Crepidula fornicata

Invasion History

First Non-native North American Tidal Record: 1931
First Non-native West Coast Tidal Record: 1931
First Non-native East/Gulf Coast Tidal Record:

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General Invasion History:

Crepidula fornicata is a sedentary, limpet-like mollusk native to the Northwest Atlantic from Newfoundland to the Gulf of Mexico. It is often extremely abundant in lower intertidal and shallow subtidal waters. There are some museum records from Puerto Rico and the Virgin Islands (Academy of Natural Sciences of Philadelphia 2013), but the Caribbean is not included in the range of C. fornicata given by authors (Bousfield 1960; Abbott 1974; Morris 1975; Rawlings et al. 2011; Rosenberg 2014). It has been introduced to the Northeast Pacific, including Puget Sound and the southern Strait of Georgia (Carl and Guiguet 1972; Carlton 1979; Cohen et al. 1998), and to European waters ranging from Norway to Spain, and the Mediterranean from France to Greece (Blanchard 1997; Sjotun 1997; Zenetos et al. 2003; Zenetos et al. 2005). [Reports of C. fornicata from Japan and Hong Kong (e.g. Blanchard 1997; DAISIE 2009) refer to the Northeast Pacific species C. onyx.] The primary vector of spread has been the transplantation of Eastern Oysters (Crassostrea virginica) from the East Coast of the US to the West Coast and Europe. Within Europe, spread has occurred through various means, including Pacific Oyster (C. gigas) transplants, mussels transplants, movement of fishing and aquaculture gear, hull fouling, or spread as larvae in ballast water or by currents (Blanchard 1997).

North American Invasion History:

Invasion History on the West Coast:

Crepidula fornicata was first reported from the West Coast in Puget Sound, Washington (WA) in 1931 (Sherwood 1931, Galtsoff 1932, cited by Carlton 1979), although it may have been introduced earlier. Carlton (1979) mentions a single specimen in the US National Museum of Natural History collections for Puget Sound in 1905. Some early collections, such as those in Tomales and Humboldt Bays in California (Bonnet 1935; Bonnet 1936, cited by Carlton 1979), and possibly some museum specimens collected in San Francisco Bay in 1973 (California Academy of Sciences 2013), probably represent dead shells introduced with plantings of Eastern Oysters (Crassostrea virginica). Other records include Willapa Bay, WA (in 1937 Hanna 1966; Carlton 1979; Cohen et al. 2001); Grays Harbor, WA (in 1976 Carlton 1979); Puget Sound, WA (Carlton 1979; Cohen et al. 1998; Cohen et al. 2001); Boundary Bay, British Columbia (BC) (Sherwood 1931, cited by Carlton 1979); and Victoria, BC (in 1939, Carlton 1979). Crepidula fornicata is reportedly abundant in southern areas of Puget Sound (Boersma et al. 2006), but absent from northern portions (Dethier and Schoch 2005).

Invasion History Elsewhere in the World:

In European waters, Crepidula fornicata was first reported in Liverpool Bay, England in 1872, but did not persist there. In the late 19th century, it appeared in many English estuaries where Eastern Oysters were planted, including the Thames and many small estuaries in Essex, Suffolk and Lincolnshire (1887-1893, Blanchard 1997; Eno et al. 1997). The oysters did not become established, but C. fornicata developed often dense populations, as in the Blackwater Estuary, Essex (Chipperfield 1951). The spread eastward was rapid, probably due to multiple vectors, including oyster transplants, hull fouling, ballast water, and larval dispersal. The slipper limpet was found in Belgium in 1911, the Netherlands in 1922, and the island of Sylt, Germany and the west coast of Denmark by 1934 (Blanchard 1997; Wolff 2005; Gollasch and Nehring 2006; Kerckhof et al. 2007). By 1948-1950, C. fornicata spread into the mouth of the Baltic, including the west (Skaggerrak) coast of Sweden (Blanchard 1997) and the east (Kattegat) coast of Denmark (Blanchard 1997; Jensen and Knudsen 2005).

It was first reported from Atlantic France in Hermanville, Normandy and Brest, Brittany in 1949 (Goulletquer et al. 2002; Blanchard 1997). Slipper limpets are now very abundant in aquaculture and fishing grounds for Pacific Oysters (Crassostrea gigas) and King Scallops (Pecten maximus). They occur further south in Arcachon Bay, France where it first appeared in 1969, but never attained the high abundances seen elsewhere (de Montaudouin et al. 2001; Goulletquer et al. 2002), and the Rias of Galicia, in northwest Spain, where it is abundant on floating rafts used for oyster and mussel culture (record from 1977, Blanchard 1997). In the Wadden Sea region, in the southeastern North Sea, populations were less dense than in Brittany and Normandy in the mid- 20th century, but have been increasing in the last decade, apparently due to climate change (Thieltges et al. 2003; Thieltges et al. 2004).

In the English Channel, C. fornicata has spread from east to west. It was found in the Solent, near the Isle of Wight in West Sussex in 1913 (Blanchard 1997), but by 1944 it had spread to Falmouth at the mouth of the Channel (Blanchard 1997). In 1958-59, it occurred in only 14% of 50 near-shore English Channel stations surveyed, but in 2006, it was found at 44% of stations, with an increase in abundance, and occurring at some stations down to 60 m depth. Expansion of its range was considered to be a possible response to a warming climate (Hinz et al. 2011). In 1960, it was found in County Kerry, on the west coast of Ireland (Arnold 1960), but did not persist there. However, it was found in Belfast Lough, Northern Ireland, off the Irish Sea, in 2007 and is now established (Minchin 2007; McNeill et al. 2010). On the Norwegian coast, C. fornicata was first found in the Oslofijord in 1968 and occurs west to Mandal, and sparingly on the west coast from Orresanden, near Stavanger, in shallow bays where oysters occur (Sjotun 1997).

In the Mediterranean, C. fornicata was first reported from a French lagoon (La Seyne sur Mer) in 1957 (Clanzig 1989) and was subsequently found in other lagoons used for oyster culture (Zibrowius 1991; Zenetos et al. 2003). It is established in lagoons and bays in mainland Italy, Sicily, Malta, and Greece (Zenetos et al. 2003; Zenetos et al. 2005).

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Description

Crepidula fornicata is a limpet-like marine snail, with an oval, convex shell. The shell can range from fairly flat to deeply arched in cross-section, depending on growth conditions. The apex, is turned to one side, not separate from the body of the shell. The shell has an interior shelf-like deck, covering about 1/2 of the aperture, giving it a boat-like appearance. The deck is slightly concave, and its edge is sinuous and asymmetrical. The color of the shell is highly variable, dirty-white to tan, with brown blotches and sometimes with radiating brown lines. The interior of the shell is brown and glossy, while the deck is white. Shells can be up to 50 mm long. Description from: Abbott 1974, Morris 1975, Gosner 1978, Lippson and Lippson 1997.

It grows in curved stacks of four or five individuals, but sometimes as many as 12 snails can be stacked on top of one another. Slippersnails are protandrous hermaphrodites. The oldest individuals, at the bottom of the stack, are female, while the youngest, at the top, are males, and the middle individuals are usually in the process of changing sex. The snails are sedentary and are usually attached to hard surfaces, such as rocks, dead or live shells, or debris such as bottles and cans (Chipperfield 1951; Gosner 1978; Lippson and Lippson 1997).

The planktonic veliger of C. fornicata is described and illustrated by Fretter and Pilkington (1970).

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Taxonomy

Ecology

General:

Crepidula fornicata is a common Atlantic filter-feeding marine gastropod, with a limpet-like body. It lives attached to solid substrates, but this can often be a live or empty shell of C. fornicata, another mollusk, or other hard-shelled animal (Gosner 1978). Crepidula fornicata is a protandric hermaphrodite. It first matures as a male, which can occur at as young as only 2 months after settling and 4 mm in size. This slipper shell often forms stacks of 2 to 20 individuals, with the oldest and largest female on the bottom, young males on the top, and individuals changing sex, in between. Males are somewhat mobile and copulate with females nearby, or below them on the stack, while females grow to fit the surface, to which they are attached, and are sedentary (Henry et al. 2010). Among populations, and stacks of individuals on Long Island's (New York) south coast bays, the size of the largest male varies from 10 to 40 mm (Hoch and Cahill 2012). As males grow, they undergo a sex-change, but usually do not mature as females before their 3rd year. The size and timing of the transition depends on whether the male is solitary or attached to a female (Coe 1938; Henry et al. 2010). The mean size of transitional individuals was 22-32 mm among five Long Island populations. Among stacks in these five populations, the largest female ranged from 20 to 50 mm (Hoch and Cahill 2012). Eggs are laid in capsules on the forward edge of the foot, each containing 180-260 eggs. Twelve animals in France laid 52-69 capsules and 9648-17940 eggs in a single spawning (Deslous-Paoli and Heral 1986). Specimens in Norway had 10,000 to 55,000 eggs per spawning, with egg production increasing with shell length (Pechenik et al. 2017). Eggs take about 17 days to hatch at 18.5°C and hatch into swimming planktotrophic veligers. The veligers settle after 11.5-14 days at 18-20°C, as juveniles 0.94 - 1.00 mm long (Collin 2003). At low food levels and temperature around 15°C development can be prolonged to 32 days (Pechenik and Lima 1984).

Crepidula fornicata can grow on a variety of substrates, including rock, wood, docks, floats, ship hulls, and shells of dead or live mollusks (including other C. fornicata) (Verrill and Smith 1873; Visscher 1927). It is most common at salinities of 20-30 PSU and inhabits shallow estuaries with a wide temperature range (Verrill and Smith 1873; Wass 1972; Leathem and Maurer 1975). In the northern part of its range in Germany, it appears to have been limited by mortality due to cold winter water temperatures and did not develop the high biomasses seen further south (Thieltges et al. 2004). In Bourgneuf Bay, central Atlantic France, increasing water temperatures and increasing chlorophyll concentrations were correlated with earlier breeding and a higher frequency of brooding females (Valdizan et al. 2011). Common molluscan hosts include Crassostrea virginica (Eastern Oyster – East Coast), C. gigas (Pacific Oyster – West Coast and Europe), and Mytilus edulis (Blue Mussel – East Coast and Europe) (de Montaudouin et al. 1999; Thieltges et al. 2006).

Crepidula fornicata is a filter feeder, trapping phytoplankton and detritus in strings of mucus on its gills, which are conveyed to its mouth (Lippson and Lippson 1997). Stable isotope measurements indicate that C. fornicata is an unselective feeder and because of its occurrence near the bottom, often on soft sediments, it ingests more detritus and benthic algae than more selective feeders, such as the Pacific Oyster (Decottignies et al. 2007a; Decottignies et al. 2007b; Lefebvre et al. 2009). In Europe, major predators include Asterias rubens (Common Starfish) and Carcinus maenas (Green Crab) (Thieltges et al. 2004).

Food:

Phytoplankton

Consumers:

Crabs; Starfish

Competitors:

Oysters; Mussels

Trophic Status:

Suspension Feeder

SusFed

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Habitats

General Habitat	Oyster Reef	None
General Habitat	Marinas & Docks	None
General Habitat	Unstructured Bottom	None
General Habitat	Rocky	None
General Habitat	Vessel Hull	None
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Epibenthic	None
Vertical Habitat	Littoral	None

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	0	Based on geographic range
Minimum Salinity (‰)	15	Experimental, lowest tested,j uveniles reared at 30 ppt, and transferred, (Pechenik and Eyster 1989)
Minimum Reproductive Temperature	10	Beginning of spawning (egg deposition) in Blackwater River, Essex (Chipperfied 1951). Minimum temperature for larval development is around 15 C (Pechenik and Lima 1984).
Maximum Reproductive Temperature	29	Maximum temperature tested for larval rearing (Pechenik and Lima 1984)
Maximum Reproductive Salinity	30	Highest tested, controls, Pechenik and Eyster 1989)
Minimum Duration	11.5	Experimental, at 20 C, high food (Pechenik et al. 1996, cited by Collin 2003b)
Maximum Duration	32	Experimental, at 15 C, low food (Pechenik and Lima 1984)
Minimum Length (mm)	4	Males, can mature at as small as 4 mm, 2 months after settling. They can reach maturity as females at 20-25 mm (Coe 1938; Henry et al. 2010).
Maximum Length (mm)	50	Abbott 1974
Broad Temperature Range	None	Cold temperate-Warm temperate
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

Crepidula fornicata is a fouling organism with potentially important impacts on human structures and shellfish and is an abundant filter-feeder and structural component of estuarine communities in invaded regions. Most information on ecological impacts of this species come from the coasts of northern Europe, from Germany to the northern Bay of Biscay. This species is included on a list of 'the 100 most invasive alien species in Europe' (DAISIE 2009). There is little specific information on its ecological or economic impacts on the West Coast of North America.

Economic Impacts

Fisheries: In European waters, Crepidula fornicata affects the survival, growth, and harvesting of commercially important shellfish. They also alter estuarine habitats in ways that may affect fish and other mobile fisheries species. Crepidula fornicata, as a filter-feeder, is widely believed to affect the growth of other bivalves by competition in a variety of ways, as well as altering habitats (see 'Ecological Impacts'). They affect fisheries more directly by fouling structures used in aquaculture and by fouling oysters, mussels, and scallops, requiring much time and effort to remove the limpets and clean the catch (Blanchard 1997; Thieltges et al. 2003; Frésard and Boncoeur 2006; Clark 2008).

Shipping: Crepidula fornicata does occur on ships’ hulls and buoys (Visscher 1927; WHOI 1952), but has not been reported as a major ship-fouling organism.

Industry: Crepidula fornicata has been reported to be an important fouling organism in power plants in the northeastern US (Holm et al. 2006), but not in European or other non-native waters.

Ecological Impacts

Herbivory: Crepidula fornicata is a filter-feeding gastropod, which traps and ingests suspended particles, mostly phytoplankton, but also detritus. In European waters, it has developed dense populations and large biomasses in bays and estuaries, with the potential to reduce phytoplankton concentrations (Blanchard 1997; Decottignies et al. 2007a; Decottignies et al. 2007b). However, not much information is available on individual and population feeding rates. In the Bay of Brest, Brittany, the invasion of C. fornicata was associated with a decrease in the spring diatom bloom and a shift of summer phytoplankton from diatoms to flagellates (Chavaud et al. 2000).

Competition: Crepidula fornicata, as an abundant, sedentary filter-feeder, has the capacity to compete with native suspension feeders by competition for food, space, or by settling directly on the shells of other organisms and interfering with their movement, feeding, or other behavior. Feeding competition has been studied most carefully with the Pacific Oyster (Crassostrea gigas), because of the latter's economic importance. Stable isotope analysis indicates that during much of the year in Brittany, food sources of the two species are distinct, because the oyster is a more selective feeder, while C. fornicata ingests much more detritus and benthic microalgae. However, in winter and early spring, when phytoplankton abundance is low, competition is possible (de Montaudouin et al. 1999; Thieltges et al. 2006; Decottignies et al. 2007a; Decottignies et al. 2007b). Crepidula fornicata competes for space on the bottom, with the native Great Scallop (Pecten maximus) and is believed to adversely affect scallop populations and fisheries in English and French waters (Frésard and Boncoeur 2006; Clark 2008). The growth and survival of Blue Mussels (Mytilus edulis) in the Wadden Sea were found to be reduced by C. fornicata, but not through competition for food. Instead attached limpets increased the hydrodynamic stress on the mussels, making it more likely for them to be detached, and shifting energy resources to increased production of byssus threads (Thieltges 2005; Thiletges and Buschbaum 2007).

Habitat Change: Crepidula fornicata has been a very successful invader in European waters, covering large areas of substrate with stacks of live animals and dead shells. The live animals produce vast quantities of feces and pseudofeces, and the shells themselves reduce bottom currents, also contributing to siltation. On one hand, the shells contribute to structure, including attachment sites for sessile organisms and hiding places for epifauna, but the siltation creates anoxic sediment, discouraging burrowing organisms (de Montaudouin and Sauriau 1999; Vallet et al. 2001; Blanchard 2009). Among faunal changes following C. fornicata's invasion are a population explosion of brittlestars (Blanchet-Aurigny et al. 2012) and a decline in recruitment of an important food fish, Solea solea (Common Sole) (Le Pape et al. 2004).

Parasite Community Effects: In experiments in the Wadden Sea, Germany, Crepidula fornicata together with the Pacific Oyster (Crassostrea gigas) and other filter feeders, such as the Softshell Clam (Mya arenaria), were found to affect transmission of the trematode parasite Himasthla elongata, by filtering out the metacercariae, without becoming infected themselves. The effect of these invaders was to reduce the parasite load on native bivalves, through dilution (Thieltges et al. 2008; Thieltges et al. 2009).

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Regional Impacts

B-II	None		Ecological Impact	Competition
Crepidula fornicata was considered to have weak community impacts in Kattegatt and Belt Sea regions (Zaiko et al. 2011)
NEA-IV	None		Ecological Impact	Habitat Change
Dense populations in Mont Saint-Michel Bay, Normandy, have created extensive shell beds, covering more than 25 km-2, and depositing 771 metric tons h-1 of organic matter into the sediment. The accumulation of organic matter makes sediment anoxic and the community becomes a shell reef, dominated by C. fornicata, other filter-feeders, and their predators living on or in the empty shells, but fewer burrowers (Blanchard 2009). Effects on benthic diversity and abundance, due to increased hard substrate on muddy bottoms, were noted in the Bay of Saint-Brieuc (increased diversity, but lower total abundance, Vallet et al. 2001) and in the Bay of Marennes-Oleron (higher diversity with higher overall abundance, de Montaudouin and Sauriau 1999). In the Bay of Brest, dense beds of C. fornicata shells were colonized by the native brittlestars Ophiocomina nigra and Ophiothrix fragilis. The spreading populations of brittlestars have probably contributed to mortality of C. fornicata (Blanchet-Aurigny et al. 2012). In three bays (Borgneuf, Pertuis Breton, Pertuis d'Antioche), the abundance of juvenile Common Sole (Solea solea) was negatively correlated with the abundance of C. fornicata (Le Pape et al. 2004).
NEA-IV	None		Ecological Impact	Competition
Crepidula fornicata and Crassostrea gigas (Pacific Oyster), in the Bay of Borgneuf, France, had substantial overlap in types of phytoplankton ingested in winter and early spring, but not in late spring and summer. The Slippersnail is more of an indiscriminate feeder, while the oyster is more selective (Decottignies et al. 2007a; Decottignies et al. 2007b). Lefebvre et al. (2009) suggest that the seasonal and system dynamics of estuaries may influence the appearance of competition among these species. In a more oceanic, well-mixed estuary, the food sources (phytoplankton) used by C. fornicata and C. gigas overlapped, but in a more estuarine bay, C. fornicata consumed more benthic microalgae. In laboratory experiments, Crepidula fornicata larvae fed at higher rates, and ate wider size range of phytoplankton than larvae of the oyster Crassostrea gigas. In Mont St. Michel Bay, larvae of C. fornicata can potentially deplete food resources for larvae of C. gigas (Blanchard et al. 2008). Crepidula fornicata competes for space with the King Scallop Pecten maximus in the Bay of Brest, Brittany, both for space on the bottom, and by attaching to the shells of the scallops (Frésard and Boncoeur 2006).
NEA-III	None		Economic Impact	Fisheries
Extensive fouling of mussels and scallops occurs in estuaries of South Devon, England. Fouling can reduce mussel growth and also increases handling time to clean and sort catches (Clark 2008).
NEA-IV	None		Economic Impact	Fisheries
Crepidula fornicata adversely affects the fishery of the King Scallop Pecten maximus in the Bay of Brest, Brittany, both by competing for space on the bottom, and by attaching to the shells of the scallops, reducing the harvest, and requiring time and effort to scrape the scallops clean. Frésard and Boncoeur (2006) model the the costs and benefits of possible programs to reduce the abundance of the slipper limpets (eradication was considered impossible) and restocking scallops.
NEA-II	None		Ecological Impact	Competition
In British waters, Crepidula fornicata is considered to compete with bivalves for phytoplankton and space (Eno et al. 1997). However, experiments comparing diets of C. fornicata and Pacific Oysters (Crassostrea gigas, or effects of attached Crepidula on oyster growth give variable results (de Montaudouin et al. 1999; Thieltges et al. 2006; Decottignies et al. 2007a; Decottignies et al. 2007b). Thieltges (2005) found that attached stacks of C. fornicata resulted in reduced growth and survival of Blue Mussels (Mytilus edulis. Since a similar effect occurred with attached 'fake limpets', the effect did not appear to the result of trophic competition. Instead, increased hydrodynamic stress caused the mussels to invest more energy in byssus production, reducing energy available for growth, which could be considered a form of interference competition (Thieltges 2005; Thiletges and Buschbaum 2007). Crepidula fornicata colonies compete for space with the commecially important Great Scallop (Pecten maximus), reducing the area vailable for settlement of larval scallops (Ménesguen and Grégoris 2018).
NEA-II	None		Ecological Impact	Habitat Change
In British waters, Crepidula fornicata is considered to alter habitats by deposition of large quantities of feces and pseudofeces, increasing the depth and extent of mud (Eno et al. 1997; Thieltges et al. 2003). In addition, the stacks of shells increase deposition by slowing water currents (Blanchard 1997; Thieltges et al. 2003). In the German Wadden Sea, C. fornicata is moving into mussel (Mytilus edulis beds, and now constitutes a major part of the biota there ( Thieltges et al. 2003; Thieltges et al. 2004). Crepidula fornicata colonies compete for space with the commecially important Great Scallop (Pecten maximus), reducing the area vailable for settlement of larval scallops (Ménesguen and Grégoris 2018).
NEA-II	None		Economic Impact	Fisheries
Dense limpet populations impede oyster and mussel culture and other fisheries, in the Thames, Scheldt and Wadden sea (Belgium-Netherlands-Germany) estuaries and require extensive cleaning of catches to remove the attached snails (Blanchard 1997; Thieltges et al. 2003). Crepidula fornicata colonies compete for space with the commecially important Great Scallop (Pecten maximus), reducing the area available for settlement of larval scallops. Modeling indicates that abundance and area of Crepdula colonies affects callop landings in the the bay of Saint-Brieuc, France (Ménesguen and Grégoris 2018).
NEA-V	None		Ecological Impact	Habitat Change
In experiments, in the Bay of Arcachon, France, the addition of Crepidula fornicata to oyster aquaculture beds did not affect growth of Pacific Oysters (Crassostrea gigas) or the abundance or diversity of the associated benthos, but the species composition of the benthos was altered, due to the increase in hard substrate (de Montaudouin et al. 1999).
NEA-II	None		Ecological Impact	Herbivory
Crepidula fornicata has developed large biomasses, which have the potential to lower phytoplankton biomass, through filter-feeding (Eno et al. 1997). However, feeding rates in the North Sea, English Channel, and Irish Sea regions, have not been quantified to our knowledge.
NEA-IV	None		Ecological Impact	Herbivory
Crepidula fornicata has developed dense populations in bays of Atlantic France, which have the potential to reduce phytoplankton concentrations (Blanchard 1997; Decottignies et al. 2007a; Decottignies et al. 2007b). In the Bay of Brest, France, a decrease in the magnitude of the spring phytoplankton bloom from 1979 to 1976, has been attributed to grazing by C. fornicata, which has doubled in abundance over that time span. Average chlorophyll concentrations have not been affected, probably due to increased nitrogen inputs and a shift in the phytoplankton community from diatoms to flagellates (Chavaud et al. 2000).

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