Lethal Parasites in Oysters from Coastal Georgia with Discussion of Disease and Management Implications
EARL J. LEWIS, FREDERICK G. KERN, AARON ROSENFIELD, STUART A. STEVENS, RANDAL L. WALKER, and PETER B. HEFFERNAN
Introduction ginica, in this century. During the last ever, as additional shellfishermen be several decades, an increasing aware gan to report increased mortalities, the Oysters in many parts of the world ness of the role shellfish pathogens play DNR initiated field surveillance at se have declined in abundance since the in the population dynamics of oysters lected areas. Results of the survey 19th century, probably in large part has been reflected in publications of showed that where mortalities occurred from indiscriminate harvesting and de Sindermann and Rosenfield (1967), they ranged from 40 to 100 percent. struction of beds (Sindermann, 1970). Sindermann (1970, 1990), Kinne Most locations exhibited mortalities of Lyles (1969) published data showing a (1983), Farley et al. (1988), Fisher 60-70 percent. similar decline in the U.S. commercial (1988), and Farley (1989, In press). To determine the cause of mortali harvest of oysters, Crassostrea vir- Disease is clearly a major factor af ties, NOAA's National Marine Fisher fecting the abundance of shellfish ies Service (NMFS) and the Georgia stocks. Malpeque Bay disease (Needler DNR began a cooperative study in and Logie, 1947) and other distinct dis January of 1986. Data in this report Earl J. Lewis, Frederick G. Kern, and Aaron Rosenfield are with the Oxford Cooperative eases caused by the parasites Perkinsus suggest that epizootic levels of infec Laboratory, Northeast Fisheries Science Center, marinus (Mackin et aI., 1950; Levine, tion with P. marinus ("Dermo") are the National Marine Fisheries Service, NOAA, 904 South Morris Street, Oxford, MD 21654. Stuart 1978), Haplosporidium nelsoni (Haskin most probable causes of the mortali A. Stevens is with the Coastal Resources Divi et aI., 1966; Sprague, 1978), and ties. The report also documents the oc sion, Georgia Department of Natural Resources, H. costale (Wood and Andrews, 1962) currence of H. nelsoni ("MSX") in the I Conservation Way, Brunswick, GA 31523. Randal L. Walker and Peter B. Heffernan are have been reported to cause mortali coastal waters of Georgia for the first with the University of Georgia's Marine Exten ties in the oyster, C. virginica (Sin time. sion Service, Shellfish Research Laboratory, P.O. dermann, 1990; Farley, In press). Box 13687, Savannah, GA 31416. Methodology In 1966 and 1968, one of the au thors (Rosenfield) made a histological Samples of apparently healthy oys study of oysters from coastal Georgia, ters were collected for histological ex as part of an Atlantic coastal survey to amination from 17 sites throughout ABSTRACT- Extensive mortalities of determine the status of oyster disease coastal Georgia during two studies (Fig. oysters, Crassostrea virginica, occurred agents and parasites. At that time, H. l). The same protocols were followed from 1985 through 1987 in coastal waters nelsoni was causing mortalities of oys for both studies, with the exception of of Georgia. Fluid thioRlycolate cultures of oysters collected from 16 of 17 locations ters from Delaware and Chesapeake the number of oysters examined, and revealed infections by the apicomplexan Bays, and P. marinus was causing seri quantifying the disease intensity of the parasite Perkinsus marin us. An asceto ous losses to oysters in the Gulf of earlier unpublished work by Rosenfield. sporan parasite, Haplosporidium nelsoni, Mexico region. Results of this study In January 1966, samples of 25 oys was also observed in histopathological ex amination of oysters from 4 of the loca (unpubJ.) document the occurrence of ters each were collected from Wassaw tions. While the range of H. nelsoni cur P. marinus in Georgia waters as early Creek and the Duplin and Woodbine rently is recognized as the east coast of the as 1966; however, H. nelsoni was not Rivers, and processed for histological United States from Maine to Florida, this observed at that time. examination. Subsequently, 15-20 ani is the first report of the parasite in Geor In November 1985, the Georgia De mals were collected and processed for gia waters. This paper documents the oc currence of these two lethal parasites in partment of Natural Resources (DNR) a follow-up evaluation in April of 1968 oysters from coastal waters of Georgia, began receiving complaints from the from each of the following four sites: along with potential disease and manage shellfish industry of widespread mor Eagle Creek and the Darien, Wil ment implications. Results of an earlier in talities of oysters, C. virginica, from mington, and Brickhill Rivers. Intensi dependent and previously unpublished sur vey are also discussed which document the commercial leases. Initial mortalities ties of infection were not recorded. presence ofP. marinus in Georgia as early were attributed to natural causes, alarm Beginning in January of 1986, oys as 1966. ing neither industry nor the DNR. How ters were collected from Mud Creek
54(2),1992 1 Table 1.-Field survey and macroscopic oyster exami nation data, 1986-87 survey.
Sa . lin- Water Mean Condi- Mean --- Sample ity temp. length tion condi· ~ l 1 BRYAN area %. (0C) (mm) range tion /. Jan. 1986 U.~'ciiJ-- Mud Creek 28' 13.0 8904 1-4 3.0 ~."\ Wilmington River Crooked R. 28' 13.0 8604 1-5 2.1 -; Mean Wassaw Creek 28 13.0 87.9 1-5 26 \ LIBERTY \. Nov. 1986 Charles Creek Jointer R. 32 230 6804 4-6 4.9 S. Latham Cr. 31 23.0 65.0 2-5 4.1 ~. Jekyll Cr. 29 22.0 52.8 2-6 4.5 Charles Cr 32 220 53.1 2-6 35 Mean 31 22.5 59.8 2-6 4.3
Nov. 1987 ~'
Animals were macroscopically ex populations. This value is calculated by 'P. marinus results based on thioglycolate cultures of rec amined and processed for histology us the summation of disease intensity in tal tissue. 2H. nelsoni results based on histological observations. ing standard Oxford Laboratory histo all animals from a site, divided by the 3Criteria for intensity data based on a numerical scale from logical techniques (Howard and Smith, number of animals tested for that site 1 to 9: 1 = very light, 3 = light, 5 = moderate. 7 = heavy. 9 =very heavy. 1983). Each oyster was measured, ex (Ray, 1954). 'NA =Data not available.
2 Marine Fisheries Review Results (Lyles, 1969) to 29.9 million pounds Andrews (1988) claimed that seaside of meats in 1989 (USDOC, 1990). bays of the eastern shore of Virginia, During 1986-87, oysters were ob While overharvesting, predation, and and usually Maryland, were free of P. tained from high salinity waters, be deteriorating water quality are believed marinus. Lewis and Kern (independent tween 28 and 32%0, with temperatures to be responsible for much of the de personal observations) found the para of l3°-23°e. Oysters ranged in length cline (Leonard et a!., 1989), diseases site in oysters from Maryland and Vir from 25 to J43 mm, and their mean have also been a significant factor. ginia portions of Chincoteague Bay. visually assessed condition varied from Traditionally, Chesapeake Bay led Prevalences as high as 96% were ob watery(-), or very poor, to medium(+) the United States in oyster production served, of which 76% were judged to (Table 1). No fat oysters were found in prior to H. nelsoni and P. mari'}us be be heavy or very heavy infections. As any of the samples. Similar data were coming endemic to the area (Anderson sociated mortalities of up to 84% were not available from 1966 or 1968 and Power, 1957). Following several reported as being caused primarily by samples. decades of severe losses due to oyster P. marinus. Thioglycolate cultures and histo diseases, there has been a complete re In Georgia, P. marinus was found as pathological examination of oysters re versal in oyster production in the na early as 1966 when it was observed in vealed the presence of P. marinus from tion. Chesapeake Bay now contributes oysters from Wassaw Creek and the 16 of the 17 sites sampled, and H. only 14 percent of the annual U.S. oys Duplin and Woodbine Rivers. With the nelsoni in oysters from 4 sites (Table ter harvest, compared to 50 percent pro exception of oysters from the Duplin 2). Parasites were found in oysters duced in the Gulf of Mexico region, River (44%), the prevalence of infec throughout coastal Georgia, without in principally by Louisiana (USDOC, tion from P. marinus never exceeded dication of a regional distribution. 1990). Commensurate with this change, 12% in the 1966-68 survey. Any mor Oysters collected from Georgia in oyster imports since 1986 have consis tality which might have occurred as a J966 and 1968 revealed the presence tently exceeded the U.S. commercial result of P. marinus infections at these of P. marinus in 0-44% of the oysters landings (USDOC, 1990), to meet the low prevalences would likely have been examined. Perkinsus marinus was ob American consumer demand. masked by what are considered nor served in 12-44% of oysters sampled Perkinsus marinus, first described in mal losses to natural causes, and thus in January of 1966, but no mortalities oysters from the Gulf of Mexico by never reported. were reported. Two years later, P. Mackin et a1. (1950), causes a chronic Perkinsus marinus is, however, con marinus was found in 0-10% of the disease which can be fatal in C. sidered to be the etiological agent re oysters examined, again with no reports virginica (Mackin, 1951). Some con sponsible for Georgia oyster mortali of associated mortalities. Examination fusion apparently exists regarding the ties observed in 1985-87, because of of oysters in 1986-87 revealed P. parasite's northern range and its pres its high prevalence and intensity in marinus occurred at all sites sampled. ence in coastal bays of Maryland and thioglycolate cultures and histological Prevalence of the disease ranged from Virginia. Quick (1977) reported its sections of the oysters examined. Sam 88 to 100%, with intensities of infec range from Massachusetts south into pling in 1986 and 1987 showed con tion ranging from very light (1) to very the Gulf of Mexico. Kern et a!. (1973) tinued high prevalence of P. marinus heavy (9). Infections showed an increase also reported the parasite to occur in infections, with a slight but progres in sample population intensity from a C. virginica growing in Hawaii. How sive increase in intensities. mean of 3.6 in January J986 to 4.3 in ever, later publications (Andrews, J988; Disease prevalence and intensity of November 1987. Mean intensity of in Sinderrnann, 1990) cite Delaware Bay P. marinus reflect seasonal parasite ac fection for the entire study was 3.9. as the northern boundary. In an unpub tivity which strongly correlate with wa Haplosporidium nelsoni was not ob lished report, Farley and Plutschak ' ob ter temperature (Quick and Mackin, served in either of the 1966 or 1968 served possible, very early infections 1971). Infections are most severe dur samples; however, the parasite was di of P. marinus in 8% of oysters diag ing summer and early fall, then de agnosed in a total of eight animals from nosed by rectal thioglycolate cultures crease in intensity as water tempera four sites during 1986 and 1987. Preva from three sites in Massachusetts. This tures drop. Results of this study failed lence of H. nelsoni from these sites suggests that oysters in waters as far to demonstrate statistically any corre ranged from 2 to 6%, with sample north as Massachusetts may indeed ex lation between water temperature and population intensities ranging from 0.1 perience P. marinus infections, as ear disease intensity. This is attributed to a to 004. Intensity of disease among in lier publications suggested. The most lack of seasonal data and does not dis dividual infected animals varied from serious effects of P. marinus infections, pute the existence of the relationship. very light (1.0) to heavy (7.0). however, occur in the Gulf of Mexico, However, the trend of our disease in where mortalities are estimated at 50% Discussion or more annually (Craig et aI., 1989). 'e. A. Farley, National Marine Fisheries Service, Since the tum of the century, annual The occurrence of P. marinus in oys NOAA, Northeast Fisheries Science Center, Ox ford, MD 21654, and D. L. Plutschak, Maryland U.S. oyster production has fallen from ters north of Delaware Bay apparently Department of Natural Resources, Oxford, MD about 158 million pounds of meats remains a rare event at this time. 21654. Personal commun.
54(2),1992 3 tensity data graphically resembles that Bay oyster epizootic (Haskin et. aI., exposed to the disease (this may in of Quick and Mackin (1971) for Florida 1966), cyclic periods of oyster mor volve reducing the legal harvest size oysters infected by P. marinus at com talities caused by H. nelsoni have con of oysters, and planting seed in the fall parable temperatures. tinued to occur along the Atlantic coast and winter after the disease process has Gross condition observed in 1986 in Massachusetts, Connecticut, New been slowed by decreased water tem 87 reflects a lack of stored glycogen or York, New Jersey, Delaware, Maryland, peratures), and 3) isolating grow-out "fatness." Low gross conditions are Virginia, and, to a limited extent, North areas from known diseased areas typical of oysters stressed by high wa Carolina (Haskin and Andrews, 1988). (Andrews and Ray, 1988). ter temperature, disease, spawning, and With the exception of New Hampshire The cross-infection of oysters by P. other events causing an animal to ex and Rhode Island, H. nelsoni has been marinus from other mollusks is a man pend disproportionate amounts of en observed in oysters from each state agement concern with regard to the iso ergy on self maintenance. This results along the east coast from Maine to lation of shellfish beds from infectious in depletion of glycogen reserves which Florida (Haskin and Andrews, 1988; sources. Ray (1954), Andrews (1955), translates into a poor condition. At the Sindermann, 1990). To date, however, Andrews and Hewatt (1957), Perkins time of the year samples were taken, parasite-induced mortalities have not (1988), and McGladdery et. al. (1991) oysters would be expected to have a been reported from Maine or states reported observations of Perkinsus and condition above medium (5). In all south of North Carolina. Perkinsus-like organisms in many other cases, the mean condition was below 5 The most severe effects of H. nelsoni mollusks along the east coast of the and no oysters above a value of 6 were are seen in Delaware and Chesapeake United States. Although their taxo observed. Bays (Haskin et. aI., 1965; Andrews nomic identity has not always been es Oyster mortalities were first reported and Wood, 1967; Farley, 1975; Lewis, tablished, the organisms are apparently from Camden County, Ga., early in No 1988). As a direct result of H. nelsoni ubiquitous and easily transmitted. Re vember 1985, and subsequently from infections, oyster production in Dela sults of earlier, unsuccessful work to Mcintosh County in the beginning of ware Bay dropped from about 8 mil cross-infect mollusks with Perkinsus January 1986. Reports occurred at a lion pounds of meats in 1953 to spp. isolated from other molluscan spe time when water temperatures were ab 167,000 pounds by 1960 (Sindermann cies led to belief in the host specificity normally high and following a period and Rosenfield, 1967). Likewise, oys of parasites. Goggins et al. (1989), of extensive rainfall associated with ter production in Chesapeake Bay fell however, demonstrated cross-infection several tropical storms and hurricanes. from 39.2 million pounds of oyster of Australian Perkinsus spp. from 6 Typically, the intensity of P. marinus meats in 1955 (Anderson and Power, molluscan sources to 10 species of mol infections seen in the surviving oysters 1957) to less than 4.1 million pounds lusks; they concluded they were deal sampled in January 1986 would not be of meats in 1989 (USDOC, 1990). Dis ing with at least 2 species of Perkinsus considered sufficient in itself to cause ease caused by Perkinsus marinus and and low levels of host specificity. The the extensive mortalities experienced H. nelsoni has had a combined effect potential for cross infection, along with in November 1985. However, by the in reducing oyster production from the observation of another species of time samples were taken the most Chesapeake Bay. Perkinsus found in scallops on the east heavily infected oysters had died. In January 1986, H. nelsoni was de coast, may be a concern where oysters Quick and Mackin (1971) reported tected for the first time in Georgia in are not infected by P. marinus. mortality in Florida oysters infected by three oysters from Mud Creek. Al McGladdery et al. (1991) recently de P. marinus to begin at a medium infec though very heavy levels of intensity scribed a new species, Perkinsus tion intensity under normal circum were observed in a few oysters (7.0), karlssoni, in the bay scallop, stances. That would approximate a H. nelsoni is not believed to be the Argopecten irradians, which was ob moderate infection intensity, or stage principal agent responsible for mortali served in specimens from the Gulf of 5, in the current study. While infection ties, because of its low prevalence and St. Lawrence and Atlantic Nova Scotia, intensity of individual oysters exceeded intensity in the sample population (0.0 Can., as well as Rhode Island, Con a stage 5, sample population intensity 0.4). Examination of the November necticut, and Cape Cod, Mass., in the for sites ranged from 3.4 to 4.9. The 1986 and 1987 samples also revealed United States. Whether P. karlssoni or added stress of extended periods of ab the presence of H. nelsoni in oysters other Perkinsus-like organisms may normally high water temperatures and from three additional locations in cross-infect C. virRinica is yet to be unusually heavy rainfall are considered coastal Georgia. demonstrated. contributing factors to the mortalities. Mortalities are increased in areas, Management Implications The same pressures likely continued such as the Chesapeake Bay, where during 1986, as climatic conditions Minimizing the effect of disease high levels of both P. marinus and H. were reported to have mirrored those caused by P. marinus involves several nelsoni coexist. In these situations, of 1985 (Stevens, Personal commun.). key strategies which include: I) Avoid Andrews (1979) believes H. nelsoni Since H. nelsoni was established as ing the transplantation of diseased seed outcompetes P. marinus. This informa the causative agent of the Delaware stock, 2) reducing the time oysters are tion highlights a potential danger to
4 Marine Fisheries Review Georgia shellfisheries, considering the apply in Georgia; climate and marsh Andrews, J. D. 1988. Epizootiology of the dis ease caused by the oyster pathogen Perkinsus recent discovery of H. nelsoni in Geor ecology of coastal Georgia contrast marinus and its effects on the oyster industry. gia oysters. greatly with the remainder of the east In W. Fisher (Editor), Disease processes in Responding to scientific evidence ern United States. This is reflected in marine bivalve molluscs, p. 47-63. Am. Fish. Soc., Spec. Pub!. 18, Bethesda, Md. that H. nelsoni is intolerant of salini the biology of local shellfish (Walker ----and W G. Hewatt. 1957. Oyster mor ties below 10%0 (Andrews, 1964; Ford, and Humphrey, 1984; Walker and tality studies in Virginia. II. The fungus dis ease caused by Dermocystidium marinum in 1985; Ford and Haskin, 1988a), oyster Tenore, 1984; Walker, 1985; Heffernan oysters of Chesapeake Bay. Eco!. Monogr. management officials now emphasize et a!., 1989a,b). For example, distribu 27:1-26. the use of lower salinity growing areas tion, growth rates, and reproductive pat ---- and S. M. Ray. 1988. Management strategies to control the disease caused by to avoid, or at least minimize, the ef terns for Georgia oysters and hard Perkinsus marinus. In W. Fisher (Editor), Dis fects of H. nelsoni on oysters (Ford clams, Mercenaria mercenaria, contrast ease processes in marine bivalve molluscs, p. and Haskin, 1988b). Because the trans greatly when compared with other ar 257-264. Am. Fish. Soc., Spec. Pub!. 18. ---- and J. L. Wood. 1967. Oyster mor plantation of seed and shell stock is a eas of the Atlantic coastline. Georgia tality studies in Virginia. VI. History and dis vital component of management, the oysters have extended reproductive pe tribution of Minchinia nelsoni (MSX), a patho gen of oysters, in Virginia. Chesapeake Sci. introduction of infected animals into riods, while polymodal reproductive 8(1):1-13. previously unaffected systems is of cycles occur in hard clams. In Geor Craig, A., E. N. Powell, R. R. Fay, and J. M. great concern (Rosenfield and Kern, gia, oysters primarily occur intertidally Brooks. 1989. Distribution of Perkinsus marinus in Gulf coast oyster populations. Es 1987; Sindermann, In press). Mortali and spawn from April to October (Har tuaries 12(2):82-91. ties, with long-lasting consequences, ris, 1980; Heffernan et a!., 1989b); Farley, C. A. 1975. Epizootic and enzootic as can be linked to the movement of shell whereas, in most of their distribution, pects of Minchinia nelsoni (Haplosporida) dis ease in Maryland oysters. J. Protozoo!. fish stocks (Farley, In press). It is likely, oysters occur subtidally. It may be rea 22(3):418-427. to some degree, that the progressive sonable to expect differences in the ----. 1989. Selected aspects of neoplastic progression in mollusks. In H.E. Kaiser (Edi spread of diseases within Chesapeake ecology and dynamics of pathogens in tor), Comparative aspects of tumor develop Bay may be linked to the movement of coastal Georgia as compared with the ment, cancer growth and progression, p. 24 infected seed stock. northeastern United States. Based on 31. Kluwer Acad. Pub!., Nether!. ----. In press. Mass mOltalities and in Another management strategy in the uniqueness of the Georgia habitat, fectious lethal diseases in bivalve mollusks and volves the development of disease-re studies are in progress to develop ap associations with geographic transfers of popu sistant stocks through selective breed proaches that will reduce mortalities lations. In A. Rosenfield and R. Mann (Edi tors), Dispersal of living organisms into aquatic ing techniques (Haskin and Ford, 1979; from the effects of H. nelsoni and P. ecosystems. Md. Sea Grant Col!. Pub!., Univ. Ford, 1987). While some success has marinus. These include allowing the Md., Coli. Park. earlier harvest of marketable oysters, ----, P. H. Wolf, and R. A. Elston. 1988. been made along these lines with re A long-term study of "microcell" disease in gard to H. nelsoni, several problems prior to the onset of mortalities result oysters with a description of a new genus, remain. First, under intense infection ing from parasitic infections. Mikrocytos (g.n.) and two new species, Mikrocytos mackini (sp.n.) and Mikrocytos pressures, even resistant strains suc roughleyi (sp.n.). Fish. Bul!. 86(3):581-593. cumb to H. nelsoni (Ford and Haskin, Acknowledgments Fisher, W (Editor). 1988. Disease processes in 1988b). Second, disease resistance marine bivalve molluscs. Am. Fish. Soc., Spec. The work was supported in part by Pub!. 18, 315 p. against P. marinus has not been the Coastal Resources Division of the Ford, S.E. 1985. Effects of salinity on survival achieved. It is unknown at this time if of the MSX parasite Haplosporidium nelsoni Georgia Department of Natural Re (Haskin, Stauber, and Mackin) in oysters. J. animals resistant to H. nelsoni are re sources and the Georgia Sea Grant Pro Shellfish Res. 5(2):85-90. sistant to other fatal oyster disease gram under grant number NA84AA ----. 1987. Progress on the development agents. Although disease resistance is of MSX-resistant oyster strains. In A. White D-OOOn. We thank C. Austin Farley, (Editor), Shellfish diseases: Current concerns viewed as a valuable asset in maricul Shawn McLaughlin, and Carl in the northeast, p. 12-14. Woods Hole ture operations, it is not readily appli Sindermann for critical review of the Oceanogr. Inst., Tech. Rep. 87-13. cable to a wild fishery. In other than ---- and H. H. Haskin. 1988a. Compari manuscript, and Jane Keller for techni son of in vitro tolerance of the oyster parasite, strictly controlled mariculture opera cal editing. Haplosporidium nelsoni (MSX) and hemocytes tions, diminished resistance by inter from the host. Cr<1ssostrea virginica. Compo breeding with wild shellfish stocks may Literature Cited Biochem. Physio!. 90A( I): 183-187. ----and . 1988b. Management likely result over time. Anderson, A. W, and E. A. Power. 1957. Fish strategies for MSX (Haplosporidium nelsoni) Management of P. marinus has been ery statistics of the United States, 1955. U.S. disease in eastern oysters. In W. Fisher (Edi Dep. Inter., Fish Wild!. Serv., Stat. Dig. 41, tor), Disease processes in marine bivalve mol shown to be more complex in the Gulf 446 p. luscs, p. 249-256. Am. Fish. Soc., Spec. Pub!. of Mexico than in the Chesapeake Bay Andrews, J. D. 1955. Notes on fungus parasites 18. region, largely because of elevated of bivalve mollusks in Chesapeake Bay. Proc. Goggins, C. L., K. B. Sewell, and R. J. G. Lester. at!' Shellfish. Assoc. 45: 157-163. 1989. Cross-infection experiments with Aus southern water temperatures (Andrews 1964. Oyster mortality studies in trlliian Perkinsus species. Dis. Aquat. Org. and Ray, 1988). It also may be prema Virginia. IV. MSX in James River public 7( I ):55-59. ture to assume that management strat seed beds. Proc. Nat!. Shellfish. Assoc. 53:65 Harris, D. C. 1980. Survey of the intertidal and 84. subtidal oyster resources of the Georgia coast. egies devised to deal with H. nelsoni ----. 1979. Oyster diseases in Chesapeake Ga. Dep. Nat. Resour., Coastal Resour. Div., in the northeastern United States will Bay. Mar. Fish. Rev. 41 (1-2):45-53. Proj. 2-234-R, 44 p.
54(2),1992 5 Haskin, H. H., and J. D. Andrews. 1988. Uncer Lewis, E. J. 1988. Dermo (Perkinsus marinus), tion of undesirable organisms. In tainties and speculations about the life cycle SSO (Haplosporidium costale), and A. White (Editor), Shellfish diseases: of the eastern oyster pathogen Haplosporidium MSX (Haplosporidium nelsoni)--current im Current concerns in the northeast, p. 19-20. nelsoni (MSX). In W. Fisher (Editor), Disease pact on shellfish. Proc. Interstate Seafood Woods Hole Oceanogr. Inst., Tech. Rep. 87 processes in marine bivalve molluscs, p. 5-22. Sem., Oct. 1987, Virginia Beach, Va., p. 113 13. Am. Fish. Soc., Spec. Publ. 18. 132. Sindennann, C. J. 1970. Principal diseases of ---- and S. Ford. 1979. Development of Lyles, C. H. 1969. Historical catch statistics marine fish and shellfish. Acad. Press, N.Y., resistance to Minchinia nelsoni (MSX) mor (shellfish). U.S. Dep. Inter., Bur. Commer. 369 p. tality in laboratory-reared and native oyster Fish., Curro Fish. Stat. No. 5007, 116 p. ----. 1990. Principal diseases of marine stocks in Delaware Bay. Mar. Fish. Rev. 41 (1 Mackin, J. G. 1951. Histopathology of infection fish and shellfish. Vol. 2. Diseases of marine 2):54-63. of Crassosrrea virginica (Gmelin) by Derm shellfish. Acad. Press, San Diego, Calif, ----., W. J. Canzonier, and J. L. Myhre. ocysridium marinum Mackin, Owen, Collier. 516 p. 1965. The history of "MSX" on Delaware Bay Bull. Mar. Sci. GulfCaribb. 1(1):72-87. ----. In press. Attitudes and activities oyster grounds 1957-1965. Am. Malacol. ----, H. M. Owen, and A. Collier. '1950. of the International Council for the Ex Union Annu. Rep. 32:20-21. Preliminary note on the occurrence of a new ploration of the Sea (ICES) concerning in ----, L. A. Stauber, and J. A. Mackin, protistan parasite Dermocysridium marinum troductions of marine organisms. In 1966. Minchinia nelsoni n.sp. (Haplosporida, n.sp. in Crassostrea virginica (Gmelin). Sci A. Rosenfield and R. Mann (Editors), Dis Haplosporidiidae): Causative agent of the ence 111 (2883):328-329. persal of Jiving organisms into aquatic eco Delaware Bay oyster epizootic. Science McGladdery, S. E., R. J. Cawthorn, and B. C. systems, Md. Sea Grant ColI. Publ., Univ. Md., 153(3742): 1414-1416. Bradford. 1991. Perkinsus karlssoni n. sp. Call. Park. Heffernan, P. B., R. L. Walker, and J. L. Carr. (Apicomplexa) in bay scallops Argopecren ---- and A. Rosenfield. 1967. Principal 1989a. Gametogenesis cycles of three bivalves irradians. Dis. Aquat. Org. 10(2): 127-137. diseases of commercially important marine bi in Wassaw Sound, Georgia: I. Mercenaria Needler, A. W. H., and R. R. Logie. 1947. Seri valve mollusca and crustacea. Fish. Bull. mercenaria (Linnaeus, 1758). J. Shellfish Res. ous mortalities in Prince Edward Island oys 66(2):335-385. 8( I):51-60. ters caused by a contagious disease. Trans. R. Sprague, y. 1978. Comments on trends in re ----, , and I989b. Soc. Can. 41(3):73-89. search on parasitic diseases of shellfish and Gametogenesis cycles of three marine bivalves Perkins, F. O. 1988. Structure of protistan para fish. Mar. Fish. Rev. 40(10):26-30. in Wassaw Sound, Georgia: II. Crassosrrea sites found in bivalve molluscs. In W. Fisher USDOC. 1990. Fisheries of the United virginica (Gmelin, 1791). J. Shellfish Res. (Editor), Disease processes in marine bivalve States, 1989. U. S. Dep. Commer., NOAA, 8(1):61-70. molluscs, p. 93-111. Am. Fish. Soc., Spec. Natl. Mar. Fish. Serv., Curro Fish. Stat. 8900, Howard, D. w., and C. S. Smith. 1983. Histo Publ. 18. 111 p. logical techniques for marine bivalve mollusks. Quick, J. A., Jr. 1977. Fungus disease of oysters. Walker, R. J985. Growth and optimum seeding U.S. Dep. Commer., NOAA Tech. Memo. In C. J. Sindermann (Editor), Disease diagno time for the hard clam, Mercenaria mercenaria NMFS-F(NEC-25, 97 p. sis and control in North American marine (L.) in coastal Georgia. Nautilus 99(4): 127 Kern, F. G., L. C. Sullivan, and M. Takata. 1973. aquaculture, p. 198-203. Elsevier Sci. Publ. 133. Labyrinrhomyxa-like organisms associated Co., Amsterdam. ---- and C. M. Humphrey. 1984. Growth with mass mortalities of oysters, Crassosrrea ----, and J. G. Mackin. 1971. Oyster para and survival of the northern hard clam virginica, from Hawaii. Proc. Natl. Shellfish. sitism by Labyrinrhomyxa marina in Florida. Mercenaria mercenaria (Linne) from Geor Assoc. 63:43-45. Fla. Dep. Nat. Resour., Mar. Res. Lab., Prof. gia, Virginia, and Massachusetts in coastal Kinne, O. (Editor). 1983. Diseases of marine ani Pap. Ser. 13,55 p. waters of Georgia. J. Shellfish Res. 4: 125 mals. BioI. Anst. Helgol., Hamburg, FRG, Ray, S. M. 1954. Biological studies of Dermo 129. 1038 p. cysridium marinum a fungus parasite of oys ---- and K. Tenore. 1984. The distribu Leonard, D. L., M. A. Broutman, and K. E. ters. Rice Inst. Pamphl., Spec. Iss., Houston, tion and production of the hard clam, Mer Harkness. 1989. The quality of shellfish grow Tex., 113 p. cefwria mercenaria, in Wassaw Sound, Geor ing waters on the east coast of the United States. ----.1966. A review of the culture method gia. Estuaries 7(2): 19-27. U.S. Dep. Commer., OAA, Off. Oceanogr. for detecting Dermocysridium marinum, with Wood, J. L. and J. D. Andrews. 1962. Mar. Assessment, Wash., D.C., 31 p. suggested modifications and precautions. Proc. Haplosporidium costale (Sporozoa) associated Levine, N. D. 1978. Perkinsus gen. n. and other Natl. Shellfish. Assoc. 54:55-69. with a disease of Virginia oysters. Science new taxa in the protozoan phylum Api Rosenfield, A., and F. G. Kern. 1987. Shellfish 136(3517):710-711. cornplexa. J. Parasitol. 64(3):549. management strategies to control the introduc
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