Bonamia ostreae -

Initially, bonamiasis occurred only in California. The parasite responsible for this infection, namely Bonamia ostreae, was exported with the transport of oysters to some other states of the U.S. (Washington and Maine), Canada (British Columbia) and Europe ^[2].

First observation in Belgium

After 1979, this parasite spread along the Belgian coast and in the Sluice Dock of Ostend ^[3]. The precise date of the first Belgian sighting is unknown. It is thought that the parasite spread rapidly throughout Europe – after the first sightings in France in 1979 – via the transport of oysters between oyster farms. After the first attempt (in 1934-1974) to set up an integral culture of flat oysters Ostrea edulis in the Sluice Dock of Ostend was stopped due to poor water quality ^{[4, 5]}, a new attempt was made in 1996. According to European guidelines, it is forbidden to introduce infected oysters into an area, if it cannot be proven whether or not the new breeding site is infected with Bonamia (as was the case for the Sluice Dock) ^[6]. Since 1979, Bonamia has been widespread in European oyster farms ^[7]. No European country could guarantee that their oysters were Bonamia-free, so they had to import certified Bonamia-free flat oysters from Canada ^[6]. However, due to a European import ban on Canadian oysters, they were soon obliged to use flat oysters from Europe ^[8]. The hope of avoiding the introduction of the parasite in the Sluice Dock turned out to be in vain: the Sluice Dock of Ostend got affected by the parasite in 1998-1999 ^[6].

Spreading in Belgium

An investigation into the presence of Bonamia ostreae in the Sluice Dock of Ostend in 2008 – carried out by the (then) national reference laboratory for bacteriological and viral contamination of bivalve molluscs, on behalf of the FASFC – turned out positive ^[9]. There is no recent data on the current infection rate in the Sluice Dock and/or the Belgian coastal zone ^[10].

Spreading in neighbouring countries

In June 1979, Bonamia ostreae was reported in cultivated flat oysters in the Île-Tudy (Southern Brittany, France) ^[11]. This was the first report of the parasite in Europe. Shortly afterwards, the presence of the parasite was detected in almost all oyster farms in Brittany ^[12]. Its presence was characterised by a high mortality rate ^[11]. Despite the occurrence of the parasite, flat oysters are still cultivated in this region, albeit with a greatly reduced yield (-90%) ^[13]. The percentage of infected flat oysters varies over the years between 2-37%, with an average of 13% ^[14].

After its introduction to France, the B. ostreae spread rapidly with the transport of cultivated oysters ^[15]. In 1980, B. ostreae was found in Asturias (Spain) ^[16], Denmark ^[15] and the Netherlands. In the Netherlands, the introduction took place in Yerseke (Eastern Scheldt) with oysters originating from France. Strict preventative measures delayed the introduction of B. ostreae into Lake Grevelingen, adjacent to Yerseke until 1998 ^[17]. In the following period (1989-2006), the infection rate during spring in Lake Grevelingen was approximately 15% ^[18].

B. ostreae has been reported in Britain (since 1982) ^[19] and Ireland (since 1987) ^[20]. Today, the parasite is widespread along the European coasts, from Morocco to Denmark ^[21]. The Danish Limfjord region remains free from this parasite ^[22].

Most likely, B. ostreae was introduced to Europe via the import of infected flat oysters from the United States (California) ^[23].

Little is known about the life cycle of B. ostreae ^[13], which makes it difficult to know the exact reasons for its success. How the oysters become infected is unknown ^[13]. However, it is certain that flat oysters can become infected in a region where the parasite occurs ^[24]. Although the parasite is usually found in blood cells (haematocytes), it can occur outside of cells, more specifically around the gills of the oyster. Therefore, it is suspected that the parasite enters the water column via the oyster’s gills and infects nearby oysters (also via the gills) ^[13].

Flat oysters in farms are regularly subjected to stress factors – such as transplantation and storage in basins – which make them extra vulnerable to infection with B. ostreae ^[17]. This could have played a role in the rapid spread of the parasite in Europe.

The transport of flat oysters has brought this parasite to Europe, while secondary transports contributed to the further spread of this exotic species within Europe ^[21]. Initially, it was assumed that only the flat oyster Ostrea edulis could serve as a vector for B. ostreae, but lately, this has been questioned. B. ostreae can survive in the tissues of non-typical hosts such as the Japanese oyster Crassostrea gigas – a species important for oyster cultivation – without causing any damage ^[25-27]. The common mussel Mytilus edulis is also immune to the attacks of this protist ^[21]. The flat oyster is generally less resistant to fluctuations in temperature, salinity or other environmental variables, which can lead to the extinction of an entire population of flat oysters ^[6].

Since the larvae of the flat oyster spend their first 8-10 days inside the oyster’s mantle cavity, they can get infected with bonamiasis when they are still inside an infected ‘mother oyster’. During their planktonic phase, these larvae contribute to the spread of the parasite ^[13].

In addition to the flat oyster, many other species of oyster are also impacted by B. ostreae, e.g. Ostrea angasi, Ostrea chilensis, Ostrea puelchana, Ostrea denselamellos, Crassostrea ariakensis and Crassostrea angulata ^[28]. B. ostreae has also been found in zooplankton samples and tissues of other macroinvertebrates ^[29].

Weakened oysters seem more susceptible to infection ^[18]. Under the future climate scenario, the susceptibility to contamination and/or mortality of flat oysters is likely to increase with the higher seawater temperatures ^[18], lower salt levels ^[18] and lower food availability ^[30]. On the other hand, B. ostreae itself seems to survive more easily at higher salinity (>35 PSU) ^[31]. By way of comparison, the seawater of the North Sea has a salt concentration of approximately 35 PSU.

Once a flat oyster is infected by B. ostreae, the parasite causes inflammation of the gill tissue and degradation of the connective tissue ^[12]. Since B. ostreae also invades blood cells (haematocytes), infection leads to exhaustion of the oyster, which eventually starves and dies ^[32]. The presence of the parasite often leads to the death of the host after two to three years ^[12]. In some populations, mortality is as high as 90% ^[15].

In France, the Netherlands and Belgium, the flat oyster almost disappeared after the introduction of B. ostreae ^[33]. In France, flat oyster production decreased from 20,000 tonnes per year in the 1970s to 1,800 tonnes in 1995 ^[34]. Despite the presence of the parasite, oysters can still be cultivated because bonamiasis only kills oysters older than two years, and flat oysters can already reproduce after one year ^[14].

To prevent the import of contaminated oysters, European guidelines have been published which subject the import of shellfish from infected and non-infected regions to controls ^[15]. In addition, all potential vectors – not just shellfish – should be checked for the presence of B. ostreae before transporting them from contaminated to non-contaminated sites with oyster cultures ^[29].

A great deal of research has been carried out about how to reduce the risk of infection with B. ostreae. A study in Galicia (Spain) showed that oyster cultures at a depth of 1-2 metres, suspended on rafts, were less prone to infection than oysters grown at depths of 8-9 metres. The explanation was that the rate of infection was higher when oysters were closer to the seabed ^[35].

Outbreaks of B. ostreae occur at temperatures of 12-20°C and could, therefore, be limited by using lower temperatures in the environment of the oyster cultures. Although, this reduction in temperature might reduce the oyster’s resistance to the parasite ^[30]. In general, the risk of infection can be reduced by reducing contact between oysters, whether infected or not. This can be done, for example, by aiming for lower densities or destroying infected individuals, although in a culture of thousands of animals packed together this is not easily done ^[36].

Finally, it is currently investigated if populations of flat oysters which are immune to infection can be obtained. Studies show that the successful breeding of resistant flat oyster populations is possible ^{[37, 38]}. However, this process is not yet fully developed as there are additional problems such as inbreeding, which leads to weakened and underdeveloped populations ^[39].

B. ostreae belongs to the protists. These are single-celled organisms with a nucleus (eukaryotic) in which the genetic material is stored. This is in contrast to bacteria, prokaryotes, that have no nucleus ^[40].

B. ostreae is 2-4 µm in size ^[7] and causes inflammation of the gill tissue and breakdown of the connective tissue in shellfish (especially oysters). The parasite invades the blood cells (haematocytes) of the host. One blood cell may contain more than 10 individuals of the parasite. Reproduction of this parasite is by transverse division ^{[12, 41]}. Over time, an infected blood cell will die and tear open, releasing the parasites. They are filtered from the seawater by other oysters and end up in their gill tissue. The parasite usually becomes fatal to the flat oyster when it reaches an age of two to three years ^[15].

A yellow to black discolouration and/or lesions on the gills, mantle and digestive glands are characteristic of infected oysters. Diseased individuals are prone to gaping. However, many infected oysters remain normal in appearance, making it difficult to distinguish infected from non-infected ones with the naked eye. As a result, the parasite may already be widespread at the time of detection. In the meantime, several molecular laboratory tests have been developed to unambiguously determine the presence of the infection ^[15]. Infected oysters are harvested at two years of age before the infection becomes fatal to the oyster. The parasite does not pose a risk to humans when eaten ^{[9, 42]}.

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