern Siberia are located in characterized by low taxonomic diversity (76 species) permafrost zones and harsh climate, which deter- compared with other large water basins, such as the mines the development of aquatic fauna, including Volga River, the rivers of the northern Urals, and Lake oligochaetes and leeches. Therefore, the faunistic Baikal. The number of oligochaete species is similar to complexes and ecological features of the inhabiting the reservoirs of the Netherlands and exceeds that of species are characterized by a rather wide ecological Lake Ladoga and Lake Onega, Biwa Lake, and the valence. Rivers and lakes located in the tundra zone water bodies of the Polar Urals. The species diversity is were poor in aquatic plants; the latter were almost even lower in Towada Lake and the water bodies of absent in large lakes and rivers, and they had abun- Northern Fennoscandia, Khubsugul Lake, and dance in small ones. The bottom sediments of the Thingvallavatn Lake (Table 3). water bodies were silted sand, pebbles, gray silt, and peat detritus. Many tundra lakes were in the stage of The leeches of the Ob’ River basin are character- overgrowing with floating bogs. The list of oligo- ized by low taxonomic diversity (14 species), following chaetes found in northwestern Siberia included 22 that of Lake Baikal (19 species) and the Upper Volga species. T. tubifex, L. hoffmeisteri, and S. ferox pre- River basin (17 species). vailed. Seven leech species were noted, E. octoculata, Estimating the distribution of oligochaetes in the Erpobdella testacea (Savigny 1820), and G. complanata Ob’ River basin, it can be stated that the fauna is were the most common. Most species of oligochaetes formed mainly by eurybiont species, without signifi- and leeches belonged to the rank of temperature- cant zonal changes (Fig. 1). The local fauna of the indifferent, eurythermic species, characterized by Irtysh River and northwestern Siberia differ the most. wide geographical ranges (Zaloznyi, 1979, 1984). The The key oligochaeta species of the fauna are T. tubifex, oligochaete Alexandrovia onegaensis Hrabe 1962 was L. hoffmeisteri, S. ferox, L. variegatus, S. lacustris, an exception, with a local distribution and a discontin- N. variabilis, and Ch. diaphanus, which are constant

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5 5

90–99% 70–89% 90–99% 50–69% 80–89% 70–79%

3 3

2 4 2 4

1 1 Fig. 1. Oriented multigraph of binary relations on a variety of measures of including descriptions of the species com- Fig. 2. Oriented multigraph of binary relations on a variety position of oligochaetes in the Ob’ River basin: 1, Upper of measures of including descriptions of the species com- Ob’ River; 2, Middle Ob’ River; 3, Lower Ob’ River; position of leeches in the Ob’ River basin. For the legend 4,Irtysh River; 5, Ob’ River in northwestern Siberia. see Fig. 1. components of the benthic biocenoses of the water Lumbricidae, 2; and Haplotaxidae, 3 species. The bodies and streams of the Ob’–Irtysh interfluve hirudofauna is characterized by less variety: there are (Zaloznyi, 2007). In the Ob’ River basin, the endemic 14 leech species belonging to five families: Acanthob- species are Rh. lepnevae, Rh. altaianus, and Pelodrilus dellidae, 1 species; Glossiphoniidae, 6; Ichtyobdelli- ignatovi Michaelsen 1903. dae, 2; Erpobdellidae, 3; and Hirudinidae, 2 species. The fauna of leeches of the Ob’ River basin contain The species diversity of oligochaetes and leeches 14 species belonging to five families. Considering the revealed for the Ob’ River basin is much less than that total number of leech species, only Hirudo medicinalis of the large basins of Europe (Volga River) and eastern Linnaeus 1758 needs confirmation of its habitat in Siberia (Lake Baikal), and is comparable with the southwestern Siberia or it is very rare in the studied fauna of certain regions of Europe and the Urals. region (Lukin, 1976; Zaloznyi, 2007). A study of the The largest number of oligochaete and leech spe- regional hirudofauna showed that four species cies was noted in the well-studied basins of the Upper (G. complanata, H. stagnalis, E. octoculata, and E. tes- and Middle Ob (more than two-thirds of their total tacea) form the basis of the leech fauna of the Ob’ number), and this indicator significantly decreases River basin (Zaloznyi, 2007). The Upper Ob’ River moving northwards. and the Ob’ River reaches in northern Siberia are characterized by the most outstanding species list (Fig. 2). The According to the zoogeographical distribution, the use of DNA barcoding techniques will make it possible to fauna of oligochaetes and leeches of the Ob’ River clarify the taxonomic composition and identify cryptic basin are dominated by species that are widespread in species of leeches (Fedorova, 2018). the Holarctic and Palearctic, as well as cosmopolitan species; the number of endemic species is insignifi- cant. CONCLUSIONS In relation to the temperature factor, the species of Analysis of the original and published data on the oligochaetes and leeches identified are mainly eury- fauna of oligochaetes of the Ob’ River basin showed thermic; less commonly, they are cold-water steno- that at least 76 species of oligochaetes, belonging to thermic. According to the prevailing feeding type, oli- seven families, inhabit the water bodies and streams gochaetes are mainly detritus feeders and phy- studied: Aeolosomatidae, 1 species; Naididae, 39; tophages, less often, predators; leeches are predators Tubificidae, 21; Enchytraeidae, 5; Lumbriculidae, 5; and parasites. With regard to the community type, oli-

BIOLOGY BULLETIN Vol. 46 No. 9 2019 FAUNA, SPATIAL DISTRIBUTION, AND ECOLOGICAL PECULIARITIES 1009 gochaetes are mainly benthic and less commonly, southern part of the Ob–Irtysh interfluve, Rybovod. Rybn. amphibionts. Khoz., 2015, no. 9, pp. 9–20. Bezmaternykh, D.M. and Vdovina, O.N., Zoogeographical composition of the macroinvertebrates of lake systems of ACKNOWLEDGMENTS the southern part of the Ob–Irtysh interfluve, Izv. Altaisk. The authors are grateful to O.S. Burmistrova, Otd. Russ. Geogr. O-va, 2016, no. 1 (40), pp. 46–52. O.N. Vdovina, S.O. Vlasov, V.V. Kirillov, M.I. Kovesh- Blagovidova, L.A. and Zaloznyi, N.A., On the fauna of oli- nikov, A.V. Kotovschikov, E.Yu. Mitrofanova, and gochaetes and leeches of the Novosibirsk Reservoir, in Bio- L.V. Yanygina for assistance in sampling and primary process- logicheskii rezhim i rybokhozyaistvennoe ispol’zovanie Novo- sibirskogo vodokhranilishcha (Biological Regime and Fish- ing of samples and to N.A. Zaloznyi for scientific advice. ery Use of the Novosibirsk Reservoir), Novosibirsk, 1976, pp. 99–105. FUNDING Bogdanov, V.D., Bogdanova, E.N., Gos’kova, O.A., and Mel’nichenko, I.P., Retrospektiva ikhtiologicheskikh i gidro- This work was carried out as part of a State Task of the biologicheskikh issledovanii na Yamale (Retrospective of Institute of Water and Environmental Problems, Siberian Ichthyological and Hydrobiological Studies on the Yamal Branch, Russian Academy of Sciences (program no. 0383- Peninsula), Yekaterinburg: Ekaterinburgskoe izdatel’stvo, 2016-0003) and with financial support from the Russian 2000. Foundation for Basic Research (project no. 17-05-00404a). Chekanovskaya, O.V., Vodnye maloshchetinkovye chervi fauny SSSR (Aquatic Oligochaetes of the Fauna of the USSR), Moscow: Akad. Nauk SSSR, 1962. COMPLIANCE WITH ETHICAL STANDARDS Dolgin, V.N., Zhernovnikova, G.A., and Zaloznyi, N.A., Conflict of interest. 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