Invasive Species Compendium

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Datasheet

Potamocorbula amurensis
(Amur River clam)

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Datasheet

Potamocorbula amurensis (Amur River clam)

Summary

  • Last modified
  • 04 August 2022
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Potamocorbula amurensis
  • Preferred Common Name
  • Amur River clam
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Mollusca
  •       Class: Bivalvia
  •         Subclass: Heterodonta
  • Summary of Invasiveness
  • Potamocorbula amurensis is considered an invasive species due to its rapid spread in the San Francisco Estuary (SFE) and its reduction of phytoplankton biomass to critical levels. The first SFE specimen of P. amurensis was report...

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Pictures

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PictureTitleCaptionCopyright
Potamocorbula amurensis (Amur River clam); Small clam. San Francisco Bay, California, USA. February 2020.
TitleSmall clam
CaptionPotamocorbula amurensis (Amur River clam); Small clam. San Francisco Bay, California, USA. February 2020.
Copyright©oceanicadventures/via iNaturalist - CC BY 4.0
Potamocorbula amurensis (Amur River clam); Small clam. San Francisco Bay, California, USA. February 2020.
Small clamPotamocorbula amurensis (Amur River clam); Small clam. San Francisco Bay, California, USA. February 2020.©oceanicadventures/via iNaturalist - CC BY 4.0
Small clam shells in hand, showing various periostracum layers.
TitleSmall shells
CaptionSmall clam shells in hand, showing various periostracum layers.
CopyrightU.S. Geological Survey, Menlo Park, CA.
Small clam shells in hand, showing various periostracum layers.
Small shellsSmall clam shells in hand, showing various periostracum layers.U.S. Geological Survey, Menlo Park, CA.
Potamocorbula amurensis (Amur River clam); Small clams. Carquinez Strait, California, USA. June 2020.
TitleSmall clams
CaptionPotamocorbula amurensis (Amur River clam); Small clams. Carquinez Strait, California, USA. June 2020.
Copyright©Chris Brown/via iNaturalist - CC BY-NC 4.0
Potamocorbula amurensis (Amur River clam); Small clams. Carquinez Strait, California, USA. June 2020.
Small clamsPotamocorbula amurensis (Amur River clam); Small clams. Carquinez Strait, California, USA. June 2020.©Chris Brown/via iNaturalist - CC BY-NC 4.0
Potamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
TitleShells
CaptionPotamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
Copyright©Kim Hyun-tae (pintail)/via iNaturalist - CC BY-NC-SA 4.0
Potamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
ShellsPotamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.©Kim Hyun-tae (pintail)/via iNaturalist - CC BY-NC-SA 4.0
Potamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
TitleShells
CaptionPotamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
Copyright©Kim Hyun-tae (pintail)/via iNaturalist - CC BY-NC-SA 4.0
Potamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.
ShellsPotamocorbula amurensis (Amur River clam); Shells, note scale in mm. Bipa-ri, Gyeongsangnam-do, South Korea. August 2020.©Kim Hyun-tae (pintail)/via iNaturalist - CC BY-NC-SA 4.0
Potamocorbula amurensis (Amur River clam); Scanning electron micrographs P. amurensis hinges. Scale bar: 500 µm. Abbreviations: as - anterior socket. at - anterior tooth. lg - ligament plate. ps - posterior socket. r - ridge.
TitleScanning electron micrographs
CaptionPotamocorbula amurensis (Amur River clam); Scanning electron micrographs P. amurensis hinges. Scale bar: 500 µm. Abbreviations: as - anterior socket. at - anterior tooth. lg - ligament plate. ps - posterior socket. r - ridge.
CopyrightOliver PG, Hallan A, Jayachandran PR, Joseph P, Sanu VF, Bijoy Nandan S (2018). ZooKeys 799: 21-46. https://doi.org/10.3897/zookeys.799.25843 /via Wikimedia Commons - CC BY 4.0
Potamocorbula amurensis (Amur River clam); Scanning electron micrographs P. amurensis hinges. Scale bar: 500 µm. Abbreviations: as - anterior socket. at - anterior tooth. lg - ligament plate. ps - posterior socket. r - ridge.
Scanning electron micrographsPotamocorbula amurensis (Amur River clam); Scanning electron micrographs P. amurensis hinges. Scale bar: 500 µm. Abbreviations: as - anterior socket. at - anterior tooth. lg - ligament plate. ps - posterior socket. r - ridge.Oliver PG, Hallan A, Jayachandran PR, Joseph P, Sanu VF, Bijoy Nandan S (2018). ZooKeys 799: 21-46. https://doi.org/10.3897/zookeys.799.25843 /via Wikimedia Commons - CC BY 4.0

Identity

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Preferred Scientific Name

  • Potamocorbula amurensis Coan (2002), Huber (2010)

Preferred Common Name

  • Amur River clam

Other Scientific Names

  • Corbula amurensis Schrenck (1861)

International Common Names

  • English: Amur River corbula; Asian bivalve; Asian clam; brackish-water corbula; Chinese clam

Local Common Names

  • Germany: Nordpazifik-Venusmuschel
  • Japan: numakodaki

Summary of Invasiveness

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Potamocorbula amurensis is considered an invasive species due to its rapid spread in the San Francisco Estuary (SFE) and its reduction of phytoplankton biomass to critical levels. The first SFE specimen of P. amurensis was reported in late 1986 and within 2 years it was the dominant bivalve in the estuary. It has been hypothesized that ballast water was the mode of introduction. Its success in the estuary is due to its ability to occupy most habitats (sediment and water depths) in the system, its pelagic larvae, and its broad physiological tolerance of salinity as adults and as larvae. It is on the alert list for ISSG (Invasive Species Specialist Group) where it is listed as among the 100 World’s Worst Invaders and is listed as a pest by NIMBUS (National Introduced Marine Pest Information System).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Mollusca
  •             Class: Bivalvia
  •                 Subclass: Heterodonta
  •                     Order: Myoida
  •                         Unknown: Myoidea
  •                             Family: Corbulidae
  •                                 Genus: Corbula
  •                                     Species: Potamocorbula amurensis

Notes on Taxonomy and Nomenclature

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Potamocorbula amurensis (Schrenck, 1861) was first identified by Carlton et al. (1990) with the aid of A. Matsukuma (National Science Museum, Tokyo). The species name P. amurensis was provisionally selected at that time as Dr Matsukuma was starting a revision of the genus. Coan (2002) in his analysis of eastern Pacific Corbulidae revised the identification to Corbula amurensis. Recent molecular phylogenetic research has established the genus to be Potamocorbula (Huber, 2010) which will be used hereafter in this document. Morphologically similar species include Corbula laevis (Hinds, 1843 as reported in Carlton et al., 1990), Corbula ustulata (Reeve, 1844 as reported in Carlton et al., 1990), and Potamocorbula rubromuscula (Zhuang and Cai, 1983 as reported in Carlton et al., 1990). Common names have included the Amur River clam, Asian clam or bivalve, Chinese clam and the overbite clam; the latter name is a common name given to P. amurensis in California by media and resource managers due to confusion with Corbicula fluminea which is also called the Asian clam.

Description

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As described by Coan (2002)

:
“Ovate, thin; right valve decidedly larger than left valve; beaks anterior to midline (approximately 41% from anterior end); anterior end sharply rounded; posterior end sharply rounded…Shell white exteriorly and interiorly…right valve with a narrow tooth, attached to shell wall below hinge-line; left valve with a long, projecting chondrophore that is conspicuously divided and with a very small tooth on its posterior end…Pallial line with a small sinus.” Specimens in SFE have included shells that could be described as subtrigonal and ovate-elongate. An exterior posterior keel is apparent on left valve. The periostracum can be thick, range in colour from tan to dark brown, or it can be very thin on individuals living in high velocity sandy habitats. The maximum length is 24.5 mm. The type locality shell (CAS 121534, Carquinez Strait, San Francisco Bay, CA, USA) is available at California Academy of Sciences, San Francisco, CA. P. amurensis was originally described by Schrenck (1861, as reported in Coan, 2002). Photos of veliger larvae are available in Nicolini and Penry (2000).

Distribution

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The confusion in the taxonomy of this group makes a definitive geographic distribution difficult. Sato and Azuma (2002) have examined the P. amurensis from the SFE and believe it to be more similar to a newly invasive Potamocorbula species observed in the Ariake Sea than to the native P. amurensis seen in northeast Japan. The species described by Sato and Azuma (2002) as Potamocorbula sp. was not seen in Japan before 1990 and the authors suggested that they arrived from China or Korea with shipments of Corbicula. Owada et al. (2013) found that of the seven locations studied in Korea, Japan and the SFE, only one location in Korea (Ganghwa-do) differed from the rest morphologically and genetically.

Potamocorbula amurensis was found for the first time on the European continent in Belgium in 2018, mostly in the mesohaline and in a few locations in the polyhaline regions of the Scheldt estuary (Dumoulin and Langeraert, 2020). If it is the same species as found in SFE, it would be the second invasion location for the species.

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: 06 Jul 2022
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Asia

ChinaPresentNative
JapanPresentNative
-HonshuPresentNativeLake Obuchi
North KoreaPresentNative
South KoreaPresentNative

Europe

BelgiumPresent, LocalizedIntroduced2018Invasive
RussiaPresentNativeNorthern extent is mouth of Amur river

North America

United StatesPresent, LocalizedIntroduced1986InvasiveSan Francisco Estuary in California
-CaliforniaPresent, LocalizedIntroduced1986Invasive

Sea Areas

Pacific - Eastern CentralPresent, LocalizedIntroduced1986Invasive
Pacific - NorthwestPresentNativeLatitudinal range 22-53 degrees N

History of Introduction and Spread

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Carlton et al. (1990) hypothesize that P. amurensis was introduced into the SFE by ballast water, most likely originating from an Asian port. The first specimen was reported in late 1986, when juveniles were reported in the northern estuary. Within a year it had spread throughout the northern estuary, and within 18 months had become the dominant bivalve in the northern estuary (Nichols et al., 1990). It spread to the southern estuary within two years where it is a common and frequently dominant bivalve (Thompson, 2005). The appearance of P. amurensis in the Scheldt estuary in 2018 or before (large adults were found in 2018) has not been traced to a source and vector.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
USA China 1985-1986 Yes No Carlton et al. (1990)
Belgium 2017-2018 Unknown Yes No Dumoulin and Langeraert (2020)

Risk of Introduction

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Embryos can survive a 2 to 30 psu salinity range at an age of 24 h (Nicolini and Penry, 2000), the larvae have a long pelagic phase (2-3 weeks), and it can survive anoxic conditions (McEnnulty et al., 2001) which increases the risk of a successful ballast water introduction of P. amurensis. This is particularly true when ballast water less than 14 days old is released in estuaries. Intra-coastal introductions by ballast water in the eastern Pacific or by recreational boating through incidental introduction of adults on anchors and in bait boxes seems most likely. However, so far P. amurensis has not been reported in other eastern Pacific estuaries. Australia considers P. amurensis to be a sufficient threat to trigger an emergency response and New Zealand has classified it as one of ‘six exotic high impact species’ included in an early detection surveillance system (ISSG, 2008). P. amurensis was discovered in the Scheldt estuary in 2018 but the method of introduction is not known (Dumoulin and Langeraert, 2020).

Habitat

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Potamocorbula amurensis have been observed in all habitats except epifaunal (i.e. attached to hard substrate) habitats in the SFE. They prefer mid-intertidal to subtidal ranges but large populations can be found in the high intertidal. Individuals have been collected in silt, clay, hard-pack clay, sand, gravel, peaty mud and shell hash. When found in hard-pack clay or high velocity areas, a single byssal thread passes through the anterior end of the shell and attaches to a piece of debris in the sediment. They live with one-half to two-thirds of their shell exposed which is verified by the presence of live barnacles on the posterior end of many shells. Large populations have been found near the freshwater endpoint in the estuary and in the southern estuary where salinities are similar to ocean salinities. P. amurensis is present in the deeper, primary sloughs in the marshes of SFE but research within the marsh finds that they are rare in the smaller secondary sloughs (Baumsteiger et al., 2017).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
BrackishBrackish - Natural / Semi-naturalWetlands Secondary/tolerated habitat Harmful (pest or invasive)
LittoralMud flats Principal habitat Harmful (pest or invasive)
LittoralIntertidal zone Secondary/tolerated habitat Harmful (pest or invasive)
FreshwaterRivers / streams Secondary/tolerated habitat Harmful (pest or invasive)
BrackishEstuaries Principal habitat Harmful (pest or invasive)
BrackishLagoons Principal habitat Harmful (pest or invasive)

Biology and Ecology

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Genetics

The first molecular phylogenetic study of the Corbulidae family by Hallan et al. (2013) found that there were three groups in the family: a limnetic-euryhaline group in which Potamocorbula resides and two marine groups. The Potamocorbula in San Francisco Estuary, the Rokkaku River Estuary in Japan and the Mangyeong River Estuary in Korea Republic (Owada et al., 2013) are all placed in the limnetic-euryhaline group The first genetic study of P. amurensis in the SFE (Duda, 1994) reported that differentiation among the populations was low, with all populations showing a high degree of variability. Larvae remain in the plankton for 2-3 weeks in early spring and autumn (Nicolini and Penry, 2000) which is sufficient time for larvae from the northern estuary to be transported to and populate the southern estuary in spring (Thompson et al., 2008). Thus, it is unlikely that populations have or will differentiate in this system unless reproductive seasons are limited to autumn and other low freshwater flow periods that would hydrodynamically separate the northern and southern estuary populations.

There is genetic data available for Potamocorbula in NCBI’s GenBank, which had 58 records for P. amurensis as of 24/9/21 (NCBI, 2021).

Reproductive Biology

Potamocorbula amurensis is dioecious (sexes are separate), develops reproductive products (eggs and sperm) when individuals are about 4 mm in length (longest shell dimension), and shows both seasonal and continuous development of reproductive products depending on location in the SFE (Parchaso, 1995). It spawns at least twice a year in the estuary (spring and autumn) and initiation of reproductive activity (sperm and egg development) has been linked to food availability in the northern estuary by Parchaso and Thompson (2002). Individuals were reported as reproductively active in field salinities ranging from 0.1 to 27.6 psu and in field temperatures ranging from 6.4 to 23°C. Although sperm and eggs are continuously produced in the southern estuary (Parchaso, 1995), larval recruitment occurs primarily in the spring with a secondary smaller recruitment in the autumn in both the northern and southern estuary (Thompson, 2005Thompson et al., 2008).

Laboratory studies by Nicolini and Penry (2000) found that spawning and successful fertilization can occur in salinities ranging from 5 to 25 psu. Eggs and sperm can tolerate a 10-step change in salinity and 2 h old embryos can tolerate salinities ranging from 10-30 psu. Spawning was induced in the laboratory by withholding food and stressing the animals. Females produce 45,000-220,000 oocytes with no apparent relationship to size of female. Larvae settled after 17-19 days in the water column in the laboratory. The combination of responding to food quickly to initiate gamete production and producing gametes and embryos that are tolerant of large changes in salinity is likely to be a good strategy for an invasive species. As suggested by Nicolini and Penry (2000), the larvae’s ability to rapidly adjust to substantial changes in salinity may also make P. amurensis particularly viable in ballast water where oceanic exchange of water is only partially successful.

Physiology and Phenology

Physiological studies of P. amurensis are limited within English and European journals although there may be Asian literature that was not available to the author. P. amurensis is an osmo-conformer that can adapt to changes in salinity within 48 h by altering intracellular concentrations of particular amino acids. Adults can tolerate very low salinities (0.1 psu) in the laboratory but die with prolonged freshwater exposure (Werner et al., 2003). Miller and Stillman (2013) found metabolic rates varied seasonally with the lowest rates in spring and highest rates in fall, but they were not able to relate metabolic variability to salinity, temperature, or food. Potamocorbula hyper-osmoregulated in low salinity but the costs of that physical adjustment were not reflected in the metabolic rate or energy stores. They conclude that Potamocorbula’s distribution is not a result of energy costs due to osmoregulation. However, Potamocorbula may pay some metabolic price for its high tolerance of salinity variation. Paganini et al. (2010) observed that Potamocorbula had 40% lower oxygen consumption rates (VO2) at salinities fluctuating between 4 and 14 than the VO2 observed at steady high (28) and steady low (2) salinities. Glycogen was reported as low by Werner et al. (2003) and high by Miller and Stillman (2013), and lipid stores were generally lower in Potamocorbula than in other bivalves (Richman and Lovvorn, 2004). Therefore, it appears Potamocorbula cannot or does not depend on energy stores during periods of stress. In examining the fatty acids in Potamocorbula,Canuel et al. (1995) suggested that they are “capable of rapid assimilation and incorporation of algal-derived organic matter into their tissues during periods of high phytoplankton abundance.” Such rapid assimilation could account for the differing glycogen results, i.e. glycogen concentration may reflect recent events.

Although the data are not shown in their report, McEnnulty et al. (2001) report that P. amurensis “has a high tolerance to low oxygen and is found in polluted or eutrophic areas”.

P. amurensis is sufficiently tolerant of a variety of trace metals that Brown and Luoma (1995) have used it as a biosentinel species (a species used to evaluate the fate and distribution of biologically available contaminants). However, the accumulation of trace metals is not without effect, as P. amurensis has limited reproductive capability with high body burdens of silver (up to 5.5 µg/g dry wt; Brown et al., 2003) and shows stress and histopathic lesions in the reproductive tissue with high levels of cadmium (10 µg/g dry wt; Werner et al., 2003).

Seasonal cycles in P. amurensis in the northern SFE, which is the geographic portal for freshwater to the estuary, are related to seasonal changes in hydrology which controls both the salinity and food availability in the system. SFE is a greatly altered ecosystem (Nichols et al., 1986) and the amount and seasonality of flow of freshwater into the system is largely controlled by man except during extreme wet years. Thus the seasonal cycles of growth and reproduction in P. amurensis tend to be similar except during periods of extreme drought and flood years (Thompson, 1999; 2005). P. amurensis individuals in the southern SFE, which is a lagoonal system with limited natural freshwater inflow except during high freshwater outflow events, grow rapidly during the annual phytoplankton bloom in spring and grow steadily but more slowly during summer and autumn (Thompson, 2005Thompson et al., 2008).

Nutrition

Potamocorbula amurensis is a suspension feeder that can filter and assimilate both phytoplankton and bacteria (<1.2 µm) from the water column. Filtration rates, estimated in a flume with varying velocities, range from 100-575 L (g/ dry weight) per day with a mean of approximately 400 L/(g dry weight) per day or 1-5 L per day per clam for the phytoplankton Chroomonas salina [Rhodomonas salina] (Cole et al., 1992). Clearance rates estimated in beaker experiments are similar: 4 L per day for a 1 cm clam {filtration rate = -40+199 x shell length (cm)} for phytoplankton (Isochrysis galbana) and 45 mL per hour per clam (independent of shell size) for bacteria (Werner and Hollibaugh, 1993).

Retention efficiency for natural bacteria is lower (28% and 13% for 1 and 2 cm long clams) than for phytoplankton (100%). Bacterial gross assimilation rates (73-75%: Decho and Luoma, 1991Werner and Hollibaugh, 1993) are somewhat lower than measured for phytoplankton (78 - 90% for a range of phytoplankton species; Schlekat et al., 2002). Bacterial carbon appears to be more quickly metabolized than phytoplankton carbon (Werner and Hollibaugh, 1993). Net assimilation rates have been estimated at 45% for bacteria (Werner and Hollibaugh, 1993) and approximately 85% for phytoplankton (Werner and Hollibaugh, 1993; Schlekat et al., 2002).

Although there have been studies showing that P. amurensis is capable of filtering copepod nauplii out of the water column (10%/day; Kimmerer and Lougee, 2015), there are no studies showing the nauplii are assimilated into the clam tissue (Kimmerer et al., 1994; Greene et al., 2011; Kayfetz and Kimmerer, 2017).

Associations

Potamocorbula amurensis is a euryhaline species (able to adapt to rapidly changing salinity) that is also able to maintain a dominant position in relatively salinity-stable portions of estuaries. Its abundance can exceed 10,000/m2 (Carlton et al., 1990) and biomass can exceed 200 g dry tissue wt/m2 (Thompson, 1999). It is not surprising therefore to find it living with a variety of euryhaline species in some locations and with species with much narrower salinity tolerances in other locations. P. amurensis occurs among many non-indigenous species in the benthic community of the SFE (Cohen and Carlton, 1998). All species listed in this discussion as co-dominants with P. amurensis in SFE are cryptogenic (likely to be non-indigenous) or have been established as non-indigenous. Based on the wide geographic range of vectors for non-indigenous species in SFE, it is not surprising that the benthic species associations of P. amurensis in SFE are quite different than those in its native habitat. Unless otherwise stated the information for SFE is from Thompson et al. (2007).

The euryhaline benthic community near the freshwater interface (salinity of 0.5-5 psu) in the SFE is numerically dominated by two oligochaetes (Varichaetadrilus angustipenis and Limnodrilus hoffmeisteri), a filter-feeding polychaete (Marenzellaria viridis [Marenzelleria neglecta]), P. amurensis, and the Asian freshwater bivalve, Corbicula fluminea. Although P. amurensis and C. fluminea have similar feeding niches there has been no apparent reduction in C. fluminea abundance since the invasion of P. amurensis. The two bivalves frequently co-occur within one sample. Two species of Corophidae amphipods occur seasonally in this community.

Common members of the benthic community in addition to P. amurensis in the mid-salinity range (5-18 psu) in the SFE are the tube dwelling amphipods Ampelisca abdita and Monocorophium alienense [Sinocorophium alienense], the cumacean Nippoleucon hinumensis, and the euryhaline filter-feeding polychaete (M. neglecta). Species that persistently occur in this community, but in relatively lower numbers than those listed above include the polychaete Heteromastus filiformis and the amphipod Grandidierella japonicaP. amurensis reduced the density of two suspension-feeding bivalves when it appeared in this community; Mya arenaria during dry years, and C. fluminea during wet years (Nichols et al., 1990). Peterson (2002) also found that there was a reduction in species who spawn and have pelagic larvae but that the core community of species that brood their young and deposit feed were unaffected by the arrival of P. amurensis.

Co-dominants with P. amurensis in the most saline portion (salinity of 18-30) of the estuary are the tube dwelling amphipods A. abdita and the cumacean N. hinumensisP. amurensis frequently co-occurs with other filter-feeding bivalves in these sections of the estuary; these bivalves include the green bagmussel (Musculista senhousia [Arcuatula senhousia]), the Japanese littleneck clam (Venerupis japonica [Ruditapes philippinarum]), the Atlantic soft-shell clam (M. arenaria) and the Baltic clam (Macoma petalum). Other persistent but relatively lower abundance members of the community include several species of Corophidae amphipods, and the deposit feeding polychaetes H. filiformis and Sabaco elongatus.

In its native range P. amurensis dominates (>70%) the abundance of the infauna in the euryhaline Mankyung Estuary in Korea (salinity range of 0.7-28) in summer. The carnivorous polychaetes Nephtys californiensis and Glycinde sp., and the surface-deposit/suspension feeding polychaete Prionospio cirrifera combine for an additional 20% of the abundance.

P. amurensis and the surface-deposit/suspension feeding polychaetes P. cirrifera and Pseudopolydora kempi jointly and almost equally make up >70% of the abundance in the benthic community in the polyhaline (salinity of 18-30) Keum Estuary in Korea. As in SFE, the filter-feeding bivalve Arcuatula senhousia co-occurs with P. amurensis in this estuary (9% of the total community abundance). A second polyhaline estuary in Korea, the Dongjin Estuary, is also dominated by P. cirrifera (31%). An approximately equal but lower abundance of the carnivorous polychaetes Glycera chirori and N. californiensis and P. amurensis each make up about 20% of total abundance of the community (Choi and Koh, 1994). The only oligohaline community with P. amurensis described in the literature is from the Amur River (Kamenev and Nekrasov, 2012) and is limited to the bivalves Corbicula japonica, Henslowiana [Euglesa] sp. and Pisidium orientale.

A Korean mudflat with interstitial salinities ranging from approximately 30-42 is numerically dominated by the suspension-feeding polychaete Laonome tridentata (65%) and P. amurensis (29%) with deposit feeding, burrowing crabs (Ilyoplax spp.) making up almost 5% of the community (Koh and Shin, 1988).

The benthic community of the most recently invaded estuary, the Scheldt River Estuary, is similar to other mesohaline areas with P. amurensis: Macoma balthica, Scrobicularia plana, M. arenaria, Corophium spp., Cyathura carinata, H. filiformis, Hediste spp. and Nereis spp. (Dumoulin and Langeraert, 2020).

Natural Food Sources

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Food SourceFood Source DatasheetLife StageContribution to Total Food Intake (%)Details
phytoplankton Aquatic|Adult gross assimilation rate 78-90% limited number of species tested
bacteria Aquatic|Adult gross assimilation rate 73-75%
zooplankton Aquatic|Adult removal rate from plankton ͂10%/day zooplankton larvae

Climate

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ClimateStatusDescriptionRemark
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)
Ds - Continental climate with dry summer Preferred Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter Preferred Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
22-55

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Depth (m b.s.l.) Optimum Aquatic|Adult 30 tolerated, observation in San Francisco Estuary, USA
Salinity (part per thousand) 0.2 42 Optimum Aquatic|Adult 0.2-42 tolerated, lower limit based on Werner et al. (2003); upper limit on Koh and Shin (1988)
Salinity (part per thousand) 10 30 Optimum Aquatic|Larval fertilization at 5-25
Water temperature (ºC temperature) -1.5 30 Optimum Aquatic|Adult 6-23 tolerated, observation in San Francisco Estuary, USA

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Acipenser trasmontanus Predator Aquatic|Adult to species Zeug et al. (2014)
Aythya affinis Predator Aquatic|Adult to species Poulton et al. (2002)
Aythya marila Predator Aquatic|Adult to species Poulton et al. (2002)
Cancer magister Predator Aquatic|Adult to species Carlton et al. (1990), Stewart et al. (2014)
Melanitta perspicillata Predator Aquatic|Adult to species Hunt et al. (2003)
Pogonichthys macrolepidotus Predator Aquatic|Adult to species Deng et al. (2007)

Notes on Natural Enemies

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Known aquatic consumers of P. amurensis in the SFE include the Dungeness crab (Cancer magister [Metacarcinus magister]; 

Carlton et al., 1990
Stewart et al., 2004
), the Sacramento splittail (Pogonichthys macrolepidotus
Deng et al., 2007
), and the white sturgeon (Acipenser transmontanus;
Urquhart and Regalado, 1991
; Kogut, 2008; Zeug et al., 2014). It is likely that any bottom feeding fish with a sufficiently large mouth, that feeds in areas where P. amurensis is found consumes some quantity of the bivalves due to their large population numbers. Birds that are known to consume P. amurensis include the greater and lesser scaup (Aythya marila and Aythya affinis;
Poulton et al., 2002
) and the surf scoter (Melanitta perspicillata
Hunt et al., 2003
). Conchiolin layers, laminae in the shells that are of an organic nature, which occurs in bivalves in the Corbulidae family, act both to increase the strength of the shell against predation from mechanical crushing and to deter gastropods from drilling through the bivalves shell (
Kardon, 1998
).

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

Corbula amurensis larvae were shown to be pelagic for 2-3 weeks in the laboratory (Nicolini and Penry, 2000) and Thompson et al. (2008) show that this is sufficient time for larvae produced in the northern estuary to transit the 40 plus km and settle in the southern estuary. Populations of P. amurensis are reduced and in some cases eradicated by migratory birds in autumn and winter in all but the deep channel areas of the SFE (Poulton et al., 2002; Thompson et al., 2008). Therefore, these shoal areas are mostly dependent on the adjacent deep-water populations to supply recruits each year.

Vector Transmission (Biotic)

Kogut (2008) reports P. amurensis survived the consumption and excretion by white sturgeon, Acipenser transmontanus, that was collected in the field and observed in the laboratory. Although this is a potential vector for spread, we have no field data to confirm that P. amurensis has been spread this way.

Accidental Introduction

Carlton et al. (1990) hypothesized that P. amurensis was introduced by ballast water. Subsequent research on their wide physiological tolerances and 2-3 week larval pelagic stage support the possibility that it could again be introduced accidentally by ballast water.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Interbasin transfersCoastal areas in Northwest Pacific between 22-53 N are all possibleCarlton et al. (1990)
Interconnected waterwaysSpread throughout San Francisco Estuary Yes Carlton et al. (1990)

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Ship ballast water and sedimentLarval through adult Yes Yes Carlton et al. (1990)

Impact Summary

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CategoryImpact
Environment (generally) Negative
Fisheries / aquaculture Negative
Native fauna Negative
Native flora Negative
Rare/protected species Negative

Economic Impact

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The SFE is the source of freshwater for over 25 million people and over 500,000 ha of farmland in the state of California, which supports a multi-billion-dollar agriculture industry. Most of the water in the state is retained in the northern state, initially as snow, and then as snowmelt in reservoirs that are operated by the state and federal governments. A very elaborate canal and pumping system then transports the water throughout the state in addition to releasing some of the water into the estuary where it is used for agricultural irrigation in addition to its use in the ecosystem.

The precipitous decline of several fish species, including one federally-designated threatened, and recently petitioned to be endangered, species has caused resource managers to alter the flow of water to water users beginning in 2007. One of the conceptual models being tested as the cause of the fish decline is a possible shift in the food web due to overgrazing of phytoplankton by P. amurensis (Sommer et al., 2007). There has been a reduction in zooplankton and mysid shrimp concurrent with the invasion of P. amurensis, both of which are important prey for larval and adult fish.

Striped bass (Morone saxatilis) is the most important sport fishery in the SFE and it has been steadily declining since the 1960s. A sharper decline in abundance of this species has been seen since 1999, concurrent with the decline of other fish species (Sommer et al., 2007). This fishery was estimated to bring US $47 million into the San Francisco Bay area in 1985 when the striped bass abundance was estimated at about a half million. In 2001, the striped bass abundance had fallen to less than 50,000; no revenue estimate has been made for present day conditions (California Department of Fish and Game, 2001).

Resource managers in California have invested hundreds of millions of dollars to restore habitat and purchase water for environmental use due to the decline in pelagic fish, mysid shrimp and zooplankton. One ecosystem restoration effort in the SFE, funded through a combined state and federal program (CALFED) has spent US $335 million. Part of this funding has been directed towards restoration of primary producers to levels seen prior to P. amurensis introduction.

Environmental Impact

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Impact on Habitats

The SFE is a high nutrient, high turbidity estuary that has low primary production due to a combination of light limitation and bivalve grazing (Cloern, 2001; Thompson et al., 2008; Cloern and Jassby 2012). The northern estuary has always had low primary production but declines following the invasion of P. amurensis lead many researchers to conclude that suspension feeding by P. amurensis resulted in the decline in phytoplankton biomass and the elimination of the annual phytoplankton bloom in that system (Alpine and Cloern, 1992; Kimmerer, 2002Thompson, 2005).

The annual primary production has been reduced to <20 g C/m2 per year from approx 100 C/m2 per year (Alpine and Cloern, 1992Jassby et al., 2002Thompson, 2005). Two copepods (Acartia spp., Eurytemora affinis [Eurytemora affinis affinis]), a rotifer (Synchaeta bicornis) and a mysid shrimp (Neomysis mercedis) concurrently declined with the phytoplankton, presumably due to food limitation (Kimmerer, 2002Feyrer et al., 2003). Some of the declines in copepods may also be due to direct filtration of juveniles by P. amurensis (Kimmerer et al., 1994). Despite what appeared to be a collapse of the food web within 5 years of the invasion of P. amurensis, many species remain. The robustness of the food web may due to its complexity and therefore weak links (Kimmerer, 2002) or due to the migration of one important, competing filter feeder, the northern anchovy (Engraulis mordax), out of the northern system following the reduction in phytoplankton biomass (Kimmerer, 2006). As expected, the food web is more complex than initially reported, and recent work has shown that it is the combination of grazing by P. amurensis and microzooplankton that limits phytoplankton growth in the northern estuary (Kimmerer and Thompson, 2014). Although the cause of a recent decline in pelagic fish in the system (Sommer et al., 2007) is probably at least partially due to changes in the pelagic food web, there is no conclusive evidence that food is the primary or only cause for the decline of the fish species. The fish species showing the largest declines include a federally threatened species, on which a petition has been filed to re-classify it as an endangered species (delta smelt: Hypomesus transpacificus), and three other species with statistically significant, large declines in abundance since the year 2000 (the longfin smelt (Spirinchus thaleichthys), the threadfin shad (Dorosoma petenense) and the striped bass (Morone saxatilis)).

The near-surface growth position of P. amurensis makes them more available to predators than the deep-burrowing bivalve that previously dominated the northern estuary (Macoma petalum, previously known as Macoma balthica). The caloric content of the two bivalves is similar (Richman and Lovvorn, 2004). Thus the invasion might be an advantage to bottom feeding predators if not for the propensity of P. amurensis to accumulate certain contaminants, selenium in particular, at near toxic levels for consumers (Stewart et al., 2004). Since its arrival in the system, predators on P. amurensis that now have liver selenium concentrations in excess of the toxicity threshold include a fish, the Sacramento splittail (Pogonichthys macrolepidotus), the Dungeness crab (Cancer magister [Metacarcinus magister]), the white sturgeon (Acipenser transmontanus) (Stewart et al., 2004) and diving ducks (scoter (Melanitta perspicillata) and scaup (Aythya spp.)) (White et al., 1987; 1988; 1989; Urquhart and Regelado, 1991Linville et al., 2002).

Prior to the invasion of P. amurensis, there were no molluscs that could withstand the extreme changes in salinity in the northern SFE. The presence of a persistent population of bivalves has increased the net production of carbon dioxide to 50-100 g C m-2 / year which greatly exceeds the carbon consumption by primary producers (20 g inorganic C m-2 /year) (Chauvaud et al., 2003). Given the invasion rate of molluscs throughout the world, the effect of P. amurensis on the carbon dioxide balance in this estuary may illustrate what is occurring worldwide.

Impact on Biodiversity

Potamocorbula amurensis has eliminated the appearance of two bivalves that used to invade the mesohaline (salinity of 5-18) portion of the estuary during dry and wet periods. During extended dry periods, the Atlantic soft shell clam (Mya arenaria) invaded in sufficient numbers to reduce the phytoplankton biomass in these embayments (Nichols, 1985). Conversely, during wet years the Asian freshwater clam (Corbicula fluminea) invaded these embayments. Neither of these clams has been successful in dominating the benthic community since P. amurensis invaded (Nichols et al., 1990). Neither the number of species nor the Shannon diversity index (based on abundance) showed a change following the invasion of P. amurensis. The Shannon diversity index (based on biomass) did show a drastic decline as did the number of suspension feeding species and species that spawn (Peterson, 2002).

Threatened Species

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Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
Hypomesus transpacificus (delta smelt)CR (IUCN red list: Critically endangered); USA ESA listing as threatened speciesCaliforniaCompetition - monopolizing resourcesUS Fish and Wildlife Service (1996)
Spirinchus thaleichthysNo DetailsPacific, NortheastCompetition - monopolizing resourcesFederal Register (2012)

Risk and Impact Factors

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Invasiveness
  • Proved invasive outside its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Pioneering in disturbed areas
  • Highly mobile locally
  • Fast growing
  • Has high reproductive potential
  • Gregarious
  • Has high genetic variability
Impact outcomes
  • Altered trophic level
  • Damaged ecosystem services
  • Ecosystem change/ habitat alteration
  • Modification of natural benthic communities
  • Modification of nutrient regime
  • Modification of successional patterns
  • Negatively impacts animal health
  • Negatively impacts aquaculture/fisheries
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
Impact mechanisms
  • Competition - monopolizing resources
  • Filtration
  • Herbivory/grazing/browsing
  • Interaction with other invasive species
  • Predation
  • Rapid growth
  • Altered food web
  • Ecosystem change/ habitat alteration
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Detection and Inspection

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Smith et al. (2012) have developed a real-time PCR assay to detect P. amurensis larvae in water.

Similarities to Other Species/Conditions

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The only eastern Pacific corbulid that might be confused with P. amurensis is Corbula luteola [Caryocorbula luteola], which occurs south of the present range of Corbula amurenis (the San Francisco Estuary; Coan, 2002). Young juveniles may be confused with juveniles of other inequivalve bivalves such as Mya arenaria and Cryptomya californica; the original specimen in SFE was initially misidentified as a member of the Myidae. As they age, the “smaller, flatter left valve is drawn into the larger and more swollen right valve” of P. amurensis (Carlton et al., 1990). M. arenaria has a deep pallial sinus compared to the shallow pallial sinus of P. amurensis and C. californica is less ovate and lacking the posterior keel (Carlton et al., 1990).

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.

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.

The only management strategy that has been proposed for containing P. amurensis has been to stop it before it arrives by controlling ballast water releases. Given the wide salinity tolerance of adult and juveniles (Nicolini and Penry, 2000Werner et al., 2003) and their apparent low oxygen tolerance (McEnnulty et al., 2001) this will be difficult unless ballast water is either totally exchanged or rendered non-biotic in some manner.

Monitoring and Surveillance

Scientists discovered P. amurensis in SFE due to a monitoring program that had been active since the late 1970s and an academic program that was sampling during the critical invasion period (Carlton et al., 1990). No actions were taken, and given the wide spread of the species by the time it was identified, it would have been unlikely that any actions would have been successful.

Should P. amurensis appear in Australia, where it is on the National List of Invasive Marine Species and considered a medium-high priority, will trigger an emergency response (Hayes et al., 2005). It is unclear what the response will be as the Rapid Response Toolbox produced by CSIRO reports that if P. amurensis is discovered, trawling is unlikely to succeed as a mechanism for removal. They also state that oxygen deprivation in ballast tanks is unlikely to be successful due to P. amurensis’ “high tolerance to low oxygen” (McEnnulty et al., 2001).

Surveillance systems are in place in New Zealand for early detection of P. amurensis and there is a plan to limit release of ballast water from areas where it is known to occur (New Zealand Ministry of Fisheries, 2001).

A PCR assay for the rapid detection of P. amurensis larvae in water samples has been developed by Smith et al. (2012) and will continue to be developed to aid countries either limit the ballast water received from areas with viable P. amurensis populations or develop a method of killing the larvae before ballast release.

Ecosystem Restoration

Potamocorbula amurensis invaded the SFE after a 100 year flood event that greatly reduced the diversity and abundance in the benthic community at the invasion location (Nichols et al., 1990). Although P. amurensis then invaded other parts of the estuary in the following two years, and did so within a normally diverse community (Thompson, 2005), its ability to monopolize the depauperate benthic community in the northern estuary signifies its likely response to newly restored habitat. This observation has resulted in limits to restoration options in the northern estuary where a major objective is to increase the primary production of the system.

Gaps in Knowledge/Research Needs

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The largest research needs include a continuing examination of the physiological characteristics of the species and continued monitoring of eastern Pacific and European estuaries. P. amurensis has apparently not spread to intra-coastal ports nor has it been introduced to other eastern Pacific locations. It seems unlikely that adults and larvae have not been included in ballast water that has been released in other ports. The only explanations we have at present for the lack of spread is that (1) there is something in its physiology that limits its transport and or settlement in most situations, (2) the balance of trade today reduces the number of ships arriving fully in ballast from Asia and thus there has been less opportunity for release of ballast water, or (3) it has invaded elsewhere but in localities without monitoring programs.

References

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Smith, K.F., Wood, S.A., Mountfore, D.O., Cary, S.C., 2012. Development of a real-time PCR assay for the detection of the invasive clam, Corbula amurensis, in environmental samples. Journal of Experimental Marine Biology and Ecology, 412:52-57. DOI: 10.1016/j.jembe.2011.10.021

Sommer, T., Armor, C., Baxter, R., Breuer, R., Brown, L., Chotkowski, M., Culberson, S., Feyrer, F., Gingras, M., Herbold, B., Kimmerer, W., Mueller-Solger, A., Nobriga, M., Souza, K., 2007. The collapse of pelagic fishes in the upper San Francisco Estuary. Fisheries (Bethesda), 32(6):270-277. DOI: 10.1577/1548-8446(2007)32[270:TCOPFI]2.0.CO;2

Stewart, A.R., Luoma, S.N., Schlekat, C.E., Doblin, M.A., Hieb, K.A., 2004. Food web pathway determines how selenium affects aquatic ecosystems: A San Francisco Bay case study. Environmental Science & Technology, 38(17):4519-4526.

Thompson, J.K., 1999. The effect of infaunal bivalve grazing on phytoplankton bloom development in south San Francisco Bay. PhD Thesis. Stanford, USA: Stanford University.

Thompson, J.K., 2005. One estuary, one invasion, two responses: phytoplankton and benthic community dynamics determine the effect of an estuarine invasive suspension feeder. In: The comparative roles of suspension feeders in ecosystems [ed. by Olenin, S., Dame, R.]. Amsterdam, Netherlands: Springer. 291-316.

Thompson, J.K., Hieb, K., McGourty, K., Cosentio-Manning, N., Wainwright-De La Cruz, S., Elliot, M., Allen, S., 2007. Habitat type and associated biological assemblages: soft bottom substrate. In: Report on the subtidal habitats and associated biological taxa in San Francisco Bay [ed. by Schaeffer, K., McGourty, K., Cosentio-Manning, N.]. Santa Rosa, USA: National Oceanic and Atmospheric Administration. 18-23, 37-46.

Thompson, J.K., Koseff, J.R., Monismith, S.G., Lucas, L.V., 2008. Shallow water processes govern system-wide phytoplankton bloom dynamics: a field study. Journal of Marine Systems. DOI: 10.1016/j.jmarsys.2007.12.006

Urquhart, K.A.F., Regalado, K., 1991. Selenium verification study, 1988-1990. Report 91-2-WQ. Sacramento, USA: California Water Resources Control Board.

US Fish and Wildlife Service, 1996. Recovery plan for the Sacramento-San Joaquin Delta native fishes. USA: US Fish and Wildlife Service. 208. http://ecos.fws.gov/docs/recovery_plan/961126.pdf

Werner, I., Clark, S.L., Hinton, D.E., 2003. Biomarkers aid understanding of aquatic organism responses to environmental stressors. California Agriculture, 57(4):110-115. DOI: 10.3733/ca.v057n04p110

Werner, I., Hollibaugh, J.T., 1993. Potamocorbula amurensis: comparison of clearance rates and assimilation efficiencies for phytoplankton and bacterioplankton. Limnology and Oceanography, 38:949-964.

White, J.R., Hofmann, P.S., Hammond, D., Baumgartner, S., 1987. Selenium verification study, 1986. Sacramento, USA: Water Resources Control Board Report.

White, J.R., Hofmann, P.S., Hammond, D., Baumgartner, S., 1988. Selenium verification study, 1986-1987. Sacramento, CA, USA: Water Resources Control Board Report.

White, J.R., Hofmann, P.S., Urquhart, K.A.F., Hammond, D., Baumgartner, S., 1989. Selenium verification study, 1987-1988. Sacramento, USA: Water Resources Control Board Report.

Yamamoto, G., 1977. Successional processes observed in the freshening brackish lakes of Shimokita Peninsula. Journal of the Faculty of Marine Science and Technology (Tokai University), 10:119-128.

Zeug, S.C., Brodsky, A., Kogut, N., Stewart, A.R., Merz, J.E., 2014. Ancient fish and recent invaders: white sturgeon Acipenser transmontanus diet response to invasive-species-mediated changes in a benthic prey assemblage. Marine Ecology, Progress Series, 514:163-174. DOI: 10.3354/meps11002

Zhuang, Q., Cai, Y., 1983. Studies on the Corbulidae (Bivalvia) off Chinese coasts. Transactions Chinese Society of Malacology, 1:57-68.

Distribution References

CABI, Undated. CABI Compendium: Status inferred from regional distribution. Wallingford, UK: CABI

Carlton J T, Thompson J K, Schemel L E, Nichols F H, 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. Introduction and Dispersal. Marine Ecology Progress Series. 81-94.

Coan E V, 2002. The eastern Pacific recent species of Corbulidae (Bivalvia). Malacologia. 44 (1), 47-105.

Dumoulin E, Langeraert W, 2020. The brackish hive conch Potamocorbula amurensis (Schrenck, 1861) (Bivalvia, Myida, Corbulidae), one newcomer to the Scheldt estuary; or the beginning of a long story. The Beach Flea. 40 (4), 1-60.

Schrenck L I, 1861. Molluscs of Amurland and the northern Sea of Japan. (Mollusken des Amur-Landes und des Nordjapanischen Meeres.). In: Reisen and Forschungen im Amur-Lande in den Jahren 1854-1856, Vol. 2. St Petersburg, USSR: Kaiserliche Akademie der Wissenschaften. 259-297.

Schrenck L V, 1861a. Molluscs of Amurland and the northern Sea of Japan. (Mollusken des Amur-Landes und des Nordjapanischen Meeres.). In: Reisen and Forschungen im Amur-Lande in den Jahren 1854-1856, Vol. 2. St Petersburg, USSR: Kaiserliche Akademie der Wissenschaften. 259-297.

Yamamoto G, 1977. Successional processes observed in the freshening brackish lakes of Shimokita Peninsula. Journal of the Faculty of Marine Science and Technology (Tokai University). 119-128.

Links to Websites

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Guide to Exotic Species of San Francisco Bayhttp://www.exoticsguide.org
Sea Grant National Aquatic Nuisance Species Clearinghousehttp://aquaticinvaders.org

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16/02/08 Original text by:

Janet Thompson, U.S. Geological Survey, 345 Middlefield Rd. MS-496, Menlo Park, CA 94025, USA

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