Syst Parasitol (2013) 84:71–79 DOI 10.1007/s11230-012-9390-7 New records of the chaetiferous leech-like annelid Paracanthobdella livanowi (Epshtein, 1966) (Annelida: Clitellata: Acanthobdellida) from Kamchatka, Russia Serge Y. Utevsky • Sergei G. Sokolov • Marina B. Shedko Received: 31 July 2012 / Accepted: 13 September 2012 Ó Springer Science+Business Media Dordrecht 2012 Abstract Acanthobdellidans are unique in their rarely Gasterosteus aculeatus, Oncorhynchus mykiss and organisation and phylogenetic relationships due to O. kisutch. New information on the distribution and the having transitional characters that combine features of biology of P. livanowi is presented. oligochaetous and achaetous annelids. Alongside the relatively well-studied Acanthobdella peledina Grube, 1851, there is another member of the group, Paracant- Introduction hobdella livanowi (Epshtein, 1966), with five rows of chaetae and an anterior sucker. It appears that the anterior Acanthobdella peledina Grube, 1851 is among the sucker is weakly developed in small juveniles but most renowned clitellate annelids due to its transi- acquires a deep cavity in adults. Smaller individuals of tional morphological characteristics, which place it P. livanowi can be distinguished from A. peledina,which between achaetous leech-like clitellates and chaetif- does not possess an anterior sucker, by the varying erous oligochaetes. Acanthobdellidans are considered breadth of their chaetae. The mid-body segment consists as the sister group of branchiobdellidans plus hirudi- of two doubled annuli in juveniles and is quadri-annulate nidans (true leeches) (Siddall et al., 2001). Their in large individuals. In Kamchatka freshwaters, hosts of advanced characters include a constant number of P. livanowi mostly include Salvelinus spp. and more segments, annulation, sucker-shaped extremities, unpaired gonopores, but, on the other hand, they have S. Y. Utevsky (&) chaetae located on the five anteriormost segments and Department of Zoology and Animal Ecology, a spacious coelom, which can be viewed as primitive V.N. Karazin Kharkiv National University, pl. Svobody 4, oligochaetous characters. The comprehensive classi- Kharkiv 61022, Ukraine cal study on the morphology of A. peledina was e-mail: [email protected] carried out by Livanow (1906), and a more recent S. G. Sokolov redescription (Purschke et al., 1993) corroborated A.N. Severtzov Institute of Ecology and Evolution RAS, earlier opinions on a combination of both hirudinean Leninskiy pr. 33, Moscow 119071, Russian Federation and oligochaetous characters in this species. e-mail: [email protected] The species diversity of acanthobdellidans was M. B. Shedko reconsidered dramatically by Epshtein (1966), who Institute of Biology and Soil Science (IBSS), Far Eastern described another taxon of the group, Acanthobdella Branch of Russian Academy of Sciences (FEB RAS), livanowi Epshtein, 1966, which was subsequently 159 Stoletiya Street, Vladivostok 690022, Russian Federation transferred to a separate genus Paracanthobdella e-mail: [email protected] Epshtein, 1987 by Epshtein (1987). This species is 123 72 Syst Parasitol (2013) 84:71–79 characterised by the well-developed anterior sucker and our new findings (Table 1), Paracanthobdella with a conspicuous deepening between the chaetae. livanowi (Epshtein, 1966) is found on adult non- Moreover, P. livanowi, as in non-hirudinean clitel- migratory chars Salvelinus kronocius Viktorovsky, lates, possesses a prostomium, a lip-like extension S. schmidti Viktorovsky, S. albus Glubokovsky, located over the dorsal side of the mouth (Epshtein, S. malma (Walbaum) and the Nachikinsky char 1987; Kutschera & Epshtein, 2006). Salvelinus sp. (an undescribed species; see Boguts- Despite the fact that acanthobdellidans, a generally kaya & Naseka, 2004) as well as on parrs (juveniles) of recognised ‘missing link’, are of great importance for S. malma, Oncorhynchus mykiss (Walbaum) and the comparative morphology and evolutionary studies, little Nachikinsky char. Information on geographical local- is known about their biology and geographical distri- ities, hosts and infection indices are presented in bution, since the two species occur in hard-to-reach Table 1. The prevalence varied from 4 to 47.6%, and regions of northern Eurasia and neighbouring territories the intensity ranged from 1 to 27. of North America. There have been no detailed records In Lake Kronotskoe, the acanthobdellidans were of the little-studied P. livanowi for several decades. attached to the membrane between the fin rays, bases of This research is aimed at filling a gap in our knowledge the fins, opercula, throat pleats and the skin of the belly of the morphology, the occurrence and the biology of of Salvelinus schmidti, on the throat pleats and the skin P. livanowi in Kamchatka, north-eastern Russia. of the belly of S. albus and on the base of a fin and the belly of S. kronocius. In chars of the Kamchatka River basin and Lake Nachikinskoe, the acanthobdellidans Materials and methods were found on the fins and/or at their bases, usually on pelvic and pectoral fins, more rarely on the anal fin, and Acanthobdellidans were collected from fish hosts, on the body, except for one specimen found in the gill anesthetised in weak ethanol and subsequently fixed cavity of S. malma from the River Azabachya. In and preserved in 70 and 96% ethanol. Parasitological juveniles of O. mykiss of the River Krasnaya, the body surveys of fish (226 specimens of six species) were and fins were infected. Acanthobdellidan bites appear conducted at different times in several water bodies of as small red spots on the fish body (Fig. 1). Kamchatka. In the eastern part of the peninsula, fish External characters of all acanthobdellidan speci- were examined in the Kamchatka River basin (the mens collected and examined largely conform with Azabachya River and the rivers that flow into Lake previous descriptions of P. livanowi given by Epshtein Azabachye: the Snovidovskaya, Kultuchnaya and (1966, 1987) (Figs. 2–5). The individuals vary from Rybovodnyi Klyuch) and in two sites at Lake Kro- 2.00 to 13.30 mm (arithmetic mean, 5.15 mm) in notskoe; and in the western part of the peninsula: in the length. In preserved specimens, the body is white or basins of the River Kol’ (River Krasnaya) and the River yellowish, and the dorsum is somewhat darker than the Bol’shaya (Lake Nachikinskoe) (Table 1). Standard venter. Neither coloration pattern nor eyes are pre- parasitological indices were calculated. Altogether 122 served. The specimens have unpaired gonopores and a specimens were collected and identified; 53 were well-developed terminal posterior sucker. The anterior examined microscopically and photographed. Squash end bears five rows of chaetae, each with four pairs. preparations were made to examine chaetae. The There is a well-developed anterior sucker separated material is stored in the collection of invertebrates from the body by a constriction. In smaller individuals, of the Department of Zoology and Animal Ecology, the anterior sucker is less developed, and shovel-like, V.N. Karazin Kharkiv National University (52 specimens) with no conspicuous deepening between the chaetae. and the Museum of Nature, V.N. Karazin Kharkiv Chaetae of the fifth and fourth rows, as well as internal National University (1 specimen, MNKNU B-1753). chaetae of the third row, are broader than other chaetae. The prostomium, located anterior to the mouth, cannot be recognised with certainty in most Results specimens. Some individuals bear an inconspicuous tubercle prior to the mouth. The complete segment is According to published records (Sokolov, 2005; quadri-annulate. In some juvenile individuals, the Sokolov & Kuzishchin, 2005; Butorina et al., 2008) complete mid-body segment consists of two doubled 123 Syst Parasitol (2013) 84:71–79 Table 1 Localities, hosts and infection data for Paracanthobdella livanowi in Kamchatka (findings of Present study, Sokolov & Kuzishchin, 2005, and Butorina et al., 2008) Locality and dates Coordinates Host species Host Total number of Prevalence Intensity Mean Mean length (cm) hosts/number of (%)* range intensity* abundance* infected hosts R. Snovidovskaya, August 1998 56°16009.1900N, Salvelinus malma (parr) 9.8–17.7 20/1 5 2 2 0.1 161°72096.500E R. Kultuchnaya, August 1998 56°13035.2200N, Salvelinus malma 12.0–21.5 18/4 22.2 1–4 2 0.44 161°71037.7200E (parr and adult) Rybovodnyi Klyuch, 56°11055.5800N, Salvelinus malma (parr) 6.5–11.0 16/5 31.3 1–2 1.4 0.44 September 2001 161°79095.600E R. Azabachya, September 2001 56°19065.5800N, Salvelinus malma (parr) 9.5–14.0 10/1 1 161°98007.2700E L. Kronotskoe, March 2003 54°73051.2700N, Salvelinus schmidti (adult) 20.0–42.0 25/1 4 1 1 0.04 160°34003.0900E Salvelinus albus (adult) 25.0–45.0 10/2 1 Salvelinus kronocius (adult) 39.0–57.8 7/2 1–2 L. Kronotskoe, July–Aug 2011 54°4301.2000N, Salvelinus schmidti (adult) 32.5–44.6 21/10 47.6 1–27 5.6 2.67 160°21036.0000E Salvelinus albus (adult) 43.5–66.6 7/2 1 Salvelinus kronocius (adult) 58 1/1 1 R. Krasnaya, August 2003 53°50029.4400N, Salvelinus malma (parr) 8.1–12.1 26/9 34.6 1–5 1.9 0.65 156°08039.5900E Oncorhynchus mykiss (parr) 6.8–11.7 45/10 22.2 1–4 1.4 0.31 L. Nachikinskoe, October 2004 53°02013.9200N, Salvelinus sp. (parr and adult) 11.8–27.5 20/3 15 1–3 1.7 0.25 157°83009.6300E * Prevalence, mean intensity and mean abundance are calculated only for the host samples greater than 10 individuals 123 73 74 Syst Parasitol (2013) 84:71–79 Fig. 1 A specimen of Salvelinus kronocius (from Lake Kronotskoe) with multiple wounds on its belly caused by Paracanthobdella livanowi Fig. 2 Paracanthobdella livanowi, a specimen (length, 6.85 mm) collected on Salvelinus malma from the River Krasnaya (MNKNU B-1753): A, entire specimen, dorsal view; B, anterior end with five rows of chaetae and a cavity between them, ventral view.