Distribution of the invasive bivalve Sinanodonta woodiana ( Lea , 1834 ) in Croatia

The Chinese pond mussel Sinanodonta woodiana is an invasive bivalve species present in the flowing and standing waters of most of Europe. Field research conducted from 2007 to 2011 indicated that this species has colonised the entire eastern part of Croatia, and that its spread westward is continuing. During our study, S. woodiana was recorded at 54 localities.


Introduction
The Chinese pond mussel Sinanodonta woodiana (Lea, 1834) is a species native to East and South-East Asia.Some authors have placed this species within the order Anodonta though newer taxonomic research has placed it in the order Sinanodonta (Bogatov and Sayenko 2002).In Europe it was first discovered in Romanian fish farms at Cefa-Oradea in 1979(Sàrkàny-Kiss 1986).In Hungary S. woodiana was recorded in 1980 (Petró 1984).In the meantime, this species has been discovered in a number of European countries: France (Girardi and Ledoux 1989), Slovakia (Košel 1995), Czech Republic (Beran 1997), Austria (Reischutz 1998), Poland (Bohme 1998), Ukraine (Urishients and Korniushin 2001), Italy (Manganelli et al. 1998), Germany (Glöer and Zeittler 2005), Serbia (Paunovic et al. 2006) and Sweden (von Proschwitz 2006).The spread of S. woodiana has continued and it has since been reported on several Indonesian islands, the Dominican Republic and Costa Rica (Watters 1997).In these countries, the species has succeeded in establishing stable populations, and continuing its spread.In the meantime, it has also been discovered in Moldova (Munjiu andShubernetski 2008), Spain (Pou-Rovira et al. 2009), and most recently in the United States (Bogan et al. 2011).
It is believed that the primary pathway of introduction of this species to Europe was with Asian fish species, such as silver carp (Hypophthalmichthys molitrix Valenciennes, 1844), bighead carp (Aristichthys nobilis Ricardson, 1844) and grass carp (Ctenopharyngodon idella Valenciennes, 1844), primarily introduced to regulate aquatic vegetation in fish ponds (Paunovic et al. 2006).Many of these fish carried bivalve larvae in their gills or fins that were not noticed due to their small size.In the Republic of Croatia, these fish were introduced to fish ponds in the 1960s (Bojčić and Bunjevac 1982).
The first data on the distribution of S. woodiana in Croatia were reported by Paunovic et al. (2006).These data were for the Danube River, which forms the border between Croatia and Serbia.International research was conducted on the Danube in 2007 and also confirmed the presence of this bivalve species in the Croatian part of the Danube (Graf et al. 2008).Its distribution in Croatia outside of the Danube River was unknown until now.Therefore, the primary objective of this paper was to determine actual distribution of S. woodiana throughout Croatia.

Study site
Research was conducted on natural watercourses such as rivers, lakes, backwaters and artificial habitats such as channels and fish ponds throughout Croatia (Pannonian-Peripannonian, Dinarid and Mediterranean geographical units).Watercourses in Croatia belong to two basins: the Adriatic and Black Sea basins.

Data collection
Research on the species Sinanodonta woodiana was conducted in the period 2007 to 2011.Bivalves were collected using a benthos net and by diving at some sites.

Results
The species Sinanodonta woodiana was confirmed at 54 localities (Figure 1; Appendix 1) mostly within the Pannonian-Peripannonian region (the Danube, Black Sea Basin).Only one case of introduction has been confirmed for the Mediterranean region -the Vrana Lake (Appendix 1, Record No. 12).It was not detected in the Dinarid Region of Croatia.
The first report of this species in Croatia was for the Danube River in September 2001 at the localities Ilok and Erdut (Paunović et al. 2006).The next report (2006) confirms its presence in the Ilova River near Kutina (Appendix 1, Record No. 3).Confirmation that this was in fact Sinanodonta woodiana was obtained in 2011 when the collected material was examined as part of another project.
The largest specimen of this species found in Croatia to date was found in the Mali Strug Channel near Stara Gradiška (Figure 2; Appendix 1, Record No. 10).The adult individual was 25.10 cm long, 14.29 cm tall and 9.72 cm wide, with a wet mass of 1.335 kg.
It is of particular concern that these individuals have been found within two Nature Parks: Lonjsko Polje (Figure 2; Appendix 1, Record No. 10) and Kopački Rit (Figure 3; Appendix 1,Records No. 52,53,54).Both of these parks represent important wetland habitats at the European level.Kopački Rit is connected to the Drava and Danube Rivers by channels, while Lonjsko Polje is situated alongside the Sava River.

Discussion
As mentioned in the introduction, the primary pathway of introduction of this species to Europe is thought to be the introduction of Asian fish species (Paunovic et al. 2006).The first find of this species in Croatian watercourses was made by scientists investigating the Danube River, which forms the border between Serbia and Croatia (Paunovic et al. 2006;Graf et al. 2008).Paunovic et al. (2006) made the assumption that the Danube is an important watercourse for the spread of this species eastwards into the Serbian watercourses.A similar conclusion was reached in this study, which confirmed the widespread presence of this species in Croatia.The species has spread from the Danube into its large tributaries, the Drava and Sava Rivers, and their tributaries.
On the other hand, we assumed that the record of this species in fish ponds indicates a second possible pathway of spread in Croatia.The transport of carrier fish and/or water from one fish pond or water course to another has also enabled the wider transport of this species.Furthermore, if the fish ponds are equipped with flowing water, bivalves can enter into the tributaries and rivers.This is a somewhat slower, though significant pathway of invasion for this species.
The find of empty shells of the species S. woodiana in Nature Park Vrana Lake in the Mediterranean region is likely the consequence of the introduction of individuals of this species from continental parts of Croatia.Vrana Lake is known for its rich fish fauna as an important destination for sports fishermen from continental Croatia, particularly during the summer vacation period.Fishermen bring bivalves with them for use as bait.Research of the malacofauna of this lake is ongoing and the presence of this species has not been confirmed.It can be assumed that any live bivalves that may have been released into the lake likely did not survive, due to stress caused by increased salinity as this lake is connected to the sea by a manmade channel.
This species is known to seriously threaten the native population of bivalves from the family Unionidae.Fabbri and Landi (1999) stated that the native species A. anatina had been completely replaced by S. woodiana in several channels with a soft substrate and high trophic level.The Chinese pond mussel is a direct competitor for food and space with native species, while another important factor is competition for fish hosts (Rashleight 1995;Fabbri and Landi 1999) as the larvae of these species develop on the gills and fins of fish.Dudgeon and Morton (1983) stated that this species reproduces two to three times per year, unlike the native species, which typically reproduce only once per year.The same authors also stated that S. woodiana becomes sexually mature in the first year of life at a shell length of 3 to 4 cm, and individuals have an average life span of 12 to 14 years.The parasite phase of the life cycle lasts 5-15 days, depending on the water temperature.Research has shown that this species is not selective with regards to the fish host, which is a significant advantage (Douda et al. 2011).The species also has a much higher rate of increase and better tolerance of hypoxia and pollution than native species (Sîrbu et al. 2005).Due to the above mentioned invasive characteristics of S. woodiana, it can be expected that all the native bivalve species in Croatia will be threatened.
Research conducted in the channels of Miedzyodrze in Poland indicated that this species is resistant to unfavourable habitat conditions, and was found in waters that partially freeze in winter (Domagala et al. 2007).The same applies for watercourses in Croatia, as during winter, the air temperature drops below freezing and shallow sections of rivers and lakes also freeze.
The shell length of individuals found in Croatian waters indicates that this species has long been present here, and finds of individuals of varying size indicates that the biotic and abiotic conditions of these habitats are favourable.In other words, the species has established stable populations capable of reproducing.
In Croatia, three additional invasive mollusc species have been confirmed to date: the bivalves Dreissena polymorpha (Pallas, 1771), Corbicula fluminea (O.F. Müller, 1774) and the snail Potamopyrgus antipodarum (Gray, 1843) (Lajtner et al. 2004;Gottstein et al. 2009).These species are known in central and eastern Croatia, indicating that the main pathway of entry and spread of invasive mollusc species are the large lowland rivers, and that the species are spreading upstream and into the tributaries.S. woodiana has not yet been found in the rivers of the Adriatic basin.There are two possible reasons for this: the Dinarid mountain range forms a geographic barrier, making contact between these two basins impossible.On the other hand, in the lower courses of the Adriatic rivers where the substrate is suitable, i.e. silty-sandy, the water is brackish.
It can be assumed that the process of expansion of this species in Croatia will continue and that this species will enter into the tributaries of the large rivers in central Croatia where both the physicochemical parameters and substrate type are suitable.It can also be expected to spread into southwestern Croatia, primarily into the fish ponds and reservoirs.In areas where it is already present, it can be expected to form dense populations.For the above reasons, regular monitoring of this species is required.