A Review of Introductions of Exotic Oystersand Biological Planning for New Importations

JAY D. ANDREWS

Introduction

Oysters have been transported bymankind since Roman times becausethey are superbly adapted to with-stand long journeys out of water. Inthis paper, the consequences of man'smovement of oysters and the biologicalrequirements for future introductions ofoysters are reviewed.

Only one species of oyster, Crass-ostrea gigas, the Pacific oyster, hasbeen introduced as a successful mem-

ABSTRACT-Importation and trans-plantation of exotic oysters has probablyresulted in the introduction into new areasof more marine invertebrate species thanany other of man's activities. Unintentionalimroductions have resulted from carelessmovements of oysters without planning orconsideration of consequences. Diseasesand parasites of marine invertebrates arepoorly known and oysters cannot be ade-quatelv diagnosed or inspected for prob-lems by biologists. The vigorous Pacificoyster. Crassostrea gigas. was introducedto the Atlamic coast of western Europe inthe past decade with serious effects onnative oyster species. Some scientists pro-pose to introduce it to the Atlamic coast ofNorth America. primarily for culture inNew England. If imroduClion is carried outproperly, diseases and parasites mav beexcluded bv breeding selected brood oystersin hatcheries under quarantine conditions.The progeny mav then be tested in con-trolled natural environments for growthrates and reaction to native diseases andparasiles. Selection of races. strains. andhybrids may be pursued in hatcheries to fitexotic oysters to new ecosystems. Intro-duction -of an exotic species is a seriousirreversible evel1t which merits careful con-sideration of the reasons for culture ofa new shellfish and Ihe consequences tonative biOla Gnd coastal ecosystems.

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ber of coastal communities around theworld. In the temperate zone of theNorthern Hemisphere only the Atlanticcoast of North America does not nowdepend on this species for oyster pro-duction. Crassostrea gigas was suc-cessfully introduced to western NorthAmerica, western European, and Aus-tralasian coasts. Most introductions be-gan as casual unplanned events thatwere soon followed by deliberate oneson a larger scale. With the aid of man,the oysters spread on the coasts to thelimit of their tolerances of climatesand salinities.

Some scientists desire to culture C.gigas in New England. A major prob-lem is keeping it confined to NewEngland and away from large oysterfisheries of C. virginica to the south.Crassostrea gigas is a vigorous, fast-growing oyster that could compete ad-vantageously with the native oyster,and possibly replace it, in the warmwaters of Chesapeake Bay and Dela-ware Bay.

The famous European flat oyster,OSlrea edulis, has been tried on bothcoasts of North America and in Japa-nese waters with I ittle success as aself-sustaining species. It is frequentlygrown in hatcheries in North Americafor experimental plantings. This favor-ite raw-bar oyster sustains a smallindustry in Maine by use of hatchery

Jay D. Andrews is Senior Marine Scientist,Virginia Institute of Marine Science and Collegeof William and Mary, Gloucester Point, VA23062. This paper is Contribution No. 968 fromthe Virginia Institute of Marine Science andCollege of William and Mary. Views or opin-ions expressed or implied are those of the authorand do not necessarily reflect the position of theNational Marine Fisheries Service. NOAA.

seed from acclimated broodstocks pre-cariously established in Boothbay Har-bor, Maine (Welch, 1966).

Extensive transplantation of nativeoysters along major coasts has longbeen used to sustain fisheries withoutregard for adaptations of local races tonew environments. Transplantation offlat oysters from one country to anotherin Europe has a long history. It wasinstigated primarily because of failureof reproduction in the cold watersof northern countries such as France,Great Britain, the Netherlands, andDenmark (ICES, 1972). Crises such ascontinent-wide unexplained mortalitiesin 1920-21 and recent (1967-76) mortal-ities from diseases also caused exten-sive importations from the Adriatic Seaand Greece as well as Spain and Portu-gal. No consideration was given toracial traits of these diverse stocks foradaptation to various local climates(Andrews, 1979b). However, the Neth-erlands is trying to build up stocks ofisolated native oysters which exhibitgreater winter hardiness than importedFrench seed oysters now sustaining theindustry (Drinkwaard, 1978). Trans-plantation between regions on a coastis a short-term marketing expedientthat is not expected to contribute torehabilitation of native stocks. How-ever, it may result in genetic mixingand the spread of pests and diseases.

The impact of exotic marine specieson endemic communities is difficult topredict until they are widespread in thenew area and irrevocably established.Introductions of marine exotics aremore difficult to isolate and to co~trol than terrestrial ones because ofrapid dispersion of larvae by currents.

Inadequate monitoring and limitedknowledge of identity, abundance, anddistribution of native species may leaveexotic species obscured for long peri-ods. Often diseases of marine inverte-brates become known only after massmortalities of the host species (Sinder-mann, 1976). Seldom can such diseasesbe proven to be introduced. The strong-est circumstantial evidence is that oftiming when stocks were transplantedor imported immediately before anepizootic mortal ity.

Categories of Importations

The transport of endemic oysters ofthe same species along a coast is de-fined as transplantation (Mann, 1979).This is not the primary concern of thisdiscussion. After hundreds of years oftransplantation the potential for furtherdamage may be minimal. However,care should be exercised in movingendemic oysters from regions of a coastthat have been isolated by land barriers,ocean currents, or even temperaturedifferences for many centuries. Ex-changes between such areas on a coastcarry the same dangers from diseasesand pests as from importation of exoticoysters of a different species. Examplesof isolated regions in North Americainclude the Gulf of Mexico and theGulf of St. Lawrence from which trans-plantings to and from the Middle Atlan-tic coast have been rare. The Mediter-ranean Sea and the Atlantic coast ofEurope could also be hazardous regionsfor exchanges of oysters.

Importations of exotic species ofoysters that result in establishment ofnew populations are called introduc-tions to distinguish them from trans-plantations along a coast. Introductionsfrom one continental coast to anotherare nearly al ways through the acti vitiesand agencies of man because wide landor ocean barriers precl ude natural dis-persal. These importations may be de-Iiberate or accidental depending uponthe roleofman. They can be subdividedinto several categories according to thepurpose of the importation, agent ofdispersal, and stage of the organismutilized (ICES, 1972). For purposes ofdiscussion, casual im portations of smalllots of oysters without planning, super-vision, or subsequent monitoring may

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be considered accidental. The risks andconsequences are the same as for strict-ly accidental importations, i.e., inad-vertent introductions. Most large-scaleimportat:ons of oysters were precededby accidental ones on a small scale.These accidental importations may pre-pare the way sociologically for sub-sequent large-scale deliberate ones.Importee oysters may exhibit excellentgrowth and survival while native spe-cies are destroyed by exotic diseasesassociated with the importation. Thisseries of events occurred recently inFrance following importation of C.gigas in 1966 (Marteil, 1976).

Adaptations of Marine Organismsto Oceanic and Continental Climates

Continental air masses cro sing largeland masses exhibit the rapid heatingand cool ing attri butes of the land withstrong warming during summers andprolonged cooling from back-radiationin winters. Coastal waters on the east-ern shores of continents share theseextremes of atmospheric temperaturewith cold winter and warm summertemperatures. In contrast, coastal wa-ters on western shores of continents,bathed by moderated oceanic air mass-es, receive mi Id weather, therefore,exhibit cool summers and mild winters.Hydrocl imographs for estuaries on theeastern coast of North America showannual temperature ranges of 20°C ormore inshore, whereas those for thewestern coast exhibit only about 10°Crange (Andrews, 1971). These differ-ences in maximal and minimal meantemperatures affect adaptations forsummer breeding and winter survivalof endemic species on the respectivecoasts.

The temperature effects on importedexotic species are most dramatic onmaritime coasts which receive ocean-tempered air masses and currents thatinduce summer upwelling of deep, coldwaters. The resulting moderated watertemperatures and nutrient enrichmentfrom upwell ing ensure rapid growth ina continuous growing season for mostorganisms. Marine species native tocontinental-type climates with widedistributions and northern ranges aremost likely to establ ish populations oncoasts with oceanic climates. In con-

trast, organisms acclimated to mildoceanic cI imates are usually not ableto survive either summer or winter ex-tremes in severe climates of continen-tal-type coasts. These adaptations toclimates explain in large measure thenumerous invasions of exotic species inthe temperate zones on the westerncoasts of continents (Hanna, 1966)whereas introduced species are rare oneastern coasts. Tropical coasts are moreeasily invaded (Courtenay and Robins,1973).

In general, Ostrea species are adapt-ed to oceanic climates and Crassostreato continental ones, although excep-tions occur as waters along a coastbecome more tropical. Consequently,Ostrea species breed at lower summertemperatures (usually < 20° C) and aremore sensiti ve to low salinities and lowwinter temperatures. They will notwithstand intertidal exposure to heat orcold. Ostrea edulis and O. lurida arethe endemic species of western Europeand western North America, respec-tively; Crassostrea virginica and C.gigas are respective endemic com-mercial oysters of eastern shores ofNorth America and Asia. These adap-tations to respective climates should beconsidered before irreversible conse-quences of importations are incurred.Examples of serious alterations of bi-otic communities by importations ofexotic oysters with their associatedfaunas are found on the maritime coastsof western Europe and western NorthAmerica (Quayle, 1964; Hanna, 1966;Dundee, 1969; ICES, 1972).

Brief History of MajorIntroductions of Oysters

Crassostrea angulata FromPortugal and Spain to France

Crassostrea angulata, the Portu-guese oyster, is known to have thrivedin southwestern Portugal and southernSpain for several hundred years (Kor-ringa, 1970). The Sado and Tejo Riversand the Gulf of Cadiz provide waterswarm enough (>20°C) for reproduc-tion of this subtropical oyster. Theoysters were little used locally. Whenthe natural public beds of O. edulis insouthwest France and northern Spainwere depleted about 1850, a famous

Marine Fisheries Review

report by Coste (1861) to NapoleonIII initiated private culture. With ascarcity of O. edulis seed stocks, C.angulata was soon imported from Por-tugal's Sado River to stock privatebeds. The initial introduction of C.angulata to the French coast was at-tributed to the dumping of a shiploadof spoiling oysters in the GirondeRiver in 1868 (Marteil, 1976). Crass-oslrea angulata proliferated in theGironde and other areas of southwestFrance providing seed stocks for ahundred years. Eventually, in the1960's, it produced five times as manyoysters in France as O. edulis (Marteil,1970). Cold summer temperatures pre-vented the Portuguese oyster fromreproducing in Brittany and morenorthern countries; therefore it wastransplanted annually to Great Britainfor growth and marketing.

Although C. angulala was consid-ered to have a less desirable taste thanthe European flat oyster, it provided inabundance relatively inexpensive oys-ters for Europe. It was a useful intro-duction to supplement production ofthe more temperature-sensitive O.edulis which is slower and more diffi-cult to grow. The Portuguese oysteroften sets and grows intertidally whichoffers cultural advantages of pest con-trol and intensive visual farming atlow tides. It is difficult to judge theextent of biological competition inFrance because O. edulis was grownprimarily in Brittany and was over-fished and depleted in southwest Francebefore C. angulata was introduced.The Portuguese oyster certainly re-placed the flat oyster in the warmwaters of southern France where thelatter was native.

Crassostrea gigas FromJapan to France (1966)

A small importation of 900 kg ofseed of the Pacific oyster was intro-duced to the Marennes area of France inMarch 1966 (ICES, 1972). The follow-ing fall (November 1966), a new dis-ease was found in the gills of C.angulata by Trochon (Marteil, 1969,1976). The disease spread widely inFrance and in the fall of 1967 anembargo was placed on further impor-tations from Japan. However, the rapid

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decl ine in production of the Portugueseoyster from mortalities caused by thegill disease resulted in a decision toimport C. gigas in commercial quanti-ties in the early 1970's. In southwesternFrance, C. gigas reproduced prolifical-ly permitting the cessation of commer-cial importations after 1975.

Another disease appeared in O.edulis in Brittany in Aber Wrach in1968 where some Pacific oysters werebeing held. Aber Disease, caused bya protozoan, Marteilia refringens,caused extensive mortalities of flatoysters in Brittany. Crassoslrea gigaswas not appreciably affected by eitherof the new diseases. A shell malady ofC. gigas has affected marketing some-what (Marteil, 1976). Crassostreagigas has completely replaced C.angulala in French waters south ofBrittany and it has tended to breedfarther north in Brittany and in theNetherlands in warm summers suchas 1976 (23°C). Intensive spatfallsthrough 1976 in southern France re-duced the growth rate by crowding.

Crassostrea virginica (1869)and C. gigas (1902) toPacific Coast of North America

The native Olympia oyster, Ostrealurida, of this coast is small, slow-growing, and difficult to culture (Kor-ringa, 1976). Overfishing of naturalbeds caused depletion of most areas inthe last half of the 19th century. Afurther decline occurred in the mid-1920's despite adoption of Europeancultural methods of diked parks toprotect the cold- and heat-sensitiveOlympia oysters from exposure to airtemperatures. From 1928 to 1945, pulp-mill wastes were blamed for the declinein southern Puget Sound (McKernan etaI., 1949). The species did not recoverproduction appreciably after the pulp-mill was closed. Oyster planters turnedtheir attention to C. gigas in the late1920's. This species grew to market-able size in 2 years from importedJapanese seed whereas the Olympiaoyster required about 4 years to attainits maximum size of 2 inches. Ostrealurida did not fulfill the needs of aregion with rich waters suitable forextensive oyster culture.

The first importations of the eastern

oyster, C. virginica, began about 1869to San Francisco Bay with completionof transcontinental railroads (Hanna,1966). Shipments of oysters from NewEngland continued to various railpoints along the coast until about 1935.Growth was excellent in the early yearsbut failure of reproduction from lowsummer temperatures required regularimportations from the east coast.Crassoslrea virginica is now rare onthe Pacific Coast with one small per-sistent population in Boundary Bay,B.C. (Bourne, 1979). Importations overa period of 60 years failed to establ ishthe species. The cool California cur-rent and accompanying upwelling keptcoastal waters too cold for regularreproduction. Nevertheless, Califor-nia permitted regular importation andplanting of market-sized oysters fromLong Island for raw-bar trade in the1960's and 1970's. During this period,risks were high of introduction of newdiseases prevalent on the east coast.

CrassOSlrea gigas has supported agrowing industry along wide reaches ofthe Pacific Coast. The earl iest importa-tions were made by oriental residentsabout 1902 (Kincaid, 1951). Beginningin the late 1920's thousands of cases ofspat on shells were shipped from Japanon decks of ships (Quayle, 1964). Highprices and competition with air ship-ments to France greatly reduced PacificCoast importations from Japan in theearly 1970's. Fortunately, the industryhas developed its own seed supply overthe years. Two areas of regular spat-falls, Pendrell Sound, B. C. , and DabobBay, Wash., supplement seed suppliesfor growing areas with irregular or nosets (Quayle, 1969; Bourne, 1979).

Crassostrea gigas FromJapan to Australasia (1947-52)

Crassoslrea gigas became estab-lished in Tasmania about 25 years ago.Five shipments from Japan to Australiawere made between 1947 and 1952(Thomson, 1952, 1959; Bourne, 1979).Three races of Pacific oysters (Mi-yagi, Kumamoto, and Hiroshima) wereshipped as spat on shells and planted attwo sites. Oysters planted at Pittwateron the southern shore of Tasmaniasurvived well. Those exposed on theshores of southern West Australia died.

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One recent shipment (1970) from Japanconcluded the importations (Medcofand Wolf, 1975). Transplantations fromPittwater were made to Pt. Sorell on thenorthern shore of Tasmania where thespecies is now firmly established. Rela-ti ve isolation at Pittwater provided aperiod for observation of growth andmortalities before native oysters wereexposed. Unfortunately, all three raceswere planted in the same area and thesurviving race of accl imated oysters isnot known-probably Miyagi or Hiro-shima oysters or a mixture.

Scattered individuals of C. gigasappeared in New South Wales in the1970's where an important commercialfishery for C. commercialis is pursued(Medcof and Wolf, 1975). Some speci-mens were found on cultch sticks usedto collect native oysters, implying thatthey were derived from larvae origi-nating in the locality. The Pacific oys-ter outgrew the native oyster on thesesticks suggesting that environmentalconditions are favorable for growth.The location and source of brood oys-ters for spat found in New South Walesare unknown but probably they werederived from small accidental or illegalimportations from Tasmania. Dispersalhas been slow in Australasia providingopportunities to monitor population in-creases, and permitting industry adap-tations if C. gigas replaces the nativerock oysters. Four Australian states per-mit transplantings of C. gigas whereasNew South Wales, with a valuablefishery based on C. commercialis, doesnot. Crassostrea gigas appeared sud-denly in New Zealand in 1970 fromunknown sources (Dinamani, 1974) andis increasing rapidly in abundance.Further spread of C. gigas in temperatezones of Australasia is to be expected.

Introduction of Exotic InvertebrateSpecies Associated With Oysters

Exotic Invertebrate Speciesin Western European Waters

The most serious introductions offoreign species accompanied importa-tion of American oysters, C. virginica,to Great Britain. Reproduction did notoccur in the cold waters, therefore theywere relaid in British waters annuallyfrom the late 1800's to 1939 for growth

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and marketing (lCES, 1972). Amongthe exotic species introduced with oys-ters from North America was the pred-atory oyster drill, Urosalpinx cinerea,found in England in 1920. It is now wellestablished on the southeastern andsouthern coasts. A gastropod com-petitor, Crepidula fornicata, which at-taches to oysters in chains, exhibitedfantastic populations in England onderelict beds called "mud and lim-pets" after its introduction about 1880(Orton, 1937). [t spread to the conti-nent and is now distributed widelyfrom Sweden to France. It has pelagiclarvae but was probably spread mostlyby man while attached to mussels andoysters. Other American species prob-ably introduced with oysters, butexhibiting more subtle, noneconomiceffects, include the bi valves Petricolapholadiformis, Mya arenaria, and amud crab, Rithropanopeus harrisi, allnow with wide distributions in northernEurope (ICES, 1972).

The introduction of C. gigas toFrance has added some oriental spe-cies to the fauna but their eventualstatus after importations ceased in1975 remains to be determined (Gruetet aI., 1976). The parasitic copepodMytilicola orientalis may be the mostdestructive species introduced becauseit attacks both oysters and mussels.Sargassum muticum, an asiatic phaeo-phyte introduced with Pacific oysters,is establ ished on the coasts of Franceand England (Maurin and LeDantec,1979). [t is spreading and interfereswith the commercial species Chondruscrispus. Two other algal species havebeen introduced: Undaria pinnafida inthe Mediterranean Sea and Laminariajaponica on the Atlantic coast ofFrance. Fi ve add itional in vertebratespecies from the Orient have beencollected in Brittany, including anannel id, a bi val ve mollusk, an antho-zoan, and two barnacle species (Gruetet ai., 1976). The two oyster patho-gens that appeared immediately afterthe first introductions of C. gigas areprobably exotics from Japan also. Theelimination of the Portuguese oysterfrom France and the serious reductionof production of the flat oyster arethe most dramatic consequences ofim portation of C. gigas.

The importation of tropical C. rhizo-phorae, the mangrove oyster, fromFrench Guyana to France defies expla-nation. Why this oyster should beexpected to survive in the cold watersof the French Atlantic coast is notevident and its use in French oysterculture is obscure. Continued importa-tions present the threat of introducingoyster diseases and parasites of thewestern Atlantic (Maurin and Gras,1979).

Exotic Mollusks on thePacific Coast of North America

A long list of exotic biota introducedfrom New England and Japan has beencompiled by Hanna (1966) and Dundee(1969). The long periods of repeatedoyster importations offered many op-portunities for establishment of exoticspecies in this mild oceanic-type cli-mate. Species capable of breedingat temperatures of 20°C or less, orfinding warm niches, were successfulcolonizers. The introduced mollusksexemplify the opportunities providedimmigrant species by man's importa-tions. In the early years, no care wasexercised in cleaning shipments ofoysters from New England or Japan ofunwanted aliens. Bonnot found 22 spe-cies of marine shells in 20 boxes ofJapanese seed in 1930 (Hanna, 1966).

All three commercially importantbivalves on the Atlantic coast of NorthAmerica were imported early to theWest Coast. Mya arenaria, appar-ently introduced accidentally with oys-ter transplantations, was immediatelysuccessful because of its adaptationfor breeding at low temperatures. Itis now distributed from Alaska to SanDiego. The American oyster, C. vir-ginica, and the hard clam, Mercenariamercenaria, did not reproduce suc-cessfully which necessitated continuedimportations to produce crops. Bothspecies can be grown commercially onthe West Coast using hatchery seed.

Several western Atlantic mollusksclosely associated with oysters forfood or substrate achieved distribu-tions on the West Coast in localizedniches where oysters are grown. Theoyster predator, Urosalpinx cinerea, isoften found on oyster beds but not in all

Marine Fisheries Rel'ie\\'

areas where salinities are favorable.All three species of Crepidula (c.fornieata, C. eonvexa, and C. plana)were introduced but only C. fornieatabecame established with a preferencefor the warm diked waters used for O.lurida culture. Many imported exoticswere first observed with oysters inlocal seafood markets (Hanna, 1966).Modiolus (Guekensia) demissus wasvery common on the warm intertidalshores of San Francisco Bay during theyears of oyster imports and was some-times marketed. The common east-ern mud snail, Nassarius (Ilyanassa)obsoletus, is now localized in warmbays where C. virginiea was imported.Several small mollusks such as Gem-ma gemma from the East Coast andBatillaria zonalis from Japan arewidely established in Puget Sound andCalifornia. Some mollusks, e.g., Areatransversa and Busyeon eanalieulatus,were present only as long as importscontinued because they did not breed.

The most spectacular accidental in-vasion of West Coast ecosystems wasmade by the Japanese clam Venerupisjaponiea. It has a wide distribution andgreat abundance in Japan. It has beenhighly successful on the West Coastand has filled a warm intertidal nichenot occupied by native clams (Quayle,1964). It is widely accepted both eco-logically and as a convenient shellfishfor human food. Several species ofVenerupis endemic to western Europeare also used for food, and are culturedthere in hatcheries for commercialplantings. The Japanese oyster drill,Oeenebra japoniea, is common onWest Coast oyster beds from acci-dental importations.

Two non molluscan species intro-duced to the West Coast from Japanare serious parasites of oysters andmussels. The flatworm predator Pseu-dostyloehus ostreophagus kills oysterspat in Puget Sound and is difficult tocontrol. A macroscopic red copepod,Mytilieola orientalis , infests intestinaltracts of mollusks which affects theirglycogen condition and saleability(Glude, 1975). This copepod genus ismore serious as a parasite of musselsthan of oysters. An extensive literatureexists on M. inteslinalis, the west-ern European species (Marteil, 1976).

December 1980

Parasites and diseases have the ad-vantage of often being able to attacknew hosts when introduced to a newecosystem, and they survive transpor-tation easily in mollusk hosts.

The Role of Importations inSpreading Diseases and Parasites

Along any given continental coastthere are marine communities, iso-lated for thousands of years by phys-ical barriers, that had no opportunityto exchange fauna with neighboringareas until modern man and his trans-portation arrived. Many races of C.virginiea occur along the North Atlanticcoast of America (Stauber, 1950) andthey appear to have retained theirgenetic traits despite much transplant-ing between regions. By transplantingoysters across these natural barriers,man has provided many opportunitiesfor parasites and diseases to findsusceptible hosts.

Malpeque Bay Diseasein Canada (1914)

The most infamous mortality of oys-ters in North America was caused byMalpeque Bay Disease in the east-ern Canadian provinces (Needler andLogie, 1947). Oysters from New En-gland were imported into MaJpequeBay, Prince Edward Island, in 1914.This was to supplement reproductionwhich had become inadequate fromoverfishing and depletion of stocks(Needler, 1931). A severe mortal ityfirst occurred in 1915-16 and theepizootic continued until about 1930.The native oysters achieved resis-tance in a few generations, but over along period due to infrequent spatfalls(Logie, 1956). The disease spreadslowly around the bays of the Islandand in 1952-55 it spread to tributariesof mainland New Brunswick in the Gulfof St. Lawrence. The causative orga-nism has not been demonstrated al-though exposure of susceptible oystersfrom Bras d'Or Lakes shows that thepathogen is still present. Curiously,the disease has not been associatedwith mortalities in the New Englandarea from which it was supposed tohave originated.

Delaware BayDisease On Mid-AtlanticCoast of NorthAmerica (1957)

The oyster industry of the Mid-Atlan-tic Coast was crippled by the sporozoanpathogen Minchinia nelsoni whichappeared in Delaware Bay in 1957(Haskin et aI., 1966), and in Chesa-peake Bay in 1959 (Andrews and Wood,1967). More than 90 percent of oystersgrowing in the two bays in waters> 15%0 salinity were killed within 2years.

The origin of this disease is un-known but imported oysters is a likelyexplanation (Rosenfield and Kern,1979). Many small lots of exotic oys-ters have been planted along the EastCoast from Louisiana to Maine (Dean,1979). Often mature oysters werebrought in secretly so that no recordsof the origins or the histories of im-portations exist. A few examples willillustrate the pattern of these carelessimportations.

Recently, C. gigas from the WestCoast of North America was planted inMaryland waters by a seafood dealerwhich resulted in a specific law in thatState prohibiting the species. The oys-ters were recovered as completely aspossible by scuba diving. An oyster-man from Delaware saw impressivespecimens of C. gigas at the SeattleWorld's Fair in 1962 and he had somesent to his home state for planting. Theoysters were confiscated by a biologistwho held them in trays in open watersin Rehoboth Bay, Del., for severalyears without serious mortality or ap-parent successful reproduction. Crass-oslrea gigas was apparently resis-tant to Delaware Bay disease whichat that time killed C. virginica inRehoboth Bay.

A bushel of C. gigas was planted inBarnegat Bay, N.J., in the early 1930's.These oysters failed to grow, which isunusual for this species, and they diedover a 2-year period. A shipment of C.cucullala (= C. commercialis) failed tosurvive air travel from Australia to NewJersey in the care of T. C. Roughley(Nelson, 1946). Two eminent scien-tists were invol ved which reflects theattitude toward importations at that

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time. None of these known incidentsfits precisely the timing of arrivalof the pathogen M. nelsoni in Dela-ware Bay.

For about 6 years prior to the ap-pearance of Delaware Bay disease,seed oysters from the James River andSeaside of Eastern Shore, Virginia,had been transplanted to DelawareBay in large quantities. It is nowknown that Seaside oysters are infectedwith an endemic pathogen, Minchiniacostalis , which is closely related toM. nelsoni (Andrews, 1979a). Possiblyby hybridization or mutation, a newvirulent race of pathogens arose inDelaware Bay waters (Andrews, 1968).However, I believe it is more likely thatthe pathogen M. nelsoni was intro-duced from Asia.

Sacculinid Parasiteof Mud Crabs IntroducedFrom Gulf of Mexico (1962-63)

One last example can be documentedof an oyster transplantation that greatlyaltered crab populations in Virginia.This event illustrates the complexity ofsuch faunal changes. Disruption of oys-ter production in Virginia by DelawareBay disease caused oystermen to searchfor new sources of supply. Live oysterswere trucked from the Gulf of Mexico(Louisiana, Texas, and Florida) to Vir-ginia for shucking at waterside plantswhere shells and wastes were discardednear native oyster beds.

A year or two after importationsbegan (1962-63), two dominant speciesof mud crabs, Eurypanopeus depressusand Rithropanopeus harrisi, werefound to be infested with a castrat-ing sacculinid (cirripede) parasite(Loxothylacus panopaei) (Van Engelet a!., 1966). These formerly dominantcrab species, which were major scav-engers of dead oysters, soon becamescarce and have remained rare for 15years to the present. A third crabspecies, Neopanope texana sayi, for-merly rare on oyster beds in Chesa-peake Bay, became abundant and isnow the dominant mud crab. It is notsusceptible to the parasite.

Fortunately, no new oyster diseaseswere introduced with these Gulfof Mexico transplantations. It is sus-pected that another disease caused

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by Perkinsus marinus (formerly Der-mocystidium marinum) was introducedto Chesapeake Bay with seed oystersfrom South Carolina or the Gulf ofMexico prior to 1940 (Andrews andHewatt, 1957).

Biological Planningfor New Importations

The rationale for introducing newspecies of commercial organisms isusually economic and political, and notbased on biological need. It could beargued that survival of the fittest is themost rational way to handle exoticoysters. Presumably, this could be jus-tified by the success of Crassostreagigas, the Pacific oyster, on the majoroyster-growing coasts of the temperatezones of the world. It has succeededbiologically in western Europe, Tas-mania, New Zealand, and the WestCoast of North America as well as itsnative areas on eastern Asian coasts. Itis vigorous, fast-growing, relativelydisease resistant, and increasingly ac-cepted as a raw-bar oyster due torapidly changing economic and socialmores (Bourne, 1979). Why not acceptthis superior oyster as the standard fortemperate zone ostreid culture? Crass-ostrea gigas was also tried in tropicalregions of the South Pacific with poorresults (Bourne, 1979). Fortunately,most consultants and FAO officials arerecommending use of native oysters inthe tropics.

The French decision to introduce C.gigas has greatly altered oyster culturein Europe (Marteil, 1969,1976). Frenchoyster growers are adapting the tech-nology of culture to C. gigas with newcultural methods and using new areasin Brittany where C. angulata was notgrown. After excessi ve spatfalls oc-curred in the early 1970's, culminatingin the hot summer of 1976, there havebeen spa:fall failures. The effects ofthe parasitic copepod Mytilicola orien-talis and introduced foul ing organismsare yet to be determined. The rapidspread of gill disease resulted in elim-ination of C. angulata, the Portugueseoyster, from France, and Aber diseasecaused a severe decrease in Ostreaedulis production (Alderman, 1979).

Once introduced into southernFrance, it wa probably inevitable that

the Pacific oyster would spread rap-idly in Europe. The economic andpolitical decision to hasten the replace-ment of C. angulata by C. gigasinvolved additional risks, but sustainedthe French industry without seriousreductions in total production (Maurinand LeDantec, 1979). The Atlanticcoast of France was the major source ofseed of O. edulis for Holland andsome C. angulata for Great Britain.The cutoff of seed oysters encourageddevelopment of hatcheries in GreatBritain to produce C. gigas spat forEngland, Germany, and France. Crass-ostrea gigas is now established as wildstocks in Holland and also grown inthe Adriatic Sea and the MediterraneanSea (France).

The proponents of use of C. gigasin New England argue that land andcold water barriers would prevent lar-vae from spreading southward (Dean,1979). But man is the problem. No lawsor regulations will prevent the touristsin Maine from taking home to Chesa-peake Bay waters live oysters soldfor raw consumption. From Massa-chusetts southward the warm summersof our continental climate should per-mit C. gigas to reproduce successfully.The spatfalls could be excessive andcover all objects in the water as hasoccurred in the Arcachon area ofFrance. Crassostrea virginica alreadyexhibits this tendency in South Caro-lina, Georgia, and some areas of theGulf of Mexico. It is not conduciveto production of quality oysters (Hop-kins, 1954).

The careful introduction of C. gigasinto Maine through hatcheries and quar-antine methods to avoid diseases andpests (Andrews, 1979) is most desirablein contrast to the French approach ofmass importation. Yet elimination ofmany agents of biological control pro-vides the exotic species with a con-trived advantage in competition withthe native oyster. Provided it does notencounter an endemic disease to whichit is susceptible, the Pacific oystershould thrive on the Atlantic coast.This species is an intertidal oysterwhose breeding populations escapemany subtidal enemies. Miyagi oysters(northern race) also tend to reproduceand grow in slightly colder waters

Marine Fisheries Review

than comparable native races (Hickey,1979). The argument that C. gigashas had opportunities to establish it-self through careless importations isnot persuasive because circumstancesand conditions of importation werenot known.

Attitudes and Rationalesfor New Introductions

It is no longer tolerable to permit thewhims of individual citizens and scien-tists to determine the distribution ofexotic species in an increasingly cos-mopolitan manner. Courtenay andRobins (1973) described the minimalresearch and public review activitiesthat should precede intentional intro-ductions even for the best of rationales,such as biological control of estab-lished pests. It should not be necessaryfor each state or country to prohibiteach species individually by specificlaws. All marine importations shouldbe made under appropriate licensingauthority after public review and withclear obligations of control of orga-nisms and responsibility for negativeconsequences. In the case of commer-cial species such as oysters, exporta-tions should be subject to the samecontrols as importations. They shouldnot remain private decisions of indi-viduals or agencies whose motives maybe profit or ego satisfaction.

The rationale or reasons for intro-ducing a new oyster species must offermore advantages than just bringing anew competing species to a coastline.Importations may benefit one sector ofa coast and endanger a commercialindustry in another sector. It is impor-tant to determine how widely the newspecies will spread naturally and withman's help. Except for special niches(e.g., Pendrell Sound), C. gigas doesnot reproduce regularly on the PacificCoast of North America, yet it spreadwidely during occasional warm yearsand persists without recruitment asbreeding populations for many years(Quayle, 1969).

Ostrea edulis is now grown in Maineby hatchery reproduction from a smallwild population adapted to the Gulf ofMaine over a 30-year period (Welch,1966). The flat oyster is a temperature-

December 1980

sensitive species that does not survivein the warm summer waters of Chesa-peake Bay. It does not pose a threat interms of growth and competition withthe cultured native oyster south ofNew England. However, careless im-portations could introduce diseases andpests. The European shell disease pre-fers warm waters (Alderman and Jones,1971). If imported, it could have disas-trous effects on native oysters alongour coast. It is reported to occur inflat oysters on Prince Edward Islandin open waters after hatchery rearingin quarantine 1

It is assumed that future importationsof shellfish species will be made underquarantine conditions using hatcheriesto produce disease-free and parasite-free progeny for testing and eventualrelease in open waters. This techniquehas proven to be feasible with oysters,and it overcomes the most seriousproblems of introductions in the past.However, this method is slow andhas not been practiced in distributingC. gigas to Europe in recent years,except in Great Britain (Walne andHelm, 1979).

The times and quantities of recentFrench importations are not readilyavailable in the literature despite thelarge volume of papers on the newdiseases. No description of C. gigasimportations is given in a comprehen-si ve review of French shellfish culture(Marteil, 1976). An uninformed readermay not realize that the Pacific oyster isan exotic species in France. Ranson(1967) showed that the prodissoconchsor larval shells of C. gigas andC. angulata are indistinguishable andMenzel (1974) claimed they are thesame species. Even if the oysters areaccepted as cospecific, isolation fromeach other for several centuries is cer-tain to have altered their immunities todiseases. Pathogens similar to thosecausing mass mortalities in easternNorth America and western Europehave been found in Asiatic and Austra-lian oysters (Kern, 1976; Sindermann,1976; Perkins and Wolf, 1976). Trial

'Drinnan, R. E., Fisheries and EnvironmentCanada, Halifax, N.S., Canada. Personal com-mun., 1979.

introductions of shellfish into severalcountries of Europe are documented byICES (1972).

Competition WithNative Species

The most important aspect of com-petition is the ability of exotic oysterspecies to reproduce successfully innew environments. On oceanic-typecoasts in the temperate zone, C. gigasis limited in its reproduction by lowsummer temperatures. However, it issuccessful to the point of severe crowd-ing in southwestern France. Tempera-tures for breeding are no problem forCrassostrea species on coasts with con-tinental-type climates. However, theraces of C. gigas evolved in Japan withsalinities near oceanic level may nottolerate the low salinities found inChesapeake Bay and other southernestuaries during winter and spring.

The amount of competition betweenexotic and native species depends uponusage and relative adaptations of exot-ics to the new environments. In aregion, such as northern Europe or NewEngland, that depends on hatchery-pro-duced seed oysters, there is no re-productive competition. Therefore, themost serious problem is eliminated. Inthe Netherlands, C. gigas has repro-duced naturally in two recent years andcompetition with O. edulis may occurfor space and food. However, Crass-ostrea species tend to set and survivemost intensively in intertidal zoneswhich reduces the competition forspace. Crassostrea gigas grows fasterthan its nati ve competitors in Australia(Medcof and Wolf, 1973), westernEurope (Marteil, 1976) and easternNorth American (Hickey, 1979).

Excessive reproduction of oysters inan area results in slow growth andstunting. This is characteristic of seedoyster areas. Accumulation of succes-sive year classes of young oysters ongrowing stocks is particularly harmfulwhen shellfish are intended for raw-bartrade, as in Europe where appearanceis important.

When crowding of oysters encom-passes most growing areas of a region,such as in Seaside Virginia, SouthCarolina and Georgia coasts, and many

7

Gulf of Mexico estuaries, harvestingmay require steaming and shakingout meats for canned products. Thesecanned oysters involve much wasteof small oysters and they bring thelowest price of all shellfish prepara-tions (Lunz, 1954). Excessive repro-duction in an estuary or region inhibitsefficient culture and is almost impos-sible to alleviate.

The potential effect of excessi vepopulations of exotic oysters on otherspecies in an ecosystem can only be sur-mised. Predators, diseases, parasites,and fouling organisms are likely toincrease when excessive abundance ofan exotic occurs from an irreversibleintroduction. The full consequencescan only become apparent with time.The most desirable introduction wouldbe one where reproduction of the spe-cies is limited by temperatures or iso-lated by hydrography to a few favorableseed areas. This now occurs in Dela-ware Bay and Chesapeake Bay with thenative oyster C. virginica. A goodexample of a successful introduction ofa species with limited reproductionareas is C. gigas on the West Coast ofNorth America.

Importance of Races

There are many races of C. virginicaalong the Atlantic Coast of NorthAmerica. These were first recognizedbecause southern oysters failed to breedin New England waters (Stauber, 1950).Morphological traits of shell thicknessand shape persist when oysters fromseveral regions are grown in trays inChesapeake Bay. Differences in sus-ceptibility and resistance to diseasesare exhibited by races not previouslyselected by the pathogens (Andrews,1968). Isozyme characterization hasshown regional genetic differencesalong the Atlantic Coast2 despite muchtransplanting.

Experience has taught oystermen touse local seed oysters if available.Some disastrous losses occurred inoysters transplanted from other regions.Thin-shelled oysters from Seaside of

2Anderson, W. W. University of Georgia,Athens, Ga. Personal commun.

8

Eastern Shore, Va., suffered severedrill predation when introduced to Del-aware Bay in the 1950's. South Carolinaoysters showed severe winter kills andremained poor when transplanted toSeaside of Virginia. The MalpequeBay disease in Canada followed trans-plantation of New England oysters. Itis the classical example of the conse-quences of mixing oyster races alonga coast.

In Virginia, at least three races ofoysters are known by growth habits,shape, and susceptibility to diseasesand predators. Most distinctive are fast-growing thin-shelled Seaside oysters.Spatfall is excessi ve and predation in-tensive. Therefore, rapid growth andearly harvesting are necessary. Onemight attribute all these traits to theenvironment, but the oysters fail togrow and survive well in low salinitywaters within Chesapeake Bay. In con-trast, Potomac River oysters are accli-mated to low salinities, but are notablefor their susceptibility to diseases, par-ticularly Minchinia nelsoni (Andrews,1968). They, too, exhibit vigorousgrowth and achieve larger sizes thanSeaside oysters. The typical oysterof Chesapeake Bay is exemplifiedby James River seed oysters whichNelson3 believed were geneticallyselected for slow growth by 100 yearsof tonging the largest ones for market.Their small mature size may be a con-sequence of early stunting in the un-favorable growing conditions of JamesRiver. These three races illustrate thegenetic adaptations necessary to growoysters in only one region of the At-lantic coast.

In Europe, winter hardiness ofOstrea edulis is a problem when seedoysters are transplanted from regionswith warmer climates. Since the severewi nter kill of nati ves in 1962-63, theNetherlands is dependent on seed oys-ters from Brittany. A culture of onewarm-season is followed because theFrench race is less hardy than natives(Korringa, 1976). There is also thethreat of Gill and Aber diseases fromimporting French oysters.

3Nelson, T. C. Rutgers University, New Bruns-wick, N.J. (Deceased). Personal commun.

In eastern Canada, Ostrea edulisintroduced from Conway, Wales, in1957-59 did not survive the cold win-ters. A stock from Holland (Loosanoff,1955) was found to be hardy in PrinceEdward Island (Medcof, 1961) afternearly three decades of selection in thecold waters of the Gulf of Maine.

Even vigorous C. gigas may en-counter difficulties in adaptation alongthe Atlantic coast from low salinities,warm climates, and diseases and pred-ators. Depending upon the races intro-duced from Asia, the species couldbe limited to certain areas and hydro-graphic regimes. Since numerous racesof C. gigas probably occur along theAsian coast, it would be advantageousto fit each new region with a race from acomparable climate on the coast oforigin (Newkirk and Haley, 1977).Much needs to be learned about raceswith respect to diseases, climates, andgenetic parameters of oysters beforethis is done. To learn by trial and errorfrom hasty, unplanned imports has un-acceptable risks for the industry andfor the stabil ity of present ecosystems.

The Role ofHatcheries in Importations

Most importations of exotic oystersin the past have been from natural setsof adult oysters or spat on shells grownin open waters. This made inspectionsfor diseases and pests difficult if notimpossible. The development of com-mercial and experimental hatcheriesin most major oyster-growing areasof the world has made it possible toavoid these problems. Hatchery-rearedspat of 2-5 mOl may now be obtained afew weeks after setting without expo-sure to natural waters. Thousands oftiny live spat are shipped safely by air todistant countries at small cost. Thesubsequent handling of tiny spat incommercial numbers to prevent preda-tion and smothering is tedious andcostly, however.

To avoid these problems of earlyhandling of cultchless spat (Andrewsand Mason, 1969), many hatcherieshave returned to the technique of set-ting on shells or shell fragments whichfacilitates early planting on oyster beds.These lots must soon be planted in open

Marine Fisheries Review

waters and hence carry the same risksas wild oysters for importations. In thedecade between 1966 and 1975, theFrench imported 500 tons of adultoysters and 7,100 tons of spat on shells.All of these were wild oysters fromBritish Columbia, Canada, and Japan,respectively.

Preimportation StudiesNeeded and Controls Required

The rationale for introduction of C.gigas is based on its vigor and fastgrowth. It appears to grow faster andduring the cold season longer thannative C. virginica. This applies onlyto the Miyagi race which is the only onetried in most new areas.

Crassostrea gigas presents the po-tential difficulties of: I) Competitionand hybridization with C. virginica,2) probable susceptibility to somenati ve diseases, and 3) some questionas to its marketability as raw oystersin competition with the native oyster.It also may be expected to spread allalong the North Atlantic coast andcompete d irectly wi th nati ve C. vir-ginica for food and space in nearlyall sal inity regimes and en vironments.One must be prepared for replacementof the native oyster.

In the opinion of the author, C. gigascould be a useful species in NewEngland where artificial reproductionin hatcheries can compensate for failureof natural spatfalls. However, based onhatchery seed, O. edulis and selectedstrains of C. virginica offer equal orbetter opportunities for culture of raw-bar oysters. Crassostrea gigas presentshigh risks in southern waters where itmay be expected to reproduce naturallyand to compete strongly and possiblyinterbreed with native oysters. Theseadvantages and disadvantages of C.gigas will be discussed and contrastedfor two large sectors of the coast,south and north of Long Island, NY

The oyster-producing areas in thestates south of Long Island generallyhave adequate spatfalls of C. virginicarather regularly, or they have the poten-tial to yield large seed oyster crops ifproperly managed. The resurgence ofDelaware Bay seed beds in the 1970's

December 1980

after severe losses to Minchinia nelsoniin the 1960's is evidence of this capac-ity. Moreover, the oyster industries inthe south are much more productivethan those in the north despite muchlower market prices and greater prob-lems of diseases and predators.

North of Long Island, the majoroyster crop is raw-bar oysters whichsell for high prices thus compensatingfor relatively low production. Supplyof seed oysters is a constant problemin the north except in occasional yearsof intensive sets. Furthermore, slowgrowth in cold waters prolongs thecycle of marketable crops.

These factors provide a division ofinterests in use of exotic oysters andproduction of seed oysters in hatch-eries. In the north, the cost of hatcheryseed is not prohibitive where naturalspatfalls do not occur, and the fast-growing C. gigas has an added appeal.Drinnan ~ reported that C. gigas out-grew C. virginica at Ellerslie, PrinceEdward Island, 4 to I by dry meatweights over a period of 12 months inopen waters. A recent report on tray-grown spat of the two species in aMassachusetts cove closed to a pond inthe warm season also found fastergrowth in C. gigas (Hickey, 1979).Another commercial operation usingC. virginica hatchery spat in trays isbeing conducted by Cotuit Oyster Co.5

because of scarcity of natural seedin Massachusetts (Matthiessen, 1979).Biologists in Maine would like to re-place native C. virginica with hatchery-grown C. gigas, along with hatcheryseed of O. edulis already being grownin floats (Dean, 1979). The failure ofC. gigas to reproduce in Massachusettsand Maine waters is a strong argumentfor use of hatchery seed in these north-ern waters. The risk of these exoticspecies spreading is thereby minimized.

In the southern sector of the NorthAtlantic coast, faster growth of C.gigas may be completely nullified bylosses resulting from native diseases,

4Drinnan, R. E. Fisheries and EnvironmentCanada, Halifax, .S., Canada. Personal com-mun., 1973.5Mention of trade names or commercial firmsdoes not imply endorsement by the NationalMarine Fisheries Service, NOAA.

slower growth in warm summer tem-peratures, and due to low salinities inseed areas. The fouling of native orexotic oysters on growing and fatteningbeds by heavy spatfalls of C. gigaswould be disastrous to the Mid-Atlanticcoast industry. Hatchery productionof seed oysters in the south is noteconomically feasible yet. Unless C.virginica is replaced by C. gigas, theproblem of separation for marketing oftwo easily distinguished species grow-ing side by side may occur. Both qualityof meats (fatness and taste) and differ-ences in appearance of meats and shellswill probably be noticeable to con-sumers. The proximity of C. gigasin New England would enhance thechances of accidental introductionin the south. Self-appointed "experi-mentel's" could easily buy shell stockin Maine and transplant it to Chesa-peake Bay for later "eating." Enact-ment and enforcement of laws to protectagainst this type of transplanting are notfeasible. Canadian importations of bothC. gigas and O. edulis are not dis-cussed further since additional barriersof distance, cold waters, and a nationalboundary provide added protection.

Introduction of C. gigas cannotstrictly be said to have occurred in NewEngland until natural wild populationsoccur, although some oysters are beingheld in Maine and Massachusetts. Inthe south, where it is not needed, muchadditional information should be col-lected before releasing this species inopen waters. The necessary tests aregoing to be difficult to conduct, con-trol, and interpret within quarantinesystems. Needed topics of study in-clude the following items.

I) Characterization of major nativeseed-source populations in eastern Asiaand along the North American Atlanticcoast before mixing and hybridizationoccur. This involves isozyme tests oflarge wild breeding populations ingenetic equilibrium (Hardy-Weinburglaw). This procedure is costly andtedious, and depends upon how manyenzyme systems need to be tested andthe number of oysters required to char-acterize races.

2) Testing of races of exotic andnative oysters for critical temperatures

9

and sal inities that induce gonad matura-tion, spawning, and favorable growthof larvae. Tolerances to salinity re-gimes and reactions to temperature andsalinity parameters in terms of survivaland growth are needed for each speciesand its major races.

3) Long-term monitoring of exoticspecies in their native habitats for prev-alences and effects of oyster diseasesand parasites; and testing of exoticoysters for susceptibility to diseasesnative to proposed sites of importation.This involves coordination of researchefforts in two widely separated regionsor countries. Testing exotic speciesagainst native pests may prove difficultwithout exposure in open waters. Dis-eases may be unknown for certainregions and artificial infection tech-niques have not been developed forother pathogens and parasites.

4) Evaluation of comparati ve growthrates under various conditions of bot-tom types, intertidal exposure, depths,and phytoplankton regimes. The meth-od of culture strongly influences growthrates and glycogen deposition. Oystersgrow faster when suspended in thewater, but currents, seasonal tempera-ture regimes, duration of spawningseason, and substrate type greatly in-fluence growth and fattening.

5) Exploration of hybrids and se-lected strains for particular uses andadaptation to localities and needs. Theavailability of hatcheries provides greatopportunities for hybridizing speciesand races and selection of superiorstrains to meet special conditions. Oys-ters resistant to sporozoan diseaseshave already been selected.

Literature Cited

Alderman, D. 1. 1979. Epizootiology of Mar-teilia refringens in Europe. Mar. Fish. Rev.41(1-2):67-69.

____ , and E. B. G. Jones. 1971. Shelldisease of oysters. Fish. Invest. Minist. Agric.,Fish. Food (G. B.), Ser. II, 26(8), 19 p.

Andrews, J. D. 1968. Oyster mortality studies inVirginia. VII. Review of epizootiology andorigin of Minchinia nelsoni. Proc. Natl. Shell-fish Assoc. 58:23-36.

____ . 1971. Climatic and ecological set-tings for growing shellfish. In K. S. Price, Jr.and D. L. Maurer (editors), Proceedings of theconference on artificial propagation of com-mercially valuable shellfish-oysters-Octo-ber 22-23, 1969, p. 97-108. Univ. Delaware,Newark.

1979a. Oyster diseases in Chesa-

10

peake Bay. Mar. Fish. Rev. 41(1-2):45-53.1979b. Scenario for introduction of

Crassostrea gigas to the Atlantic Coast ofNorth America. In R. Mann (editor), Exoticspecies in mariculture, p. 225-231. The MITPress, Cambridge, Mass.

____ , and M. Castagna. 1978. Epizootiol-ogy of Minchinia costa tis in susceptible oys-ters in Seaside bays of Virginia's EasternShore, 1959-1976. J Invertebr. Pathol. 32:124-138.

____ , and W. G. Hewatt. 1957. Oystermortality studies in Virginia. II. The fungusdisease caused by Dermocystidium marinumin oysters of Chesapeake Bay. Ecol. Monogr.27:1-26.

____ , and J. L. Wood. 1967. Oystermortality studies in Virginia. VI. History anddistribution of Minchinia nelsoni, a patho-gen of oysters, in Virginia. Chesapeake Sci.8:1-13.

____ , and L. W. Mason. 1969. Cultchlessseed oysters being developed. Md. Dep. Chesa-peake Bay Aff., Commer. Fish. News 2(6).

Bourne, N. 1979. Pacific oysters, Crassostreagigas (Thunberg), in British Columbia and theSouth Pacific Islands. In R. Mann (editor),Exotic species in maricullUre, p. I-53 TheMIT Press, Cambridge, Mass.

Coste, P. 1861. Voyage d'exploration sur Ielittoral de la France et de I·ltalie. Seconded. Paris.

Courtenay, W. R., Jr., and C. R. Robins. 1973.Exotic aquatic organisms in Florida with em-phasis on fishes: a review and recommenda-tions. Trans. Am. Fish Soc. 102:1-12.

Dean, D. 1979. Introduced species and the Mainesituation. In R. Mann (editor), Exotic speciesin mariculture, p. 149-164 The MIT Press,Cambridge, Mass.

Dinamani, P. 1974. Pacific oyster may posethreat to rock oyster. Catch 74, Fish. Manage.,Div. Minist. Agric. Fish., Wellington, N. Z.1(6):5-9.

Drinkwaard. A. C. 1978 Molluscs. Int. Counc.Explor. Sea Shellfish Committee Admin Rep.

Dundee, D. S. 1969. Introduced molluscs of theUnited States. Malacologia 9:264.

Glude, J. B 1975 A summary report of PacificCoast oyster mortality investigations 1965-1972. In ?roceedings of the third U.S.-Japanmeeting on aquaculture at Tokyo, Japan.October 15-16, 1974, p. 1-28. Jpn. Sea Reg.Fish. Res Lab., Niigata.

Gruet, Y, M. Heral, and J-M. Robert. 1976.Premieres observations sur I' introduction de lafaune associee au naissain d 'hultres japonaisesCrassostrea gigas (Thunberg), importe surla cote atlantique fran~aise. [In Fr., Engl.summ.] Cah. BioI. Mar. 17:173-184.

Hanna, G. D. 1966. Introduced mollusks ofwestern North America. Occas. Pap. Calif.Acad. Sci 108 p.

Haskin, H. H., L.A. Stauber, and J. A. Mackin.1966. Minchinia nelsoni n. sp. (Haplosporida,Haplosporidiidae): causative agent of the Del-aware Bay oyster epizootic. Science (Wash.,DC.) 153:1414-1416.

Hickey, 1. M. 1979. Culture of the Pacific oyster,Crassostrea gigas, in Massachusetts waters.In R. Mann (editor). Exotic species in maricul-lure, p. 129-148. The MIT Press, Cambridge,Mass.

Hopkins, S. H. 1954. Oyster setting on the GulfCoast. Proc. Natl. Shellfish. Assoc. 45:52-55.

ICES. 1972 Report of the working group onintroduction of non-indigenous marine organ-isms. Int. Counc Explor. Sea. Coop. Res.

Rep. 32, 59 p.Kern, F. G. 1976. Sporulation of Minchinia sp.

(Haplosporida, Haplosporidiidae) in the Pa-cific oyster Crassostrea gigas (Thunberg)from the Republic of Korea. J. Protozool.23:498-500.

Kincaid, T. 1951. The oyster industry of WillapaBay, Washington. The Tribune, Ilwaco,Wash., 45 p.

Korringa, P. 1970. The basic principles of shell-fish farming on the continental coast of Eu-rope. In Proceedings of the Symposium onMollusca. Part III, p. 818-823. Mar. BioI.Assoc. India Symp. Ser. 3.

____ . 1976. Farming the flat oysters of thegenus Ostrea. Dev. Aquaculture Fish. Sci. 3,Elsevier Sci. Publ. Co., N.Y, 238 p.

Logie, R. R. 1956. Oyster mortalities, old andnew, in the maritimes. Fish. Res. Board Can.,Prog. Rep. Atl. Coast Stn. 65, p. 3-11.

Loosanoff. Y. L. 1955. The European oyster inAmerican waters. Science (Wash., D.C.) 121:119-121.

Lunz, GR. 1954. The general pattern of oystersetting in South Carolina. Proc. Natl. Shell-fish. Assoc. 45:47-51.

Mann, R. 1979. Exotic species in aquaculture:An overview of when, why and how. In R.Mann (editor), Exotic species in mariculture,p. 331-354. The MIT Press, Cambridge, Mass.

Marteil, L. 1969. Donnees generales sur lamaladie des branchies. Rev. Trav. Inst. PechesMarit. 33:145-150.

1970. La culture des hUltres et desmoules en France. [In Fr., Engl. abstr.] InProceedings of the Symposium on Mollusca,Part Ill, p. 994-998. Mar. BioI. Assoc. India,Symp. Ser. 3.

____ . 1976. La conchyliculture Fran~aise.Part 2. Biologie de I'hultre et de la moule.Rev. Trav. Inst. Peches Marit. 40: 149-345.

Matthiessen, G. C. 1979. The oyster industry ofMassachusetts and the introduction of exoticspecies. In R. Mann (editor), Exotic species inmariculture, p. 212-224. The MIT Press,Cambridge, Mass.

Maurin, c., and P. Gras. 1979. Experiments onthe growth of the Mangrove oyster, Crass-ostrea rhizophorae, in France. In R. Mann(editor), Exotic species in mariculture, p. 123-128. The MIT Press, Cambridge, Mass.

____ , and J. LeDantec. 1979. The cultureof Crassostrea gigas in France. In R. Mann(editor), Exotic species in mariculture, p. 106-122 The MIT Press. Cambridge, Mass.

McKernan, D. L., Y. Tartar. and R. Tollefson.1949 An investigation of the decline of thenative oyster industry of the state of Wash-ington, with special reference to the effectsof sulfite pulp mill waste on the Olympiaoyster (Ostrea I/lrida). Wash Dep. FishBioi Rep. 49: 115-165

Medcof, J. C. 1961. Trial introduction of Euro-pean oysters (Ostrea edulis) to Canadianeast coast. Proc Natl Shellfish. Assoc.50:113-124.

____ , and P. H. Wolf. 1975. Spread ofPacific oyster worries NSW culturists. Aust.Fish 34(7):32-38.

Menzel, W. 1974. Portuguese and Japanese oys-ters are the same species. 1. Fish. Res. BoardCan. 31:453-456.

Needler, A. W. H. 1931. The oysters of Mal-peque Bay. BioI. Board Can. Bull. 22, 35 p.

____ , and R. R. Logie. 1947. Seriousmortal ities in Prince Edward Island oysterscaused by a contagious disease. Trans. R. Soc.Can., Ser. 3,41(5):73-89.

Marine Fisheries Review

Nelson, T. C. 1946. On the need for developingnew strains of oysters through selective breed-ing of domestic stock, cross breeding withother species and the introduction of speciesfrom other areas. Conv. Addresses Natl. Shell-fish. Assoc., p. 1-7.

Newkirk, G. E, and L. E. Haley. 1977. The roleof natural populations in the genetic improve-ment of species used in aquaculture. In J. W.Avault, Jr. (editor), Proc. 8th Annu. Meet.,World Mariculture Soc. p. 567-578.

Orton, J. H. 1937. Oyster biology and oysterculture. Ed. Arnold and Co., Lond.

Perkins, EO., and Wolf, P. H. 1976. Finestructure of Marteilia sydneyi sp. n. - haplo-sporidan pathogen of Australian oysters. 1.Parasitol. 62:528-538.

Quayle, D. B. 1964. Distribution of introducedmarine mollusca in British Columbia waters.J. Fish. Res. Board Can. 21:1155-1181.

____ . 1969. Pacific oyster culture in Brit-

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ish Columbia. Bull. Fish. Res. Board Can.169, 192 p.

Ranson, G. 1967. Les especes d'hultres vivantactuellement dans Ie monde, definies par)eurscoquilles larvaires ou prodissoconques. Etudedes collections de quelques-uns des grandsMusees d 'Histoire Naturelle. Rev. Trav. Inst.Peches Marit. 31(5):127-129.

Rosenfield, A., and E G. Kern. 1979. Molluscanimports and the potential for introduction ofdisease organisms. In R. Mann (editor),Exotic species in mariculture, p. 165-191. TheMIT Press, Cambridge, Mass.

Sindermann, C. J. 1979. Oyster mortalities andtheir control. In T. V. R. Pillay and W. A. Dill(editors), Advances in aquaculture. Paperspresented at the FAO Technical Conference onAquaculture, Kyoto, Japan, 26 May-2 June1976, p. 349-361.

Stauber, L. A. 1950. The problem of physiolog-ical species with special reference to oysters

and oyster drills. Ecology 31:109-118.Thomson, 1. M. 1952. The acclimatization and

growth of the Pacific oyster (Gryphaea gigas)in Australia. Aust. J. Mar. Freshwater Res.3:64-73.

1959. The naturalization of the Pa-cific oyster in Australia. Aust. J. Mar. Fresh-water Res. 10:144-149.

Van Engel, W. A., W. A. Dillon, D. Zwerner,and D. Eldridge. 1966. Loxothylacus pano-paei (Cirripedia, Sacculinidae) an introducedparasite on a xanthid crab in Chesapeake Bay,U.S.A. Crustaceana 10:110-112.

Walne, P. R., and M. M. Helm. 1979. Introduc-tion of Crassostrea gigas into the UnitedKingdom. In R. Mann (editor), Exotic speciesin mariculture, p. 83-105. The MIT Press,Cambridge, Mass.

Welch, W. R. 1966. The European oyster,Ostrea edulis, in Maine. Proc. Natl. ShellfishAssoc. 54:7-23.

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