Mytilicola intestinalis (mussel red worm)

Mytilicola intestinalis is a parasitic copepod that occurs in the intestinal tract of various species of bivalves. This parasite was first described in mussels (Mytilus galloprovincialis) from the Gulf of Trieste, Adriatic Sea (Steuer, 1902; 1905) and then in this mussel as well as a related species (Mytilus edulis) from another location in the Mediterranean Sea (Cheng, 1967). It was subsequently reported in mussels from the North Sea (Germany) and England during the mid to late 1930s and first recorded in mussels from the Netherlands in 1949 (Korringa, 1951; Bol, 2002), from Ireland in 1948 (Grainger, 1951) and from Denmark in 1964 (Jensen and Knudsen, 2005). Although Lauckner (1983) surmised from various reports that M. intestinalis could have originally occurred in the Mediterranean Sea and subsequently spread to the North Sea, the north-westward migration of M. intestinalis is not well substantiated. Nevertheless, Streftaris et al. (2005) list M. intestinalis as a non-indigenous species in the Atlantic. Distribution along the west coast of Europe is patchy with a high prevalence in some locations (up to 100%) and no detectable presence in others (Lauckner, 1983). A patchy distribution was also noted from several sites around Italy where M. intestinalis was detected in mussels from only two of seven locations (Trotti et al., 1998). To date, it has been reported beyond the Mediterranean Sea and the west coast of Europe on only one occasion, in the unusual circumstance of being found in a plankton sample in the Indian Ocean-Malacca Strait area 67 nautical miles from the nearest shore (Wickstead, 1960).

Mytilicola intestinalis is a cycloid copepod that inhabits the intestinal tract of its mollusc host. The body of adult M. intestinalis is usually red in colour, cylindrical and elongated; it has thoracic segments with paired processes and the segmentation of the abdomen is incomplete. The male becomes sexually mature at about 2.8 mm in length and can grow to a maximum length of 4.5 mm. The female becomes sexually mature at about 4.6 mm in length, reaches a maximum length of about 9.0 mm and in addition can have paired egg sacs attached to the genital segment located posterior to the thorax and possibly extending beyond the posterior end of the abdomen. Female M. intestinalis in young mussels (between 10 mm and 35 mm in length) were significantly shorter in length than those from adult mussels, possibly because of the smaller dimensions of the intestine in small mussels (Williams, 1967).

The head of M. intestinalis carries a median red eye spot, the first pair of antennae has four segments and the second has three. The second antennae are modified as a pair of stout hooks that are used as anchors for resisting expulsion from the host. There is an overall reduction in the length and complexity of the appendages in comparison to free-living copepods. The loss of complexity is greatest in the mouthparts where the mandibles are entirely lacking and maxillulae, maxillae and maxilipeds are extremely simplified (Hockley, 1951). Juvenile stages of M. intestinalis (Copepodite II to V) and sexually immature preadult stages, all less than about 2.5 mm in length, also inhabit the intestinal tract of the host. Orlando (1973) demonstrated that M. intestinalis has sex chromosome heteromorphism.

Factors that may determine infestation rates and spread of Mytilicola intestinalis include host population density, the amount of flushing in the water column, wave action, current speed, turbulence, salinity, depth of water, and location within an estuary (Davey and Gee, 1976; Rohde, 1993; Robledo et al. 1994b). Hosts from lower shore levels and from sheltered areas are invariably more heavily infested than individuals from higher-shore levels and exposed localities (Lauckner, 1983). Fuentes et al. (1995) found that the prevalence of M. intestinalis in mussels (M. galloprovincialis) cultured in the Ría de Arousa (Galicia, NW Spain) was not affected by any of the 3 factors investigated, namely location in the ría, mussel stock deployed and situation within the raft.

Spreading into new areas by this parasite mainly occurs as a result of transportation of infected mussels on the bottom of ships making mussels in the vicinity of ports more likely to be infested than mussels for other areas (Rohde, 1993). An unusual record of M. intestinalis was published by Wickstead (1960) who found two adult female specimens of M. intestinalis in a surface plankton sample in the Indian Ocean-Malacca Strait area at a location 67 nautical miles from the nearest shore in water 951 metres deep. Although various reasons for finding intestinal parasites of European bivalves at this location in the water column were discussed (including the possibility of infected bivalves attached to the hull of the ship), Wickstead (1960) could not explain the phenomenon.

The introduction of Mytilicola intestinalis from an origin in the Mediterranean Sea to the Atlantic coast of Europe is not well substantiated (Lauckner, 1983). Nevertheless, records of first reports in various European countries give the impression of the spread of this parasite. Specifically, it was first described during the early 1900s in mussels in the Mediterranean Sea (Steuer, 1902, 1905). It was subsequently reported in mussels from Germany and England during the mid to late 1930s and first recorded in mussels from the Netherlands in 1949 (Korringa, 1951; Bol, 2002), from Ireland in 1948 (Grainger, 1951) and from Denmark in 1964 (Jensen and Knudsen, 2005). Also, Minchin (1996) and Streftaris et al. (2005) list M. intestinalis as a non-indigenous species in the Atlantic. Despite the extensive transplantation of economically important bivalves from Europe to other parts of the world, M. intestinalis has apparently not become established beyond the Mediterranean Sea and Atlantic coast of Europe.

The risk of introduction lies in transplanting infested bivalves from one location to another. Because M. intestinalis is not capable of leaving one host for another, it can only be spread if the infested bivalve harbours fecund adult females. Also, the environment into which the nauplius larvae emerge must be suitable for the development of the subsequent free-living stages and suitable bivalve hosts must occur in the vicinity to take up the first copepodite stage. Although this combination of circumstances may occur in some shipping ports (i.e. M. intestinalis in molluscs fouling ship hulls) or sea-side shellfish markets, M. intestinalis has not yet been reported outside of the geographic range identified in the mid 1960s. Currently, the greatest risk of introduction is associated with the bivalve aquaculture industry during transplantation and transportation of seed and farmed stocks. However, the risk can be significantly reduced by the implementation of regulations that prohibit the movement of infested bivalves.

Mytilus galloprovincialis and Mytilus edulis are believed to be the primary hosts for Mytilicola intestinalis. However, other bivalves are known to be infested including Ostrea edulis, Crassostrea gigas, Cerastoderma (=Cardium) edule, Tapes decussatus (Ruditapes decussatus), Paphia decussata (a synonym of R. decussatus?), and in the laboratory Paphia pullastra (Venerupis senegalensis?) and the gastropod Crepidula fornicata, but the intensity of infection is usually low (Baird et al., 1951; Hepper, 1953; Hepper, 1956; Dare, 1982; Carballal et al. 2001). Cheng (1967) indicated that the gastropods Zizyphinus zizyphinus, Gibbula cineraria, and Gibbula varia were also known natural hosts of M. intestinalis. Hepper (1956) stated that M. intestinalis does not readily infest O. edulis in the presence of mussels and is unlikely to become epidemic in oysters. Thus, Cheng (1967) concluded that M. intestinalis prefers mussels but if they are not available, it will parasitize O. edulis. Results of field exposure experiments by Dare (1982) confirmed that the oyster juveniles (seed) of O. edulis and Crassostrea gigas could be infested by M. intestinalis but C. gigas was far less susceptible than O. edulis. From these experiments, Dare (1982) concluded that the risk of moving M. intestinalis to new areas through the transportation of C. gigas juveniles less than 25 mm in shell length was negligible and O. edulis should be regarded as a potential vector for this parasite, although the risk is likely to be slight with juveniles less than 15 mm in shell length.

Parasite burden tends to increase with host size but this correlation is unlikely to represent an accumulation of parasites with increased host age because of the short life span of M. intestinalis (Davey and Gee 1976). Larger hosts accumulate more parasites as a result of a higher filtration rate in larger bivalves (Davey and Gee 1976; Paul 1983).   The relatively recent inadvertent introduction into European waters of a related bivalve intestinal parasite, Mytilicola orientalis, is a concern because it infests native oysters and mussels that are important fisheries resources in Europe. This introduction warrants cautious observation for potential synergy resulting in disease consequences for bivalve hosts (Stock 1993).

Very few natural enemies are known for Mytilicola intestinalis. A microsporean hyperparasite has been reported from 20% of M. intestinalis from mussels on the Spanish Mediterranean coast but its effect on M. intestinalis populations is not known (Lauckner, 1983). Also, biotic interference with other parasites could exist. For example, mussels showing a decline in condition due to heavy Polydora invasion are usually infected with fewer M. intestinalis (Lauckner, 1983, citing work of Williams 1968). The most significant control on M. intestinalis populations may be the survival of the planktonic larvae, the ability of the infective stage to find a suitable host and density-dependent factors within the host (Davey et al. 1978).

None reported in the past 20 years.