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SPIXIANA 38 2 161-168 München, Dezember 2015 ISSN 0341-8391

First Russian record of Erpobdella monostriata: DNA barcoding and geographical distribution

(Annelida, Hirudinida, Erpobdellidae)

Serge Utevsky, Pavel G. Dubov & Alexander A. Prokin

Utevsky, S., Dubov, P. G. & Prokin, A. A. 2015. First Russian record of Erpob­ della monostriata: DNA barcoding and geographical distribution (Annelida, Hiru­ dinida, Erp­obdellidae). Spixiana 38 (2): 161-168. New information on the range of Erpobdella monostriata (Lindenfeld & Pietrus­ zynski, 1890) was obtained. Results of our study show that this leech occurs not only in Central Europe but reaches European Russia. However, E. monostriata has not been recorded from the vast interspace between its localities in Central Europe and a dystrophic lake in the Voronezh Oblast in Russia, the easternmost spot of its range known so far. The taxonomic identity of the leeches was confirmed both by a morphological examination and a molecular phylogenetic analysis based on COI sequences. Genetic differentiation between western and eastern samples of the species points towards exploring more specimens and markers. If not disjunct, the present geographical gap of records may be explained by low population sizes and the scarcity of suitable habitats; recent climate changes might cause population expansions in the east. Serge Utevsky, Department of Zoology and Animal Ecology, V. N. Karazin Kharkiv National University, Maidan Svobody 4, Kharkiv 61022, Ukraine; e-mail: [email protected] Pavel G. Dubov, Voronezh State University, Universitetskaya sq., 1, Voronezh 394006, Russia Alexander A. Prokin, Voronezh State University, Universitetskaya sq., 1, Voro­ nezh 394006, Russia; and Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Nekouz district, Yaroslavl Oblast 152742, Russia; e-mail: [email protected]

Introduction has been found non-monophyletic (Siddall 2002). Further phylogenetic analyses and taxonomic revi­ Erpobdellid leeches are common members of fresh­ sions are needed to reveal the evolutionary history water benthic communities. They are macrophagous of erpobdellids and resolve taxonomic uncertainties. predators of aquatic invertebrates originating from The taxonomy of a number of common erpob­ hematophagous ancestors (Siddall 2002). Some of the dellid species has been confused or neglected. The species in this group have been used in ecological taxonomic identity of Erpobdella monostriata (Lin­ studies and water quality assessment (Lukin 1976, denfeld & Pietruszynski, 1890) was confused for a Schenková et al. 2007, Nesemann & Moog 2002). The long time since its formal description. This taxon classical systematics of erpobdellids was based on was initially described as Nephelis octoculata var. the annulation of segments. In the molecular phylo­ monostriata Lindenfeld & Pietruszynski, 1890. Then genetic era, the importance of annulation has been the preoccupied epithet “monostriata” was employed reconsidered and the genus Erpobdella sensu stricto again to designate another leech taxon, Herpobdella

161 ©Zoologische Staatssammlung München/Verlag Friedrich Pfeil; download www.pfeil-verlag.de atomaria var. monostriata Gedroyb, 1916, which is ding to the description in the literature. The Google currently recognized as a synonym of the correct Earth (version 4.3) online application (http://earth. designation of this species, Erpobdella vilnensis (Lis­ google.com/) was used. The record points were plotted kiewicz, 1925) (Agapow & Bielecki 1992, Nesemann on a map using QGIS 2.0. & Neubert 1999). In his seminal monographs, Lukin (1962, 1976) DNA extraction, amplification and sequencing mentioned only “Erpobdella monostriata” (Gedroyb, Small pieces (approx. 5 × 2 × 1 mm) of skin and muscle 1916) for the Carpathians and adjacent areas and tissue were cut from the lateral part of the body. Care did not record Erpobdella monostriata (Lindenfeld was taken not to reach the digestive system, which often & Pietruszynski, 1890) for Ukraine and the former contains remnants of unknown prey species. Genomic USSR. Recently Utevsky et al. (2012) have recorded DNA was isolated using the GENE ELUTE Mammalian Erpobdella vilnensis (Liskiewicz, 1925) from the Genomic DNA minprep kit from Sigma-Aldrich (Stein­ Ukrainian Carpathians and south-western Ukraine heim, Germany). The mitochondrial cytochrome oxidase subunit one and by doing so fixed the nomenclatural problem (COI) fragment was amplified using LSO and HCO E. vilnensis E. monostriata of confusing with at the primers described in Folmer et al. (1994). PCR was putative eastern border of the range of the former. performed by applying 35 cycles of 1 min at 94 °C, 1 min At the same time, the geographical distribution of E. at 46 °C, and 2.5 min at 72 °C, following a 4 min dena­ monostriata is still poorly studied. It has been unclear turation step at 94 °C. In order to purify the PCR pro­ how far its range extends to the east. Until recently ducts two enzymes, Exonuclease I and Shrimp alkaline Erpobdella monostriata was not found in the former phosphatase (SAP) (Fermentas, Thermo Fisher Scienti­ Soviet Union (Lukin 1962, 1976) and newly inde­ fic, USA), were used. Exonuclease I (0.2 μl) and SAP pendent countries of Eastern Europe. This research (1 μl) were added to 10 μl of the PCR product. After that, addresses the information gap in our knowledge of the mixture was incubated for 45 min at 37 °C and fol­ the geographical distribution of E. monostriata. lowed by a 15 min incubation at 80 °C. The purified products were sequenced in both directions with ampli­ fication primers under BIG DYE Terminator cycling conditions, purified by ethanol precipitation, and run Material and methods on an Applied Biosystems 3730xl sequencer by Macro­ gen (Seoul, Korea). Sequence chromatograms were Sample collection edited and assembled with the help of ChromasPro 1.32 Samples of E. monostriata were collected during the (Technelysium Pty., Queensland, Australia). The cor­ summer season of 2011 and on 16th June, 2013 from a rectness of COI sequences was verified at the amino acid small forest lake Ugolnoe in the Usman Pine Forest in level. The obtained sequences were assigned GenBank the Voronezh Oblast, Russia near the village of Maklok Accession Numbers. Some COI sequences belonging to (51°48'40.20" N, 39°24'23.58" E), relaxed in 10 % ethanol, other erpobdellid species from previous studies were fixed and preserved in 96 % ethanol. Altogether, 37 in­ also used for inferring a phylogenetic tree (Table 1). dividuals were studied by using morphological and molecular methods. A newly sequenced specimen of Phylogenetic analysis Erpobdella vilnensis from the Mykolayiv Oblast, Ukraine The COI sequences were unambiguously aligned using (see Utevsky et al. 2012) was also used for the analysis. ClustalW associated with BioEdit v7.1.7 (Hall 1999). The The specimens are stored in the collection of inverte­ length of the aligned COI sequences was 660 bp. The brates of the Department of Zoology and Animal Eco­ best-fit models for each partition, the first, second and logy, V. N. Karazin Kharkiv National University. third codon positions of COI, were identified with the Bayesian information criterion (Schwarz 1978) using Measurements KAKUSAN4 (Tanabe 2011): GTR with proportion of Measurements were made with an eyepiece micrometer. invariant sites (+I), HKY85+I and HKY85 with gamma Arithmetical means of the body length and width and distribution (+G) respectively. their standard errors were calculated. The measure­ Phylogenetic relationships were determined by ments were based on 32 specimens. Bayesian inference using MrBayes v3.1.2. (Ronquist & Huelsenbeck 2003). Two arhynchobdellid species Hiru­ do orientalis Utevsky et Trontelj, 2005 (Hirudiniformes) Mapping and Orobdella jimai Oka, 1895 (Erpobdelliformes) were Geographical coordinates were assigned to the new and used as outgroup taxa to reveal the phylogenetic relati­ previous localities where E. monostriata was found. onships between erpobdellid taxa. Searches were per­ Agapow & Bielecki (1992) and later publications were formed in two parallel runs with four chains each for considered. In the field, the geographical position was five million generations, sampled every 100th generati­ determined using a global positioning system (GPS) on. After discarding the first 25 % of the sampled trees, device. In other cases, localities were identified accor­ final topologies were consented following the 50 %

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majority rule. Numbers of base differences per site catchment area; the balance of biogeochemical fluxes (p-distances) and their standard errors were calculated changes due to dramatic alterations in vegetation and using MEGA5 (Tamura et al. 2011). soil permeability (Bitner et al. 2001, Meyer et al. 1995, Strauss & Lamberti 2000). Habitat

The basin of the Ugolnoe Lake is a former riverbed of Results a left-bank tributary of the Voronezh River, ceased to exist during the formation of the estuary of the Usman Morphology River during an activation of the Voronezh neotectonic uplift (Khlyzova et al. 2007). The name “ugolnoe” comes External characters (Fig. 1) of the specimens exam­ from a facility that was located here in the late 19th and ined are in agreement with the previous description early 20th centuries to produce birch charcoal. According of E. monostriata by Nesemann & Neubert (1999). The to hydrochemical characteristics determined by Zhi­ leeches are small, the average total length including votova & Koroteeva (2002), the lake should be classified suckers is 15.13 ± 0.56 mm (range 8.50-21.00 mm). as a dystrophic (humic) water. The maximum body width is 2.16 ± 0.12 mm (range Forest wildfires of 2010 had a significant impact on 1.50-5.20 mm). The body surface is smooth, papillae the hydrochemical and hydrobiological regime of wa­ ters of the Usman Pine Forest, including the Ugolnoe are lacking. A mid-body segment consists of five Lake. It is known that after wildfires the absolute and annuli equal in length. The gonopores are separated relative (compared to nitrogen) content of organic car­ by four annuli. The coloration of living leeches is bon and a number of ions increased in surface waters light brownish. All preserved specimens have a due to the accumulation of ash and fly ash from the mid-dorsal dark longitudinal stripe located along

Table 1. Collection sites and sequence accession data for the leech species analysed.

Species Collection site GenBank Reference accession No. Erpobdella monostriata Voronezh Oblast, Russia KP300764 This study (Lindenfeld & Pietruszynski, 1890) Erpobdella monostriata Mecklenburg-Western HM246601 Trajanovski et al. 2010 (Lindenfeld & Pietruszynski, 1890) Pomerania, Lake Neustädter See, Germany Erpobdella monostriata Magdeburg, Germany DQ009665 Pfeiffer et al. 2005 (Lindenfeld & Pietruszynski, 1890) Erpobdella nigricollis (Brandes, 1899) Kassel-Wehlheiden, Germany DQ009664 Pfeiffer et al. 2005 Erpobdella nigricollis (Brandes, 1899) Mecklenburg-Western HM246603 Trajanovski et al. 2010 Pomerania, Lake Neustädter See, Germany Erpobdella testacea (Savigny, 1820) France AF116027 Apakupakul et al. 1999 Erpobdella vilnensis (Liskiewicz, 1925) A stream flowing to the KP300763 This study, Utevsky et al. 2012 Southern Bug, Mykolayiv Oblast, Ukraine Erpobdella vilnesis (Liskiewicz, 1925) Wörlitzer Park, Germany DQ009663 Pfeiffer et al. 2005 Erpobdella vilnensis (Liskiewicz, 1925) Mecklenburg-Western HM246585 Trajanovski et al. 2010 Pomerania, Germany Erpobdella octoculata (Linnaeus, 1758) Uzbekistan HQ336344 Oceguera-Figueroa et al. 2011 Erpobdella octoculata (Linnaeus, 1758) Lake Ohrid, Macedonia HM246555 Trajanovski et al. 2010 Erpobdella octoculata (Linnaeus, 1758) Lake Prespa, Macedonia HM246599 Trajanovski et al. 2010 Dina ohridana Sket, 1968 Lake Ohrid, HM246594 Trajanovski et al. 2010 Albania/Macedonia, Dina lepinja Sket & Šapkarev, 1986 Macedonia, Lake Ohrid HM246539 Trajanovski et al. 2010 Dina lineata (O. F. Müller, 1774) Mecklenburg-Western HM246611 Trajanovski et al. 2010 Pomerania, Germany Trocheta haskonis Grosser, 2000 Wörlitzer Park, Germany DQ009668 Pfeiffer et al. 2005 Orobdella jimai Oka, 1895 Nagano, Japan AB679674 Nakano 2012 Hirudo orientalis Utevsky & Trontelj, 2005 Azerbaijan JN104645 Trontelj & Utevsky 2012

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Fig. 2. Phylogenetic relationships between major groups of Palaearctic erpobdellids obtained by Bayesian inference Fig. 1. Erpobdella monostriata (Lindenfeld & Pietruszynski, and based on COI sequences. Posterior probabilities are 1890). A. Entire specimen with a characteristic mid- shown for clades. The tree is rooted at Hirudo orientalis. dorsal dark longitudinal stripe. B. Clitellum, ventral view, with two gonopores separated by four annuli: M, male gonopore; F, female gonopore. Erpobdella species are shown in Table 3. The sample of E. vilnensis collected in south-western Ukraine (Utevsky et al. 2012) joined a well-supported clade the entire body without interruption. The stripe is with its conspecifics. blurred and associated with clouds of dark pigment in many specimens. In most of living leeches, the Geographical distribution stripe is indistinct or lacking whereas this distin­ guishing feature emerges in specimens fixed and Altogether 64 localities of E. monostriata were con­ preserved in strong ethanol. sidered. Its range reaches as far to the west as 06°22'07.82" in the Netherlands. The easternmost Barcoding and phylogeny locality is 39°24'23.58", a new record from the Rus­ sian Federation. The northern frontier of the explored The resulting Bayesian tree (Fig. 2) indicates that the sample of the leech specimens collected in Russia Table 2. The number of base differences per site from joined a clade with two other samples of E. mono­ averaging over all sequence pairs within each Erpobdella striata from Germany. The posterior probability of the species (π) and its standard error (based on p-distances). monophyletic group is 1.00. The p-distances between the Russian sample and two sequences HM246601 Species π and DQ009665 are 0.015 ± 0.005 and 0.018 ± 0.006 re­ E. monostriata 0.014 ± 0.005 spectively. The p-distance between the two samples E. nigricollis 0.002 ± 0.001 originating from Germany is as low as 0.004 ± 0.003. The mean p-distance within E. monostriata was E. vilnensis 0.018 ± 0.006 0.014 ± 0.005 (Table 2). The distances between the E. octoculata 0.057 ± 0.022

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Fig. 3. Geographical distribution of Erpobdella monostriata (Lindenfeld & Pietruszynski, 1890). Previous records are mapped with circles and the new record from Russia is represented by a star. range of E. monostriata is 56°04'08.73" in Sweden et al. 2008, Raczyñska & Chojnacki 2009, Koperski (Fig. 3). The southern frontier of the range is still 2010, Koszalka 2012), Lithuania (Uwe Jueg, personal unclear (see below). Reliable records of E. mono­ communication), Belarus (Haaren et al. 2004) and striata were found for eight European countries: the Russia (this research). Netherlands (Haaren et al. 2004), Germany (Grosser 1996, 2003, Jueg 1998, 2013, Jueg et al. 2007, Haesloop 2002, Pfeiffer et al. 2005, Westendorff et al. 2008, Discussion Trajanovski et al. 2010, Enting & Arndt-Dietrich 2012), Denmark (Trontelj et al. 1996), Sweden (Uwe Both morphological and molecular analyses showed Jueg, personal communication), Poland (Agapow that the leeches sampled in the Ugolnoe Lake, Voro­ & Bielecki 1992, Fleituch 2003, Bielecki et al. 2004, nezh Oblast, Russia should be assigned to Erpobdella 2011a,b, Szczèsny 2005, Nabodnik et al. 2004, Aga­ monostriata (Lindenfeld & Pietruszynski, 1890). The pow et al. 2006, Agapow & Nabodnik 2006, Agapow leeches possess a distinguishing feature of the spe­

Table 3. The number of base differences per site from averaging over all sequence pairs between Erpobdella species and their standard errors (based on p-distances).

Species 1 2 3 4 1 E. monostriata 2 E. nigricollis 0.096 ± 0.012 3 E. testacea 0.131 ± 0.013 0.116 ± 0.012 4 E. vilnensis 0.117 ± 0.013 0.107 ± 0.013 0.132 ± 0.013 5 E. octoculata 0.139 ± 0.013 0.117 ± 0.012 0.124 ± 0.012 0.123 ± 0.012

165 ©Zoologische Staatssammlung München/Verlag Friedrich Pfeil; download www.pfeil-verlag.de cies, the mid-dorsal dark longitudinal stripe located by Lukin (1929) for the Kharkiv Oblast of north- along the entire body. That coloration pattern has eastern Ukraine. never been found in other Erpobdella species. The There are no impermeable geographical barri­ COI tree recovers a well-supported clade of Erp­ ers in Eastern Europe that could disrupt the range obdella monostriata. The eastern specimen differs of E. monostriata. However, our analysis revealed a by less than 2 % from GenBank sequences of two substantial genetic differentiation between western western E. monostriata, but the latter form a strongly and eastern populations of the species. These dif­ supported clade, suggesting geographic structure. ferences can be caused by isolation by distance or Being more than eight times higher than within distinct postglacial colonization histories that have species differences of E. monostriata, the p-distance been already reported for freshwater leeches in the between E. monostriata and other Erpobdella species Western Palaearctic (Trontelj & Utevsky 2012). ranges from 0.096 to 0.139. This can be considered The lack of Eastern European records may be as reliable evidence of the species status of the also explained by low population sizes and the E. monostriata clade (see Birky 2013). Our analyses scarcity of suitable habitats. According to previous also corroborated species-level genetic differences records, in 2000 only one individual of this species between E. monostriata and E. vilnensis that went designated as “Erpobdellidae sp.” was found in the through a long period of nomenclatural confusions Sinyutino bog situated in the Usman Pine Forest (see Agapow & Bielecki 1992). Further analyses (Prokin & Silina 2007). It might be supposed that dealing with more samples and diverse molecular recent climate changes, i. e. exceptionally warm and markers are necessary to reveal accurate intraspe­ dry springs and summers in 2010 and 2011 (All- cific relationships within E. monostriata and its place Russian Research Institute of Hydrometeorological among other erpobdellid taxa. Information 2013) and forest wildfires (see above) Recent studies suggest that ranges of a number have favoured a population expansion in the Ugol­ of Western Palaearctic leech species extend more noe Lake and after that E. monostriata could be found easterly then considered before. For example, Hirudo during an ecological survey. Moreover, we cannot verbana Carena, 1820 occurs in Uzbekistan (Utevsky suppose any invasive pathways and vectors for this et al. 2010) and E. vilnensis has been recorded from species’ range expansion. We can further speculate south-western Ukraine (Utevsky et al. 2012) and that the environmental changes are not favourable Kyrgyzstan (Jueg et al. 2013). Our research, in turn, for E. monostriata in the long term as this leech prefers indicates that E. monostriata, recorded mainly from colder boreal freshwaters of Europe. Central Europe, reaches the Don basin in Russia in This research suggests that E. monostriata occurs the eastern portion of its known range. Records from from the Netherlands to the European Russian Feder­ the Czech Republic, Slovakia, Hungary and Greece ation. Its range may extend even more easterly where (Fauna Europaea 2013) and Spain (Camargo 1992) favourable habitats and climate conditions occur. should be substantiated. According to Vladimír Košel’s personal communication, E. monostriata does not occur in Slovakia and the Czech Republic. Acknowledgements The southernmost recent record has been made in This research was supported in part by a grant from the Bulgaria (Moskova & Uzunov 2011). The species Slovenian-Ukrainian Intergovernmental Science & was also recorded from the Upper Tisza (Zakarpat­ Technology Cooperation Program. The pictures and tia, Ukraine) (Afanasyev et al. 2013). The two latter DNA sequences of E. monostriata and E. vilnensis were records were made from mountain rivers that are obtained using the facilities and equipment of the De­ not typical habitats of E. monostriata, which prefers partment of Biology, University of Ljubljana, courtesy lowland lakes and less often rivers (Agapow & of Prof. Boris Sket and Prof. Peter Trontelj. Our special Bielecki 1992, Jueg 2013). Moreover, the records are thanks go to Andrei Atemasov for mapping occurrence not based on morphological examinations. Therefore, records of E. monostriata. We are very thankful to Uwe the southern frontier of the species range remains Jueg and Vladimír Košel for the important information unclear. Erpobdella monostriata has not been found in on the geographical distribution of E. monostriata. the vast interspace between its localities in Central Europe and the new locality in the Voronezh Oblast References (Fig. 3). It is still unknown whether E. monostriata occurs in Ukraine but we may hypothesize that the Afanasyev, S. A., Lietitskaya, Y. N. & Manturova, O. V. species could be either overlooked or confused with 2013. Altitude distribution and structural organi­ related erprobdellid leeches between its eastern and zation of hydrobionts’ communities in the rivers western localities recorded in the previous studies. of the mountainous part of the Tisa River basin. This species might be recorded as Erpobdella testacea Hydrobiological Journal 49 (4): 16-25.

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