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Resistant flat oysters offer hope against Bonamiasis
ParasitologyToday, vol. 4, no. 5, I988
120
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Resistant Flat Oysters Offer Hope Against Bonamiasis R. Elston and L. Holsinger
Bonamia ostreae, provisionally a member ofthe Acetospora, is a blood cell parasite ofthe European flat oyster, Ostrea edulis. The central role ofthis parasite in debilitating the flat oyster industry in Europe was discussed recently in Parasitology Today’. Even more recent discoveries have revealed the intriguing history of the spread of the disease throughout North America and to Europe, showing that not all stocks of0. edulis show the same susceptibility to bonamiasis. These developments offer hope that diseaseresistant oysters will revitalize the European oyster industrf3. Large quantities of Dutch stock flat oysters were introduced into the northeastern United States in the late 1940s in the hope that a significant industry would develop. This introduction established the only known naturally reproducing population of flat oysters in North America at Casco Bay, Maine. Like their introduced ancestors, the present day population of Casco Bay oysters remain Bonamia free but highly’susceptible to the disease. Populations introduced to other sites on the eastern seaboard of the United States are reported to have been infected at various times with the parasite but there has been no definitive confirmation of this. It is clearly documented, however, that a parasite of the flat oyster, with identical morphology to 6. ostreae, was associated with high mortality levels in flat oysters in California in the mid- I 960s4,‘. These California oysters included populations from the eastern seaboard that were descendants of the Dutch importations to North America. The disease, imprecisely termed ‘microcell disease’ along with other oyster diseases, received little attention outside California. Although survival among the introduced California oysters was very low it was sufficient to maintain cultured and semi-wild populations that were infected with the parasite. During the mid-l 970s an oyster hatchery and seed supply business was established at Moss Landing, California, which used the infected populations of 0. edulis as brood stock. Large quantities of this seed were shipped to the productive French flat oyster beds in Brittany. This initiated the well-documented epizootic of bonamiasis which began in France6,7. Following the first reports of the disease in Britanny in 1980, bonamiasis has been reported in other European countries including Holland, Spain, Denmark, England8*9 and most recently (I 987) in Ireland u. McArdle, pers. commun.). Interestingly, it has not been found in the Mediterranean, although infected oysters have been reportedly
transported to Mediterranean sites. The index source of the disease in North America is unknown but presumably the parasite is well adapted to another host, probably a bivalve mollusc, from which it was transferred to 0. edulis either on the Atlantic seaboard or in California. A similar disease has been associated with mortalities in the dredge oyster of New Zealand, Jiostrea lutaria’ (M. Hine, pers. commun.). This parasite, while similar, is morphologically and serologitally distinct and therefore is considered to be a different species of Bonamia. The identity of the American and European parasites and the distinctiveness of the New Zealand parasite were determined definitively using a library of nine monoclonal antibodies developed by French scientists at the IFREMER laboratory (French Institute for Research on the Utilization of Marine Resources) at La Tremblade, France (E. Mialhe, pers. commun.). Other reports however, indicated that 6. ostreae could infect 0. chilensis” and J. lutaria’ ’ when these oysters were exposed to it in Europe. The latter report Indicated that “the pathological characteristics were identical” in J. lutaria and 0. edulis when infected with 6. ostreae which supports the view that the New Zealand infections of J. lutaria are caused by a similar but distinct parasite.
Resistant oysters in Washington Brood stock from the California hatchery was moved to Washington State in the late 1970s where it has subsequently been used in an intensive breeding programme. Descendants of this brood stock were examined in I985 and found to be infected with Bonamia, but the Washington oysters did not seem to suffer significant mortalities as a result of the infection. Comparison of the ability to survive of Washington oysters with that of susceptible populations indicated that the Washington stock had a substantial resistance to mortality although the biological mechanism of this resistance is unknown3. The resistant Washington population exhibits a mortality rate as low as 4% in fouryear-old oysters when grown under optimal cultural conditions (Table I ). Mortality in susceptible oysters can approach 100%3. Thus these resistant populations of oysters offer the best hope today of re-establishing the flat oyster in Bonamia-infected areas where it is not possible to eradicate the disease. Further laboratory and field data on the resistance phenomenon are needed. Researchers from the French government agency (IFREMER) and American scientists from Battelle, Pacific Northwest Laboratories are collaborating to provide this data. Hopefully, this will lead to field trials of the resistant populations in Europe in 1988. In addition to providing evidence of resistant populations of the flat oyster, field experiments suggest that it is possible to reduce the impact of bonamiasis
Table I. Mortality rates of resistant and susceptible Ostreo edulis grown in seabed and water column culture
Test Group= Age A B c3 c2 Cl a A.
3 4 4 3 2
ResistantkusceptiblebCulture type’ Cumulative annual mortality 47.0 SB s R 21.5 SB R WC 4.0 WC R 7.3 20.0 R WC
Band C represent three test sites; at site C, three year classes(C3, three years of age, etc.) of the resistant population were tested. b R-resistant population of oysters; S-susceptible population described in the table may, in fact, have some degree of resistance since other susceptible populations undergo nearly 100% mortality when first infected with Bonomia. c Culture type indicates that the oysters were cultivated either on the seabed (SB) or in hanging net devices in the water column (WC).
Parasitology Today, vol. 4, no. 5, 1988
by specific management of ,oyster beds. Field observations suggest that the disease spreads much more readily in dense populations of oysters. Also, mortality appears to be reduced in offbottom cultures compared with oysters that are grown directly on the seabed. In resistant populations, mortality declines with the age of the oyster so that the highest mortality rates occur in oysters up to one year old, which are less valuable than their older cohoS;. Recently completed experiments carried out in our laboratory showed that experimental Bonamia infections proceeded most rapidly at 16 and 12°C, followed by 20°C. At 24°C, the infection rate was substantially reduced. The disease also affects oysters where winter water temperatures range from 0 to 5°C. Thus, temperature does not appear to limit the disease up to about 20°C. The resistant populations of oysters in Washington remain infected with Bonamia although when tissues are examined histologically the infection appears to be localized and contained. Study of oyster tissue from infected populations shows that many individual animals have extensive haemocytic inflammatory reactions
121
but do not contain identifiable parasites. This suggests that there are stages of the infection that are not yet recognizable as bonamiasis by histological methods although the relationship, if any, of these haemocytic reactions to the presence of the parasite has not been established. Interestingly, in experimental infections, mortality does not begin until 3-7 months following exposure of oysters to the parasite. To add to the enigma, Mediterranean sites and one Californian site have never shown evidence of the infection even though it is almost certain that infected flat oysters were at one time placed in these areas. These fascinating basic research problems, which have immense significance for the understanding of the life cycle of the parasite, the mechanism of host reaction and the influence of environmental factors on the disease, require further investigation.
Acknowledgement: Our work is supported by the US Department of Energy under Contract DE-AC06-76RLO 1830.
S t u d e n t s - 3 0 % Diiscount on a subscription to
ParasitologyToday Parasitology Today is now available at the substantial discount of 30% off 1988 prices to all students enrolled at recognized institutions. A student subscription comprises 12 monthly issues staging from any month in 1988. Prices include air delivery world wide. You can subscribe today by completing the form below and mailing it with your cheque (made out to Elsevier) for UK £21.00, USA and Canada $37.00, Europe Df195.00, Rest of World Dfll 10.00, together with valid p r o o f of your current student status (photocopy of student card, letter from Head of Department, etc.), to one of the addresses on the subscription card bound in this issue. Please start my subscription to available issue (I 988).
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References I Anon. (1987) Parasitology Today 3, 36 2 Elston, R.A. et al. (1986) Diseases of Aquatic Organisms 2, 49-54 3 Elston, R.A. et al. (1987) Aquaculture 64, 237242 4 Katkansky, S.C, et al. (1969) Calif Fish Game 55, 69-74 5 Katkansky, S.C. and Warner, R.W. (1974) Calif. Fish Game (Tech. Rep. No. 25) 6 Balouet, G. et al. (1983) Aquaculture 34, I - 14 7 Comps, M, et a/. (I 980) C.R. Acad. Sci IV 290, 383-384 8 Bucke, D., and Feist, S. (1985) in Fish and Shell~sh Patholo~ (.Ellis, A.E. ed,), pp 387-392, Academic Press, London 9 Van Banning, P. (1985) in Fish and Shellfish Pathology (Ellis, A.E: ed), pp 393-39, Academic Press, London 10 Tige, G. et al. (1982) Bull. Inst. P~ches Marit. 328,3-13 II Bucke, D., and Hepper, B, (1987) Bull. Eur. Assoc, Fish Pathol. 7, 79-80
Ralph Elston and Lisa Holsinger are at the Battelle Marine Research Laboratory, 439 West Sequim Bay Road, Sequim, WA 98382, USA.
Next month in Parasitology Today, David Bucke of the Fish Diseases Laboratory, Weymouth, discusses the intriguing pathophysiology of Bonamia ostreae
120
,I,a
I”
4
Resistant Flat Oysters Offer Hope Against Bonamiasis R. Elston and L. Holsinger
Bonamia ostreae, provisionally a member ofthe Acetospora, is a blood cell parasite ofthe European flat oyster, Ostrea edulis. The central role ofthis parasite in debilitating the flat oyster industry in Europe was discussed recently in Parasitology Today’. Even more recent discoveries have revealed the intriguing history of the spread of the disease throughout North America and to Europe, showing that not all stocks of0. edulis show the same susceptibility to bonamiasis. These developments offer hope that diseaseresistant oysters will revitalize the European oyster industrf3. Large quantities of Dutch stock flat oysters were introduced into the northeastern United States in the late 1940s in the hope that a significant industry would develop. This introduction established the only known naturally reproducing population of flat oysters in North America at Casco Bay, Maine. Like their introduced ancestors, the present day population of Casco Bay oysters remain Bonamia free but highly’susceptible to the disease. Populations introduced to other sites on the eastern seaboard of the United States are reported to have been infected at various times with the parasite but there has been no definitive confirmation of this. It is clearly documented, however, that a parasite of the flat oyster, with identical morphology to 6. ostreae, was associated with high mortality levels in flat oysters in California in the mid- I 960s4,‘. These California oysters included populations from the eastern seaboard that were descendants of the Dutch importations to North America. The disease, imprecisely termed ‘microcell disease’ along with other oyster diseases, received little attention outside California. Although survival among the introduced California oysters was very low it was sufficient to maintain cultured and semi-wild populations that were infected with the parasite. During the mid-l 970s an oyster hatchery and seed supply business was established at Moss Landing, California, which used the infected populations of 0. edulis as brood stock. Large quantities of this seed were shipped to the productive French flat oyster beds in Brittany. This initiated the well-documented epizootic of bonamiasis which began in France6,7. Following the first reports of the disease in Britanny in 1980, bonamiasis has been reported in other European countries including Holland, Spain, Denmark, England8*9 and most recently (I 987) in Ireland u. McArdle, pers. commun.). Interestingly, it has not been found in the Mediterranean, although infected oysters have been reportedly
transported to Mediterranean sites. The index source of the disease in North America is unknown but presumably the parasite is well adapted to another host, probably a bivalve mollusc, from which it was transferred to 0. edulis either on the Atlantic seaboard or in California. A similar disease has been associated with mortalities in the dredge oyster of New Zealand, Jiostrea lutaria’ (M. Hine, pers. commun.). This parasite, while similar, is morphologically and serologitally distinct and therefore is considered to be a different species of Bonamia. The identity of the American and European parasites and the distinctiveness of the New Zealand parasite were determined definitively using a library of nine monoclonal antibodies developed by French scientists at the IFREMER laboratory (French Institute for Research on the Utilization of Marine Resources) at La Tremblade, France (E. Mialhe, pers. commun.). Other reports however, indicated that 6. ostreae could infect 0. chilensis” and J. lutaria’ ’ when these oysters were exposed to it in Europe. The latter report Indicated that “the pathological characteristics were identical” in J. lutaria and 0. edulis when infected with 6. ostreae which supports the view that the New Zealand infections of J. lutaria are caused by a similar but distinct parasite.
Resistant oysters in Washington Brood stock from the California hatchery was moved to Washington State in the late 1970s where it has subsequently been used in an intensive breeding programme. Descendants of this brood stock were examined in I985 and found to be infected with Bonamia, but the Washington oysters did not seem to suffer significant mortalities as a result of the infection. Comparison of the ability to survive of Washington oysters with that of susceptible populations indicated that the Washington stock had a substantial resistance to mortality although the biological mechanism of this resistance is unknown3. The resistant Washington population exhibits a mortality rate as low as 4% in fouryear-old oysters when grown under optimal cultural conditions (Table I ). Mortality in susceptible oysters can approach 100%3. Thus these resistant populations of oysters offer the best hope today of re-establishing the flat oyster in Bonamia-infected areas where it is not possible to eradicate the disease. Further laboratory and field data on the resistance phenomenon are needed. Researchers from the French government agency (IFREMER) and American scientists from Battelle, Pacific Northwest Laboratories are collaborating to provide this data. Hopefully, this will lead to field trials of the resistant populations in Europe in 1988. In addition to providing evidence of resistant populations of the flat oyster, field experiments suggest that it is possible to reduce the impact of bonamiasis
Table I. Mortality rates of resistant and susceptible Ostreo edulis grown in seabed and water column culture
Test Group= Age A B c3 c2 Cl a A.
3 4 4 3 2
ResistantkusceptiblebCulture type’ Cumulative annual mortality 47.0 SB s R 21.5 SB R WC 4.0 WC R 7.3 20.0 R WC
Band C represent three test sites; at site C, three year classes(C3, three years of age, etc.) of the resistant population were tested. b R-resistant population of oysters; S-susceptible population described in the table may, in fact, have some degree of resistance since other susceptible populations undergo nearly 100% mortality when first infected with Bonomia. c Culture type indicates that the oysters were cultivated either on the seabed (SB) or in hanging net devices in the water column (WC).
Parasitology Today, vol. 4, no. 5, 1988
by specific management of ,oyster beds. Field observations suggest that the disease spreads much more readily in dense populations of oysters. Also, mortality appears to be reduced in offbottom cultures compared with oysters that are grown directly on the seabed. In resistant populations, mortality declines with the age of the oyster so that the highest mortality rates occur in oysters up to one year old, which are less valuable than their older cohoS;. Recently completed experiments carried out in our laboratory showed that experimental Bonamia infections proceeded most rapidly at 16 and 12°C, followed by 20°C. At 24°C, the infection rate was substantially reduced. The disease also affects oysters where winter water temperatures range from 0 to 5°C. Thus, temperature does not appear to limit the disease up to about 20°C. The resistant populations of oysters in Washington remain infected with Bonamia although when tissues are examined histologically the infection appears to be localized and contained. Study of oyster tissue from infected populations shows that many individual animals have extensive haemocytic inflammatory reactions
121
but do not contain identifiable parasites. This suggests that there are stages of the infection that are not yet recognizable as bonamiasis by histological methods although the relationship, if any, of these haemocytic reactions to the presence of the parasite has not been established. Interestingly, in experimental infections, mortality does not begin until 3-7 months following exposure of oysters to the parasite. To add to the enigma, Mediterranean sites and one Californian site have never shown evidence of the infection even though it is almost certain that infected flat oysters were at one time placed in these areas. These fascinating basic research problems, which have immense significance for the understanding of the life cycle of the parasite, the mechanism of host reaction and the influence of environmental factors on the disease, require further investigation.
Acknowledgement: Our work is supported by the US Department of Energy under Contract DE-AC06-76RLO 1830.
S t u d e n t s - 3 0 % Diiscount on a subscription to
ParasitologyToday Parasitology Today is now available at the substantial discount of 30% off 1988 prices to all students enrolled at recognized institutions. A student subscription comprises 12 monthly issues staging from any month in 1988. Prices include air delivery world wide. You can subscribe today by completing the form below and mailing it with your cheque (made out to Elsevier) for UK £21.00, USA and Canada $37.00, Europe Df195.00, Rest of World Dfll 10.00, together with valid p r o o f of your current student status (photocopy of student card, letter from Head of Department, etc.), to one of the addresses on the subscription card bound in this issue. Please start my subscription to available issue (I 988).
Parasitology Today from
the next
I enclose my personal cheque for £ .............../D[I .............../$ ............... made out to Elsevier. Name ........................................................ Signature ................................................ Address ............................................................................................................................ .................................................................... Postal Code ...........................................
Name of Institution ....................................................................................................... Remember to send valid proof of your student status with this form.
Note: Current subscribers who are eligible for student discount may claim the discount only on expiry of their current subscription. No refunds, credits or extensions of the subscription period can be given.
Enter no 190 on adverl;ising enquiry form
References I Anon. (1987) Parasitology Today 3, 36 2 Elston, R.A. et al. (1986) Diseases of Aquatic Organisms 2, 49-54 3 Elston, R.A. et al. (1987) Aquaculture 64, 237242 4 Katkansky, S.C, et al. (1969) Calif Fish Game 55, 69-74 5 Katkansky, S.C. and Warner, R.W. (1974) Calif. Fish Game (Tech. Rep. No. 25) 6 Balouet, G. et al. (1983) Aquaculture 34, I - 14 7 Comps, M, et a/. (I 980) C.R. Acad. Sci IV 290, 383-384 8 Bucke, D., and Feist, S. (1985) in Fish and Shell~sh Patholo~ (.Ellis, A.E. ed,), pp 387-392, Academic Press, London 9 Van Banning, P. (1985) in Fish and Shellfish Pathology (Ellis, A.E: ed), pp 393-39, Academic Press, London 10 Tige, G. et al. (1982) Bull. Inst. P~ches Marit. 328,3-13 II Bucke, D., and Hepper, B, (1987) Bull. Eur. Assoc, Fish Pathol. 7, 79-80
Ralph Elston and Lisa Holsinger are at the Battelle Marine Research Laboratory, 439 West Sequim Bay Road, Sequim, WA 98382, USA.
Next month in Parasitology Today, David Bucke of the Fish Diseases Laboratory, Weymouth, discusses the intriguing pathophysiology of Bonamia ostreae