Mytilicola intestinalis - Red worm disease
SCIENTIFIC NAME
Mytilicola intestinalis Steuer, 1902
1951 - 1970
Mediterranean Sea
Aquaculture - importing live animals
Shipping (hull fouling)
In 1902, this parasite was described based on specimens found in deep-sea mussels from the Adriatic Sea (the sea between Italy and Croatia) [2]. Therefore, the Mediterranean area is considered the area of origin of Mytilicola intestinalis [3].
It has been suggested that this parasite occurs naturally in Northern Europe but hasn't been noticed before because of its low infection rate [4].
First observation in Belgium
In August 1950, Belgian mussel farmers discovered the red worm disease for the first time in Mytilus edulis mussels, imported from the Netherlands into the Sluice Dock of Ostend. In the months that followed, it appeared that this parasite already existed along the entire Belgian east coast – from Ostend to the Belgian-Dutch border [5].
Spreading in Belgium
During inspections of mussels collected from groynes and harbour piers along the entire Belgian coast between 1950 and 1958, Mytilicola intestinalis was found mainly along the east coast. Northeast of the port of Zeebrugge, the population increased steadily during this period. By 1958, 28% (locally up to 66%) of the mussels got infected by this parasite (compared to only 4-8% in 1950). To the west of the port, the parasite appeared to be much less prevalent (around 10% by 1958) and to the west of Ostend, it was almost non-existent. This distribution would be mainly due to the prevailing eastward sea currents. The dike of the port of Zeebrugge acts as a barrier to the further westward spread of this parasite [6].
In 1971, Mytilicola intestinalis was once again reported in the Sluice Dock of Ostend. In October 1971, more than 24% of the mussels were found to be infected [7]. Although recent information is lacking, this parasite is probably still present along our coast, but people just don’t pay attention to it [8, 9]. Moreover, the related species Mytilicola orientalis is also likely to infect mussels along the Belgian coast [10].
Spreading in neighbouring countries
In contrast with the Mediterranean Sea where Mytilicola intestinalis occurs within the Mediterranean mussel Mytilus galloprovincialis, mostly edible blue mussels Mytilus edulis are infected in Northern Europe.
The first observation of this parasite outside of the Mediterranean Sea was in a mussel from Portsmouth (UK), in 1937 [11]. However, it did not stop there. In 1938, infected mussels were found near Cuxhaven and East Frisia, located in the German Wadden Sea [4]. From here, the north-eastern coast of the North Sea was colonised in northern (towards Denmark) and south-western (towards the Netherlands) directions [12]. Subsequently, the species was reported in Ireland (1948) [13], the French Atlantic coast (Normandy, 1949) [14], the Netherlands (Zandkreek, 1949) [15] and Northwest Denmark (Limfjord, 1964) [11].
After its introduction in Northern Europe, Mytilicola intestinalis grew to epidemic proportions within the mussel population in the 1950s. Today – more than 50 years later – this parasite is still widespread in the North Sea region [16]. In Europe, this species occurs from Denmark to Italy, including the United Kingdom and Ireland, but not in the Baltic Sea [17]. Today, the species isn’t a problem for mussel farming anymore [18], although in England and Spain – where up to 80% of the mussels are infected in some places – the non-native species is still abundant [19].
Meanwhile, with the help of molecular techniques, a cryptically related species, namely Mytilicola orientalis [10], has been commonly identified in the Netherlands (Delta area and the Wadden Sea). Mytilicola orientalis was introduced together with Japanese oysters Crassostrea gigas in France in the 1970s and appeared in the southern North Sea in the 1990s. Mytilicola orientalis infects, besides the blue mussel Mytilus edulis, also the Japanese oyster Crassostrea gigas. Observations are hampered by the fact that the males are only genetically distinguishable from each other and morphologically identical.
Mytilicola intestinalis was probably transported from the Mediterranean with infected mussels for aquaculture or with mussels attached to the hulls of ships [3]. After its introduction in the North Sea near the German Wilhelmshaven and Cuxhaven [20] in 1938, the species spread in two directions: towards the north (Denmark) and southwest (see above) [12].
Mytilicola intestinalis is a parasite of mussels, including the Mediterranean mussel Mytilus galloprovincialis and the edible blue mussel Mytilus edulis [4]. Along the Belgian coastline, which is rich in mussels, this parasite can find many suitable hosts [3].
In contrast to other parasites, Mytilicola intestinalis only produces a relatively small number of offspring (about 300 eggs per cycle). The larvae of this parasite swim freely for a few days, which allows a limited active distribution [3]. Given that a successful reproduction requires both male and female parasites to be present in the same mussel, the infection rate of mussel populations is limited. When a low amount of mussels is infected, there will be few mussels in which both sexes are present at the same time [4].
Mussels need a solid substrate to settle. Mussels that occur at the bottom of shallow waters near the coast appear to have a higher infection rate than mussels attached to piers, ropes or in hanging cultures. Presumably, this has something to do with the tendency of Mytilicola intestinalis to swim to the bottom – away from the light – in search of hosts
Mytilicola intestinalis tolerates a wide range of temperatures, from -1.4 to 30°C [3]. Nonetheless, the water temperature does influence the reproductive cycle of this copepod. In northern Europe, an increase in water temperature leads to a population increase from March to September, while this seasonality is absent in the Mediterranean [4].
The broad salt tolerance of this parasite is demonstrated by its occurrence in both brackish estuaries (5 PSU) and the open sea (35 PSU) [3], although it seems to have a harder time infecting mussels in estuaries [22]
Initially, it was thought that this parasite was responsible for the massive death of mussels and the subsequent disturbance of the mussel industry in the Netherlands (1949) and Germany (1950). In France, high mussel mortality was observed between 1965 and 1970 and in 1982, also because of infection with Mytilicola intestinalis. The mussel farmers saw their yield go from 10,000 tons (1981) to 4,000 tons (1984) in just 3 years [23]. It was suspected that the parasite hampered the filtering capacity and food intake of the mussels, thereby negatively influencing their growth rate and body weight [23]. Because infected mussels use more energy, the parasite could lead to massive mussel mortality in extreme conditions [4].
However, this statement was controversial. It could not be ruled out that other pathogens or adverse environmental conditions were responsible for the high mussel mortality instead [24]. More recently, it was demonstrated that this parasite only feeds on material that is not consumed by the mussel itself. Thus, only unnecessary nutrients are used by the parasite [4]. It is still not clear if Mytilicola intestinalis has a (strong) negative effect on the body weight of the infected mussel [25]. However, attachment of the parasite may irritate and damage the mussel's intestines [19]. Other indirect effects cannot be excluded either. The parasite may make the mussel more susceptible to (other) pathogens, parasitic infections or toxic substances [4].
Control on the introduction of shellfish into non-infected areas may be the most effective measure to prevent infections by Mytilicola intestinalis [26]. In addition, the degree of infection can be reduced by keeping the density of mussels low during breeding [27]. Mussels growing on poles and ropes in fast-flowing water, the open sea or brackish water appear to be less affected by this parasite [4, 21]. Treatment of the mussels with insecticides turned out the be effective in experimental settings but is not recommended in-situ because of their toxicity to other (non-hazardous) marine organisms and the environment [23].
Oysters can also get infected by the red worm disease, but the percentage remains negligibly low and, so far, no negative effects have been observed [27]. The presence of this parasite in the digestive system of mussels does not pose a threat to the consumer [17]
In mussel dissections, Mytilicola intestinalis is easily recognized by its red colour and worm-like appearance. Because of this, infection by Mytilicola intestinalis is often called the red worm disease, which is a confusing terminology because it is a copepod and not a worm.
Adults have short paired protrusions on their dorsal side. The head possesses one red eyespot and three pairs of antennae. The second pair of antennae can act as an anchor due to their hook-like shape and prevent the parasite from being pushed out of the digestive system by the host [28].
Female individuals are, with a maximum length of 9 mm, about twice as big as male individuals. Females have two external egg pockets that are attached to the back of their body and are also coloured red [29] (Figure 1).
Due to its parasitic lifestyle, the morphology of Mytilicola intestinalis has undergone evolutionary simplifications. This species is much smaller than other free-living copepods and has reduced mouthparts [28].
Figure 1: Left - male, Right - egg-bearing female [28].
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