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Corbicula fluminalis

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Corbicula fluminalis

Summary

  • Last modified
  • 04 October 2022
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Corbicula fluminalis
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Mollusca
  •       Class: Bivalvia
  •         Subclass: Heterodonta
  • Summary of Invasiveness
  • C. fluminalis is an inland water, filter-feeding bivalve native to Asia and Africa that is an invasive species in Europe. It was recorded for the first time in Germany in 1984 (Weser River). However, for a second location, in the Danube,...

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Identity

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Preferred Scientific Name

  • Corbicula fluminalis (Müller, 1774)

Other Scientific Names

  • Tellina fluminalis Müller, 1774

Local Common Names

  • Netherlands: toegeknepen korfmossel

Summary of Invasiveness

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C. fluminalis is an inland water, filter-feeding bivalve native to Asia and Africa that is an invasive species in Europe. It was recorded for the first time in Germany in 1984 (Weser River). However, for a second location, in the Danube, the year for invasion is estimated at 1980. It is widespread in the Rhine, Mosel and Weser rivers, and is therefore present in Germany, the Netherlands, France, Luxembourg and Belgium. In Poland it has invaded the lower basin of the Odder River. Along the Danube, in Ukraine, northern Serbia and Hungary there have been reports of populations of C. fluminalis. It is also present in the northeast lakes of Italy. It is considered invasive by Panov et al. (2009b) due to its high risk of establishment, dispersal and negative ecological and socioeconomic impacts. This species is an economic pest for the gravel industry (IUCN, 2013) although damage to industrial facilities has not been reported in Europe. Despite the fact that in the native range of Corbicula sp. human populations benefit from them (e.g. as a food resource for humans or other animals, and using shell products), in the introduced range it is so far only used as bait in sport fisheries and has no significant social importance or economic benefit.

 

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Mollusca
  •             Class: Bivalvia
  •                 Subclass: Heterodonta
  •                     Order: Veneroida
  •                         Unknown: Corbiculoidea
  •                             Family: Corbiculidae
  •                                 Genus: Corbicula
  •                                     Species: Corbicula fluminalis

Notes on Taxonomy and Nomenclature

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Müller (1774) first identified Corbicula fluminalis, as Tellina fluminalis from “In fluvio Asie Euphrat”.

By 1971 over 100 living species were distinguished in the Corbiculidae family. However, this distinction was based on phenotypical traits. Nowadays, the establishment of new species based only on observed anatomical differences is considered irrational (Boss, 1971; Morton, 1979). Still, the confusion in the Corbiculidae is exacerbated by the numerous ecomorphs reported over its native range (Djajasasmita, 1977; Kijviriya, et al., 1991; Daget, 1998).

Jickeli, in 1874, synonymized Corbicula consobrina Cailliaud, Corbicula cor Lamarck, Corbicula saulcii Bourguignat, and Corbicula crassula `Mousson' Bellardi with C. fluminalis for North African distribution. Prime (1895) in an overview of the Corbiculidae identified C. fluminalis Deshayes, within the Syrian type. Therefore, further synonyms were given: Corbicula saulcyi Bourguignat and Corbicula purpurea Prime from the Tigris; Corbicula difficilis Prime from Egypt; Corbicula radiata Deshayes from the Upper Nile; Corbicula rivalis Deshayes; Corbicula purpurea Prime from Antioch and Corbicula delessertiana Prime from the Pyramids.

 

In the attempt to end ecomorphotype confusion in the Asia range, Morton (1986) recognized 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).

 

Daget (1998) reviewed the freshwater bivalve distribution of Africa and Corbicula ecomorphs were placed within three species: C. fluminalis, C. africana and C. astartina. C. fluminalis is further divided in four subspecies: C. fluminalis consobrina (Cailliaud, 1827) for the Nile Basin and West Africa; C. fluminalis cunningthon Smith 1906 for Lakes Victoria, Edward and Albert; C. fluminalis tanganyicensis (Crosse, 1881) for Lake Tanganyica; C. fluminalis africana (Kraus, 1848) for East and South Africa, from Lake Malawi (Nyassa) to the Cape Province (Daget, 1998 (in Korniushin, 2004)). However, Daget's (1998) distribution is not absolutely reliable since it is stated in the introduction that the objective is not a systematic family revision, but to elaborate a catalogue and indicate the references. The author even states that this work should not perjure any conclusion of future taxonomist’s surveys that rely on genetics tools (Daget, 1998).

 

Korniushin’s (2004) review of C. fluminalis was based on several morphological characteristics and places the C. fluminalis range in Central Asia, the Caucasus, Middle East and North Africa. Other, Corbicula species should be treated as synonyms if they show the same phenotypical characters presented in Korniushin’s description and if present inside the given range. The native distribution of Korniushin is based on biflagellate sperm, hermaphroditic and facultative incubation of larvae on gills. In his review Korniushin confirms C. africana as a different species for South Africa and Lake Malawi (Nyassa). Korniushin (2004) even suggests a genetic revision for all the Corbicula species within Great African Lakes.

 

Description

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Korniushin (2004) reviewed the morphological characteristics and reproduction pathways of C. fluminalis in its native range based essentially on a wide range of morphological traits, in specimens from West and Central Asia; North Africa; the African Great Lakes; South Africa and Canton in China (including C. purpurea from Russia). The morphological traits are phenotypically variable with extensive differences in shell morphology and size, coloration of inner and outer shells and number of ribs (Korniushin, 2004).
 
The lectotype of C. fluminalis in the Museum of Copenhagen measures 29.9 mm and 29.7 mm in length and height, respectively (Korniushin, 2004). In a Berlin museum another lectotype measures 20.6 mm and 19.2 mm, in length and height respectively (in Skuza et al., 2009).
 
In Africa, C. fluminalis from Lake Edward is smaller at 13 mm in length and 10.9 mm in height and others report C. fluminalis consobrina as 30.5 mm (length) and 26.5 mm (height) from Ismalia, Egypt and for Asian C. fluminalis from Azerbaijan as 22.4 mm (length) and 22.2 mm (height) (Korniushin, 2004). In Europe, in Lake Garda in Italy, specimens of 13.57 mm (length) and 15.79 mm (height) are found (Ciutti and Cappelletti, 2009). From Hungary, at the Paks nuclear power plant, specimens are found of 23.72 mm (height) and 23.61 mm (length) (Bódis et al., 2008).
 
The simple measurements of shell dimensions do not give accurate information (Korniushin, 2004) and only confirm phenotypical plasticity (e.g. Cataldo and Boltovskoy, 1999).
 
Korniushin’s (2004) review mentions rather pronounced, sharp, narrow and regularly spaced ribbed (13-16 per cm) shells, with similar coloration (e.g. a dark periostracum, outer side yellow or light brown and inner side light purple). The umbo of larger specimens is reallocated posteriorly, making the shells markedly asymmetric (Korniushin, 2004). Anatomical soft tissue characters include narrow siphons with circular apertures; siphonal papillae rather scarce, about 40 around inhalant siphons (one or two rows) and 12-20 around exhalant siphons (one incomplete row); a ring of dark pigment is usually present internally at base of each siphon; papillae of fused mantle lobes and numerous free mantle edges, the first organized into one or two rows; radial muscles of mantle edge well developed and arranged in bands (Korniushin, 2004).
 
Corbiculidae eggs are large (80-125 mm) in comparison to other bivalve eggs (e.g. Sphaeridae) (Morton, 1982; Kramer and Galloway, 1986; Byrne et al., 2000) and rich in yolk for embryonic development (Kraemer and Galloway, 1986).
 
Larvae are D-shaped and weakly calcified, the hinge edge does not present irregularities and no structures are observed. No accurate measurements are given on C. fluminalis due to non-existent data on reproductive incubation under natural conditions (Korniushin, 2004). Biflagellate spermatozoa measurements significantly distinguished populations from Africa and Asia. Differences in shell measurements and spermatozoa morphology suggest different clonal lineages over the distribution range (Korniushin, 2004).

Distribution

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C. fluminalis is thought to be native to northwest Africa and Oriental Africa, the Middle East and Central Asia (Korniushin, 2004).

Accurate distributions are difficult to achieve, since most of the records are old and rely only on phenotypical traits and are sometimes impossible to trace to a location. For example, a report of C. fluminalis in the Yalaminskikh River (Denahena, 1947) is probably is in Azerbaijan and Lake Abbeje in northeast Africa (Haas, 1932). However, no certain statement can be made.
 
Korniushin reviews sets of C. cf. fluminalis from southeast China as closer to Corbicula japonica and genetic data based on COI sequences confirms this situation (Park and Kim, 2003; Sousa et al., 2007a; Hedtke et al., 2008). This taxon is re-reconsidered as Corbicula cf. japonica (Prime) (Korniushin, 2004). Records of C. fluminalis from southwest China, in the Pearl River and Yangtze River estuaries (Morton, 1982; Park and Kim, 2003, respectively), also require confirmation.
 
In Central Asia, Izzatullaev (1980) distinguished C. fluminalis and other species, namely C. purpurea (which has been proposed as a synonym for C. fluminalis by Korniushin (2004)) and Corbiculina tibetensis (Prashad, 1929) and Corbiculina ferghanensis (Kursalova and Starobogatov, 1971), which Korniushin (2004) considered them very similar in their shell morphology to C. purpurea. However, these species have not been considered as synonyms in this review due to scarcity of anatomical and genetic information.
 
Previous studies done by Zhadin (1952) and Kasymov (1972) basically agree with distribution records in northern Iran, Afghanistan, Mesopotamia, Syria, Baluchistan, Kashmir, India, Transcaucasia, and Middle Asia. Morton (1979) assumed a Middle Asian but not Far Asian distribution.

Distribution Table

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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.

Last updated: 17 Dec 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

BurundiPresentNativeC. fluminalis tanganyicensis in Lake Tanganyica
CameroonAbsent, Unconfirmed presence record(s)Possible in Chad Lake as Daget (1998) considers Corbicula tsadiana a morphotype of Corbicula consobrina; Mandahl-Barth (1988) set as a race of C. fluminalis
ChadAbsent, Unconfirmed presence record(s)Possible in Lake Chad as Daget (1998) considers C. tsadiana a morphotype of C. consobrina; Mandahl-Barth (1988) set as a race of C. fluminalis
Congo, Democratic Republic of thePresentNative
EgyptPresentNative
EthiopiaPresent, LocalizedNativeC. fluminalis is reported from lakes and shores of the lower Huash River and the Lake Tana (Tsana), Abyssinia (Norther Ethiopea). Near Bahr-el-Asrak, Blue Nile
GabonAbsent, Unconfirmed presence record(s)Corbicula gabonensis ( = C. fluminalis)
KenyaAbsent, Unconfirmed presence record(s)C. fluminalis cunningtoni recorded in Lake Victoria
MalawiAbsent, Invalid presence record(s)C. fluminalis africana in Lake Malawi or Nyassa
MozambiqueAbsent, Invalid presence record(s)Lake Malawi or Nyassa. C. fluminalis africana
NigerPresentNativePossible in Lake Chad as Daget (1998) considers C tsadiana a morphotype as C. consobrina; Mandahl-Barth (1988) set as a race of C. fluminalis
NigeriaPresentNativePossible in Lake Chad as Daget (1998) considers C. tsadiana a morphotype as C. consobrina; Mandahl-Barth (1988) set as a race of C. fluminalis
SenegalAbsent, Unconfirmed presence record(s)Presence of C. fluminalis consorbina (identified as Corbicula meridionalis and Corbicula senegalensis)
South AfricaAbsent, Invalid presence record(s)By morphological characters Kornuishin sets Corbicula africana as a valid taxa present in Gauritz River, Natal; Transvaal in Oliphant River, Lepenula River
SudanPresentNative
TanzaniaPresentNative
UgandaPresentNativeC. fluminalis cunningthon, Lake Victoria. Edward and Lake Mobotu, Sese Seko (Lake Albert)
ZambiaPresent, LocalizedNativeC. fluminalis tanganyicensis, Lake Tanganyica

Asia

AfghanistanPresentNative
ArmeniaAbsent, Unconfirmed presence record(s)Transcaucasia
AzerbaijanPresentNative
China
-GuangdongAbsent, Unconfirmed presence record(s)Corbicula cf. fluminalis from the Pearl River
-ShanghaiAbsent, Unconfirmed presence record(s)Specimens of C. fluminalis collected in estuary of Yangze River
GeorgiaAbsent, Unconfirmed presence record(s)C. fluminalis reported from Transcaucasia
IndiaPresentPresent based on regional distribution.
-Jammu and KashmirPresentNativeC. fluminalis reported in Kashmir
IranPresentNative
IraqPresent, LocalizedNative
IsraelPresentNative
JordanPresentNative
KazakhstanPresent, LocalizedNativeC. fluminalis in the mouth of the Amu-Darya River, Aral Sea
PakistanPresentNative
Saudi ArabiaPresentNativeIn article by Al-Safidi, 1990, it is referred to as Corbicola fluminalis
SyriaPresentNative
TurkeyPresentNative
TurkmenistanPresentNativeC. fluminalis is reported in Turkemia in the valley of the Murgab River
UzbekistanPresentNative

Europe

BelgiumPresent, LocalizedIntroducedInvasiveFirst time recorded in 1992
FrancePresent, WidespreadIntroducedInvasive
GermanyPresent, LocalizedIntroducedInvasive
HungaryPresent, LocalizedIntroducedInvasiveFirst record Ven-Duna at Baja in June-Danube River
ItalyPresent, LocalizedIntroducedInvasive
LuxembourgPresentIntroducedInvasiveFound in River Mosel during a benthos survey between 1994-1996
NetherlandsPresentIntroducedFirst recorded in Meuse and Rhine Delta
PolandPresent, LocalizedIntroduced2004InvasiveIn lower part of Odder River
PortugalAbsent, Invalid presence record(s)C. fluminea was identified as C. fluminalis by mistake (Morton, 1996)
RomaniaPresent, Few occurrencesIntroducedInvasiveRecord of one population on border with Serbia in Danube River
RussiaPresentPresent based on regional distribution.
-Central RussiaPresentNativeDistribution in Central Asia as C. fluminalis
-Eastern SiberiaPresentNativeC. fluminalis extrema is described in Southeast Siberia
-Southern RussiaPresentNativeC. fluminalis is reported as distributed through the Caucasus and Central Asia
-Western SiberiaPresentNativeC. fluminalis, this species is found in Siberian rivers, including Irtysh River
SerbiaPresent, LocalizedIntroducedInvasivePresent in Danube River and Sava River
SwitzerlandAbsent, Unconfirmed presence record(s)1997Classification of C. fluminalis only by differences in shells
UkrainePresentIntroducedInvasiveIntroduced in Danube River Basin in early 1980s
United KingdomPresentIntroduced1997

North America

United StatesAbsent, Invalid presence record(s)Until now no specimens of C. fluminalis were recorded in the USA

South America

Brazil
-Rio Grande do SulAbsent, Unconfirmed presence record(s)Corbicula fluminea, Corbicula largillierti and C. aff. fluminalis in Guaiba Lake

History of Introduction and Spread

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The invasive range of C. fluminalis is, for now, restricted to European countries (Bij de Vaate and Greijdanus-Klass, 1990; Haesloop, 1992; Voloshkevich and Son, 2002). In the Weser Estuary (Germany), C. fluminalis was first detected in 1984. By this time the population had extended for 30 km and already had colonized connected harbours, a tributary river and the vicinity of an industrial plant (Haesloop, 1992).

A C. fluminalis population in the Netherlands was first reported in the lower basin of Rhine River by Bij de Vaate and Greijdanus-Klass (1990). However, the presence of two forms or species in the Rhine has been reported since 1987 (Kinzelbach, 1991; Den Hargot et al., 1992). The possible cause of introduction was ballast waters (Gittenberger and Janssen, 1998).
 
In 1992, by invading the River Meuse, a tributary of the Rhine, C. fluminalis expanded its range to Belgium, reaching the far west and south, at Viersel (Canal Bocholt-Herentals) and Tihange (River Meuse), respectively (Swinnen et al., 1998). In a survey carried out from 1999 to 2000, C. fluminalis was found in only three canals (Albert, Bocholt-Herentals, and Zuid-Willemsvaart) (Nguyen and Pauw, 2002).
 
The expansion in the River Rhine was more extensive, with C. fluminalis entering Germany from the Netherlands, with a first invasion estimated in 1991 (Bernauer and Jansen, 2006). The species spread along the French and German borders (Rajagopal et al., 2000; Pfenninger et al., 2002). The furthest upstream point of invasion relies on a record from Switzerland, by Wittenberg (2006).
 
C. fluminalis spread into the lower Mosel River in Germany and reached France, where the population was discovered in a benthos survey and already had a range of 337 km (Bachmann et al., 1997). Colonization through the Mosel River reached the Luxembourg border (Bachmann and Usseglio-Polatera. 1999). In the interior of France, C. fluminalis is found in the River Mosel (Bachmann and Usseglio-Polatera, 1999; Renard, 2000), and in the tributary of the Meurthe River (Piscart et al., 2005). Brancotte and Vincent (2002) point out the major importance of navigation channels in dispersion of Corbicula sp. within France and the major role of the Rhine River.
 
In Poland specimens of C. fluminalis were first reported in the River Odder in 2005 with 2004 the estimated year of introduction (Labêcka et al., 2005; Skuza et al., 2009).
 
The second location of invasion was the Danube River, already described by Galil et al. (2007) as one of the most important European invasion corridors. There, C. fluminalis dispersion in the upstream direction seems to be connected with shipping, primarily via exchange of ballast water (Paunovic et al., 2007). The first report of C. fluminalis in the lower basin of the Danube occurred in Ukraine in 2000-2001, with 1980 the estimated year of introduction (Voloshkevich and Son, 2002). 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). Upstream colonization allowed Danube colonization in Hungary. This species was for the first time reported in Ven-Duna at Baja and till Paks in the vicinity of a power plant (Csányi, 1999). However, Paunovic et al. (2007) point out the need for investigation on Pleistocene Asian clams against recent ones in the region, to define them as either introduced or reintroduced taxa.
 
In some isolated cases like Italy, C. fluminalis was first identified in 2004 at Lake Passo di Lavazzé (in Trentino Province) (Lori et al., 2005) and then in Lake Garda (Verona Province); the pathway of invasion is still unknown (Ciutti and Cappelletti, 2009). However, the 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).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Belgium 1992 Interconnected waterways (pathway cause) Yes No Nguyen and Pauw (2002); Swinnen et al. (1998) Started colonizing in the River Meuse and some major connecting canals in Belgium
France   Interconnected waterways (pathway cause) Yes No Brancotte and Vincent (2002) Invaded in at least seven different ways of which the upstream colonization in the Rhine has a dominating role
Germany   Hitchhiker (pathway cause); Interconnected waterways (pathway cause) Yes No Bachmann et al. (1997); Bernauer and Jansen (2006); Haesloop (1992) In the Wesser River with first introduction and in the Rhine and Mossel rivers by upstream colonization from the Netherlands population
Hungary   Interconnected waterways (pathway cause) Yes No Bódis et al. (2008) Restricted to the downstream section of the Paks (nuclear power plant)
Italy South Asia 2004 Yes No Cianfanelli et al. (2007); Gherardi et al. (2008) Unintentional introduction. Pathway still unknown
Luxembourg   Interconnected waterways (pathway cause) Yes No Bachmann and Usseglio-Polatera (1999) River Mossel border
Poland 2004 Hitchhiker (pathway cause) No No Labêcka et al. (2005) Lower Odder River
Romania   Interconnected waterways (pathway cause) No No Paunovic et al. (2007) North Serbia in Danube River
Serbia   Interconnected waterways (pathway cause) Yes No Paunovic et al. (2007) Danube River; tributary river Sava was also invaded, first the lower part (Makis) and upstream to Sabac
Switzerland Asia   Hitchhiker (pathway cause) Yes No Wittenberg (2006) Introduced from Asia via North America
Ukraine South East Asia   Hitchhiker (pathway cause); Interconnected waterways (pathway cause) Yes No Alexandrov et al. (2007); Voloshkevich and Son (2002)

Risk of Introduction

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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 (Gallil et al., 2007; Panov et al., 2007. C. fluminalis populations occur in the north of the western corridor (the network of rivers and canals in North Europe) and the southern corridor (the Danube) (Haas et al., 2002).

Power plant water system facilities can enhance the probability of success of Corbicula population as they offer refuges with warmer conditions (Nguyen and Pauw, 2002), allowing, for example, the survival of C. fluminalis during winter in Germany (Haesloop, 1992); and rapid stabilization and propagation of Corbicula species in Belgium that spread though service water systems of power plants along the River Meuse and connecting canals (Swinnen et al., 1998; Nguyen and Pauw, 2002). In the Odder River, Poland, C. fluminalis is also present in the vicinity of these industries as well as in Hungary (Csányi, 1999; Labêcka et al., 2005).

Europe’s approved laws on improving water quality may facilitate invasion by providing better environmental conditions for all stages of life of the invader (Karatayev et al., 2007) as this seems to be correlated with the reinvasion of zebra mussel in some European rivers (Bij de Vaate et al., 1992; Jantz and Neumann, 1992; Burlakova, 1998) and other invasive species in the Laurentian Great Lakes (of North America; Mills et al., 2003). The improved water quality could enhance Corbicula populations at the early stages because Corbicula spp. are quite sensitive to pollution (Cataldo et al., 2001a; Karateyev et al., 2007).

Given that the closely related species Corbicula fluminea has become a major invasive species in North and South America, C. fluminalis represents a threat to these regions if introduced.

 

Habitat

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This species is known to colonize a wide variety of habitats in the native range, being able to inhabit brackish waters in lower estuarine areas (e.g. Rivers Kura, Amur-Darya and Euphrates) and freshwater rivers and lakes (e.g. Rivers Jordan and Orontes and the African Great Lakes) (Martens, 1871; Decksbach, 1943; Aliev, 1960; Schuett, 1982; Daget, 1998). However, the Great African Lakes populations need genetic confirmation as C. africana is recognized as a valid taxon by Korniushin (2004) in Malawi/Nyassa Lake.

 

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
BrackishInland saline areas Principal habitat Natural
BrackishInland saline areas Principal habitat Productive/non-natural
OtherStored products Present, no further details Harmful (pest or invasive)
Terrestrial ManagedIndustrial / intensive livestock production systems Present, no further details Harmful (pest or invasive)
Terrestrial ManagedIndustrial / intensive livestock production systems Present, no further details Productive/non-natural
LittoralIntertidal zone Principal habitat Productive/non-natural
LittoralSalt marshes Principal habitat Productive/non-natural
FreshwaterIrrigation channels Present, no further details Harmful (pest or invasive)
FreshwaterLakes Present, no further details Natural
FreshwaterLakes Present, no further details Productive/non-natural
FreshwaterReservoirs Principal habitat Harmful (pest or invasive)
FreshwaterReservoirs Principal habitat Natural
FreshwaterReservoirs Principal habitat Productive/non-natural
FreshwaterRivers / streams Principal habitat Natural
FreshwaterRivers / streams Principal habitat Productive/non-natural
FreshwaterPonds Secondary/tolerated habitat Natural
BrackishEstuaries Principal habitat Harmful (pest or invasive)
BrackishEstuaries Principal habitat Natural
BrackishEstuaries Principal habitat Productive/non-natural
BrackishLagoons Principal habitat Harmful (pest or invasive)
BrackishLagoons Principal habitat Natural
BrackishLagoons Principal habitat Productive/non-natural

Biology and Ecology

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Genetics

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).

C. fluminalis presents ploidys in sets of 18 homologous chromosomes; diploid specimens have been found in the introduced European range (Pfenninger et al., 2002), and triploids have been found in Poland (Skuza et al., 2009). The population in the Odder River, Poland, has an arrangement of phenotypical chromosomes according to criteria proposed by Levan et al. (1964): division in 1 metacentric, 5 submetacentric and 12 subtelo-acrocentric chromosomes (Skuza et al., 2009).
 
Diploids of C. fluminea and C. papyracea have equal chromosomical set groups composed of 18 chromosomes and in a similar arrangement compared with 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 in Europe there exists evidence of cryptic hybridization between C. fluminea and C. fluminalis. The hybrid specimens were rare in abundance compared with the two major forms and they did not reach the adult stage (Pfenninger et al., 2002).
 
Reproductive Biology
 
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, which are considered a marker for androgenesis, and presence of monoflagellated spermatozoa, indicating sexual reproduction (Glaubrecht et al., 2003McKone and Halpern, 2003; Ishibashi et al., 2003).
 
The reproductive strategies in C. fluminalis are controversial. According to Korniushin (2004), the interpretation of C. fluminalis as an estuarine non-incubating dioecious taxon described by Morton (1982, 1986) for species from the River Pearl, China, is apparently wrong. C. fluminalis is now described as a facultative incubating species, due to the discovery of larvae incubating in the gills of museum specimens. In Europe, Rajagopal et al. (2000) reports C. fluminalis as non-incubatory, whereas Kinzelbach and collaborators (unpublished data in Korniushin, 2004) refer to the presence of intrabranchial larvae. Note that nourishment by ingesting of suppressed larvae or eggs (Fretter, 1984) is not reported in the Corbiculidae (Korniushin and Glaubrecht, 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 µmm (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).
 
Reproductive forms with androgenesis have been recorded in C.fluminalis (Korniushin, 2004) and in another 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), analysing androgenic lineages of Corbicula sp. 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.
 
For C. fluminalis there are no fecundity data for natural populations. However, a study of museum specimens revealed hundreds of incubatory clam stages (Korniushin, 2004). The data are not clear and do not reveal how the population behaves. However, for the Corbiculidae the level of recruitment strongly depends on the quantity of food available (Kraemer and Galloway, 1986; Williams and McMahon, 1986; 1989; Doherty et al., 1987; Cataldo and Boltovskoy, 1999).
 
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 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 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 than C. fluminalis which spends 33% in October and 20% in March. Rajagopal et al. (2000) define C. fluminalis as dioecious with a very low percentage of hermaphrodites and C. fluminea as hermaphrodite with an incubation larval strategy.
 
Another example is in cooling water channel of the Paks nuclear plant, central Hungary, 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 Corbicula 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 the water column (Bickel, 1966).
 
Nutrition

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.
 
Associations
 
In southern Iraq some epizoic algae were collected from turtles and molluscs, including C. fluminalis. Seven species were collected: Basicladia chelonum, Cladophora glomerata, C. profunda, Lola implexa, Oedogonium, Lyngbya lutea, and Nodularia (Islam and Hameed, 1982).
 
Environmental Requirements
 
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).
 
C. fluminalis can tolerate brackish water with a salinity of 50 ppt (Morton, 1986). Even though there are no available data for pH limits for C. fluminalis or C. fluminea, mortality rates can be enhanced by lower pH values (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) although Volkora (1962) notes that 0°C is tolerated in C. fluminalis.

Climate

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ClimateStatusDescriptionRemark
BS - Steppe climate Preferred > 430mm and < 860mm annual precipitation
BW - Desert climate Preferred < 430mm annual precipitation
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
54

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Salinity (part per thousand) Optimum 50 tolerated (Morton, 1986)
Water temperature (ºC temperature) Optimum 0 tolerated (Volkora, 1962)

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Aix sponsa Predator Nematodes|Juveniles to genus
Alosa sapidissima Predator Nematodes|Juveniles to genus
Anas acuta Predator Nematodes|Juveniles to genus
Anas clypeata Predator Nematodes|Juveniles to genus
Anas platyrhynchos Predator Nematodes|Juveniles to genus
Anas rubripes Predator Nematodes|Juveniles to genus
Angiostrongylus cantonensis Parasite Aquatic|Adult to genus
Aythya valisineria Predator Nematodes|Juveniles to genus
Cercaria corbiculae Parasite Aquatic|Adult to species
Chaetogaster limnaei Aquatic|Adult to species
Fulica americana Predator Nematodes|Juveniles to genus
Haplochromis Predator Aquatic|Adult to genus
Ictalurus furcatus Predator Nematodes|Juveniles to genus
Ictalurus punctatus Predator Nematodes|Juveniles to genus
Ictiobus bubalus Predator Nematodes|Juveniles to genus
Ictiobus niger Predator Nematodes|Juveniles to genus
Iheringichthys westermanni Predator Nematodes|Juveniles to genus
Leporinus obtusidens Predator Nematodes|Juveniles to genus
Lophotaspis orientalis Parasite Aquatic|Adult to genus
Multipeniata Aquatic|Adult to species
Neovison vison Predator Aquatic|Adult to genus
Odontesthes humensis Predator Nematodes|Juveniles to genus
Ondatra zibethicus Predator Nematodes|Juveniles to genus
Oreochromis mossambicus Predator Nematodes|Juveniles to genus
Oxydoras kneri Predator Nematodes|Juveniles to genus
Paraloricaria vetula Predator Nematodes|Juveniles to genus
Pimelodus albicans Predator Nematodes|Juveniles to genus
Pimelodus maculatus Predator Nematodes|Juveniles to genus
Procyon lotor Predator Aquatic|Adult to genus
Pterodoras granulosus Predator Nematodes|Juveniles to genus
Rallus longirostris Predator Nematodes|Juveniles to genus
Ricola macrops Predator Nematodes|Juveniles to genus
Spirinchus thaleichthys Predator Nematodes|Juveniles to genus

Notes on Natural Enemies

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There are no reports of predators in the European range of Corbicula sp. but it can be assumed that local fish and birds predate C. fluminalis.

Means of Movement and Dispersal

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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). 
 
Accidental Introduction
 
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, is ship ballast waters, which is the probable cause of C. fluminalis introduction to the Rhine River  (Gittenberger and Janssen, 1998; Karatayev et al., 2007) and upstream movement in the Danube (Paunovic 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).
 
Therefore, at local and national levels, the commercial or recreational activities in rivers and connectivity of canals are responsible for a rapid upstream colonization (Brancotte and Vincent, 2002; Panov et al., 2009a).
 
Karatayev et al. (2007) suggest that the rate of spread of the exotic species, including C. fluminalis, may be accelerated or slowed by various human activities.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
DisturbanceAnthropogenic ecosystem disturbances can provide pathways for invasion Yes Panov et al. (2007)
FisheriesCommercial fishing gear Yes Karatayev et al. (2007)
Hunting, angling, sport or racingUse as bait in sport fisheries Yes Brancotte and Vincent (2002); Karatayev et al. (2007)
Interconnected waterwaysEuropean corridors Yes Brancotte and Vincent (2002); Panov et al. (2007)
Self-propelledUpstream and downstream in rivers Yes Prezant and Chalermwat (1984); Voelz et al. (1998)
StockingStocking fish activities Yes Karatayev et al. (2007)

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stock Yes
Bait Yes Brancotte and Vincent (2002); Fox (1970)
Bulk freight or cargo Yes
Debris and waste associated with human activities Yes
Floating vegetation and debrisByssal attachment of pediveliger larvae and juveniles downstream spread Yes Prezant and Chalermwat (1984)
Machinery and equipmentCommercial fishing gear Yes Karatayev et al. (2007)
Ship ballast water and sedimentTransport pediveliger larvae and juveniles Yes Karatayev et al. (2007)
Ship hull foulingTransport pediveliger larvae and juveniles Yes Karatayev et al. (2007)
Ship structures above the water line Yes
Soil, sand and gravel Yes
WaterPediveliger larvae and juveniles, passive colonization Yes Prezant and Chalermwat (1984)

Impact Summary

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CategoryImpact
Biodiversity (generally) Negative
Economic/livelihood Negative
Environment (generally) Positive and negative
Human health Negative
Transport/travel Negative

Economic Impact

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Corbicula spp. have been reported as economic pests for the gravel industry (Sinclair and Isom, 1961 for C. flluminea; IUCN, 2013 for C. fluminalis). Gravel needs to be steamed before being used for concrete, otherwise the clams, which have been dredged together with the gravel, start tunneling through the concrete before it hardens.
 
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 such as those that are well documented for Corbicula fluminea in the USA and eastern Russia (Yanov and Rakov, 2002). 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 Impact

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Impact on Habitats

No well documented impacts of C.fluminalis on habitats have been found. The following information has been gathered for other invasive Corbicula spp. and are expected to be similar 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). The feeding behaviour of Corbicula sp. can induce wide effects in the invaded ecosystem by enhancing light penetration that increases the macrophyte coverage (Phelps, 1994a; Karatayev et al., 2007). Corbicula can also increase sedimentation rates, at local scales, as they constantly remove the seston and deposit them as faeces and pseudofaeces (Prokopovich, 1969). It is an important coupler between benthic and pelagic process because it uses organic matter from both the water column and sediments (Leff et al., 1990; Hakenkamp and Palmer, 1999). Corbicula influence macrobenthos in the partitioning of nitrogen through their motion and excretion and play an important role on primary production by recycling nitrogenous material (Yamamuro and Koike, 1993).
 
Bioturbation of sediments through bivalve movements increases water and oxygen content in the sediments, releasing nutrients and transferring metals from the sediment to the water column (Vaughn and Hakenkamp, 2001; Ciutat and Boudou, 2003).
 
Faeces and pseudofaeces of Corbicula sp. increase the organic matter in sediments (Vaughn and Hakenkamp 2001) and this situation could theoretically provide additional food for deposit feeding species (Roditi et al., 1997). However, this relationship was not observed (Hakenkamp and Palmer, 1999; Karatayev et al., 2005). Corbicula sp. feeds on sediment removing benthic bacteria, diatoms and its own deposited matter (Reid et al., 1992; Hakenkamp and Palmer, 1999).
 
Corbicula sp. as ecosystem engineers will have an impact on habitat structure, biomineralization, oxygenation and benthic planktonic community structure. It can alter the nutrient cycle and the food web structure interfering with the community stability (Mattice, 1979; Phelps, 1994a; Crooks, 2002; Karatayev et al., 2005; 2007; Sousa et al., 2009).
 
The accumulation of dead shells increase the roughness the bottom enhancing heterogeneity to soft bottoms which can provide benthos protection against erosion, by decreasing velocity flow in formed reefs of empty shells and clams (Gutiérrez et al., 2003; Sousa et al., 2009). Shell production in bivalve species play an important role in cycling CO2 and Ca (Chauvaud et al., 2003).
 
Impact on Biodiversity

In the absence of specific information on C. fluminalis, this section also includes details from other introduced Corbicula spp

García and Protogino (2005) show that C. fluminea is a source of food to fishes that might induce accumulation of heavy metals in higher trophic levels. 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).
 
Empty shells, left after the 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, Portugal, 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).
 
In the Tennessee River, USA, Isom (1971) reported that the loss of native mussel (Unionidae) diversity was due to impoundment and overharvesting or by fish-host association; however, it is mentioned that a new pest (Corbicula sp.) has successfully established and is considered by many authors to be responsible for the unionid decline (Parmalee, 1945; Cummings and Mayer, 1992; Williams et al., 1993). The invasion in Europe threatens native unionid species (Reis, 2003; Geist and Kuehn, 2005).
 
Vaughn and Spooner (2006), in a scale-dependant survey, revealed 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 addition 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 sp. preferentially invades sites where native mussel communities are already in decline by anthropogenic ecosystem disturbances (Strayer, 1999) and its impact on native mussels is much weaker than that of the zebra mussel Dreissena polymorpha (Strayer, 1999). Perhaps Corbicula cannot dominate indigenous bivalves in near-natural habitats (Fuller and Imlay, 1976).
 
The survival of larval stages of native mussels can be affected by larvae of 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 the juvenile stages of some species of unionid mussels. During decomposition, the ammonia concentration exceeds the acute levels of LC50(Cherry et al., 2005; Cooper et al., 2005).

Social Impact

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The major concern in terms of social impact is Corbicula as a possible vector of disease. 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 (Darrigan, 2002; Sousa et al., 2008b). As information on C. fluminalis as a vector is scarce it is necessary to provide information on other disease vectors within Corbiculidae family.

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). 

Risk and Impact Factors

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Invasiveness
  • Proved invasive outside its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Capable of securing and ingesting a wide range of food
  • Gregarious
  • Reproduces asexually
  • Has high genetic variability
Impact outcomes
  • Altered trophic level
  • Damaged ecosystem services
  • Ecosystem change/ habitat alteration
  • Infrastructure damage
  • Modification of hydrology
  • Modification of natural benthic communities
  • Modification of nutrient regime
  • Modification of successional patterns
  • Monoculture formation
  • Negatively impacts human health
  • Negatively impacts animal health
  • Reduced native biodiversity
  • Soil accretion
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
Impact mechanisms
  • Competition - monopolizing resources
  • Competition (unspecified)
  • Pest and disease transmission
  • Filtration
  • Fouling
  • Herbivory/grazing/browsing
  • Hybridization
  • Interaction with other invasive species
  • Predation
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally deliberately
  • Difficult to identify/detect as a commodity contaminant
  • Difficult/costly to control

Uses

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Economic Value

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).
  
Social Benefit
 
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).
 
Environmental Services
 
Individuals of Corbicula have been recommended for the biological assessment of water quality (Kerans and Karr, 1994; Carlisle and Clements, 1999).
 
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 List

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Animal feed, fodder, forage

  • Bait/attractant
  • Fishmeal
  • Invertebrate food

Environmental

  • Soil improvement
  • Wildlife habitat

General

  • Laboratory use
  • Pet/aquarium trade
  • Research model
  • Sociocultural value

Genetic importance

  • Test organisms (for pests and diseases)

Human food and beverage

  • Live product for human consumption
  • Meat/fat/offal/blood/bone (whole, cut, fresh, frozen, canned, cured, processed or smoked)

Materials

  • Shell

Diagnosis

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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).

Detection and Inspection

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The reports of C. fluminalis invasion are always when populations are already established, e.g. by dead shells on the shorelines in Italy (Ciutti and Cappelletti, 2009); in a sampled benthos survey in the Mosel River, France (Bachmann et al., 1997); and in reports of fishermen nets in the Danube River, Serbia (Paunovic et al., 2007).

Similarities to Other Species/Conditions

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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 Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

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).

SPS measures
 
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).
 
Public awareness
 
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).
 
Eradication
 
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).
               
Control
 
Movement control
 
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).
 
Biological control
 
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 Needs

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C. fluminalis is a poorly understood species, few consistent reports exist on its life cycle, reproductive behaviour and patterns of growth (Korniushin, 2004). Korniushin’s 2004 review is for now the most extensive work done on this species.

However, if the distribution of Korniushin (2004) is to be corroborated by genetic data, introduction pathways for C. fluminalis need to be reviewed. African Corbicula distribution is far from being complete - the distinction between C. artartina from C. fluminalis and C. africana has never been done. Little knowledge exists on C. fluminalis from Gabon (Preston, 1909), considered by Mandahl-Barth (1974) as a different species in Gabon. Also C. fluminalis species in Senegal require more study as there is so little information available.
 
On Lake Chad, Corbicula populations are controversial, and were not analysed by Korniushin (2004). Daget (1998) placed them as C. consobrina, and Mandahl-Barth (1988) as a race of C. fluminalis (in Glaubrecht et al., 2007). The existence of fossils records in Lake Chad and nearby regions like Algeria and central Sahara could indicate a refuge for C. fluminalis within Lake Chad (Fischer-Piette, 1949).

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.

References

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Links to Websites

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WebsiteURLComment
ALARM (Assessing Large Scale Risks for biodiversity with tested methods)http://www.alarmproject.net/alarm/
DAISIE Delivering Alien Invasive Species Inventories for Europehttp://www.europe-aliens.org/index.jsp
GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gatewayhttps://doi.org/10.5061/dryad.m93f6Data source for updated system data added to species habitat list.
Global register of Introduced and Invasive species (GRIIS)http://griis.org/Data source for updated system data added to species habitat list.

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03/01/10 Original text by:

Fabiana Freitas, University of Aveiro, Portugal

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