sign in sign up
<<
Home , Galba (gastropod), Helisoma, Hygrophila (gastropod), Planorbella, Planorbella duryi, Planorbella trivolvis

Aquatic Invasions (2010) Volume 5, Issue 2: 201-205 This is an Open Access article; doi: 10.3391/ai.2010.5.2.12 Open Access

© 2010 The Author(s). Journal compilation © 2010 REABIC

Short communication

The finding of North American freshwater gastropods of the Haldeman, 1842 (: ) 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: [email protected] (TS), [email protected] (ES), [email protected] (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 truncatula (Pulmonata: ) and Sibirenauta sibirica (Pulmonata: ). Morphological studies of the shell, the 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 etc.). In West Siberia, in a cooling water gastropods invading new geographical regions reservoir at the Tyumen Heat and Power Plant, has greatly increased during the recent years. For eleven gastropod species were found, four of instance, Roll et al. (2008) listed nineteen alien which are alien gastropods. One of them, freshwater gastropod species introduced to Israel wautieri (Mirolli, 1960), was dominant water bodies, one of them identified as Planor- in both mass and abundance (Sharapova 2008). bella duryi (Wetherby, 1879) originating from In the Novosibirsk reservoir of the Ob River, the North America (e.g. Baker 1945; Clarke 1981). European gastropod species Viviparus viviparus In Italian inland waters eleven non-indigenous (Linnaeus, 1758) was found to have colonized gastropods were detected, two of which assigned the littoral zone in abundances of up to 6 kg/m2 to and P. anceps (Menke, (Andreev et al. 2008). There was even a finding 1830). P. duryi was found in natural habitats in of the tropical Pomacea caniculata five localities, whereas P. anceps was found in a (Lamarck, 1819), usually found in home aqua- single site only (Cianfanelli et al. 2007). Apart riums, in the discharge outfall from Belovskaya from Italy, species of the genus Planorbella thermal power plant in West Siberia (Yanygina Haldeman, 1842 – P. anceps, P. duryi and/or et al. 2009). However no species of Planorbella P. trivolvis (Say, 1817) – were also identified in has been found to date at this site. All of the various European countries such as Iceland, investigators mentioned above agree that one of France (including Corsica), Malta, Portugal the ways to introduce gastropods into new (including Madeira), Spain, United Kingdom, habitats is by the aquarium trade. Denmark, Germany, Hungary, Poland, Latvia, Non-indigenous gastropod species have not Ukraine, and the countries which share Lake yet been reported as invading inland waters of Prespa, i.e. Albania, Greece and Macedonia East Siberia, including and adjacent (Eröss et al. 2005; Anistratenko and Haliman, areas. The present study thus represents the first 2006; Gollasch and Nehring 2006; Cianfanelli et report of an alien freshwater gastropod in East al. 2007; Son 2007; Glöer and Meier-Brook 2003 Siberia.

201 Т. Sitnikova et al.

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 (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 of planorboid shape which is not inverted. The shell surface was smooth except for growth increments, a bit glossy (Figure 2A- Figure 1. Study area. A – Angara River, inlet of a stream; B – C) and without basal carinae and thread-like sampling site, a small backwater formed by the stream mouth; striae. The was not strongly expanded C – stream. Photos by R. Kamaltynov. 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

202 Planorbella in East Siberia

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 praeputial organ was cup-shaped and its length praeputium with a praeputial organ (Figure 2F) was almost equal to that of the penis of similar to that of P. duryi. The distal end of the P. trivolvis. The cup of the penial gland was penial sheath and proximal end of the prae- bilobated similar to that of P. duryi. putium were connected by the accessory duct. The radula was musivoglossate, with a ribbon The penis was encased in the connective-tissue length of 1.9-2.1 mm and a width of 0.80-0.86 sheath, which is lined on the outside with mm. It consisted of about 124-130 bilaterally prismatic epithelium. The ejaculatory duct of the symmetrical transverse rows of 41-45 teeth penis opened 0.5 mm from the papilla as was (Figure 2D), with 20-22 marginal teeth on each shown by Hubendick (1955). The terminal part side of the central (9 primary and 11-13 of the penis was covered by a thin cuticle and secondary teeth). The radular formula thus was had a small tip (stylet) (Figure 2G-H) that has 20(22) –1 – 20(22). Teeth were positioned in a not been mentioned in literature for P. duryi. The way that they do not directly adjoin (Figure 2D).

203 Т. Sitnikova et al.

The primary marginal teeth always had plates (Van der Schalie and Berry 1973). P. trivolvis is with 3 main cusps, the central one of which was an R-adapted or R-selected species with a high often bicuspid. The secondary marginal teeth proportion of available energetic resource for were very narrow with 4-6 cusps. The central reproduction (Dillon 2000). teeth were comparatively small (Figure 2E). The Aquarium trade is well developed in East base of a central tooth was trapezoid and became Siberia, including Ust-Ilimsk. Therefore the narrower at the dental rectangular plate. The occurrence of North American gastropods in the dental plate was half of the length of the base vicinity of this city in our opinion could be the and bore 2 cusps. Radular teeth morphology and result of aquarium release. The warm water in size of investigated specimens were similar to the stream running from the cooler of the Pulp those of P. duryi and P. trivolvis but the radular and Paper Plant appeared favorable for these formula and a comparatively small number of migrating 3 km downstream and reaching transverse rows coincided more with the Angara River. So far no Planorbella P. truncatum. specimens have been found in the Angara River It should be mentioned that there were some proper. Whether or not the snails reproduced and similarities between the investigated specimens can survive the winter in this comparatively and P. truncatum (Miles, 1861), e.g. a flat warm biotope is not yet known and difficult to and relatively small size of mature predict. specimens (less than 10 mm). Significant variation of the anatomy of Planorbella species Acknowledgements living in their natural environment has been described (Baker 1945) and makes identification The authors thank G. Dvoeglazova for field assistance, E. Timoshkina for the initial English version of this paper, Dr. at the species level difficult. However, Peter Glöer for the important critical comments and Dr. considering all characters described here, we are Frances Lucy for editing English. This work has partially confident that our Planorbella specimens most been supported by RFBR Grants № 08-04-10077k and 08- likely represent P. duryi duryi (Wetherby, 1879), 04-98034 and Integration Project of the Siberian Branch of the subgenus Seminolina Pilsbry, 1934. Russian Academy Science № 49. Note that fossil shells identified as trivolvis (= ) were found in References the Pleistocene deposits of the Kolyma River Andreev NI, Andreeva SI, Vinarski MV, Lazutkina EA (2008) (north-eastern Russia) (Lindholm 1932). Alien species of mollusks in water bodies of Western However, no other reports on fossil or modern Siberia. Ecologic-economical effect of the nature Planorbella findings in present water bodies of management during the recent stage of development in East Siberia are available at the moment. the West-Siberian region. Data II International scientific-practical conference. Omsk, pp 7-10 According to Starobogatov et al. (2004), the Anistratenko VV, Haliman IA (2006) The bivalve mollusc Eurasian Galba truncatula and the Siberian Anadara inaequivalvis (Bivalvia, Arcidae) in the Sibirenauta sibirica inhabit small water bodies northern part of the Sea of Azov: completion of of Russia, including Pribaikalye. The third colonization of the Azov-Black Sea Basin. Vestnik Zoologii 40(6): 505-511 species we found and assigned to the planorbid Baker FC (1945) Molluscan family Planorbidae. Urbana, genus Planorbella has its origin in North University of Illinois Press, 530 pp America and is clearly an invader which is new Burch JB, Jung Y (1992). Freshwater snails of the University to the aquatic fauna of East Siberia. Planorbella of Michigan Biological Station area. Walkerana 5(13): i- vi, 1-216 species are common from Arctic Canada to Cianfanelli S, Lori E, Bodon M (2007) Non-indigenous Florida, being sporadically introduced to other freshwater molluscs and their distribution in Italy. In: F. regions by aquarium hobbyists and water Gherardi F (ed) Biological invaders in inland waters: gardeners (Dillon 2000, 2007). It is known that Profiles, distribution and threats. Springer, The Nether- lands, pp 103-121, doi:10.1007/978-1-4020-6029-8_5 natural populations for example of P. trivolvis Clarke AH (1981) The freshwater molluscs of Canada. occurring in eutrophic waters are characterized National Museum of Natural Sciences, Ottawa, 46 pp by an annual life cycle, while in mesotrophic Dillon RT (2000) The ecology of freshwater molluscs. waters individuals grow slower and live Cambridge University Press, 509 pp, doi:10.1017/ approximately two years (Eversole 1978). CBO9780511542008 Dillon RT (2007) Freshwater gastropods of North America Reproduction under aquarium tank conditions project (available from: http://www.cofc.edu/~fwgna/spe starts at a water temperature of 20°С, with cies/planorbidae/h_trivolvis.html, accessed 17th February maximal egg attachment occurring at 24°C. The 2010) snails become mature at an age of 3-4 months

204 Planorbella in East Siberia

Eversole AG (1978) Life cycles, growth and population Sharapova TA (2008) Distributional and ecological bioenergetics of the snail, Helisoma trivolvis (Say). peculiarities of invading mollusks in the cooler reservoir Journal of Molluscan Studies 44: 209-222 at the Tyumen Heat and Power Plant in West Siberia. Eröss ZP, Fehér Z, Hunyadi A (2005) Invasion of a North Vestnik zoologii 42(2): 185-187 American alien, Planorbella anceps (Menke, 1830) Starobogatov YaI (1990) Tendency of evolutionary trans- (: : Planorbidae), in the ancient formations of radulae of modern mollusks In: Shileiko Lake Prespa. Tentacle 13: 6-7 AA (ed), Evolyutsionnaya morfologiya mollyuskov Gollasch S, Nehring S (2006) National checklist for aquatic (Zakonomernosti morfofunktsional’nykh perestroek alien species in Germany. Aquatic Invasions 1: 245-269, radulyarnogo apparata) [Evolutionary morphology of doi:10.3391/ai.2006.1.4.8 mollusks (Consistent patterns of morphofunctional Glöer P (2002) Süßwassergastropoden Nord- und Mittel- rearrangements of the radular apparatus)], Moscow State europas. Conchbooks, Hackenheim, 446 pp University, Moscow, pp 37-91 Glöer P, Meier-Brook C (2003) Süsswassermollusken. Ein Starobogatov YaI, Prozorova LA, Bogatov VV, Saenko EM Bestimmungsschlüssel für die Bundesrepublik (2004) Molluscs. In: Tsalolikhin S (ed), Key to Deutschland, 13th ed. DJN, 134 pp freshwater invertebrates of Russia and adjacent lands, Hubendick B (1955) Phylogeny in the Planorbidae. Nauka, St.Petersburg, 6: 6-492 Transactions of the Zoological Society of London 28: Son MO (2007) Invasive mollusks in fresh and brackish 453-542 waters of the northern Black Sea region. Odessa, Druk, Kerth K (1983) Radulaapparat und Radulabildung der 132 pp Mollusken. I. Vergleichende Morphologie und Ultra- Taylor DW (2003) Introduction to Physidae (Gastropoda: struktur. Zoologische Jahrbücher. Abteilung für ); biogeography, classification, morphology. Anatomie und Ontogenie der Tiere 110: 205-237 Revista de Biologia Tropical 51 (Suppl. 1): 1-287 Lindholm WA (1932) On the finding of American Helisoma Van der Schalie H, Berry E (1973) The effects of temperature trivolvis Say (Gastropoda, Planorbidae) in the Pleisto- on growth and reproduction of aquatic snails. Sterkiana cene of Kolyma River. Trudy Soveta po izucheniyu 50: 1-9 proizvoditel’nyh sil, Ser. Yakutskaya, 11: 65-72 Yanygina L, Kirillov V., Zarubina E (2009) Invasive species Roll U, Dayan T, Simberloff D, Miens HK (2009) Non- in the biocenosis of the cooling reservoir of Belovo indigenous land and freshwater gastropods in Israel. Power plant (The south of west Siberia). Russian Biological Invasions 11: 1963-1972, doi:10.1007/s10530- Journal of Biological Invasions 2: 60-68 008-9373-4

205