Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 418, 2017
Article Number 37
Number of page(s) 6
DOI https://doi.org/10.1051/kmae/2017023
Published online 21 August 2017

© V. Prié and J.-F. Fruget, Published by EDP Sciences 2017

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://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.

1 Introduction

Non-indigenous invasive species are one of the most important threats to biodiversity and ecosystems (Carlton and Geller, 1993; Sala et al., 2000; Cox, 2004). Freshwater ecosystems are particularly impacted by these invasive species (Lodge et al., 1998; Orr, 2003). Among freshwater invertebrates, freshwater bivalve species are being introduced worldwide at an increasing rate, mainly because of human activities (Darrigran, 2002; Karatayev et al., 2007). In France alone, nine species of freshwater bivalves have been introduced: Mytilopsis leucophaeata (Conrad, 1831) from 1835, Dreissena polymorpha (Pallas, 1771) since 1852, Corbicula fluminea (O.F. Müller, 1774), Corbicula fluminalis (O.F. Müller, 1774) and Corbicula leana Prime, 1867 since the 80s (although taxonomic issues are controversial, leading to a doubt regarding the introduction dates) (Mouthon, 1981; Pigneur et al., 2011; Hesse et al., 2015), Sphaerium transversum (Say, 1829) since 1984, Sinanodonta woodiana (Lea, 1834) since 1982 (Mouthon, 2008; Adam, 2010), Euglesa compressa (Prime, 1852) since about 2010 (Mouthon and Forcellini, 2017) and Dreissena rostriformis bugensis (Andrusov, 1897) since 2011 (Bij de Vaate and Beisel, 2011; Marescaux et al., 2015). Introduction processes are likely going on nowadays. But the lack of taxonomists and field malacologists makes invasive species detection challenging. Ecosystems invasions may be overlooked, especially when the species involved are similar in shell shape to those pre-existing; or when they live in hard to survey environments such as downstream ecosystems of large rivers.

The zebra mussel D. polymorpha is a common species in France. Generally abundant, widespread and of no conservation concern, the zebra mussel does not attract naturalists' attention. The quagga mussel D. rostriformis bugensis is similar in shell shape and lives in the same habitats. It has been noticed in France for the first time in 2011 (Marescaux et al., 2012). It is likely that the quagga mussel's expansion in France has remained unnoticed or overlooked for the last decade.

This note presents new data about the ongoing invasion of the quagga mussel in France and discusses its potential distribution for now and tomorrow.

2 Material and methods

2.1 Data collection

Data comes from environmental DNA (eDNA, Taberlet et al., 2012) samples, as already been used for detecting Dreissena species (Lance and Carr, 2012; De Ventura et al., 2017); direct observation during scuba-diving malacological surveys; and dredging of sediment. Water samples were analyzed by SpyGen® for eDNA extraction, amplification and sequencing (for details on this unpublished protocol, see the methods developed by Valentini et al., 2016 for fishes and amphibians; and for freshwater bivalves, await Prié et al., in prep.). Direct observation in scuba diving involved four divers during five days in the Saône River and allowed taking pictures in the field and collecting specimens by hand. The collected specimens were then processed in the lab and flesh samples were extracted, amplified and sequenced by Eurofins®. Dredging was performed in the Rhône main channel using a boat and a standard triangular dredge. Collected sediment samples were curated in the lab.

2.2 Data location

Data presented here comes from the Vignoble Lake (Escaut coastal drainage) and the Saône River (Rhône coastal drainage), respectively in 2015 using environmental DNA and in 2016 using environmental DNA and with direct observation during a malacological survey. Locations and collection date were as follows:

  • Vignoble Lake, 50.341667 N, 3.499510 E, 07/09/2015, Environmental DNA, sampling X. Cucherat, identification V. Prié (Biotope);

  • Saône River, Pontaillier-sur-Saône, 47.305809 N, 5.420149 E, 19/07/2016, direct observation during scuba-diving survey, collection and identification V. Prié (Biotope);

  • Saône River, Maillys, 47.125213 N, 5.339523 E, 19/07/2016, direct observation during scuba-diving survey, collection and identification V. Prié (Biotope);

  • Saône River, Tillenay, 47.188770 N, 5.365820 E, 19/07/2016, direct observation during scuba-diving survey, collection and identification V. Prié (Biotope);

  • Saône River, 47.275757 N, 5.389430 E, 19/07/2016, direct observation during scuba-diving survey, collection and identification V. Prié (Biotope);

  • Saône River, Pontaillier-sur-Saône, 47.305562 N, 5.419387 E, 19/07/2016, environmental DNA, sampling and identification V. Prié (Biotope);

  • Saône River, Maillys, 47.125214 N, 5.339523 E, environmental DNA, sampling and identification V. Prié (Biotope);

  • Rhône River, Chavanay, 45.416863 N, 4.743379 E, 12/04/2016–28/06/2016–01/09/2016–26/10/2016, sediment sampling in the deep main channel with triangular dredge, collection J.F. Fruget (Aralep), identification Jeanne Dessaix (Aralep);

  • Rhône River, Saint-Rambert-d'Albon, 45.298781 N, 4.805102 E, 12/04/2016–07/07/2061–01/09/2016–25/10/2016, sediment sampling in the deep main channel with triangular dredge, collection J.F. Fruget (Aralep), identification Jeanne Dessaix (Aralep);

  • Rhône River, Arcoules, by-passed section, 45.358505 N, 4.767272 E, 13/04/2016–07/07/2016–02/09/2016–03/11/2016, sediment sampling with triangular dredge, collection J.F. Fruget (Aralep), identification Jeanne Dessaix (Aralep).

2.3 Species identification

In the Saône and Rhône Rivers, the specimens were identified in the field by their shell morphology which combined the following diagnostic characters: asymmetry of the shell valves as seen from the ventral view, byssus located near the hinge (Fig. 1A); periostracum dark brown with no zebra lines (Fig. 1B); rounded ventral margin with no acute ventrolateral ridge or carina (Fig. 1C), which are the main differences with the zebra mussel; absence of apophysis (Fig. 1D), which is the main difference with M. leucophaeata. Live specimens were noticed first by their remarkably long siphon (Fig. 1E). All these morphological characters correspond to quagga mussel description (Pathy and Mackie, 1993; Sablon et al., 2010).

Five specimens were sampled and COI gene fragments were amplified using standard protocols (e.g. Prié et al., 2012) for barcoding purpose (GenBankaccession numbers MF469063, MF469064, MF469065). Additionally, 16S eDNA sequence fragments were amplified from samples collected in the Saône River and Vignoble Lake. COI fragments from live specimens and 16S fragments from eDNA were aligned with available sequences mined from GenBank using BioEdit 7.2.5 (Hall, 1999).

thumbnail Fig. 1

Dreissena rostriformis live specimen collected in the Saône River in 2016. (A) Ventral view showing the asymmetric shell shape and the position of the byssus; (B) lateral view, left valve, with no zebra lines pattern; (C) frontal view showing the diagnostic rounded shell edges; D: zoom on the hinge; E: a living specimen in the Saône River, with long siphon extended. Scale bar: 20 mm (D and E not to scale).

2.4 Taxonomy

The use of the names D. rostriformis (Deshayes, 1838) or D. bugensis (Andrusov, 1897) for the introduced quagga mussel has been controversial (Stepien et al., 2003; Rosenberg and Huber, 2012; Bieler et al., 2015). These nominal species are here considered as synonyms following the conclusions of the molecular phylogenies established by Therriault et al. (2005) and Stepien et al. (2014). According to the principle of priority, the name D. rostriformis should then be applied to the quagga mussel. However, the nominal subspecies D. rostriformis rostriformis is a marine deep-water mussel which is not known to be an invader and remains endemic to the Caspian Sea. The invasive quagga mussel is believed to be a descendant which evolved in the isolated Black Sea. The Black Sea had a freshwater period, possibly leading to an ecological adaptation of its quagga mussel population. Indeed, the quagga mussel found today in Europe lives in a different range of salinity. It is therefore arguable that the European quagga mussel could be considered a distinct species. However, we lack reproduction experiments as both clade cannot be acclimated to a common salinity level. Given the taxonomic uncertainty, and even if this is not satisfactory, we here refer to the European quagga mussel as D. rostriformis bugensis.

3 Results

3.1 Presence data

In the Vignoble Lake, we have no direct observation of quagga mussels and only eDNA revealed its presence, together with the zebra mussel. In the Saône River, the species was abundant. Live specimens have been seen in every surveyed site between Pontailler-sur-Saône and Maillys (Fig. 2), mixed with D. polymorpha. Individuals were always fixed to substrate (pebbles, stones and rocks) and sometimes to another freshwater mussel species (most often Potomida littoralis). Southwards in the Rhône, live specimens were found in the sediment collected in the main channel by dredging. Hundreds of specimens were collected from a substrate of pebbles and gravels, suggesting the species has reached the lower Rhône since many generations. eDNA samples do not allow quantification of the species occurrence, but amplified fragments were very abundant in all sample sites.

thumbnail Fig. 2

D. rostriformis data in France. Bluelines: main rivers; gray dotted lines: canals; orange dots: data 2011–2014; red dots: data from 2015; white dots: absence data 2015–2017.

3.2 Absence data

Based on previous tests comparing the effectiveness of eDNA surveys to traditional methods (Prié et al., in prep.), we showed that the eDNA detection method is very accurate for freshwater bivalves. We consider it is trustful enough to be used for absence assessment. Since 2015, eDNA samples were collected from various places in France, in the Rhône, Loire drainages and in Mediterranean coastal rivers (Fig. 2). None revealed quagga mussel eDNA fragments.

Malacological investigations in Cruas and Tricastin in the lower section of the Rhône, using traditional methods accurate enough for the detection of the species, did not allowed finding any quagga mussels either. We therefore consider the species as absent from these places for now.

4 Discussion

4.1 Historical data

The quagga mussel D. rostriformis is native from the Caspian Sea; the subspecies D. rostriformis bugensis being considered as coming from the Dniepr and Bug deltas in the Black Sea (Orlova et al., 2004; Son, 2007). Its first expansion into rivers dates back to the years 1940–1990: to the north along the Dnieper River; to the East through the Don River and then on to the Volga River; and to the north-east through the Dniester River (Orlova et al., 2004; Woźniczka et al., 2016). The quagga mussel has colonized western Europe only recently: it was recorded in the lower part of the Danube River only in 2004 (Micu and Telembici, 2004). The Danube is a key river for the European southern invasion corridor, being connected to the Rhine basin (Panov et al., 2009; Leuven et al., 2009), and from there to almost all major coastal drainages in France via canals. The species has probably spread very rapidly from the early 21st century, as it was first observed in the Rhine River in Netherlands in 2004 too (Imo et al., 2010; Heiler et al., 2013), then in the Dutch section of the Meuse River in 2007 (Marescaux et al., 2012) and in the Albert Canal, which connects the Meuse River, in Belgium in 2009 (Sablon et al., 2010). Not surprisingly, the species was observed in the French section of the Meuse and Moselle Rivers in 2011 (Bij de Vaate and Beisel, 2011; Marescaux et al., 2012); and in the French section of the Rhine River in 2014 (Wagner, 2014). We here observe an important extension in two more River drainages, the Escaut, which is close and directly connected to the Meuse River drainage; and a lot further south in the Rhône River drainage, first record of occurrence in a Mediterranean drainage occurrence in France (Fig. 2). This significant leap augurs a further extension in most French drainages.

4.2 Existing colonization routes in France and future perspectives

Coastal drainages' geographical isolation is a driving force of genetic drift and subsequent speciation processes. Today's human development, with the establishment of canals, tends to mix up previously isolated faunas. Artificial connections between coastal drainage systems provide a serendipitous opportunity for invasive species to spread out of their introduction localities.

The quagga mussel displays a more important invasive potential than the zebra mussel. Replacement of zebra mussel by quagga mussel is now well documented, having been observed at several locations in its initial expansion routes around the Black Sea (Dniepr, Don, Volga) as well as in Europe (Marescaux et al., 2015) and northern America (e.g. Stoeckmann, 2003; Wilson et al., 2006; Ram et al., 2011; Stewart, 2014). We can therefore expect an important expansion of the quagga mussel population in the Rhône drainage, including its tributaries, but also in the adjacent drainages: canals provide artificial pathways from the Rhône to the Seine, Loire and Garonne drainages (Fig. 3).

thumbnail Fig. 3

Potential past and future expansion corridors. Blue lines: main French rivers; blue dotted lines: canals; small dots: data before 2014; large dots: data after 2014; large arrows: possible past expansion ways; thin arrows: possible future expansion ways.

5 Conclusion

Zebra mussels are introduced in France for a long time, are common where they occur, and naturalists do not pay attention to them. The similar-shaped quagga mussel was observed for the first time in north-eastern French Rivers in 2011. It has probably spread out slowly to adjacent watercourses using canals, but has been overlooked. We here synthetize its current distribution in France based on direct observation and eDNA studies. Actual distribution is probably much wider than what sparse data suggest. Existing pathways via canals suggest the quagga mussel can colonize the main French drainages in a near future.

Hydrobiologists from central and western France should watch out: if not yet there, quagga mussels may arrive in the next few years.

Acknowledgments

Benjamin Adam, Xavier Cucherat, Nicolas Legrand, Laurent Philippe, Nicolas Patry, Lucas Berenger (Biotope), Jeanne Dessaix (Aralep), Tony Déjean, Alice Valentini, Pauline Jean (SpyGen). This work was conducted within the scope of the LIFE project “Life13BIOFR001162 Conservation of the Giant Pearl Mussel in Europe”. We also thank an anonymous reviewer for valuable comments about the quagga mussel's taxonomy and origins.

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Cite this article as: Prié V, Fruget J-F. 2017. Heading south: new records of the invasive quagga mussel Dreissena rostriformis bugensis (Andrusov, 1897) in France and further perspectives. Knowl. Manag. Aquat. Ecosyst., 418, 37.

All Figures

thumbnail Fig. 1

Dreissena rostriformis live specimen collected in the Saône River in 2016. (A) Ventral view showing the asymmetric shell shape and the position of the byssus; (B) lateral view, left valve, with no zebra lines pattern; (C) frontal view showing the diagnostic rounded shell edges; D: zoom on the hinge; E: a living specimen in the Saône River, with long siphon extended. Scale bar: 20 mm (D and E not to scale).

In the text
thumbnail Fig. 2

D. rostriformis data in France. Bluelines: main rivers; gray dotted lines: canals; orange dots: data 2011–2014; red dots: data from 2015; white dots: absence data 2015–2017.

In the text
thumbnail Fig. 3

Potential past and future expansion corridors. Blue lines: main French rivers; blue dotted lines: canals; small dots: data before 2014; large dots: data after 2014; large arrows: possible past expansion ways; thin arrows: possible future expansion ways.

In the text

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