Mytilicola intestinalis, Steuer, 1902 – Red worm
disease?
Synonyms
None known.
Common names
The condition caused by this parasitic copepod is
known as “red worm disease”; Le copepod rouge (FR).
Identification
This is a parasitic copepod
living in the intestine of bivalves, in particular mussels, but also oysters. It
has a characteristic red color, which makes it very conspicuous inside the host.
Adults have elongate (“worm-like”) bodies with very short appendages. Cephalic
appendages, including mouthparts have been described and illustrated (Hockley,
1951). Females are larger than males, 9 mm against 4.5 mm (Gee & Davey, 1986).
The paired external egg-sacs of the females are also red. Adult copepods are
found in the posterior part of the intestine of the mussel whereas the
copepodite stages are found in the stomach digestive gland, and anterior part of
the intestine (Gresty, 1992).
Mytilicola intestinalis, male and ovigerous female (from Hockley 1951)
Similar species: Mytilicola
orientalis, 1935 (syn: Mytilicola ostreae, Wilson, 1938), NON
Myicola ostreae (Hoshina & Sugiura, 1953) (=Mytilicola ostreae
Hoshina & Suguira, 1953). The latter species parasitizes gills rather than
intestine of bivalves. Both species are found in European countries, often
associated with the introduced Pacific oyster, Crassostrea gigas
(Thunberg, 1793). More species of similar parasitic copepods from mussels and
oysters have been described from the Pacific Ocean (see e.g.
http://www.pac.dfo-mpo.gc.ca/science/species-especes/shellfish-coquillages/diseases-maladies/pages/pcgmu-eng.htm).
Distribution
Native area
Most likely the Mediterranean where it was first described from Mytilus
galloprovincialis Lamarck, 1818 in the Adriatic Sea. In 1914 it was found in
Mytilus edulis Linnaeus, 1758 in the Mediterranean (Bolster, 1954).
Introduced area
In 1937 a single specimen was found in Mytilus edulis at Portsmouth in
southern England, but it was not until 1951 that this was published, and 1947 is
usually listed as the first date (Campbell, 1970). In 1938 it was found in the
German Wadden Sea (Bolster, 1954). M. intestinalis was first found in the
Limfjord in 1964 (Theisen, 1964, 1966) and only in 1994 were the first infected
mussels found in the Danish Wadden Sea (Theisen, pers comm.). The first record
from the French Atlantic coast was from 1949 (Goulletquer et al., 2002). In the
Netherlands the first observations were also from 1949 (Wolff, 2005), and in
Belgium from 1950 (Kerckhof et al., 2007). In Ireland the first record was from
1948 (Minchin, 2007). It has not yet been found in Norway or Sweden (Hopkins,
2001; Främmande arter, alert list). Nor has it been found in Poland, Lithuania,
Latvia, Estonia or Finland.
There is an old record of this
species from the Malacca Strait, Indian Ocean (Wickstead, 1960), but there are
no records of the species since then, so this record must be considered dubious.
Vector
Probably infected mussels transported as fouling on ships' hulls or infected
mussels transferred for aquaculture (Hockley, 1951; Theisen, 1966; Korringa,
1968). Secondary dispersal through free swimming larvae seems unlikely as the
actively swimming stages last only a few days (Hockley, 1951).
Ecology
Most of the information available
is on prevalence and effects of the parasite on the host animals, and very
little information is available about the ecology of the parasite. Mytilicola
intestinalis in Mytilus galloprovincialis seems fairly rare in the
Aegean Sea, infecting about 11% of the mussels with 1-4 individuals per mussel (Rayyan
et al., 2004). However, these were mussels cultured on hanging ropes, which are
less prone to infection by this parasite (Theisen, 1987). It also seems rare in
M. galloprovincialis from Italy whereas almost 60% of the M.
galloprovincialis imported to Italy from Spain were infected (Trotti et al.,
1998), and even higher infection rates were recorded from cultured mussels from
the Spanish Atlantic coast (Fuentes et al., 1995).
The effect on Mytilus edulis
depends on the number of parasites, but even the presence of one copepod may
cause visible effects (Korringa, 1968), but see also below for impacts. The
highest number of parasites are found in large sized mussels. This has been
attributed to higher filtration rates rather than age (Williams, 1967; Paul,
1983), though this has also been contested (Davey, 1989). In most places
relatively low numbers (1-10 individuals) of parasites are found (Grainger,
1951; Williams, 1969; Theisen, 1987). Mussels in beds on the bottom are more
heavily infected than mussels on vertical surfaces away from the bottom (Korringa,
1968). The smallest mussel infected was about 10 mm long (Williams, 1967). Fewer
parasitic copepods are found in mussels infected by the shell-boring polychaete
Polydora ciliata (Johnston, 1838) (Williams, 1968). Adult females have
almost the same diameter as the intestine of the host, but a groove formed by
appendages on the dorsal side permits the flow of food to pass, the copepod only
picking up enough for its own nutrition (Hockley, 1951). What constitutes the
diet of M. intestinalis has been discussed, but it seems certain that it
does not include mussel tissues (Davey, 1989; Gresty, 1992). If an adult
parasite is expelled it is not able to move enough to find a new host (Grainger,
1951).
Mytilicola intestinalis
is able to tolerate a wide range of temperatures, at least between -1.4° and 30°
C, and also is extremely euryhaline (Korringa, 1968).
Reproduction
Fertilization is assumed to take place within the host
(Grainger, 1951), and sex ratio is always skewed towards males (Hockley, 1951;
Theisen, 1966). It has been claimed that it needs at least 18° C to initiate
reproduction (Williams, 1969), but may continue as long as the temperature
remains above 6° C (Bolster, 1954), though this has been contested (Koringa,
1968; Davey, 1989). There seems to be two annual spawning periods (Williams,
1969; Davey et al., 1978), but in northern European waters the winter spawning
(December – February) may not be successful in infecting new hosts (Williams,
1969). Mytilicola intestinalis produces 200-300 eggs (Thieltges et al.,
2008). Eggs detached and grown in the laboratory hatched after 7 days at 18° C
(Hockley, 1951). There are a nauplius and a metanauplius larval stages, which
are free-swimming. The infective stage is the first copepodite, and there are 5
successive copepodite stages before it reaches the immature adult stage (Gee &
Davey, 1986). The nauplius is positively phototropic. Some copepodite I
specimens have positive phototaxis, others negative (Grainger, 1951), and this
stage is only free swimming for 3-4 days after which it moves to the bottom to
search for a host (Campbell, 1970). Development from release of nauplius to
copepodite I is about 2 days at 13-14° C. The free swimming larvae have poorly
developed mouth parts and may not need to feed. The copepodite II is reached
after about 12 days and copepodite III after 15-20 days (Grainger, 1951), though
the infective copepodite I may survive longer if a host is not found (Gee &
Davey, 1986).
Impact
The physical impact to mussel
tissues is caused by the copepod moving about and scraping the intestinal
epithelium and scar tissue formation (Moore et al., 1977). However, there is
considerable controversy about the seriousness of this parasite. Coincidence of
outbreaks of M. intestinalis and mass mortality in mussel beds have
caused some authors to blame the parasite for the economic losses (Korringa,
1968; Blateau et al., 1992). Other studies have shown little or no effects on
the meat content (“condition”) of the mussels (Dethlefsen, 1975; Paul, 1983;
Davey, 1989). Some studies have found that high numbers M. intestinalis
caused decreased condition of mussels, but only under certain circumstances (Gee
et al., 1977). Densities of more than 10 copepods per mussel may render the
mussels unmarketable due to low condition. Apparently only mussels close to or
on the bottom are infected (Korringa, 1968; Theisen, 1987). Hence long-line
culture should not be affected, as long as spat is not transferred from infected
mussel beds. Low rates of infestation have been found in line cultures in German
waters (Buck et al. 2005) and high rates of infection has been found in Spain
(Paul, 1983; Fuentes et al., 1995), where part of the seed mussels came from
intertidal beds. Other effects on the mussel host include retarded spawning,
reduced shell growth, decreased filtration rate, and weakened byssus attachment,
although most of these serious effects were only found in early studies and
could not be confirmed in more recent studies (Bayne et al., 1978; Davey, 1989).
Whether this is due to inappropriate procedures or faulty observations in the
early studies, or whether the mussels have actually adapted to the parasite over
time is unknown (Gresty, 1992).
M. intestinalis
may also infect oysters, and the native European flat oyster, Ostrea edulis
Linnaeus, 1758, seems to be more susceptible to infection than Pacific oyster,
Crassostrea gigas (Dare, 1982), and although they are not heavily
infected, transport of live seed oysters may transfer the parasite to new areas.
Management
Mytilicola intestinalis
has been declared a “controlled pest” in the U.K., which means that transport of
mussels from areas infected is carefully monitored (Gresty, 1992). Decreasing
stocking density in mussel farms may decrease the problem (Blateau et al.,
1992), and in France mussel farmers have created a union which works for
voluntary decreasing stocking density to prevent outbreaks of this parasite (Mongruel
& Thébaud, 2006). Also, various pesticides have been tested as curative
treatment for this parasite (Blateau et al., 1992), but this is highly toxic to
a number of aquatic organisms. Free swimming stages can be killed by chlorine (Korringa,
1968). Probably the most efficient measure is control of transfer of live
mussels from infected areas.
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