Skip to main content
Log in

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

  • Published:
Russian Journal of Biological Invasions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. 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.

  2. 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.

    Article  Google Scholar 

  3. Britton, J.C. and Morton, B., Polymorphism in Corbicula fluminea (Bivalvia: Corbiculoidea) from North America, Malacol. Rev., 1986, vol. 19, pp. 1–43.

    Google Scholar 

  4. 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.

    Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. 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.

    CAS  PubMed  Google Scholar 

  7. 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

  8. 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.

    Article  CAS  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. Howlett, D. and Baker, R., Corbicula fluminea (Müller): new to UK, J. Conchol., 1999, vol. 36, no. 6, pp. 83–84.

    Google Scholar 

  12. 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.

    Article  Google Scholar 

  13. Johnson, M., Zaretskaya, I., Raytselis, Y., et al., NCBI BLAST: a better web interface, Nucleic Acid Res., 2008, vol. 36, pp. 5–9.

    Article  Google Scholar 

  14. 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.

    Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

    Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. 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.

    Article  Google Scholar 

  20. 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.

    Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. Mouthon, J., Sur la présence en France et au Portugal de Corbicula (Bivalvia, Corbiculidae) originaire d’Asie, Basteria, 1981, vol. 45, pp. 109–116.

    Google Scholar 

  23. 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.

    Article  Google Scholar 

  24. 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.

    Google Scholar 

  25. National Center for Biotechnology Information. https:// www.ncbi.nlm.nih.gov/. Accessed January 25, 2020.

  26. 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.

    Article  Google Scholar 

  27. 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.

    Article  Google Scholar 

  28. 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

    Article  CAS  PubMed  Google Scholar 

  29. 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.

    Article  Google Scholar 

  30. 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.

    Article  Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Article  Google Scholar 

  33. 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.

    Article  Google Scholar 

  34. 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

    Article  Google Scholar 

  35. 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.

    Google Scholar 

  36. Prime, T., Notes on species of the family Corbiculadæ, with figures, Ann. Lyceum Nat. History New York, 1867, vol. 8, p. 68.

    Google Scholar 

  37. 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.

    Article  Google Scholar 

  38. 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.

    Article  CAS  Google Scholar 

  39. 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.

    Article  Google Scholar 

  40. 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.

    Google Scholar 

  41. 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.

  42. 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.

    Article  Google Scholar 

  43. 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.

    Article  CAS  Google Scholar 

  44. 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.

    Article  Google Scholar 

  45. 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.

    Google Scholar 

  46. 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.

    Google Scholar 

  47. Zhadin, V.I., Mollyuski presnykh i solonovatykh vod SSSR (Molluscs of Fresh and Brackish Waters of the USSR), Moscow–Leningrad: Akad. Nauk SSSR, 1952.

  48. 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.

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. S. Voroshilova.

Ethics declarations

Conflict of interest. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care of animals were followed.

Additional information

Translated by N. Ruban

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2075111721010148

Keywords:

Navigation