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All issues No 421 (2020) Knowl. Manag. Aquat. Ecosyst., 421 (2020) 24 Full HTML
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Issue
Knowl. Manag. Aquat. Ecosyst.
Number 421, 2020
Article Number 24
Number of page(s) 4
DOI https://doi.org/10.1051/kmae/2020017
Published online 05 June 2020

© I. Karaouzas et al., Published by EDP Sciences 2020

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

The Asian clam Corbicula fluminea Müller, 1774 is regarded as one of the most persistent invasive species in freshwater ecosystems, due to its great potential for dispersion and nuisance characteristics responsible for high ecological and economic impacts (Sousa et al., 2008a, 2008b). It can dominate macroinvertebrate communities, physically alter benthic habitats, and disrupt regulating ecosystem services (Sousa et al., 2008b, 2014). Despite policy and management efforts to reduce invader spread, C. fluminea continues to spread across freshwater systems (Caffrey et al., 2016). The rapid growth, high fecundity, early sexual maturity, short life span, and its association with human activities make C. fluminea a non-indigenous invasive species likely to colonize new environments (Sousa et al., 2008a). It has undergone a massive global range expansion since the 1940s, spreading from its native range in Southeast Asia, to North, Central and South America, and then to Europe (Crespo et al., 2015).

C. fluminea has spread to most European rivers including the Rhine, Garonne, Loire, Seine, and Rhone (Marescaux et al., 2010) and in the entire Danube Basin (e.g. Csányi, 1999; Bij de Vaate and Hulea, 2000). It has also spread to river basins in the Iberian and Italian Peninsula (Cianfanelli et al., 2007; Pérez-Quintero, 2008) and in hydrologically unconnected watersheds including the UK (Elliott and zu Ermgassen, 2008) and Ireland, where it was recorded for the first time in 2010 (Lucy et al., 2012). Expansion of invasive range and flourishing populations are also recently reported in Poland (e.g. Oder river; Cebulska and Krodkiewska, 2019) and western Turkey (Serdar, 2018).

In this contribution, C. fluminea is reported for the first time in Greece, being the southernmost record of the species in the Balkan Peninsula. The Asian clam was found in the Evros River Basin, the second largest river in southeastern Europe (after the Danube), and the main river in the Balkan Peninsula, with a total length of about 530 km and a drainage area of 53,000 km2. This transboundary river is shared among Bulgaria, Turkey, and Greece.

On the 8th of September 2018, 12 individuals of C. fluminea were found during a routine EU Water Framework Directive monitoring in the lower part of the Erythropotamos river, only 2.5 km from its confluence with the main-stem of the Evros river (Fig. 1); specimens were photographed alive on-site and re-released into the water. Benthic conditions are dominated by silt, and there are also gravel and sandy substrates with some woody debris. Margins are rich in aquatic macrophytes (including floating plants, such as Trapa natans) and fringed with helophytes (e.g. Sparganium sp., Typha sp.). The sampled site is rich in fish; 17 species have been recorded in recent years. Due to low river waters creating exposed river beds, the living clams were incidentally located in the shallows. Physicochemical parameters of the sampling location were measured with a GPS Aquameter from Aquaread Ltd.

thumbnail Fig. 1

Map showing the sampling site of Corbicula fluminea.

Due to the taxonomic uncertainties involving the Corbicula genus, the identity of the species was verified by genetic analysis. Whole genomic DNA was extracted from small tissue pieces preserved in 96% ethanol, using a standard high-salt protocol (Sambrook et al., 1989), from 2 individuals. A fragment of the cytochrome oxidase c subunit I gene (COI) was amplified by PCR using universal primer modified versions, i.e., LCO22me2 and HCO700dy2 (Walker et al., 2006, 2007). PCR conditions are described in Froufe et al. (2014) with an annealing temperature of 48 °C. Amplified DNA templates were purified and sequenced (forward and reverse) by the commercial company Macrogen, using the same primers. The sequences obtained were compared with sequences present in GenBank using BLAST (Altschup et al., 1990) and with the BOLD database (Ratnasingham and Hebert, 2007). No indels and no stop codons were observed, after translating all sequences to amino acids. The identification of the newly sequenced individuals (a single haplotype: GenBank SUBMITTED) as C. fluminea was confirmed by both BOLD (99.8% match) and BLAST (99.6%).

The physicochemical characteristics of sampling locality are presented in Table 1. Overall, the physicochemical quality of the sampling site was good, as classified according to the physicochemical quality index (Skoulikidis et al., 2006); however, fish-based assessments of the lower Erythropotamos water body have indicated moderate to poor conditions in recent years, mainly due to degradation from water abstraction, hydromorphological changes and seasonal eutrophic conditions that affect natural fish assemblages (Zogaris et al., 2018). Although the potential use of Corbicula species for biomonitoring purposes has been suggested (e.g. Doherty, 1990), C. fluminea is considered generally intolerant to severe pollution (e.g. Ilarri et al., 2010). Europe's Directives on improving ecological quality may have facilitated invasion by providing better environmental conditions for all life stages of C. fluminea (Karatayev et al., 2007) as this seems to be correlated with the reinvasion of zebra mussel in some European rivers (Jantz and Neumann, 1992) and other invasive species in the Laurentian Great Lakes of North America (Mills et al., 2003).

Table 1

Physicochemical parameters and habitat characteristics of C. fluminea collection site.

In most cases dealing with biological invasions, it is very difficult to trace the introduction vectors and pathways and the subsequent dispersion. In Europe for example, inland waterway connectivity facilitates the spread of invasive non-autochthonous species (Leuven et al., 2009; Panov et al., 2009). European floodplains (i.e. low altitude rivers) are the main corridor routes consisting of an interlinked network of 30 main canals with more than 100 branches, and more than 350 ports (Panov et al., 2009; Galil et al., 2008). An increasing number of dams have also facilitated many lentic alien and translocated species (Koutsikos et al., 2019) and large river systems such as the Evros have experienced recent developments, particularly in the Evros river basin's Bulgarian section.

We speculate that C. fluminea reached the Greek waters of Erythropotamos river most possibly through passive downstream transport from Bulgaria. The Evros river basin has been called an “open-door” for invasive alien biota (Ozulug et al., 2018). This refers to human-assisted aquatic species dispersal which disperses downstream of Bulgarian entry points. In this way, the north-south running Evros and its tributaries such as the Erythropotamos, are pathway gates for species entering the Aegean basins of Greece and Turkey from Bulgaria's Danubian and Black Sea basin invasive alien biota (Zogaris et al., 2019). In recent years this transport could have been either facilitated by human activities, such as increased hydro-electric dam-building, fishing and various recreational activities or by bird transfer (Crespo et al., 2015; Coughlan et al., 2017) or naturally by downstream drift. C. fluminea has found to be capable of floating after being exposed to gentle water currents produced by an aquarium filtration system (current speeds, 10 to 20 cm/sec; Prezant and Chalermwat, 1984). The first record of C. fluminea in Bulgaria was from the Danube River at Vetren in 2001 and after 11 years the species has occupied the entire Bulgarian stretch of the Danube, from Vrav to Vetren, where it reached densities up to 16,560 ind/m2 (Hubenov et al., 2013). Recently, the species was also found in lentic waters, two reservoirs and one sand-pit lake, located at altitudes of up to 525 m a.s.l. (Hubenov et al., 2013). Based on the Bulgarian invasion experience with the species, it is anticipated that the entire Evros River Basin is or soon will be occupied by the clam. Thus, more detailed surveillance is urgently needed in order to assess the degree of C. fluminea establishment in the basin and adjacent freshwater bodies.

Acknowledgements

This contribution represents incidental observations and collections made during the National Water Framework Directive monitoring project funded by the Ministry of Environment and Energy and by the European Union. We thank D. Kommatas and the boat-based electrofishing unit for assistance in field work, Dr. E. Dimitriou scientific coordinator of the project and the two anonymous for their valuable comments.

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Cite this article as: Karaouzas I, Zogaris S, Froufe E, Lopes-Lima M. 2020. Rival at the gate: first record of the Asian clam Corbicula fluminea Müller, 1774 (Bivalvia: Corbiculidae) in Greece. Knowl. Manag. Aquat. Ecosyst., 421, 24.

All Tables

Table 1

Physicochemical parameters and habitat characteristics of C. fluminea collection site.

In the text

All Figures

thumbnail Fig. 1

Map showing the sampling site of Corbicula fluminea.
In the text

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