Skip to main content
Log in

Opening the black box of the invasion of Corbicula clams (Bivalvia, Corbiculidae) in South America: a genetic and morphological evaluation

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Among species of Corbicula, only the hermaphroditic androgenetic lineages are invasive while sexual species are restricted to the native range (mainly Asia). Four androgenetic lineages of Corbicula spp. have been identified in American and European freshwater systems, with the Corbicula sp. form A/R lineage being abundant on both continents. This lineage is considered an important invasive species because of its impact on aquatic ecosystems and industrial cooling systems. The present study identified the invasive lineages of Corbicula spp. in freshwater environments of South America based on morphometric data and used genetic marker (mtDNA COI gene) to investigate their genetic relatedness to the invasive lineages from Europe and North America. Four important results arise: (1) there are two invasive lineages of Corbicula in South America, Corbicula sp. form C/S and Corbicula sp. form A/R, and they are clonally expanding their distribution in continental aquatic systems of South America; (2) populations with intermediate morphotype were detected in three distinct sites of Brazil; (3) one population with individuals presenting a new COI haplotype was recovered with an intermediate morphotype; (4) the morphotype of the invasive lineages of Corbicula spp. in South America presents high correlation with their COI haplotypes.

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
Fig. 3

Similar content being viewed by others

Data availability

The data of this study are included as an electronic supplementary file.

References

  • Arano, B., G. Llorent, M. Gardia-Paris & P. Herrero, 1995. Species translocation menaces iberian waterfrogs. Conservation Biology 9: 196–198.

    Article  Google Scholar 

  • Araújo, R., D. Moreno & R. A. Ramos, 1993. The asiatic clam Corbicula fluminea (Muller 1774) (Bivalvia, Corbiculidae) in Europe. American Malacological Bulletin 10: 39–49.

    Google Scholar 

  • Aristizábal, M. V. D. L. H., 2008. Primer registro en Colombia de Corbicula fluminea (Mollusca: Bivalvia: Corbiculidae), una espécie invasora. Boletín de Investtigaciones Marinas y Costeras 37: 197–202.

    Google Scholar 

  • Bagatini, Y. M., R. S. Panarari, J. Higuti, E. Benedito-Cecilio, A. J. Prioli & S. M. A. P. Prioli, 2005. Morphological and molecular characterization of Corbicula (Mollusca: Bivalvia) at Rosana Resevoir, Brazil. Acta Scientiarum Biological Science 27: 397–404.

    CAS  Google Scholar 

  • Beasley, C. R., C. H. Tagliaro & W. B. Figueiredo, 2003. The Occurrence Of The Asian Clam Corbicula Fluminea In The Lowe Amazon Basin. Acta Amazonica 33: 317–324.

    Article  Google Scholar 

  • Belz, C. E., G. Darrigran, O. S. M. Netto, W. A. Boeger & P. J. R. Junior, 2012. Analysis of four dispersion vectors in Inland Waters: The case of the invading bivalves in South America. Journal of Shellfish Research 31: 777–784. https://doi.org/10.2983/035.031.0322.

    Article  Google Scholar 

  • Bespalaya, Y. V., I. N. Bolotov, O. V. Aksenova, A. V. Kondakov, M. Y. Gofarov, T. M. Laenko, S. E. Sokolova, A. R. Shevchenko & O. V. Travina, 2018. Aliens are moving to the Arctic frontiers: an integrative approach reveals selective expansion of androgenic hybrid Corbicula lineages towards the North of Russia. Biological Invasions. https://doi.org/10.1007/s10530-018-1698-z.

    Article  Google Scholar 

  • Bespalaya, Y. V., O. V. Aksenova, M. Y. Gofarov, A. V. Kondakov, A. V. Kropotin, O. D. Kononov & I. N. Bolotov, 2021. Who inhabits the world’s deepest crater lake? A taxonomic review of Corbicula (Bivalvia: Cyrenidae) clams from Lake Toba, North Sumatra, Indonesia. Journal of Zoological Systematics and Evolutionary Research 59: 400–410. https://doi.org/10.1111/jzs.12428.

    Article  Google Scholar 

  • Borges, P. D., S. Ludwig & W. A. Boeger, 2017. Testing hypotheses on the origin and dispersion of Limnoperna fortunei (Bivalvia, Mytilidae) in the Iguassu River (Paraná, Brazil): molecular markers in larvae and adults. Limnology 18: 31–39. https://doi.org/10.1007/s10201-016-0485-8.

    Article  CAS  Google Scholar 

  • Cao, L., C. Damborenea, P. E. Penchaszadeh & G. Darrigran, 2017. Gonadal cycle of Corbicula fluminea (Bivalvia: Corbiculidae) in Pampean streams (Southern Neotropical Region). PLoS ONE 12: 1–16. https://doi.org/10.1371/journal.pone.0186850.

    Article  CAS  Google Scholar 

  • Castañeda, R. A., E. Cvetanovska, K. M. Hamelin, M. A. Simard & A. Ricciardi, 2018. Distribution, abundance, and condition of an invasive bivalve (Corbicula fluminea) along an artificial thermal gradient in the St. Lawrence River. Aquatic Invasions 13: 379–392.

    Article  Google Scholar 

  • Carranza, A., Agudo-Padrón, I., Collado, G.A. et al. 2023. Socio-environmental impacts of non-native and transplanted aquatic mollusc species in South America: What do we really know?. https://doi.org/10.1007/s10750-023-05164-z

  • Crespo, D., M. Dolbeth, S. Leston, R. Sousa & M. A. Pardal, 2015. Distribution of Corbicula fluminea (Müller, 1774) in the invaded range: a geographic approach with notes on species traits variability. Biological Invasions 17: 2087–2101.

    Article  Google Scholar 

  • Darrigran, G., 1992. Variación temporal y espacial de la distribución de las especies de Corbicula Megerle, 1811 (Bivalvia, Corbiculidae), en el estuario del Río de la Plata, República Argentina. Neotropica 38.

  • Darrigran, G., 2002. Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biological Invasions 4: 145–156.

    Article  Google Scholar 

  • Darrigran, G., I. Agudo-Padrón, P. Baez, C. Belz, F. Cardoso, A. Carranza, G. Collado, M. Correoso, M. G. Cuezzo, A. Fabres, D. E. Gutiérrez-Gregoric, S. Letelier, S. Ludwig, M. C. Mansur, G. Pastorino, P. Penchaszadeh, C. Peralta, A. Rebolledo, A. Rumi, S. Santos, S. Thiengo, T. Vidigal & C. Damborenea, 2020. Non-native mollusks throughout South America: emergent patterns in an understudied continent. Biological Invasions 22: 853–871. https://doi.org/10.1007/s10530-019-02178-4.

    Article  Google Scholar 

  • Darrigran, G., I. Agudo-Padrón, P. Baez, et al., 2022. Species movements within biogeographic regions: exploring the distribution of transplanted mollusc species in South America. Biological Invasions. https://doi.org/10.1007/s10530-022-02942-z.

    Article  Google Scholar 

  • Drummond, A. J. & A. Drummond, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214. https://doi.org/10.1186/1471-2148-7-214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DrydenDrydenMardia, I. L. K. V., 1992. Size and shape analysis of landmark data. Biometrika 79: 57–68. https://doi.org/10.1093/biomet/79.1.57.

    Article  MathSciNet  Google Scholar 

  • Ellstrand, N. C. & K. A. Schierenbeck, 2000. Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences 97: 7043–7050.

    Article  CAS  ADS  Google Scholar 

  • Facon, B., P. Jame, J. P. Pointier & P. David, 2005. Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. Journal of Evolutionary Biology 18: 524–535. https://doi.org/10.1111/j.1420-9101.2005.00887.x.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira-Rodríguez, N., R. Sousa & I. Pardo, 2018. Negative effects of Corbicula fluminea over native freshwater mussels. Hydrobiologia 810: 85–95.

    Article  Google Scholar 

  • Folmer, O., M. Black, W. Hoeh, et al., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    CAS  PubMed  Google Scholar 

  • Ghabooli, S., A. Zhan, P. Sardiña, E. Paolucci, F. Sylvester, P. V. Perepelizin, et al., 2013. Genetic diversity in introduced golden mussel populations corresponds to vector activity. PLoS ONE 8: e59328. https://doi.org/10.1371/journal.pone.0059328.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Gomes, C., R. Sousa, T. Mendes, R. Borges, P. Vilares, V. Vasconcelos & A. Antunes, 2016. Low genetic diversity and high invasion success of Corbicula fluminea (Bivalvia, Corbiculidae)(Müller, 1774) in Portugal. PLoS ONE 11: e0158108. https://doi.org/10.1371/journal.pone.0158108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedtke, S. M., K. Stanger-Hall, R. J. Baker & D. M. Hillis, 2008. All-male asexuality: origin and maintenance of androgenesis in the Asian clam Corbicula. Evolution 62: 1119–1136. https://doi.org/10.1111/j.1558-5646.2008.00344.x.

    Article  CAS  PubMed  Google Scholar 

  • Hedtke, S. M., M. Glaubrecht & D. M. Hillis, 2011. Rare gene capture in predominantly androgenic species. PNAS 108: 9520–9524. https://doi.org/10.1073/pnas.1106742108.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  • Houki, S., M. Yamada, T. Honda & A. Komaru, 2011. Origin and Possible role of males in hermaphroditic androgenic Corbicula clams. Zoological Science 28: 526–531. https://doi.org/10.2108/zsj.28.526.

    Article  PubMed  Google Scholar 

  • Ituarte, C. F., 1981. Primera noticia acerca de la introduccion de pelecipodos asiaticos en el area rioplatense. Neotropica 27: 79–82.

    Google Scholar 

  • Ituarte, C. F., 1994. Corbicula and Neocorbicula (Bivalvia: Corbiculidae) in the Paraná, Uruguay, and Río de La Plata Basins. The Nautilus 107: 129–135.

    Google Scholar 

  • Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405. https://doi.org/10.1093/bioinformatics/btn129.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T., S. Devillard & F. Balloux, 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 1–15. https://doi.org/10.1186/1471-2156-11-94.

    Article  Google Scholar 

  • Keenan, K., P. McGinnity, T. F. Cross & P. A. Prodöhl, 2013. diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods in Ecology and Evolution 4: 782–788. https://doi.org/10.1111/2041-210X.12067.

    Article  Google Scholar 

  • Klingenberg, C. P., 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.

    Article  PubMed  Google Scholar 

  • Komaru, A., K. Konishi, I. Nakayama, T. Kobayashi, H. Sakai & K. Kawamura, 1997. Hermaphroditic freshwater clams in the genus Corbicula produce non-reductional spermatozoa with somatic DNA content. Biological Bulletin 193: 320–323.

    Article  CAS  PubMed  Google Scholar 

  • Komaru, A., A. Kumamoto, T. Kato, R. Ishibashi, M. Obata & N. Nemoto, 2006. A hypothesis of ploidy elevation by formation of a female pronucleus in the androgenic clam Corbicula fluminea in the Tone River estuary, Japan. Zoological Science 23: 529–532. https://doi.org/10.2108/zsj.23.529.

    Article  PubMed  Google Scholar 

  • Konishi, K., K. Kawamura, H. Furuita & A. Komaru, 1998. Spermatogenesis of the freshwater Clam Corbicula aff. fluminea Müller (Bivalvia: Corbiculidae). Journal of Shellfish Research 17: 185–189.

    Google Scholar 

  • Labaut, Y., P. A. Macchi, F. M. Archuby & G. Darrigran, 2021a. Homogenization of macroinvertebrate assemblages and Asiatic Clam Corbicula fluminea invasion in a river of the Arid Patagonian Plateau. Argentina. Frontiers in Environmental Science 9: 728620. https://doi.org/10.3389/fenvs.2021.728620.

    Article  Google Scholar 

  • Labaut Y., P. A. Macchi, F. M. Archuby, & G. Darrigran, 2021. Pesca con carnada viva como vector dispersante de la invasión de la almeja asiática Corbicula fluminea en Patagonia, Argentina. Memoria del III Simposio Internacional de Aguas Continentales de las Américas Restauración y Conservación de los Ecosistemas con Enfoque Participativo. 5, 6 y 7 de julio, 2021, Panajachel, Sololá, Guatemala. pp. 35. http://rid.unrn.edu.ar/handle/20.500.12049/8092

  • Lajtner, J., Z. Marusic, G. I. V. Klobucar, I. Maguire & R. Erben, 2004. Comparative shell morphology of the zebra mussel, Dreissena polymorpha in the Drava river (Croatia). Biologia-Bratislava 59: 595–600.

    Google Scholar 

  • Lasso, C. A., R. Martínez-Escarbassiere, J. C. Capelo, M. A. Morales-Betancourt & A. Sánchez-Maya, 2009. Lista de los moluscos (Gastropoda-Bivalvia) dulceacuícolas y estuarinos de La cuenca del Orinoco (Venezuela). Biota Colombiana 10: 63–74.

    Google Scholar 

  • Lee, T., S. Siripattrawan, C. Ituarte & D. Ó Foighil, 2005. Invasion of the clonal clams: Corbicula lineages in the New World. American Malacological Bulletin 20: 113–122.

    Google Scholar 

  • Librado, P. & J., Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. https://doi.org/10.1093/bioinformatics/btp187.

    Article  CAS  PubMed  Google Scholar 

  • López-Soriano, J., S. Quiñonero-Salgado, C. Cappelletti, F. Faccenda & F. Ciutti, 2018. Unraveling the complexity of Corbicula clams invasion in Lake Garda (Italy). Advances in Oceanography and Limnology. https://doi.org/10.4081/aiol.2018.7857.

    Article  Google Scholar 

  • Ludwig, S., M. K. Tschá, R. P. Patella, A. J. Oliveira & W. Boeger, 2014. Looking for a needle in a haystack: molecular detection of larvae of invasive Corbicula clams. Management of Biological Invasions 5: 143–149. https://doi.org/10.3391/mbi.2014.5.2.07.

    Article  Google Scholar 

  • Ludwig, S., E. H. Sari, H. Paixão, L. C. Montresor, J. Araújo, C. F. Brito & C. B. Martinez, 2021. High connectivity and migration potentiate the invasion of Limnoperna fortunei (Mollusca: Mytilidae) in South America. Hydrobiologia 848: 499–513. https://doi.org/10.1007/s10750-020-04458-w

    Article  Google Scholar 

  • Mansur, M.C.D., Callil, C.T., Cardoso, F.R., Ibarra, J.A.A., Silva, J.S.V., & R.C.C.L. Souza, 2004. Uma retrospectiva e mapeamento da invasão de espécies de Corbicula (Mollusca, Bivalvia, Veneroida, Corbiculidae) oriundas do sudeste asiático, na América do Sul. In: Silva JSV and Souza RCCL, Água de lastro e bioinvasão. Interciência, Rio de Janeiro, pp. 39.

  • Mansur, M.C.D., Santos, C.P., M.V., Nehrke, 2012. Corbiculidae na América do Sul: Espécies nativas e invasoras, dispersão e a situação das pesquisas no Brasil (Mollusca: Bivalvia). In: Ecos do XIX Encontro Brasileiro de Malacologia, Rio de Janeiro, Technical Books, pp 467.

  • Martínez, R., 1987. Corbicula manilensis molusco introducido en Venezuela. Acta Científica Venezeolana 38: 384–385.

    Google Scholar 

  • McMahon, R.F., 1983. Ecology of an Invasive Pest Bivalve, Corbicula. In: The Mollusca, Vol. 6, W. D. Russell-Hunter, ed. Academic Press, New York. pp.505.

  • McMahon, R.F., 1999. Invasive Characteristics of the Freshwater Bivalve, Corbicula fluminea. Lewis Publisher: 315–343.

  • Park, J. K., J. S. Lee & W. Kim, 2002. A single mitochondrial lineage is shared by morphologically and allozymatically distinct freshwater Corbicula clams. Molecular and Cells 14: 318–322.

    Article  CAS  Google Scholar 

  • Park, J. & W. Kim, 2003. Two Corbicula (Corbiculidae: Bivalvia) mitochondrial lineages are widely distributed in Asian freshwater environment. Molecular Phylogenetics and Evolution 29: 529–539. https://doi.org/10.1016/S1055-7903(03)00138-6.

    Article  CAS  PubMed  Google Scholar 

  • Paschoal, L. R. P., D. D. P. Andrade & G. Darrigran, 2015. How the fluctuations of water levels affect populations of invasive bivalve Corbicula fluminea (Müller, 1774) in a Neotropical reservoir? Brazilian Journal of Biology 75: 135–143. https://doi.org/10.1590/1519-6984.09113.

    Article  CAS  Google Scholar 

  • Pérez, C. H. F., C. S. Cárdenas & P. L. Simon, 2022. Patagonia Invadida: Primer Registro de Corbicula Fluminea (Müller, 1774) en la Cuenca del Río Chubut, Chubut, Argentina. Historia Natural 121: 165–172.

    Google Scholar 

  • Peso, J. G., D. C. Pérez & R. E. Vogler, 2011. The invasive snail Melanoides tuberculata in Argentina and Paraguay. Limnologica 41: 281–284. https://doi.org/10.1016/j.limno.2010.12.001.

    Article  Google Scholar 

  • Peñarrubia, L., R. M. Araguas, O. Vidal, C. Pla, J. Viñas & N. Sanz, 2017. Genetic characterization of the Asian clam species complex (Corbicula) invasion in the Iberian Peninsula. Hydrobiologia 784: 349–365. https://doi.org/10.1007/s10750-016-2888-2.

    Article  CAS  Google Scholar 

  • Pfenninger, M., F. Reinhardt & B. Streit, 2002. Evidence for cryptic hybridization between different evolutionary lineages of the invasive clam genus Corbicula (Veneroida, Bivalvia). Journal of Evolutionary Biology 15: 818–829.

    Article  CAS  Google Scholar 

  • Pigneur, L. M., A. M. Risterucci, N. Dauchot, X. Li & K. Van Doninck, 2011. Development of novel microsatellite markers to identify the different invasive lineages in the Corbicula complex and to assess androgenesis. Molecular Ecology Resources 11: 573–577. https://doi.org/10.1111/j.1755-0998.2010.02963.x.

    Article  CAS  PubMed  Google Scholar 

  • Pigneur, L. M., J. Marescaux, K. Roland, E. Etoundi, J. P. Descy & K. Van Doninck, 2011b. Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe. BMC Evolutionary Biology 11: 147. https://doi.org/10.1186/1471-2148-11-147.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pigneur, L. M., S. M. Hedtke, E. Etoundi & K. Van Doninck, 2012. Androgenesis: a review through the study of the shellfish Corbicula spp. Heredity 108: 581–591. https://doi.org/10.1038/hdy.2012.3.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pigneur, L. M., E. Etoundi, D. C. Aldridge, J. Marescaux, N. Yasuda & K. Van Doninck, 2014a. Genetic uniformity and long-distance clonal dispersal in the invasive androgenic Corbicula clams. Molecular Ecology 23: 5102–5116. https://doi.org/10.1111/mec.12912.

    Article  PubMed  Google Scholar 

  • Pigneur, L. M., E. Etoundi, D. C. Aldridge, J. Marescaux, N. Yasuda & K. Van Doninck, 2014. Genetic uniformity and long-distance clonal dispersal in the invasive androgenic Corbicula clams. Molecular Ecology 23: 5102–5116. https://doi.org/10.1111/mec.12912.

    Article  PubMed  Google Scholar 

  • Pimpão, D. M. & D. S. Martins, 2008. Occurrence of the Asian mollusk Corbicula fluminea (Müller 1774) (Bivalvia: Corbiculidae) in the lower Rio Negro, Central Amazoan Region, Brazil. Acta Amazonica 38: 589–592.

    Article  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256. https://doi.org/10.1093/mollbev/msn083.

    Article  CAS  PubMed  Google Scholar 

  • Rambaut, A. & A. J. Drummond, 2007. Tracer v1.4: MCMC tracer analyses tool. See http://tree.bio.ed.ac.uk/software/tracer/]. PubMed.

  • Rambaut, A., 2009. FigTree v1.3.1: Tree figure drawing tool. Website: http://tree.bio.ed.ac.uk/software/figtree.

  • Reyna, P., J. Nori, M. Ballesteros, A. Hued & M. Tatián, 2018. Targeting clams: insights into the invasive potential and current and future distribution of Asian clams. Environmental Conservation 45: 387–395. https://doi.org/10.1017/S0376892918000139.

    Article  Google Scholar 

  • Rius, M. & J. A. Darling, 2014. How important is intraspecific genetic admixture to the success of colonizing populations? Trends in Ecology & Evolution 29: 233–242. https://doi.org/10.1016/j.tree.2014.02.003.

    Article  Google Scholar 

  • Robertson, A. & W. G. Hill, 1984. Deviation from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficient. Genetics 107: 703–718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohlf, F. J., 2006. TpsDig2 Software, ver.2.10, State University New York, Stony Brook:

    Google Scholar 

  • Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180.

    Article  CAS  PubMed  Google Scholar 

  • Santana, D. O., M. J. M. Silva, A. Bocchiglieri, S. M. Pantaleão, R. G. Faria, B. B. Souza, S. M. Rocha & L. F. O. Lima, 2013. Mollusca, Bilvavia, Corbiculidae, Corbicula flumínea (Müller, 1774): first record for the Caatinga biome, northeastern Brazil. Check List 9: 1072–1074.

    Article  Google Scholar 

  • Santos, S. B., S. C. Thiengo, M. A. Fernandez, et al., 2012. Espécies de moluscos límnicos invasores no Brasil. In: Moluscos límnicos invasores do Brasil: biologia, prevenção e controle, Porto Alegre, Redes Editora, pp 412.

  • Seebens, H., T. M. Blackburn, E. E. Dyer, P. Genovesi, P. E. Hulme, J. M. Jeschke, et al., 2017. No saturation in the accumulation of alien species worldwide. Nature Communications 8: 14435. https://doi.org/10.1038/ncomms14435.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Semenas, L. & V. Flores, 2005. Presence of Corbicula fluminea in the Upper Negro River Basin (Patagonia, Argentina). Journal of Freshwater Ecology 20: 615–616.

    Article  Google Scholar 

  • Siripattrawan, S., J. K. Park & Ó. Foighil, 2000. Two lineages of the introduced Asian freshwater clam Corbicula occur in North America. Journal of Molluscan Studies 66: 423–429. https://doi.org/10.1093/mollus/66.3.423.

    Article  Google Scholar 

  • Sousa, R., R. Freire, M. Rufino, J. Méndez, M. Gaspar, et al., 2007. Genetic and shell morphological variability of the invasive bivalve Corbicula fluminea (Müller, 1774) in two Portuguese estuaries. Estuarine, Coastal and Shelf Science 74: 166–174. https://doi.org/10.1016/j.ecss.2007.04.011.

    Article  ADS  Google Scholar 

  • Sousa, R., A. J. A. Nogueira, M. B. Gaspar, C. Antunes & L. Guilhermino, 2008. Growth and extremely high production of the non-indigenous invasive species Corbicula fluminea (Müller, 1774): Possible implications for ecosystem functioning. Estuarine, Coastal and Shelf Science 80: 289–295. https://doi.org/10.1016/j.ecss.2008.08.006.

    Article  ADS  Google Scholar 

  • Tiemann, J. S., A. E. Haponski, S. A. Douglass, T. Lee, K. S. Cummings, M. A. Davis & Ó. Foighil, 2017. First record of a putative novel invasive Corbicula lineage discovered in the Illinois River, Illinois, USA. BioInvasions Records 6: 159–166. https://doi.org/10.3391/bir.2017.6.2.12.

    Article  Google Scholar 

  • Thompson, J. D., 1991. The biology of an invasive plant. BioScience 41: 393–401.

    Article  Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping erros in microsatellite data. Molecular Ecology 4: 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x.

    Article  CAS  Google Scholar 

  • Vastrade, M., E. Etoundi, T. Bournonville, M. Colinet, N. Debortoli, S. M. Hedteke, E. Nicolas, L. M. Pigneur, L. Virgo, J. F. Flot, J. Marescaux & K. Van Doninck, 2022. Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula. Peer Community Journal 2: 73. https://doi.org/10.24072/pcjournal.180.

    Article  Google Scholar 

  • Voelz, N. J., J. V. McArthur & R. B. Rader, 1998. Upstream mobility of the Asiatic clam Corbicula fluminea: identifying potential dispersal agents. Journal of Freshwater Ecology 13: 39–45.

    Article  Google Scholar 

  • Zhan, A., P. V. Perepelizin, S. Ghabooli, E. Paolucci, F. Sylvester, P. Sardina, et al., 2012. Scale-dependent post-establishment spread and genetic diversity in an invading mollusk in South America. Diversity and Distributions 18: 1042–1055. https://doi.org/10.1111/j.1472-4642.2012.00894.x.

    Article  Google Scholar 

Download references

Acknowledgements

Special thanks to Damminsky PB (Institutos Lactec), S.B. dos Santos (UERJ), H. Tagliaro (UFPE), M.C.D. Mansur (UFRS), K. Kotzian (UFSM), T.D.H.A. Vidigal (UFMG), O. M. Netto (MAxClean), and D. Pimpão (INPA), for providing samples for this study. We also thank the Instituto Lactec, UNLP (11/N927), CONICET (PIP 1017), PICT-2019-01417 and Conselho de Desenvolvimento Científico e Tecnológico (CNPq) for supporting this study, and for Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for scholarship assistance of SL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sandra Ludwig.

Additional information

Handling editor: Manuel Lopes-Lima

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 57 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ludwig, S., Darrigran, G. & Boeger, W.A. Opening the black box of the invasion of Corbicula clams (Bivalvia, Corbiculidae) in South America: a genetic and morphological evaluation. Hydrobiologia 851, 1203–1217 (2024). https://doi.org/10.1007/s10750-023-05378-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-023-05378-1

Keywords

Navigation