Invasion History

First Non-native North American Tidal Record: 1988
First Non-native West Coast Tidal Record: 1988
First Non-native East/Gulf Coast Tidal Record:

General Invasion History:

Macoma petalum was formerly treated as a synonym of M. bathica by many authors, and known as the 'Baltic Clam'. It now appears to be part of a complex of at least two sibling species, derived from Pacific ancestors which made multiple invasions of the Atlantic through the Arctic Ocean (Vainola 2003; Nikula et al. 2007). Temperate Northwestern Atlantic populations, based on enzyme allele frequencies, are genetically distinct from East Atlantic and East Pacific populations (Meehan and Carlton 1988; Meehan et al. 1989). Meehan applied the name M. petalum to Northwest Atlantic populations.

In the Northeast Pacific, populations in San Francisco Bay are M. petalum and are distinct from populations in Alsea Bay and Coos Bay, Oregon, which resemble European M. balthica (Meehan and Carlton 1988; Meehan et al. 1989). Further genetic analysis by Vainola (2003) suggested that Pacific populations from British Columbia (M. balthica balthica), were distinct from the European populations (M. balthica rubra), at the subspecies level. However, subsequent sampling indicated that both genotypes are present in European waters, suggesting that multiple Pacific-Arctic-Atlantic invasions have occurred in the Tertiary and Pleistocene (Nikula et al. 2007).

The full biogeographic picture of the M. balthica complex is unresolved. In particular, the northward limit of Macoma petalum in the Northwest Atlantic is unclear. The nature of the boundary between M. petalum and European-Arctic M. balthica is not known (Beukema and Meehan 1985). Populations sampled in the St. Lawrence River estuary, Quebec, were M. balthica, with similarities to Pacific populations (Vainola 2003).

North American Invasion History:

Invasion History on the West Coast:

Molecular studies (amino acid electrophoresis) by Meehan and Carlton (1988) and Meehan et al. (1989) indicate that the San Francisco Bay population is distinct and belongs to the Northwest Atlantic species M. petalum. A second West coast population of M. petalum has been identified in Grays Harbor, Washington (Nikula et al. 2007). The extent and history of West Coast invasions of M. petalum is unclear (Carlton 1979; Meehan et al. 1989; Cohen and Carlton 1995).

The date of introduction of M. petalum to San Francisco Bay is not known. A few shells identified as 'M. balthica' were found in sediments 2000 to 6000 years B. P., but 'M. balthica' shells are absent from Indian shell middens (Meehan et al. 1989), suggesting that M. balthica may have been absent or extinct when M. petalum was introduced. Alternatively, M. petalum may have replaced a native population of M. balthica. Clams of the genus Macoma were found in San Francisco Bay in 1841 by the United States Exploring expedition, by various collectors in the 1860s, and by the 'Albatross' survey in 1912-1913. A transfer with oysters (Crassostrea virginica) from the East Coast seems like the most likely vector (Cohen and Carlton 1995), though a later introduction with ballast water cannot be excluded. Macoma balthica occurs in all regions of the Bay, from Collinsville in the Delta to San Pablo Bay and Central and South Bays, and is especially abundant in shallow water (Nichols and Thompson 1985a; Nichols and Thompson 1985b; Meehan et al. 1989; Cohen and Carlton 1995; Cohen et al. 2005; Brusati and Grosholz 2006).

A second West coast population of M. petalum has been identified in Grays Harbor, Washington (Nikula et al. 2007). Again, transplant of Eastern Oysters (Crassostrea virginica) is a likely vector, but ballast water is also possible.

Macoma balthica, considered to be conspecific with the Arctic-Northeastern Atlantic form, has been found in British Columbia and Oregon, and is presumed to be native to the Northeast Pacific (Meehan et al. 1989; Vainola 2003; Nikula et al. 2007). It was collected in 1837 in the Columbia River, and has been collected in Puget Sound (Meehan et al. 1989).


Description

Limecola petalum was formerly treated as a synonym of L. bathica by many authors, and known as the 'Baltic Clam', when both wer placed in the genus Macoma. It is now recognized as a member of a circumboreal species complex of estuarine clams (Meehan and Carlton 1988; Vainola 2003; Nikula et al. 2007). Limecola petalum is an oval shaped, laterally compressed clam with small umbones. A strong brown ligament is located behind the umbones, linking the two valves. The hinge lacks lateral teeth. The pallial sinus is larger in one valve than the other. The shell is usually dingy white, with a chalky texture, but sometimes has a rosy flush. Adults range from about 10 to 38 mm (Abbott 1974, as M. balthica; Gosner 1978). Definite identification of L. petalum from Atlantic or North Pacific L. balthica requires molecular methods (Meehan and Carlton 1988; Meehan et al. 1989; Vainola 2003; Nikula et al. 2007). However, some statistical differences have been found in comparing American East coast populations (L. petalum) and European (L. balthica) populations. Limecola petalum shells have a higher frequency of red or yellow in the interior of their shells than European L balthica, and they have fewer white shells, a lower weight-to length ratio, and a higher siphon weight for their size (Beukema and Meehan 1985; Kamermans et al. 1999).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Bivalvia
Subclass:   Heterodonta
Order:   Veneroida
Superfamily:   Tellinoidea
Family:   Tellinidae
Genus:   Limecola
Species:   petalum

Synonyms

Macoma balthica (Linnaeus (in part), 1758)
Macoma fragilis (auct. non Fabricius, 1780)
Psammobia fusca (Say, 1826)
Macoma petalum ((Valenciennes in Humoldt & Bonpland), 1821)

Potentially Misidentified Species

Limecola balthica
'Macoma balthica' was formerly regarded as a circumpolar species, but now appears to be part of a complex of at least two sibling species. Temperate Northwestern Atlantic populations, based on enzyme allele frequencies, are genetically distinct from East Atlantic and East Pacifc populations (Meehan et al. 1988; Meehan et al. 1989). Meehan has applied the name M. petalum (Vaenciennes 1821) to Northwest Atlantic populations. Populations in San Francisco Bay are M. petalum, and distinct from populations in Alsea Bay and Coos Bay, Oregon (OR), which resemble European M. balthica (Meehan et al. 1988; Meehan et al. 1989).

Limecola contabulata
NW Pacific, www.femorale.com, Japan,

Macoma iniquinaa
NE Pacific, Los Angeles-Alaska (Abbott 1974; Coan and Valentich-Scott, in Carlton 2007)

Macoma nasuta
NE Pacific, Mexico-Alaska (Abbott 1974; Coan and Valentich-Scott, in Carlton 2007)

Macoma secta
NE Pacific, Mexico-British Columbia (Abbott 1974; Coan and Valentich-Scott, in Carlton 2007)

Macoploma acolasta
NE Pacific, Bodega Bay-San Diego (Abbott 1974; Coan and Valentich-Scott, in Carlton 2007)

Rexithaerus indentata
NE Pacific, silty bays (Coan and Valentich-Scott, in Carlton 2007)

Ecology

General:

Limecola petalum is a small clam, typically found in the shallow subtidal to upper intertidal, often in silty brackish waters (Gosner 1978; Coan and Valentich-Scott, in Carlton 2007). The sexes are separate. Females in Chesapeake Bay produced 50,000 -500,000 eggs per female (Long et al. 2008). In San Francisco Bay, with a temperature range of ~10-25°C, spawning occurred in late winter and fall, depending on food supply and additional unknown factors (Thompson and Nichols 1988), but is likely to be much more seasonal in regions with a wider range of temperatures. The larvae are planktotrophic and research from Holland showed that they take a mean of 16-19.5 days to metamorphosis at 15°C, depending on food levels (Bos et al. 2007). In the Chesapeake Bay, larvae settle in spring, at about 10-14°C (Shaw 1965, cited by Chanley and Andrews 1971).

Limecola petalum is tolerant of a wide range of estuarine conditions. Adult M. petalum (from Chesapeake Bay) acclimated at 30°C had 50% mortality when transferred to 33-34°C for 24 hours (Kennedy and Mihursky 1971). When gradually transferred from 16-17 PSU, L. petalum had 97% survival at 2.5 PSU, and 100% survival at 30 PSU (Castagna and Chanley 1973). Limecola petalum is capable of deposit-feeding in sediment, mostly on benthic microalgae, and suspension-feeding in the water column (Thompson and Nichols 1988; Poulton et al. 2004). As a small, often abundant clam, with a fragile shell, it is an important food item for predators ranging from crabs to fishes and birds (Cohen and Carlton 1995).

Food:

Detritus, phytoplankton

Trophic Status:

Deposit Suspension Feeder

DepSusFed

Habitats

General HabitatGrass BedNone
General HabitatUnstructured BottomNone
General HabitatOyster ReefNone
General HabitatSalt-brackish marshNone
Salinity RangeOligohaline0.5-5 PSU
Salinity RangeMesohaline5-18 PSU
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEndobenthicNone


Tolerances and Life History Parameters

Minimum Temperature (ºC)0Based on field occurrences and range in the Northwest Atlantic (Abbott 1974).
Maximum Temperature (ºC)3324 hr LC 50, Kennedy and Mihursky 1971
Minimum Salinity (‰)2.5Experimental, acclimated at 5-10 ppt (Castagna and Chanley 1973)
Maximum Salinity (‰)35Typical marine salinity
Minimum Reproductive Temperature10Chespeake Bay, field range for larval set, Chesapeake Bay (Shaw 1965, cited by Chanley and Andrews 1971)
Maximum Reproductive Temperature14Chespeake Bay, field range for larval set, Chesapeake Bay (Shaw 1965, cited by Chanley and Andrews 1971)
Minimum Duration16Larval duration at 15 C, M. balthica, Netherlands (Bos et al. 2007)
Maximum Duration19.5Larval duration at 15 C, M. balthica, Netherlands (Bos et al. 2007)
Minimum Length (mm)10Reproduction begins at or near this size (Gosner 1978; Thompson and Nichols 1988)
Maximum Length (mm)38(Abbott 1974, as M. balthica; Gosner 1978)
Broad Temperature RangeNoneCold temperate-Warm temperate
Broad Salinity RangeNoneOligohaline-Euhaline

General Impacts

Macoma petalum is historically a very abundant bivalve in San Francisco Bay (Nichols and Thompson 1985a; Nichols and Thompson 1985b). Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004). In some habitats, such as Spartina marshes, it is still the dominant bivalve (Brusati and Grosholz 2006).

Ecological Impacts

Herbivory- Macoma petalum is capable of deposit-feeding (mostly on benthic microalgae) in sediment and suspension-feeding in the water column, and is still a significant filter-feeder in parts of San Francisco Bay (Thompson and Nichols 1988; Poulton et al. 2004).

Food/Prey- Macoma petalum, has been an important food resource for crabs, fishes, waterfowl, and shorebirds (Cohen and Carlton 1995; Poulton et al. 2004). Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004).

Competition, Habitat Change- Both in its native range, and in San Francisco Bay, M. petalum appears to be inversely correlated with Gemma gemma (Amethyst Gem Clam). This could be the result of feeding competition or alteration of sediment through Macoma's production of pseudofeces (Thompson 1982).

Regional Impacts

NEP-VNorthern California to Mid Channel IslandsEcological ImpactHerbivory
Limecola petalum, historically a very abundant bivalve in San Francisco Bay (Nichols and Thompson 1985a; Nichols and Thompson 1985b), is capable both of deposit-feeding in sediment and suspension-feeding in the water column. Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004).
NEP-VNorthern California to Mid Channel IslandsEcological ImpactFood/Prey
Limecola petalum, historically a very abundant bivalve in San Francisco Bay (Nichols and Thompson 1985a; Nichols and Thompson 1985b), has been an important food item for crabs, fishes, and waterfowl (Cohen and Carlton 1995; Poulton et al. 2004). Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004).
P090San Francisco BayEcological ImpactHerbivory
Limecola petalum, historically a very abundant bivalve in San Francisco Bay (Nichols and Thompson 1985a; Nichols and Thompson 1985b), is capable both of deposit-feeding in sediment and suspension-feeding in the water column. Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004).
P090San Francisco BayEcological ImpactFood/Prey
Limecola petalum, historically a very abundant bivalve in San Francisco Bay (Nichols and Thompson 1985a; Nichols and Thompson 1985b), has been an important food item for crabs, fishes, and waterfowl (Cohen and Carlton 1995; Poulton et al. 2004). Since 1987, it has been outnumbered and outweighed at many locations by the non-native clam Corbula amurensis, but still plays an important role in the food web of the bay (Poulton et al. 2004).
NEP-VNorthern California to Mid Channel IslandsEcological ImpactHabitat Change
Gemma gemma (Amethyst Gem Clam) appears to be negatively correlated with Limecola petalum. Pseudofeces of L. petalum may make the sediment unfavorable for G. gemma (Thompson 1982).
P090San Francisco BayEcological ImpactHabitat Change
Gemma gemma (Amethyst Gem Clam) appears to be negatively correlated with Limecola petalum. Pseudofeces of L. petalum< may make the sediment unfavorable for G. gemma (Thompson 1982).
NEP-VNorthern California to Mid Channel IslandsEcological ImpactCompetition
Gemma gemma (Amethyst Gem Clam) appears to be negatively correlated with Limecola petalum. This could be due, in part, to feeding competition (Thompson 1982).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
CAR-VII Cape Hatteras to Mid-East Florida 0 Native Estab
NA-ET3 Cape Cod to Cape Hatteras 0 Native Estab
NA-ET2 Bay of Fundy to Cape Cod 0 Native Estab
NEP-V Northern California to Mid Channel Islands 1988 Def Estab
P090 San Francisco Bay 1988 Def Estab
P093 _CDA_P093 (San Pablo Bay) 1988 Def Estab
NEP-IV Puget Sound to Northern California 1996 Def Estab
P280 Grays Harbor 1996 Def Estab
P070 Morro Bay 2011 Def Unk

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude
28371 Cohen, et al. 2005 (SF Bay Area RAS) 2004 2004-05-25 Port Sonoma, San Pablo Bay Def 38.1156 -122.5026

References

Abbott, R. Tucker (1974) <missing title>, Van Nostrand Reinhold, New York. Pp. <missing location>

Beukema, J. J.; Meehan, B. W. (1985) Latitudinal variation in the linear growth and other shell characteristics of Macoma balthica, Marine Biology 90: 27-30

Bos, Oscar G.; Philippart, Catharina J. M.; van der Meer, Jaap (2007) Effects of temporary food limitation on development and mortality of Macoma balthica larvae, Marine Ecology Progress Series 330: 155-162

Brusati, Elizabeth D.; Grosholz, Edwin, D. G (2006) Native and introduced ecosystem engineers produce contrasting effects on estuarine infaunal communities., Biological Invasions 8: 683-695

California Department of Fish and Wildlife (2014) Introduced Aquatic Species in California Bays and Harbors, 2011 Survey, California Department of Fish and Wildlife, Sacramento CA. Pp. 1-36

Carlton, James T. (Ed.) (2007) <missing title>, University of California Press, Berkeley. Pp. <missing location>

Castagna, M.; Chanley, P. (1973) Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the western mid-Atlantic coast., Malacologia 12(1): 47-96

Chanley, Paul; Andrews, J. D. (1971) Aids for identification of bivalve larvae of Virginia, Malacologia 11(1): 45-119

Coan, Eugene V.; Valentich-Scott, Paul (2007) The Light and Smith Manual: Intertidal Invertebrates from Central California to Oregon, University of California Press, Berkeley CA. Pp. 807-859

Coan, Eugene V.; Valentich-Scott, Paul; Bernard, Frank R. (2000) <missing title>, Santa Barbara Museum of Natural history, Santa Barbara CA. Pp. <missing location>

Cohen, Andrew N. and 10 authors (2005) <missing title>, San Francisco Estuary Institute, Oakland CA. Pp. <missing location>

Cohen, Andrew N.; Carlton, James T. (1995) Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta., U.S. Fish and Wildlife Service and National Sea Grant College Program (Connecticut Sea Grant), Washington DC, Silver Spring MD.. Pp. <missing location>

Duarte, Bernardo; Fonseca, Vanessa F.; · Reis?Santos, Patrick; Caçador, Isabel (2022) Bioinvasion by Spartina patens alters sediment biogeochemical functioning of European salt marshes, Biological Invasions <missing volume>(Published onlin): Published online

Foss, Stephen (2011) <missing title>, California Department of Fish and Game, Office of Spill Prevention and Response, Sacramento. Pp. 54

Gosner, Kenneth L. (1978) A field guide to the Atlantic seashore., In: (Eds.) . , Boston. Pp. <missing location>

Homberger, Lena; Xu, Jiawu; Dirk; Brandis; Chan, Tin-Yam; Keirsebelik, Heleen; Normant-Saremba, Monika; Schoelynck, Jonas ; Chu, Ka Hou; Ewers-Sauced (2022) Genetic and morphological evidence indicates the persistence of Japanese mitten crab mitochondrial DNA in Europe for over 20 years and its introgression into Chinese mitten crabs, Neobiota 73: 137–152

Hopkins, Dale R. (1986) Atlas of the distributions and abundances of common benthic species in San Francisco Bay, California, US Geological Survey Water Resources Investigations Report 86-4003: 1-16+ 25+228

Kamermans, Pauline, (1999) Morphological differences in Macoma balthica (Bivalvia, Tellinacea) from a Dutch and three southeastern United States estuaries, Journal of Sea Research 41: 213-224

Kennedy, V. S.; Mihursky, J. A. (1971) Upper temperature tolerances of some estuarine bivalves., Chesapeake Science 12(4): 193-204

Meehan, Brian W. (1985) Genetic comparison of Macoma balthica (Bivlalvia: Tellinidae) from the eastern and western North Atlantic Ocean, Marine Ecology Progress Series 22: 69-76

Meehan, Brian W., Carlton, James T. (1988) Unravelling a complex interoceanic dispersal history of the bivalve Macoma balthica, Journal of Shellfish Research 73(3): 361

Meehan, Brian W., Carlton, James T., Wenne, Roman (1989) Genetic affinities of the bivalve Macoma balthica from the Pacific coast of North America: evidence for recent introduction and historical distribution, Marine Biology 102(2): 235-241

Miller, Alexander Whitman (2000) <missing title>, University of California at Los Angeles, Los Angeles. Pp. <missing location>

Neira, Carlos; Grosholz, Lisa; Levin, Lisa A.; Blake, Rachael (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid., Ecological Applications 16(4): 1391-1404

Nichols, Frederic H.; Thompson, Janet K. (1985a) Time scales of change in the San Francisco Bay benthos., Hydrobiologia 129: 121-138

Nichols, Frederic H.; Thompson, Janet K. (1982) Seasonal growth in the bivalve Macoma balthica near the southern limit of its range, Estuaries 5(2): 110-120

Nichols, Frederic H.; Thompson, Janet K. (1985b) Persistence of an introduced mudflat community in South San Francisco Bay, California, Marine Ecology Progress Series 24: 83-97.

Nikula, Raisa; Strelkov, Petr; Vainola, Risto V (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae), Evolution 64(1): 928-941

Peterson, Heather A.; Vayssieres, Marc (2010) Benthic assemblage variability in the upper San Francisco estuary: A 27-year retrospective, San Francisco Estuary and Watershed Science <missing volume>: published online

Poulton, V.K.; Lovvorn, J.R.; Takekawa, J.Y. (2004) Spatial and overwinter changes in clam populations of San Pablo Bay, a semiarid estuary with highly variable freshwater inflow., Estuarine, Coastal and Shelf Science 59: 459-473

Robinson, April; Cohen, Andrew N.; Lindsey, Brie; Grenier, Letitia (2011) Distribution of macroinvertebrates across a tidal gradient, Marin County, California, San Francisco Estuary and Watershed Science 9(3): published online

1995-2015 Malacolog. http://www.acnatsci.org

Shaw, William N. (1967) Seasonal fouling and oyster setting on asbestos plates in Broad creek, Talbot County, Maryland, 1963-65., Chesapeake Science 8(4): 228-236

Thompson, J. K..; Nichols, F. H. (1988) Food availability controls seasonal cycle of growth in Macoma balthica (L.) in San Francisco Bay, California, Journal of Experimental Marine Biology and Ecology 116: 43-61

Thompson, Janet K. (1982) Population structure of Gemma gemma (Bivalvia: Veneridae) in South San Francisco Bay, with a comparison to some northeastern United States estuarine populations, Veliger 24(3): 281-290

Vainola, R. (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex., Marine Biology 143: 935-946

van Deurs, Mikael and 7 auhtors (2021) Impacts of the invasive round goby (Neogobius melanostomus) on benthic invertebrate fauna: a case study from the Baltic Sea, Neobiota 68: 19-30

Yamada. Sylvia Behrens; Shanks, Alan L.; Thomson, Richard E. (2022) Can the timing and duration of planktonic larval development contribute to invasion success? A case study comparing range expansion in the European green crab, Carcinus maenas, and the native lined shore crab, Pachygrapsus crassipes, in the northeast Paci, Biological Invasions Published online: Published online