Potamocorbula amurensis
(Amur River clam)

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).

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.

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).

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).

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, 2005; Thompson 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, 2005; Thompson 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, 1991; Werner 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 japonica. P. 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. hinumensis. P. 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).

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

Deng et al., 2007

Urquhart and Regalado, 1991

Poulton et al., 2002

Hunt et al., 2003

Kardon, 1998

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

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).

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, 2000; Werner 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.

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.

16/02/08 Original text by:

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