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Corresponding author: Irina A. Kaygorodova ( irina@lin.irk.ru ) Academic editor: Fredric Govedich
© 2015 Irina A. Kaygorodova.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kaygorodova IA (2015) Annotated checklist of the leech species diversity in the Maloe More Strait of Lake Baikal, Russia. ZooKeys 545: 37-52. https://doi.org/10.3897/zookeys.545.6053
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In this paper, the very first checklist of the freshwater leeches of Maloe More Strait, a special part of Lake Baikal, is presented. It includes 14 free-living and parasitic species, of which four species belong to endemic Baikal genera – two species from Baicalobdella and one species each from Baicaloclepsis and Codonobdella. The checklist highlights six potentially new morphological species recorded for the first time in the area. The exact systematic position is stated for all leech species. Each species from the list is provided with information on taxonomic synonymy, data on its geographic distribution, and ecological characteristics. New species records are additionally provided with brief morphological characteristics and photos of their external morphology.
Hirudinea , checklist, endemic, Maloe More Strait, Lake Baikal
The Baikal leeches (Hirudinea) are one of the least studied groups of invertebrates due to underestimation of their role in aquatic ecosystems and intractability of their taxonomy. In fresh and brackish waters, some leeches serve as invertebrate predators while others are infamous for their ability to feed on the blood of either invertebrates or vertebrates. The first group includes macrophagous leeches. These leeches have a large size relative to other freshwater invertebrates and a high density in the littoral zone of reservoirs and lowland streams making them critical to fish nutrition. This role is obviously underestimated at present. This may be attributed to peculiarities of their habitation and consequently of their sample collection. Macrophagous leeches are rarely found in hydrobiological collections; therefore, their abundance has not been taken into account and their role in ecosystems has often been undervalued. The second group consists of parasitic forms, which constitute the main part of the leech diversity, and their role in ecosystems is absolutely different. Being epizoic parasites, they have relevance to transmission of bacterial and viral infections (e.g.
An exploration of the Baikal parasitic leech diversity was begun by pioneering 19th century German zoologist Adolf Eduard Grube. Clepsine echinulata Grube, 1871 (now Baicaloclepsis echinulata (Grube, 1871)), Piscicola torquata Grube, 1871 (now Baicalodbella torquata (Grube, 1871)) and Codonobdella truncata Grube, 1873 may have been the first freshwater leeches recorded from Lake Baikal, but their host relationships had not been identified. Non-parasitic leeches of Lake Baikal were excluded from any scientific interest for a long time due to their belonging to the common Siberian faunal assemblage, and the scientific pursuit of unique endemic elements. Later, the famous Russian scientist Nikolai Livanow, studying Baikal samples, described the species Protoclepsis tesselatoides Livanow, 1902, which has some morphological differences from the Palaearctic Protoclepsis tessulata (Müller, 1774) (now Theromyzom tessulatum) parasitizing waterfowl. Next, the endemic “flat” leech Torix baicalensis Shchegolew, 1922 (now Paratorix baicalensis) was discovered by
The data included here are based on previously published records and additional field investigations from 2002–2014. Collected material has been deposited in the laboratory of Molecular Systematics, Limnological Institute SB RAS, Irkutsk, Russia. The list provides morphologic and taxonomic notes where needed, as well as distribution ranges of genera and species. The accepted modern names of the type species of genera are provided. The systematic arrangement at family and more inclusive levels is based on the currently accepted classification system. Within this paper, family, subfamily, genus and species names are arranged alphabetically. The checklist includes 14 species and subspecies along with several new distribution records, including four endemic species, and six potential new species.
Previously published information and an extensive collection of specimens, collected by the author in the period from 2002 to 2014 were used in this paper. Most of the specimens came from the task-oriented expedition on the Maloe More Strait which was undertaken in 2013. All sampling locations are shown in Fig.
Map of the Maloe More Strait of Lake Baikal. Red dots indicate leech sampling localities: 1 Tutay Bay 2 Sakhurte Bay 3 Olkhon Gates Strait 4 Kurkut Bay 5 Ulirba Bay 6 Mukhor Bay 7 Shide Bay 8 Khuzhir-Nugho Bay 9 Khuzhir-Nugho Bay against of Sarma village) 10 Sarma River 11 Mukhor-Khale Bay 12 Khagden-Khale Bay 14 Kurma Bay 15 Otto-Khushun Bay 16 Lake Surkhaytor-Hur 17 Lake Zunduk 18 Zunduk Bay 19 Codoviy Bay 20 Lake Zama 21–24 Northern transit of the Maloe More 25 Cape Khoboy 26 Nyurgon Bay 27 Kharansa Bay 28 Odonim Bay 29 Khuzhir Bay 30 Elgay Bay 31 Lake Khankhoy 32 Shibetey Bay 33 Semisosennaya Bay 34 Khargoy Bay 35 Kharin Irgi Bay 36 Khul Bay 37 Zagli 38 Lake Nur 39 Ushun Bay.
Newly collected specimens were photographed alive, placed in separate vials, fixed and kept in 80% ethanol solution. Current systematic keys (
Holarctic.
Alboglossiphonia heteroclita (Linnaeus, 1761).
Hirudo heteroclita: Linnaeus 1761; Hirudo papillosa: Braun 1805; Hirudo trioculata: Carena 1820; Clepsine caranae: Moquin-Tandon 1826; Clepsine striata: Apáthy 1888; Clepsine polonica: Lindenfeld and Pietruszynski 1890; Glossiphonia heteroclita: Blanchard 1894; Glossiphonia heteroclita: Harding and Moore 1926.
Holarctic species.
papillosa (Pawlowski, 1936)
widespread in the Holarctic region.
Maloe More: Tutay Bay, Kurkut Bay, Zagli Bay, Mukhor Bay, Kurma Bay, Lake Zunduk, Lake Zama, Codoviy Bay, Lake Khuzhir.
A. heteroclita lives in various types of flowing and stagnant waters (
Hirudo hyalina: Müller 1774; Clepsine hyalina: Moquin-Tandon 1826; Glossiphonia hyalina: Blainville 1827; Glossiphonia heteroclita f. hyalina: Pawlowski 1936.
Palaearctic region.
Maloe More: Kharin Irghi Bay, Kurma Bay, Shide Bay, Lake Khuzhir, Lake Khankhoy, Lake Surkhaytor-Nur, Lake Zunduk, Lake Zama, Codoviy Bay.
This species is a benthic ectoparasite of snails. It was found in the mantle cavity of representatives of Lymnaeidae, for instance Lymnaea stagnalis (Linnaeus, 1758) and Stagnicola corvus (Gmelin, 1791). In Baikal, A. hyalina feeds on Planorbidae, Lymnaeidae, and Valvatidae.
Palaearctic and Nearctic.
G. complanata (Linnaeus, 1758).
Kurma Bay, Lake Surkhaytor-Nur, Lake Zunduk, Lake Zama.
Length is up to 25 mm. Three pairs of eyes. On the dorsal side there are longitudinal rows of dark pigmentation (Fig.
Specimens were collected in the littoral zone. Life cycle is typical for majority of the genus. It prefers to sit on the rocks, or slowly crawl. This leech feeds almost exclusively on molluscs, and sometimes on worms or larvae of insects. With its elastic proboscis, it pierces the delicate covers of the victim and sucks its blood. The Maloe More Glossiphonia sp. 1, like other glossiphoniids, takes care of its young.
Kurma Bay, Lake Zama.
The size varies from 7 to 12 mm. This leech has a bright amber colour due to tiny pale brown pigment cells uniformly strewn along the body dorsally and one pair of dark longitudinal median rows (Fig.
Glossiphonia sp. 2 occupies the same ecological niche as the previous Glossiphonia species, parasitizing small invertebrates preferentially molluscs.
Cosmopolitan.
Helobdella stagnalis (Linnaeus, 1758)
Hirudo stagnalis: Linnaeus 1758; Hirudo pulligera: Daudin 1800; Glossiphonia perata: Johnson 1816; Erpobdella bioculata: Lamark 1818; Clepsine bioculata: Savigny 1822; Glossobdella pulligera: Blainville 1827; Clepsine stagnalis: Fillipi 1837; Glossiphonia bioculata: Maquin-Tandon 1846; Glossiphonia circulans: Maquin-Tandon 1846; Clepsine modesta: Verrill 1972; Glossiphonia modesta: Vaillant 1890; Glossiphonia stagnalis: Blanchard 1894; Glossiphonia (Helobdella) stagnalis: Moore 1922; Bakedebdella gibbosa: Sciacchitiano 1939.
Cosmopolitan.
Maloe More: Tutay Bay, Zagli Bay, Mukhor Bay, Shide Bay, Lake Khankhoy, Lake Surkhaytor-Nur, Lake Zunduk, Codoviy Bay.
This species is considered one of the most common freshwater leeches in the world. Within Baikal, H. stagnalis inhabits shallow bays and salinas. This Helobdella species cannot swim; it crawls on aquatic plants and other objects, using its suckers as organs of attachment. Most suck the haemolymph of freshwater invertebrates such as oligochaetes, larvae of insects, and freshwater snails (
Palaearctic region.
H. marginata (Müller, 1774)
Hirudo marginata: Müller 1774; Hirudo variegates: Braun 1805; Hirudo cephalota Carena 1820; Hirudo oscillatoria: Saint-Amas 1825; Piscicola tesselata: Maquin-Tandon 1826; Piscicola linearis: Kollar 1842; Glossobdella cephalota: Blainville 1827; Haemoharis marginata: Filippi 1837; Glossiphonia marginata: Maquin-Tandon 1846; Hirido flava: Dalyell 1953; Glossiphonia flava: Johnston 1865; Glossiphonia marginata: Blanchard 1892.
Palaearctic region. A closely related taxon Hemiclepsis marginata asiatica Moore, 1924, is known from Cashmere to Sumatra. Its relationship to the nominate subspecies is still doubtful.
Maloe More: Kurma Bay, Mukhor Bay, Khuzhir-Nugho Bay, Lake Khankhoy, Lake Surkhaytor-Nur, Lake Zunduk.
This species inhabits Europe and Asia. In Central Europe, however, it is rare, whereas in Eastern Siberia it is widespread. As a sanguivorous ectoparasite it feeds on fishes and amphibians. Hemiclepsis marginata is able to move actively. When not on a host, H. marginata usually is found beneath large stones in shallow water or on submerged macrophytes. It can be found in all types of freshwater habitats and often thrives in stagnant water, weedy ponds, and, less often, in streams.
Holarctic.
T. pallens Philippi, 1867
Hirudo tessulata: Müller 1774; Hirudo tesselata: Bosc 1802; Nephelis tesselata: Savigny 1822; Erpobdella tesselata: Fleming 1822; Ichthyobdella tesselata: Blainville 1828; Erpobdella vulgaris var. tesselatum: Blainville 1828; Clepsine tessulata: Müller 1844; Glossiphonia tessulata: Maquin-Tandon 1846; Glossiphonia aecheana: Thompson 1846; Hirudo vitrina: Dalyell 1853; Glossiphonia vitrina: Johnston 1865; Theromyzon tessulatum: Philippi 1867; Hemiclepsis tesselata: Vejdovsky 1883; Glossiphonia tesselata: Blanchard 1892; Protoclepsis tesselata: Livanow 1902.
Palaearctic and Nearctic regions. A closely related taxon Protoclepsis tesselatoides Livanow, 1902 was synonymised in T. tessulatum (
Maloe More: Lake Zunduk, Lake Zama.
This is a widespread but rare species. It can be found in warm bays of Baikal and adjacent freshwater reservoirs. It prefers stagnant water. Feeds on the blood of vertebrates. Most likely hosts might be fishes, water birds or amphibians.
Ulirba Bay.
Specimens are 12 mm in length and about 2 mm in width and can stretch up to 15-17 mm, becoming 1 mm in width. It has four pairs of eyes as do all representatives of the genus. A special colouration of the body sets them apart from all other known species (Fig.
Representatives of this genus are known as bloodsuckers of birds (
Endemic to Lake Baikal.
Baicaloclepsis echinulata (Grube, 1871)
Clepsine echinulata (part.): Grube 1871; Haementeria echinulata: Dogiel & Bogolepova 1957.
Endemic to Lake Baikal.
Maloe More: Zagly Bay, Khargoy Bay, Semisosennaya Bay, Elgay Bay.
Endemic to Lake Baikal. Large leeches (length of 30-40 mm, width of 10-15 mm). Baicaloclepsis grubei were found only within the Maloe More Strait at relatively shallow depths of 14-40 m. This leech cannot swim and apparently can move only slowly. Since B. grubei has a comparatively small posterior sucker, it is unlikely that it can provide a strong fastening to a host. In addition, this species probably spends a significant part of its life in a free-living state. All specimens were collected from benthic samples. The question of a potential host of this bloodsucking leech remains open.
Endemic to Lake Baikal.
Baicalobdella torquata (Grube, 1871).
Trachelobdella torquata (part.):
Endemic to Lake Baikal.
Maloe More: Kurma Bay; Olkhon Gates Strait; Kharansa Bay.
This species inhabits the littoral zone of Lake Baikal (0–200 m). This species is less abundant in the Maloe More area than its sister species, B. torquata. In contradistinction to B. torquata, it parasitizes only Baikal cottoid fishes. Baicalobdella cottidarum can be found directly on a host or in a free-living state on the surface of benthic substrates.
Piscicola torquata Grube, 1871; Trachelobdella torquata (part.):
Endemic to Lake Baikal.
Maloe More: Khagden-Khale Bay; Otto-Khushun Bay; Nyurgon Bay; Odonim Bay; Ulirba Bay; Mukhor Bay; Sakhurte Bay; Khul Bay; Ushun Bay.
This is a typical component of the littoral zone of open water in Baikal. This species was found at depths of 0.5–10 m. These small leeches are 5-8 mm in length, with a width of 2-3 mm. Body colour varies from light green to pale rust, retaining a characteristic mosaic pattern on the dorsal side of the urosome. Baicalobdella torquata feed on Baikal endemic amphipods.
Endemic to Lake Baikal.
C. truncata (Grube, 1873).
Northern transit of Maloe More Strait, Nyurgon Bay, Kharansa Bay, opposite the Cape Khoboy, Shibetey Bay.
Body length of 8–10 mm. It differs from the type species, Codonodbella truncata, by the existence of a distinctive pigmentation on the dorsal side and the representative shape of the body (Fig.
This leech is an inhabitant of open waters. Within the Maloe More, it was recorded in the northern part of the strait at a depth of 30–140 m.
Palaearctic and Nearctic regions.
Erpobdella octoculata (Linnaeus, 1758).
Kurkut Bay, Kurma Bay, Zagli Bay, Shide Bay, Kharin Irghi Bay, Tutay Bay, Ulirba Bay.
The leeches are about 25–35 mm in length and 3–4 mm in width. Eight eyes. The leech has a pale pink body tinge. Dorsal pigmentation is almost absent. There are only a few dark spots irregularly scattered on the dorsal surface (Fig.
This freshwater ribbon leech is common in the sor zone of Lake Baikal (
Lake Zama, Lake Zunduk, Codoviy Bay.
This non-parasitic macrophagous leech species has a restricted distribution even within the Maloe More. It was found only in lakes and bays of the most north-western coast of the strait.
This is the first comprehensive checklist of the Baikal leech species inhabiting the Maloe More Strait. At present, 14 species are documented. This species diversity includes both widespread Holarctic and Palaearctic leeches and also endemic leech species from two different orders (Rhynchobdellida and Arhynchobdellida), three families (Glossiphoniidae, Piscicolidae, and Erpobdellidae) and nine genera. The most diverse is the group of glossiphoniid leeches, which consists of nine species belonging to six genera (Alboglossiphonia – 2 spp., Glossiphonia – 2 spp., Helobdella – 1 sp., Hemiclepsis – 1 sp., Theromyzon – 2 spp., Baicaloclepisis – 1 sp.). The Maloe More piscine leeches include representatives of two endemic genera (Baicalobdella – 2 spp. and Codonobdella – 1 sp.). Among the Arhynchobdellida, two species of the genus Erpobdella were found in the Maloe More. Six species in the checklist, including both representatives of Erpobdella, two of Glossiphonia, as well as one each from Theromyzon and Codonobdella were referred in this paper, with caution, to unidentified species since their morphology differed from all currently described species. With high probability, these six non-identified species are potentially new to science. All six of these, for the first time were recorded within the Maloe More. Some of these new morphotypes had previously been found in other parts of Lake Baikal. Thus, leeches similar to Erpobdella sp. 1 had already been reported from Chivyrkuy Bay (
This study was financially supported by the Russian Foundation for Basic Research (RFBR) grant nos. 11-04-01394, 12-04-10007, and 14-04-00345. The author is grateful to Natalya Sorokovikova and Lyudmila Fedorova for support of the field work. Professional divers Igor Khanaev and Alexey Bormotov assisted us in obtaining samples from inaccessible places (for hydrobiological tools).