At the end of the nineteenth century, C. fornicata was accidentally introduced in Europe where it found favourable conditions to settle and develop: free surfaces of sandy-coarse sediment, optimal water temperatu...
At the end of the nineteenth century, C. fornicata was accidentally introduced in Europe where it found favourable conditions to settle and develop: free surfaces of sandy-coarse sediment, optimal water temperature range, copious suspended organic matter as food and no specific predators; all this contributed to a rapid growth and reproductive success.
Oyster farming is the main cause of introduction and dispersal. Dredging and trawling of the oyster-growing areas has contributed to the spatial spread of C. fornicata. It is now demonstrated that these fishing practices have, for decades, played a main role in the spread.
The name of the genus Crepidula means a slipper in Latin. The species epithet fornicata was given by the naturalist Linnaeus, due to the arched form of the colony (fornix = arch in Latin). The taxonomy adopted in the last ERMS classification places Crepidula in the family Calyptraeidae, which was given by Lamarck in 1799; the previous family name Crepidulidae (Flemming, 1822) is also found. The higher classification of the Gastropoda of Bouchet and Rocroi (2005) places Crepidula in clade Littorinimorpha of the Caenogastropoda. The genus Crepidula contains about thirty species distributed across the continents; some classification problems can arise when different Crepidula species are present in the same area.
C. fornicata is a marine gastropod with a brown shell. Individuals reach about 6 cm long. The septum divides the interior of the shell into two parts: the external one where the foot and head can move and the internal one where the visceral mass is protected. Growth is rather rapid and a size of 2 cm is reached in 2 years. The plasticity of this species is important and shell can be deformed.
The first particularity of this species is that the individuals gather under attractive substances and form colonies, called ‘chains’. Individuals settle on top of each other, forming clusters. Only one juvenile remains at the top of the stack, the others move to form a new colony. The population extends in three dimensions.
In a standard colony there are 5 or 6 individuals, but in dense populations, this creates amazing numbers of stacks with complex colonies where the juveniles attach anywhere and support a new chain.
Newel and Kofoed (1977) described the morphology of the feeding system and measured the feeding rates in C. fornicata. This ubiquistous species ingests a wide variety of organic and inorganic food, at a rate of about 1 litre h-1 g-1, and also ingests some of its own larvae (Pechenik et al., 2004). The pelagic larva is also able to filter a wide range of particles (Blanchard et al., 2008). The radula can also capture some deposited matter. This feeding mode helps it find sufficient food to develop large populations, contrary to other grazing patellids (Hoagland, 1977).
Being fixed, the animals have developed a particular reproduction. The species is protandric. Juveniles are males and individuals become rapidly hermaphrodites from the second year, and then are females during the rest of their life (10 years). Between males and females of the same stack, fecundation is direct and sperm can be stored in a receptacle. Females of 2 cm long can be ovigerous. The brood is protected, eggs are laid grouped in bags (about 50 eggs bag-1) and are first stored near the head and later fixed on the lower shell. After about a month, each female releases 10-20,000 free larvae. They are veliger, barrel-shaped with a central ring of filaments to move in the plankton. Their size (min. 400 µm) and their strength make them suitable for experimental use (Pechenik and Lima, 1984; Pechenik et al., 2002b, 2004). The pelagic phase is about 3-weeks long (depending of the temperature) then larvae metamorphose and fall to the bottom where they look for suitable supports. All kinds of hard material can be used but they prefer a congener shell.
Being ubiquitous, eurythermic and euryhaline, this species can be observed in all kinds of environments: rocky, gravel or sandy bottoms, as well as in muddy areas where are measured the highest densities in Europe. These characteristics have helped it to spread so successfully.
C. fornicata is native to the Atlantic coast of the USA and fossils are found along the Massachussetts coasts (Zeigler et al., 1965). It is found together with three congeneric species: Crepidula plana, Crepidula convexa and Crepidula aculeata. Walne (1956) described its geographical area as ranging from Escuminac point (47°N) on the Canadian coastline, to the Caribbean islands. It seems that in its native area, C. fornicata is weakly spreading, due to unfavourable hydrological conditions (low winter temperatures, strong currents) and a great number of predators (Hoagland, 1977).
C. fornicata was imported into Europe along with American oysters (Crassostrea virginica) dredged from oyster beds of Atlantic estuaries. Hoagland (1985) wrote that the European populations came from Long Island Sound. Large quantities of oysters were introduced in England and with them also C. fornicata, both juveniles and adults.
The geographical distribution of C. fornicata now stretches over 24 degrees of latitude, reaching all European seasides and the English Channel which currently appears to be the most colonized area (Blanchard, 1997). It is currently limited to the northern hemisphere. In the western USA, it was imported with oysters in Puget Sound during the 1930s, and is now common along the Washington state coastline (Hoagland, 1974, 1977). In 1968, spreading populations were noted in the bays of Tokyo and Sagami in Japan (Habe and Maze, 1970).
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.
The introduction of C. fornicata in Europe was well documented at the beginning of the twentieth century, first by British naturalists and then by scientists in other countries. It was observed that the main vector of introduction was the oyster, first Crassostrea virginica (from USA to Europe), then the European native oyster Ostrea edulis (from England to other European countries), and also the Japanese oyster Crassostrea gigas which was imported all over the world from USA and Japan to European shores (Blanchard, 1997).
The consumption of the native oyster (Ostrea edulis) became fashionable in London in the middle of the nineteenth century, to the point where stocks rapidly decreased. To face the growing demand, some fishmongers decided to import American oysters (Crassostrea virginica). Fresh oysters were delivered in barrels and to stored in bays (such as Liverpool Bay and the Thames estuary) before being sold. This trade went on until the 1920s (Cole, 1952; Utting and Spencer, 1992; Minchin et al., 1995). These American oysters originated from areas (probably Long Island Sound, following Hoagland (1985)) where C. fornicata was also present. The imported oysters carried limpets fixed on their shells and although many of the introduced limpet populations died some of them survived and developed in their new environment.
The first live animals were found in the south of Liverpool Bay by naturalists (McMillan, 1938). “Crepidula fornicata has been found amongst the shells of Ostrea virginica (Gmelin) of which, vast numbers were planted (apparently in vain) on the shore near Beaumaris” said Darbishire in 1886. Some years later, others were then observed on the eastern coast of England and in the Thames estuary (Crouch, 1893; Cole, 1915). A population progressively developed in the rivers Blackwater and Crouch, which became the centre of future spread in England. The larval pelagic phase of the species was also one of the causes of spread and can partly explain species observations along the southern coasts of the North Sea, coming from the Thames estuary and spreading northwards towards Belgium, The Netherlands, Germany and Denmark.
A second step in introduction was observed during the Second World War with the landing in Normandy, on D-Day, of thousands of vessels and floating landing stages. These vessels were stored for several months or even years in the Thames estuary and harbours along the Channel, especially in the Severn which was highly colonized by C. fornicata. Immediately after the war, limpet populations were observed at the landing places (Arromanches) and the harbours of Cherbourg and Brest where allied boats had been waiting to discharge their cargos at the end of the war. These boats had come from the USA (Boston or Baltimore) or northern Europe.
The last introduction of C. fornicata took place during the development of the Japanese oyster (Crassostrea gigas) industry, during the 1970s. The Portuguese oyster (Ostrea angulata) had recently been introduced for aquaculture but had been attacked by a virus at the end of the 1960s. To meet the general decrease in stocks, the introduction of a new species (already tested by several oyster farmers) was decided upon. Tons of oyster spats and adult populations of C. gigas were rapidly introduced from the USA and Japan, and along with them many parasites and alien species. The worldwide introduction of the Japanese oyster is known to be one of the great ecological disasters (Zibrowius, 1991). It is generally now accepted and proven by molecular analyses that O. angulata is a synonym of C. gigas.
Once it was introduced into each oyster pond, population centers developed progressively and C. fornicata became a problem not only in the European oysterbeds, but also outside of them. Dredging and trawling along the oyster beds dispersed the populations in throughout the area. It was demonstrated that in the dredged areas, C. fornicata became much more developed that in areas were this activity was prohibited or limited (Blanchard, 1997). Forty years after this massive introduction, fishery practices have dispersed C. fornicata to many of the bays and estuaries in Europe. Estimations of stocks often give thousands of fresh tons per km-2.
The risk of introductions in new areas is very likely, because no real control can be set on such a marine species which is capabale of larval transport. Moreover, naval traffic is increasing so that feasability of accidental transport is real on hulls or in tank waters; fishery pressure by dredging is also increasing along the coasts. Global warming may also favour the spread of this species from temperate areas to further northwards. Coasts of the northern countries, such as in the Baltic sea or Ireland, could be colonized in the future.
Few publications focus on the natural habitat of C. fornicata (McGee and Target, 1989; Shenk, 1986). The habitat of the C. fornicata is varied but is preferred as: a depth between 0 and 15 metres, a bay or estuary protected from direct flow and water agitation, a flat sandy and gravelly ground with shells (empty or not), and a lack of specific predators. Several publications have noted that this typical habitat is similar to that of most oyster species (Hoagland, 1977).
Dupont et al. (2003) conclude from molecular genetic data that the French populations of C. fornicata established after 1940, and derive from several genetically diverse source populations, either in Europe or in North America.
The protandric status of the species and the fact that individuals are fixed in the same colony, are a reproduction warranty (Dupont et al., 2006). Each female lays between 10 and 20,000 eggs at each time and can have 3 or 4 laying periods in a year (Richard et al., 2006). The eggs are protected in bags during 3 weeks until they become strong larvae which are delivered in the plankton where they stay and grow for 1 month, depending on the water temperature and the available food (Pechenik and Lima, 1984; Pechenik et al., 2002). They grow from 400 to 1000 µm during this period, then they metamorphose and fall on the bottom to look for a suitable grounds (especially shells, but also gravel or anything rather flat and smooth).
Physiology and Phenology
This species is ubiquistous which allows it to develop in all kinds of environmental conditions, even brackish waters. The flow is created by the cilia movement in the mantle cavity, so that the water enters on a side, then through the gills, where particles are trapped, and goes out on the opposite side (Newell and Kofoed, 1977). When the turbidity level rises or when the water quality is no longer suitable, the filtering rate decreases, although the species is able to survive in poor conditions.
This suspension-feeding species eats phytoplanckton during both the pelagic larval phase and as an adult. During the adult phase, C. fornicata filters at about the same rate as other filter feeding molluscs (Newell and Kofoed, 1977), but the quality of the particles (size and composition) can be extremely varied (detritic particulate matter, pure phytoplankton, dissolved matter). Also a large range of size in phytoplankton seems to be eaten by the larva. Blanchard et al. (2008) have compared the growth conditions of oyster and C. fornicata larvae under several food conditions and the latter is obviously less selective in cell size.
In the USA, the large whelk Busicon carita is known predator of shellfish. The decapode Pagurus pollicaris eats the juveniles (Shenck, 1986), the sponge Cliona celata and the gastropod Ocenebra erinacea pierce the shells (Orton, 1924) as does the driller Urosalpinx cinerea (Pratt, 1974). The flatfish Pleuronectes limanda [Limanda limanda] (Orton, 1924) and the bass Dicentrarchus labrax (Kelley, 1987) eat and scratch large quantities of adult animals. The starfish, Asterias rubens eat individuals (Orton, 1924). Several carnivorous crabs are observed when limpets are scratched and meat exposed, after dredging for example.
No use of natural enemies is carried out in the field to control C. fornicata. The highest densities of C. fornicata are in oyster ponds where it is dangerous for shellfisheries to introduce enemies which are not species specific.
The species is generally fixed, so adults are dispersed on the sea bottom individually or as stacks with current during the periods of high wave energy. Crepidula fixed on wood or floating vessels can be carried far from their native areas, as it is mentioned for the first observation in Belgium (Polk, 1962) or Greece (Galil and Zenetos, 2002).
Oyster-farming practices with exchanges of spat or adult batches is the main cause of the C. fornicata introduction in European oyster beds. In addition, fishery practices of throwing overboard all the non-valuable species, especially with C. fornicata, for several decades, is the main cause of dispersal around the shellfish areas (Hamon et al., 2002).
When the population is dense, the ground cover can reach densities of up to 10,000 individuals/m-2 as in the bays of Brittany (Blanchard, 2009), and severe and irreversible impacts can occur on the sediment, on the biodiversity or on the concentration of suspensed matter. Only dense populations have a real impact.
The activities which have fallen victim to C. fornicata such as dredging or trawling, and shellfish-farming especially oysterfarming, are those which, for less than a hundred years, contributed, accidentally or not, to its spread. Dense limpet populations disturb fishery or oyster farming activities to such an extent that in some bays (Sheldt estuaries in Zeeland, Thames estuary and Fal River (Fitzgerald, 2007) in Great Britain, the Norman gulf or the Atlantic Marennes pond in France, cleaning operations are necessary. Regularly, oyster grounds must be cleaned before sowing new seed or when the C. fornicata populations create a too large negative effect. When limpets are fixed on oysters, oyster farmers must pick off limpets before selling the products, which creates an extra economic burden (Blanchard, 1997).
Expensive treatment methods have been developed, often without success. Public spending is constantly increasing. Yet applying the regulations or laws at the earliest observations would suffice to halt this spread. We are now observing in dense areas, the consequences of insufficient surveillance and precautions during the importation period.
C. fornicata is a suspension feeder filtering about 1 litre h-1g-1. For a dense population of several thousands of individuals, the diversion of tons of phytoplankton and organic matter can have an impact on the available concentration and a trophic competition can occur with the other suspension-feeders. It seems that in most areas, no mortality is observed in other species due to lack of food. Only during some periods of the year, when the food level is low, signs of slower growth can be observed in the other species (de Montaudouin and Sauriau, 1999; Decottignies et al., 2007a, b). Competition can also occur for larvae, because the limpet larvae have a high feeding rate, but Blanchard et al. (2008) observe that oyster and limpet larvae generally eat different kinds of food.
C. fornicata stacks, when numerous in densely colonized areas, prevent other larvae and juveniles from settling and spatial competition occurs. Most species shift into other areas but many other of epifaunal species decrease in number or disappear because of available ground surfaces (Blanchard, 2009). For the flat fish Solea solea, Le Pape and al. (2004) demonstrated that the spatial competition which occurs between the fish and the C. fornicata favours the latter.
Impact on Habitats
Dense populations spread and completely cover the ground, so that the sediment disappears under the stacks and has no more exchange with the water. By trapping the suspended matter and producing lots of mucous pseudofaeces, a dense population transforms the primary sandy sediment into a muddy one with a high organic content, which becomes rapidly anoxic and unsuitable for other species. Empty shells are trapped in this mud and the sediment becomes more compact. The levels of bottom sediment rise by firstly, disturbing the normal flow, the limpet population stops the finer particles in the suspended matter which is trapped; secondly, the large biodeposited matters of such populations stay in place and are not scattered by streams. The bottom then accumulates several centimeters of mud each year where dead shells are included.
When the original ground is a nursery for commercial fishes, the complete occupation of the area means the disappearance of the fish which has economical consequences (Le Pape et al., 2004). In some bays where natural mud deposition is observed, presence of dense colonized limpet populations reinforces the ground modifications (Ehrhold et al., 1998). Above 50% coverage, return to the previous situation becomes no longer possible (Blanchard, 2009).
Impact on Biodiversity
With a growing limpet community the ground is progressively covered, the original endofauna disappears often completely when new epifauna increases on the stacks and in the interstices. A new limpet community appears with lot of suspension-feeders (bryozoans, ascidians, fixed annelids and cirripeds) and several little carnivorous species of crustaceans in the interstices. The biodiversity seems to have decreased, if we consider the large scale of a bay, but at a local scale, the number of species is rather the same (de Montaudouin and Sauriau, 1999).
Thirty species of Crepidula can be found over the world, but only some can be confused with C. fornicata, the others being of different size, colour, ornementations (lines, spots) or shape. Generally, phenoplasticity is common in the genus Crepidula, so care must be taken as C. fornicata can be present in different forms depending of the shape of the support, and can be extremely flat or completely rolled up around a stone.
New industrial uses of this product, either the meat or the shell, should be investigated. Up to now, the different uses found in the literature are not satisfactory: the shell is used generally as calcareous improvement and the meat is often used for poultry. The chemical or the pharmacological industries have to look into this product to find new openings.
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