Genetic and shell morphological variability of the invasive bivalve Corbicula fluminea (Müller, 1774) in two Portuguese estuaries

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Abstract

The identification of different species inside the Corbicula genus is complicated due to the high variation of shell shape, colour and sculpture of the individuals. The species Corbicula fluminea has been present in the River Minho estuary (NW Portugal) at least since 1989. More recently, individuals of the same genus colonized an adjacent estuary (River Lima estuary). Although appearing also to be C. fluminea, the individuals of the Lima estuary differ from those of Minho estuary in the colour and shape of the shell. Therefore, the two populations were compared by conventional morphometric measures (shell length, width and height), geometric morphometric methods (landmarks analysis using the interior of the shell) and genetic analysis (based on the mitochondrial cytochrome c oxidase subunit I gene sequence). Genetic analysis showed an identical mtCOI sequence indicating that both populations belong to the species C. fluminea. However, results of conventional and geometric morphometric analysis showed significant differences in shell shape between individuals from the two populations. These differences may be due to (a) phenotypical plasticity in response to different environmental and/or ecological conditions existing in the two estuaries, (b) different origins of the populations and/or distinct routes until reaching the two estuaries and (c) inter-population genetic differences caused by processes occurring after the introduction of the species in the two estuaries (e.g. differential selection).

Introduction

The original distribution of the Corbicula genus in the beginning of the last century was confined to lentic and lotic ecosystems of Asia, Africa and Australia (Pilsbry and Bequaert, 1927 in Lee et al., 2005). Since then, some species have spread throughout the world due to a combination of human and natural dispersion mechanisms (Araujo et al., 1993, McMahon, 1999, McMahon, 2002). The first documented occurrence, outside their native range, was in the United States Pacific coast, in the 1920s. Forty years later, its distribution was extended to the United States Atlantic coast (McMahon, 1999). During the 1970s, specimens belonging to this genus spread into South America (Ituarte, 1994) and, in the 1980s, into Europe (Mouthon, 1981).

Portuguese rivers have been colonized by Corbicula at least since the 1980s (see Mouthon (1981) for the first published European description), although local fishermen in the River Tejo recognized the presence of individuals of this genus and used them as bait, in the early 1950s. The principal Portuguese hydrological basins (e.g. Minho, Lima, Douro, Vouga, Mondego, Tejo, Sado and Guadiana) have been colonized by this genus. However, the taxonomy of the species present remains uncertain in the most part of the cases. This is not a surprise since the studies that have been performed with European, American and Asiatic populations have been showing that the identification of different species within the Corbicula genus is very difficult, due to the marked variation in shell morphology, colour, sculpture and reproductive biology of the individuals (Komaru and Konishi, 1999, Rajagopal et al., 2000, Renard et al., 2000, Siripattrawan et al., 2000, Qiu et al., 2001, Park et al., 2002, Pfenninger et al., 2002, Park and Kim, 2003, Lee et al., 2005).

Due to their invasive and dispersal potential, some species of the Corbicula genus can cause important ecological and economical impacts, such as changes in food webs, bioaccumulation of environmental contaminants, competition with native bivalves and serious biofouling problems (Phelps, 1994, Darrigran, 2002). Consequently, taxonomical, biological and ecotoxicological studies concerning Corbicula species are fundamental to support management actions to overcome problems resulting from their invasion and habitat colonization.

The Minho and Lima estuaries, located in the NW of Portugal, were colonized by Corbicula: in the Minho estuary, the presence of Corbicula fluminea has been recorded since 1989 (Araujo et al., 1993), while in the Lima estuary, the presence of a bivalve also classified as C. fluminea was noticed in 2002 (Sousa et al., 2006a, Sousa et al., 2006b). The observation of individuals from both populations suggests that they have morphological differences in the shape and colour of the shells. In addition, they have been showing apparently distinct invasive and dispersal patterns (Sousa et al., 2005, Sousa et al., 2006a, Sousa et al., 2006b, Sousa et al., in press b, Sousa et al., in press c), even considering the earlier introduction of the species in the Minho estuary. Therefore, the main objective of this study was to compare the Corbicula populations of Minho and Lima estuaries, using conventional morphometric measures (shell length, width and height), geometric morphometric methods to determine differences in shell shape (based on landmarks analysis using the interior of the shell) and genetic analysis (based on the mitochondrial cytochrome c oxidase subunit I gene sequence). Additionally, mtCOI sequences of individuals from both populations were compared with pre-existing mtCOI sequences in an attempt to identify the origin of both populations.

Section snippets

Study area

The Rivers Minho and Lima are located in the NW of the Iberian Peninsula (Fig. 1a,b). These rivers spring in Spain and both hydrological basins have considerable geological and hydrological similarities (Sousa et al., 2005, Sousa et al., 2006a, Sousa et al., in press a, Sousa et al., in press b, Sousa et al., in press c). The River Minho is about 300 km long, with an estuary of about 40 km. The River Lima is about 108 km long and has an estuary of about 20 km.

Sampling and laboratory analysis

Individuals were collected using a Van

Colour and morphometry

The inner shell colour of the two populations is different. Individuals from the Minho estuary have an inner nacre purple surface (primarily in the margin of the shell), whereas the ones from the Lima estuary have a whitish coloration. However, this difference is not as clear as the report example in Park et al. (2002).

Shape analysis revealed evident shell differences between the two estuarine populations. The conventional morphometric measures used showed clearly that Lima individuals having

Discussion

In molluscs, shell characteristics have been widely used in species identification. However, their exclusive use for taxonomic and systematic studies is controversial and, at least in some cases, needs to be complemented by genetic analysis (Wilke and Falniowski, 2001). Consequently, in this study morphometric and genetic analysis was used to compare two Corbicula populations colonizing two adjacent Portuguese estuarine ecosystems.

Previous studies performed with Corbicula populations showed

Acknowledgements

Ronaldo Sousa is supported by a PhD grant (SFRH/BD/18426/2004) and Marta Rufino by a Postdoctoral grant (SFRH/BPD/14935/2004) from the Portuguese Foundation for Science and Technology—FCT. This work was partially funded by FEDER European funds, through the project RISKA (POCTI/BSE/46225/2002). Special thanks are addressed to Dr. Sandra Doherty for the English revision and to Eduardo Martins and Gonçalves for technical assistance.

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