Abstract
Variability of the first invasive population of C. fluminea (O.F. Müller, 1774) from the Volga basin is studied using the mitochondrial cytochrome c oxidase subunit I gene fragment (COI mtDNA), and morphological features of the shells are characterized. A comparison with C. fluminalis (O.F. Müller, 1774) from the Kura River basin is made in order to avoid errors in species identification. All analyzed individuals belong to the most widespread R morphological type. The only nucleotide sequence haplotype we found is identical to the widespread variant prevailing in the populations of Corbicula with R morphological type in Europe and also in America. There were mollusks of different shell size groups in the sample. Corbicula larvae were detected in qualitative zooplankton samples and in the gills of adults. Therefore, the studied population reproduces independently and may possibly become a source for further species expansion.
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REFERENCES
Araujo, R., Moreno, D., and Ramos, M.A., The Asiatic clam Corbicula fluminea (Müller, 1774) (Bivalvia: Corbiculidae) in Europe, Am. Malacol. Bull., 1993, no. 10, pp. 39–49.
Bespalaya, Y.V., Bolotov, I.N., Aksenova, O.V., et al., Aliens are moving to the Arctic frontiers: an integrative approach reveals selective expansion of androgenic hybrid Corbicula lineages towards the north of Russia, Biol. Invasions, 2018, vol. 20, pp. 2227–2243.
Britton, J.C. and Morton, B., Polymorphism in Corbicula fluminea (Bivalvia: Corbiculoidea) from North America, Malacol. Rev., 1986, vol. 19, pp. 1–43.
Cianfanelli, S., Lori, E., and Bodon, M., Non-indigenous freshwater mollusks and their distribution in Italy, in Biological Invaders in Inland Waters: Profiles, Distribution, and Threats, Gherardi, F., Ed., Dordrecht: Springer, 2007, pp. 103–121.
Elliott, P. and Ermgassen, P.S., The Asian clam (Corbicula fluminea) in the River Thames, London, England, Aquat. Invasions, 2008, vol. 3, no. 1, pp. 54–60.
Folmer, O., Black, M., Hoeh, W., et al., DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates, Mol. Mar. Biol. Biotechnol., 1994, vol. 3, pp. 294–299.
Gomes, C., Sousa, R., Mendes, T., et al., Low genetic diversity and high invasion success of Corbicula fluminea (Bivalvia, Corbiculidae) (Müller, 1774) in Portugal, PLoS One, 2016, vol. 11, no. 7. https://doi.org/10.1371/journal.pone.0158108
Hedtke, S.M., Glaubrecht, M., and Hillis, D.M., Rare gene capture in predominantly androgenetic species, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 9520–9524.
Hedtke, S.M., Stanger-Hall, K., Baker, R.J., and Hillis, D.M., All male asexuality: origin and maintenance of androgenesis in the Asian clam Corbicula, Evolution, 2008, vol. 62, pp. 1119–1136.
Houki, S., Yamada, M., Honda, T., and Komaru, A., Origin and possible role of males in hermaphroditic androgenetic Corbicula clams, Zool. Sci., 2011, vol. 28, pp. 526–531. https://doi.org/10.2108/zsj.28.526
Howlett, D. and Baker, R., Corbicula fluminea (Müller): new to UK, J. Conchol., 1999, vol. 36, no. 6, pp. 83–84.
Ishibashi, R., Ookubo, K., Aoki, M., et al., Androgenetic reproduction in a freshwater diploid clam Corbicula fluminea (Bivalvia: Corbiculidae), Zool. Sci., 2003, vol. 20, pp. 727–732.
Johnson, M., Zaretskaya, I., Raytselis, Y., et al., NCBI BLAST: a better web interface, Nucleic Acid Res., 2008, vol. 36, pp. 5–9.
Karatayev, A.Y., Burlakova, L.E., and Padilla, D.K., Contrasting distribution and impacts of two freshwater exotic suspension feeders, Dreissena polymorpha and Corbicula fluminea, in The Comparative Roles of Suspension-Feeders in Ecosystems, Dame, R.F. and Olenin, S., Eds., Dordrecht: Springer, 2005, pp. 239–262.
Komaru, A., Yamada, M., and Houki, S., Relationship between two androgenetic clam species, Corbicula leana and Corbicula fluminea, inferred from mitochondrial cytochrome b and nuclear 28S rRNA markers, Zool. Sci., 2013, vol. 30, pp. 360–365.
Korniushin, A.V., A revision of some Asian and African freshwater clams assigned to Corbicula fluminalis (Müller, 1774) (Mollusca: Bivalvia: Corbiculidae), with a review of anatomical characters and reproductive features based on museum collections, Hydrobiologia, 2004, vol. 529, pp. 255–270.
Lee, T., Siripattrawan, S., Ituarte, C.F., and Foighil, O.D., Invasion of the clonal clams: Corbicula lineages in the New World, Am. Malacol. Bull., 2005, vol. 20, pp. 113–122.
Machordom, A., Araujo, R., Erpenbeck, D., and Ramos, M.A., Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea), Biol. J. Linn. Soc., 2003, vol. 78, pp. 235–252.
Marescaux, J., Pigneur, L.-M., and Van Doninck, K., New records of Corbicula clams in French rivers, Aquat. Invasions, 2010, vol. 5, pp. 35–39.
McMahon, R.F., The occurrence and spread of the introduced Asiatic freshwater clam, Corbicula fluminea (Müller, 1774), in North America: 1924–1982, Nautilus, 1982, vol. 96, pp. 134–141.
Minchin, D., The distribution of the Asian clam Corbicula fluminea and its potential to spread in Ireland, Manage. Biol. Invasions, 2014, vol. 5, no. 2, pp. 165–177.
Mouthon, J., Sur la présence en France et au Portugal de Corbicula (Bivalvia, Corbiculidae) originaire d’Asie, Basteria, 1981, vol. 45, pp. 109–116.
Munjiu, O. and Shubernetski, I., First record of Asian clam Corbicula fluminea (Müller, 1774) in the Republic of Moldova, Aquat. Invasions, 2010, vol. 5, suppl. 1, pp. 67–70.
Nabozhenko, M.V. and Nabozhenko, S.V., Corbicula fluminalis (Müller, 1774), a bivalve mollusc species new for the Russian sector of the Caspian basin, Nauka Yuga Ross., 2016, vol. 12, no. 1, pp. 61–64.
National Center for Biotechnology Information. https:// www.ncbi.nlm.nih.gov/. Accessed January 25, 2020.
Nichols, S.J. and Black, M.G., Identification of larvae: the zebra mussel (Dreissena polymorpha), quagga mussel (Dreissena rosteriformis bugensis), and Asian clam (Corbicula fluminea), Can. J. Zool., 1994, vol. 72, pp. 406–417.
Okawa, T., Kurita, Y., Kanno, K., et al., Molecular analysis of the distributions of the invasive Asian clam, Corbicula fluminea (O.F. Müller, 1774), and threatened native clam, C. leana Prime, 1867, on Kyushu Island, Japan, BioInvasions Rec., 2016, vol. 5, no. 1, pp. 25–29.
Park, J.K. and Kim, W., Two Corbicula (Corbiculidae: Bivalvia) mitochondrial lineages are widely distributed in Asian freshwater environment, Mol. Phylogenet. Evol., 2003, vol. 29, pp. 529–539. https://doi.org/10.1016/S1055-7903(03)00138-6
Paunović, M., Csányi, B., Knežević, S., et al., Distribution of Asian clams Corbicula fluminea (Müller, 1774) and C. fluminalis (Müller, 1774) in Serbia, Aquat. Invasions, 2007, vol. 2, no. 2, pp. 99–106.
Peñarrubia, L., Araguas, R.M., Vidal, O., et al., Genetic characterization of the Asian clam species complex (Corbicula) invasion in the Iberian Peninsula, Hydrobiologia, 2017, vol. 784, pp. 349–365.
Pfenninger, M., Reinhardt, F., and Streit, B., Evidence for cryptic hybridization between different evolutionary lineages of the invasive clam genus Corbicula (Veneroida, Bivalvia), J. Evol. Biol., 2002, vol. 15, pp. 1–13.
Pigneur, L.M., Etoundi, E., Aldridge, D.C., et al., Genetic uniformity and long-distance clonal dispersal in the invasive androgenetic Corbicula clams, Mol. Ecol., 2014, vol. 23, pp. 5102–5116.
Pigneur, L.-M., Hedtke, S.M., Etoundi, E., and Van Doninck, K., Androgenesis: a review through the study of the shellfish Corbicula spp., Heredity, 2012, vol. 108, pp. 581–591.
Pigneur, L.-M., Marescaux, J., Roland, K., et al., Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western-Europe, BMC Evol. Biol., 2011, vol. 11, p. 15. https://doi.org/10.1186/1471-2148-11-147
Popa, O.P. and Popa, L.O., Sinanodonta woodiana (Lea, 1834), Corbicula fluminea (Müller, 1774), Dreissena bugensis (Andrusov, 1897) (Mollusca: Bivalvia): alien invasive species in Romanian fauna, Trav. Mus. Natl. d’Hist. Nat. Grigore Antipa, 2006, vol. 49, pp. 7–12.
Prime, T., Notes on species of the family Corbiculadæ, with figures, Ann. Lyceum Nat. History New York, 1867, vol. 8, p. 68.
Rajagopal, S., Van der Velde, G., and Bij de Vaate, A., Reproductive biology of the Asiatic clams Corbicula fluminalis and Corbicula fluminea in the River Rhine, Arch. Hydrobiol., 2000, vol. 149, pp. 403–420.
Renard, E., Bachmann, V., Cariou, M.L., and Moreteau, J.C., Morphological and molecular differentiation of invasive freshwater species of the genus Corbicula (Bivalvia, Corbiculidae) suggest the presence of three taxa in French rivers, Mol. Ecol., 2000, vol. 9, pp. 2009–2016.
Siripattrawan, S., Park, J.-K., and Foighil, D., Two lineages of the introduced Asian freshwater clam Corbicula occur in North America, J. Moll. Stud., 2000, vol. 66, pp. 423–429.
Skolka, M. and Gomoiu, M.-T., Alien invertebrates species in Romanian waters, Ovidius Univ., Ann. Nat. Sci., Biol.-Ecol. Ser., 2001, vol. 5, pp. 51–55.
Son, M.O., Mollyuski-vselentsy v presnykh i solonovatykh vodakh Severnogo Prichernomor’ya (Invasive Molluscs in Fresh and Brackish Waters of the Northern Black Sea region), Odessa: Druk, 2007.
Sousa, R., Antunes, C., and Guilhermino, L., Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview, Int. J. Limnol., 2008, vol. 44, pp. 85–94.
Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725–2729.
Tiemann, J.S., Haponski, A.E., Sarah, A., et al., First record of a putative novel invasive Corbicula lineage discovered in the Illinois River, Illinois, USA, BioInvasions Rec., 2017, vol. 6, no. 2, pp. 159–166.
Vaate, A.D. and Greijdanus-Klaas, M., The Asiatic clam, Corbicula fluminea (Müller, 1774) (Pelecypoda, Corbiculidae), a new immigrant in the Netherlands, Bull. Zool. Mus., 1990, vol. 12, no. 12, pp. 173–178.
Vaate, B.D. and Hulea, A.O., Range extension of the Asiatic clam Corbicula fluminea (Müller, 1774) in the River Danube: first record from Romania, Lauterbornia, 2000, vol. 38, pp. 23–26.
Zhadin, V.I., Mollyuski presnykh i solonovatykh vod SSSR (Molluscs of Fresh and Brackish Waters of the USSR), Moscow–Leningrad: Akad. Nauk SSSR, 1952.
Zhivoglyadova, L.A. and Revkov, N.K., Invasion of the bivalve mollusk Corbicula fluminalis (O.F. Müller, 1774) (Bivalvia: Cyrenidae) into the Lower Don basin, Vodn. Bioresur. Sreda Obitaniya, 2018, vol. 1, no. 1, pp. 44–50.
ACKNOWLEDGMENTS
We are grateful to the crew of the R/V Akademik Topchiev for assistance in sampling the material. We thank an anonymous reviewer for valuable comments and suggestions.
Funding
This study was performed within the framework of a state assignment of the Federal Agency for Scientific Organization (FASO, Russia), project no. АААА-А18-118012690105-0, and was partially supported by the Russian Foundation for Basic Research, project no. 17-05-00782 A.
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Voroshilova, I.S., Pryanichnikova, E.G., Prokin, A.A. et al. Morphological and Genetic Traits of the First Invasive Population of the Asiatic Clam Corbicula fluminea (O.F. Müller, 1774) Naturalized in the Volga River Basin. Russ J Biol Invasions 12, 36–43 (2021). https://doi.org/10.1134/S2075111721010148
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DOI: https://doi.org/10.1134/S2075111721010148