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The Asian Pond Mussels Rapidly Colonize Russia: Successful Invasions of Two Cryptic Species to the Volga and Ob Rivers

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The Asian Pond Mussels Rapidly Colonize Russia: Successful Invasions of Two Cryptic Species to the Volga and Ob Rivers BioInvasions Records (2020) Volume 9, Issue 3: 504–518 CORRECTED PROOF Rapid Communication The Asian pond mussels rapidly colonize Russia: successful invasions of two cryptic species to the Volga and Ob rivers Alexander V. Kondakov1, Yulia V. Bespalaya1,*, Ilya V. Vikhrev1, Ekaterina S. Konopleva1, Mikhail Yu. Gofarov1, Alena A. Tomilova1, Maxim V. Vinarski2 and Ivan N. Bolotov1 1N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Northern Dvina Emb. 23, 163000 Arkhangelsk, Russia 2Saint-Petersburg State University, Universitetskaya Emb. 7/9, 199034 Saint-Petersburg, Russia *Corresponding author E-mail: [email protected] Citation: Kondakov AV, Bespalaya YV, Vikhrev IV, Konopleva ES, Gofarov MY, Abstract Tomilova AA, Vinarski MV, Bolotov IN (2020) The Asian pond mussels rapidly The Asian pond mussels (Sinanodonta spp.) are invasive species rapidly spreading colonize Russia: successful invasions of throughout the world. In Russia, non-native populations of Sinanodonta woodiana two cryptic species to the Volga and Ob and S. lauta were firstly discovered in an artificially heated section of the Yenisei rivers. BioInvasions Records 9(3): 504– River, Eastern Siberia. Here, we report that these mussels successfully colonized 518, https://doi.org/10.3391/bir.2020.9.3.07 the downstream of the Volga River, where they established rather abundant Received: 10 February 2020 populations (3–36% of the total samples of freshwater mussels). Furthermore, these Accepted: 24 May 2020 species were recorded from the Belovo Reservoir, Ob River, Western Siberia. Published: 10 July 2020 Based on our molecular data, we propose that the recent invasion of Sinanodonta Handling editor: Mikhail Son woodiana and S. lauta in Russia was associated with fish stocks imported from Thematic editor: Kenneth Hayes Kazakhstan. The rapid expansion of these mussels throughout Russia was caused by a human-mediated dispersal of infested fishes from a site(s) of initial invasion to Copyright: © Kondakov et al. other freshwater systems, i.e. the Volga (at least since 2002), Yenisei (2004), and This is an open access article distributed under terms of the Creative Commons Attribution License Ob (2007) rivers. Recent establishments of Sinanodonta woodiana and S. lauta in (Attribution 4.0 International - CC BY 4.0). native environments of the Volga River appear to have major ecological consequences, OPEN ACCESS. as it is the largest river in European Russia and the entire Europe harboring species- rich native mussel and fish assemblages. Key words: Sinanodonta woodiana, Sinanodonta lauta, invasive species, hidden invasion, European Russia, Western Siberia, China Introduction The freshwater mussel genus Sinanodonta Modell, 1945 contains several species native to East Asia (Lopes-Lima et al. 2020) but are rapidly spreading throughout Europe, the Caribbean Islands, Southeast Asia, and Australasia (Bolotov et al. 2016; Vikhrev et al. 2017; Konečný et al. 2018). In Russia, native populations of Sinanodonta spp. are known from the Russian Far East (Sayenko et al. 2017; Kondakov et al. 2018; Lopes-Lima et al. 2020; Bolotov et al. 2020). In particular, Sinanodonta schrenkii (Lea, 1870) was recorded from the Amur and Razdolnaya river basins, while S. lauta (Martens, 1877) was found in a few rivers southwest of Vladivostok (Lopes-Lima et al. 2020; Bolotov et al. 2020). Kondakov et al. (2020), BioInvasions Records 9(3): 504–518, https://doi.org/10.3391/bir.2020.9.3.07 504 Invasions of two cryptic Asian mussel species to the Volga and Ob rivers The invasion of Asian pond mussels in Russia was firstly discovered in the Yenisei River, Eastern Siberia (Bespalaya et al. 2018). Two species, i.e. Sinanodonta woodiana (Lea, 1834) and S. lauta, established a dense mussel bed in an artificially heated section of this river near the city beach of Krasnoyarsk. It was found that S. lauta from the Yenisei shares a COI haplotype that is distant from those discovered in native Russian populations being closely related to those from South Korea. Conversely, S. woodiana reveals the commonest invasive haplotype being recorded from a variety of European countries and northern Myanmar (Froufe et al. 2017; Vikhrev et al. 2017; Bespalaya et al. 2018; Konečný et al. 2018; Urbańska et al. 2019; Kondakov et al. 2020). It was shown that this temperate lineage of S. woodiana is native to the Yangtze River, China (Bolotov et al. 2016; Bespalaya et al. 2018; Konečný et al. 2018; Kondakov et al. 2018, 2020; Huang et al. 2019). Later, S. lauta and S. woodiana were recorded from the Ili River basin in Kazakhstan, and their samples from this country enigmatically share the same COI haplotypes as the non-native Yenisei populations (Kondakov et al. 2020). In contrast, samples from the Amu Darya River in Uzbekistan belong to S. woodiana sharing a unique COI haplotype that has never been recorded in both invasive and native populations of this lineage (Kondakov et al. 2018, 2020). This study aims to (1) report two more Russian river basins invaded by the Asian pond mussels including the successful colonization of the lower reaches of the Volga River, the largest freshwater basin in Europe; (2) estimate affinities and possible origin of the non-native Sinanodonta populations in Russia by means of molecular techniques; (3) describe morphological features and age of the new alien populations; and (4) discuss possible causes and consequences of this rapid expansion throughout the country. Materials and methods Data collecting To find new non-native populations of Sinanodonta spp. in Russia, we regularly monitored social networks and regional mass-media using key words such as “giant mussel/shell”, “mutant mussel”, and “huge mussel” (in Russian), because records of such large freshwater mussels attract a full attention of local communities (e.g. Bespalaya et al. 2018). Based on this information, we found two perspective areas for fieldworks: the Lower Volga River, European Russia and the Belovo Reservoir in the Ob River basin, Western Siberia. The fieldworks were carried out from 11 to 13 September 2019 (Belovo Reservoir) and from 25 to 28 October 2019 (Volga River). In each area, we surveyed several sites to estimate the presence of Sinanodonta spp. and their relative abundance compared to native freshwater mussel species. In every site, a total sample of freshwater mussels was collected and was identified to the species level using morphological criteria, Kondakov et al. (2020), BioInvasions Records 9(3): 504–518, https://doi.org/10.3391/bir.2020.9.3.07 505 Invasions of two cryptic Asian mussel species to the Volga and Ob rivers except for Sinanodonta species, which can be distinguished by molecular characters only (Bespalaya et al. 2018; Kondakov et al. 2020). The number of collected specimens for each species was registered, and all native mussels were released back to their habitat. From each site, we snipped a Sinanodonta sample (up to 10 specimens) and collected dry shells of these specimens. A small foot tissue snip from every specimen was preserved in 96% ethanol immediately after collecting (Bolotov et al. 2017). Morphological analyses and age determination Sequenced samples of Sinanodonta spp. from each site were used for morphological analyses (Supplementary material Tables S1 and S2). Shell length, shell height, and shell width (all at the maximum diameter) were measured using a digital caliper (Digimatic Coolant Proof, Mitutoyo, Japan) (Bespalaya et al. 2018). Two morphometric indexes, i.e. the shell convexity index (SCI = width/length ratio × 100) and the shell elongation index (SEI = height/length ratio × 100) were calculated using shell measurements (Bolotov et al. 2018). To estimate the age of Sinanodonta spp., we counted annual growth rings, which are clearly visible on the shell surface (Kondakov et al. 2020). Based on the maximum age, we estimated the year of birth of the oldest mussel in a sample that can be used as an approximate proxy to assess the possible time of initial invasion of Sinanodonta species to a freshwater system. However, this estimate does not work for sites in which Sinanodonta populations were established a long time ago (e.g. Kazakhstan) due to a short lifespan of these mussels and can be biased by local re-colonization dynamics of mussel settlements. Molecular and phylogeographic analyses New cytochrome c oxidase subunit I (COI) gene sequences were generated from 42 specimens as described in our previous study (Bolotov et al. 2016). Additionally, we collected 24 COI sequences of S. lauta and 72 COI sequences of the temperate lineage of S. woodiana from NCBI GenBank (Table S1; references: Bespalaya et al. 2018; Froufe et al. 2017; Huang et al. 2019; Kondakov et al. 2018, 2020; Soroka 2005, 2010; Soroka et al. 2014; Vikhrev et al. 2017; Zhang et al. 2016). To estimate the phylogeographic affinities of our samples, we applied a median joining network approach using Network v. 4.6.1.3 with default settings (Bandelt et al. 1999). Distribution mapping The ranges of Sinanodonta spp. were mapped mostly using original data (Table 1) with ESRI ArcGIS 10 software (www.esri.com/arcgis). Free open sources, i.e. Natural Earth Free Vector and Raster Map Data (http://www. naturalearthdata.com), GSHHG (http://www.soest.hawaii.edu/pwessel/gshhg), Kondakov et al. (2020), BioInvasions Records 9(3): 504–518, https://doi.org/10.3391/bir.2020.9.3.07 506 Invasions of two cryptic Asian mussel species to the Volga and Ob rivers Table 1. Records
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