Corbicula fluminea (Asian clam)
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PicturesTop of page
|Title||Collection of live clam shells|
|Caption||Corbicula fluminea (Asian clam); a collection of live clam shells at various stages of development.|
|Copyright||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
|Collection of live clam shells||Corbicula fluminea (Asian clam); a collection of live clam shells at various stages of development.||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
|Title||Clam shells at various stages of development|
|Caption||Corbicula fluminea (Asian clam); clam shells at various stages of development. Note Biro for scale.|
|Copyright||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
|Clam shells at various stages of development||Corbicula fluminea (Asian clam); clam shells at various stages of development. Note Biro for scale.||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
|Caption||Corbicula fluminea (Asian clam); single shell. Note scale against pen tip.|
|Copyright||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
|Shell||Corbicula fluminea (Asian clam); single shell. Note scale against pen tip.||©Crown Copyright-2009/GB Non-Native Species Secretariat (GB NNSS)|
IdentityTop of page
Preferred Scientific Name
- Corbicula fluminea Muller, 1774
Preferred Common Name
Other Scientific Names
- Corbicula fluminalis Muller, 1774
- Corbicula leana Prime, 1864
- Corbicula manilensis Philippi, 1844
International Common Names
- English: Asiatic clam; clam, Asian; prosperity clam
- Spanish: almeja Asiatica
Local Common Names
- Korea, Republic of: black clam; jaecheop; kkamak jogae
- Taiwan: freshwater clam
Summary of InvasivenessTop of page
C. fluminea has caused numerous problems in its new range of distribution. C. fluminea spreads when it is attached to boats or carried in ballast water, used as bait, sold through the aquarium trade and carried with water currents. Its reproductive success and ability to spread rapidly has resulted in this species having one of the most rapid expansions of any non-native species in North America. Before the invasion of the zebra mussel Dreissena polymorpha, in North America, C. fluminea was described by McMahon (1983) as ‘one of the most important molluscan pest species ever introduced into the United States’. Aldridge and Muller (2001) review the potential impacts that the spread of C. fluminea may have on British industry and aquatic systems.
In the DAISIE project, C. fluminea is listed on the 100 worst invasive species.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Mollusca
- Class: Bivalvia
- Subclass: Heterodonta
- Order: Veneroida
- Superfamily: Corbiculoidea
- Family: Corbiculidae
- Genus: Corbicula
- Species: Corbicula fluminea
Notes on Taxonomy and NomenclatureTop of page
In the attempt to end ecomorphotype confusion in the Asia range, Morton (1986) recognizes only two species: Corbicula fluminea a freshwater species and all estuarine dioceous non-brooding species as C. fluminalis. However, this division was refuted when several phylogenetic studies showed clear differences among species (Hillis and Patton, 1982; Hatsumi et al., 1995; Lee and Kim, 1997; Renard et al., 2000; Siripattrawan et al., 2000).
DescriptionTop of page
C. fluminea is a small clam with an inflated shell, slightly round to triangular in shape. The most distinctive feature is the shell which bears numerous heavy concentric ridges. The shell is usually pale brownish or yellowish brown, olivaceous to black. Internally there are three cardinal teeth in each valve and the lateral teeth are heavily serrated. The nacre varies from white to salmon or deep purple. Qiu et al. (2001) reported yellow and brown shell colour morphs amongst specimens collected from Anyue County in Sichuan Province in China. The shells of the yellow morphs were straw yellow on the outside and white on the inside; those of brown morphs were dark brown and purple, respectively. Further analyses revealed that the yellow and brown morphs are triploid and tetraploid, respectively. Both morphs were simultaneous hermaphrodites and brood their larvae in the inner demibranchs. The results indicate that C. fluminea at different ploidy levels is able to reproduce by self-fertilization. The life span is about one to seven years, and it can grow to a shell length of 50-65 mm, although it is usually less than 25 mm.
DistributionTop of page
Although C. fluminea is a freshwater species native to southern and eastern Asia (Russia, Thailand, Philippines, China, Hong Kong, Taiwan, Korea and Japan) and Africa (Britton and Morton, 1979), it is now found in freshwater and salt water throughout the USA, including all five Gulf states and northern Mexico, and much of Europe. It was probably brought into the USA by Chinese immigrants as a source of food. It was first documented in North America in 1924 (Counts, 1981) and was abundant in many catchments in eastern and western USA by 1957 (McMahon, 1983). C. fluminea has also been introduced into Europe, with reports of its presence in Portugal (Mouthon, 1981), France (Mouthon, 1981), the Netherlands (bij de Vaate and Greijdanus-Klaas, 1990), Germany (bij de Vaate, 1991), Spain (Araujo et al., 1993) and Britain (Aldridge and Muller, 2001). It was reported in the River Garonne in France in 1980-1981, in Germany’s River Weser in 1983, and the River Rhine in 1987. By 1991, it was common throughout the lower and middle Rhine system (Den Hartog et al., 1992). Aldridge and Muller (2001) give an account of the distribution and abundance of C. fluminea in Britain. The presence of C. fluminea in South America has also been documented (Ituarte, 1981; 1994).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Country||Distribution||Last Reported||Origin||First Reported||Invasive||References||Notes|
|Atlantic, Eastern Central||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Atlantic, Northeast||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Atlantic, Southeast||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Atlantic, Southwest||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Atlantic, Western Central||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Indian Ocean, Eastern||Present||Native||Invasive||Aguirre & Poss, 1999|
|Pacific, Northwest||Present||Native||Invasive||Chen, 1976|
|Pacific, Southeast||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|Pacific, Western Central||Present||Introduced||Invasive||Aguirre & Poss, 1999|
|China||Present||Native||Invasive||Aguirre & Poss, 1999|
|-Hong Kong||Present||Native||Invasive||Aguirre & Poss, 1999|
|Japan||Present||Native||Invasive||Aguirre & Poss, 1999|
|Korea, Republic of||Present||Native||Invasive||Aguirre & Poss, 1999|
|Philippines||Present||Native||Invasive||Aguirre & Poss, 1999|
|Taiwan||Present||Native||Invasive||Aguirre & Poss, 1999|
|Thailand||Present||Native||Invasive||Aguirre & Poss, 1999|
|-British Columbia||Present||Introduced||Invasive||Counts, 1981|
|-New Jersey||Present||Introduced||Invasive||Counts, 1986|
|-New Mexico||Present||Introduced||Invasive||Counts, 1986|
|-New York||Present||Introduced||Invasive||Counts, 1986|
|-North Carolina||Present||Introduced||Invasive||Counts, 1986|
|-South Carolina||Present||Introduced||Invasive||Counts, 1986|
|-South Dakota||Present||Introduced||Invasive||Counts, 1986|
|-West Virginia||Present||Introduced||Invasive||Counts, 1986|
CENTRAL AMERICA AND CARIBBEAN
|Panama||Present||Introduced||Invasive||Counts et al., 2003|
|Brazil||Present||Introduced||Invasive||Duarte & Diefenbach, 1994|
|-Rio Grande do Sul||Absent, unreliable record||Introduced||Invasive||Martins et al., 2006||Corbicula fluminea, Corbicula largillierti and C. aff. fluminalis in Guaiba Lake|
|Belgium||Present||Introduced||Invasive||Nguyen & Pauw, 2002|
|Czech Republic||Present||Introduced||Invasive||Beran, 2000|
|Germany||Present||Introduced||Invasive||Bij de Vaate, 1991|
|Netherlands||Present||Introduced||Invasive||Bij & de Vaate Greijdanus-Klaas, 1990|
|Portugal||Present||Introduced||Invasive||Mouthon, 1981; Nagel, 1989|
|Russian Federation||Present||Native||Invasive||Aguirre & Poss, 1999|
|Spain||Present||Introduced||Invasive||Araujo et al., 1993|
|UK||Present||Introduced||Invasive||Aldridge & Muller, 2001|
|Australia||Present||Introduced||Invasive||Britton & Morton, 1979|
History of Introduction and SpreadTop of page
In northern Serbia, C. fluminalis is present in the Danube River and in the Sava River. This species is considered rare in Serbia (Paunovic et al., 2007). There is no information about the time of introduction. However, Corbicula sp. were not found in previous investigations (Arambasic, 1994) and dense populations of C. fluminea were first recorded between 1980 and 1995 (Paunovic et al., 2007).
Introduction of C. fluminea in Lake Garda is reported to be due to stocking activities (Gherardi et al., 2008) and this particular lake has been invaded by others species, in past decades, suggesting the vulnerability of this ecosystem (Casellato et al., 2006; 2007; Ciutii and Cappelletti, 2009).
Risk of IntroductionTop of page
In Europe, inland waterways facilitate transfer of invasive alien species (Ketelaars, 2004; Galil and Minchin, 2006; Galil et al., 2007; Panov et al., 2007). High abundances of invasive species in Europe can easily transfer, in addition to natural spreading by anthropogenic pathways (Gherardi et al., 2008; Panov et al., 2009a).
The potential for species to expand their range has been enhanced due to increasing trade and the construction of canals. The waterways in Europe occur at low altitudes and presently the main European corridor routes consist of an interlinked network of 30 main canals with more than 100 branches, and more than 350 ports (Panov et al., 2007). In Europe a network of invasion corridors promote a wider and faster spread of invaders (Gallil et al., 2007; Panov et al., 2007).
Europe’s approved laws on improving water quality may facilitate invasion by providing better environmental conditions for all stages of live of the invader (Karatayev et al., 2007). For example, the reinvasion of zebra mussel in rivers (Bij de Vaate et al., 1992; Jantz and Neumann, 1992; Burlakova, 1998); and the improvement of Laurentian Great Lakes water has been correlated with the enhancement of successful invaders (Mills et al., 2003). The improved water quality could enhance Corbicula population at the early stages as C. fluminea are quite sensitive to pollution (Cataldo et al., 2001a; Karateyev et al., 2007).
Biology and EcologyTop of page
Recent investigations suggest a similar mode of reproduction in Corbicula fluminalis, C. fluminea, Corbicula leana and Corbicula australis (Morton, 1986; Araujo et al., 1993; Komaru et al., 1997; 2000; Byrne et al., 2000; Korniushin, 2004).
Larvae are D-shaped and weakly calcified, the hinge edge does not present irregularities and no structures are observed. C. fluminea release the clams at 250 µm and incubate their larvae for 100-125 h (King et al., 1986; Kennedy et al., 1991).
Corbicula sp. show a wide genetic variation related to polyploidy, or the processes of deletion, androgenesis and clonality, with mechanistically diverse genetic interactions amongst clones of Corbicula (Komaru et al., 1997; 1998; Komaru and Konishi, 1999; Qiu et al., 2001; Pfenninger et al., 2002; Lee et al., 2005; Hedtke et al., 2008).
Diploids of C. fluminea and C. papyracea have equal chromosomical set groups composed of 18 chromosomes and in a similar arrangement compared to C. fluminalis (Okamoto and Arimoto, 1986; Komaru and Konishi, 1999; Park et al., 2000; Qui et al., 2001; Lee et al., 2002).
In the Rhine River there exists evidence of cryptic hybridization between C. fluminea and C. fluminalis. The hybrid specimens were rare in abundance compared to the two major forms and they did not reach the adult stage (Pfenninger et al., 2002).
This genus exhibits a wide variety of reproductive strategies, involving sexually reproducing species with both sexes or hermaphrodites and several other unusual reproductive features, ranging from oviparity and ovoviviparity to euviviparity (Ituarte, 1994; Byrne et al., 2000; Glaubrecht et al., 2003; Korniushin and Glaubrecht, 2003).
Siripattrawan et al. (2000) suggested that all freshwater species in the genus Corbicula should be considered clonal lineages. However, this does not apply in European populations since here morphotypes assigned to C. fluminea are meiotic and capable of hybridization with C. fluminalis (Pfenninger et al., 2002). Correlation with spermatozoa morphology and reproductive mode was characterized in Corbicula by biflagellated sperm considered a marker for androgenesis, and presence of monoflagellated spermatozoa indicating sexual reproduction (Glaubrecht et al., 2003).
Fertilization occurs inside the paleal cavity and larvae are incubated in the gills. Larvae can be densely packed in the interlamellar space or irregularly distributed (Korniushin, 2004). Released larvae might be smaller in comparison with other species (e.g. C. fluminea and C. australis), which have been recorded at 250 mm (Kennedy et al., 1991; Byrne et al., 2000). In the Indonesian islands intramarsupial larvae can reach 350 mm (Glaubrecht et al., 2003). The smaller size is due to a slighter prodissoconch II, because prodissoconch I is quite similar to C. fluminea (mean value of 196.9 µm) (Kennedy et al., 1991; Korniushin, 2004).
In the genus Corbicula androgenesis has been reported, despite being rare in nature, because it could lead to species extinction in dioecious species (McKone and Halpern, 2003). Hedtke et al. (2008) reported that egg parasitism seems to be the mechanism that allows androgenesis in the Corbiculidae to avoid extinction.
Reproductive forms with androgenesis have been recorded in C. fluminalis (Korniushin, 2004) and in other three species: C. leana (Komaru et al., 1998), C. fluminea (Ishibashi et al., 2003) and C. australis (Byrne et al., 2000). Fecundation occurs and the oocyte ejects the entire maternal nuclear genome as two polar bodies (Komaru et al., 1998; 2000; Ishibashi et al., 2003). The descendents remain with the paternal genetic information, but retains the mitochondria. However, Hedtke et al. (2008), analyzing androgenic lineages in the American continent found mtDNA contamination corroborating earlier findings by Lee et al. (2005), and gives the egg parasitism process as the probable explanation for disruption in mtDNA lineages.
The presence of hermaphroditic specimens and biflagellate sperm present in Asiatic and African C. fluminalis populations, suggest the same reproduction strategy as found in C. fluminea, C. leana and C. australis (Morton, 1986; Araujo, 1993; Byrne et al., 2000; Komaru et al., 1997; 2000; Korniushin, 2004).
Physiology and Phenology
Morton (1986) reported that C. fluminea and C. fluminalis do not overlap in their distributions in any ecosystem. Yet mixed populations of the two species have been found in the Dutch, German and French parts of the River Rhine (Rajagopal et al., 2000; Nguyen and Pauw, 2002; Bernauer and Jansen, 2006), in the River Mosel (Bachman et al., 1997), the Serbian Danube (Paunovic et al., 2007) and lakes in Italy (Ciutti and Cappelletii, 2009).
In Europe, in terms of abundance the data are variable, examples given include in Italy where living specimens of C. fluminea and C. fluminalis have maximum densities of 19 individuals m-2 and 5 individuals m-2, respectively (Ciutti and Cappelletti, 2009). In Hungary C. fluminalis relative abundance is high with reported abundances of 36.5 individuals m-2 and C. fluminea has a high peak of 16.5 individuals m-2 (Bódis et al., 2008).
In the invaded range in Europe the sympatric populations of C. fluminea and C. fluminalis have been studied to explain this coexistence (Rajagopal et al., 2000; Mouthon and Parghentanian, 2004; Bódis et al., 2007).
In central France, in invaded canals, C. fluminalis has two reproductive periods, the first one in winter with a low number of larvae produced and the second extending from March to October, with a peak density in June and July (Mouthon and Parghentanian, 2004). In four cohorts, the life span is four years and with a maximum length of 24 mm in collected specimens. In the same ecosystem C. fluminea has one reproductive season from March to September/October, with two peaks in June and August, the presence of 5 cohorts, longevity from 2.5 to 3 years and with maximum specimens reaching 36 mm. The incubation and spawning periods seem to be triggered by unexpected falls in chlorophyll-a concentration) (Mouthon and Parghentanian, 2004). According to Rajagopal et al. (2000), C. fluminalis reveals a better tolerance to low temperatures than C. fluminea, its minimal temperature for reproduction being 6ºC.
Rajagopal et al. (2000) studied in detail the co-existance of C. fluminea and C. fluminalis in the Rhine River. The survival of both species was explained by differences in reproductive strategies and possible food preferences (Rajagopal et al., 2000). The reproductive season is in non-overlapping periods; the restraining temperature for reproduction of C. fluminea only allows two release peaks of pediveliger larvae in May/June and September, and the more resilient C. fluminalis release their gametes in October/November and in March/April. Both species have a second peak that is shorter and lower in percentage in spawning. The spawning of C. fluminea is positively correlated with chlorophyll-a content in the water column (Rajagopal et al., 2000). In contrast to C. fluminalis body mass increased from December to March, when chlorophyll-a concentrations were very low, indicating alternative food sources for this species other than algae (e.g. bacterioplankton, detritus). In terms of allocated energy for reproduction C. fluminea spends 51% in May and 21% in September, much more that C. fluminalis which spends 33% in October and 20% in March. Rajagopal et al. (2000) defines C. fluminalis as dioecious with a very low percentage of hermaphrodites and C. fluminea is hermaphrodite with an incubation larval strategy.
Another example is in cooling water channel of the Paks nuclear plant where C. fluminalis has one reproductive period identified in June. Meanwhile, C. fluminea has two reproductive periods: one in the winter and the second in June. Compared with the C. fluminea population situated upstream of Budapest a different reproductive strategy was identified with two well-defined reproductive periods that occurred in June and November. The presence of heated water delayed the reproductive period at Paks (Bódis et al., 2008).
This discontinuity in co-inhabiting of C. fluminea and C. fluminalis in the Flemish waters in Belgium seems to corroborate the conclusions made by Rajagopal et al. (2000) that beside reproductive strategy, spawning periods and food preferences, other environmental factors are also of importance for their co-existence (Nguyen and Pauw, 2002).
The most studied species is C. fluminea; therefore it can be used to illustrate some typical behaviours. Populations of C. fluminea lower their filtration rates in winter and many clams seem to be inactive through this time due to lower temperatures. Although filtration rates are inversely dependent on particle suspended concentration, Corbicula sp. have a filter-feeding plasticity and alternative feed modes that enhance their invasive success (Lauritsen, 1985; Way et al., 1990). Concerning water levels, when Corbicula is exposed to low water levels this situation inhibits long migration, and causes reductions in populations (White and White, 1977). Mass mortality events are described in severe low water periods associated with low temperatures in Lake Constance (Switzerland) (Werner and Rothhaupt, 2008). On the other hand, spring floods in the Ohio River cause high mortality to C. fluminea in all age classes, directly related to the magnify of suspended sediments in water column (Bickel, 1966).
Corbicula sp. ingest food to assure their growth and constitute the energy reserves required to develop embryos that feed from the secreting cells of the adult’s dermibranchiae (Britton and Morton, 1982). Corbiculidae are known to feed above the suspended particles (Foe and Knight, 1985; Lauritsen 1986a; Leff et al., 1990; Boltovskoy et al., 1995). However, individuals are also capable of pedal feeding using the cilia of the foot allowing them to collect organic material from the sediment (Way et al., 1990; Reid et al., 1992).
Hakenkamp and Palmer (1999) showed that the growth of Corbicula was optimal when both modes of nutrition, filter feeding and pedal feeding, were used.
The Corbiculidae are burrowing bivalves. Given the sympatric distribution of C. fluminea
and C. fluminalis
in Europe it is possible that the sediment preferences can be similar in both species (Csányi, 1999; Nguyen and Pauw, 2002; Mouthon and Parghentanian, 2004; Labêcka et al., 2005; Paunovic et al., 2007; Ciutti and Cappelleti, 2009).
For C. fluminea
, ideal sediments are sand mixed with silt and clay, while rocky and pure silt exclude this species especially if the concentration of oxygen is low (Leff et al., 1990; Karatayev et al., 2003). C. fluminea
inhabits by decreasing order of preference: fine sand, organically-enriched fine sand, coarse sand. However, C. fluminea
can inhabit a vast variety of substrata, from fine sand to gravel (Belanger et al., 1986).
Even though, there is no available data for pH limits for C. fluminalis or C. fluminea, mortality rates can be enhanced by lower pH values. Asiatic clams were reported to be dying over 3 year period due to pH lower than 5.6 in Mosquito Creek in Florida (Kat, 1982; Karatayev et al., 2007).
There are no data on C. fluminalis or C. fluminea concerning oxygen, calcium or upper and lower temperature limits (Karatayev et al., 2007). Nevertheless, in C. fluminea low dissolved oxygen inhibits growth (Belanger, 1991), and high temperatures cause massive mortalities and declines in body mass (Sousa et al., 2005; Vohmann et al., 2010). Lower temperatures prevent populations from reaching higher abundances (French and Schloesser, 1991) and/or restrict their colonization in the invasive range (Bates, 1987).
In a survey of the Minho River, Portugal, the major abiotic agents that influenced the distribution of C. fluminea were redox potential, nutrient concentration, water hardness, organic matter and sediment characteristics, explaining almost 60% of the total variation (Sousa et al., 2008a).
Natural Food SourcesTop of page
|Food Source||Life Stage||Contribution to Total Food Intake (%)||Details|
ClimateTop of page
|A - Tropical/Megathermal climate||Preferred||Average temp. of coolest month > 18°C, > 1500mm precipitation annually|
|C - Temperate/Mesothermal climate||Tolerated||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
Natural EnemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Acipenser||Predator||All Stages||McMahon, 1983|
|Ameiurus serracanthus||Predator||All Stages||McMahon, 1983|
|Aplodinotus grunniens||Predator||All Stages||McMahon, 1983|
|Cyprinus carpio||Predator||All Stages||McMahon, 1983|
|Ictalurus furcatus||Predator||All Stages||McMahon, 1983|
|Ictiobus bubalus||Predator||All Stages||McMahon, 1983|
|Ictiobus niger||Predator||All Stages||McMahon, 1983|
|Lepomis macrochirus||Predator||All Stages||McMahon, 1983|
|Lepomis microlophus||Predator||All Stages||McMahon, 1983|
|Minytrema melanops||Predator||All Stages||McMahon, 1983|
|Pimelodus maculatus||Predator||All Stages||Garcia & Protogino, 2005|
|Pterodoras granulosus||Predator||All Stages||Garcia & Protogino, 2005|
|Ricola macrops||Predator||All Stages||Garcia & Protogino, 2005|
Notes on Natural EnemiesTop of page
A review by Sickel (1986) lists 14 fish species, 13 duck species, raccoons, crayfish and flatworms are listed as natural predators. In a more recent survey in South America, García and Protogino (2005) recognize C. fluminea as a food source in eight fish species by clam’s presence in their guts.
Means of Movement and DispersalTop of page
Natural Dispersal (Non-Biotic)
Corbicula sp. juveniles will spread passively in the water column, both in lotic or lentic ecosystems (Prezant and Chalermwat, 1984). In rivers, colonization in the downstream direction is easily achieved for the juveniles since they will be transported by the current flow or by byssal attachment to floating vegetation (Prezant and Chalermwat, 1984). However, upstream movement is thought to be via secondary transportations by animals or man (Britton and Murphy, 1977; Rodgers et al., 1977; McMahon 1983). Another dispersal tactic in C. fluminea is the secretion of long mucous threads in smaller specimens and the exhalant siphons which act as a draglines to buoy the descendents into the water column (Prezant and Chalermwat, 1984).
Vector Transmission (Biotic)
The following propagation mechanisms have been observed in C. fluminea spreading on the American continent. One of the dispersal mechanisms reported in the drainage systems in Texas of C. fluminea was via migratory birds (Britton and Murphy, 1977). The pediveliger larvae and juveniles can be transported on the feet or feathers of aquatic birds, spreading Corbicula up and downstream of rivers (McMahon, 1982). Some reports seem to support dispersion via fish; however, this must be treated with caution, because it is questionable if Corbicula could survive the conditions inside fish guts (McMahon, 1982). Even so, in Brazil (Upper Paraná River) in the fish Pterodora granulosus a considerable amount of closed C. fluminea were found at the end of its intestine (Cantanhêde et al., 2007).
The expansion of mollusc species is closely related to anthropogenic activities. The internationalization of trade was responsible for the introduction of many species into different countries (Mills et al., 1993; Fofonoff et al., 2003; Ruiz and Carlton, 2003).
At a global level the common means of transportation applied to most aquatic species, are the ballast ship waters, which is the probable cause of C. fluminea introduction to the Rhine River (Gittenberger and Janssen, 1998; Bij de Vaate and Greijdanus-Klaas, 1990; Bij de Vaate, 1991; Karatayev et al., 2007). The Rhine-Meuse Delta in Rotterdam is the main continental port, and the largest port in Europe, accounting for 76.5% of the total trans-shipment in Dutch ports (Ministry of Transport, Public Works and Water Management, 2009).
In Europe, the introduction of C. fluminalis happened in two events: in the southwest, in the Danube River in that is considered as the major site for the invaders colonization (Galil et al., 2007; Panov et al., 2007), and in the north Europe in the Meuse and Rhine rivers delta and Wesser River (Bij de Vaate and Greijdanus-Klass, 1990; Haesloop, 1992).
Therefore, at local and national levels, the commercial or recreational activities and canals connectivity in rivers are responsible for a rapid upstream colonization, (Brancotte and Vincent, 2002; Panov et al., 2009a).
Corbicula sp. are not yet commercialized as bait in Europe as they are in the USA (Britton and Murphy, 1977; Sickel and Heyn, 1980; Brancotte and Vincent, 2002). In Europe (France), there are reports confirming the capture of C. fluminea to use as a decorative species in freshwater aquariums (Brancotte and Vincent, 2002). Tourist activities could be another potential vector of dispersal (McMahon, 1982). Accidental propagation of C. fluminea in USA occurs by transport with sand and gravel (Counts, 1986) and larval transportation in live minnow shipments (Britton and Murphy, 1977).
Karatayev et al. (2007) suggest that the rate of spread of the exotic species including C. fluminalis as well as others may be accelerated or slowed by various human activities.
One of the proposed mechanisms for Corbicula sp. invasion in the American continent was intentional introduction. Considering the vast cultivation in aquaculture of this item in Japan and Taiwan, it was assumed that Asian immigrants possibly brought some specimens as a known source of food (Britton and Morton, 1979; McMahon, 2000).
Pathway CausesTop of page
|Digestion/excretion||In the terminal part of the intestine of Pterodoras granulosus, C. fluminea clams are found intact||Yes||Cantanhêde et al., 2007|
|Pet/aquarium trade||C. fluminea reported as a decorative item for freshwater aquariums||Yes||Brancotte & Vincent, 2002|
Impact SummaryTop of page
Economic ImpactTop of page
In the USA, C. fluminea has caused millions of dollars worth of damage to intake pipes used in the power and water industries. Large numbers, both dead or alive, clog water intake pipes and the cost of removing them is estimated at about a billion US dollars each year (Anon., 2005). Juvenile C. fluminea get carried by water currents into condensers of electrical generating facilities where they attach themselves to the walls via byssus threads, growing and ultimately obstructing the flow of water. Several nuclear reactors have had to be closed down temporarily in the USA for the removal of Corbicula from the cooling systems (Isom, 1986). In Ohio and Tennessee where river beds are dredged for sand and gravel for use as aggregation material in cement, the high densities of C. fluminea have incorporated themselves in the cement, burrowing to the surface as the cement starts to set, weakening the structure (Sinclair and Isom, 1961). Isom (1986) has reviewed the invasion of C. fluminea of the Americas and the biofouling of its waters and industries.
In the United States Corbicula sp. is consider a pest species (Counts, 1981; Isom, 1986). In power plant facilities they can clog condenser tubes (Potter and Liden, 1986). In the United States alone, cost damages in a nuclear station by C. fluminea were estimated at US $2.2 billion annually in the early 1980s (OTA, 1993). In the Delta-Mendota Canal, with a deficient design, the accumulation of sediment and Corbicula clams reduced the canal capacity (Arthur and Cederquist, 1976). In South America fouling problems were only recorded in power plants in Brazil in 2000 (Zampatti and Darrigan, 2001). In Russia there are reports of biofouling problems in reservoirs by Corbicula sp. in numerous locations: southern Primorye, Sakhalin and Khabarovsk (Yanov and Rakov, 2002). Control methods in the power plant industry are reviewed by Post et al. (2006).
European populations of Asian clams have not until now caused any major economic impact in industrial facilities (Swinnen et al., 1998; Paunovic et al., 2007). However, measures need to be taken before situations arise. Bachmann et al. (1997) on the Mosel River, states “the structure and the dynamics of these populations must now be carefully observed, in order to prevent possible economic and ecosystem damages” and Strauss (1982) refers to a French design system that manages to exclude fouling bivalves from cooling units.
Environmental ImpactTop of page
C. fluminea is a known biofouler in power plant and industrial water systems; it has also caused problems in irrigation canals and pipes. It also has a major impact on aquatic ecosystems.
Impact on Habitats
The effects of C. fluminalis on the ecosystem are expected to be similar to C. fluminea due to their physiological and ecological resemblance (Karatayev et al., 2007).
C. fluminea has one of the highest filtration rates per biomass, compared to sphaeriids and unionids (McMahon, 1991). Consequentially one of the major impacts will be on reduction of planktonic communities (Cohen et al., 1984; Lauritsen, 1986b; Leff et al., 1990).
Impact on Biodiversity
García and Protogino (2005) show that C. fluminea is a source of food to fishes, than might induce accumulation in higher trophic levels of accumulated heavy metals. C. fluminalis can effectively bioaccumulate heavy metals such as Zn, Cu, Hg or Cd (Pourang, 1996). However a clear relationship between feeding habits and bioaccumulation of Cd, Cu and Zn it is not clearly confirmed (Villar et al., 2001).
The high resistance of C. fluminea to toxic substances compared to other species can enhance their probability to exclude endemic taxa in polluted disturbed ecosystems (Burress et al., 1976).
Empty shells after animal dies persist in the benthos providing a suitable habitat for other species especially on soft bottoms (Gutiérrez et al., 2003). The most recent studies on positive effects on ecosystems by Corbicula sp. relies on ecosystem engineer pathways; Lake Constance, Switzerland (Werner and Rothhaupt, 2007) is one example. In Lake Constance recent C. fluminea colonization enhanced the proliferation of typical hard-substrate species on a soft-benthic surface (e.g. Caenis sp. enhanced their density) (Werner and Rothhaupt, 2007).
In the Minho River C. fluminea was first registered in 1989, and nowadays dominates the benthic biomass with about 98% of total biomass in the freshwater tidal estuarine area (Sousa et al., 2008d).
Isom (1971) reported that the loss of mussel native diversity was due to impoundment and overharvesting or by fish-host association; however, it is mentioned that a new pest (Corbicula sp.) is a most successful taxa in the Tennessee River, is consider by many authors as responsible for unionids decline(Parmalee, 1945; Cummings and Mayer, 1992; Williams et al., 1993). The invasion of Europe can put unionids species at risk (Reis, 2003; Geist and Kuehn, 2005).
Vaughn and Spooner (2006), in a scale-dependant survey, reveal that cushions of unionid mussels exclude Corbicula sp. from their patches. However, Corbicula in a prior study by Clarke (1986) is capable of competitive exclusion of Canthyria (Unionidae). Assuming the taxonomic and functional similarities, the addiction of a Corbicula specimen into a mussel community might represent as much difference as an introduction of unionid species (Vaughn and Spooner, 2006).
Nonetheless, Corbicula preferentially invades sites where native mussel communities are already in decline by anthropogenic ecosystem disturbances (Strayer, 1999) and their impact on native mussels is much weaker than zebra mussels Dreissena polymorpha (Strayer, 1999). Perhaps Corbicula cannot dominate indigenous bivalves in nearly or quite natural habitats (Fuller and Imlay, 1976).
Considering the interactions between native larvae mussels and Corbicula, the situation is quite different from interactions between adult stages. The survival of larvae stages can be indeed affected by Corbicula sp. through direct food competition, sediment disturbance and displacing species downstream (Strayer, 1999; Yeager et al., 2000).
Another situation to take into consideration involves the die-off of C. fluminea in warmer water events. Clam die-offs clearly have the potential to cause death in juveniles stages of some species of unionid mussels. The decomposition of clam die-off ammonia concentration exceeds the acute levels of LC50. The DO reduction associated with clam’s die-offs might pose a risk to unionids (Cherry et al., 2005; Cooper et al., 2005).
Impact: BiodiversityTop of page
C. fluminea is known to alter benthic substrata and competes with native species of bivalves for food and space. It is also able to tolerate polluted environments better than native species of bivalves. Several studies have shown that the filter feeding of C. fluminea had resulted in a significant removal of suspended matter from the water column; Cohen et al. (1984) reported a large decrease in phytoplankton in the Potomac River which was attributed to Corbicula. A decrease in seston in streams with high populations of Corbicula has also been reported (Leff et al., 1990). These declines in particulate matter have important repercussions for the rest of the biota. Corbicula is also known to increase the rate of sedimentation which would require more frequent dredging to maintain water flow; this would not only be expensive and but also have serious effects on the river ecosystem. Although there is as yet no evidence that C. fluminea is directly responsible for declines in populations of threatened native species in the USA and Britain there is some concern that they could lead to such declines by outcompeting them for space and food (Aldridge and Muller, 2001).
Social ImpactTop of page
The major concern in terms of social impact is Corbicula as a possible vector of diseases. The high abundances of Corbiculidae family and the vast and wide range of organisms that use bivalves as a final or secondary host are indeed responsible for health problems in its native range in humans and animals (Sousa et al., 2008b).
Echinostoma sp. is the most referenced parasite within Corbicula sp. detected for the first time by Bonne (1941) in Corbicula rivalis ‘Busch’ Philiphi, 1850. Echinostomiasis is spread over South-East Asia and the Far East (mainland China, Taiwan, India, Korea, Malaysia, Philippines, and Indonesia) (Huffman and Fried, 1990). Corbicula is one of the hosts and some parasite forms cause severe diseases in man, and are still a public health problem in endemic areas. Pathway transmission is by eating clams raw or barely cooked (Carney et al., 1980). A case study in Lake Lindu in Sulawesi showed had a high rate of infection in some parts of the valley reaching 96% with Echinostroma lindonensis (=E. echinatum). The situation changed when Tilapia mossambicus was introduced into Lake Lindu and began feeding on the veliger stage of Corbicula clams leading this species almost to extinction. Therefore, the rates of infection decreased in Sulawesi and now echinostomiasis is reported as an historical disease (Kusharyono and Sukartinah, 1991). The prevalence of infection ranges from 44% in the Philippines to 5% in mainland China, and from 50% in northern Thailand to 9% in Korea. This also represents a social and economic problem in the affected countries, since it is prevalent in remote rural places among low-wage earners and in women of child-bearing age, and is aggrevated by social economical factors (Graczyk and Fried, 1998).
There exists a wide variety of parasites in the Corbiculidae and their success as disease vectors is enhanced by Corbicula sp. abundance and distribution (Darrigran, 2002; Sousa et al., 2008b).
UsesTop of page
In Asia, the use of Corbicula and their applications in the regional and national economy are diverse. Intensive aquaculture relies on this bivalve which has great economic importance on DianSan Lake in Shangai (Xu et al., 1988), and in Vietnam, where the production of Corbicula subsulcata reaches 600-1,000 t/yr (Phung, 2000). In the Pearl River, China, Corbicula sp. are used for food and the manufacture of lime from the shells (Miller and McClure, 1931). In Taiwan, it is not considered a high-value aquaculture product and it is consumed mostly as a side dish and in soups. In 1987, it had the fourth highest total shellfish market quantity, around 8000 mt produced at 3.7 mt/ha (Phelps, 1994b). Harvesting activities are reported in Luzon in Laguna Bay, Philippines, and in Sulawesi in Lake Lindu Corbicula sp. are harvested for human food (Arriola and Villaluz, 1939; Bonne and Sandground, 1939).
Corbicula sp. are considered a healthy food and have the highest glycogen content (50%) of any shellfish (Phelps, 1994b). They are also considered of high medicinal importance, e.g. C. leana in Japan (Ikematsu and Kammakura, 1975). The health and medicinal importance might rely on the caloric content estimated at 5.02 Kcal/g in dry weight (Sickel, 1976). They also contain appreciable amounts of vitamin B12 (Halarnkar et al., 1987). Iritani et al. (1979) showed that rats fed with C. japonica significantly reduced their high cholesterol levels, this is explained by the several sterols present in the clam, making them a hypolipidemic food item (Iritani et al., 1979).However, in Japan, water extracts from C. japonica were shown to be lethal to mice via injection. The toxicity exhibits a regional variation independent from seasonality or sexual periods. In addition, both Corbicula sandai and C. leana have the same toxin but less potent (Arita et al., 2001).
In Tennessee, Corbicula was produced commercially for fish bait (Williams, 1969; Sickel and Heyn, 1980); in Sacramento, California, in 1974, 553,889 lbs of bait clams (C. fluminea) were sold for US $83,689 (McAllister, 1976).
The aquaculture potential of C. fluminea in invaded places was analyzed by Phelps (1994b). This clam has never been marketed for food in the US, except canned or smoked, with the canned form mostly commercialized to the Oriental market. Even so, Asians were found harvesting for the Asiatic clam in the Potomac River, above Washington, DC and selling it in large quantities in New York, because they prefer to consume this item fresh (Phelps, 1994b).
C. fluminea has importance in polyculture; it may promote superior water quality in catfish-rearing ponds (Buttner, 1981). Corbicula is not affected by the presence of catfish (Ictalurus punctatus) and is of importance as a biofilter if water temperature does not exceed 30ºC (Buttner, 1986).
There are few reports of pearls in Corbicula and their commercialization. Takahashi (1986) reports pearls found in C. leana. There also exists a study by Horiguchi and Tsujii (1967) for enhancement of black pearl culture using C. sandai and C. japonica, the authors established a relationship between pearl colour and gamma ray irradiation and manganese. The potential of the freshwater clams (C. fluminea) for the artificial production of pearls, with special emphasis on techniques of pearl seed implantation was analyzed by Kropf-Gomez (1993).
In Laguna de Luzon (Philippines), Corbicula sp. is gathered in huge quantities approaching a commercial scale. This item is used to feed domestic ducks (Anas platyrhynchos), and is also a food item for the habitants, especially the working classes (Villadolid and Del Rosario, 1930). These authors also suggest measurements of conservation of this economically-important species. Corbicula sp. is harvested in other places like Lake Lindu in Indonesia (Carney et al., 1980), Japan (Cahn, 1951), and in the USA in Potomac River above Washington, DC (Phelps, 1994b).
Asiatic clams can act as bioindicators of viruses; there has been documented absorption of 99.94% of viruses by clams (Payne, 1985). Faust et al. (2009) documented the absorption of bird flu virus from infected waters, thus potentially reducing the infectivity. Some benefits in public human health can be reported as Corbicula can be used as a functional bioindicator of Giardia and Cryptosporidium in infected waste and in irrigation waters (Graczyk et al., 1997; 2003; Miller et al., 2005).
Individuals of Corbicula have been recommended for the biological assessment of water quality (Kerans and Karr, 1994; Carlisle and Clements, 1999). C. fluminea’sworldwide distribution, high abundances and spatial distribution in lotic and lenthic ecosystems in polluted and pristine environments, makes possible to confer this bivalve with an interesting ecotoxicological feature, and could allow a worldwide comparison (Sousa et al., 2008b,c). The combination of quite easy maintenance in laboratory conditions, possible transplanted field experiments, dissection and separation of different organs, and also its ability to bioaccumulate and bioamplify several contaminants make C. fluminea a very convenient model in ecotoxicology (Way et al., 1990; Bassack et al., 1997; Baudrimont et al., 1997a,b; Inza et al., 1997; Narbonne et al., 1999; Tran et al., 2001; Cataldo et al., 2001a,b; Achard et al., 2004; Sousa et al., 2008b).
Pourang (1996) reports using C. fluminalis, among others macrozoobenthonic taxa, in the assessment of concentrations of heavy metal (Mn, Zn, Cu, Pb) in superficial sediments in the Anzali wetlands (Iran). C. fluminalis showed lower heavy metals concentrations compared to the other taxa studied.
Uses ListTop of page
Animal feed, fodder, forage
- Fodder/animal feed
Human food and beverage
- Cured meat
- Fresh meat
- Live product for human consumption
Similarities to Other Species/ConditionsTop of page
Since there are sympatric populations of C. fluminalis and C. fluminea in Europe (Swinnen et al., 1998; Csányi, 1999; Pfenninger et al., 2002; Paunovic et al., 2007; Ciutti and Cappelletti, 2009), these may have the same habitat requirements (Karatayev et al., 2007). Additionally, in recent surveys both species appear to have similar reproduction pathways (Korniushin, 2004).
The principal feature to differentiate the morphotypes are the shell characteristics. C. fluminalis has a smaller size (around 25 mm), with a triangular, rounded base form and thicker shell than C. fluminea; has concentric ridges that are thinner and less spaced, with 13-16 per cm (Zhadin, 1952; Korniushin, 2004).
As an example, in Italy, Lake Garda, the two species of Corbicula sp. were clearly distinguishable from patterns of shell sculpture, shape and colour. C. fluminalis shells shows finer ridges and a violet inner surface, whereas C. fluminea has coarser ridges with pale inner surface (Ciutti and Cappelletti, 2009).
Prevention and ControlTop of page
The first steps on slowing or stopping the spread of invasive species is for international cooperation in acceptance of measurements discussed and approved in IMO Conventions on hull fouling and ballast waters and ICES Code of Practice (Karatayev et al., 2007). Corbicula sp. invades disturbed habitats more often then unmodified ones. The maintenance and restoration of natural conditions may be one of the best defences against benthos domination by exotic mussels (Stein and Imlay, 1976). Management programs, mitigation measures and eradication efforts on invasive species do only make sense when being undertaken by all affected countries (Gollasch, 2007).
There exists a report of C. fluminea (identified as C. manilensis) being sold in open markets in Hawaii (Kailua, Oahu Island). With the potential threat of invasion, the Department of Agriculture Plant Quarantine Office has twice confiscated shipments of C. manilensis (Burch, 1978). No similar reports exist for C. fluminalis.
Early warning systems
In addition to the ALARM project a new electronic journal was created “Aquatic Invasions” as an important part of the developing European early warning systems on invasive species in Europe (Panov et al., 2009b).
Education of public can indeed reduce the spread of an invasive species (Karatayev et al., 2007). In order to minimize human mediated transport, measures should be taken such as the education of the fishermen in not using Corbicula as bait outside invaded places (Aldridge and Muller, 2001). Caution should be taken in not transferring sand or gravel from invaded locals (Counts, 1986); stocking activities and transport of these clams outside invaded range (Karatayev et al., 2007).
Elimination of an entire invasive population is rarely attempted (Simberloff, 2002); it is very expensive and may have detrimental non-target effects. However, Aldridge et al. (2006) proposed an effective and selective processes to kill invaders, focussing on zebra mussels, the biobullets. This new technique may provides us with a useful method to eradicate invasive mussels by releasing less chemicals to the environment, reducing anthropogenic ecosystem disturbances and protecting the native species from being killed in extermination process (Aldridge et al., 2006).
In spite of mass mortality of C. fluminea in Lake Constance by low-water events associated with low temperatures, Werner and Rothhaupt (2008) suggest that similar natural events can control population and in regulated reservoirs a quick water level decrease could be use to regulate invader molluscs.
After invasion the best measure is to reduce the spreading (Aldridge and Muller, 2001). This includes the washing-down of boats use on invaded locales and the barges used on transporting sediment. Equipment like hand dredges and nets should be cleaned with appropriate effective methods like hot water (above 50ºC), and chlorinated water (Thompson and Sparks, 1977; Aldridge and Muller, 2001).
No species-specific techniques are available for the eradication of Corbicula sp. However, some population density controls are proposed by Covich et al. (1981) using crayfish, and by Robinson and Welborn (1988) using benthic-foraging fish that control formation of dense patches.
Gaps in Knowledge/Research NeedsTop of page
In addition to the studies of Hedtke et al. (2008) it is suggested there should be a worldwide database for multiple androgenic lineages of Corbicula. Also it is recommended to create a phylogeny of Corbicula using single copy genes because of unexpected polyphyly in androgenic lineages. The rRNA genes are suggested by Hedtke et al. (2008) due to their conservative characteristics within the eukaryotes.
ReferencesTop of page
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Uma Sabapathy Allen
Human Sciences, CAB International, Wallingford, Oxon, OX10 8DE, UK
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- = Present, no further details
- = Evidence of pathogen
- = Widespread
- = Last reported
- = Localised
- = Presence unconfirmed
- = Confined and subject to quarantine
- = See regional map for distribution within the country
- = Occasional or few reports