New data on species diversity of Annelida (Oligochaeta, Hirudinea) in the Kharbey lakes system, Bolshezemelskaya tundra (Russia)

Abstract One of the features of the tundra zone is the diversity of freshwater bodies, where, among benthic invertebrates, representatives of Annelida are the most significant component in terms of ecological and species diversity. The oligochaete and leech faunas have previously been studied in two of the three largest lake ecosystems of the Bolshezemelskaya tundra (the Vashutkiny Lakes system, Lake Ambarty and some other lakes in the Korotaikha River basin). This article provides current data on annelid fauna from the third lake ecosystem in the region, Kharbey Lakes and adjacent water bodies. The annelid fauna includes 68 species, including 51 oligochaete species, and 17 species of leeches. For each species, we give information on currently recognised classification, taxonomic synonymy, geographical distribution, findings of the species within the Russian tundra, and brief ecological characteristics.


Introduction
The tundra covers an area of approximately 15 % of the entire territory of Russia, along the entire coast of the Arctic Ocean, from the Finland border in the west to the Bering Strait in the east. Bolshezemelskaya tundra is a vast plain with an area of 1,660 km 2 located between the Pechora and Usa rivers (in the west and south) and the Ural Mountains in the east, adjacent to the Barents Sea in the north. Hills with prevailing heights of 100-150 m and moraine ridges of up to 250 m high characterises its relief. The main part of the Bolshezemelskaya tundra is occupied by permafrost. Here, peat bog and silt-marsh soil types prevail; in the south, there are weakly podzol-gley soils. The climate is subarctic, with long cold winters and short cool summers. Many rivers which are tributaries of the Pechora and Usa flow through the plain. The main watershed is located in its central part, with the largest lakes systems in the east of the Bolshezemelskaya tundra: the Vashutkiny, Padimeyskiye, Kharbey Lakes and the other lakes of the Korotaikha River basin.
In this study, we focused on the waters of the Kharbey system, the main element of which is Bolshoy Kharbey Lake, located in the headwaters of the River Kharbeytyvis, the right tributary of the Seyda River. In addition, this system includes the lakes Golovka and Maliy Kharbey. The larger lakes are interconnected by natural channels and are surrounded by numerous shallow adjacent lakes and have a glacial origin. The Bolshoy Kharbey is the largest lake of the system (Vinberg and Vlasova 1976); its area is 21 km 2 , and depth is up to 18 m (70% of the lake has a depth of 1-6 m). The shoreline of the lake is indented, forming bays and gulfs. The lakeshore habitats are dry, mostly low, and peaty in some places. Bottom sediments in littoral habitats are pebble-boulder or sandy, in deeper water, the sandy substrate is covered with silt. There are many temporary water bodies in the catchment area of the Kharbey lakes. To the west of the Kharbey lakes, there is Lake Syattey-ty, which consists of two connected reservoirs (Fig. 1). The area of the larger lake, Bolshoy Syattey-ty, is 7.4 km 2 ; the catchment area is 66.2 km 2 . Gradually-sloping shores located near numerous small lakes are overgrown with sedge and willow; depth of these smaller lakes is 3.2-7.4 m; bottom sediments are mostly sandy and sometimes silty.
The first studies of the Kharbey system were carried out in [1965][1966][1967][1968][1969][1970][1971][1972] in order to evaluate the productivity and environmental features of lakes (Vinberg and Vlasova 1976). In these lakes, as in other lake systems of the Bolshezemelskaya tundra, a diverse and unique flora and fauna was described. However, there are no data on the species composition of annelids. Later, Zaloznyj (1978) found six species of leeches in this lake. In the late 1990s and early 2000s, complex studies of the ecosystem state, including the structural characteristics of benthic and plankton communities, were conducted in the Kharbey lakes, and these studies provided data on the faunal composition of various taxonomic groups, including Annelida (Fefilova et al. 2014, Baturina et al. 2014a.
The aim of this study is to further investigate the annelid species diversity and spatial distribution in the Kharbey Lakes system, as one of the largest systems of the Bolshezemelskaya tundra, combining the available literature data with new information about the Annelida fauna.

Materials and methods
Previously published information and an extensive collection of new specimens from fresh water bodies of the Kharbey Lake area collected by M. Baturina and O. Loskutova in 1998-99, 2009, 2010, and 2012 were used in this study. Within this study, the following water bodies of the Kharbey lakes system (Bolshezemelskaya tundra) were investigated: Lake Bolshoy Kharbey, Lake Golovka, and some unnamed smaller lakes adjacent to Lake Bolshoy Kharbey, arbitrarily identified as K1, K2, L, D1, and D2 (Fig.  1B). Additionally, 41 small temporary habitats (including swamps, depressions, and ponds), located within the catchment area of B. Kharbey, were investigated. In 2014, hydrobiological material was collected in Lake Syattey-ty (Bolshezemelskaya tundra) and small water bodies in its watershed. Main sampling locations are shown in Fig. 1.
Oligochaete samples were taken with a Petersen grab (sampling area 400 cm 2 ) on soft substrates and with a handle blade trawl (Zinchenko et al. 2014) on gravel substrates. Since the common hydrobiological equipment (sweep net, dredge, scraper, bottom grab, etc.) is often ineffective in collecting parasitic and predatory leeches, we inspected various aquatic plants and animals, as well as submerged objects (rotten wood, driftwood, snags, stones, etc.) for attached hirudinids. Some leeches were picked out from zoobenthic samples. In most cases, piscivorous leeches were collected directly from captured living hosts.
Newly collected specimens were fixed and kept in 80% ethanol solution. Morphological analysis was performed using a stereomicroscope MSP-2 var. 2 (LOMO) and compound microscope Leica DM 4000. The worm species determinations were based on existing taxonomic keys (Chekanovskaya 1962;Lukin 1976;Nesemann and Neubert 1999;Timm 2009) in accordance with the present-day classification of each group. As to names of higher oligochaete taxa, there is still no unanimous opinion; therefore, we left them as in Timm (2009). Voucher specimens were deposited at the Institute of Biology, Syktyvkar (Oligochaeta) and Limnological Institute, Irkutsk (Acanthobdellida and Hirudinea).

Data resources
The data underpinning the analysis reported in this paper are deposited at GBIF, the Global Biodiversity Information Facility, and are available at https://doi. org/10.15468/b24asb.

Results
This research describes the Annelida fauna of one of the largest lakes systems of Bolshezemelskaya tundra, Kharbey lakes. We show a list of oligochaete species (Oligochaeta), leeches (Hirudinea) and leech-like parasites (Acanthobdellida) for various types of water bodies of the Kharbey lakes system and the nearby Syattey-ty lakes system, and revise taxonomic and nomenclatural changes since the last fauna surveys The numbers indicate the major studied systems of tundra lakes: 1 -the Kharbey lake system, 2 -the Padimeyskiye lake system, 3 -Lake Ambarty, 4 -the Vashutkiny lake system; 5 -Lakes of the Pechora River Delta; 6 -lakes of the More-yu River basin (lower reaches); 7 -lakes of the More-yu River basin (upper reaches); 8 -lakes of central part of Bt; 9 -Lake Ngosovey. (B) Insert showing the Kharbey Lake system: K1, K2, D1, D2, and L are small lakes adjacent to Lake Bolshoy Kharbey.
in the lakes of Bolshezemelskaya tundra (Finogenova 1962(Finogenova , 1966Lukin 1962Lukin , 1966Zaloznyj 1978;Popchenko 1978Popchenko , 1988. The Oligochaeta fauna of tundra water bodies is considered to be significantly poorer in comparison with the nearby northern areas, such as the Kola Peninsula (Jakovlev 1982;Popchenko 1988). The main components of the fauna were cosmopolitan species or species that are widespread in the Palaearctic or Holarctic zoogeographic regions. Fifty-one oligochaete species were found in Lake Bolshoy Kharbey, its accessory water bodies and temporary watersheds; 15 of these were not previously observed in the systems of large lakes of the Bolshezemelskaya tundra, such as Vashutkiny and Ambarty. However, the overlap of the oligochaete species composition in all three lakes systems was more than 50%. Despite this taxonomic diversity, the list of known widespread species is relatively short in most water bodies of the Kharbey Lakes system: there were only three species (Lumbriculus variegatus (Müller), Tubifex tubifex (Müller) and Spirosperma ferox Eisen) recorded in the bulk of the studied water bodies, and 33 species were only observed once.
Oligochaete worms dominated the total numbers and biomass of zoobenthos at different depths on all the studied sediment types in the Kharbey system. The average abundance of oligochaetes showed the highest values in the upper and lower littoral zones (0-3-6 m), whereas on silts in the profundal zone (depths 6-9 m, max 18 m), the average abundance of the group was half as great. In most biotopes, S. ferox and T. tubifex were among the dominant species. On the gravel-pebble substrates of the littoral zone, subdominants included Nais barbata Müller, Uncinais uncinata (Øersted), Tubificinae gen. sp. juv., and Enchytraeidae gen. sp. juv.; the same species were also dominant on sandy sediment, along with Cognettia glandulosa (Michaelsen), L. variegatus and Piguetiella blanci (Piguet). On clayey substrate of the littoral and sublittoral zones, there was a group of minor species: Chaetogaster diaphanus (Gruithuisen), Nais alpina Sperber, Nais bretscheri Michaelsen, Nais pseudobtusa Piguet, U. uncinata, S. ferox and Lophochaeta ignota (Štolc), Enchytraeidae gen. sp. juv.; on profundal silts were N. pseudobtusa and Vejdovskyella comata (Vejdovský).
The species distribution of oligochaetes in lakes is usually determined by the substrate (O'Toole et al. 2008) and the oxygen regime (Timm 1987). At the same time, high diversity of naidids is probably associated with the variety of sediments and aeration in the littoral zone; as opposed to the profundal zone, where the dominants are tubificines. The complex of species S. ferox -T. tubifex, typical for the profundal zone of the most lakes, varies among the lakes under study: S. ferox remains the dominant species in the littoral and sublittoral zones, and T. tubifex descends to the less aerated deep-water zone, consistent with previous observations for small oligotrophic profundal lakes (Timm 1987).
The leech and leech-like taxonomic diversity includes 17 species belonging to three orders (Acanthobdellida Grube, Rhynchobdellida Blanchard and Arhynchobdellida Blanchard), five families (Arhynchobdellidae Grube, Glossiphoniidae Vaillant, Piscicolidae Johnston, Erpobdellidae Blanchard and Haemopidae (Richardson)), and nine genera (Acanthobdella Grube, Glossiphonia Johnston, Helobdella Blanchard, Hemiclepsis Vejdovský, Theromyzon Philippi, Piscicola de Blainville, Cystobranchus Diesing, Erpobdella de Blainville, and Haemopis (Savigny)). We collected only three of the five leech species recorded by Zaloznyj (1978) in the Kharbey lakes: Glossiphonia complanata (Linnaeus), Glossiphonia concolor (Apathy), and Piscicola geometra (Linnaeus). Of the newly recorded species, the tundra piscine parasite P. geometra has a specific segmentally repeated geometrical pattern of greenish-brown pigment on the dorsal side, but smaller body size dimensions in comparison with typical representatives of the species. Moreover, the new checklist includes 5 species (Acanthobdella peledina Grube, Theromyzon tessulatum (Müller), Piscicola sp., Erpobdella monostriata (Lindenfeld et Pietruszynski), and Erpobdella sp.) recorded for the first time for the Kharbey system. Among these, there are two potentially new species (Erpobdella sp. and Piscicola sp.), which differ from published descriptions. At the same time, eight species noted by previous authors (Lukin 1976;Zaloznyj 1978) from the Kharbey lakes -Glossiphonia verrucata (Müller), Hemiclepsis marginata (Müller), Helobdella stagnalis (Linnaeus), Theromyzon maculosum (Rathke), Erpobdella octoculata (Linnaeus), Erpobdella nigricollis (Brandes), Erpobdella testacea (Savigny), and Haemopis sanguisuga (Linnaeus) -were not found in our samples, although they may, supposedly, live there as noted by previous authors (Lukin 1976;Zaloznyj 1978). The burbot leech Cystobranchus mammillatus Malm, which we found in the Pechora River, is quite likely to be present in the Kharbey system. Despite earlier records listing two macrophagous leeches, E. octoculata and E. nigricollis, as the most numerous species (Lukin 1976), our samples did not contain these species. Although we did not find E. testacea, similar leeches, corresponding to E. monostriata in recent taxonomic revisions (Agapow and Bielecki 1992;Nesemann and Neubert 1999;Utevsky et al. 2015), were numerous numerous in Lake Bolshoy Kharbey and small lakes. Despite having a wide distribution range, G. verrucata, which is quite sensitive to habitat quality, has seemingly become too scarce in Western Europe; and we did not find this species in the northwestern part of Russia. The absence of the two most common Palaearctic species, H. stagnalis and H. marginata, in our samples from Kharbey lakes is very strange and unexpected. These findings can probably be attributed to sampling methods that were not focused on leeches. The "large false horse" leech H. sanguisuga is especially difficult to find since it often leaves water and lays its cocoons in moist soil near the shore (up to a vertical 2-3 cm above the water surface) (Nesemann and Neubert 1999). The presence of the waterfowl parasite T. maculosum in the Kharbey area was highly expected due to its previous findings in different lakes of the Komi region (Lukin 1957(Lukin , 1962, although this discrepancy could be due to prior misidentifications. Information on exact systematic position, geographical distribution and brief ecological characteristics for each Annelida species is given in the list below. Geographic distribution. Holarctic species. In the Russian tundra: Murmansk Region, coast of the White Sea (Timm and Abarenkov 2018).
Ecology. The species was recorded on clay, silted sand, large pebbles, often in moss and algal cover (depth 0.8 m, maximum up to 5.2 m). 2010), the Ob River delta (Timm and Abarenkov 2018), the northern part of Western Siberia (Zaloznyj 1984), the Yamal Peninsula (Stepanov 2016).
Ecology. The species was recorded on stones with algal cover and on sand, at depths of 0.5-3.8 m.
Ecology. The species of rare in studied region; it was found on silted sand at a depth of 3.8 m.

Nais alpina Sperber, 1948
Geographic distribution. In Europe and North America (Great Lakes). In the Russian tundra: Murmansk Region Popchenko 1978), Vaygach Island (Leshko et al. 2008), lakes in the More-yu River basin, lakes in the Kara River basin (Baturina and Loskutova 2010), lakes in the Malaya Usa River basin (Baturina et al. 2014b).
Ecology. The species inhabits stones with algal cover or sand with detritus (depth 0.2-1.3 m).
Ecology. The species was recorded on sands, stones with algal cover, as well as on clay and submerged macrophytes (depth 0.5-2.8 m).
Ecology. Within the studied water bodies, N. behningi was found on stony sediments with moss cover (depth 0.7-2.0 m).
Ecology. The species inhabits stony ground and mosses among large pebbles, typically at a depth of up to 1.0 m; it occasionally occurred at a depth of 2.5 m.
Ecology. In bulk of the studied water bodies, N. communis was observed on silted sand, boulders with moss and algal cover, and submerged macrophytes (depth 0.3-1.2 m). In Lake Golovka, it lives on a silted substrate at a depth of 7.5 m. It was also found in small lakes with moss mats floating off shore.
Ecology. Specimens were sampled among pebbles and boulders, as well as on sand or submerged macrophytes (depth 2.5 m or less).
Ecology. The species was recorded along the lakeshore at a depth of 0.8 m or less, on pebble-gravel or silty substrates, and in hollows and small bodies of water, formed by cross-country tracks.
Ecology. Specimens were sampled from different hard substrates or on the vegetated areas (depth 0.3-2.0 m). In water bodies adjacent to Kharbey, N. pseudobtusa prefers clayey or silted sand (depth of 7.5 m); single specimens were found in small isolated lakes with floating moss mats and thick sedge overgrowths.
Ecology. The species was found mainly on sand between stones at a depth of 1.0 m or less.
Ecology. The species was collected from submerged macrophytes, or stones and sand with moss cover (depth 0.2-1.3 m). It was also found in small water bodies or in humid depressions without open water.
Ecology. The species inhabits sandy and stony-sandy substrates with algae and moss at depths of 0.5-2.5 m except Lake Bolshoy Kharbey, where it occurs at a depth of 6.2 m.
Ecology. The worms were often found in silt, less often on sandy-stony substrate with algae and moss cover, or on submerged macrophytes (depth 0.2-2.5 m, occasionally up to 6.0 m).
Ecology. In the studied lakes, S. appendiculata inhabits mainly silt or stones with algal cover (depth 0.2-6.0 m). The worms were less often found in small or temporary ponds with floating moss mats and overgrowths of sedges off the shore. Geographic distribution. Holarctic species. In the Russian tundra: Murmansk Region (Finogenova 1975;Timm and Popchenko 1978), the Pechora River delta (Baturina 2018), lakes in the More-yu River basin (Baturina and Loskutova 2010), lakes in the Malaya Usa River basin (Baturina et al. 2014b), the Anadyr River basin (Morev 1983b).
Ecology. The species was recorded in most lakes of the study area, mainly on silted sand or clay (depths 0.5-1.1 m), rarely deeper on silted stony-sand or detritus (depths 4.2-6.0 m).
Ecology. The species is rare. It was noted in Lake Bolshoy Kharbey on silted sands (depth 9.5-13.8 m); in adjacent to Kharbey lakes is on clay substrate (depth no more than 0.8 m).
Ecology. The worms are very mobile; they prefer submerged macrophytes as substrate. S. lacustris was also observed on silted stones (depth 0.3-1.0 m).
Ecology. The species was recorded on silt, silted sand, and boulders, from the edge of the water to a depth of 4.5 m. In adjacent to Kharbey lakes, U. uncinata prefers moss and algal cover among the rocks in the shore zone. Common species for tundra zone.
Ecology. Within the area of study, V. comata was recorded infrequently, living on sand, silt, and clay (depths 4.5-6.5 m, rarer up to 9.8 m).
Ecology. The species prefers sandy-clay or clay at the shore sites. Rarer, V. macrochaeta was observed on clay sediments at a depth of 8.0-9.5 m.
Ecology. The species is rare in the area. It was found in the coastal zone of only two lakes, where it was on stones with algae and moss cover, sand or submerged macrophytes.

Naidium bilobata Bretscher, 1903
Geographic distribution. Europe. In the Russian tundra: Lake Ambarty and some other lakes in the Korotaikha River basin (Popchenko 1978), lakes in the Malaya Usa River basin (Baturina and Loskutova 2010).
Ecology. The species is common in the tundra zone. It lives on various sediments (including rocky, sandy, clayey, or silty) in the littoral zone of lakes.
Ecology. The species prefers soft silts of profundal zone of the lakes (depth of 6.0-6.5 m).
Ecology. This species is rare in the tundra lakes. It was found on clayey substrate at a depth of 1.7 m.
Ecology. The species is recorded in most lakes of the Kharbey system. Limnodrilus hoffmeisteri prefers silts, but it was also found on sandy-clay sediment and stones with algal cover (from the water edge to 5.2 m in depth).
Ecology. The species was found on stones with moss or algal cover and clayey ground (depth 1.1-2.0 m). It was not widely distributed in the Kharbey lakes system previously. Geographic distribution. It was found in Western Palearctic, Africa, Great Lakes of North America, and Lake Titicaca in South America. In the Russian tundra: Murmansk Region (Stalmakova 1974), the Pechora River delta (Baturina 2018), lakes in the More-yu River basin (Baturina and Loskutova 2010), the Ob River and Lena River deltas (Timm and Abarenkov 2018), the Yamal Peninsula (Stepanov 2018).
Ecology. This species is widespread in the area; it was found in most studied water bodies. It inhabits various grounds: stony, sandy, and muddy, often occurs on stones covered by moss or algae or submerged macrophytes (from the water edge up to 9.0 m). In most lakes, S. ferox is dominant in number.
Ecology. The species lives in silt, clay and sand (from the water edge up to 9.5 m in depth).
Ecology. This is one of the numerous and widespread oligochaete species in the Kharbey lakes system. It was found on various substrates (from the water edge to 8.0 m in depth).
Ecology. Single specimens were washed out from moss cover of sandy-silty substrates or submerged macrophytes.
Location. Temporary ponds of the Kharbey system (67°58'00"N, 62°34'60"E). Ecology. The worms were found in ponds that do not have an open water surface, in moss covering the swampy substrate.
Ecology. The species was encountered mainly on sandy and sandy-gravel substrate with moss cover in the shore zone. Single specimens were found on the boggy parts of the small lake.
Ecology. The species was observed in most lakes of the area; L. variegatus often numerically dominated, inhabiting sands or silts between stones, submerged macrophytes, and stones with moss or algal covering (at depth up to 1 m).
Ecology. This species is in the area. It lives on stones with algal covering, silty or sandy substrates (depth up to 1.5 m).
Ecology. This species is known as predator of small molluscs. The leeches were found on swamped places, as well as in small lakes with silted sand substrate. Geographic distribution. Palaearctic region. In tundra zone of Russia: the basin of the Usa (Lukin 1962).

Genus
Location. The species was not found in the area. Ecology. This leech parasitises molluscs, amphibians, and fishes; H. marginata is seemingly very rare species in the Komi region. Lukin (1962) has occasionally found one specimen in the Usa River.  (Zaloznyj 1978), the Yamal Peninsula (Stepanov 2016).

Subfamily
Location. The species was not recorded in the Kharbey lakes. It was only found in an oxbow lake in the Pechora River delta (68°8'8.2"N, 53°36'33.8"E).
Ecology. The leeches were found in the moss cover of the substrate in two swamped lakes, which do not have an open water surface.
Ecology. Piscicola geometra is considered to be an oxyphilic species. It inhabits both rivers and stagnant water bodies with a favorable oxygen regime. This is an ectoparasite predominantly of cyprinids, with no obvious host preference. A single specimen was sampled from the dorsal fin of a whitefish.

Piscicola sp.
Morphology. Very small leech, its body length is 7 mm and diameter is 1.5 mm. Pigmentation is uniform, does not form a specific pattern on the dorsal side of the body, unlike the widespread P. geometra.
Ecology. This leech inhabits various types of water bodies; it is considered the most numerous Erpoddella in most Palearctic freshwater bodies. These leeches avoid of humic substances, and practically do not occur in distrophic waters. However, E. octoculata can inhabit highly polluted water bodies.

Erpobdella monostriata (Lindenfeld & Pietruszynski, 1890)
Nephelis octoculata var. monostriata Lindenfeld & Pietruszynski, 1890 Erpobdella vilnensis (Liskiewitz, 1925) in part Geographic distribution. Widespread in the Palaearctic region and occurs from the Netherland (van Haaren et al. 2004) in the west to the Voronezh region of Russia in the east (Utevsky et al. 2015). In tundra zone of Russia: this Erpobdella is relatively low in numbers in the northwestern European part of Russia: basin of the Northern Dvina, Vychegda and Usa rivers where, E. nigricollis dominates according to Lukin (1957).
Ecology. The species was found in Arctophila thickets in a small body of water, and in silt of Lake Kharbey.

Haemopis sanguisuga Blanchard, 1894
Geographic distribution. Transpalearctic species. Widespread in all Europe and Asia up to Far East. In tundra zone on Russia: Lukin describes them as characteristic for Northern Eurasia (1976) and specifically for Komi Republic water bodies (1957).
Location. There is no specimen in our collection from the Kharbey area. Ecology. This so called "large false horse leech" is a predator and lives mainly in shallow ponds, occasionally in temporary ponds where sediments remain wet; it is found only in the shore zone.