Aquatic Invasions (2010) Volume 5, Issue 2: 201-205 This is an Open Access article; doi: 10.3391/ai.2010.5.2.12 © 2010 The Author(s). Journal compilation © 2010 REABIC

Open Access

201

Short communication

The finding of North American freshwater gastropods of the genus Planorbella Haldeman, 1842 (Pulmonata: Planorbidae) in East Siberia

Тatiana Sitnikova1*, Еlena Soldatenko2, Ravil Kamaltynov1 and Frank Riedel3

1Limnological Institute of SD RAS, Ulan-Batorskaya str. 3, Irkutsk, 664033, Russia 2Zoological Institute RAS, Universitetskaya nab., 1, Sankt-Petersburg, 199034, Russia 3Freie Universität Berlin, Institute of Geological Sciences, Berlin, Germany E-mail: sit@lin.irk.ru (TS), sold.zoo@mail.ru (ES), paleobio@zedat.fu-berlin.de (FR)

* Corresponding author

Received: 14 January 2010 / Accepted: 12 March 2010 / Published online: 19 March 2010

Abstract

Specimens belonging to North American representatives of the genus Planorbella Haldeman, 1842 of the gastropod family Planorbidae were found for the first time living at the inlet of a warm stream running from the Ust-Ilimsk Pulp and Paper Plant into the Angara River along with the two common indigenous species Galba truncatula (Pulmonata: Lymnaeidae) and Sibirenauta sibirica (Pulmonata: Physidae). Morphological studies of the shell, the radula and the genitals showed that the newly found Planorbella specimens can most likely be attributed to P. duryi duryi (Wetherby, 1879) while it also contains morphological characters of other species in this genus. It is assumed that the occurrence of Planorbella in East Siberian water bodies is a result of unintentional release from aquarium tanks.

Key words: alien species, Planorbella, water bodies, East Siberia

The number of reports of non-indigenous gastropods invading new geographical regions has greatly increased during the recent years. For instance, Roll et al. (2008) listed nineteen alien freshwater gastropod species introduced to Israel water bodies, one of them identified as Planor-bella duryi (Wetherby, 1879) originating from North America (e.g. Baker 1945; Clarke 1981). In Italian inland waters eleven non-indigenous gastropods were detected, two of which assigned to Planorbella duryi and P. anceps (Menke, 1830). P. duryi was found in natural habitats in five localities, whereas P. anceps was found in a single site only (Cianfanelli et al. 2007). Apart from Italy, species of the genus Planorbella Haldeman, 1842 – P. anceps, P. duryi and/or P. trivolvis (Say, 1817) – were also identified in various European countries such as Iceland, France (including Corsica), Malta, Portugal (including Madeira), Spain, United Kingdom, Denmark, Germany, Hungary, Poland, Latvia, Ukraine, and the countries which share Lake Prespa, i.e. Albania, Greece and Macedonia (Eröss et al. 2005; Anistratenko and Haliman, 2006; Gollasch and Nehring 2006; Cianfanelli et al. 2007; Son 2007; Glöer and Meier-Brook 2003

etc.). In West Siberia, in a cooling water reservoir at the Tyumen Heat and Power Plant, eleven gastropod species were found, four of which are alien gastropods. One of them, Ferrissia wautieri (Mirolli, 1960), was dominant in both mass and abundance (Sharapova 2008). In the Novosibirsk reservoir of the Ob River, the European gastropod species Viviparus viviparus (Linnaeus, 1758) was found to have colonized the littoral zone in abundances of up to 6 kg/m2 (Andreev et al. 2008). There was even a finding of the tropical snail Pomacea caniculata (Lamarck, 1819), usually found in home aqua-riums, in the discharge outfall from Belovskaya thermal power plant in West Siberia (Yanygina et al. 2009). However no species of Planorbella has been found to date at this site. All of the investigators mentioned above agree that one of the ways to introduce gastropods into new habitats is by the aquarium trade.

Non-indigenous gastropod species have not yet been reported as invading inland waters of East Siberia, including Lake Baikal and adjacent areas. The present study thus represents the first report of an alien freshwater gastropod in East Siberia.

Т. Sitnikova et al.

202

Gastropods were collected from the inlet of a relatively warm and shallow stream Katymovo (Figure 1C) which flows into the Angara River (Figure 1A). The sampling site is 3 km downstream of Ust-Ilimsk town (58°01,939'N and 102°45,070'E). At time of sampling, the depth of the stream was approximately 10 cm, its bed being composed of small and medium-sized boulders, pebbles and gravels (Figure 1B), which are usually covered by silt and small macrophytes. Local people reported that the stream represents an outflow of the main discharge of Ust-Ilimsk Pulp and Paper Plant. Its water temperature was ca. 18°С, which is about 11°С higher than that of the Angara River.

Gastropods were collected from the exposed parts of the boulders and fixed in 70% ethanol. The samples were examined under a light stereomicroscope (Leica and MBC-10), as well as by means of an electron scanning microscope (SEM) HITACHI (Model S-570). Prior to the investigations with the aid of the SEM, the radulae and penises were cleaned, washed in ethyl alcohol of various concentrations, dried and platinum shadowed in a vacuum tube of ion shadowing HITACHI IB-5. To identify the gastropod species and describe the morphology of Planorbella, we used the publications of Baker (1945), Hubendick (1955), Kerth (1983), Burch and Jung (1992), Clarke (1981), Staro-bogatov (1990), Taylor (2003), Glöer (2002) and Starobogatov et al. (2004).

Altogether 28 specimens of 3 gastropod species were obtained from the sampling site: 2 specimens of Galba truncatula (Müller, 1774) (Lymnaeidae), 23 specimens of Sibirenauta sibirica (Westerlund, 1876) (Physidae) and 3 specimens of Planorbella (Planorbidae).

The Planorbella specimens exhibit almost identical shell morphologies and similar sizes, the diameter being 8-9.5 mm at 4-4.5 whorls. The shells were sinistral (dextral in P. anceps), with a flat spire of planorboid shape which is not inverted. The shell surface was smooth except for growth increments, a bit glossy (Figure 2A-C) and without basal carinae and thread-like striae. The aperture was not strongly expanded and exhibits a thin outer lip. In respect of the soft parts, foot, tentacles and snout were dark purplish with fine whitish dots. The body was characterized by brown spots which were visible through the shell (Figure 2B). One of the three specimens was juvenile, the other two were mature. The penial complex of the latter was of bilobate shape, about 3 mm long, including

Figure 1. Study area. A – Angara River, inlet of a stream; B – sampling site, a small backwater formed by the stream mouth; C – stream. Photos by R. Kamaltynov.

Planorbella in East Siberia

203

Figure 2. Shell (A–C), radular teeth (D–E) and genital apparatus (F–H) of Planorbella duryi duryi. Scale bar: A–C 1 mm, D – 150 μm, E – 10 μm, G – 300 μm, H – 30 μm. Photographs by E. Soldatenko.

penial sheath with a massive penis and praeputium with a praeputial organ (Figure 2F) similar to that of P. duryi. The distal end of the penial sheath and proximal end of the prae- putium were connected by the accessory duct. The penis was encased in the connective-tissue sheath, which is lined on the outside with prismatic epithelium. The ejaculatory duct of the penis opened 0.5 mm from the papilla as was shown by Hubendick (1955). The terminal part of the penis was covered by a thin cuticle and had a small tip (stylet) (Figure 2G-H) that has not been mentioned in literature for P. duryi. The

praeputial organ was cup-shaped and its length was almost equal to that of the penis of P. trivolvis. The cup of the penial gland was bilobated similar to that of P. duryi.

The radula was musivoglossate, with a ribbon length of 1.9-2.1 mm and a width of 0.80-0.86 mm. It consisted of about 124-130 bilaterally symmetrical transverse rows of 41-45 teeth (Figure 2D), with 20-22 marginal teeth on each side of the central tooth (9 primary and 11-13 secondary teeth). The radular formula thus was 20(22) –1 – 20(22). Teeth were positioned in a way that they do not directly adjoin (Figure 2D).

Т. Sitnikova et al.

204

The primary marginal teeth always had plates with 3 main cusps, the central one of which was often bicuspid. The secondary marginal teeth were very narrow with 4-6 cusps. The central teeth were comparatively small (Figure 2E). The base of a central tooth was trapezoid and became narrower at the dental rectangular plate. The dental plate was half of the length of the base and bore 2 cusps. Radular teeth morphology and size of investigated specimens were similar to those of P. duryi and P. trivolvis but the radular formula and a comparatively small number of transverse rows coincided more with P. truncatum.

It should be mentioned that there were some similarities between the investigated specimens and P. truncatum (Miles, 1861), e.g. a flat umbilicus and relatively small size of mature specimens (less than 10 mm). Significant variation of the anatomy of Planorbella species living in their natural environment has been described (Baker 1945) and makes identification at the species level difficult. However, considering all characters described here, we are confident that our Planorbella specimens most likely represent P. duryi duryi (Wetherby, 1879), subgenus Seminolina Pilsbry, 1934.

Note that fossil shells identified as Helisoma trivolvis (= Planorbella trivolvis) were found in the Pleistocene deposits of the Kolyma River (north-eastern Russia) (Lindholm 1932). However, no other reports on fossil or modern Planorbella findings in present water bodies of East Siberia are available at the moment.

According to Starobogatov et al. (2004), the Eurasian Galba truncatula and the Siberian Sibirenauta sibirica inhabit small water bodies of Russia, including Pribaikalye. The third species we found and assigned to the planorbid genus Planorbella has its origin in North America and is clearly an invader which is new to the aquatic fauna of East Siberia. Planorbella species are common from Arctic Canada to Florida, being sporadically introduced to other regions by aquarium hobbyists and water gardeners (Dillon 2000, 2007). It is known that natural populations for example of P. trivolvis occurring in eutrophic waters are characterized by an annual life cycle, while in mesotrophic waters individuals grow slower and live approximately two years (Eversole 1978). Reproduction under aquarium tank conditions starts at a water temperature of 20°С, with maximal egg attachment occurring at 24°C. The snails become mature at an age of 3-4 months

(Van der Schalie and Berry 1973). P. trivolvis is an R-adapted or R-selected species with a high proportion of available energetic resource for reproduction (Dillon 2000).

Aquarium trade is well developed in East Siberia, including Ust-Ilimsk. Therefore the occurrence of North American gastropods in the vicinity of this city in our opinion could be the result of aquarium release. The warm water in the stream running from the cooler of the Pulp and Paper Plant appeared favorable for these snails migrating 3 km downstream and reaching the Angara River. So far no Planorbella specimens have been found in the Angara River proper. Whether or not the snails reproduced and can survive the winter in this comparatively warm biotope is not yet known and difficult to predict.

Acknowledgements

The authors thank G. Dvoeglazova for field assistance, E. Timoshkina for the initial English version of this paper, Dr. Peter Glöer for the important critical comments and Dr. Frances Lucy for editing English. This work has partially been supported by RFBR Grants № 08-04-10077k and 08-04-98034 and Integration Project of the Siberian Branch of the Russian Academy Science № 49.

References

Andreev NI, Andreeva SI, Vinarski MV, Lazutkina EA (2008) Alien species of mollusks in water bodies of Western Siberia. Ecologic-economical effect of the nature management during the recent stage of development in the West-Siberian region. Data II International scientific-practical conference. Omsk, pp 7-10

Anistratenko VV, Haliman IA (2006) The bivalve mollusc Anadara inaequivalvis (Bivalvia, Arcidae) in the northern part of the Sea of Azov: completion of colonization of the Azov-Black Sea Basin. Vestnik Zoologii 40(6): 505-511

Baker FC (1945) Molluscan family Planorbidae. Urbana, University of Illinois Press, 530 pp

Burch JB, Jung Y (1992). Freshwater snails of the University of Michigan Biological Station area. Walkerana 5(13): i-vi, 1-216

Cianfanelli S, Lori E, Bodon M (2007) Non-indigenous freshwater molluscs and their distribution in Italy. In: F. Gherardi F (ed) Biological invaders in inland waters: Profiles, distribution and threats. Springer, The Nether-lands, pp 103-121, doi:10.1007/978-1-4020-6029-8_5

Clarke AH (1981) The freshwater molluscs of Canada.

National Museum of Natural Sciences, Ottawa, 46 pp Dillon RT (2000) The ecology of freshwater molluscs.

Cambridge University Press, 509 pp, doi:10.1017/ CBO9780511542008

Dillon RT (2007) Freshwater gastropods of North America project (available from: http://www.cofc.edu/~fwgna/spe cies/planorbidae/h_trivolvis.html, accessed 17th February 2010)

Planorbella in East Siberia

205

Eversole AG (1978) Life cycles, growth and population bioenergetics of the snail, Helisoma trivolvis (Say). Journal of Molluscan Studies 44: 209-222

Eröss ZP, Fehér Z, Hunyadi A (2005) Invasion of a North American alien, Planorbella anceps (Menke, 1830) (Mollusca: Gastropoda: Planorbidae), in the ancient Lake Prespa. Tentacle 13: 6-7

Gollasch S, Nehring S (2006) National checklist for aquatic alien species in Germany. Aquatic Invasions 1: 245-269, doi:10.3391/ai.2006.1.4.8

Glöer P (2002) Süßwassergastropoden Nord- und Mittel-europas. Conchbooks, Hackenheim, 446 pp

Glöer P, Meier-Brook C (2003) Süsswassermollusken. Ein Bestimmungsschlüssel für die Bundesrepublik Deutschland, 13th ed. DJN, 134 pp

Hubendick B (1955) Phylogeny in the Planorbidae. Transactions of the Zoological Society of London 28: 453-542

Kerth K (1983) Radulaapparat und Radulabildung der Mollusken. I. Vergleichende Morphologie und Ultra-struktur. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 110: 205-237

Lindholm WA (1932) On the finding of American Helisoma trivolvis Say (Gastropoda, Planorbidae) in the Pleisto-cene of Kolyma River. Trudy Soveta po izucheniyu proizvoditel’nyh sil, Ser. Yakutskaya, 11: 65-72

Roll U, Dayan T, Simberloff D, Miens HK (2009) Non-indigenous land and freshwater gastropods in Israel. Biological Invasions 11: 1963-1972, doi:10.1007/s10530-008-9373-4

Sharapova TA (2008) Distributional and ecological peculiarities of invading mollusks in the cooler reservoir at the Tyumen Heat and Power Plant in West Siberia. Vestnik zoologii 42(2): 185-187

Starobogatov YaI (1990) Tendency of evolutionary trans-formations of radulae of modern mollusks In: Shileiko AA (ed), Evolyutsionnaya morfologiya mollyuskov (Zakonomernosti morfofunktsional’nykh perestroek radulyarnogo apparata) [Evolutionary morphology of mollusks (Consistent patterns of morphofunctional rearrangements of the radular apparatus)], Moscow State University, Moscow, pp 37-91

Starobogatov YaI, Prozorova LA, Bogatov VV, Saenko EM (2004) Molluscs. In: Tsalolikhin S (ed), Key to freshwater invertebrates of Russia and adjacent lands, Nauka, St.Petersburg, 6: 6-492

Son MO (2007) Invasive mollusks in fresh and brackish waters of the northern Black Sea region. Odessa, Druk, 132 pp

Taylor DW (2003) Introduction to Physidae (Gastropoda: Hygrophila); biogeography, classification, morphology. Revista de Biologia Tropical 51 (Suppl. 1): 1-287

Van der Schalie H, Berry E (1973) The effects of temperature on growth and reproduction of aquatic snails. Sterkiana 50: 1-9

Yanygina L, Kirillov V., Zarubina E (2009) Invasive species in the biocenosis of the cooling reservoir of Belovo Power plant (The south of west Siberia). Russian Journal of Biological Invasions 2: 60-68