MOLLUSCAN INTRODUCTIONS AND TRANSFERS

A Maryland Sea Grant Publication College Park Maryland MOLLUSCAN INTRODUCTIONS AND TRANSFERS MOLLUSCAN INTRODUCTIONS AND TRANSFERS

Rrsx CoNSIDERATIONs AND IMPLICATIONS

A Symposium Proceedings

Edited by ] ames T. Carlton and Aaron Rosenfield

...,.~ . (...... -~j/4!1!!f~~ A Maryland Sea Grant Publication ·~ .. . College Park, Maryland Published by the Maryland Sea Grant College, University of Maryland, College Park.

Publication of this book is supported by grant #NA46RG009l from the National Oceanic and Atmospheric Administra­ tion to the Maryland Sea Grant College and by Grant #NA90AA-D-SG 184.

The papers in this book were presented at a special symposium, Molluscan Introductions and Transfers: Risk Consider­ ations and Implications, presented at the 82nd Annual Meeting of the National Shellfisheries Association and the Institute of , held April 4-5, 1990 in Williamsburg, Virginia. All the papers are reprinted with the permission of the Journal of Shellfish Research.

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Printed on recycled paper. Contents

Contributors...... vii

james T. Carlton and Aaron Rosenfield Introduction to the special symposium on molluscan introductions and transfers: Risk considerations and implications ......

James T. Carlton Introduced marine and estuarine mollusks of North America; An end-of-the-20th-century perspective..... 3

Melbourne R. Carriker Introductions and transfers of mollusks: Risk considerations and implications ...... 21

Roger Mann, Eugene M. Bu"eson and Patrick K. Baker The decline of the Virginia fishery in Chesapeake Bay: Considerations for introduction of a non-endemic , gigas (Thunberg, 1793) ...... 25

Douglas W. Lipton, Eileen F. Lavan and Jvar E. Strand Economics of molluscan introductions and transfers: The Chesapeake Bay dilemma...... 35

Cameron Ray Hackney, Marylin B. Kilgen, and Howard Kator Public health aspects of transferring mollusks...... 45

Patrick M. Gaffney and Standish K. Allen, Jr. Genetic aspects of introduction and transfer of molluscs...... 59

Susan E. Ford Avoiding the transmission of disease in commercial culture of molluscs, with special reference to Perkinsus marinus ("Denno") and Haplosporidium nelsoni (MSX) ...... 63

NOTE: When referencing these papers, please cite the original source: Journal ofShcl(flsh Research. Volume, page numbers and year for each paper arc as follows: Carlton and Rosenfield, 11(2):487, 1992: Carlton, 11(2):489-505. 1992; Carriker, 11 (2):507-5 I 0, 1992: Mann, Burrcson and Baker, I 0(2)::179-3RR, 1991; Lipton, Lavan and Strand, 11 (2):511-519, 19n; Hackney, Kilgcn and Kat or, 11 (2):521-533, 1992; Gaffney and Allen, 11 (2):535-538, 1992; Ford, II (2):539-546, I 992.

v Contributors

Standish K. Allen, Jr. Howard Kator Haskin Shellfi.<.h Research Laboratory School of Marine Science Rutgers University Virginia Institute of Marine Science Port Norris. New Jersey 08349 College of William and Mary Glouce:.ter Point, Virginia 23062 Patrick K. Baker Virginia Institute of Marine Science Marylin B. Kilgen School of Marine Science Department of Biology College of William and Mary Nicholls State University Gloucester Point, Virginia 23062 Thibodaux, Louisiana 70310

Eugene M. Burreson Eileen F. Lavan Virginia Institute of Marine Science Marine Environmental and Estuarine Studies Program School of Marine Science University of Maryland College of William and Mary College Park, Maryland 20742 Gloucester Point, Virginia 23062 Dougla~· W. Lipton Melbourne R. Carriker Department of Agricultural and Resource Economics College of Marine Studies University of Maryland University of Delaware College Park, Maryland 20742 Lewes, Delaware Roger Mann James T. Carlton Virginia Institute of Marine Science Maritime Studies Program School of Marine Science Williams College-Mystic Seaport College of William and Mary 50 Greenmanville Avenue Gloucester Point, Virginia 23062 Mystic, Connecticut 06355 Aaron Rosenfield Susan E. Ford Northeast fisheries Science Center Haskin Shellfish Research Laboratory National Marine Fi:.heries Service Rutgers University Oxford, Maryland 21654 Port Norris, New Jersey 08349 lvar E. Strand Patrick M. Gaffney Department of Agricullural and Resource Economics College of Marine Studies University of Maryland University of Delaware College Park, Maryland 20742 Lewes, Delaware 19958

Cameron Ray Hackney Department of Food Science and Technology Virginia Polytechnic Institute and Technology and State University Blacksburg, Virginia 24601

Vll Introduction to the Special Symposium on Molluscan Introductions and Transfers: Risk Considerations and Implications

]ames T. Carlton and Aaron Rosenfield

The collection of papers that appears within these proceedings of a great deal of attention. This attention is particularly strong is the outcome of a Symposium entitled ''Introductions and Trans­ among individuals and groups associated with intentional move­ fers of Mollusks: Risk Considerations and Implications". The ments of molluscan species, not only for aquaculture purposes but Symposium was held as part of the 82nd Annual Meeting of the also for scientific study, aquarium use, new product development National Shellfisheries Association in April 1990 in Williamsburg, and depuration. In addition others are interested in the unplanned, Virginia. One paper from this Symposium was publisherl earlier in accidental translocation of exotic mollusc species and transfers or this Journal (Mann et al. 1991). In addition to those papers that indigenous species, either of which when released into new envi­ appear here, six other papers were presented orally during the ronments may become nuisances themselves or act as carriers for Symposium. Unfortunately these latter papers were not completed other plants or that become pests, parasites, pathogens, or in time to be included in this issue of the Journal of Shellfish competitors with resident organisms. There are always risks asso­ Research. Although the editors would like to allow additional ciated with translocation of animals and plants resulting in impacts time, it was concluded that further delays would risk outdating the that could be either positive or negative from the viewpoints of papers submitted by the rest of the Symposium participants. environmental and resource sustainability. Careful consideration The occur world wide in extraordinary diversity, must be given to the ecological, genetic, sociological, economic, abundance, and distribution both in aquatic and terrestrial habitats. aesthetic and political impacts that may result from undesirable They are readily available and harvestable; with common sense introductions regardless if they are deliberate or accidental. On the and a little knowledge and care they are among the easiest of the other hand, the use of mollusks for purposes of aquaculture, stock invertebrates to collect, manipulate, transport, and maintain for enhancement and improvement, sanitation, recreation, science and extended periods using relatively uncomplicated conditions and technology, education, and food production could bring enormous inexpensive holding facilities. It is no wonder their exploitation for benefits. However, such programs must be well thought out and food, ornamentation, dye materials, tools, construction material, carefully designed, and must be considerate of maintaining envi­ music, toys, utensils, money, and shell collections has been prac­ ronmental integrity and ecological balance. ticed for millennia. More recent imaginative and remarkable ad­ This Symposium thus considers some of these risks and ben­ vances have been made in the use of mollusks for aquaculture, efits involved with both known and anticipated introductions and genetic engineering (including the development of transgenics), transfers of mollusks, and discusses the potential implications, toxicology, and biomedicine. The use and application of mollusks past, present, and future, of these movements. in fields such as these necessarily involve the shipment and im­ We are most grateful to the National Marine Fisheries Service portation, that is, the translocation of mollusks from one location Office of Research and Environmental Information for providing to another. As can be deduced from the title of this Symposium funding for this Symposium, and particularly to Dr. Glenn A. considerable apprehension and concern exists today over the risks Rittner and Dr. Carolyn Brown for their generous support and or dangers associated with the potential movement of molluscan help in planning and conducting the Symposium. species from one ecosystem to another. These movements create a strong potential for the introduction of new species or the infusion of new genetic material into regions where they may have pro­ LITERATURE CITED found impacts on native species. Mann, R., E. M. Burreson & P. K. Baker. 1991. The decline of the In very recent years the subject of the natural and human me­ Virginia oyster fishery in Chesapeake Bay: considerations for intro­ diated invasions of nuisance species into ecosystems where they duction of a non-endemic species, Crassostrea gigas (Thunberg, have not been resident before has and continues to be the subject 1793). 1. Shellfish Res. 10:373--388.

Introduced Marine and Estuarine Mollusks of North America: An End-of-the-20th-Century Perspective

]ames T. Carlton

ABSTRACT A review of the introduced marine and estuarine (brackish water) bivalves and prosobranch and pulmonate gastropods of the Atlantic, Gulf and Pacific coasts of North America reveals an established fauna of 36 non-indigenous species. Sixteen species are native to temperate or tropical coasts of North America, and have been transported to regions of the continent where they did not occur in historical time; the remaining 20 species are from Europe, the Mediterranean, South America, the Indo-Pacific, and the northwestern Pacific. The movement of Pacific (Japanese) and Atlantic commercial to the Pacific coast, and ship fouling, boring, and ballast water releases, have been the primary human-mediated dispersal mechanisms. Regional patterns are striking: 30 species are established on the Pacific coast, 8 on the Atlantic coa~t. and I on the Gulf coast (three species occur on both coasts); 19 (63%) of the Pacific species occur in alone. These panems may be linked to a combination of human-mediated dispersal mechanisms and regional geological-biological Pleistocene history: at lea~! 27 species of Japanese and Atlantic coast mollusks were introduced to the American Pacific coast by the oyster indu;try, in large part into geologically young regions with low native molluscan diversity. With the exception of a few species, there is linle experimental elucidation of the ecological impact of the introduced marine mollusks in North America. Negative effects by introduced gastropods on native gastropods have been demonstrated on both the Atlantic and Pacific coasts; for one species, the Atlantic pulmonate marsh Ovatella on the Pacific coast, experimental evidence suggests that its establishment did not arise at the expense of native species. No introduced marine mollusk in North America has had a greater ecological impact than the periwinkle Littorina littorea. which colonized the Atlantic coast from Nova Scotia to New Jer.~ey in the 30 year period between 1860 and 1890, and subsequendy altered the diversity, abundance, and distribution, of many and plant species on rocky as well as soft bottom shores Future marine invasions, through ballast water release and perhaps through aquaculture activitieS, can be expected with confidence.

KEY WORDS: mollusks, introductions, invasions, nonindigenous, exotics

INTRODUCTION potential to become naturally established. I have excluded opistho­ branch mollusks (sacoglossans, nudibranchs and pyramidellids), "A good deal of chess play ha~ also been done with pending a global and/or continental review of the candidate spe­ . cies. There are no introduced polyplacophorans () or sca­ ---Charles S. Elton (1958) phopods (tusk shells) in North America. I also exclude most At the close of the 20th cemury we are witnessing rapidly records of single specimens of living mollusks whose anomalous growing interest in the phenomenon of biological invasions of presence outside their recorded ranges appears to be due to dis­ coastal waters. As a result of an increasing number of uninten­ carding through hobby (aquarium) or fishing activities. tional invasions of marine organisms due to the release of ballast Mechanisms of introduction of non-indigenous marine organ­ water through international shipping activities, and of increasing isms to North American waters have been reviewed by Carlton pursuit of the intentional use and release of marine organisms for (1985, 1987, 1989, 1992a). The most important human activities mariculture purposes and for open sea fisheries enhancement, con­ have been or are the following: ( 1) the transportation of organisms cern is growing relative to the potential ecological, genetic, eco­ on the outside (fouling species) or on the inside (boring species) of nomic, and social risks that may be associated with future inva­ ships, (2) the transportation of organisms inside vessels in solid sions. ballast, such as rocks, sand, and detritus, (3) the movement of l review here the diversity, distribution, regional invasion pat­ oysters, and the concomitant movement of organisms on the oyster terns, and ecological impacts of the introduced marine and estu­ shells or in associated sediments and detritus, (4) the intentional arine (brackish water) bivalves and prosobmnch and pulmonate release of species for fisheries purposes, and (5) the release of gastropods of the Atlantic, Gulf, and Pacific coasts of North larvae, juveniles, or adults of marine organisms in the ballast America. Introduced species (exotic, non-indigenous, alien, or water of coastal, transoceanic, and interoceanic vessels. I review invader species) are those taxa transported by human activity to below the relative importance of each of these mechanisms to the regions where they did not exist in historical time (Carlton 1987). established introduced mollusks in North America. While there has been no previous continent-wide review of the METHODS introduced mollusks, Quayle (1964), Hanna (1966) and Carlton (1975, 1979a, 1979b) have provided regional lists and treatments Field, museum, and literature work from 1962 to 1979 are for the Pacific coast. Abbott (1974), Bernard (1983) and Turgeon summarized by Carlton (1979a). Field work during that period was ( 1988) list many ofthe species discussed here. I include all species conducted from Vancouver Island to southern ; 18 mu­ which have been recorded as free-living outside of mariculture seums or private collections on the west and east coasts of the operations. One species, the Japanese sea Patinopecten United States and Canada were studied. From 1979 to 1992 field yessoensis, is included because of its current mariculture use and work was conducted from Newfoundland to Virginia, as well as on

3 4 MOLLUSCAN INTRODUCTIONS AND TRANSFERS the Pacific coast, and museum collections were revisited to exam­ torical biogeography in the north Atlantic Ocean remain uninves­ ine additional species. Throughout both periods l corresponded tigated. with malacologists and other biologists and undertook continual Regional patterns (Table 3) are striking: 30 species are estab­ literature reviews. The records and dates recorded here are thus lished on the Pacific coast, 8 on the Atlantic coast, and I on the based upon field work, museum collections, personal communi­ Gulf coast (3 species, the snail Ovatella, the Corbicula, and cations, and the literature, and form the basis of a monograph now the shipworm Teredo bartschi occur on both the Atlantic and in preparation. I present here an abstract of this work. Pacific coasts). Most (27 species) of the introduced mollusks on the Pacific coast originate either from Asia or the Atlantic coast of North America. Of the Pacific species, 5 are recorded from only l RESULTS locality: the Atlantic Busycotypus and the Asian clam Po­ Regional Pattern$ of Invasion tamocorbula occur only in San Francisco Bay, the Atlantic clam Mercetulria occurs only in Colorado Lagoon, Alamitos Bay, the Table I is a comprehensive synthesis of the introduced marine Atlantic oyster Crassostrea virginica now survives only in the and estuarine mollusks reported since the early 19th century in Serpentine and Nicomekl Rivers of the Boundary Bay region, North America. The introduced mollusks can be placed into 4 British Columbia, and the shipworm Lyrodus takanoshimensis has categories (Table 2): established (naturally reproducing popula­ been reported only from Ladysmith Harbor, British Columbia. I tions are known), establishment not certain (no recent records, but do not include here the clam Macoma "balthica," whose San the species may still be present), not established (not found in Francisco Bay population appears to arise from an Atlantic coast recent surveys or, if present, naturally reproducing populations are stock, as this genotype may in fact be widespread in central Cal­ not known), and cryptogenic (Carlton 1987; status as introduced or ifornia embayments. native is not known). Four species are restricted to the Pacific Northwest (Washing­ Thirty-six species of non-indigenous marine and estuarine mol­ ton and British Columbia): the Japanese Cecitul manchurica lusks are established on the Pacific, Atlantic, and Gulf coasts of and fraterculus, the Japanese clam Trapezium liratum North America (Table 3). Sixteen species are native to temperate and the (Crassostrea gigas (which rarely reproduces or tropical coasts of North America, and have been transported to south of Willapa Bay, W A). Two additional species reported only regions of the continent where they did not occur in historical from British Columbia are the questionably established Clanculus time. Thus, 14 species (Table 2) native to the Atlantic coast have ater and Sabia conica. Four Atlantic species are well established been transported to the Pacific coast (Table 3 indicates 15 species in a few restricted localities: the slipper Crepidula convexa on this route; this includes the European Ovatella, established on occurs only in San Francisco and Boundary Bays (newly recog­ the American Atlantic coast). At least 3 species (Rangia cuneata, nized in British Columbia by Robert Forsyth); the mudsnail Jly­ Mytilopsis leucophaeata and Teredo btlrtschi) have been trans­ anassa obsofeta occurs only in San Francisco, Willapa, and ported from their apparently native southern ranges to more north­ Boundary Bays; the angel wing clam Petricola pholadiformis oc­ em localities (shown in Table 3 as 1 species from the Gulf of curs only in San Francisco, Newport, and Boundary Bays, and the Mexico and 2 species from the northwest Atlantic, respectively), gem clam Gemma gemma is restricted to 5 bays in central Cali­ The remaining 20 species include 4 from Europe, 1 questionably fornia (Bodega Harbor (not Bodega Bay), Tomales Bay, Bolinas from Europe (the shipworm Teredo navalis), I from the Mediter­ Lagoon, San Francisco Bay, and Elkhorn Slough). Seven oyster­ ranean (the galloprovincialis), I from South Amer­ associated introductions occur in British Columbia/Washington ica (the mussel ), I questionably originating in the and in California, but for reasons that remain unclear do not occur Indo-Pacific (the shipworm Lyrodus pedicellatus), and 12 from the "naturally" in Oregon bays and estuaries: these are the Japanese northwestern Pacific. snail Batillaria attramentaria and the Atlantic gastropods llya­ Four species (Table 2) are questionably established; field work nassa obsoleta, Crepidula convexa, C. fornicata, C. platul, and has not been focused on locating these species in recent years, and Urosalpinx cinerea; the fifth species, the Japanese clam Venerupis they may still be present Seven species have not become region­ philippitulrum, occurs in Netarts Bay, Oregon only by virtue of an ally established: the Atlantic periwinkles Littorina littorea and intensive planting program (the only bay in Oregon where the Tectarius muricatus, once found living in California and the Gulf Japanese oyster drill Ceratostoma inortultum is also established). of California respectively; the European snail Truncatella subcy­ The Asian clam Theora lubrica and the Atlantic mussel Geu­ lindrica, found in 1880 to be common at Newport, Rhode Island; kensia demissa occur disjunctly in San Francisco Bay and again in the Asian clam Laternula limicola, found over a period of several southern California bays. The abundant and widespread freshwater years in Coos Bay, Oregon in the 1960s; the European oyster clam Corbicula jluminea appears occasionally in estuarine situa­ edulis, widely released on the American Pacific coast, and tions in Oregon and California. The tropical Atlantic shipworm the South American mytilid Mytella charruatul which appeared in Teredo bartschi has been introduced to at least 2 sites in western numbers in Jacksonville, Florida in 1986. Of these, Littorina lit­ Mexico, and is probably more widespread than these records in­ torea and have become established on the Atlantic dicate. coast. The Japanese sea scallop Patinopecten yessoensis while Of the 30 introduced species on the Pacific coast, then, only 12 present in mariculture operations in British Columbia has not been are relatively widespread. These are the gastropods Crepidulafor­ reported in natural sets. nicata, Crepidula plana, Batillaria attramentaria, Urosalpinx ci­ Cryptogenic species include (Table I) the pulmonate limpet nerea, Ceratostoma inortultum, and Ovatella myosotis, and the SiphoMria pectinata and the shipworm Teredo navalis. Nine­ bivalves Mytilus galloprovincialis, Musculista senhousia, Veneru­ teenth century or earlier shipping has been implicated in creating pis philippinarum, Myra aretulria, Teredo navalis, and Lyrodus the modem distributions of both species, but details of their his- pedicellatus. INTRODUCED MARINE MOLLUSKS OF NORTH AMERICA 5

TABLE 1. Introduced marine and estuarine mollusks of North America (exclU!live of opisthobranch gastropods). Common names after Turgeon 1988; (*) species listed without common name in Turgeon 1988; ( +) species not listed in Turgeon 1988.

NATIVE TO/Introduced To (date of collection)/MECHANISM (M) Species (see keys, below) References and Remarks

GASTROPODA: Prosobranchia Trochidae Clancuius ater Pilsbry, 1911 ( + topsnail) NW PACIFIC/NE Pacific: BC: Queen Clarke, 1972. Not reponed since 1964; status Charlotte Sound (1964). M: BW? not known. Pomatiopsidae Cecina manchurica A. Adams, 1861 NW PACIFICINE Pacific: BC (date?); WA: Morrison, 1963a, Duggan, 1963, Carlton, (+Manchurian cecina) Whatcom Co. (1961); Willapa Bay (1963). 1979a, Kozloff and Price, 1987:210. High M: COl intenidal, commoo, co-occurring with Ovateila myosotis, found by digging down inside piles of old oyster shells in damp, rich organic debris (Willapa Bay, 1977, JTC), a microhabitat similar to the one in its native Japan (Davis, 1979: 117). Also at base of salt marsh plant Salicornia. Littorim~littoreu (Linnaeus, 1758) (common NE ATLANTIC/NW Atlantic: (<1840) Carlton, 1982, Carlton eta!. 1982, Venneij, peri winkle) Canada to V A/NW 1982a,b, Lubchenco, 1978, 1983, 1986, ATLANTIC/NE Pacific: see remarks. M: Breochley, 1982, Brenchley and Carlton, Atlantic: SB or IR; Pacific: DA 1983, Kemp and Benness, 1984, Benness, 1984, Blackstone, 1986, Yamada and Mansour, 1987, Petraitis, 1989. Became extinct in Nonh America in precontact times; reestablished through either intentional release (for food) or accidentally with ballast rocks. CoUectt:d in San Francbco Bay in 1968-1970 and again in 1977 (Carlton, 1969, 1979a), but not found since despite sporadic searches throughout the bay (JTC, personal observations), Now one of the most predominant mollusks of the Atlantic rocky shore, and in some regions the marshes and mudflats, from Newfoundland to New Jersey. Tectarius muricatUJ (Linnaeus, 1758) (beaded NW ATLANTIC/Mexico: Gulf of California Bishop, 1992, Chaney, 1992. No records since periwinkle) (1986, 1988). M:? 1988. Truncatellidae Tnmcatella subcylindrica (Linnaeus, 1767) NE ATLANTIC/NW Atlantic: RI: Newpon Burch ( 1962) is the most recent to repeat this ( +) (1880). M: SB? early record of Verrill (1880), who found this species to be common; it has not been collected since. Potamididae Batillaria attramentaria (Sowerby, 1855) NW PACIFIC!NE Pacific: BC (1959) to WA Hanna. 1966, MacDonald, 1969a, 1969b, ( = Batillaria zom~lis auctt.) (Japanese false (1920s), but not Grays Harbor or Wil!apa Whitlatch, 1974, Carlton, 1979a, Whitlatch cerith) Bay; CA: Tomales Bay (1941); Montt:rey Bay: and Obrebski, 1980, Yamada, 1982 Elkhorn Slough (1951). M: COl Abuodantlocally on mudflats. Hipponicidae Sabia conica (Schumacher, 1817) (*hoofsnail) NW PACIFIC/NE Pacific: BC: Queen Cowan, 1974, Carlton, 1979a, Kay, 1979. Charlottt: Sound: Table Island (1940); Current status not known Vancouver Island (1963). M: BW? Calyptraeidae Crepidula conve.xa Say, 1822 (convex NW ATLANTICINE Pacific: BC: Boundary Hanna, 1966, Carlton and Roth, 1975, slippersnail) Bay (R. Forsyth. personal communication, Carlton, 1979a. Very common on snail 1991); CA: San Francioco Bay (1898); M: shells on mudflats along shores of San CO! Francisco Bay.

continued on next page 6 MOLLUSCAN lNTRODUCflONS AND TRANSFERS

TABLE I. continued

NATIVE TO/Introduced To (date of coUectlon)IMECHANISM (M) Species (see keys, below) References and Remarks

Crepidulafornicata (Linnaeus, 1758) NW ATLANTICINE Pacific: WA: Puget Hanna, 1966, Carlton, 1979a (common Atlantic slippe~nail) Sound (1905?); Grays Harbor (1970s); Willapa Bay (1937); CA: Humboldt Bay (S. Lamed, collector, 1989); Tomales Bay?; San Francisco Bay (1898). M: CO!

Crepidulap/ana Say. 1822 (eastern white NW ATLANTIC/NE Pacific: WA ?: Puget Carlton, 1979a, Wicksten, 1978 (as Crepidula slippersnail) Sound?; Willapa Bay (1937); CA: San peiforans) Francisco Bay (1901). M: COl

Muricidae Ceratostoma inornatum (Recluz, 1851) NW PACIFICINE PACIFIC: BC (1931); WA: Chew, 1960, Hanna, 1966, Squire, 1973, ( = Ocenebra japonka (Dunker, 1860)) south to (1924); Willapa Bay Radwin and D'Attilio, 1976, Carlton, (+Japanese oyster drill) (present populations since 1960s?); OR: 1979a. Locally common on oyster beds in Netarts Bay (1930-34); CA: Tomales Bay the Pacific Northwest. (1941); Morro Bay?; M: COl.

Urosalpinx cinerea (Say, 1822) (Atlantic NW ATLANTICINE Pacific (1890 and later Carlton, l979a; populations last reported in oyster drill) years): BC: Boundary Bay; WA: Puget Humboldt Bay in 1950 are still present (S. Sound and Willapa Bay; CA: Humboldt, Larned, collector, 1989). Locally common San Francisco, Tomales, and Newport Bays. on oysters and rocks. M: COl Busycotypus canaliculatus (Linnaeus, 1758) NW ATLANTIC/NE Pacific: CA: San Stohler, 1962, Carlton, 1979a (who reviews (channeled whelk) Francisco Bay (1938). M: COl? evidence for retention of 1938 date). Nassariidae 1/yanassa obsoleta (Say, 1822) ( =Nassarius NW ATLANTIC/NE Pacific: BC: Boundary Hanna, 1966, Carlton, 1979a, Race, 1982 obso/etus) (eastern mudsnail) Bay (1952); W A: Willapa Bay (1945); CA: Astronomically abundant in San Francisco San Francisco Bay (1907). M: COl Bay. Nassarius fraterculus (Dunker, 1860) NW PACIFlC/NE Pacific: BC: Boundary Bay Hanna, 1966, Carlton, 1979a, Cernohorsky, {Japanese nassa) (1959); WA: Puget Sound region (1960). M: 1984:184-185 cor Pulmonata Melampodidae Ovatel/a myosotis (Drapamaud, 1801) NE ATLANTIC/NW Atlantic: Nova Scotia to Stimpson, 1851, Morrison, 1963a, Abbott, ( = Phytia setifer (Cooper, 1872)) West Indies; Bermuda; NW ATLANTICINE 1974, Carlton, 1979a, Berman and Carlton, (*European ovatella) Pacific: BC: Boundary Bay (1965) to 1991. Earliest Pacific coast record is 1871 Mexico: Scammons Lagoon (1972) M: (San Francisco Bay); earliest record on Atlantic: SB; Pacific: COl Atlantic coast is 1841 (Massachusetts). Very common in high sal! marsh and drift habitat~ Siphonariidae Siphonaria pectinata (Linnaeus, 1758) (striped MEDITERRANEAN?/NW Atlantic (19th Morrison, 1963b, 1972. Morrison believed this falselimpet) century or earlier): FL to Mexico, Caribbean species to be introduced from the Cuba, and northern South America. M: S Mediterranean on ships R. T. Abbott (personal communication, 1990) concurs. G. Venneij (personal communication, 1990) questions this conclusion based on habitat and broad Western Atlantic distribution. Cryptogenic (see text) Mytilidac Mytilus gal/oprovincialis Lamarck, 1819 MEDITERRANEANINE Pacific: Northern CA McDonald and Koehn, 1988, Koehn, 1991, { =M. edu/is auctt). (+Mediterranean (date?) to southern CA (1880s?), Mexico Seed, 1992. Late twentieth century mussel) M: S distribution probably enhanced by ballast water transport as well as ship fouling. An abundant fouling mussel.

continued on next page iNTRODUCED MARINE MOLLUSKS OF NORTH AMERICA 7

TABLE I. continued

NATIVE TO/Introduced To (date or collection)!MECHANISM (M) Species (see keys, below) Re£ert'nces and Remarks

Musculista .wmlwu.Yia (Benson, 1842) NW PACIFIC/NE Pacific: BC: Boundary Bay Hanna, 1966, Morton, 1974, Carlton, 1979a. (R. Forsyth, personal communication, Abundant locally in dense mats over soft 1991); Puget Sound ( 1959); northern CA: bottoms. Bodega Harbor (1971) to Elkhorn Slough (1965), earliest record for Pacific coast is 1941 (San Franci~o Bay); southern CA: NewJXIt1 Bay (1977) to San Diego Bay (1976); Mexico: Papilote Bay, south of Ensenada (1970). M: Pacific NW, northern CA: COl; southern CA-Mexico: BW?

Geukensia demissa (Dillwyn, 1817) (ribbed NW ATLANTIC/NE Pacific: CA: San Hanna, 1966, Carlton, 1979a, Sarver eta!., mussel) Francisco Bay (1894), southern CA: I 992. Juvenile Geukensia occur in fouling Alamitos (1957), Anaheim (1972) and on ships, suggesting a mechanism for Newport (1940) Bays, Bolsa Chica Lagoon, intracoastal transport from San Francisco Orange Co. (M. Wicksten, personal Bay to southern California. Abundant in communication, 1979). M: San Francisco marshes, mudflats, and at bases of retaining Bay: COl; southern California: S?ICOT? walls in San Francisco Bay.

Perna perrw (Linnacus, 1758) {+edible brown EASTERN SOUTH AMERICAIGulf of Hicks and Tunnell, 1993. Also recorded from mussel) Mexico: TX: Port Aransas (1990) to Port Namibia to Mozambique (Kennelly, 1969) Mansfield (1991). M: BW/S

Mytella charruarw (d'Orbigny, 1846) ( +, EASTERN SOUTH AMERlCAINW Atlantic: Lee, 1986. Appeared briefly in large numbers charru mussel) FL: Jacksonville (1986). M: BW?IS? in seawater intake of power plant in 1986, but disappeared by 1987 (H. Lee, personal communication, 1992). Perhaps released in ballast water of oil tankers from Venezuela.

Pectinidae Patinopecten yessoensis (Jay, 1856) NW PACIFlCINE Pacific: BC (1984-85), see Raised in open sea aquaculture operations in (+Japanese sea scallop) remarks. M: lR BC (T. Carey, personal communication, 1990), but naturally reproducing populations not reported as of 1992.

Anomiidae chinensis Philippi, 1849 (=Anomia NW PACIFlCINE Pacific: WA: Samish Bay Carlton, 1979a. Current status not known. May iischkei Dautzenberg and Fischer, 1907) (1924), Willapa Bay (1952); OR: Tillamook be established (Hanna, 1966, Abbott, 1974), (+Chinese jingle) Bay (<1970s). M: COl although Bernard (1983) believed otherwise.

Ostreidac Crassostrea g1gas (Thunberg, 1793) (Pacific NW PACIFIC!NE Pacific: Cultured from AK Pacific: Galstoff, 1932, Barrett, 1963, Hanna, oyster) to Mexico; well established in BC, WA, 1966, Quayle, 1969, Carlton, 1979a, sporadically reproducing south to CA: Bourne, 1979, Chew, 1979, Ketchen et al. Tomales Bay. NW Atlantic: Sporadic 1983, Foster, 1991:41. Atlantic: Galtsoff, plantings along Atlantic and Gulf coasts 1932, Nelson, 1946; Turner, 1949, 1950, since 1930s. No established populations Mann, 1979, Mann eta!. 1991. reported as of 1992, despite reported Experimental introductions in 1875 in WA unauthorized private plantingb of 1000s of (Barrett, 1963:48--49) were followed by bushels in Chesapeake Bay about 1988--90. regular attempts throughout the Pacific M:lR. Northwest staning in 1902; CA plantings began in 1928.

Crassostrea virginica (Gmelin, 1791) (eastern NW ATLANTICINE Pacific: BC: Boundary Elsey, 1933, Barrett, 1963, Hanna, 1966, oyster) Bay only (since 1917-1918). Population in Carlton, 1979a, Bourne, 1979. Plantings Willapa Bay WA is now extinct {K. Sayee, began in 1869--1870 in San Francisco Bay personal communication, 1990) with completion of Transcontinental Railroad, and continued along entire Pacific coast in subsequent years.

continued on next page 8 MOLLUSCAN INTRODUCTIONS AND TRANSFERS

TABLE I. continued

NATIVE TO/Introduced To (date of collectlon)/MECHANISM (M) Species (see keys, below) References and Remarks

Ostrea edu/is Linnaeus, 1758 (edible oyster) NE AlLANTICINW Atlantic: ME (1949) and Loosanoff, 1962, Welch, 1966, Hidu and Rl (1991). NE Pacific: See remarks. M: Lavoie, 1991. May be established in bays Maine: IR: Rhode Island: ? and harbors of Rhode Island (J. D. Karlsson, collector, 1991). Raised in aquaculture facilities on the Pacific coast, but not known to be naturally established (rare natural settlement has occurred in Tomales Bay CA (Davis and Calabrese, 1969)). Raised along NW Atlantic coast with small natural sets north to Halifax County, Nova Scotia (M. Helm, personal communication, 1990).

Mactriade Rangia cuneata (Sowerby, 1831) (Atlantic GULF OF MEXICOINW Atlantic: FL east Hopkins and Andrews, 1970. Newly rangia) coast to Chesapeake Bay (1955); NY: established in lower Hudson River perhaps Hudson River (1988, C. Letts, collector). due to release as larvae in ballast water from M: to Chesapeake Bay: COI?/BW?, to Atlantic or Gulf coasts Hudson River: BW

Tellinidae Macoma ''balthica'' (Linnaeus, 1758) (Baltic NW ATLANTICINE Pacific: San Francisco Meehan et al. 1989. The genetic similarity of macoma) Bay. M: cor San Francisco Bay populations to NW Atlantic populations (as opposed to specimens from Europe or further north on the Pacific coast) suggest that the San Francisco M. "ba/thica·· were probably introduced in the 19th century. Very common.

Semelidae Theora lubrica Gould, 1861 (Asian semele) NW PACIFIC/NE Pacific: CA: Los Angeles Seapy, 1974, Carlton et al. 1990. It is of Harbor, Anaheim Bay, Newport Bay interest to note the increase of this species (earliest southern CA record,.i%8); San in 1978--79 in polluted environments in the Francisco Bay (1982). M: BW Inland Sea of Japan (Sanukida eta!. 1981), the source of much ballast water carried to the NW Pacific, and its appearance in the early 1980s in San Francisco Bay. Intracoastal movement to San Francisco Bay from southern CA is also possible.

Dreissenidae DreissefUl polymorplw (Pallas, 1771) (+zebra NE ATLANTIC/NW Atlantic: estuarine Griffiths et al. 1991, Strayer, 1991, Hebert et mussel) populations in NY: Hudson River (summer al. 1991, Carlton, 1992b, Nalepa and 1992, up to 5/oo, W. Walton, personal Schloesser, 1992. Ballast water in coastal communication, 1992). M: from Europe to vessels and ballast, bilge, or incidental the Great Lakes (1988), BW; within North water in small sailing vessels could transport America: see Carlton, 1992b zebra between estuaries along the Atlantic coast. Usually in low densities in brackish water (W. Walton, personal communication, 1992).

Mytilopsis /eucophaeata (Conrad, 1831) (dark NW ATLANTIC-GULF OF MEXICO/NW Rehder, 1937, Jacobson, 1953. Specimens are falsemussel) Atlantic: NY: Hudson River (1937); MA: no believed to have been collected from the locality (Marelli and Gray, 1985:118), lower Charles River, near Boston perhaps Boston: Charles River? M: S!BW (R. T. Abbott, personal communication, 1990; R. Turner, personal communication, 1992). Native{?) from Chesapeake Bay south.

continued on next page INTRODUCED MARINE MOLLUSKS OF NORTH AMERICA 9

TABLE 1. continued

NATIVE TOIIntroduced To (date of collection)IMECHANISM (M) (see keys, below) References and Remarkli

Trapeziidae Trapezium liratum (Reeve, 1843) (+Japanese NW PACIFIC/NE Pacific: BC: Ladysmith Carlton, 1979a. Populations are present in BC trapezium) Harbor ( 19497); WA: Willapa Bay'! ( 1947'!). (R. Fon.yth, personal communication, M: COl 1991). Status in WA not known. Never established inCA; report in Abbott (1974) of appearance "prior to 1935" based upon interceptions in Pacific oyster shipments. Nesding in fouling communities. Corbiculidae Corbicula fluminea (Muller, 1774) (=C. NW PACIFIC/NE Pacific: estuarine Counts, 1986, 1991; estuarine populations: mani/ auctt.) (Asian clam) populations in OR: Siuslaw River; CA: Diaz, 1974, Carlton, 1979a, Nichols eta!. Smith River, San Francisco Bay; NORTH 1990, Counts, 1991:105. Abundant locally, AMERICAINW Atlantic: estuarine but in lower densities in brackish water. populations in Chesapeake Bay: James River. Freshwater populations throughout the United States, northern Mexico. M: from Asia toN. America (1920s-1930s), IR; within North America: see Counts, 1986 Venerupfs philippirwrum (A. Adams and NW PACIFIC/NE Pacific: BC (1936) to CA: Fisher-Piette and Metivier, 1971 (specific Reeve, 1850) (=Tapes semidecussata Monterey Bay: Elkhorn Slough (1949). OR: and synonymy), Bourne, 1982, Reeve, 1864; = T. japonica Deshayes, Netarts Bay (see remarks). M: COl except Anderson et al. 1982, Bernard, 1983, 1853; also placed in subgenus Ruditapes). for OR: IR Ketchen et al. 1983. Generic placement (Japanese litdeneck) follows E. Coan and P. Scott (personal communication, 1992). Intentional plantings in OR: Netarts Bay sporadically from 1960s--1980s resulted in a naturally reproducing population (Gaumer and Farthing, 1990); also planted in other OR bays, where specimens should be expected. Common to abundant in <:oarser sediments. Gemma gemma (Totten, 1834) (amethyst NW ATLANTIC/NE Pacific: CA: Bodega Carlton, 1979a. Records from north of Bodega gemclam) Harbor (1974) to Elkhorn Slough (1965); or south of Monterey Bay are based upon earliest record 1893, S.an Francisco Bay. misidentifications. Abundant in soft M:COI sediments. Mercerwria mercerwria (Linnaeus, 1758) NW ATLANTIC/NE Pacific: CA: Alamitos Crane eta!. 1975, Murphy, 1985a, 1985b. (northern quahog) Bay (1967). M: IR The only established population on the Pacific coast of this common Atlantic species is in this small CA bay. Hertz and Hertz (1992) report a single live specimen from Mission Bay, San Diego, probably from discarded bait or food. Petricolidae Petricola pholadiformis (Lamarck, 1818 (false NW A TI..ANTIC/NE Pacifi~:: WA: Willapa Hanna, 1966, Carlton, 1979a. In higher shore angel wing) Bay (1943); CA: San Francisco Bay (1927), hard shale, day, mud substrates. Newport Bay (1972). M: COl Myidae Mya arerwria Linnaeus, 1758 (softshell) NW ATI..ANTICINE Pacific: AK (1946) to Carlton, 1979a, Bernard, 1979. Became Monterey Bay: Elkhorn Slough (<1911). extinct on Padfi~: coast from southern AK M:COI south in late Tertiary; reestablished (earliest record 1874, San Francisco Bay) through accidental introduction with Atlantic oysters. Now one of the most common upper bay clams from WA to San Francisco Bay.

continued on next page 10 MOLLUSCAN INTRODUCTIONS AND TRANSFERS

TABLE I. continued

NATIVE TO/Introduced To (date of oollection)/MECHANISM (M) Species (see keys, below) Refennces and Remark5

Corbulidae Potamocorbuia amurensis (Schrenck, 1861) NW PACIFIC/NE Pacific: CA: San Francisco Carlton et .a\. 1990, Nichols et al. 1990. In ( + Amur river corbula) Bay (1986). M: BW densities of tens of thousands per square meter in estuarine reaches of San Francisco: to be expected in other CA bays through intracoastal transport of larvae in ballast water. Teredinidae Lyrodus pedice/latus (de Quatrefage>, 1849) INDO-PACIFIC?/NE Pacific: CA: San Kofoid .and Miller, 1927, Turner, 1966, (=Teredo diegensis Bartsch, 1927) (blacktip Franci~co Bay (1920); Monterey Bay Ecklebarger and Reish, 1972, Carlton, shipworm) (1935); Santa Barbara to San Diego Bay l979.a (earliest southern CA record 1871"). M: S Lyrodus takanm·himensis Roch, 1929 { +) NW PACIFICINE Pacific: BC: Ladysmith Popham 1983. Harbor (1981). M: COl (in wooden oyster boxes) Teredo bartschi W. Clapp, 1923 (Bartsch NW ATLANTIC/NW Atlantic: NJ: Barnegat NW Atlantic: Hoagland and Turner, 1980, shipworm) Bay (1974), CT: Long Island Sound: Hoagland, 1981, 1986, Richards et al. Waterford (1975); NE Pacific: Gulf of 1984. Gulf of California: R. Turner in California: La Paz (<1971); Mexico: Keen, 1971:282, Hendrickx, 1980. Reported Sinalao (1978-79). M: S by Abbott (1974) as introduced to CA, a record based upon specimens from San Diego B.ay in the 1920s (Kofoid and Miller, 1927). May no longer be present in Barnegat B.ay in thermal effluents, but still established in Long Island Sound heated power plant effluents at Mlllstone. Teredo navalis Linnaeus, 1758 (naval NE ATLANTlC?INE Pacific: BC: Pendrell Turner, 1966, Carlton, l979a. Coos B.ay shipworm) Sound (1963); WA: Willapa Bay (1957); record: JTC, field records. Cryptogenic in OR: Coos Bay (1988); CA: San Francisco NW Atlantic: early American records Bay (1913): southern CA? NW ATLANTIC: include reports both from visting vessels see remarks. M: S (Russell, 1839, MAJ and from established populations (DeKay, 1843, NY). Grave (1928) enigmatically noted, ''The date of its first appearance in [Woods Hole] is not known," noting records as early as 1871. If introduced, it may have arrived centuries ago with visits of earlie~t European vessels. Teredo furcifera von Martens in Semon, 1894 NW ATLANTIC (Caribbean north to FL)INW Hoagland and Turner, 1980, Richards et al., J+J Atlantic: NJ Barnegat B.ay (1974). M: S 1984. Probably only temporarily established in Barnegat Bay in thermal effluents of power plant (K. E. Hoagland, personal communication, 1992) and may no longer be present there. Turner (1966) records an earlier nonestablished population in NC. Latemulidae Laternula limicola (Reeve, 1863) (=L. NW PACIFICINE Pacific: OR: Coos Bay Keen, 1969. Not recorded in Coos Bay since japonica aucn.) ( +) (1963). M: BW 1965, and not re-discovered there despite intensive searching from 1986-1989 (JTC and students, field records).

Mechanisms of introduction s Ships (fouling and boring) SB Ships (solid ballast: rocks, sand) BW Ship~ (ballast water) CO! Fisheries: Accidental release with commercial oyster industry IR Fi~heries: Intentional release DA Fisheries: Accidental release with discarded algae (seaweed) in shellfish packing continued on next page INTRODUCED MARINE MOLLUSKS OF NORTH AMERICA II

TABLE 1. continued

NATIVE TO!Introduced To (date of collection)/MECHANISM (M) Spedes (see keys, below) References and Remarks

Regions (as used here:) Northwest (NW) Pacific Asia: China, Japan, Korea Northea~t (NE) Pacific Pacific coast of North America: Alaska to Mexico Northwest (NW) Atlantic = Atlantic coast of North America: Canada to Florida Northeast (NE) Atlantic Europe: northern and western AK Ala>ka NJ New Jersey BC British Columbia NW Northwest CA California NY New York CT Connecticut OR Oregon FL Florida Rl Rhode Island MA Massachusetts TX Texas ME Maine VA Virginia NC North Carolina WA Washington NE Northeast

It is of interest to note that 19 (63%) of the 30 species occur in Atlantic oyster importation ceased due to Jack of breeding success San Francisco Bay. Only the embayments of the Pacific Northwest and because of competition with the increasing importation and approach this number of established species, with Willapa Bay culture of the Pacific oyster. Pacific oyster importations stopped having 12 species, Puget Sound II species, and Boundary Bay 13 after sufficient natural sets and regional aquaculture operations species. These numbers will increase with further exploration (for were able to supply adequate amounts of seed. example, Trapezium liratum, Crepidula convexa and Crepidula These industries led to the introduction of at least 22 mollusks plana should be expecte

TABLE2. Introduced marine and estuarine mollusks of North America: Established and other species arranged by donor region. RegWns: See Table 1, footnote.

Donor Region Receiver Region

ESTABLISHED C ecina rrwnchurica NW Pacific NE Pacific Barillaria attramentaria NW Pacific NE Pacific Ceralostorrw inorrwtum NW Pacific NE Pacific Nassarius fraterculus NW Pacific NE Pacific Muscu/ista senlwu.1ia NW Pacific NE Pacific Crassostrea gigas NW Pacific NE Pacific Theora lubrica NW Pacific NE Pacific Trapezium liratum NW Pacific NE Pacific Corbicu/a fluminea NW Pacifk NE Pacific N America NW Atlantic NW Pacific NE Padfic Potaf1Wcorbula amurensis NW Pacific NE Pacific Lyrodus takanoshimensis NW Pacific NE Pacific Lyrodus pedicel/a/us Indo-Pacific? NE Pacific Littorina littorea NE Atlantic NW Atlantic Ovatella myosotis NE Atlantic NW Atlantic Ostrea edulis NE Atlantic NW Atlantic Dreissena polymorpha NE Atlantic NW Atlantic Mytilus galloprovincialis Mediterranean NE Pacific Teredo navalis NE Atlantic? NE Pacific Crepidula convexa NW Atlantic NE Pacific Crepidula fornicata NW Atlantic NE Pacific Crepidula plana NW Atlantic NE Pacific Urosalpinx cinerea NW Atlantic NE Pacific Busycotypus canaliculatus NW Atlantic NE Pacific llyanassa obsoieta NW Atlantic NE Pacific Ova/ella myosotis NW Atlantic NE Pacific Geukensia demissa NW Atlantic NE Pacific Crassostrea virginica NW Atlantic NE Pacific Macoma "balthim" NW Atlantic NE Pacific Gemma gemma NW Atlantic NE Pacific Mercenaria mercennria NW Atlantic NE Pacific Petricola pholadiformis NW Atlantic NE Pacific Mya arenaria NW Atlantic NE Pacific Perna perna South America Gulf of Mexico Rangia cuneata Gulf of Mexico NW Atlantic Teredo bartschi NW Atlantic Cf: Long Island Sound NW Atlantic NE Pacific Mytilopsis /eucophaeata NW Atlantic NY: Hudson River ESTABLISHMENT NOT CERTAIN Clanculus arer NW Pacific NE Pacific Sabia conica NW Pacific NE Pacific Anomia chinensis NW Pacific NE Pacific Teredo fure~fera NW Atlantic NJ: Barnegat Bay NOT ESTABLISHED Littorina littorea NW Atlantic NE Pacific Ostrea edulis NE Atlantic NE Pacific Teclarius muricatus NW Atlantic NE Pacific Truncarelia subcylindrica NE Atlantic NW Atlantic Mytella charrunna South America NW Atlantic Patinopecten yessoensis NW Pacific NE Pacific Laternuia limicola NW Pacific NE Pacific CRYYfOGENIC Siphonaria pectinata Mediterranean? NW Atlantic? Teredo navalis NE Atlantic'! NW Atlantic? charruana in Florida and Perna perna in Texas. Ballast water or from where it may have been carried in ballast water to the Hudson the movement of commercial oysters may have transported the River. clam Rangia cuneata from the Gulf of Mexico to Chesapeake Bay, On the California coast, a complex mixture of ballast water, from where it may have spread down the coast to Florida, and ship fouling, or the movements of shellfish may have led to the INTRODUCED MARINE MOLLUSKS OF NORTH AMERICA 1 J

TABLE 3. Summary of introduced marine and estuarine mollusks (excluding opisthobranchs) of North America.

Establishment Not Established Not Certain Established Cryptogenic To Pacific coast (Norrheast Pacific) from· Northwe~t Pacific 12 3 2 Indo-Pacific? Northwest Atlantic 15 2 Northeast Atlantic~ Northeast Atlantic Mediterranean

Subtotal 30 5 To Atlanric coast (Northwest Atlantic/from: NortheaM Atlantic 4 l"? Gulf of Mexico I Northwest Atlantic 2 South America North America

Subtotal 8 2 To Gulf of Mexico from. Mediterranean 1? South America

Subtotal

Total 39(*) 4 7 2

(*)Total of 36 >pecies; Ovateiia. Corbicr~la. and Teredo bartschi arc each >cored twice (sec Table 2), because they originate from different donor regions depending upon the recipient regiom. transportation of the Atlantic mussel Geukensia demin-a from cen­ DISCUSSION tral California to southern California and of the Japanese mussel Musculista scnhousia from the northern Pacific coast to southern Regiono/ Palterns and Mechanisms of Introduction California. Superimposed upon these potential intracoastal mech­ The striking differences between the number of molluscan in­ anisms and routes is the probability that Asian mollusks have been vasions on the Atlantic, Pacific, and Gulf coasts of North America introduced more than once to the Paciftc coast; early introductions (Table 3) may be due to a combination of human-mediated dis­ of the mussel Musculista arc linked to the commercial Pacific persal events and regional geological and biological Pleistocene oyster industry, while its appearance in the 1970s in southern history. The two are diff1cult to separate. California may be due to ballast water release directly from Asian A global mechanism for the potential introduction of non­ ports. Similarly, the Asian clam Theora lubrica may have been indigenous mollusks to all shores is shipping. With the ebb and introduced in separate incidents from Asia to both central and flow of human colonization and commerce, shipping has had a southern California; nearly 15 years separate its initial discovery in differential impact upon different regions at different times. Soci­ southern California bays (to where it was probably introduced in etal changes (the colonization of new lands, the opening and clos­ the ballast water of ships returning from Indonesia and southeast ing of ports due to political changes, the birth of new or the demise Asia during the Vietnam War) from its later discovery in San of old commoditic~, regional and world wars) and shipping Francisco Bay. The latter invasion may be linked (Table 1 , re­ changes (the replacement of wood with iron ships, increased ves­ marks) to an increase in Theora's population in regions which now sel speed, the development of more effective antifouling paints, supply large amounts of ballast water to the Bay. the advent of ballast water in the 1880s) have led to new invasions In contrast to these complex dispersal histories, 2 bivalves have in largely unpredictable manners. Colonization and commercial appeared in North America whose introduction is clearly linked to shipping have occurred on a regular basis between Europe and ballast water release. These are the Asian corbulid clam Pota­ Atlantic America since the early 17th century (or for about four mowrbula amurensis and the Eurasian zebra mussel Dreissena centuries). While contact between Europe and Pacific America is polymorpha. Potamocorbula established large populations in San just as old, regular shipping did not commence until the early 19th Francisco Bay in the 1980s (Carlton eta!. 1990, Nichols eta!. century, or about two centuries later (Carlton 1987). Despite this 1990), at the same time Dreissena was establishing large popula­ two century dichotomy, shipping does not contribute significantly tions in the Great Lakes (Griffiths eta!. 1991). Dreissena is in­ to the regional differences in invasions between the Atlantic and cluded here by virtue of its spread into brackish (oligohaline) Pacific coa~ts (Table 4). waters (Table 1). A second species of Dreissena (May and Mars­ A major mechanistic distinction occurs, however, in the history den 1992), whose specific name remains unclear, also introduced of commercial oyster movements to the two coastlines. Massive by ballast water into the Great Lakes, has not appeared (as of inoculation of the Pacific coast of North America for 60 years November 1992) in estuarine environments in North America. between 1870 and the 1930s with millions of tons of living oysters 14 MOLLUSCAN lNTRODUCllONS AND TRANSFERS

TABLE4. Introduced marine and estuarine mollusks: Mechanisms of introduction of established species (M) in parentheses Indicates one or two possible transport mechanisms; see key, Table 1 footnote.

To:

Atlantic Pacific Golf Coast c .... Coast

MECHANISM Shipping: Fouling/Boring Mytilopsis (BW) Mytilus Perna (BW) Teredo Geukensia (COl) Lyrodus pedicellatus Teredo (2 spp.) Shipping: Solid Ballast LittorifUl (lR) Ovatella Shipping: Water Ballast Rangia (**) Theora Perna (5) Mytilopsis (S) Potamocorbula Dreissena (*) Musculista (COl) Commercial Oyster Rangia (**) Cedna Industry Batillaria Crepida/a (3 spp.) Ceratostoma Urosalpiru: Busycotypus 1/yanassa Nassarius Ovate /Ia Geukensia (S) Museu/isla (BW) Macoma Trapezium Venerupis Gemma Perricola MJ" Lyrodus takanoshimensis Imentional Liuorina (SB) Crassostrea (2 spp.) Release Ostrea Venerupis (Oregon) Corbicu/a (**) Mercenaria Corbicula (*"'*)

* Drei.uena was transported to North America in ballast water from Europe (Carlton, 1992b), but its occurrence in the oligohaline zone of the lower Hudson River is probably due to natural transport as larvae or as juveniles on floating materials from the upper River basin. ** Rangia may owe its reappearance on the Atlantic coast in Holocene times either to the transportation of oysters from the Gulf of Mexico to Chesapeake Bay or to its transportation as larvae in ballast water from the Gulf. Ba!!ast water is the probable mechanism of it~ re<:ent introduction to the oligohaline portions of the Hudson River. Genetic analyses would be of interest to establish whether the Hudson River population originates from the Atlantic coast (such as Chesapeake Bay) or the Gulf coast, if indeed these potential parental fXJpnlations are genetically distinct. •u Corbicula was probably transfXJrted and released intentiona!!y in Western North America no later than the 1920s-1930s (perhaps in more than one incident); subsequent dispersal from western to ea~tem America has been both through anthropogenic means (the use of the clam as bait, for example), and by natural dispersal along water corridors. from Japan and from the Atlantic coast led to the simultaneous Mytilus galloprovincialis, occurs in open unintentional inoculation of scores if not hundreds of species of coast, high energy environments on the Pacific coast; all remain­ associated protists, invertebmtes, algae, seagrasses, and perhaps ing species are restricted to bays and estuaries. While the extraor­ fish. No such introductions of exotic oysters on this scale occurred dinarily diverse molluscan fauna of these open coast rocky shores on the Atlantic coa~t of North America. may thus, in tum, resist invasion, few human-mediated mecha­ As a result, 27 species of Asian and Atlantic mollusks have nisms serve to transport rocky shores species, and it may be that become established on Pacific shores. The bays and estuaries of few if any non-indigenous species from comparable habitats the Pacific coast where these species are established are geologi­ around the world been released into these communities. Thus, on cally young (recently flooded, < 10,000 years old) and do not have the Pacific coast, there was an apparently coincidental combina­ a diverse native biota, suggesting that these systems were rela­ tion of biotically depauperate regions subjected to invasions by a tively susceptible to invasion (Carlton 1975, Carlton 1979b, transport mechanism that served to bring species appropriate to Nichols and Thompson 1985). Only one introduced species, the those habitats from other regions of the world. INTRODUCED MARINE MOLLUSKS OF NORTH AMERICA 15

It is of interest to note that in a parallel sense the most signif­ important in regulating phytoplankton dynamics in the Bay (Carl­ icant molluscan invasion of the Atlantic shore also occurred in a ton et al. 1990). geologically young (recently deglaciated, < 10,000 years old), bi­ On the Pacific coast and Atlantic coasts, interactions between ocically depauperate environment. The European periwinkle Lit­ several pairs of native and introduced gastropods have been ex­ torina littorea invaded hard and some soft bottom intertidal com­ amined. Interactions between the introduced European periwinkle munitie~ of the Atlantic coast in the presence of relatively few Littorina littorea and native gastropods on the Atlantic coast have native herbivorous or omnivorous gastropods. Why, however, been studied by a number of workers. In experimental studies, other western European rocky shore gastropods failed to colonize Petraitis ( 1989) found that Littorina littorea negatively affected the American Atlantic shores during centuries of intensive shipping is growth of the native limpet Tectura testudinalis. Yamada and not clear. It may be that European populations of the common Mansour ( 1987) also experimental!y demonstrated that LittoriM periwinkle Littorina saxatilis have been mixed in with aboriginal littorea can depress the growth rate of the native rocky shore snail populations and thus gone undetected. However, it is clear that a Littorina saxutilis. Brenchley (1982) documented that Littorina variety of other small to medium size European snails (such as littorea wa~ the most abundant consumer of eggs of the native trochids and patellid ) either were not introduced or were mudsnailllyanassa obsoleta in mid-intertidal habitats on the At­ not successful. Here again transport mechanisms may have been lantic coast. Brenchley and Carlton (1983) further demonstrated mre, with little solid (rock) ballast originating from these habitats that there has been a historical change in the distribution of llya­ (which may suggest that ballast rocks may not have been the nassa due to competitive exclusion by Littorina littorea, with mi­ means of introduction of Lirtorina littorea to America). crohabitat displacement in the mid intertidal zone of 70% of Jlya­ The near absence of recorded introduced mollusks in the Gulf nassa, calculated from littorinid removal experiments. Littorina of Mexico may be linked, as with the Atlantic coast, to the absence also limits both the upper and lower distribution of /lyanassa. of large scale importations of commercial oysters or other shellfish On the other hand, Race ( 1982) found that the Atlantic llya­ from other region~. Pre-ballast water shipping contributed few or nassa obsoleta, introduced to San Francisco Bay, in tum limits the no clear introductions, although a detailed biogeographic analysis distribution of the native mudsnail Cerithidea californica, by of the shipworms of the Gulf of Mexico would be of interest. The means of competitive interactions and by predation on Cer­ recent appearances of the South American fouling bivalves My­ ithidea's egg capsules. Whitlatch and Obrebski (1980) found that tella and Perna in Aorida and Texas may suggest that the global while the introduced Japanese snail Batillaria and the native Pa­ increase in ballast water-mediated invasions (Carlton 1985, 1987) cific coast snail Cerithidea can be sympatric in Tomales Bay, CA, may be an active mechanism that will add to the non-indigenous similar-sized individuals exclude each other when feeding on the mollusks of the Gulf. The movement of the zebra mussel Dreis­ same size diatoms. sena polymorpha down the Mississippi River and its arrival Berman and Carlton (I 991) examined the potential interactions (perhaps by 1993) in the oligohaline waters of that delta will between the introduced Atlantic marsh snail Ovatella myosotis and add a second species to the list of Gulf marine and estuarine in­ the native Pacific coast marsh snails Assiminea californica and vasions. Littorina subrotundata. No observational or experimental evi­ dence of competitive superiority by Ovatella could be found, and Er:ologir:allmpacts they concluded that the establishment of the introduced species in With the exception of a few species, there is little experimental high shore, semiterrestrial environments did not arise at the ex­ elucidation of the ecological impact of the introduced marine mol­ pense of the native species. lusks in North America. Carlton (1979b) reviews general ecolog­ While the introduced freshwater bivalves Corbicula fluminea ical considerations, including a remarkable, albeit anecdotal, early and Dreissena polymorpha have had and are having profound account of the interactions between the introduced Atlantic marsh impact~ on the communities in which they have invaded (refer­ mussel Geukensia demissa and the California clapper rail. Nichols ences in Table I), ecological interactions of these species in brack­ and Thompson (1985) document the persistence of an ''introduced ish water remain largely uninvestigated. mudflat community" in San Francisco Bay, where all of the mol­ Perhaps no introduced marine mol!usk in North America has lusks are introduced (Macoma "balthica," indicated as native in had a greater impact than the periwinkle Littorina littorea, which their paper, was later shown to be a probable introduction to the colonized most of the Atlantic coast from Nova Scotia to New Bay (Meehan et al. 1989)). Jersey in only 30 years, between 1860 and 1890 (references in Remaining largely uninvestigated is the alteration of benthic Table 1). Perhaps because little or no economic impact has been community dynamics by the abundant introduced bivalves on the associated with this invasion, it ha<; attracted relatively little notice Pacific coast, such as Mytilus galloprovincialis, Geukensia de­ globally as a classic example of an invasion, aquatic or terrestrial. missa, Musculista senhousia, Mya arenaria, Cnusostrea virgin­ Littorina has fundamentally altered the distribution and abundance ica, Venerupis philippinarum, and Gemma gemma. AI! of these of algae on rocky shores (references in Table 1), altered hard­ species can occur in great densities. Certain community-level in­ bottom, soft-bottom, and salt marsh habitat dynamics (Bertness teractions for some of these species (such as Geukensia, Mya, and 1984) negatively interacted with native gastropods (reviewed Gemma) are known in their donor regions, but are applied with above), dramatically altered the hennit crab shell resource (pro­ difficulty to the Pacific coast where different suites of potentially viding an abundant larger shell) and modified shell utilization interacting species occur. Only the most recent bivalve introduc­ and preference patterns of the native hermit crab Pagurus longi­ tion, the Asian clam Potamocorbula amurensis, has been the sub­ carpus (Blackstone 1986), and as grazing herbivores and vacuum­ ject of intensive observational studies relative to its rapid predom­ ing omnivores, may have important impacts on a wide variety of inance in certain parts of San Francisco Bay, reaching densities of small invertebrates, such as barnacles, whose newly settled larvae > 10,000 per square meter at sites where the former biota has are consumed in large numbers (see "Life Habit" review in become rare or absent (Nichols et al. 1990). Potamocorbula thus Brenchley and Carlton 1983). joinsMya, Musculista, and Gemma as species potential!y critically In summary, all but the snail Ovate/fa of the abundant species 16 MOLLUSCAN iNTRODUCTIONS AND TRANSFERS of introduced mollusks that have been studied have been shown to North America, and of Potamocorbula amurensis in San Francisco have dramatic impacts on the pre-existing structure of the com­ Bay, argue strongly that future, ballast-water mediated invasions munities in which they have invaded. These results would suggest will continue to be a regular phenomenon in North America. On that the extensive populations of those species not yet studied may any day, perhaps any hour, it is likely that the larvae of dozens of also have had, or are having, substantial impacts on population species of mollusks are released into coastal waters of North dynamics and interactions among co-occurring species, both na­ America by ballast water. Similarly, steadily increasing local, na­ tive and introduced. Numerous fruitful investigations remain to be tional, and global pressures to expand mariculture industries undertaken. through the importation of new candidate species will almost cer­ tainly mean the accidental (or intentional) release of novel species. Fulun lr~vasions These predictions arise from the projection that the basic mech­ Predictions of what species will invade, and where and when anisms of human-mediated transport of non-native species out­ invasions will occur, remain one of the more elusive aspects of lined at the beginning of this paper will remain in place for many biological invasion science (Mooney and Drake 1986; Drake et al. years to come. This forecast is despite the existence of a number 1989). Thousands of species of marine and estuarine mollusks that of international guidelines (including those of the International occur in Europe, Africa, South America, Asia, and Australia over­ Council for the Exploration of the Sea, Carlton, 1989) that exist to lap in basic environmental requirements with habitats that occur in prevent the release of detrimental species through fisheries and North America. Selecting probable invasion candidates from this mariculture activities, and despite growing international awareness vast fauna, and predicting competitive, predatory, or other inter­ of the role of ballast water in transporting exotic species trans­ actions with previously established molluscan species or ecologi­ oceanically and interoceanic ally. While our inability to always cal equivalents as potential mediators of successful establishment, distinguish between certain mechanisms of introduction of exotic is a frustrating task. It is doubtful, for example, if an examination species may make full control difficult, identifying and quantify­ of the Asian biota would have identified the clam Potamocorbula ing the role of such mechanisms, followed by cooperative man­ amurensis, among a background of scores of other estuarine taxa, agement efforts, are the necessary precursors to eventually mod­ as a high profile potential invader. ifying the rate of "chess play" of new invasions. Nevertheless certain limited projections may be made. The ACKNOWLEDGMENTS New Zealand fresh and brackish water snail Potamopyrgus anti­ podarum, established in western Europe, and occurring in densi­ For generously supplying records and advice, I thank R. ties of up to 800,000 snails per square meter, is a probable future Tucker Abbott, the late Frank Bernard, Timothy Carey, John invader of eastern North American fresh and oligohaline habitats Chapman, Kenneth Chew, Eugene Coan, Michael Helm, K. (ITC, C. L. Secor, and E. L. Mills, in preparation). Abundant Elaine Hoagland, Robert Forsyth, John Karlsson, the late Myra fouling bivalves in India and Asia, such as the mussels Modiolus Keen, Scott Larned, Harry Lee, Christopher Letts, Roger Mann, striatulus and Limnopernafortunei (Morton 1977), may yet reach James Mclean, Arleen Navarret, Kathleen Sayee, Paul Scott, Ru­ North America. If large scale inoculations of the Pacific oyster dolf Stohler, Ruth Turner, Geerat Venneij, William Walton, and Crassostrea gigas on the Atlantic coast commence in the 1990s (as Mary Wicksten. My graduate students at the University of Oregon opposed to the many smaller previous releases), successful estab­ Institute of Marine Biology (OIMB), including Patrick Baker, lishment may take place (presumably the species will be raised on Jody Berman, Chad Hewitt, and Jolm Megahan, my postdoctoral the Atlantic coast from larvae or clean seed, and the introduction associates at OIMB, including Richard Everett, Jonathan Geller, of associated organisms with large stocks of adult oysters will not and Gregory Ruiz, and my constant field companion, Debby Carl­ take place). ton, were my coworkers in the field in Coos Bay. This work began Also predictable are the eventual detection of natural sets of the as a revision of G (no period follows his first name, G) Dallas Japanese sea scallop Patinopecten yessoensis in British Columbia, Hanna's 1966 Pacific coast monograph, an undertaking I began in the spreading of the European edible oyster Ostrea edulis from 1969 under the aegis of the late Allyn G. Smith, the late Leo G. Rhode Island south and west into Long Island Sound, the estab­ Hertlein, the late Doc Hanna, Charles R. Stasek, and Victor Zullo, lishment of the periwinkle Littorina littorea in San Francisco Bay all then at the California Academy of Sciences in San Francisco. if not elsewhere on the Pacific coast, the establishment of the New This work was supported in part by a National Science Foundation Zealand green lipped mussel (Carlton \992a: (NSF) National Needs Postdoctoral Fellowship at the Woods Hole 16) in California (to where it is now imported daily in large num­ Oceanographic Institution, by NSF Grant No. DAR-8008450 and bers for direct human consumption) and the spreading of the Asian by the NOAA/Oregon Sea Grant College Program, project RIEM- clam Potamocorbula amurensis from San Francisco Bay to other 19. Stimulus to prepare this brief overview was provided by the bays on the Pacific coast. organization of a special symposium, "Molluscan Introductions Broadly, the recent appearances of Rangia cuneata in the Hud­ and Transfers: Risk Considerations and Implications,'' held at the son River, of Perna perna in Texas, of two species of the zebra 82nd Annual Meeting of the National Shellfisheries Association mussel Dreissena in the Great Lakes and thus much of the rest of on April4-5, 1990, in Williamsburg, Virginia.

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Introductions and Transfers of Mollusks: Risk Considerations and Implications

Melbourne R. Carriker

Writings on ecological biogeography provide a global histori­ major sequels come to mind: a) a wide spectrum of other organ­ cal perspective for presentations to be given at this symposium isms can piggyback on or in the invaders, b) potential genetic (Ekman 1953, Briggs 1974, Vermeij 1978, Pielou 1979, Cox and changes can occur in both invaders and residents, and c) physical Moore 1985, Mooney and Drake 1986). In the course of geologic alteration of the invaded habitat can result (Sindermann 1970, epochs, floral and faunal populations of the world have become 1977, Vermeij 1978, Bourne 1979, Rosenfield and Kern 1979, naturally distributed into generally defined geographic areas Courtney and Taylor 1986, Ward 1986, Fisher 1988). Let's con­ whose boundaries have expanded or retreated over the centuries. sider these consequences in more detail: In quite recent geologic history, however, humans have been al­ a) Organisms carried on, or within invaders, for example, tering this pattern critically, wittingly and sometimes unwittingly, could include: manipulating artificially the redistribution of many species popu­ Disease microorganisms (viruses, bacteria, fungi, yeasts, lations. Molluscs have been no exception. These introductions and sporozoans, ciliates, dinoflagellates), transfers have occurred, sometimes beneficially, more often in Multicellular parasites (copepods, trematodes, cestodes, muddled uncontrolled ways, and occasionally with "disastrous odostomid snails, pinnotherid crabs), backlash consequences" to the receiving communities (Odum Predators, especially their larvae and young (muricid and 1971, Rosenfield and Kern 1979, Mooney and Drake 1986). Elton naticid snails, conchs, , crabs), is quoted as writing ''. . about this spate of invasions . . make Competitors contending for food and space (barnacles, no mistake: we are seeing one of the great historical convulsions in bryozoans, sea squirts, chitons, limpets, other com­ the world's fauna and flora" (Dobson and May 1986)! mercial bivalves). In this overview I introduce the symposium, consider the sig­ nificance of artificial dispersal of marine molluscs, and whether In this lengthy list, disease microorganisms and parasites with the reportedly worrisome problems of these invasions are exag­ a single host and with direct waterborne transmission and short gerated or real. Speakers in the symposium will no doubt set me generation times, are potentially the most pernicious in cultivated straight, and bring us all up-to-date on the problems, advantages, molluscan populations (Sindermann 1970, 1977, Dobson and May and safety practices related to human-directed introductions and 1986). The likelihood of introductions of disease microorganisms transfers of commercial and potentially commercial marine mol­ is very high (Fisher 1988); and because checks and balances in the luscs. new .habitat are rarely the same as in the original environment, That dispersal has been occurring with increasing intensity, is invading microorganisms are less apt to be restrained. Because of confmned by many biological surveys. Results of these show that their long association with, and natural immunity to their hosts, marine molluscan biota, especially commercial estuarine and pathogens carried by invaders can have deleterious effects on un­ coastal populations, continue to be moved about widely (for ex­ protected resident species. Unquestionably, diseases will continue ample, Korringa 1942, Allen 1953, Carriker 1955, Hanna 1966, a significant problem in mariculture; the limiting factor in their Anselll%8, Mann 1979, Counts 1983). Large scale global inter­ control is the meager knowledge available about them (Sinder­ mingling, fueled by an increasing commercial market for edible mann 1970). Nonetheless, Sindermann (1970) is optimistic about molluscs, will undoubtedly accelerate its pace. their eventual control. Little, also, is known about multicellular But why the flap over the fact that several molluscan species parasites: how they become established in new hosts remains es­ populations are becoming geographically homogeneous? Why not sentially unexplored (Fisher 1988). adopt the noninterference attitude of "let nature take its course"? b) The genetic consequences of introductions and transfers of Some would suggest that, anyway, little can be done about the molluscan species can be examined instructively with reference to problem, and besides some invasions can be beneficial. Take for how readily they will hybridize. In this context, closely related example, the case of the early, little-controlled importation of invading and native species will produce hybrids differing in fit­ Crassostrea gigas to the West Coast of the United States, which ness from that of the natives. If survival and reproduction of these reaped a valuable commercial industry, a recreational fishery, and hybrids is greater than that of the natives, it is probable that in­ a seed-producing operation (Bourne 1979, Chew 1979). vaders carry genes, which in combination with natives genes, are But alas! because an introduction has been profitable in one advantageous. The rapid introgression of favorable genes will venture does not guarantee that others will be also. Courtney and likely decrease the distinctiveness of the native species-with un­ Robins (1989) put it this way; "What is happening is at best a predictable consequences. If fitness of hybrids is inferior to that of lottery in which an occasional lucky or even well thought-out the natives, then introgression of alien genes will probably de­ success is replayed, only to result in losses in the form of noncor­ crease the fitness of hybrids in the short term; whether reduced rectable environmentaJ mistakes of varying severity.'' fitness persists, will be determined by whether or not it is elimi­ If invasions do constitute a gamble, we should next explore the nated by natural selection. As to whether distantly related species consequences of uncontrolled introductions and transfers. Three will hybridize, is probably not possible to predict. If they should,

21 22 MOLLUSCAN JNTRODUCTIOSS Al'

LITERATURE CITED Allen, F. E. 1953. Distribution of marine invertebrates by shlp>. Austra­ Ehrlich, P.R. 1986. Which animal will invade? In: H. A. Mooney and lian J. Mar. f'reshwal. Res. 4:307-316. J. A. Drake, Eds., Ecology of Biological Invasions of North America Andrews, J. D. 1979. Scenario for introduction of Cra.~.w!lrea gigas to the and Hawaii, pp. 79--95. Ecological Studies 58, Springer-Verlag, New Atlantic Coast of North America. In: R. Mann, Ed., Exotic Species in York. Mariculture. pp. 225~231. MIT Press, Cambridge, Massachusetts. Ekman, S. 1953. Zoogeography of the Sea. Sidgwick and Jackson Lim­ Ansell, A. D. 1968. The rate of growth of the Mercennria ited, London, 417 pp. mercerwria (L.) throughout the geograph1cal range. J. Cons. Perm. Fisher, W. S. Ed. 1988. Disease Processes in Marine Bivalve Molluscs. Int. Explor. Mer. 31((3):364-409. Amer. Fish. Soc. Spec. Pub!. \8. Bethesda, Maryland, 315 pp. Bourne, N. 1979. Pacific oysters, Cra.uoo~trea gigas Thunberg, in British Garton, D. W. & W. R. Haag. 1989. Relationship between shell length, Columbia and the South Pacific Islands. In: R. Mann, Ed., Exotic metabolism and heterozygosity in the introduced zebra mussel Dreis­ SJ)C'ies in Mariculture, pp. 1-53. MIT Press, Cambridge, Massachu­ sena polymorplw. Amer. Zoo/. 29(4): Abstr. 31, p. 7A.

~etts. Hanna. G. D. 1986. Introduced mollusks of Western North America. Occ. Brigg~. J. C. 1974. Marine Zoogeography. McGraw-Hill Book Co., New Papers Calif. Acad. Sci. 48, 108 pp. York, 475 pp. Hedgpeth, J. W. \957. Estuaries and lagoons. 11. Biological aspects. In: Chew, K. K. 1979. The Pacific Oyster (Crassosrrea gigas) in the West J. W. Hedgpeth, Ed., Treatise on Marine Ecology and Paleoecology, Coast of the United States. In: R. Mann, Ed., Exotic Species in Mar­ pp. 693~729. Geol. Soc. Amer., Memoir 67. iculture, pp. 54--82. MIT Press, Cambridge, Massachusetts. Korringa, P. 1942. Crepida/a fornicata's invasion in Europe. Basteria Cairns, J. Jr. 1988. Integrated resource management: the challenge of the 7(112):12-23. next ten years. In: W. J. Adams, G. A. Chapman, and W. G. Landis, Mann, R. Ed. 1979. Exotic Species in Mariculture. MIT Press, Cam­ Eds., Aquatic Toxicology and Hazard Assessment, pp. 559-566. bridge, Massachusetts, 363 pp. Tenth Vol., ASTM STP 971, Amer. Soc. Testing Materials, Philadel­ Mooney, H. A. & 1. A. Drake, Eds. 1986. Ecology of Biological Inva­ phia. sions of North America and Hawaii. Ecological Studies 58. Springer­ Carriker, M. R. 1955. Critical review of biology and control of oyster Verlag, New York, 321 pp. drills Urosa/pinx and Eupleura. Spec. Sci. Rep!.: Fish. No. 148, U.S. Mooney, H. A., S. P. Hamburg & J. A. Drake. 1986. The invasions of Fish & Wildt. Serv., Washington, DC, 150 pp. plant; and animals into California. In: H. A. Mooney and J. A. Drake, Carriker, M. R. 1967. Ecology of estuarine benthic invertebrates: a per­ Eds., Ecology of Biological Invasions of North America and Hawaii, spective. In: G. H. Lauff, Ed., Estuaries, pp. 442-487. Publ. No. 83, pp. 250-272. Ecological Studies 58. Springer-Verlag, New York. Amer. Assoc. Adv. Sci., Washington, DC. Newkirk, G. F. 1979. Genetic aspects of the introduction and culture of Counts, C. L. Ill. 1983. Bivalves m the genus Corbicula Muhlfeld 1811 nonindigenous species for aquaculture. In: R. Mann, Ed., Exotic Spe­ (Mollusca: Corbicuhdae) in the United States: sy~tematics and zooge­ cies in Mariculture, pp. 192-211. MIT Press, Cambridge, Massachu­ ography. Ph.D. Dissertation, University of Delaware, Newark, xxii + ;etts. 451 pp. Courtney, W. R. Jr. & C. R. Robins. 1989. Fish introductions: good Odum, E. P. 1971. Fundamentab of ecology. 3rd Ed. W.B. Saunders management, mismanagement, or no management? Aquatic Sd I (I): Co., Philadelphia, 574 pp. 159--172. Pielou, E. C. 1979. Biogeography. John Wiley & Sons, New York, 351 Courtney, W. R. Jr. & J. N. Taylor. 1986. Strategies for reducing risks pp. from introductions of aquatic organisms· a philosophical perspective. Pimentel, D., M.S. Hunter, J. A. LaGro, R. A. Efroymson, J. C. Fisheries 11(2):30-33. Landers, F. T. Mervis, C. A. McCarthy & A. E. Boyd. 1989. Bene­ Cox, C. B. & P. D. Moore. 1985. Biogeography, An Ecological and fits and risks of genetic engineering in agriculture. BioScience 39:606- Evolutionary Approach. 4th Ed. Blackwell Sci. Publ., Boston, 244 pp. 614. Dobson, A. P. & R. M. May. 1986. Patlem of invasions by pathogens and Regal, P. J. 191!6. Models of genetically engineered organisms and their parasite~. In: H. A. Mooney and J. A. Drake, Eds., Ecology of Bio­ ecological impact. In: H. A. Mooney and J. A. Drake, Ed~ .• Ecology logical Invasions of North American and Hawaii, pp. 58--76. Ecolog­ of Biological Invasions of Nonh America and Hawaii, pp. 111-129. ical Studies 58, Springer-Verlag, New York. Ecological Studies 58. Springer-Verlag, New York 24 MOLLUSCAN INTRODUCTIONS AND TRA."'SFERS

Rosenfield, A. & F. G. Kern. 1979. Molluscan imports and the potential Turner, G. E., &J_ 1988. Codes of practice and manual of procedures for for introduction of disease organisms. in: R. Mann, Ed., Exotic Spe­ consideration of introductions and transfers of marine and freshwater cies in Mariculture, pp. 165--189. MIT Press, Cambridge, Massachu­ organisms. Intemat. Coun. Explor. Sea, Copenhagen, Denmark. Co­ setts. operative Res. Rept. No. 159, 44 pp. Sindermann, C. J. 1970. Principal Diseases of Marine Fish and Shellfish. Venneij, G. 1. 1978. Biogeography and Adaptation. Patterns of Marine Academic Press, New York, 369 pp. Life. Harvard University Press, Cambridge, Massachusetts, 332 pp. Sindermann, C. J. 1977. Disease diagnosis and control in North American Ward, J. E. & C. J. Langdon. 1986. Effects of the ectoparasite Boonea marine aquaculture. Development in Aquaculture and Fisheries Sci­ ( = Odostomia) impressa (Say) (Gastropoda: Pyramidellidae) on the ence, 6. Elsevier Sci. Publ. Co., New York, 329 pp. growth rate, filtration rate, and valve movements of the host Crassos­ Tiedje, l. M., R. K. Colwell, Y. L. Grossman, R. E. Hodson, R. E. rrea virginica (Gmelin). J. Exp. Mar. Bioi. £col. 99:163---180. Lenski, R.N. Mack & P. J. Regal. 1989. The release of genetically Williams, E. H. 1990. Pacific giant clams. Caribbean Mar. Sci. Newslet­ engineered organisms: a perspective from the Ecological Society of ter 1990(1):5. America. Special Feature. The planned introduction of genetically en­ Wooster, W_ S. 1969. The ocean and man. In: The Ocean, Scientific gineered organisms: ecological considerations and recommendations. American Book, pp. 123-130. W. H. Freeman and Co., San Francis- Ecology 70(2):296--315. '"· The Decline of the Virginia Oyster Fishery in Chesapeake Bay: Considerations for Introduction of a Non-Endemic Species, Crassostrea gigas (Thunberg, 1793)'

Roger Mann, Eugene M. Burreson and Patrick K. Baker

ABSTRACT The Chc~apeake Bay oy:.ter fishery for Crassostr~u l'lrginica (Gmehn) ~~ m a ~tate of continuing dcdine. Two di~Ca~e,, 1/ap/osporidium nelsom and Perkinsus mannus have cffcdtvely eliminated oyster; from many >CCtions of the Bay. De>ptte over 30 year; of dt>ea;e a~tJVlty the nallve oy>h:r> have developed neither tolerance nor absolute resistance to these discm.c>, and do not exhibit any recovery m dtsease endemic area; in Virgmia_ Repletion program; have cmnplctcly failed to recover to permanent production area; lo>t to disease_ Prc;cnt fi'>h<'ry rnatJagcment adivitle'> are limited to a controlled retreat away from the di;ease in an arena where di.,ea.,e di.,tnbutwn i~ o;allmty and temperature (and hen\:e climate) related and, therefore. beyuml human intlu~nee. D1;ea;e resi;tance is the pivotal issue Thi., commentary budd' on the reahty that "Without resJ>tance to both diseases no recovery to o;ustaincd, stable production on all formerly productive oyster bottom is possible lt i; improbable that such rni.,tancc can be developed in Cru.1.1mtrea 1·irginica. A consideratiOn i; made of the ca.,e ror imroductlOn of a non-endem1c >pecJes, Crunu_\trea gigas (Thunberg) to assist in attaining this goal

KFY WORDS: CrmJm/rea gJg

INTRODUCTION data collection to allow a balanced decision concerning large ;cale fi~hcry rejuvenation efforts in Virginia. The premeditated movement of aquatic .\pecie., for aquaculture and fi~hcry enhancement purposes ha~ been an adivc component De~eloping the Rationale: llistorical Perspective and Current Situation of animal hu~bandry for over two thousand year~. Pn:~cnt tli.!y activity i~ e~sentially international in ~cope. Stimuli for ~uch Why should an attempt be made to restore or rejuvenate the movemcnb are many and variable. from btological control to de­ oyster resource ofChesapeakc Bay? Although the initial. and per­ velopment of local and national economies to revitalization of fectly dcfcn~iblc. response to this yuc~tion would probably be dcpre;sed econmmes \Offering from native ;pecies depletion because it supports a commercially valuable industry we believe caused by di;ease. overe"ploitation. pollution or some combina­ that the direct commercial exploitation aspect is of quite secondary tion thereof. Elton ( llJ5X). in hi., cla.,sic text on introduced .,pe­ importance. Benthic communities of Chesapeake Bay in precolo­ cic ... comments on the cxten;ive movement of oy.,ter~ around the nial time' were dominated by intertidal oyster reefs. Oyster reefs globe as part of commercial fi.,hery activity. In tht~ commentary were important geological a~ well as biological structures. Reefs we examine argument~ for introduction of the Pi.!cific or Japane~e wpported extensive communitie~ that, in tum, provided the base oyster, Crasso.1trea gigas (Thunberg). to Che.,apeakc Bay tu wp­ level~ of food webs that eventually support comercially important plement prnductton that is currently supported only by depleted tlnfi<;h and crab ~pccie~, important trophic intcrm;tions that are stocks of native Cm.I.\OStrea \'lrgimca (Gmclin) often underestimated in current attempts to "manage" finfish and Comprehcn.,ive gUJdelmes for consideration of and effecting crab stocks on a species by specie~ ba~i>. Demise of thi' produc­ introductions have been developed independently by ICES (lntcr­ tive benthic community has perhaps re~ulted in comparable demi~e nattonal Council for the Exploration of the Seas). EIFAC (Euro­ of the commercial finfish and crab stocks. Limiting tishmg effort pean Inland Pishcrie; Advismy Commi~~ionl and AFS (the Amer­ on other species will have only marginal positive impacts. Further, ican Fisheries Soctetyl. These guidelines empha~ize the followmg: the role of the oyster in harvesting primary productivity in Ches­ (a) a clear rationale for introduction. apeake Bay cannot be understated The calculations offered by (b) selection of candidate species. mduding a con.,·ideratton of Newell { 19X9) arc illuminating-a two order of magnitude de­ associated pests. para~itcs and disease.,, crca~c in filtration capacity compared to pre~ 1870 oyster stocks! (c) te~tin)!. utilizing quarantine systems. before a decision to Whereas the rc;ident oyster population once had the capacity to proceed with introduction. filter the water~ of the bay in 3.3 days, the present stocks can only (d) mtroduction u.,ing quarantine procedures and monitoring manage the same task in approximately 325 day:,-----and the stocks i.!l'tcr relea~e to provide data for subsequent consideration; are still declining. A healthy and substantial oy;ter ;tuck in Chc~­ for mtroduction~ apeake Bay would probably be the single most effective mecha­ Our commentary will focus on items tal through (c) of the nism of ~imultancously harvesting microplankton, reducing the above li~t. including a bnef discus-,ion of the legal climate in this impact of eutrophication, ~u~taining a directly harvestable rc­ particular ca'c. and conclude with a description of future efforts in ~ource. improving water quality and maintaining a diverse and 'table food web. Unfortunately, four centurie'i of neglect. mis­ management und wholesale mining of the oy.,!er re~ource (both 'Cuntnbutwn number 17 !4 from the V1rgima !mtl!Utc of Marine Snenc~. living and shell, the latter for indu.,trial purposes-see Haven, School of Marine Science. Col kg<' of William and \1~· Hargi; and Kendall 1978, Kennedy and Brci~ch 1981 } has resulted

25 26 MOLLUSCAN lNTRODUt-"TJONS AND TRllliSFERS in the present scenario where spar~e. di~casc ravaged populatmns nudcd. high salinity oyster bed would require <1 minimum of three survive in disparate, low salinity sanctuaries as subtidal cru~t~ of years without 'ieriou~ dl';ease lo~se~ before a ~ingle crop of mar­ living material overlaying a ba~e of reef material. The importance ketable oy~ter~ would be attained. Clearly, management around of the oyster as a cornerstone specie~ in Chesapeake Bay ~urpas~es typical, rather than atyp1cal, rainfall and streamflow condition~ i~ that of the directed fishery in both ecological and economic term~. unpredictable and imprudent yet it is the latter that cmbodic~ a disproportionate political power The subject of natural disease resistance and the development and which, by default, wiH eventually drive decision processes of disease resistance in cultured stocks of the native oyster. Cra.\­ concerning restoration and rejuvenation including possible intro­ sosrrea virgin ira, has received considerable attention. Di~tinction ductions. With this political reality clearly stated we will proceed should be made between tolerance to a greater para~ite burden, with a greater focu~ on the directed commercial fishery aspect of wherein mortalities w11l eventually occur but at a decreased rate. the discussion. and resistance, where no p<~rasite related losses arc observed. The The oyster (Crassostrea virginica) resource of Chesapeake Bay notion that di~case resistance would ;~llow recolonization of pres­ has been in continuing decline since the turn of the century (Ha­ ently barren areas, with the ensuing rejuvenation of the industry, ven, Hargis and Kendall 1978, Kennedy and Breisch 19k L Hargis i~ untenable with re~pect to Chesapeake Bay for several reasons. and Haven 1988). Prior to 1960, average annual oyster production Natural populations, with their enormous fecundities, have failed was 3.5 million bushel~ in Virginia

Selection of Specie.~ for Introduction: Why Crassostrea giga.~? extcn~ivcly (both accidentally and intentionally) moved beyond its native oriental range for culture purposes to locations in the Pacific When considering the selection of species for introduction it is basin (Costa Rica through Alaska, Australia, New Zealand), and important to effectively match the donor and recipient environ­ the Atlantic basic (North Sea through Mediterranean and Atlantic ments to insure greatest possibility of successful survival of the Coast of Morocco). Comprehensive summaries of these activities mtroduced specie~. The Chesapeake Bay environment can be char­ are given in Mann (1979, 1981) and Menzel (1990). Crassostrea acterized as having a continental climate with large air and water gigas is the ba~is of the largest oyster fisheries in the world. temperature ranges: large temporal and spatial salinity variation; a During 1987 the leading oyster producing countries in the world geologically young, sedimentary basin that has been extensively were Korea and Japan with production of 303,233 and 258,776 dredged to facilitate past and current wmmercial shipping; a re­ metnc tons respectively, this product being predominantly gion where ~alinity related endemic diseases currently limit native oyster distribution, and an irretrievably altered watershed that (;Ur­ TABLE I, rently serves as home to over 14 million people. In summary, this is a high stress environment that is drastically altered from that Crassostrea species: Distribution and Synonyms. Source material: I. Ahmed, 1971; 2. Boffi, 1979; 3, Carreon, 1%9; 4. Chen, 1972; S. prior to colonial settlement-the environment in which Crasms· Dang, 1972; 6, Durve, l%7; 7. Kamara eta!., 1976; 8, Kong and rrea virginica nourished to form reefs that were major geological Luh, 1977; 9, Mann, 1981; 10. Menzel, 1974; IL Newhall and features as well as dominant components of the benthic commu­ Carriker, 1983; 12. Shafet" and Sabatie, 1986; 13. Tebble, 1966; 14, nity of Chesapeake Bay. The magnitude of change over the past Torigoe, 1981; IS. Zenkevitch, 1%3, four centuries ~hould be underscored. De~plle continuing effort~ to improve water quality in the bay it must he realized that the cu­ Atlantic coast of North America: v~rgm1ca ( = rhizophorae), 11. mulative abuses of urban and agricultural development to the hay Brasil: brasiliensis ( = rhizophorae = virginica?), 2, 7 watershed make the goal of restoration of the bay to its former We~tem Europe, English Channel to Morocco (now rare): angulata. 10. pristine condition (as described in Captain John Smith's log~} un­ 13 tenable. Intertidal oyster reefs no longer exist in the bay, they have Europe, North Sea through Mediterannean to Morocco: gigas, 9. 12. been tonged and dredged to subtidal depths generally exceeding Pacific coast of North Amenca: gigas. 9. 12. one meter. The quantitative change in oyster reef structure asso­ Japan. Korean Pcnim,ula through Y1etnam: g1gas. araikensis Ciated w1th their degradation from intertidal to subtidal features is ( = rivularis), nippona. 5, 14. illu~trated by the fact that present, immediate subsurface shell India: gryphoides, madrasensis, rivularis ( = araikenbib). 1, 6. depo~it~ have been radiocarbon dated at several hundred years ThailandiMalay~ia: belcheri ( = nippona"l). 4, 8. Philippines. ircdali ( = madrascn~i~ or even = rivularb"!). 3 before pre~ent (DcAlteris 1988). We't Afnca: gasar ( = tulipa). 7. It is appropriate to begin a search for an alternate spec1es within Black Sea: taurica, 15 the genus Crassosrrea-rccf forming ~pecie~ tolerant of mid to 28 MOLLUSCA:>/ INTRODUCTIONS AND TRANSFERS

TABLE 2. Temperature and salinity ranges of adults of Crassostrea specie>. Optimum ranges given in parentheses.

Temperature (C) Salinity (ppt)

Species Growth Spawning Growth Spawning Reference virginica 5-34 (28--32) 18--25 (23) >5 (12-27) >8 7,8,20,21,2Dl angulata 20--30 20 21--43 <33 3,4, \6 araikensis 7--40 (30--40) 5.11,16 gasar 25-30 5-34 14--20 1,28,29 gigas 3-35 01-34) 16-30 (20-25) 10--42 (35) 10--30 (20--30) 2.4, 15' 18,19,24,25 gryphoides 19---33 27-31 4--40 (30--40) 13-29 II, 13,23 iredali 30--33 <45 >15 4 madrasensis 26 (30) 1--41 (8-25) 17-35 (20--35) 16,17,26,27,30 mppona no data rhizophorae 22--40 (2fi.-37) 4,5, 12 lauric a 3-28 17-18 32 Reference: Ajana, 1980; 2 Allen et aL, 1988; )_ Amemiya. 1926:4. Bardach et al.. 1972; 5. Boveda and Rodriguez, 1967:6. Breese and Malouf, 1977; 7. Butler, 1949; 8. Chanley, 1958; 9 Davis, 1958; JO_ Davb and Calabrese, 1964; II. De~ai et al., 1982; 12. DosSantos and Nascimento, 1985; 13. Durve, 1965; 14. His et al., 1989; 15. Hughes-Games. 1977. 16. Jhingran and Gopalakrishnan, 1974; 17. Joseph and Madhyastha, 1984; 18. Kmg, 1977; 19. Le Gall and Raillard, 1988; 20. Luu~anuff, 1958; 21 Luusanuff, 1969: 22_ Loosanoffand Davis, 1952; 23. Mane, !978; 24. Munmaka and Lannan, 1984; 25. Nell and Holliday, 1988; 26. Rao, 1951; 27. Rao and Nayor, 1956; 28. Sandison. 1%6; 29. Sandi;un and Hill, 1966; 30. Stephen, 1980; 31. Well~. 1961; 32. Zenkevitch, 1963

C. gigas. By comparison the United States, ranking third, pro­ C. gigas appears resistant to challenge by both Bonamia ostreae duced 217,632 metric ton~ (a mix of C. gigas and C. virginim) and Marteilia refringens, diseases that continue 10 decimate native and France, producing predominantly C. gigas after initial intro­ European oysters. The analogie~ with Chesapeake Bay are pain­ duction of the species some 15 years earlier, ranked founh at fulty obviou~. 123,162 metric tons. Crassustrea gigas is elegantly ~uited for hatchery production as demonstrated by the enormous success of Risk AnaJ,sis for Introduction of Diseases wi.lh Crassostrea gigas the hatchery-based industry in the U.S. Pacific Nonhwest. Com­ mercial production based on hatchery produced seed oysters in the The argument in support of po~sible use of Crassostrea gigas Northwest far exceeds present oyster production from the entire in re~toration of the presently unproductive areas of the bay has, to Chesapeake Bay. Domestic oyster production cannot satisfy the th1s juncture, appeared positive. Questions of diseases associated market need and the United States has, since 1985, held the du­ with C. gigas in its native and introduced range remain-are there bious distinction of being the world's leading importer of oyster~ such diseases and could they be transferred to the bay with an in fresh and frozen form. introduction? Crassostrea gigas has, in its native range, no known The native nonhern European oysters 0.1·tret1 edulis and Crw­ diseases that have been associated with large-scale mortalities sostrea angulata were decimated by disease in the mid 1970~. (Koganezawa 1975). In addition, it has been used successfully as Production of the fonner fell from 15,000 tons to the present day an introduced species in area~ where the native oysters have been level of 2,500 tons per year. Production of the latter fell from decimated by diseases. Crassostrea gigas has been resistant to the 60,000 tons per year to zero. The industry was saved from eco­ local diseases and no new disease introductions have been posi­ nomic extinction by the introduction of C. gigas. European C. tively documented even though, in certain areas, C. gigas has been gigas production (including French) now employs over 20,000 introduced with few, if any, control measures. For example, C. people and produces approximately 140,000 tons of oysters per gigas is not susceptible to Bonamia ostreae and Marteilia refrin­ year, this representing over 80% of the total production. Further, gens. diseases that have caused massive mortalities in Ostrea edu­ lis, the native species in western Europe, and it has not been susceptible to similar protozoan diseases where it has been intro­ TABLE 3. duced in Australia and New Zealand. In addition, C. gigas is Temperature and salinity ranges of Crasso.strea larvae. Optimum resistant to the viral diseases that caused mass mortalities of the ranges given in parentheses. Referenct' material as in Table 2 in France. The Japanese oyster is the basis for the hatchery-based industry in the Pacific Northwest and no new Species Temperature (C) Salinity (ppt) Referen« diseases (that cause measurable monality) have been introduced into that region (Giude 1975) even though there have been periodic virgimca 20-33 8---39 (10-291 3.9. 10 importations of C. gigas since 1902 and early introductions were angulata 21--43 (28---35) 3.4.16 effected without any control measures being enforced. Andrews araikensis 20-28 (26---28) 10-30 (201 gigas 18---35 (30) 19---35 2.14.15 ( 1980) reviewed oyster introductions around the world and dis­ rhizophorae <30 (25) 20-40 (281 12 cu~sed potential problems with such importations and precautions necessary to avoid disease introductions. no data available for ga~ar. gryphoide;. iredali. madrasensis. The extensive movement of C. gigas has provided, in addition nippona and taurica. to the native range, many potential sources for broodstock for a iNfRODUCTION OF C. GIGAS IN CtiESAPEAKE BAY 29 proposed introduction. For the present di~cussion we will essen­ sugge~ts that the viruses were already pre~ent in France. Unfor­ tia!ly limit our consideratum of source broodstock to that from the tunately, no attempt was made to i~olate viruse~ at that time, so we state of Washington. Despite the fact that the ped1grees of these will never know with certainty if the viruses were already present. stoch are not definitively documented. the ~tocb arc mo~tly of Potential implications: GNV and HIV have never been ob­ Myagi Prefecture origin but many years of hatchery breeding may served in C. giga.1 from the Pacific Northwe~t. In addition, the have resulted in some limited crossing with stocks from other very characteristic gill lesion caused by GNV has never been ob­ sources, they do have a known and documented history concerning served (R. A. Ebton, personal communication, 14 March 1990). associated pests, parasites, and diseases. The listing below in­ There are many report~ in the literature of other viruses in cludes only those organisms reported from C. gigas that arc actual oysters and other marine molluscs, including five different viruses or potential disea~e agents in oysters or other bivalve molluscs. It from the , C. virginica (Johnson 1984). There is no does not include the numerous parasites, mostly metazoan, found finn evidence that any of these viruses (other than HIV and GNVJ in oysters world-wide that have never been implicated in host can be pathogenic to their hosts. mortality 3. Bacterial Diseases. I. Diseases of Unknown Etiology. a. Bacillary Necrosis. Many species of bacteria in the genus Hematopoietic Neoplasia. This disease results in a mas~ive Vibrio are present naturally in seawater. They are not normally tissue invasion of abnormal blood cells and is analogous to leu­ pathogenic, but can become so because of adverse environmental kemia in vertebrates. It has been implicated in large-scale mortal­ conditions, usually high temperature. These bacteria have been ities of mussels in the state of Washington and of soft-shel! clams implicated in often complete mortality of larvae in hatcheries from in Chesapeake Bay. The syndrome has been reported in C. gigas, various regions of the world. Juvenile oysters have also been re­ C. virginica, and 0. lurida. but has not been associated with ported to be affected in hatcheries in Maine. Affected oyster spe­ mortality in these species. A virus has been suggested as the cause cies include C. gigas, C. virginica and Ostrea edulis (Elston 1984, for thi~ di~ease, but the evidence is weak. Sindermann and Lightner 1988). Potential implications: This syndrome i~ already present in Potential implications: Vibrios and other bacteria that may Chesapeake Bay and ha~ been ob~erved occasionally in C. vir­ cause this problem are present naturally in seawater. Rigorous ginica. hatchery sanitation measures usually are sufficient to prevent mor­ 2. Viral Diseases. talities. The Virginia Institute of Marine Science oyster hatchery has experienced no problem of this type. a. Oyster Velar Virus. This disease affects oyster larvae and b. Nocardiosis. This disease is caused by the actinomycete has been reported from two hatcheries in the state of Washington bacterium Nocardia and often results in raised green to yellow (Elston and Wilkin~on 1985). It has been observed occasionally in nodules on the mantle. It is apparently at least partially responsible hatchenes from March to August in larvae greater than 150 1-lffi in for the historically reported phenomenon of sununer mortality in shell height. Infection results in lo~~ of motility and death of adult C. gigas in the Pacific Northwest (see Friedman, Beattie, larvae. Mea~ured lo~~e~ of hatchery production up to 50% have Elston and Hedrick 1991). Similar nodules have been observed in been recorded. but there i~ no established link between the disease other oysters from other areas. including C. virginica (Elston, and mortality since it has not been experimentally tran~mit!ed. Beattie, Friedman, Hedrick and Kent 1987), but the cause of the There have been no reported outbreaks of the disease in recent nodules has not been determined in those cases. years (R. A. Elston. Battelle Center for Marine Disease Control. Potential implications: This is a husbandry disease with local Sequim, WA. per~onal conununication). environmental sources of the bacterium in Washington and British Potential implications: This virus is primarily a hatchery Columbia which is restricted to certain embayments. It is not a problem where larvae are held at high density in tanks, but even in disease of major concern in those areas. hatcheries the virus has never caused mortality over 50%. It is not c. Rickettsiae. Rickettsiae are obligate intracellular organisms expected to be a problem in nature where density of larvae is much and have been reported from digestive diverticula epithelial cells lower than in hatcheries and transmission of viral particle~ be­ in C. gigas, C. virginica, and many other bivalve molluscs (Kinne tween larvae i~ greatly reduced. 1983), but are not known to be responsible for mortality. b. Hemocytic Infection Virus (HIV) and Gill Necrosis Virus Potential implications: Rickettsiae have already been reported (GNV). These iridoviruses have been reported from C. gigas in from C. virginica in Che~apeake Bay. France. Both viruses were implicated in mass mortalities of the Portuguese oyster C. angulata in France during the 1970s (Comps 4. Protozoan Diseases. and Bonami 1977). but neither virus causes mortality in C. gigas in the same area (Comps 1988). In fact, Comps (1988) ~tales that a. Marteilia refringens. This parasite has been responsible for the ability of C. g1gas to re~ist mortality from these viruses re­ massive mortality of the native oyster Ostrea edulis in France. solved a very serious economic problem associated with the total Marteilia refringens ha~ also been reported in C. gigas in France elimination of the Portuguese oy~ter. (Cahour 1979), but prevalence and intensity were low and only There has been ~orne ~peculation that C. gigas is a carrier for early stages of development were observed. The infections were these viruses and that one or both of them was introduced into considered to be transient and no mortality has been observed inC. France with importation~ of C. gigas from Japan. According to gigas. Henri Grizel, IFREMER, France, (personal communication, 12 Potential implications: This parasite is known only from Eu­ March 1990) the lesions characteristic of the viral infections were rope and does not develop nonnally in C. gigas. There is little observed in C. angulata prior to introduction of C. ~:igas, which chance of importing this parasite if the brood stock is limited to C. 30 MOLLUSCAN INTRODUCfTONS AND TRANSFERS gigas from the state of Wa~hington, and ICES guidelines for quar­ never been very strong. A recent, thorough, ten year <>tudy (Davey anline of broodstock arc followed. 1989) on a related species in mussels found no evidence of host b. Haplosporidium spp. A parasite that is morphologically mortality and the author argues forcefully that Mytilicola has been similar to Haplosporidium nelsoni (MSX) has been observed in C. wrongly indicted in previous mortalities. gigas in Korea (Kern 1976). Prevalence was very low, only 0.28% Potential implications: This parasite infects adult oysters and in I ,438 oysters examined, and no mortality has been reported. can be easily controlled by quarantine of broodstock in the hatch­ One of the four infected oysters contained spores and they were ery. restricted to epithelium of the digestive diverticula, as they are in In summary. quarantine of broodstock in a hatchery and the use H. nelsoni. Another haplosporidan was reported in a single C. of first generation offspring for any field studies, that is compli­ gigas from California (Katkansky and Warner 1970). Spore~ were .ance with ICES guidelines for introduction of non-native organ­ observed throughout the connective tis~ue, similar to Haplospori­ i~ms, will prevent introduction of all disease agents listed above dium costale (SSO) in C. virginicu. but spore size wa'i intenne· except viruses, bacteria and the ovarian parasite Marteilioides diate between H. nelsoni and H. costa/e. Pla~modial ~tage~ of a chungmuensis, which i~ not known to cause mortality. If brood­ haplosporidan were observed in a single C. gigas from Washing­ Mock were limited to one source. the ~tate of Washington, such ton (Percya 1964). problems could be minimized in that no pathogenic viruses are Potential implications: There has been speculation that the known in adult C. gigas from Washington and M. chungmuensis two haplosporidans from Korea and California are H. nelsoni and is absent from that area. There are no published reports of a serious H. costate re~pectively and that they were introduced to Chesa­ disease outbreak in C. gigas from Washington and there are no peake Bay region with unauthorized private plantings of C. gigas documented disease introductions (that have resulted in measur­ during the 1950s; however, there is no direct evidence and it able mortality) from the numerous introductions of C. gigas that remains only speculation. There is no danger of importing these, have occurred around the world. Some incidental parasites have or any other, parasites with C. gigas if imtial broodstock are kept been introduced, but such introductions would not have occurred in quarantine and only uninfected progeny from the hatchery are if ICES guidelines had been followed used in ~usceptibility ~ludic~ or pos~ible introductions. c. Marteilioides chungmuensis. This parasite infects eggs of Susceptibility of Crassostrea gigas to Diseases Endemic to Chesapeake C. gigas in Japan and Korea (Comps. Park and Desportes 1986). Bay: Perkinsus marlnus and Haplosporidium nelson! It is related taxonomically to important oyster pathogens such as Marteilia refringens discussed above, but M. chungmuensi~ is not Of the two diseases endemic to the bay Perkinsus mannus is known to cause mortality. Thi~ para~ite may be what Becker and the only one amenable to laboratory experimentation. Haplos­ Pauley (1968) observed in eggs of C. gigas in California. Les~ poridium nelsoni challenge can only be adequately effected by in than 10% of the egg~ were infected in any one female oyster and situ exposure in H. nelsoni endemic areas. All stages of P. mari­ there was no evidence of oyster mortality. nus are infective and the addition of finely minced, infected oyster Potential implications: Transmissmn stud1e~ have never been tissue ha~ been found to be very effective at initiating new infec­ attempted with this para~ite and the life cycle i~ unknown: how­ tions in previously unexposed oysters in laboratory systems (Mey­ ever, this parasite infects eggs ~uggcsting that quarantine of brood­ cr~.etal.l991). stock may not provide sufficJCnl control. Th1s parasite ~~ appar­ The ~usceptibility of both C. virginica, originating from Mob­ ently not pathogenic and it has never been reported from the Pa­ jack Bay broodstock, and C. g1gas. Fl animals cultured at cific Northwest. Gloucester Point. VA from a broodstock imported from Washing­ d. Mikrocytos mackini. This parasite infects vesicular connec­ ton state in February 1989 and maintained in quarantine under tive tissue cells and causes abscess-type focal inflammatory le­ ICES guidelines throughout study, toP. marinus was examined in sions in the mantle and gonad of C. gi~-:as. It is known only from two ~eparatc experiments by Meyers. et a!. (1991). In the first British Columbia, Canada although a similar parasite has been experiment of 83 days duration 40% of the C. gigas became in­ observed in C. gigas from Hawaii (Farley, Wolf and Ebton J9RR). fected compared to 100% of the C. virginica. In the second ex­ Average mortality of 34'k was ob~ervcd during early occurrence~ periments prevalence was high in both species after 60 day~. but of the disease before gmwers learned proper man;.~gement tech­ differed in intensity with moderate to high levels in C. virginim niques to avoid mortanitation procedures limit water and food availability and thereby cated in sporadic mortalities of C. gigm·. but the evidence has provide continuing stress on maintained animals, it is probable that INTRODUCTION OF C. GIGAS IN CHESAPEAKE BAY 31 di~ea~c. if present, would have already manife~ted itself; however, Chc~apeake Bay and competitive interaction with the native ~pe­ no evidence of di~ea~e organisms has been ~ceo in hbtolog1cal cies, C. vir~:iniw, both within the bay and potentially oubide the sections of sampled animals. bay if C. gigas were to ~pread to either the north or the ~outh of the bay mouth. During the period 1940 through 1960 te~ting of C The Dilemma: Where to Now? gtgas wa~ conducted in the lagoon ~y~tem~ of the Delmarva pen­ in~ula and Delaware Bay. Resident populatmn~ have not re~ulted To this point we have presented argument~ to ~upport the fol­ although the~c may have been precluded by the nature of the lowing: introductions. Adequate documentation i~ unavailable. The Del­ (I) Native oyster populations continue to be decimated by en­ marva coastal lagoons and intertidal flats still maintain consider­ demic diseases, leaving large areas of fonnerly productive able oyster resources. On the Atlantic ~eaboard north of the mouth bottom unproductive in disease endemic area~. of Delaware Bay, where P. marinus is absent, the native oyster (2) Current management practices have failed to reclaim to continues to exist as disjunct populations of various sizes, but permanent production areas lost to disease. alway~ at levels well below hi'itorical records. These regions have (3) Selected strains of native oysters, developed at Rutgers again suffered variou~ly from disease, including H. nelsoni, sus­ University, have developed tolerance to H. nelsoni: how­ tained harvesting and degrees of environmental degradation. Re­ ever, the surviving population in the Chesapeake Bay ha~ cent efforts to revive the Connecticut oyster industry through ex­ developed neither tolerance nor resistance to the two en­ tensive shell planting and resource management are meeting with demic diseases when they occur in combination as dem­ some success. Limited, culture based production exists in New onstrated by their absence from disease endemic area~. England, and both cultured and wild caught oysters are available (4) It is timely to consider another oyster species that may have from the Canadian Maritime provinces. Investigations at Rutgers improved tolerance or resistance to the endemic diseases to University, described earlier, concerning increased tolerance to H. assist in reclamation of currently unproductive bottom. nelsoni offer some hope of expanded oyster production in this (5) A ~urvey of the available literature, although limited, sug­ geographic region but large scale production and reintroduction of gests that Cras.1·ostrea gigas has salinity and temperature the native species remains an enonnou~ task. With respect to pos­ tolerances similar to the native oyster. sible establishment of C. gigas south of Chesapeake Bay, the data (OJ Laboratory challenges of Crassostrea gigas with Perkinsus of tables 2 and 3 are of limited use in estimating range extension marinus strongly suggest that it is much more tolerant than in that definitive temperature and ~alinity tolerance tests have not the native species of oyster. been published for C. gigas. Such data are clearly desirable. Some From this basis we will proceed to present arguments in favor further information may be obtained from detailed examination of of continuing examinatmn of the proposed introduction and the current oriental culture practices within the native range of C. benefits that will accrue. It is important to underscore that any gigas (see Kusuki 1990); however, caution must again be applied further pursuit of this line of inve~tigation in terms of disease in determining which geographic type of C. g1gas is being de­ challenge will necessitate de facto introduction of Cras.wstrea scribed. gigas into Che~apcake Bay waters_ This is the only way to effect Competitive interactions in a two species scenario in Chesa­ meaningful challenge with H. nelwni. Despite the availability of peake Bay with C. gigas in higher salinities and C. virginica in ICES protocols to insure practically minimal introduction of asso­ lower salinities are difficult to predict because only a few mean­ ciated pests, para~ites and diseases. and triploid induction tech­ ingful analogies exist. One such analogy i~ the Chinese culture of niques to minimize spawning (review by Beaumont and Fair­ C. gigas relative to that of the Suminoe oyster, Crassostrea rivu­ brother 1991), there is no practical manner to absolutely insure laris. The latter species is, like the Myagi type of C. gigas, fast that no spawning of ~tock introduced for experimental purposes growing and often quite large; however, it is generally acknowl­ will occur. A comprehensive examination of such issues as tem­ edged by Chinese workers (personal communication to Roger perature and salinity tolerances of the various life h1story stages of Mann) to tolerate lower salinities. What limits the distribution of (' xigas, and laboratory examination of susceptibility to local each of the Crass0-1trea species in the Chinese fisheries? This is predators and physical environment can only provide greater abil­ not adequately documented, thus limiting our predictive capability ity to evaluate pos~ible establishment and range extension inChes­ for Chesapeake Bay if a reproductively active population of C. apeake Bay. They cannot provide an avenue to eliminate the pos­ gigas i~ introduced. The second analogy is the estuarine environ­ sibility of spawning. In situ H. nelsoni challenge of C gigas has ment of the Gironde on the Charente River in western France (the already been the subject of pointed debate among academics, reg­ major seed oyster producing area for C. gigas) and in south west ulatory bodies and industry at both an intra and interstate basis. France where harvest pressure is comparatively light, allowing Effecting such a study cannot be accomplished without limited risk greater densities of oysters to develop (Hera! and Deslous-Paoli of development of a self sustaining, resident population of C. 1990). The fonner location can be used as an analogy to the James gigas in Chesapeake Bay. Proceeding with such H. nelsoni chal­ River seed oyster beds and the latter location as an analogy to a lenges arc an integral and neces~ary component of identification of situation in Chesapeake Bay where C. gigas is introduced as a disease tolerant or resistant stocks, be they of native or non­ reproductively active population to currently unproductive bottom endemic origin. Eventually, a balanced deci~ion mu~t be made by in di~ease endemic areas and allowed to proliferate without exces­ regulatory agencies concerning the competing pressure'i to expe­ ~ive harvc~t pres~urc. Such a situation would obviously necessitate dite rejuvenation of an ailing industry and consider the unpredict­ ~cvcral prerequisites including regulatory approval to effect in situ able biological consequences of introduction of a non-endemic disease challenge, a demonstrated resistance to H. nelsoni. and a species funher regulatory decision to effect refurbishment by release of A major source of debate ~ub~umed in the question of in situ reproductively active C. gigas cultured through ICES protocols. testing is the poss1ble impact of a resident C. gigas population in The argument for a comprehensive examination of both the Chi- 32 MOLLUSCAN li'

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Fishing News Books, Ltd., Sur­ (Crassostrea •·irfiinica) resistant and su~ceptible to Minrhmia ne/.mni rey, England. caused mortality. Ph.D. Dissertation. Rutgers University, New Katkansky, S. C. & R. W. Warner. 1970. Sporulation of a haplosporidan Brunswick, NJ. 232 p in a Pacific oyster (Crassostrea gigas) m Humboldt Bay, California. 1. Durve, V. S. 1965. On the seasonal gonadal change and spawning in the Fish. Re.L Bd. Canada 27(7):1320-1321 adult oyster Crassostrea J?r.phoide.~ (Schlothcim). 1. Mar. Bioi. A.1- Kennedy, V. S & L. L. Breisch. 1981. Maryland's oysters: research and .wc. India. 7(2):328-344 management. Maryland Sea Grant, University of Maryland, College Durve. V. S. 1967. On the nomenclature of two Indian backwater oy~ter;. Park, MD. 286 p. 1. Mar. Bioi. A.Hoc.lndia. 9(1):173-178. Kern, F. G 197li. Sporulatmn of Minchinia sp. (Hap!osporida, Haplo­ Elton, C. S. 1958. The ecology of invasions by animals and plants. 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Aquaculture 41:!: 189- cultured oysters m Japan and its prevention. Proc. 3rd U.S.-Japan 210. Meeting on Aquaculture, 1974:29-34 Farley, C. A .. P. H. Wolf & R. A. Elston. 1988 A long-term study of Kong. C. P. & L.A. Luh. 1977. Notes on the efficiency of various ma­ ""microcell · disease in oysters with a descnpllon of a new genus, teriab tested as oyster spat collectors in Cowie Bay. Sabah. Malaysian Mi/l.rocytos (g. n.), and two new species, Mi/l.rocyros mac/l.ini (sp. n.) Awicult. Jour. 50(4):462-479 and Mikrocyws rouJ?hleyi (sp. n.). fr.~h. Bull. 86(3):581~593 Kusuki. Y. (1990). Oyster culture in Japan and adjacent countries: Cras­ ford, S. E. 1986. Companson of hemolymph proteins between resistant sostrea gigas (Thunberg). In: Estuarine and Marine Bivalve Mollusc and susceptible oyster;, CraJSostrea virJ?inica. e~posed to the paras1te Culture R. W. Menzel (Ed). CRC Press, Boca Raton, FL. pp. 227~ Haplosporidium ne/soni (MSX). }.Invert. Pathol. 47:283--294 244. Ford. S. E. & H. H. Haskin. 1987. Infection and mortality patterns in Le Gall, J. L. & 0. Raillard. 1988. Influence de Ia temperature sur Ia strains of oy;ters Crassmtrea l"irginica selected for res1stance to the physiologic de l'huitre Crassostrea gigas. Oceams 14(5):603-608. parasite Haplospondium ne/o~oni (MSX). 1. Parasitol. 73:368-376. Loosanoff. V. L. 1958. Some aspects of behavior of oysters at different Friedman. C. S .. J. H. Beattie, R. A. Elston & R. P. Hedrick. 1991 temperatures. Bioi. Bull. 114( 1):57-70 Investigation of the relationship between the presence of a Gram­ Loosanoff, V. L. 1969. Maturation of gonads of oysters, Crassostrea positive bacterial infection and summer mortality of the Pacific oyster, virJ?inica. of different geogr.1ph1cal areas subjected to relatively low Cra.~sostrea gigas Thunberg. Aquaculturr. 94( I): 1-16. temperatures. Ve/lger I 1(3):153--163 Glude, J. B. 1975. A summary report of Pactfic coa~t oyster mortality Loosanoff. V. L. & H. C. Davis. 1952. Temperature requirements for investigations 1965~1972. Proc. 3rd U.S.-Japan Meeting on Aquacul­ maturation of gonads of northern oysters. Bioi. Bull. 103(1):80-96. ture, 1974:1-28 Mane, U. H. 1978. Survival and behavior of oysters in water of low 34 MOLLUSCA!'i INTRODUCTIO:-IS AND TRANSFERS

;alinitJes at Ratnagiri on the west coast of lnd1a. J_ Molluscan Studres Pollard, D_ A & P. A Hutchings. 1990. A Review of Exotic Marine 44(2):243--249 Organisms lmroduccd to the Australian Region. II. Invertebrates and Mann, R. (Ed.). 1979. Exotic species in mariculture. The MIT Press. Algae. Asian Fisherie:.· Science 3:223-250 Cambridge, MA. 363 p. Quayle, D. B. 1989. Pacific Oyster Culture in British Columbia. Can Mann, R. \981. The role of introduced bivalve mollusc species in mari­ Bull. Fish. Aqua. Sci. 21!! culture. J. World Marir:u/r. Soc. 14:546--559 Rao, K V- l 951. Observations on the probable effects of salinity on the Meyers, J. A., E. M. BuTTeson, B. J. Barber & R. Mann. 1991. Suscep­ spawning, development, and setting of the Indian backwater oyster, tibility of diploid and triploid Pacific oysters. Cras.wurea t:i?as m 0.1treu madra.1·ensis Preston_ Proc_ Indian Acad. Sci. 33:231-256. ea;tern oysters, Crus.wstrea virginica, to Perkinsus murinuJ _ J. Shell­ Rao, K. V. & K. N. Nayor. 1956. Rate of growth in spat and yearlings of fish Res. 10:433---437. the Indian backwater oyster Ostrea madrasen,o;i,o; Preston. Indian J. Men1..el, R. W. 1974. Portuguese and Japane;e oyster; are the same spe­ Fisheries 3(2):231-260. cies. Journal of the Fisheries Research Board of Canada 31(4):453--456. Reeb, C A_ & 1_ c_ Avi:.e 1990. A genetiC di:.continuity in a continu­ Menzel, R. W. (Ed). 1990 Estuarine and Manne Bivalve Mollu;c Cul­ ously distributed species: mitochondrial DNA 1n the American oyster ture. CRC Press, Boca Raton, FL. 361 pp. Genetics 124:397--406 Muranaka, M.S. & J. E. Lannan_ 1984_ Brouk>tock management of Sandi:.on, E. E. 1966. The effect of salinity fluctuations on the life cycle Crassostrea gigas: environmental mfluenccs on broodstock condition­ of Gryphaea ~-:asar ((Adanson) Dautzenberg) in Lagos Harbor, Nige­ ing. Aquaculture 39(1--4):217-22!!. ria. J. Animal Ecol. 35(2):379-3!!9. Myhre, J. L. 1973. Levels of mfechon in :.pat of Craswstrea \'irginica and Sandison, E_ E_ & M. B. Hill. 1966. The distribution of Balanus pailidus mechanisms of resistance to the haplosporidan parasite Minchinia nel­ stutsburi Darwin, Gryphaea gamr ((Adanson) Dautzenberg), Mer· soni. M.S. Thesb. Rutgen. University. New Brunswick. NJ. 102 p. cierella enigmatica Fauvel and Hydroides uncinata (Philippi) in rela­ Nell. J_ A. & 1. E. Holliday. 1988. Effects of salinity on the growth and tmn to sahnity in Lagos Harbor and adjacent creeb. J. Animal Ecol. survival of Sydney ruck oy~ter (Sacco.nrea mmmercialis) and Pacific 35(1):235-250. oyster (Craswstrea giga.1) larvae and spat. Aquaculture 68(1):39---44. Shafee. M S_ & M. R. Sabat1e. 19!!6. Croissance et Mortalite des Newhall, S. & M. R. Carriker_ 1983. Sy:.temat1c relationship of the oy>­ Huitres dans Ia Lagune de Oualid1a (Maroc). Aquaculture 53:201-214 ters Crassostrea rhiwplwrae and C. virginica: a comparative ultr.l­ Sindennann, C. J_ & D_ V_ Lightner. 1988. D1sease diagnosis and control structural study of the values_ American Malaco/ogica/Bull_ 1:35--42. in North American marine aquaculture. El~evier, New York. 431 p. Newell, R.I. E. 1985. Physiological effects of the MSX parasite Haplo· Stephen, D. 1980. The reproductive biology of the Indian oyster Crassos­ sporidium nelsoni (Haskin. Stauber & Mackin) on the American uy-.ter trea madrasensiJ (Preston): I. Gametogenic patterns and salinity Crasso.nrea virginica (Gmelin). J. Shellfish Res. 5:91-95 Aquaculture 21(2):139---146. Newell, R.I. E 1989_ Ecological changes in Chesapeake Bay: Are they Tebble, N 1966. Briti;h Bivalve Seashells. British Museum of Natural the result of overharve<;ting the Amencan Oyster (Crass

Douglas W. Lipton, Eileen F. Lavan, and lvar E. Strand

INTRODUCTION THE MARYLAND EXPERIENCE

The major reason for introduction or tran~fer of molluscan Several useful and insightful histories of the Maryland oyster species is economic gain. As Mann (I 979) state~. the economic indu~try have been offered over the year~ (e.g. Power 1970, Wcn­ incentive increases when an existing fishery becomes depleted or ncr~tcn 1978). The most recent and comprehensive is the Kennedy devastated due to ovcrfishing, degradation of environmental qual­ and Breisch (19~3) work in which the dichotomy of the politics ity, or disease. Also, even if there is no existing native fishery. surrounding the oyster management and the science of oyster prop­ great demand for a product may provide enough economic incen­ agation is explained. The results of the mismanagement can be tive for an introduction. Whether the introduction is intended to seen in the precipitous drop in Maryland oyster production be­ benefit a puhlic or private fishery. the public sector's role is par­ tween the late 1800's and late 1920's (Fig. 1). Landings appar­ amount in the decision to allow or disallow introductions. Econ­ ently stabilized over the next 30 years to 1950. Although there are omist~ have two interrelated roles in the public decision process lc~~ons to be learned from the early period, we focus on the po<>t­ regarding molluscan introduction~. Fir~ I. estimates of the net hen­ war event<> efits (benefits minus costs) to the variou~ group~ affected by the In order to understand the current situation, the period from introduction ~hould be provided. This will involve estimating the 1950 through 1989 i~ divided, from the point of view of landings, net benefits to harvester~. proce~~or~ and consumer~ hut also into an apparently ~tahle period (1950-l9XO) and a declining pe­ might include benefits and cosb external to the~c group~. An riod (19Xl-19X9) example is where introduction of filter feeders provides benefits of The oy~tcr ~e

Paper prc>cntcd at the Annual Meeting of The North American Shellfish 'The oy>tcr >cason is referred to in terms of the year in which it hcgan Association, Williamsburg. VA. April 2-5, IYYU. Revised 12/91. f'inal Thus, the oyster season tasting from September of 19!::0 to March of I Yt; I Version 10192. i> denoted as the t9ll0 oy<;tcr season

35 36 MOLLUSCAN INTRODUCTIONS AND TRANSFERS

•~"~'~lli~onsorM~o~o"""'""'•'•'------~ higher salinity areas of the Bay. However, some sections of Mary­ "' ~ MSX In Vlrolnta land's Tangier Sound, Pocomoke and Fishing Bay were also affected. / '1.--"-y \ Maryland was fortunate, however, as the disease did not move '~~ \._~ {'\ ~''. ~in Mo

Md and Va eaten by season Mtd·AIIanllc islation also required processors to make I 0% of their shucked and V"O'"'" he

2Reasons for the shift relate both to costs of acquiring the shell and the 1960 1970 1960 1988 relative productivity of the two types of shell. Although cost/bushel data Year for fresh shell does not extend back to \960, there are records in 1970 showing that the cost of dredged shell was about $.15/bushe\ whereas the -C~napeake IIIIMaryland 0Gull -Pociflc Dlmporto cost of fresh shell was around $.25/bushel. It has also been shown that a Figure 2- Oyster production and imports by region and selected bushel of dredged shell has potentially greater effect on future oyster years. production than a bushel of fresh shell (Cabraal, 1978). EcONOMICS OF INTRODUCTIONS 37

There was a reason for concern over the price in this period. _ Millions of Maryland Bushels,______3 5 The real price 3 obtained by Maryland watennen was greatest in the 1962 season when both Maryland and Virginia harvests were low. ' h The near doubling of Maryland production in the 1966 season ,,,, ,,., 1: caused real prices to drop by nearly 20% in the short-run and by f ,, ~· about 40% in the longer run. The lowest real price received by '',,l>

Maryland watennen occurred in the 1974 season. ' The importance of the period is in the change in the role of the 1.5 - .. f state in ''managing'' the industry. At the beginning of the period, ,_, the role was primarily to make it difficult for the industry to ' deplete the natural oyster beds. The discovery of an inexpensive ', alternative to provide seed created a different role for the State. '' 0 The choice was made to increase production, rather than build up 1950 1955 1960 1965 1970 1975 1960 1985 natural beds. Rather than being regulators, the State became the Season source of growth. However, the production was constrained by the market-production was not to surpass 2.5 million bushels. Figure 3. Maryland oyster harvest, by season, 1950-1988.

Diseased Waters 1981-1988 The pattern of decline in Maryland oyster landings over the The dominant factor in the Maryland oyster industry after 1980 period differs slightly from the pattern observed in other regions4 was the reappearance of the disease MSX and greater outbreaks of (Fig. 3). Over the entire period (1980-1988), Maryland's decline Denno (Perkinsus marinus). Unlike the previous invasion in the in landings was 82%, while other regions declined only 37%. The 1960's which was limited to Maryland's portion of Tangier Sound, Gulf states' oyster production increased to a record 29 million this invasion affected most of Maryland's major oyster bars from pounds of meats by 1983, but harvests declined continually to 16 1981-1983. There was a brief reprieve in disease-related mortality million pounds in 1988. Only Pacific oyster production was in 1984 and 1985, but a return of MSX in previously infected areas greater in 1988 than it was in 1982, and that increase was only 600 and an expansion into more areas followed in 1986-1988. thousand pounds. The trend in oyster harvests during the period parallels the Imports, which are principally low value canned or smoked course of MSX infection. Harvest declined from over 2.5 million oysters, increased from 27 miltion pounds of meats to a record 52 bushels during the 1980-1981 season to just over a million bushels million pounds in 1987. Imports declined to 27.5 million pounds in the 1983 season. In the next two seasons, the catch increased to in 1990. almost 1.6 million bushels. This brief revival did not last and Interestingly, the source of production for the increased im­ production fell to around 0.4 million bushels in the 1987 and 1988 ports and West Coast production is the species, Crassostrea gigas. seasons. The reason is it has not been exposed to the levels of infestation of The more than doubling of the real ex-vessel price of oysters either MSX or Denno that occur in Maryland, Virginia, Delaware from the 1980 ($8 per bushel) season to the 1987 ($20 per bushel) and New Jersey. Thus, the obvious interest in importing it into season did not offset the effect on watennen income of the decline Maryland,-and Chesapeake Bay waters to test its hardiness against in oyster harvest. As a result, gross revenues fell from over $20 those diseases. million dollars to less than $8 million. The higher prices, however, It is within the context of a devastated East Coast oyster in­ did act to keep the level of effort (as measured in mandays) rela­ dustry that the introduction of C. gigas is being contemplated. In tively constant even though the landings were declining. The num­ Maryland, harvesters have turned to an alternative resource, the ber of individuals commercially harvesting and selling oysters de­ softshell clam (Mya arenaria) for some economic relief. In Vir­ clined by around 40%. The low resource abundance had the effect ginia harvest and culture of the hardshell clam (Mercenaria mer­ of removing most of the part-time fishennen and raising the level cenaria) have helped cushion the impact of a declining oyster of effort of full-time fishennen. industry for some watennen. If C. gigas could be introduced, The sporadic nature of the MSX infection made it difficult to another possible source of income could make the difference be­ develop a comprehensive strategy for the oyster repletion pro­ tween continuing to fish or having to leave fishing altogether. gram. The amount and location of shell and seed plantings de­ pended more on availability of seed and the location of disease EFFECTS OF RECENT MOLLUSCAN INTRODUCTIONS than on any other factor. Initially during the period, seed oyster plantings closely followed the index of spat set in the previous Introductions of many aquatic species have taken place over the year. With the 1983 and 1984 season being particularly poor for centuries. However, many attempts to establish populations have spatfall, seed plantings in 1984 and 1985 were extremely small not been reported. The establishment of a reproducing population even though they included several year classes of submarket oys­ of the species is, presumably, the goal of an introduction. How­ ters. Seed plantings increased steadily from 1985 and peaked in ever, this goal is not always realized. As such, the examples we 1988, assisted by relatively good spat sets during the drought years have are somewhat self-selecting; that is, many of the failures are from 1985 through 1987. In 1989, seed plantings were down 37% not documented in the literature because researchers have little to from 1988 but were still the second highest of the decade.

4 Comparisons are made on a calendar year basis and in meat-weight rather ~Real prices are actual prices adjusted for the general level of inflation. than bushels because the available data are given in these tenns. 38 MOLLUSCAN l:-!TRODUCTIONS AND TRANSFERS report. Thus, our examples of introductions are those that have fishery. The landings have increased dramatically of late, from been mostly successful to date. France is the notable exception, 700 metric tons in 1982 to approximately 1400 metric tons in 1989 the victim of many unfavorable experiences. (Chew 1990). Production figures demonstrate that although a spe­ cies may require little effort to become established, its long-tenn Briti.fh ColumbW success as a fishery requires good management. Another accidental introduction, Ceratostoma inorno.tum (the More than twelve known exotic species have been acddentally Japanese oyster drill) was potentially threatening to the local oys­ introduced in British Columbia (Quayle 1964). The introductions ter stocks. Fortunately, its lack of a pelagic larval stage resulted in of Crassostrea virginica and Crassostrea gigas, however, were negligible initial dispersal. When first observed, regulations were intentional immediately enacted to prevent further spread. However, its pres­ Ostrea /urida (the Olympia oyster) is the sole native oyster of ence has caused closing of some oyster beds (Quayle 1984). An­ British Columbia, and wa~ the basis of the early oyster industry. other introduced oyster drill species, Purpura clavigera, does have Overfishing, and later, competition from introduced species led to a pelagic larval stage. Distribution appeared unavoidable, but a its decline as a major fishery (Ketchen eta!. 1983). Its diminutive prompt, aggressive eradication program removed adults and egg size, slow growth, and high labor cost caused the industry to seek capsules in the initial location area, and no others have been de­ other species for commercial use (Bourne 1979). tected (Quayle 1964). Crassostrea virginica was first introduced to British Colum­ Other organisms accidentally introduced with the Japanese oys- bian waters in significant numbers in 1906, although minor intro­ ter include: ductions had occurred previously. Attempts ceased in 1936 due to Batillaria zona/is-a somewhat common but innocuous gastro­ limited natural spatfa!l and high mortality rates (Quayle 1964). pod. Currently only a small population exists in Boundary Bay. Along Mytilicola orientalis-a parasitic copepod, also reasonably with C. virginica, Urosalpinx cinerea (Eastern oyster drill), and common in areas. Apparently the copepod does not cause harm Nassarius obsoletus (Eastern mud snail) were accidentally intro­ to oysters, although it may pose a problem with mussels. duced. U. cinerea has the potential to cause severe damage to Lim no ria tripunctata-the marine wood borer, responsible for commercial shellfish populations. However, its population is ap­ significant damage to wood pilings in Southern British Columbia. parently small and declining due to the limit of a ~uitab!e envi­ Pseudostylochus ostreophagus-a flatworm predator of small ronment. N. obsoletus is well established in some areas, but ap­ oy~ters, has not posed a serious problem in British Columbia, parently has not created any ecological harm. although it is a problem with oyster spat in Japan. Mya areno.ria was planted in Puget Sound from Willapa Har­ Sargassum mutkum-a seaweed which has not posed any prob­ bor, Washington, and water movement patterns distributed the lems except as a nuisance to people using the shores for recre­ species northward along the U.S. and British Columbian coasts ation. (Quayle 1964). To date, the British Columbian and U.S. West Mikrocytos mackini-the Denman disease, an oyster ailment, Coast market for softshell clams has not developed to provide the was discovered after the introduction of the Japanese oyster. incentive for significant commercial exploitation of the established However, there is not conclusive evidence linking it to the Jap­ M. arenaria population. A significant recreational fishery has de­ anese oyster. The industry is said to have "learned to live with veloped. The lack of high fi~hing mortality has probably contrib­ it" (Bourne 1979). uted to the successful establishment of theM. areno.ria population. As previously noted, the introduction of C. gigas into British Crassostrea gigas has been introduced to British Columbia on Columbia is considered successful, even though it was accompa­ numerous occasions. The initial introductions are believed to have nied by accidental imports. C. gigas has prospered where the taken place in 1912 or 1913. The first significant official intro­ native oyster (0. Iurida) failed. The accidentally introduced V. duction occurred in 1926, with oysters from both Japan and the japonica is viewed as an important resource. Although serious state of Washington (Quayle 1969). Reliable seed sources were a biological and economic damage could have resulted from a few of problem at the start of the industry as no local seed was available, the other accidental introductions, quick action and good fortune and the imported seed had low survival (1m and Langmo 1977). It denied them any significance. is too cold in most British Columbian waters for regular breeding, but Pendrall and Hotham Sounds have good breeding conditions, V.S. West Coast and now serve as the main sources of seed oysters. Imported seed has been completely displaced due to the natural set and the supply California, Oregon, and Washington have followed similar of domestic hatchery seed. C. gigas now constitutes the entire routes in mollusc introductions. 0. lurida is the native oyster commercial oyster industry in British Columbia, at a catch of species, currently comprising a small percentage of the commer­ nearly 1800 tons in 1980 (Ketchen eta!. 1983). Although the C. cial oyster catch. C. virginica was introduced in the late 1800's to gigas introduction resulted in numerous accidental imports, as a and Washington. As in British Columbia, its whole, the introduction is viewed as a success. establishment as a commercial fishery failed, but its import was Venerupis japonica (Manila clam) was accidently introduced responsible for the introduction of NasJ·arius obsoletus and Mya with C. gigas (Quayle and Bourne 1972, Bourne 1982, Ketchen et areno.ria (Quayle 1964). Nassarius obsoletus, although abundant, a!. 1983, Chew 1989). It is believed to have been included with is apparently innocuous, as aforementioned. The success of M. oyster introductions on more than one occasion, establishing a areno.ria, as in British Columbia, is limited by the lack of a strong strong population in the southern areas of the Province. Later market. intentional plantings in 1962 and 1969 in Northern British Colum­ Crassostrea gigas was first introduced to the Northwestern bia were unsuccessful. The V. japonica catch fluctuates greatly, states of the U.S. unsuccessfully in 1902 (Chew 1979). The first and in good years comprises a significant portion of the local clam marginally successful introduction to Washington occurred in EcONOMICS OF INTRODUCTIONS 39

1919. With subsequent introductions, commercial cultivation of introduction to open waters. Therefore, all culturing of exotic C. gigas was realized by 1928. As in British Columbia, the C. species is done in landbased pond operations (Fassler, personal gigas industry of the U.S. west coast at first relied upon seed communication). The practice of purely landbased operations is imported from Japan. For some time, the Washington State De­ costly. Consequently, only a smattering of exotic molluscan in­ partment of Fisheries monitored the concentration of oyster larvae troductions have ensued. One (now bankrupt) oyster farm cultured in natural spawning areas (such as Dabob and Willapa Bays) and C. gigas, C. virginica, and 0. edulis, which all did very well from notified culturers, who then collected the pelagic larvae on cultch a biological standpoint. There was a slight problem with the mud for their own leased beds. However, spat was not abundant enough wonn (Polydora sp.), but placing the oyster in warmer water to allow the industry to become independent from Japanese seed. killed the wonn. Although achieving biological success, the high Currently, culturists rely on purchasing larvae from hatcheries to costs of the operation precluded the possibility of economic suc­ sustain the industry and the dependence upon Japan for seed has cess. lessened (Burrel11985; Chew, personal communication). C. gigas A recently opened oyster farm is anticipating its first harvest does best in Washington; prolonged periods of relatively high this year, 1991 (Archibald, personal communication). At present, water temperatures may be the reason for its limited success in only 0. edulis is cultured for harvest. In order to approximate the California (Chew 1979). Regardless of the limitations of the nat­ oyster's natural habitat, salmon and kelp are also maintained in the ural set, C. gigas is the basis for the oyster industry in both states. ponds. Sea urchins and are present to control the envi­ Oregon harvests have never been significant. The 1988 commer­ ronment in the main kelp growing ponds. To minimize the possi­ cial catch for the U.S. west coast totaled 7.97 million pounds, of bility of introducing disease and other organisms, all eyed larvae which 6.6 million pounds originated in Washington. The ex-vessel are purchased from a single Maine hatchery. Each shipment is then value of the harvest in 1988 was $14.5 million. Although such a kept in separate growing tanks. The company is optimistic about harvest may appear impressive, they represent a decline from the the economic success of the harvest; for there is promise of great record 1946 harvest of 13.4 million pounds of meats. Expansion of demand for the product. It is now left to the market to detennine the industry has probably been limited by the size of the market, if the introduction and culture of 0. edulis in Hawaii under such competition from low cost imported oysters, and until recently, the costly conditions is economically feasible. availability of East and Gulf Coast oysters. Other recognized accidental introductions with C. gigas to Maine these states are O.japonicu, V. japonica, and P. nstrenphagus. C. The native oyster of Maine is C. virginica. The present stock is inorrw.tum, as in British Columbia, has limited distribution due to sparse, with successful spawnings in only the warmest of years its lack of a pelagic larval stage. With regulations, further distri­ (Lewis, personal communication). As a result, Atlantic oyster pro­ bution has been avoided. duction is erratic, yet it remains a significant component of the Venerupis japonica grows well in these areas, particularly in oyster industry. Reported commercial harvests of C. virginica the slightly warmer waters. Harvests fluctuated somewhat in the were 2,510 bushels in 1988, and 3,715 bushels in 1989, worth early years, possibly due to the erratic nature of reproduction in $277 thousand. small populations, but has increased greatly since 1975, and may Ostrea eduli.1· was introduced in Maine in 1949 (Loosanoff be stabilizing. The 1980 harvest was second in pounds landed and 1955). Although oysters from Holland were brought to Connect­ economic value (at $1.1 million) to Panopea generosa ( i.:ut for research purposes, a few bushels were held in reserve at clam). In Washington, approximately 1.5 million pounds were the Boothbay Harbor Maine Laboratory where spawning occurred. landed in 1981, while the commercial harvests in California and Some spat survived and later reproduced, fanning the foundations Oregon are negligible. Ninety-five percent of the commercial of a resident population. Thoughts turned to further introduction of catch is from natural set, but culturists are beginning to use hatch­ the species in order to replace a then-failing softshcll clam indus­ ery seed on leased beds. try. Later introductions were made at various points along the Ostrea edulis was introduced to northern California and Wash­ coast from Boothbay Harbor to Merepoint Bay (Welch 1963). ington beginning in 1951. The oysters originated from the newly Although 0. edulis is fairly well distributed, the populations are developing 0. edulis population of Maine (Loosanoff 1955) not very large, with the industry having just attained commercial is no natural spawning in the west coast waters, and al­ There significance in 1984. The 1988 harvest was 6,346 bushels, and in though a few hatcheries produce 0. edulis seed, interest in cul­ 1989: 14,435 bushels. No accidental introductions accompanying turing the European oyster in these areas is limited-the majority the 0. edulis introduction have been discovered. The oyster is of interest remaining with C. gigas (Hulbrock, Chew, personal harvested from both natural and leased cultivation beds; leased communication). There is no evidence of accidental introductions beds utilizing both naturally produced spat and hatchery seed with the European oyster. There is a protozoan parasite (Borw.mia (Lewis, personal communication). The hope is for 0. eduiis to fill ustrea) discovered in \965, but it may be native to California and a market niche in the domestic market for gourmet oysters, and for Washington waters (Katkansky et al. 1969). It attacks 0. edulis' possible export to Europe. immune system, but apparently does not hann C. gigas or C. virRinica. 0. edulis populations in Washington, having been ex­ France posed to the disease, have been found to harbor the parasite while resisting damage (Elston eta\. 1987). Ostrea edulis is the sole native oyster species of France. The oyster, considered an important component of French culture, has Hawaii always been in high demand. The fishery, however, has a volatile hi~tory. Two distinct diseases caused production to fall in 1920 Hawaiian molluscan shellfish introductions are unique in that and 1950 (Goulletquer undated). In 1968, the protozoan parasite according to state law, non-native organisms are prohibited from Marteilia refringens further reduced stocks. The origin of these 40 MOLLUSCAN JNTRODUCTIONS AND TRANSFERS

diseases and the protozoan is uncertain. M. refringens is limited to disease to a declining industry. The utilization of C. gigas has estuarine areas, between which it was transferred with the move­ helped overcome that failure. C. gigas has eventually gained mar­ ment of oysters. (Goulletquer undated). In 1979 Bonamia ostrea, ket acceptance as an alternative to C. angulata, although both are a protozoan that generates microcell disease, was introduced. The considered inferior to the native 0. edulis. The French have pre­ protozoan was introduced with 0. edulis adults from Washington sumably decided that an inferior oyster is better than no oyster. state, the progeny of infected Californian oyster stocks (Elston et Further research on both of these species and others bring hope to al. 1987, Mann 1983). These oysters were intended to supplement the industry, which apparently has decided that one tragedy should the low French stocks. B. ostrea is considered by many the final not preclude further development. blow to the industry, causing the flat oyster fishery in Brittany to fall from a harvest of 4,000 tons in 1978 to 2,000 tons in 1987. Australia Other oysters were introduced over the years to meet the high The experience of Australia in regards to mollusk introductions French demand and later, to compensate for the falling stocks of depends on the state involved. In Tasmania and South Australia, 0. edulis. Crassostrea angulara (Portuguese oyster) was intro­ C. gigas has been successfully introduced and is forming the basis duced in the 1860's without official regulation. The oysters for a cultured oyster industry. In 1989--1990, 3.5 million dozen thrived, with harvests reaching 85,000 mt in 1960 (Goulletquer oysters worth 13.7 M$Aus were harvested (Ayres 1991). In both and Hera! 1991). However, C. angulara experienced high mortal­ these states there is no extant native oyster to compete with. How­ ities from an iridovirus damaging the labia and gills in 1964 and ever, in New South Wales there is an existing fishery based on the 1965 (Farley 1991), and again from 1970 to 1972 from damage to native (Saccostrea commercialis). An unofficial or the blood by yet another iridovirus (Grizel and Hera! 1991). The accidental introduction of C. gigas occurred in the seed production latter outbreak was estimated to cost the industry $90 million a area of Port Stephens sometime prior to 1985. After several year~ year in revenues (Goulletquer and H6ral 1991). The present C. of trying to eradicate C. gigas, because it interferes with the setting angulata population is negligible. of S. commercia/is, the government finally decided to allow the Unofficial importations of C. gigas began in 1966 because of cultivation and sale of C. gigas from Port Stephens (Ayres 1991). the oystennen's frustrations with the declines in 0. edulis and C. angulata. Officials, alarmed by an increase in C. angulata mor­ New Zealnnd talities, prevented further C. gigas introductions until studies in The native oyster in New Zealand is the rock oyster (Saccos­ Japan cleared C. gigas of any responsibility for the C. angulata trea glomerata) which was the basis of an oyster culture industry. deaths. Official introductions of C. gigas from both Japanese and C. gigas was accidently introduced to New Zealand waters in the British Columbian waters ensued in 1971. C. gigas, as previously 1960's and 1970's (Dinamani 1991). Distribution was aided by the mentioned, is resistant to Bonamia ostrea. The resistance of the traditional movement of S. glomerata seed in which was mixed C. Pacific oyster to the diseases of the Portuguese oyster as well gigas seed. In the course of about a decade, C. gigas went from a allowed the expansion of an otherwise failing oyster industry in density on spat collectors of 1/1000 to 4/5. Harvests in 1985 France (Grizel and Hera! 1991). Presently, C. gigas is the princi­ reached 2000 mt. C. gigas is now the basis of the New Zealand pal species in the French oyster industry, accounting for 92% of cultured oyster industry. the 1990 landings which were a record 150,000 metric tons valued at $210 million (Goulletquer and H6ral 1991). It will not repro­ NET BENEFlTS OF MOLLUSCAN INTRODUCTIONS duce in the northern waters of France, however, reproducing best in the warmer waters of southern France. Estimating Direct Net Benefits Accidental introductions did occur with the importation of C. In some ways, the estimation of net benefits for molluscan gigas, although precautions were taken in the official introduc­ introductions is easier than most cost-benefit analysis. Many net tions. A few of these species are still present, although in low benefits from environmental improvements arise from consumers' numbers. These species include: Balanus amprhitrite and B. al­ use of goods not sold in the marketplace. These non-market goods bicostatus, Aiptasia pulchella, Anomia chinensis (Grizel and pose special difficulties in measurement. For example, improve­ H6ral). The low numbers render the organisms of relatively little ments in water quality may improve recreational fishing opportu­ concern to the French, although the significance of any accidental nities, but because there is not a market with corresponding prices introduction, harmful or not, should not be denied. and quantities of fishing, there are unique problems in measuring Currently, research is underway to seek out other oyster species the change in benefits to sportfishennen (Bockstael, Hanemann with a resistance to B. ostrea. As mentioned, a strain of 0. edulis and Strand 1986). Fortunately, molluscs are market goods for in Washington state was found to carry, but not be highly damaged which we can observe changes in prices and quantities, and thus, by the parasite. Also, breeding the immune C. gigas at the same estimate supply, demand and corresponding welfare changes from time as 0. edulis reduces the severity of the protozoan in 0. introductions. edulis. Other species that have been studied in labs include 0. Although detailed data on the distribution of oysters in the chiliensis from Chile in quarantined system in 1981. Studies were marketplace are not available, it is common knowledge that the abandoned due to lack of success (Mann 1983). 0. puelchana, of flow of West Coast C. gigas to the East Coast has increased since Argentina, however, appeared insusceptible to the parasite in the collapse of the Chesapeake oyster fishery. It is not known to hatchery lab studies and was subsequently planted in northern what extent consumers are aware or care about what oyster species Patagonia waters in 1988, the success of which is still to be de­ they are consuming. In cases where a species is introduced to termined (Goulletquer undated). replace a depleted local species, and the two species are consid­ The French oyster industry has experienced what may be the ered by the consumer to be close substitutes, demand studies based most severe problem encountered thus far with the introduction of on a time series of prices and quantities of the depleted species species, when 0. edulis of America's West Coast brought new may serve to estimate demand for the introduced species. Thus, in EcONOMICS OF INTRODUCTIONS 41

France where there was an industry based on C. angulata, it is not organism that outcompetes native resources and causes a popula­ surprising to expect similar demand for C. gigas. Of course, the tion decline of the native resource such as occurred in New reliability of forecasts from historical data are diminished the fur­ Zealand. The introduction may also inadvertently introduce other ther out in time those forecasts must be made. Traditional con­ undesirable species, disease organisms or parasites that can disrupt sumer welfare measures (i.e., consumer surplus) can be made the ecosystem. The end result may simply be a nuisance or con­ once the demand for the introduced oyster is detennined. sidered a disaster. The results may be either reversible or irrevers­ The measurement of producer benefits, as in the case of con­ ible. sumers, must be measured net of costs. Total value of the harvest, probably the most often cited figure of success of an introduction, Uncertainty and the Use of Benefit-Cost Analysis is not a measure of producer welfare unless culturing and harvest­ ing are costless activities. Cost estimates can be made from current The fundamental issue surrounding introduction of molluscan data on culturing, harvesting and processing costs to the extent species is the uncertainty of the effects. Even though the history of these are available. Bosch and Shabman (1989) have developed molluscan introductions, reviewed above, shows few disastrous such cost estimates for Virginia oyster growers, and these could be external effects, the evidence is clear that molluscan introduction appropriately modified for the different species. In cases where have resulted in inadvertent species being introduced with the data is not available, an economic-engineering approach can prove mollusks. Some might say that it was a stroke of luck that no useful (Park and Jackson 1984). The opportunity cost of the pro­ disasters occurred. A finite probability exists that an ecological ducer's labor (i.e., what he could earn in the next best employment and economic disaster can occur with an introduction of C. gigas opportunity) should be included in the cost estimate. In areas into the Chesapeake Bay. How does one consider uncertainty where there are few alternative opportunities, the opportunity cost within the benefit cost framework? of labor tends to be low and results in higher producer benefits. There are two primary ways it has been considered- through the Thus, in France, where there was a large oyster industry with few use of expected net benefits and through a game-theoretic ap­ alternative opportunities, the benefits of the introduction of C. proach. When using expected net benefits, the distributions about gigas are higher than in an area where there are several alternative the costs and benefits are used and the expected value of net fishing and culturing alternatives. benefits is calculated. In concept, this is a straightforward pro­ If the introduction is for purposes of restoring a public fishery, cedure but the distributions about net benefits are not easy to the net benefit to producers will depend on how the resource is detennine, especially the ones concerning future events. Often, managed. If an open access management regime is maintained, higher discount is given to more risky choices. then net benefits to producers will be less than if a bottom leasing The uncertainty involved in the decision on whether to allow an program or limited entry program on public grounds are producers introduction can also be approached through game theory. Bishop will be Jess than if a bottom leasing program or limited entry (1978) applied this approach when examining extinction of a po­ program on public grounds are instituted. This is the well-known tentially valuable species due to building a dam. The game is result of rent dissipation in common property fisheries (c.f., Gor­ depicted as follows: don 1954, Copes 1972). Simply replacing one species with an­ States other does not necessarily eliminate the man-induced factors that caused the decline of the native species. One must still deal with No Maximum the problem of overlishing, potential disease, and a decline in ActiOn Disaster Disaster Losses water quality. Introduction 0 b No introduction Mew;urillg "Exurnol" Costs of Mollusk Introductions ' Man has two choices, to allow or not allow an introduction. If he Although the direct net benefits of mollusk introductions may docs not allow the introduction, the net benefits foregone are de­ be many years off, the costs of these potential introductions are noted as a. If the introduction is allowed and causes a disaster in being incurred today mainly in the form of research dollars. Costs existing populations this is denoted by b. The last column indicates of general research on mollusk introductions that is applicable to a the maximum losses under the introduction and no introduction variety of species and variety of areas cannot fairly be assigned scenario. totally to the cost of introduction of one species in one area. One strategy in playing this game is to adopt the minimax However, as a specific introduction is contemplated, more of the principle----<:hose the strategy that minimizes maximum possible research dollars are focused on determining the impact and like­ losses (Ciriacy-Wantrup 1968). Thus, if we feel the damages from lihood of success for that given area. a potential disaster exceed the benefits from an introduction with The actual cost of performing the introduction or transfer, and no disaster, then under the minimax principle the decision would monitoring and maintenance may be substantial. However, once it be not to allow the introduction. is determined what functions have to be performed, predicting the Clearly, before any strategy is chosen, measures of the conse­ costs would not be an overwhelming task. For example, the mag­ quences of introductions and damages must be made. As discussed nitude of costs will be much greater when introducing a non­ earlier, measuring a, the foregone benefits of not allowing the reproducing organism into an area for yearly harvest, as compared introduction has difficulties, but they are not insurmountable. Two to an introduction of an organism that can successfully reproduce. issues will accompany this estimate; how should the stream of net The most contentious issue regarding mollusk introductions benefits be discounted over time; and what are the characteristics and their costs is the potential that an introduction may be accom­ of the uncertainty of these measurements. panied by deleterious effects to other resources in an area. These It is entirely possible that the introduction of C. gigas into can include the case of an otherwise successful introduction of an Chesapeake Bay will have negative net benefits. Given the nega- 42 MOLLUSCA~ INTRODUCTIONS M'D TRANSFERS tive publicity surrounding the health and safety aspects of eating decisions. lt, however, can aid, as Finkel ( 1990) states in "nar­ molluscan shellfish, it is possible the demand for the product is rowing the riff between good decision processes and good out­ highly inelastic so that a slight increase in the available quantity comes''. That is, one can ignore economic and risk analysis in the will be accompanied by a large decline in price. It may also be that decision to make a species introduction, and by chance have a the Chesapeake Bay has a comparative disadvantage relative to positive outcome anyway. This, however, does not validate the other areas for producing gigas. This may be due to natural envi­ decision process. Our summary of the infonnation on molluscan ronmental differences as well as production costs in this region. introductions to date seem to fall into the category of poor decision Measuring b, the potential damages is much more problematic. processes and good outcomes. Most of the introductions were Although it is probably not possible to predict all the potential done unofficially or unintentionally. Fortunately, the diseases and consequences of introductions into an area, it may be possible to organisms that were introduced, for the most part have had min­ narrow the field of potential damages, and provide an estimate of imal effects on the local ecology. The rna jor exceptions are the maximum loss from this subset of damages. For example, at pre­ introduction of oyster diseases in France, and the demise of the sent in Maryland it would only take the destruction of three spe­ native rock oyster in New Zealand. cies, the blue crab, native oyster and soft clam, to virtually elim­ For the Chesapeake Bay, the magnitude of the potential ben­ inate the Maryland bay fishery. These two species with an ex­ efits from an introduction of C. gigas will depend on the avail­ vessel value of $31.2 million in 1988 make up approximately 60% ability of alternative native species that will allow watennen and of Maryland's Chesapeake Bay landings. The net los~ to harvest­ processors to continue to operate in their professions. For exam­ ers from a $31.2 million a year fishery would be significantly less ple, increases in striped bass populations, hard and soft clams, and because of the costs of harvesting. If this loss was irreversible or other species would reduce the need for a renewed oyster fishery. occurred over a long period, discounting would again be an im­ Benefits will also depend greatly on the consumer perception of C. portant issue. The timing of when the disaster occurred would also gigas as an alternative for C. virginicu. If they are not considered be important, particularly when it is coupled with discounting. substitutes, Chesapeake Bay production of C. gigas along with In the case of uncertainty surrounding the benefit estimates, we west coast production and import~ will result in a substantially probably have some intuition about what the probability distribu­ lower price, requiring fewer watennen, culturists and processors tion of net benefits looks like. In the case of the disaster our to handle larger quantities of product at low profit margins, in intuition about probabilities is severely diminished. If the proba­ order to maintain profit levels. The potential cost from an intro­ bility distributions are known, it is possible to play the game with duction of C. gigas will depend on what i~ at risk. In terms of other standards. For example, one could compare the expected native oyster populations, there currently appears to be much less value of the introduction and no introduction scenarios, and at risk in Virginia as compared to Maryland, because of the dis­ choose the action with the greater expected value. Clearly, this is tribution of the oyster diseases MSX and Dcrmo. The economic a much less conservative approach than the minimax principle. magnitude of an ecological disaster resulting from the introduction Policymakers may want to look at other moments of the probabil­ would rise if other commercially important species were involved, ity distributions such as the variance to help in the decision pro­ such as blue crabs. Another possibility which would raise the cess. impacts would be the introduction of a nuisance organism, such as Finkel ( 1990) offers an excellent guide on how to represent the a fouling organism like the zebra mussel. The good decision pro­ uncertainty present in an analysis, and how policymakers (risk cess requires the resource manager to weigh the~e factors in the managers) should use that infonnation in making a decision. It will decision of whether to allow an introduction. be necessary to assume some probability distribution for damages from an introduction. Monte carlo techniques are particularly use­ ACKNOWLEDGMENTS ful in analyzing these types of problems when a number of dif­ ferent probability distributions must be combined. We wish to thank Dr. Aaron Rosenfield for urging us to write CONCLUSIONS this paper and for his and Fred Kerns constructive comments in its preparation. Funding wa~ provided by the Maryland Cooperative Economics offers no perfect prescription for making decisions Extension Service and the Maryland Agricultural Experiment Sta­ about molluscan introductions and similar types of environmental tion. MAES contribution #8579 and scientific article #A6393.

LITERATURE CITED Archibald, Richard. Personal Communication. Bourne, N. 1979. Pacific Oysters, Crassostrea gigas (Thunberg), in Brit­ Ayres, P. 1991. Introduced Pacific Oysters in Australia. Prepared for the ish Columbia and the South Pacific Islands. Mann, R., ed. Exmic Oyster Ecology Workshop, Maryland Sea Grant Coliege, University of Species in Mariculture: 1-53. Maryland, College Park: 2-7. Bourne, N. 1982. Distribution, Reproduction, and Growth of Manila Clam, Tapes philippinarum (Adams and Reeves), in British Columbia. Bishop, R. C. 1978. Endangered species and uncertainty: The economics Journal of Shellfish Research 2(1):47-54. of a safe minimum standard. Amer. J. Agric. Econ. 60(1):10-19. Burrell, Y. G., Jr. 1985. "Oyster Culture··. Huner, J. V. and E. E. Bockstael, N. E., W. M. Hanemann, and I. E. Strand. 1986. Mea.~Uring Brown, editors. In: Crustacean and Mollusk Aquaculture in the United the Benefits of Water Quality Improvements Using Recreation Demand States. pp. 235-274. Models. Report on EPA contract No. CR-811043-01-0. 256 pp. Cabraal, R. A. 1978. "Systems Analysis of !he Maryland Oyster Fish­ Bosch, D. 1., and L.A. Shabman. 1989. The decline of private sector ery: Production, Management, and Economics.'' Ph.D. Dissertation. oyster culture in Virginia: Causes and remedial policies. Mar. Res. Depanment of Agricultural Engineering, University of Maryland. Economics 6:227-243. 309 pp. EcONOMICS OF INTRODUCTIONS 43

Chew, K. K. 1979. The Pacific Oyster (Crassostrea gigas) in the West tions on Survival and Growth of the European Rat Oyster, Osrrea Coast of the United States. Mann, R., ed. Exotic SpeL"ies in Maricul­ edulis, in California. Calif. Fi.~h. and Game. 55(1):69-74. ture 54--82. Ketchen, K. S., N. Bourne, and T. H. Butler. 1983. History and present Chew, K. K. 1989. "Manila Clam Biology and Fishery Development in status of fisheries for marine fishes and invertebrates in the Strait of Western North America." Manzi, J. J. and M. Castagna, editors. De­ Georgia, British Columbia. Can. J. Fish. Aql«lt. Sci. 40:1095-1119. veloplrU.'nU in Aquaculture and Fisheries Science. 19:243--292. Kennedy, V. S. and L. L. Breisch. 1981. "Maryland's Oysters: Research Chew, K. K. Personal Communication. and Management.'' Maryland Sea Grant, University of Maryland, Col­ Ciriacy-Wantrop, S. V. 1968. Resource Conservation: Economics and lege Park, Maryland. 286 pp. Policies. 3rd ed. Berkeley and Los Angeles: University of California Kennedy, V. S. and L. L. Breisch. 1983. "Sixteen Decades of Political Div. Agri. Sci., 395 pp. Management of the Oyster Fishery in Maryland's Chesapeake Bay." Clime, Richard. Personal Communication. Jourrtal of Environment Martagement 16:153--171. Copes, P. 1972. Factor rents, sole ownership and the optimum level of Lewis, Robert. Personal Communication. fisheries exploitation. Manchester School of Economics and Social Loosanoff, V. L. 1955. The European Oyster in American Waters. Sci­ ence. 121:119-121. Studie.~ 41:145-163. Dinamani, P. 1991. Introduced Pacific Oysters in New Zealand. Prepared Mann, R. 1979. Exotic Species in Aquaculture: An Overview of When for the Oyster Ecology Workshop, Maryland Sea Grant College, Uni­ Why and How. In: Exmic Species in Mariculture (Mann, R., ed.). pp. versity of Maryland, College Park: 8-11. 331-354. Mann, R. 1983. The Role of Introduced Bivalve Mollusc Species in Elston, R. A., M. L. Kent and M. T. Wilkinson. 1987. Resistance of Mariculture. J. World Maricu/. Soc. 14:546--559. Ostrea edulis to Bortamia ostrea Infection. Aqunculture 64:237-242. Maryland Department of Natural Resource (DNR). 1987. Maryland's Oys­ Farley, C. A. 1991. Mass Mortalities and Infectious Lethal Diseases in ter resource: Status and Trends. Bivalve Mollusks and Associations with Geographic Transfers of Pop­ Newell, R. l. E. "Ecological Changes in Chesapeake Bay: Are They the ulations. In: Dispersal of Liviilg Organisms into Aquntic Ecosystems Result of Overharvesting the American Oyster, Crassostrea virginica? (Rosenfield, A. and R. Mann, editors). University of Maryland Press In Understanding the Estuary: Advances in Chesapeake Bay Research. pp. 1-15. Proceedings of a Conference. 29-31. Chesapeake Research Consor­ Fassler, Richard. Personal Communication. tium Publication 129. March 1988. Finkel, A.M. 1990. Confronting Uncertainty in Risk Martagement. Re­ Park, W. R. and D. E. Jackson. 1984. Cost Engineering Analysis. John sources for the Future, 68 pp. Wiley & Sons, New York, 335 pp. Gordon, H. S. 1954. The economic theory of a common-property re­ Power, G. H. 1970. "Everything You Ever Wanted to Know About Oys­ source: The fishery. J. Polit. Econ. pp. 124--142. ter and More." Maryland Law Review, 50:44-76. Goulletquer, P. Oyster Production and Management in France, Summary Quayle, D. B. 1964. Distribution of Introduced Marine Mollusca in Brit­ Undated mimeo. ish Columbia Waters. J. Fish. Res. Bd. Canada. 21(5):1155-1181. Goulletquer, P. and M. Hera!. 1991. Aquaculture of Crassostrea gigas in Quayle, D. B. 1969. Pacific Oyster Culture in British Columbia. Bull. France. Prepared for the Oyster Ecology Workshop, Maryland Sea Fish. Res. 8()(Jrd Can. 169. 193 pp. Grant College, University of Maryland, College Park: 8-11. Quayle, D. B. and N. Bourne. 1972. The Clam Fisheries of British Co­ Grizel, H. and Hera!, M. 1991. Introduction into France of the Japanese lumbia. Fish. Res. Board Can. Bull. 179. Oyster (Cra.~sosrrea gigas). J. Com·. int. Explor. Mer. 47:399-403. Welch, W. R. 1963. The European Oyster, Ostrea edulis, in Maine. Pro­ Hulbrock, R. Personal Communication. ceed. Nat. Shellfish. Assoc. 54:7-23. lm, K. H. and D. Langmo. 1977. Economic Analysis of Producing Pacific Wennersten, J. R. 1978. "The Almighty Oyster: A Saga of Old Somerset Oyster Seed in Hatcheries. Proceed. Nat. Shellfish. A.uoc. 67:17-28. and the Eastern Shore, 1850--1920." Maryland Historical Magazine, Katkansky, S.C., W. A. Dahl~trom and R. W. Warner. 1969. Observa- 74(1):80--94.

Public Health Aspects of Transferring Mollusks

Cameron Ray Hackney, Marylin B. Kilgen and Howard Kator

ABSTRACT This paper diSCUsses microorganisms associated with molluscan shellfish borne illness, their growth after harvesting, transportation and storage, and their response to depuration and relaying. Organisms of public health concern are categorized as to whether they originated in the natural environment or are present as the result of pollution. The organisms of concern and their significance were determined by examining the Nonh East Technical Services Unit of the Food and Drug Administration and Centers for Disease Control data bases over a 15-17 year period. Enteric viruses accounted for most of the illness, followed by naturally occurring marine vibrios. Other microorganisms accounted relative few incidences of illne;s. Vibrio~ and certain indicator bacteria will increase in number during storage and transportation. Furthermore, vibrios are resistant to depuration. Relaying wiU cause reduction in enteric bacteria and viruses but not marine vibrios.

KEY WORDS: pathogens, shellfish, public health

INTRODUCTION mollusks, whereas CDC defines shellfish to include bi-valves, uni-valves and crustacea. This paper will discuss microorganisms associated with mol­ The information in tables I and 2 is useful for estimating the luscan shellfish borne illness and their growth after harvesting and risk from microbial contaminants. Most of the illnesses associated during transportation and storage. Also, their response to depura­ with molluscan shellfish have been associated with either enteric tion and relaying will be discussed. Organisms of public health viruses or naturally occurring marine organisms of the family concern can be divided by their source. They may originate in the Vibrionaceae. Other microorganisms account for far fewer ill­ natural environment or be present as the result of pollution. The nesses. The first section will deal with agents associated with organisms of concern and their significance can be estimated by pollution followed by a section on pathogens associated with the examining the data bases of the North East Technical Services environment. Unit of the U.S. Food and Drug Administration (NETSU) and the The effect of depuration (controlled purification) and relaying Centers for Disease Control (CDC) over a 15-17 year period (Ta­ on various microorganisms will be discussed. Controlled purifica­ bles 1 and 2). These data bases do not agree because of their tion and relaying is a process whereby shellfish are allowed to nature. The CDC data base is a summary of foodbome outbreaks purge themselves of contaminants, either in a natural setting or in reported by the states. It is possible that an outbreak will be pub­ land based facilities (Richards 1988). Controlled purification is lished in the CDC publication Mortality and Morbidity Weekly usually a land based process, where the shellfish are put into tanks and yet, not appear in the data base because the outbreaks fonn with purification systems for the water. Relaying is the process of was not submitted by the state. On the other hand, the NETSU transferring the mollusks from polluted water to areas approved for data base is a summary of outbreaks and cases reported in the shellfish harvesting. The process of controlled purification is literature and includes personal communications. Thus, it is more based on reduction of indicator (fecal coliforrns) counts, whereas complete but at the same time less precise. The NETSU data relaying depends upon a specified time. The time for controlled includes individual cases that were not reported as outbreaks. The purification is usually far shorter than that of relaying, 2-3 days CDC defines an outbreak as two or more persons becoming ill versus 14 days. It is important to have an understanding of the after consuming a common food at the same time. lllness that only relationship between indicator microorganisms and the various affects specific individuals will not be reported in the CDC data types of pathogens in these systems. For eXample, the time re­ base. For example, the NETSU data base lists several cases of quired for depuration of indicator bacteria and enteric bacterial Vibrio vulnificus, but because this bacterium only affects individ­ pathogens is similar. However, rates vary greatly between indica­ uals in high risk categories, no outbreaks (two or more individuals tor bacteria and some enteric viruses. In addition, the depuration having a similar illness after consuming the same food), have been of naturally occurring vibrios is quite different than that of indi­ reported. Thus, illnesses from this organism do not appear in the c::ator bacteria (Richards 1988). With respect to relaying, the num­ CDC data base. Finally, the defmition of shellfish used by the data bers of naturally occurring bacteria such as vibrios are increased or bases is different. The NETSU data base includes only bi-valve at least stay the same. This is because Vibrios are indigenous to the

45 46 MOLLUSCAN INTRODUCTIONS Al'.TI TRANSFERS

TABLE I. reported outbreaks of viral illness associated with have lllness Associated with Naturally Occurring Pathogens in Shellfish: involved fecally contaminated bi-valve shellfish; however, viruses 1 2 Summary of CDC and NETSU Data, 1973-1987. • have the potential to contaminate seafood during processing. This has happened with other food products. More than 100 enteric viruses can be found in human feces. Reported By Picomaviruses make up the largest of all virus families with nearly CDC3 NETSU3 200 host-specific picomaviruses having been identified in man. Of these, 69 enteroviruses inhabit the enteric tract (White and Fenner Cases Outbreaks c~ 1986, Gerba 1988). These viruses have a naked icosahedral capsid No.% No.% No.% 25~30 nm in diameter, appear as smooth and round in outline, are Pathogens constructed from 60 protomers, and replicate in the cytoplasm. Aeromonas 0 0 7 (0.1) Each protomer is comprised of a single molecule of four polypep­ Bacillus cereus 6 (0.7) 2 (4.3) tides, VP 1, 2, 3 and 4, or ID, IB, IC and lA respectively. The Plesiomonns 0 0 18 (0.3) genome is a single stranded RNA linear molecule of positive po­ 6 Vibrio cholerae 01 16 (1.8) 3 (6.4) 7 (0.1) larity with a M.W. of 2.5 X 10 • The molecule is polyadenylated V. cholerae non-01 II (1.2) 2 (4.3) 125 (2.3) at its 3' end with the protein VPg covalently linked to its 5' end. V. fluvialis 0 0 3 (0.1) Enteroviruses have been subdivided into the species group Po­ V. hollisae 0 0 5 (0.1) lioviruses (PY), Coxsackie viruses, Echoviruses and Enterovi­ v. mimicus 0 0 6 (0.1) ruses. While polioviruses are frequently isolated from bi-valve V. parahaemolyticus 298 (32.9) 18 (38.3) 98 (1.8) shellfish, they are mostly vaccine strains and are not a cause of V. vulnificus 0 0 104 (1.9) Total 331 25 373 concern with respect to public health. Hepatitis type A (HAY) is the picornavirus of most concern in shellfish. 1 No illnesses associated with parasites or C. botulinum, were reported in Enteric viruses are obligate parasites and of course do not mul­ these data ba;;es. 2 tiply in shellfish. They do however, survive quite well. For ex­ The number in parentheses is the % of total illness of Table~ I and 2 ample, in oysters polioviruses survive more than 30 days in combined. shucked product stored under refrigeration. ~ The term shellfish in the COC data base includes all molluscan and crustacean shellfish. In the NETSU data base only bivalve shellfish are Hepatitis Type A (HAV) (Enterovirus Type 72) considered. The onset of HAY is associated with the clinical symptoms of marine environment and their numbers are not affected by pollu­ fever, malaise, anorexia, nau~ca and lethargy. Symptoms also tion. Of course waters used for relaying arc classified by pollution, include dark urine, jaundice and an enlarged, tender, palpable not by absence of naturally occurring pathogens. liver. In children, most infections are anicteric; however, these-

AGENTS ASSOCIATED WITH POLLUTION TABLE 2. Agents associated with pollution include certain enteric viruses lllness Associated with Contamination of Shellfish by Fecal 1 2 3 and bacteria. As mentioned earlier, enteric viruses are agents most Pollution: Summary of CDC and NETSU Data, 1973-1987. • • often associated with shellfish borne illness. Of the enteric bacteria only salmonellae, Campylobacter jejuni and Shigella have been Reported By associated with illness from molluscan shellfish in the United States. Pathogenic Escherichia coli has been implicated with shell­ CDC3 NETSU3 fish borne illness in other countries, such as Japan. Many other c ..., Outbreaks c~ pathogens have been isolated from molluscan shellfish but have not been implicated in illnesses associated with mollusks. These No.% No.% No.% include Yersinia enterocolitica and Listeria monocytogenes. In Salmonellae (non-typhi) 80 (8.8) 3 (6.4) this discussion, only organisms that have caused documented ill­ Salmonella ryphi ness are discussed. Hepatitis A 335 (36.9) 9 (19.2) 356 (6.6) Hepatitis (unspecified) 4479 (82.9) Human Enteric Viruses Norwalk and similar viruses 42 (4.6) 2 (4.3) 82 (1.5) Human enteric viruses are of concern in seafood products, Shigella 77 (8.5) 4 (8.5) 93 (1.7) especially in raw molluscan shellfish that may have been harvested Staphyiocvccus aureus 14 (1.5) 2 (4.3) 5 (0.1) from fecally polluted waters. Viruses are inert in food systems and Campylobacter 16 (0.3) are only active inside the host; therefore, they will not multiply Clostridium perfringens 28 (3.1) 2 (4.3) during storage after harvesting. Only a few viruses can be trans­ Total 907 (100) 47 (100) 5404 (100)

mitted through food. These are usually transmitted by the fecal 1 oral route which includes contamination from human sewage. En­ No illnesses associated with parasites, C. botulinum, enterococci, or S. typhi were reported in the~e data bases. teric virus infections are limited mostly to the intestine. However, 2. The number in parentheses is the % of total illness of Tables l and 2 when the infection goes past the intestine, a more serious illness combined. such as hepatitis may result. When a person becomes infected they J The term shellfi;h in the CDC data base includes all molluscan and shed viruses in their feces which may in tum contaminate seafood crustacean shellfish In the NETSU data ba~e only bivalve molluscan shell­ through pollution or poor personal hygiene habits. Most of the fish are considered. PUBLIC HEALTH ASPECTS OF TRANSFERRING MOLLUSKS 47 verity of the disease increases with age (Overby ct a!. 1983, Bryan NANBH). Other names include fecal-oral non-A non-B hepatitis. 1986, White and Fenner 1986, Cliver 1988). and A-like non-A non-B hepatitis. It should not be confused with When HAV is ingested it multiplies primarily in the intestinal hepatitis C, also called parenterally transmitted non-A non-B hep­ epithelium. Secondary infection of the parenchymal cells of the atitis (PT-NANBH), orB-like non-Anon-B hepatitis, which is a liver is through the blood stream. The virus is found in the feces common cause of hepatitis in the U.S. (Gouvea 1991). approximately one week prior to the clinical signs. It may also be HEY has a particle diameter of 32-34 nm, a buoyant density of found in the blood approximately one week prior to the appearance 1.29 g/ml in KTar/Gly gradient, and is very labile. Serologically of the main clinical sign of dark urine. It disappears after serum related smaller (27-30 nm) particles are often found in feces of transaminase levels reach their peak. The onset time for symptoms patient~ with Hepatitis E and are presumed to represent degraded is normally four weeks, but may range from 2--6 weeks. Infection viral particles. HEY has a single stranded polyadenylated RNA with HA V results in permanent immunity. genome of approximately 8 kb (Gouvea 1991). Enteral HEY can HAV is spread by the fecal-oral route. It is hyperendemic in be more severe than HAV with a high incidence of cholestasis. countries which are overcrowded, have inadequate sanitation and The incubation period for hepatitis E varies from 2 to 9 weeks. poor hygiene. Most infections in these communities occur in child­ Disease usually is mild and resolved in 2 weeks leaving no se­ hood and are subclinical. In more developed countries the disease quelae. The fatality rate is 0.1-1% except in pregnant women. is seen most often between the ages of 15 and 30. This group is reported to have a fatality rate approaching 20%. The Contaminated food and water and person to person contact are highest attack rate is in young adults, especially pregnant women the main routes of transmission of HAY. Each year 20,000 to in the third trimester (Gouvea 1991). The incidence of chronic 30,000 cases are reported to the Centers for Disease Control active hepatitis is extremely low in HEY (Overby et a!. 1983, (CDC). Of these cases, approximately 140 are due to foods (0.5% White and Fenner 1986). of the total). Most of these food-borne outbreaks are due to mis­ Enteral HEY i~ transmitted mainly by sewage contaminated handling of foods by infected individuals (Cliver 1988). Outbreaks water in epidemics. It is also transmitted sporadically by person to can also occur due to inadequate cooking of contaminated foods person contact. In the middle East and Africa, it appears to be and by human sewage contamination of drinking water supplies, endemic (Overby ct a!. 1983). Cliver (1988) noted water­ swimming waters and shellfish growing waters. associated outbreaks have been reported for years from India, In the 1950's the first documented case of shellfish-associated Africa, the USSR, and most recently, Mexico. Cases have been HAY occurred in Sweden. The first case was documented in the associated with consuming raw shellfish (Rippey 1990). No re­ U.S. in the 1960's (Richards 1985, Cliver 1988, Gerba 1988). search has been conducted on the fate of HEV in shellfish during Richards ( 1985) reported approximately 1400 cases of molluscan depuration or relaying. This work is needed as the potential for shellfish-associated HA V since 1961. The Centers for Disease spread in the U.S. is great. Control reported 335 cases of shellfish-related HA V from 1973 to 1987. The North East Technical Services Unit of the U.S. Food Unclassijud Viruses and Drug Administration reported approximately 438 cases of shellfish-associated HAY from 1973 to 1990 (CDC 1973-1986, These include the non-specific agents of gastroenteritis includ­ Rippey 1991). ing Norwalk and Norwalk-like agents, Snow Mountain agent, and Prevention and control of HA V can be accomplished at several Small Round Viruses (SRV's). The Norwalk group is 25-32 nm in levels. Municipal sewage systems should be properly functioning diameter, while the SRV's are 27-40 nm. The SRV's have been to prevent contamination of public water supplies and shellfish identified in the feces of infants with diarrhea using Immune Elec­ producing waters. Also, proper classification of shellfish growing tron Microscopy (IEM). The incubation period for the Norwalk areas and restricting shellfish harvest only to approved areas is agent is from 24 to 72 hours. Infection results in the sloughing of important in preventing HA V contamination from untreated hu­ intestinal villi followed by rapid regeneration. Clinical symptoms man sewage. include diarrhea, nausea, vomiting, abdominal cramps, and in Considerable research has been conducted on the fate of enteric some cases, headache, myalgia and low grade fever. Symptoms viruses, including HAY, during depuration and relaying. This re­ are more serious in adults. Immunity following an infection with search was hampered until recently because cell cultures were not Norwalk virus is only temporary, lasting approximately one year. available to propagate HAY virus. HAY viruses seems to be re­ This may be one of the reasons for the very high attack rate in at sistant to depuration in comparison to indicator bacteria and many risk individuals of 50-90% (Cliver 1988). other enteric viruses (Richards 1991). Sobsey (cited by Richards Outbreaks of viral gastroenteritis due to the Norwalk agent has 1991) examined the depuration of poliovirus,£. coli, enterococci, been associated with swimming in waters contaminated with hu­ the bacteriophage MS-2 and HAV. The organisms were taken up man sewage, fecal contamination of food or drinking water and naturally by feeding in contaminated water in laboratory tanks. consumption of uncooked or partially cooked shellfish harvested Each organism depurated at a different rate, with poliovirus being from estuaries contaminated with human sewage. The first docu­ depurated the quickest, followed by E. coli, enterococci, the bac­ mented shellfish-associated outbreak of gastroenteritis involving teriophage MS-2 and HAV. HAV remained in the oyster for more Norwalk virus was in 1979 in Australia, where more than 2000 than five days after being exposed to dean water at various tem­ people were involved. Since this time, there have been many peratures and salinities. This implies that commercial depuration documented outbreaks in the U.S. Norwalk virus illness associated would not eliminate HAY from shellfish. with shellfish is a continuing problem and has increased with the last decade while HA V infections have decreased. Between 1973 Non-A, Non-B Enteral Hepalili$; Hepalili$ E and 1990, the USFDA NETSU reported 176 shellfish-related out­ The disease caused by Hepatitis E Virus (HEY) is called hep­ breaks of Norwalk gastroenteritis, 71 outbreaks of Snow Mountain atitis E, or enterically-transmitted non-A non-B hepatitis (ET- agent, and 5924 cases of gastroenteritis of unknown etiology, 48 MOLLUSCAN INTRODUCOONS AND TRANSFERS many of which may have been caused by Norwalk like viruses tracks disease incidence by several mechanisms, including labo­ (Rippey 1991). The Centers for Disease Control reported 3524 ratory-based Salmonella Surveillance system and the Morbidity shellfish-related cases of unknown etiology from 1973 to 1987 and and Mortality Weekly Report (MMWR). These systems do not 42 cases from Norwalk virus (COC 1973--1987). Richards (1985) agree and data in one system often is not included in the other reported over 6,000 cases of shellfish-associated gastroenteritis systems. When examining the annual foodbome disease incidence over the past 50 years. It is presumed that many of these are of data for the 14 year period from 1973 to 1986, an average of 55 viral etiology, possibly Norwalk or Norwalk-related agents. Over foodbome outbreaks of non-typhoidal Salmonella infections af­ 75% of these cases have been reported since 1980, which shows fecting a total of 3944 persons were reported each year to CDC. increased awareness and reporting practices in regards to shellfish During this same time frame, only 6 seafood borne outbreaks illnesses. involving 147 cases were reported. Two of these outbreaks involv­ Good personal hygiene and good manufacturing practices, ing 40 cases were shellfish-associated (Chapter 8). Examining the proper classification of recreational and shellfishing waters and other surveillance systems; during the 14 year period from 1973 to prevention of sewage contamination in drinking, swimming, or 1987, an annual average of 32,957 and 35,490 Salmonella cases shellfish growing waters are the most effective preventive mea­ were reported through the laboratory-based Salmonella Surveil­ sures for the Norwalk and related gastroenteritis viruses since they lance system and the Morbidity and Mortality Weekly Report are found only in human sewage. (MMWR), respectively. Because these agents do not grow in tissue culture, very little The NETSU data base, which attempts to document all cases of infonnation is available on their fate during transfer. Outbreaks shellfish borne disease outbreaks from 1894 to 1990, reported only have been associated with depurated clams imported to the U.S. two shellf1sh associated outbreaks of confinned non-typhoidal sal­ from the United Kingdom. However, these clams were most likely monellosis between 1894 and 1973 (Rippey 1991). A 100-case depurated in contaminated water. outbreak that occurred in Florida in 1947 was traced to contami­ nated oysters. The other outbreak occurred in New York in 1967 ENTERIC BACTERIA ASSOCIATED WITH POLLUTION and involved 22 eases. This outbreak was associated with oysters imported from England (Rippey and Verber 1988). No cases of SalmoneUa Salmonella infections from shellfish were reported to the NETSU From a historical perspective, S. typhi is a bacterium of con­ between 1973 and 1988. However, several sporadic cases of sal­ cern; however, no cases have been associated with shellfish since monellosis associated with shellfish occurred in 1989 and 1990 the 1950s. The food poisoning type has been associated with shell­ (Rippey 1991). In September, 1989, three cases of salmonellosis fish. The food poisoning syndrome develops after ingestion of a were associated with mussels harvested in Maine and consumed in food that contains a sufficient number of Salmonella cells to cause Connecticut. S. in/antis was isolated in two of the cases. In Oc­ infection, usually between 100,000 and 100,000,000 cells. (The tober and December, 1989 oyster associated cases were reported in infective dose can be much lower in certain high fat foods such as Florida. In 1990, four separate oyster associated cases were re­ cheese or chocolate.) The symptoms usually develop 12-14 hours ported in Florida (Rippey 1991). after ingestion of the food, although incubation times of greater In other countries outbreaks of salmonellosis have been asso­ than 24 hours are not uncommon. Symptoms consist of mainly ciated with shellfish. For example, an outbreak of salmonellosis diarrhea along with nausea, vomiting, abdominal pain, headaches associated with clams (Venus verrucosa) was reported in Italy and chills. The symptoms are often accompanied by prostration, (Cantoni eta!. 1985). In this outbreak fifty people were affected. muscle weakness, moderate fever and drow~iness. Symptoms usu­ The causative agents were S. typhimurium and S. mbandalw.. The ally last only 2-3 days. The death rate is less than 0.2% (Jay estimated count per clam was 400-800 cells which implies that the 1987). infective dose was low. The NETSU data base on shellfish asso­ Raw foods, particularly those of animal origin, are the major ciated outbreaks-Foreign Reports, did not report outbreaks due to vehicles of salmonellosis (Cox and Bailey 1987, Allred et a!. Salmonella during the period from 1973-1990. 1967). The five most common food vehicles for Salmonella in the Isolations of salmonellae from shellfish is not uncommon. United States are beef, turkey, homemade ice cream (containing Fraiser and Koburger ( 1984) examined various including eggs), pork and chicken (Jay 1987, Cox and Bailey 1987). Turkey clams and oysters from the east and west coasts of Florida for the is the most common vehicle in Canada. However, many other presence of Salmonella. The highest incidence of Salmonella was foods have been involved in salmonellosis. For example, in 1985, from clams harvested from the Gulf (west) coast of Florida. The the largest outbreak ever reported (18,000 cases) was tmced to shellfish were analyzed very quickly after harvest and the authors pasteurized milk produced in Illinois. felt that quick analysis greatly increased recovery of salmonellae. In the United States most outbreaks of salmonel!osis are traced In addition, individual animals were analyzed instead of using to contaminated products of terrestrial animals. However, vehicles composite samples. The authors felt this increased the probability for sporadic salmonellosis are rarely identified. While CDC and of isolating different sero-types of Salmonella. In this study 43% NETSU foodbome surveillance data indicate that seafood is a of the clams tested were positive for Salmonella. This is one of the much less common vehicle for Salmonella than are other foods few studies that report the numbers of Salmonella present in the such as chicken and red meat, fish and shellfish may be respon­ samples. In analysis of oyster meats the levels of Salmonella iso­ sible for at least a small proportion of the total number of Salmo­ lated was 2.2 per 100 grams of tissue. It was noted that this level nella cases that occur each year in the United States. However, of salmonellae would be unlikely to cause illness in most consum­ current data are inadequate to make any attempt at estimating ers. Eleven different sero-types of Salmonella were isolated, with attributable risk. Seafood has been infrequently incriminated as a as many as six sero-types being isolated from the same group of vehicle of foodbome salmonellosis. samples. The authors went on to theorize that salmonellae might When examining the importance of salmonellae in seafood, it be part of the free living micro-flora of shellfish. is useful to examine the overall incidence reported to CDC. CDC Andrews eta!. (1974) examined the colifonns as indicators of PUBLIC HEALTH ASPECTS OF TRANSFERRING MOLLUSKS 49

Salmonella in oysters and clams. Over an 18 month period 263 Matev et al. compared the depuration of S. typhimurium and S. oyster and 96 clam samples were tested for coliforms, fecal enteritidis to that of E. coli and Staphylococcus aureus in artifi­ coliforms and the presence of Salmonella. Thirty-nine of the oys­ cially contaminated Black Sea mussels. E. coli was recovered for ter and 5 of the clam samples were positive for Salmonella. It was six days compared to four days for the Salmonella and two days observed that the indicators did give an indication of the presence for S. aureus. Rowse and Fleet (1982) observed that both Salmo­ of Salmonella. However, high numbers of indicators did not nec­ nella and E. coli survived in oyster feces and could be released in essarily mean that the pathogen was present. the overlying waters. Survival depended on water temperature. In In later work this same group examined the comparative va­ later studies Rowse and Fleet (1984a,b) studied the effects of lidity of members of the total and fecal coliforms groups for in­ water temperature and salinity on the depuration of S. charity and dicating the presence of Salmonella in the eastern oyster (Cras­ E. coli from the Sidney Rock oyster. In this study the organism wstrea virginica). In this study 539 oyster samples and corre­ was eliminated at similar rates. For this species, elimination was sponding harvest water samples were analyzed. Occurrence of most rapid at 18-22°C and salinities of 3.2-4.7%. Higher or lower Salmonella more closely paralleled increases in fecal coliform temperatures and lower salinities slowed depuration. Eyles and counts compared to total coliform counts. More Salmonella was Davey (1988) observed that isolation of Salmonella from the Sid­ isolated from water, meeting the total coliform standard compared ney rock oyster was correlated to rainfall and to a lesser extent low to the fecal coliform standard. Salmonella was not isolated from salinity waters. The presence of salmonellae in this study was samples that met both the sanitary survey and fecal coliform stan­ related to high E. coli counts. dard. This study points out the importance of using both the san­ itary survey in conjunction with microbial analysis to insure Campylobacter jejuni and Other Species safety. Campylobacter are curved, spiral Gram-negative rods that are Andrews et a!. (1976) studied the validity of members of the nonsporeforming and microaerophilic (Simbert 1984). Campylo­ total coliforms and fecal coliform groups for indicating the pres­ bacters grow between 25 and 43°C, are motile, oxidase positive ence of Salmonella in hard clam (also called quahaug). In this and do not ferment or oxidize carbohydrates (Stein eta\. 1992, study 214 samples were tested over a two year period. The har­ Franco 1988). The campylobacters can be broadly placed into two vesting waters were tested for coliforms and fecal coliforms and groups on the basis of the catalase test. The catalase-positive classified a~ to whether it met either the total coliform standard of campylobacters are most frequently associated with human dis­ less than or equal to 70 coliforms per 100 mLs or less than or equal ease. to 14 fecal coliforms per 100 mLs. The clams were further clas­ Campylobacteriosis may be the first or second leading cause of sified as to whether they met the market guideline of 230 fecal food poisoning in Western countries including the United States coliforms per 100 grams of tissues. None of the clams harvested (Seattle-King County Depart. Pub. Hlth. 1984, Totten 1987, from waters meeting either slandard contained Salmonella. Fur­ Franco 1988). Only recently has its importance been realized be­ thermore, Salmonella was not isolated from any meat sample cause methodology to detect the organism in food and feces was meeting the market guideline. Salmonella was isolated from some not available (Doyle 1981). of the samples which exceeded the National Shellfish Sanitation Campylobacter species were once thought to be primarily im­ Program's standards. From this work the investigators concluded portant to veterinary medicine. Prior to 1974 these bacteria were that fecal coliforms were adequate indicators of shellfish safety, placed in the genus Vibrio because of their shape (Blaser 1981, with respect to Salmonella. Doyle 1981). The organism, now known as C. jejuni was grouped Timoney and Abston (1984), studied the contamination and with V. fetus. In the 1974 edition of Bergey's Manual the genus elimination of E. coli and S. typhimurium in the hard clam, Mer­ Campylobacter was created. The genus Campylobacter currently cenaria mercenaria. The bacteria were eliminated at similar rates; consists of at least 18 species, subspecies, and biovars, with 17 however, E. coli levels declined more rapidly than salmonellae. names officially recognized by the International Committee on The organisms were eliminated from the clams becoming associ­ Systematic Bacteriology (Franco 1988, Stem eta\. 1992). ated (non-ionicly bound) with feces and pseudo-feces particulate Human illness is associated with three species of Campylobac­ matter. Most of the test organisms were eliminated between six ter, C. jejuni, C. coli and C. laridis. These organisms are carried and twenty-four hours. This study indicates that E. coli is a good in the intestinal tract of animals and therefore, may contaminate indicator with respect to salmonellae. foods of animal origin. In addition, fecal contamination of har­ Hood et al. (1983), examined the relationship among fecal vesting waters may allow shellfish to be a vehicle for the patho­ coliforms, E. coli and Salmonella species in freshly harvested, gens (Rippey 1991). C. jejuni is recognized as a leading cause of Gulf of Mexico coast oysters and clams. Salmonella was only acute bacterial gastroenteritis. It is recognized as both a food and found in samples which exceeded the National Shellfish Sanitation water borne pathogen. Foodborne illness is usually associated with Program's market guideline of 230 fecal coliforms per 100 grams the consumption of products of animal origin. In addition, C. coli of product. These investigators reported that low levels of fecal and C. laridis are also recognized causes of gastroenteritis, but coliforms and E. coli were good indicators of the absence of Sal­ less frequently than C. jejuni. These three species are collectively monella. However, high levels of these indicators did not neces­ referred to as the C. jejuni group. sarily indicate the presence of Salmonella.

Elimination of Salmonellae and E. coli from Shellfish Campylobacteriosis Associated with Shellfish Consumption It is interesting that there are species differences in depuration NETSU reported I domestic shellfish-associated outbreak of rates of species of Salmonella. For example, Cook and Ellender campylobacteriosis between 1894 and 1988, an outbreak of 16 (1986) examined the depuration of S. typhimurium, S. montevideo cases due to contaminated hard clams that occurred in New Jersey and poliovirus in Gulf oysters. S. montevideo persisted longer than in 1980. In addition, Campylobacter was suspected in several S. typhimurium. outbreaks reported to the NETSU where the etiological agent was 50 MOLLUSCAN lNTRODUCfiONS AND TRANSFERS listed as unknown (Rippey and Verber 1988). In the 1991 update of contamination by a handler. Cantori et al. (1980) reported an of the NETSU data base several outbreaks and cases of Campy­ outbreak of shigellosis from mussels (Mytilus galloprovincialis). lobacter associated with shellfish were reported. Most of these The report was written in Italian and only the abstract was in illnesses were reported in the state of Florida. In one outbreak in English. The outbreak occurred in Milan in 1978 and approxi­ 1989 two people became ill three days after consuming oysters. C. mately 100 people were affected. Studies of the mussels revealed jejuni, Vibrio paraheamolyticus and V. vulnificus were all isolated the presence of S. dysenteriae and S. boydii. from the individuals. In another incident, a single case of con­ Taylor and Nakamura (1964) reported that S. sonnei and S. firmed Campylobacter infection was reported in Lee County, Flor­ flexneri could survive at 25°C in clams for more than 50 days and ida. That same year in December, four separate cases of confirmed in oysters for more than 30 days. Campylobacter were reported (Rippey 1991). In 1990 six separate As is the case for the salmonellae, 3 surveillance systems for cases of illness from Campylobacter were reported in Florida. Five shigellosis exist at CDC. For the years 1978-1987, an average of of the incidents involved oysters and clams were implicated in the 7 foodborne outbreaks affecting a total of 573 persons were re­ other case. The age of the victims ranged from 23 to ?0 years of ported each year to the foodbome disease surveillance system age. In addition another case of Campylobacter illness from oys­ (CDC 1989). Seven outbreaks involving 137 cases were seafood ters was suspected in Alabama in 1989 (Rippey 1991). borne. Four of the 7 outbreaks, involving 77 cases, were shellfish associated (Chapter 8). During the same period an annual average Isolation from SheJifish of 14,460 and 18,498 total foodborne cases were reported through Arumugaswamy and Proudford (1987) reported the isolation of the laboratory-based Shigella Surveillance system and the C. jejuni and C. coli from the Sidney Rock oyster. These inves­ MMWR, respectively. NETSU (Rippey and Verber 1988) re­ tigators were able to detect these organisms in 17 of 79 samples. ported 4 shellfish-associated outbreaks involving a total of 93 This work is interesting, because the Sidney Rock oyster is usually cases of shigellosis in the United States between 1894 and 1988. harvested from water of fairly high salinity. Campylobacter spe­ Nine persons were reported ill in Massachusetts in 1977, II in cies are reported to be very sensitive to environmental conditions; California and 26 in Arizona in 1979, and 47 in Texas in 1986. however, in the Sidney Rock oyster, survival was reported during Between 1978-1987 NETSU reported 84 cases of shellfish­ refrigeration and freezing. Arumugaswamy et a1. (1988) allowed associated shigellosis (Rippey and Verba 1989). the oysters to feed in waters containing approximately I 0,000 cells In 1989 and 1990 additional cases of shigellosis from the con­ of C. jejuni and C. coli per mL. The oysters were then su~ected sumption of oysters were confirmed or suspected (Rippey 1991). to depuration. They were depurated within the 48 hour period The cases were for the most part sporadic and only two outbreaks usually allowed for depuration systems. These investigators also occurred. All the cases were reported in the state of Florida. The investigated survival of the organisms during storage as shellstock two outbreaks where Shigella was suspected as the causative agent at 20 and 30°C, on the half shell during refrigeration, shucked and occurred in October 1989. In both incidences, four people became bottled, stored refrigerated and frozen. The organisms failed to ill after consuming oysters. In the first outbreak four of nine peo­ multiply during room temperature storage, but did survive for 2-9 ple became ill one day after eating the oy~ters. S. sonnei and/or days. At 3 or lOoC the organism survived 8-14 days. Survival was Vibrio paralulemolyti<·us and V. fuluviali.l" were suspected. In the better at the lower temperature and in the shucked product. The other suspected outbreak four of four people became ill. Again organisms survive for months during frozen storage at - 20-24"C. either Shigella or a Vibrio was suspected. One case of Shigella in Another Campylobacter species linked to illness is C. laridis. This a two year old girl was reported in November of the same year. In organism has been isolated from mussels (Owen eta!. 1988). 1990, four separate cases of shigellosis were reported. Three of the victims were female and the other was a male. Oysters were the Shigella vehicle in all cases.

Shigella are Gram-negative, non-motile, non-sporeforming Pathogenic Escherichin coli rods-shaped bacteria. The illness caused by Shigella (shigellosis) accounts for less than I 0% of the reported outbreaks of food borne E. coli is often thought of as an indicator of fecal pollution. In illness in this country. Shigella rarely occurs in animals; princi­ 1887, Escherich observed the ubiquity of what we now designate pally, a di~ease of humans except other primates such as monkeys as Escherichia coli in human stools. Shardinger, in 1892, sug­ and chimpanzees. The organism is frequently found in water pol­ gested that members of this species be used as an index of fecal luted with human feces. pollution because they could be recovered more easily than Sal­ Symptoms of the illness include: abdominal pain; cramps; di­ monella species (Kator and Rhode~ 1991, Banwart 1989). Patho­ arrhea; fever; vomiting; blood, pus, or mucus in stools; tenesmu~. genic strains fall into four categories; enterotoxigenic, entero­ The on-set time is 12 to 50 hours. The infective dose is very low pathogenic, cnteroinvasive and hemorrhagic (Medallion 1987, and can be as few as 10 cells depending on age and condition of Mehlman 1982, Frank 1988). The first three arc usually as~ociatcd host. The disease is caused when virulent Shigella organisms at­ with human fecal contamination, whereas, hemorrhagic strains are tach to, and penetrate, epithelial cells of the intestinal mucosa. most often associated with fann animals. After invasion, they multiply intracellularly, and spread to con­ tiguous epithelial cells resulting in tissue destruction. ASIJociation with Shellfish

Association with Shellfish Much of the research on isolation and incidence of pathogenic E. coli in shellfish has been done in Japan. Sato ( 1971) was per­ Sewage pollution has been associated with outbreaks of haps the first person to report on the isolation of enteropathogenic shigellosis from shellfish. The number of cases are limited. The E. coli from oysters. From July 1969 to February 1971, this author organism does not survive well and illness is most often the result examined 160 commercial samples of foods including 66 ground PUBLIC HEALTH ASPECTS OF TRANSFERRING MOLLUSKS 5I pork samples, 34 chicken samples and 60 oyster samples. Nine­ varies from 6 hours to five days. Initially, the stool is brown with teen of the 60 oyster samples were positive for enteropathogenic fecal material but it quickly assumes the classic "rice water" E. coli. The author lists the serotypes of the strains isolated; how­ appearance. Enonnous amounts of fluids are passed effortlessly, ever, only the abstract was in English and this reviewer could not resulting in dehydration and circulatory collapse. The stool is rich detennine which serotypes were specifically associated with the in potassium and bicarbonate. Renal function is suppressed and the oyster isolates. Other work published in Japan include an article by patient suffers from severe thirst, leg cramps, hoarse speech, Kokubo (1978) that describes a study where 405 oyster samples weakness and rapid pulse (Morris and Black 1985, Blake et al. were examined for the presence of E. coli and a portion of the 1980, Sakazaki 1979). Fortunately, cholera gravis is relatively isolates were tested for pathogenic strains of E. wli. Only four uncommon. Cholera gravis results in only I in 25-100 infections pathogenic strains were isolated. One strain produced only heat from the El tor biotype and in 1 in 5-10 infections by the classical labile enterotoxin, while the other three strains produced only heat biotype. People with type 0 blood are more susceptible to the stable enterotoxin. Ogawa et al. (1980) studied the incidence of severe disease (Sakazak:i 1979). enteropathogenic E. coli in sea water, oysters, river water, and The infective dose for V. cholerae is estimated to be approxi­ sediment samples over a 10 year period. In this extensive study mately one billion cells; however, consumption of antacid~ or enteropathogenic E. coli was isolated from 14.4% of the sea water medication to lower ga<;tric acidity markedly lowers the infective samples, 14% of the oyster samples, 15.3% of the river water dose (Blake 1987). V. cholerae 01 induces illness by elaborating samples and 3.7% of the sediment samples. The relationship be­ cholera toxin which stimulates the production of cyclic AMP tween E. coli levels and enteropathogenic E. coli levels was ex­ (Holmgien 1981). Therefore, only toxigenic strains can cause cellent. As the numbers of E. coli increased, the frequency of cholera. Non-toxigenic strains of V. cholerae can cause diarrhea isolation of the pathogenic strains increased. Perez Martinez eta!. but not cholera and have also been implicated in wound infections. (1981) investigated the incidence of enteropathogenic E. coli in Cholera in the United States is relatively rare. The U.S. has raw oysters obtained from supennarkets in Mexico using inocula­ been spared any identified cholera outbreak from 1911 untill973, tion of suckling mice to evaluate for toxin. Only 3.7% of the then a single unexplained case occurred in Texas. A second chol­ isolates produced heat-stable toxin. Stephen et al. (1975) reported era outbreak occurred during August, September and October of the isolation of both enteropathogenic and enterotoxigenic E. coli 1978 when II people were infected with V. cholerae 01 El Tor from mussels in India. from recontaminated cooked crabs (Blake et al. 1980). In 1981, There are currently no data to indicate that any seafood, in­ there were two cases of cholera involving residents of the Texas cluding shellfish, is an important source for diarrheagenic E. coli Gulf Coast and 17 additional cases on an oil rig in the Gulf (Morris infections in this country. Neither the CDC arulllal summaries and Blake I985). Thirteen cases of domestically acquired cholera (from 1973 through 1987) or the NETSU data base (Rippey 1991) occurred in 1986; I2 in Louisiana and one in Florida (CDC I986). report any shellfish borne illness associated with pathogenic E. Inadequate cooking or improper handling of crustaceans seems to coli. have been the vehicle in this outbreak. Ten of the patients had severe diarrhea and 7 required hospitalization. The V. cholerae OI NATURALLY OCCURRING BACTERIA was of the El Tor biotype. Of course, an epidemic of cholera is currently under way in certain South American countries. Poor Vibrionacae sanitation and consumption of raw fecally contaminated seafood is The members of the family vibrionacae of concern include V. responsible for many of the cases. It is not believed that this clwlerae 01 and non 01, V. parahaemolyticus, V. vulnificus, V. outbreak is a threat to the U.S. because of better sanitation and mimicus, V. hollisae, V. fluvalis, Pleisomonas shigelloides, and sewage disposal. Aeromonas. A brief description of these organisms is presented V. cholerae 0 I is widely distributed and is probably part of the below. For the most part, these organisms are associated with the indigenous bacterial flora in estuarine waters (APHA 1985, Col­ marine environment, show a definite seasonal variation, and are well I984). There is evidence of seasonal variation and most cases easily killed during heating. of domestically acquired cholera have occurred during the late V. cholerae is usually divided into two groups, serotype 01 and summer and fall; with August being the primary month for infec­ non-OI V. cholerae. Those groups can be further subdivided as tion (Madden et al. I982). toxigenic and non-toxigenic. Toxigenic strains are capable of pro­ ducing cholera toxin or a very similar toxin. Non 01 V. clwhrae Toxigenic V. cholerae 01 is the causative agent of endemic or asiatic cholera. The OJ ser01ype contains two biotypes; classical At least 70 other groups of V. cholerae are known to exist. and EI tor, both of which may contain toxigenic and non-toxigenic They are referred collectively as non-01 V. cholerae or non­ strains. The biotypes are differentiated by sensitivity to polymyxin agglutinable (NAG) V. cholerae. The majority of the strains iso­ Band Murkee's group four phage and by the ability to agglutinate lated from seafood and patients are non-toxigenic strains; less than chicken red blood cells (Sakazaki 1979). The classical biotype 5% of the non-01 strains from human sources in the United States predominated worldwide until the 1960's. TheEl tor biotype is produce cholera toxin. The non-toxigenic strains are principally currently predominant world wide and is the biotype associated associated with gastrointestinal illness; but in the U.S. about 1/l of with recent cases in the U.S. and South America (Blake el a!. the human isolates are from extra-intestinal sources, including 1980, Levine I981, Morris and Black 1985, CDC 1986). wound infection, ear infection and primary and secondary septi­ Symptoms of V. cholerae OJ infection can range from asymp­ cemia (Morris and Black 1985). Associated symptoms of gastro­ tomatic or mild diarrhea to severe cases (cholera gravis). In severe enteritis have included diarrhea (100% of cases; 25% have bloody cases, V. cholerae 01 can cause profuse watery diarrhea, dehy­ stools), abdominal cramps (93%) and fever (71%). Nausea and dration and death if not promptly treated. The incubation period vomiting occurs in 21% of the victims. The diarrhea may occa- 52 MOLLUSCA)'.' INTRODUCTIONS AND TRANSFERS sionally be severe; with as many as 20-30 watery stools per day the waters of the Gulf of Mexico off the Texas coast. However, (Morris and Black 1985). Almost all of the cases of non-01 V. Paille et al. (1987) observed seasonal variation in numbers of V. cholerae infections in the U.S. have been associated with eating parahaemolyticus in oysters and waters of Louisiana. raw oysters. While V. parahaemolyticus is a common contaminant of sea­ Considering the relative frequency of isolates from seafood, the food, often present in high numbers, almost none of the isolates incidence of illness is very low. There is evidence that victims from seafood are capable of causing gastroenteritis in man (Fujino often have an underlying liver disease, which might be a host et al. 1974, Blake 1980, Hackney 1981). The test most widely factor for the disease. Also, in most cases the disease may not be used to differentiate between virulent and avirulent strains is the severe enough to warrant medical attention and therefore, the in­ Kanagawa reaction, which tests a strain's ability to produce a heat cidence may be unreported. However, it can be observed from stable hemolysin in an agar medium containing 7% NaCI, man­ Table l that non 01 V. cholerae accounted for a large percentage nitol and fresh human or rabbit red blood cells. The heat stable of the cases associated with the naturally occurring vibrios. hemolysin is the main virulence determinant for V. parahaemolyti­ Non-01 V. cholerae strains are widely distributed in the envi­ cus. Isolates from the marine environment and seafood are pre­ ronment of the United States, Asia and Europe. They occur most dominantly Kanagawa negative. Thompson and Vanderzant frequently in bays and estuaries with salinity in the area of 0.4- (1976) reported only 0.18% of the isolates from water, shellfish 1.7% (Colwell and Kaper 1978); but have also been found in rivers and sediments of the Gulf of Mexico were Kanagawa positive. In and brackish inland lakes of salinity levels as low as 0.01 %. Their Japan 99% of the sea and fish isolates are Kanagawa negative presence in oysters and water samples does show a seasonal vari­ (Sakazaki 1979). Food poisoning victims usually only excrete ation with the highest numbers being isolated June-August (Mad­ Kanagawa positive isolates. Studies have demonstrated that iso­ den eta!. 1982). Non-01 V. cholerae are free living organisms and lates do not change in the intestines and that Kanagawa positive are part of the autochatonous flora. types are probably part of marine V. parahaemolyticus popula­ tions, but present in low numbers. Vibrio paraluumolyticus Vibrio ~ulnificus V. parahaemolyticus was first associated with food poisoning in 1950 in Osaka, Japan (Fujino eta!. 1974). Since its discovery, V. vulnificus has been called the new ''terror of the deep'' and V. parahaemolyticus is implicated in greater than 1,000 outbreaks is one of the most invasive species ever described (Oliver 1985). per year in Japan and accounts for 45-70% of that country's bac­ Jt has been identified as a halophilic "lactose-positive" marine terial food poisonings. Food poisoning in Japan is usually related vibrio. Foodbome infection may result after consuming contami­ to the consumption of raw seafood during the warm months. Typ­ nated, raw or undercooked seafood, particularly oysters and ical symptoms include diarrhea (sometimes bloody), abdominal clams, with illness usually srarting 16--48 hours after ingestion. cramps, nausea, vomiting, headaches, fever and chills (Fujino et The organism penetrates the intestinal tract and produces a primary a!. 1974). The infective dose for humans is between 103 and 107 septicemia. The illness usually begins with malaise, followed by viable cells; however, a decrease in stomach acidity may decrease chills, fever, and prostration. Vomiting and diarrhea are uncom­ infective dose. The time for onset of symptoms is usually 9-25 mon, but sometimes occur shortly after chills and fever. Hypoten­ hours and the duration of the illness is usually 2.5-3 days. No i>ion (systolic blood pressure ;:;.go mmHg) is present in approxi­ deaths have been reported in the United States, but a death rate of mately 33% of the cases (Blake et a!. 1979). The fulminating 0.04% is reported for Japan. In Japan, raw seafood is the usual infection progresses rapidly and may cause death in 40-60% of the vehicle for the organism, but in the U.S. most of the foods im­ patients (Oliver 1985). Primary septicemia by V. vulnificus is plicated in V. parahaemolyticus outbreaks are cooked seafoods NOT OBSERVED in normal healthy people and is ONLY asso­ that have been recontaminated; although raw oysters and raw crabs ciated with certain risk factors including: liver disease, gastric have been implicated in some outbreaks (Barker 1974, Blake disease, malignancy, hemochromatosis and chronic renal insuffi­ 1980, Spite eta!. 1978). CDC data indicates that it is the agent ciency (Oliver 1985, Blake et al. 1979). Healthy individuals can most responsible for illness associated with molluscan shellfish. develop a gastroenteritis from this bacterium. The most common The NETSU data base indicates that it ranks sixth as a leading vehicle for the organism is raw oysters. cause of illness. In any case, it is a significant cause of illness in V. vulnificus is wide spread in the environment and has been shellfish. isolated from estuarine waters of most coastal states. Infection via V. parahaemolyticus is widely distributed in nature and has the intestinal tract is most often associated with the consumplion of been isolated from coastal waters worldwide. Its presence has been raw oysters, but it is sometimes difficult to isolate from the mol­ documented in virtually all the marine coastal environs of the lusks. Oliver ( 1981) demonstrated that antimicrobial factors in United States from the coast of Maine, south to the Gulf of Mex­ oysters could be lethal to V. vulnificus when the oysters were ico, all along the west coast and from the coastal waters of Hawaii homogenized for analysis. Kelly and Dinuzzo (1985) demon­ (Fujino 1974, Blake 1980), It is not considered to be a microor­ strated that the presence of V. vulnificus in oysters was probably ganism of the open sea because of its sensitivity to cool temper­ due to filtration of the bacterium from sea water rather than active atures and high hydrostatic pressure (Kaneko and Colwell 1978, multiplication in oysters. Colwell 1984, Schwan and Colwell 1974). Its presence in estu­ The presence of V. vulnificus in water and shellfish is seasonal arine environments and in the seafood harvested from these envi­ being most prevalent when the water temperature is high (>20"'C). ronments usually shows a seasonal variation, being present in the Low salinity (0.5-1.6%) also favors the presence of V. vulnificus highest numbers during the summer months (Kenako and Colwell in seawater (Kelly 1982). Some strains of V. vulnijicus show 1978, Hackney et al. 1980). Thompson and Vanderzant (1976) did bioluminescence and these strains may also be pathogenic (Oliver not observe a positive correlation between numbers and season in 1986). Environmental isolates are phenotypically indistinguish- PuBLIC HEALTH ASPECTS OF TRANSFERRING MOLLUSKS 53 able from clinical isolates and produce virulence factors identical fish salad, salt mackerel, raw oysters and undercooked oysters. In to clinical isolates (Tison and Kelly 1986). the U.S. raw oysters are probably the most implicated food. It is interesting that V. vulnificus is not listed in the CDC data According to the NETSU data base, P. shigelloides has only base. This is because this data base only lists outbreaks and not been implicated in 18 cases during the 15 year period from 1973- individual cases. Since this organism only affects comprised in­ 1987. This accounted for less than 0.5% of the cases of illness dividuals no outbreaks have been reported, just individual cases. associated with molluscan shellfish. This organism is causing concern. For example, in Louisiana, Miller and Koburger (1985) reviewed infections by P. warning labels are now required on sacks of oysters. Also, in shigelloides and reported by the percent of people experiencing California, oyster from the Gulf coast must have a warning label. symptoms which included diarrhea (94%), abdominal pain (74%), The warning suggests that individuals who have a compromised nausea (74%), chills (49%), fever (37%), headache (34%), and immune system or have other risk factors described above, should vomiting (33%). The onset of symptoms usually occurred 24-50 not eat raw oysters. hours after ingestion of the food. The illness was self limiting and usually lasted 24-48 hours. V. mimicus Most strains of P. shigelloides have a minimum growth tem­ perature of 8°C, but at least one strain has been reported to grow V. mimicus is biochemically similar to V. cholerae, with the at 0°C. They seem to survive well in shellstock oysters held at exception that the strains are sucrose negative. In earlier publica­ refrigeration temperatures. The organism is sensitive to pH of <4 tions, they were listed as V. cholerae of the Hieberg group 5; and salt concentrate of >5% (Miller and Koburger 1986). In ad­ however, DNA homology studies demonstrated that may of the dition, being a member of the family Vibrioneae, it should be sucrose negative strains were a separate species and in 1981 the kiiled by relatively mild cooking temperatures. name mimicus was proposed because of their similarity to V. cho­ lerae (Shandera et al. 1983, Colwell 1984). Both toxigenic and AeromoiiiJS non-toxigenic strains have been isolated, however, the food poi­ soning cases have been mostly from the non-toxigenic strains. Aeromona~ hydrophilia is listed as a cause of diarrheal illness Symptoms of the illness have included diarrhea in most cases, but by the NETSU data base. However, there is some question as to approximately 67% of the cases had nausea, vomiting and abdom­ whether it is truly a pathogen. inal cramps. Diarrhea may be bloody and will last 1 to 6 days. Other agents that have caused illness from consuming mollus­ Raw oysters and boiled crawfish (crayfish) have been impli­ can shellfish that arc of natural origin include Clostridiwn perfrin­ cated as vehicles for the organism. V. mimicus is widely distrib­ gens and Bacillus cereus. There is some question as to whether uted in nature and can be found in fresh as well as brackish waters. these organisms caused illness from consuming raw shellfish or It does show seasonal variation, being present in highest numbers were contaminants of cooked products that were temperature in the wanner months (Bockemuhl et al. 1986, Colwell 1984). abused. The data bases do not make this clear. B. cereus was most likely associated with cooked products or products that were stored V. hoUisae for a long period of time. On the other hand, it is probable that C. perfringens was in some outbreaks associated with raw products. V. hollisae (formerly EF 13) has been implicated in approxi­ mately 36 cases of food poisoning. Symptoms have included di­ Clostridium perjringens arrhea and in approximately half the cases vomiting and fever. Seafood was implicated as the vehicle for V. hollisae, including Clostridium perfringens has been associated with human dis­ raw oysters, clams and shrimp (Morris et al. 1982). ease, mostly gas gangrene, for over 90 years. However, it was not The ecology of V. hollisae is not well understood because it until the 1940's that it was ftrst associated with food poisoning. C. grows poorly or fails to grow in TCBS, the medium most used in peifringens food poisoning is associated with proteinaceous food isolation of members of the genus Vibrio. products. The bacterium has exacting growth requirements, re­ quiring thirteen amino acids and six vitamins. Foods of animal V. fumi!;si and Vibrio fluvialis origin are more likely to provide these needed growth require­ ments. Meat and poultry products account for most of the reported V.furnissi was previously classified as biovar U of V.jluvialis. illness with seafood products only accounting for approximately V. furnissi has been implicated in food borne illness (Brenner et al. 2% of the reported outbreaks (Banwart 1989). 1983). It produces gas from glucose, which is an unusual charac­ Most of the outbreaks of C. perfringens food poisoning have teristic among Vibrio species. Symptoms of illness include diar­ been associated with food service establishments. Cooking of rhea, abdominal cramps, and sometimes nausea and vomiting. foods contaminated with C. perfringens will kill vegetative cells of Most of the cases listed by NETSU are probably V. furnissi. the organism, but the spores will survive. Cooking tends to lower PhisonwiiiJS shi.geiWides the oxidation/reduction potential of foods and heat shocks the spores into activation, creating ideal conditions for growth of the P. shigelloides (formerly Aeromonas shigelloides) has been organisms. Time-temperature abuse of the cooked food allows the implicated in human gastroenteritis for 40 years (Miller and organism to grow to high numbers. C. perfringens grows very Koberger 1985). P. shigelloides is widespread in nature, being quickly, with a generation time of as low as 8.5 minutes reported mostly associated with fresh sutface water, but may also be found in some foods (Willardsen et al. 1979). Growth can occur at tem­ in seawater. It shows a seasonal variation in its isolation similar to peratures as high as 50-52.3°C (Shoemaker and Pierson 1976). that of marine vibrios; being more often isolated during the Thus, if wanning trays in food service establishments are not kept wanner months (Miller and Koburger 1985). at proper temperatures, growth can occur. Time-temperature abuse Foods implicated as vehicles for P. shigelloides include cuttle of cooked products is usually a critical factor in most food poi- 54 MOLLUSCAN INTRODUCTIONS AND TRANSFERS

sonings of C. perfringens origin. The number of organisms nor­ public could be assured that the shellfish were indeed depurated. mally found in foods is usually low compared to the high number In addition, enumeration of the organism is easier. required to induce illness. The critical number needed to induce The symptoms of C. perfringens food poisoning include severe illness has been estimated at between 106 ~ 5 x \OH (Labbe, 1988 abdominal cramps and a pronounced diarrhea. Nausea and vom­ and Hatheway eta!. 1980). iting are rare and headache and fever are usually absent. The The source of the C. perfringens can be from soil, dust, water, on-set of symptoms is usually 8-12 hours after ingestion of the spices, or the food itself. Type A is the strain mostly associated food and the illness usually does not persist for more than 24 with food poisoning. It is considered to be part of the microflora hours. The illness is caused by sporulation of the vegetative cells of soil. Virtually all soils examined have contained type A C. in the intestine accompanied by production of an intracellular en­ perfringens at levels between log 3-4 per gram (Labbe, 1989). terotoxin. The enterotoxin can be produced in food during sporu­ Also, it is associated with the intestinal contents of most animals lation but it has not been proven that illness has resulted from being present at levels of log 3--5. This level is usually observed in preformed toxin in foods (Labbe and Harmon, 1992). infants after 6 months of age (Labbe 1988). This bacterium has also been isolated from the intestinal contents and surlace of fish BaciUus cereus but at considerably lower levels. In addition, it is often isolated at Bacillus cereus is a Gram-positive, facultatively aerobic spore­ low levels from shellfish and has been suggested as an indicator of forming rod. The cells are large and the spores do not swell the fecal pollution. sporangium. These and other characteristics including biochemical The presence of C. perfringens in shellfish has been docu­ features are used to differentiate and confirm the presence B. mented worldwide. Burow (1974) reported that 56% of mussel cereus although these characteristics are shared with B. cereus var. samples were positive for the organism. Ina! et al. (1974) also mycoides, B. thuringiensis and B. anthracis. Differentiation of reported the isolation of C. perfringens from mussels in Turkey. ttJese organisms depends upon determination of motility (most B. Ayres (1975) reported the organisms isolation from a number of cereus are motile), presence of toxin crystals (B. thuringiensis), shellfish including the European flat oyster, mussels, and hard t.emolytic activity (B. cereus and others are beta hemolytic while dams. Fruin (1978) reported that most of the C. perfringens iso­ B. anthracis is usually non-hemolytic) and rhizoid growth which is lated from foods including clams were type A. Saito (1990) re­ characteristic of B. cereus var. mycoides (Harmon eta!. 1992). ported high incidence of C. perfringens in oysters in Japan. Fur­ Bacillus cereus food poisoning is the general description al­ thermore 12% of the isolates from oysters were positive for en­ ttJough, two types of illness are recognized which are caused by terotoxin production. This compared to six percent of the isolates two distinct metabolites. The diarrheal type of illness is caused by from food handlers, 2% of isolates from dogs, and 10% of water a large molecular weight heat labile protein while the vomiting isolates being positive for enterotoxin production. (emetic) type of illness is believed to be caused by a low molecular Tia Son and Fleet (1980) observed that oysters (Crassostrea weight, heat-stable peptide. commercia/is) were commonly contaminated with low levels of C. The symptoms of B. cereus diarrheal type food poisoning perfringens and Bacillus cereus. These organisms could be re­ mimic those of Clostridium perfringens food poisoning. The onset moved by depuration or relaying to clean water. Their depuration of watery diarrhea, abdominal cramps and pain occurs 6-15 h rates were similar to that of enteric bacteria such as Escherichia following consumption of contaminated food. Nausea may accom­ coli. They further observe that in artificially contaminated oysters pany diarrhea, but vomiting (emesis) rarely occurs. Symptoms that C. perfringens rapidly died off during storage, whereas counts persist for 24 h in most instances. The emetic type of food poi­ of B. cereus remained stable to refrigeration. soning is characterized by nausea and vomiting within 0.5 to 6 h Examination of CDC (Chapter 8 of this report) data shows that after consumption of contaminated foods. Occasionally, abdomi­ C. perfringens accounted for 5.4% of the outbreaks and 16.6% of nal cramps and/or diarrhea may also occur. Duration of symptoms the cases of illness associated with fish over the 15 year period is generally less than 24 h. The symptoms of this type of food from 1973--1987. Additionally, it was responsible for 4.3% and poisoning parallel those caused by Staphylococcus aureus food­ 3.1% of the outbreaks and cases associated with shellfish respec­ borne intoxication. tively during the same period. Since the illness associated with C. The type most likely associated with shellfish i~ the diarrheal perfringens is usually mild, the number of cases are probably type. The emetic type has almost exclusively been associated with much higher. rice and starchy products. The presence of large numbers of B. The NETSU data base did not report any cases of shellfish born cereus (greater than 106 organisms/g) in a food is indicative of illness since 1894. Since the CDC data base includes crustaceans active growth and proliferation of the organism and is consistent in its classification of shellfish, it is possible that the shellfish with a potential hazard to health. These high numbers could be borne illness caused by C. perfringens reported by CDC may not reached during prolong storage out of water, or during transport to have involved molluscan shellfish. other states. Analysis of the incidence of seafood borne illness caused by C. perfringens, indicates that C. perfringens is of little importance as THE EFFECT OF HARVESTING, TRANSPORTATION AND a seafood borne pathogen. The number of outbreaks are low and STORAGE ON THE NUMBERS OF MICROORGANISMS most likely due to contamination and temperature abuse. It may be IN SHELLFISH of greater importance as an indicator of pollution than as a patho­ gen. Madden et a!. recommends that C. perfringens be the indi­ This section will only be concerned with bacteria since enteric cator of choice for depuration systems. These workers noted that viruses do not multiply in shellfish. C. perfringens was far more likely to be present in polluted shell­ Only a few studies have addressed the fate of pathogens and fish than Escherichia coli because the spores survive well in the indicators during transportation and storage. In our laboratories we environment. Yet, they are depurated from shellfish at similar have examined the fate of indicators during transportation from rates. By using C. perfringens as an indicator of depuration the Louisiana to Florida and Virginia. Non £. coli fecal coliforms PUBLIC HEALTH ASPECTS OF TRANSFERRING MOLLUSKS 55 increased much faster than E. coli and often reach extremely high shows that fecal coliforms increase in numbers during storage and counts by the end of the trip. The oysters were harvested from transportation of shellfish harvest during the summer from the waters meeting the fecal coliform standard of 14 or less per tOO Gulf coast. mLs. The oysters were harvested and put into sacks on the boats. Cook and Ruple (1989), also examined the fate of fecal The fir~! oysters were harvested before 6 AM and the boat arrived coliforms and E. coli during the trip from the harvest area to the at the dock at approximately 4 PM. Approximately 425 sacks were plant. In general E. coli increased only during the time on the boat. loaded onto a refrigerated truck. The refrigeration was turned on Non E. coli fecal coliforms increase at all stages of transportation after loading and the oysters were transported to Virginia over a and during the summer months dominated the fecal coliform pop­ period of 27 hours. Both E. coli and fecal coliform counts were ulation. These studies clearly indicated that fecal coliforms are not <18/100 g for samples taken dockside. During the trip fecal adequate indicators of fecal contamination in shell stock oysters. Similar coliform levels increased to levels of greater than 400 per 100 studies with soft shell clams have demonstrnted that fecal coliform<; are grams. E. coli levels remained very low. The fecal co!iforms were not good indicators of fecal contamination during the sununer. identified to be Klebsiella species. In other studies, oysters were Cook and Ruple (1989) also studied the effect of transport on monitored in route from Louisiana to Apalachicola Bay, Florida. levels of vibrios in oysters. Many of the vibrios including V. These studies were conducted in the months of July and August. In vulnificus and V. parahaemolyricus increased by 3-4 orders of these studies the results were far more dramatic. The initial fecal magnitude during time from harvest to the plant. coliform counts averaged 13,000 per 100 grams when the oysters Marine vibrios do not depurate at the same rate as enteric reached the dock. E. coli only accounted for a small fraction of the bacteria and may be present far longer than indicators. This ob­ fecal coliform count. In one trip the E. coli MPN was 50 per 100 servation, coupled with the growth of vibrios demonstrated by g and in the other study the MPN was 20 per 100 gram~. Four Cook and Ruple may indicate that immunocompromised individ­ hundred sacks of oysters were loaded onto a truck and during the uals should not- assume that depurated shellfish are safe to con­ 15 hour trip the fecal coliform counts increased from 13,0001100 sume. A significant reduction in bacterial counts is observed dur­ grams to 240,0001100 gm. The E. coli counts increased from 50 to ing depuration (not relaying); however, a certain bacteria of the 701100 gms. In other studies from our laboratories, oyster samples normal microflora are resistant to depuration. These include vibrio were taken dockside as the harvesting boats landed and at the species (Richards 1991). V. puruhuemolyricus counts of naturally wholesale market during June and July. A total of 53 samples were contaminated oysters were unchanged during depuration. Like­ taken dockside and 30 samples were taken at the wholesale level. wise, depuration does not significantly affect counts of V. vulnifi­ Fecal coliform counts a'/eraged 11121100 grams dockside and cus or V. cholerae. These pathogens could increase in numbers 10,0001100 grams at the wholesale market. This data clearly during storage and transportation.

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Genetic Aspects of Introduction and Transfer of Molluscs

Patrick M. Gaffney and Standish K. Allen, Jr.

ABSTRACT Attempts to predict the biological impact of an introduction have traditionally focused on the ecological dynamics of competition and predation, or the concomitant introduction of parasite~ or disease organisms. We focus here on a subject that has received less attention: the genetic effects of introductions on native populations. These may be broadly defined as direct or indirect changes in the genetic composition of an endemic population attributable to the arrival and establishment of a non-native population. Direct effects occur when the gene pool of the native population is open to the introgression of genes from the introduced population. Indirect effects occur when hybridization between the native and introduced populations is not possible, but alterations in gene frequencies result from ecological interactions with the introduced organism A transfer is defined here as the movement of individuals of a given species to another area within the current geographic range of that species. An introduction is defined as the importation of individuals of a given species into an area where it is not endemic. The nature and extent of genetic effects are determined primarily by the degree of reproductive isolation between the introduced and resident populations, the nature of the isolating mechanisms (pre- vs. postzygotic), and the relative sizes of the two populations. We consider the introduction of the Pacific oyster Crassostrea gigas to mid-Atlantic waters and conclude that the genetic impacts of such an introduction are likely to be indirect only. The magnitude of such impacts will depend on ecological factors affecting the success of the introduction and cannot be accurately predicted at present.

KEY WORDS: introductions, hybridization, oyster, Crassosrrea

Attempts to predict the biological impact of an introduction In order to estimate the genetic effects of a particular introduc­ have traditionally focused on the ecological dynamics of compe­ tion, we must consider two factors: I) the strength of the barrier, tition and predation, or the concomitant introduction of parasites if any, to gene flow between the native and introduced popula­ or disease organisms. We focus here on a subject that has received tions, and 2) the degree of genetic differentiation between them less attention, the genetic effects of introductions and transfers on (Figure 1). We will consider three cases along this spectrum. native populations. These may be broadly defined as direct or indirect changes in the genetic composition of an endemic popu­ TRANSFERS lation attributable to the arrival and establishment of a non-native At one end of the spectrum are "transfers," which we define population. Direct effects occur when the gene pool of the native as adt'Qixtures of native and introduced populations belonging to population is open to the introgression of genes from the intro­ the same biological species. Although the two populations may duced population. Indirect effects occur when hybridization be­ differ to some extent genetically, they readily interbreed. The tween the native and introduced populations is not possible; alter­ genetic consequences of interbreeding will depend on the degree to ations in gene frequencies result from ecological interactions with which the introduced population differs from the native popula­ the introduced organism. tion. Three considerations are important for assessing the genetic If the species is characterized by the existence of locally impacts of introductions and transfers: time scale, the ameliorating adapted stocks or populations, the immediate result of introgres­ role of natural selection, and the meaning of fitness. Immediate sion will be the disruption of coadapted gene complexes and a genetic effects---those evident in the first few generations follow­ consequent reduction of fitness in the descendants of hybrid mat­ ing an introduction--may differ substantially from long-term ef­ ings. Only when the number of animals introduced is large relative fects. This is because natural selection continually acts to remove to the native population will this transient effect be noticeable. less adapted genotypes from a population. For example, the inter­ Following the transfer, natural selection will act to restore mean breeding of an introduced population with natives may at first lead population fitness and form new coadapted gene complexes. After to the production of poorly adapted hybrid progeny, thus lowering the winnowing action of natural selection, the native population mean population fitness. Over time, however, natural selection may even reach a higher "adaptive peak" as favorable new genes will act to improve the mean fitness of the population, either by contributed by the introduced population increase in frequency. eliminating the alleles responsible for hybrid inferiority, or by When the endemic population is small and locally adapted, as favoring the development of reproductive isolation between the may commonly occur in terrestrial or island populations of organ­ native and introduced populations. Finally, attributes that enhance isms with restricted dispersal capacities, transfers may destroy the biological fitness, the ability of an individual to survive and trans­ unique phen01ype of the local population, even if overall popula­ mit its genes to the next generation, may not be desirable attributes tion fitness is not compromised. The homogenizing effect of in­ from a human perspective. For example, genetic changes resulting discriminate transfers is popularly labelled "genetic pollution," in earlier reproduction or smaller adult size may increase fitness, and results in the loss of interpopulation diversity and distinct local to the chagrin of the human consumer. phenotypes. This concept is most appropriately applied to rare or 60 MOLLUSCA~\ INTRODUCTIONS AND TRANSFERS

Genetic Distance defines species on the basis of reproductive isolation, there are many cases where good biological species produce hybrids, even small large under natural conditions. Contemporary species concepts (re­ viewed by Templeton 1989) more readily accommodate situations genetic exchange possible where reproductive isolation is less than absolute yet species nev­ ertheless behave as distinct, cohesive evolutionary lineages. When interspecific hybridization is possible, we must ask TRANSFERS INTRODUCTIONS whether it is probable. This requires a careful con~ideration of the Figure I. The continuum of genetic difference between populations in biology of the native and introduced species, and the nature of the relation to reproductive isolation. Transfers involve freely interbreed­ mechanisms that effect reproductive isolation. Reproductive iso­ ing conspeciflc populations; introductions involve distinct species be­ lating mechanisms (RIMs) are conveniently categorized as pre­ tween which varying amounts of gene How are possible. and postzygotic. Examples of the prczygotic RIMs range from behavioral differences that prevent interspecific mating (e.g., time endangered terrestrial vertebrates restricted to small isolated pop­ of spawning) to gametic incompatibility. Postzygotic reproductive ulations; it is not particularly apropos in the case of shellfish pop­ isolation occurs when hybrids are formed, but are less viable or ulations, which are typically very large and characterized by ex­ sterile. tensive gene flow between geographic regions. If the primary barrier to hybridization is prezygotic, direct ge­ In cases where the native population does not represent the netic effects will occur when occasional breaches result in gene pinnacle of adaptedness-for example, where rapid environmental flow between the two ~pecies. The immediate results may range change has outstripped the capacity of the population to rc~pond from detrimental to beneficial, while long-term effects-from the genetically-the introgrcssion of new genes may result in imme­ perspective of the organism, not the human consumer-may range diate benefits. Similarly, when the population possesses commer­ from negligible to positive. As discussed above, the size of the cial!y undesirable characteristics, the influx of genes conferring a introduced population and the extent of gene flow play key roles in more desirable phenotype may be beneficial from the human per­ determining the magnitude of short- and long-term genetic im­ spective. Moav eta!. (1978) demonstrated how the introduction of pacts. selected populations may be used for the genetic improvement of If on the other hand the primary barrier to hybridization is commercially exploited wild fish populations. postzygotic, then the mere presence of one species may impose a Perhaps the most important factor affecting the immediate ge­ burden on the other. This occurs when the two species readily netic impact of a transfer is the size of the introduced population cross-fertilize, but the progeny show reduced viability or sterility, relative to the native population. In most cases, involving com­ effectively resulting in gametic wastage. The possibility of wasted mercial shellfish, the transferred population is infinitesimal com­ gametes becomes important when the introduction is massive, or if pared to the resident population, with the result that any immediate the introduced species is able to become established and attain genetic impact, negative or positive, will be difficult to detect. high density. In this case, both species will lose gametes to the However, if the transfer introduces beneficial genes to the native formation of interspecific hybrids. If the two species occupy the population, these will increase in frequency over time and a long­ same niche and have no prezygotic RIMs, then the loss of gametes term positive effect may result from even a small transfer. becomes critical, and one species may drive the other to extinc­ Transfers have been a regular practice in commercial shellfish tion. This situation is analogous to the use of sterility induced by populations for over a century (e.g., Ingersoll1881, cited in Ha­ chromosomal rearrangements in insect population control (Foster ven eta!. 1978); indeed, Elton (1958) considered oyster culture to eta!. 1972). Which species wins the competition will depend on be ''the greatest agency of all that spreads marine animals to new the population sizes and reproductive outputs of the two species. quarters of the world.'' Unfortunately, no clear evidence on the In practice, it is unlikely that two distinct species will occupy genetic impact of such transfers is available. Interpopulation cross­ precisely the same niche; this, coupled with the widespread larval ing of C. virginica produced negligible or positive effects on larval dispersal typical of shellfish, would likely lead to the stable co­ survival (Newkirk 1978) or reduced larval survival (Mallet and existence of the two species in some areas, with other habitats Haley 1984). Juvenile growth (Mallet and Haley 1983) and sur­ supporting one or the other species only. vival (Mallet and Haley 1984) were higher in the progeny of When interspecific hybridization does occur, the evolutionary interpopulation crosses than in the progeny of intrapopulation dynamics of the hybrid and parental populations can be complex crosses. These limited results suggest that both immediate and (e.g., references in Levin 1979). The fate of an introgressed gene long-term genetic effects of transfers will range from negligible to depends not only on its fitness on the new genetic background, but positive. However, as these authors noted, environment typically also on the fitness of alleles at linked loci, and the rate of recom­ plays a larger role than genetics in overall performance, and ge­ bination between it and linked loci (Barton and Bengtsson 1986). notype-environment interactions are common. The effect of a par­ Consequently, it is very difficult to predict the nature and extent of ticular transfer is thus difficult to predict accurately without de­ genetic changes in a recipient population due to the introgression tailed information on the resident and introduced populations and of heterospecific genes. their performance at the site of introduction. INTRODUCTIONS: INDIRECT GENETIC EFFECTS INTRODUCTIONS: DIRECT GENETIC EFFECTS In the event the barrier to hybridization cannot be breached, the An introduction is defmed here as the importation of a species only genetic effects the introduced species may exert on the native into an area where it is not endemic. The genetic effects of an species will be indirect, and will depend on the nature of interac­ introduction on an endemic species will be determined largely by tions between the two species. Two different scenarios may be the permeability of the barriers to interspecific hybridization. Al­ outlined: 1) The alien has only marginal success in becoming though the classical biological species concept of Mayr (1963) established. Its genetic effect on the native species is negligible. 2) GENETIC ASPECTS OF INTRODUCTION 61

The alien becomes well-established, occupying a niche that over­ The Pacific oyster has been introduced repeatedly into eastern laps partially with the native species. Ecological interaction in waters, including Maine (Dean 1979), Massachusetts (Galtsoff et areas of sympatry will drive genetic changes in both species. The al. 1950, Dean 1979, Hickey 1979), Long Island Sound (Dean effects of such changes on the two gene pools will depend on the 1979), the Chesapeake Bay (Cranston Morgan, pers. comm.) and relative abundance and reproductive output of sympatric vs. allo­ several southern states (Galtsoff et al. 1950). Its failure to become patric populations, and on the amount of gene flow among popu­ established in these localities may be the result of the ''gametic lations of each species. warfare" described above, rather than an inhospital environment, as it has been successfully introduced to a wide range of environ­ A Concrete Example: Crassostrea vlrglnlca and Crassostrea gigas mental regimes (Mann 1983). The continued decline of the American oyster (C. virginica) Where the American oyster has been introduced to exotic wa­ fishery in the mid-Atlantic region has raised the prospect of intro­ ters, it has sometimes succeeded in establishing small but stable ducing the Pacific oyster (C. gigas) to areas which no longer populations. Examples include Pearl Harbor, Hawaii (Brock 1960) support commercial harvests of the former (Mann 1979, Virginia and Boundary Bay, British Columbia (Elsey 1933, Quayle 1964). Sea Grant 1990). At the same time, this notion is strongly opposed In Hawaii, there appears to have been no indigenous oyster by those who fear dire biological impacts, in the form of intro­ adapted to the relatively limited estuarine habitat present there, duced parasites or disease organisms, competitive exclusion or and the establishment of C. virginica followed the planting of even "genetic pollution" of the American oyster. We leave the almost 40,000 oysters at the end of the nineteenth century (Brock question of parasites, diseases and ecological impacts to others in 1960). This population persists today (John Ewart, pcrs. comm.). this symposium, and address here the potential genetic effects of In British Columbia, the only indigenous oyster is ; the introduction of C. gigas to the mid-Atlantic region. oysters of the genus Ostrea are generally incapable of cross­ The first issue to be resolved is whether any direct genetic fertilizing Crassostrea species (Davis 1950, Menzel 1987). In any effects are likely, i.e., what RIMs exist between the two species? case, by the time C. virginica was introduced there, the native Both eggs and sperm from one species are effective at stimulating oyster population was severely depleted. Repeated introduction~ spawning by the other species in the laboratory (Galtsoff and beginning at the tum of the century eventually resulted in the Smith 1932). Cross-fertilization also appears to occur readily in establishment of extensive American oyster beds in two small both directions (reviews in Menzel 1987, Gaffney and Allen in tributaries of Boundary Bay (Elsey 1933). It is possible that the prep.). We have found no published data on the interspeciflc com­ introduction of the Pacific oyster at about the same time may have petitive abilities of sperm, but preliminary evidence indicates that limited the subsequent spread of the American oyster on the west the schedule of meiotic events is not altered in either species by coast of North America, by either genetic (i.e., "gametic war­ hetemspecific fertilization (Bernat and Gaffney unpubl., Scarpa, fare") or ecological interactions. The apparent persistence of C. Allen and Gaffney unpubl.). Overall, it appears that prezygotic virginica populations as discrete entities coexisting with sympatric RIMs between the two species are very weak.. populations of C. gigas (Bourne 1979) is further evidence against The question of postzygotic RIMs between the two species is the likelihood of successful hybridization in nature. problematic. The literature (see Menzel 1987 for review) is inad­ In conclusion, we believe on the basis of presently available equate to settle this question, because hybridization experiments data that the introduction of C. gigas to mid-Atlantic waters is have rarely been followed by genetic verification (Gaffney and unlikely to have any direct genetic effects on native oyster popu­ Allen 1991). Recent experimental data confirm the view that hy­ lations. Indirect genetic effects might occur if the Pacific oyster brids do not survive to metamorphosis (Allen and Gaffney 1991). succeeded in becoming established; the magnitude of such effects Therefore it seems likely that introduced C. gigas would be capa­ could range from negligible to extensive, depending on the nature ble of cross-fertilizing native oysters, and that the hybrids so of ecological interactions between the species. Our current under­ formed would represent wasted gametes. In places where native standing of the ecology of bivalve introductions does not allow us oysters vastly outnumbered the introduced species, the loss of to predict confidently the nature or extent of any such indirect gametes would seriously hinder the spread of the latter. Any C. genetic effects. gigas zygotes formed during a mass spawning of the two species would probably be spread so thin after larval dispersal that they ACKNOWLEDGMENTS would be incapable of propagating a second generation by ho­ mospecific mating. In areas devoid of indigenous oysters, on the We thank our colleagues for frank and stimulating discussions other hand, if ecological conditions were favorable and minimum during the workshop on "Genetic Impacts of Introducing Non­ critical densities were attained, an inrroduced species such as C. Native Oyster Species in the Mid-atlantic Region'' held at Rutgers gigas might stand a good change of becoming established. Such Shellfish Research Laboratory, March 15-16, 1990. This is New areas could act as reservoirs from which larvae would be dispersed Jersey Agriculture Experiment Station Publication No. D-32001- to sites where growth and survival were satisfactory, but repro­ 3-90 and Contribution 92-53 of the Institute of Marine and duction effectively undermined by gametic wastage. Coastal Sciences.

LITERATURE CITED Allen, S. K., Jr. & P. M. Gaffney. 1991. Hybridization among three species Brock, V. E. 1960. The introduction uf aquatic animals into Hawaiian of Crassostrea. Jour1Ull of Shellfish Research 10:301. (Abstract). waters. lnternationale Revue der gesamten Hydrobiologie 45:46J-480. Barton, N. & B. 0. Bengtsson. 1986. The barrier to genetic exchange Davis, H. C. 1950. On interspecific hybridization in Ostrea. ScieiiCe Ill: between hybridising populations. Heredity 56:357-376. 522. Bourne, N. 1979. Pacific oysters, Crassostrea Kigas Thunberg, in British Dean, D. 1979. Introduced species and the Maine situation. Pages 149-- Columbia and the South Pacific islands. Pages 1-53 in R. Mann, 164 in R. Mann, editor Exotic Species in Mariculture. MIT Press, editor. Exotic Species in Mariculture. MIT Press, Cambridge. Cambridge. 62 MOLLUSCAN lNTRODUCfiONS AND TRANSFERS

Elsey, C. R. 1933. Oysten; m British Culumb1a. Bulletin of the Biological population matings and crosses of the oyster Crassosrrea virgmrca. Board ofCarwda 34:1-34. Canadian Journal of Fisheries and Aquatic Sciences 40:948--954. Elton, C. S. 1958. The Ecology of Invasions by Animals and Plants. ---. 1984. General and specific combining abilities of larval and ju­ Methuen and Co. Ltd., London. venile growth and viability estimated from natural oyster populations. Foster, G. G., M. 1. Whitten, T. Prout & R. Gill. 1972. Chromosome Marine Biology 81:53-59. rearrangements for the control of insect pests. Science l76:875-880. Mann, R. 1983. The role of introduced bivalve mollusc species in marl­ Gaffney, P.M. & S. K. Allen Jr. 1991. Hybridization in Crassostrea: a culture. Journal of the World Maricuiture Society 14:546--559. critical review. Journnl of Shellfish Research 10:303. (Abstract). Mayr, E. 1963. Animal Species and Evolution. Harvard University Press, Galtsoff, P. S. & R. 0. Smith. 1932. Stimulation of spawning and cross­ Cambridge. Menzel, W. 1987. Hybridization of oysters and clams. Pages 47-59 inK fertilization between American and Japanese oysters. Scumce 76:371- Tiews, editor. Selection, Hybridization, and Genetic Engineering in 372. Aquaculture. Volume 2. Heenemann, Berlin. Haven, D. S., W. J. Hargis Jr. & P. 0. Kendall. 1978. The Oyster In­ Moav, R., T. Brody & G. Hulata. 1978. Genetic improvement of wild fish dustry of Virginia: Its Status, Problems and Promise. Virginia Institute populations. Science 20 I : I 090-1094. of Marine Science, Gloucester Point, Virginia. (VIMS Special Papers Newkirk, G. 1978. lntemction of genotype and ;alinity in larvae of the in Marine Science No_ 4) oyster Crassostrea virginica. Marine Biology 48:227-234. Hickey, J. M. 1979. Culture of the Pacific oyster, Crassostrea gigas, in Quayle, D. B. 1964. Distribution of introduced marine Mollmca in British Massachusetts waters. Pages 129---148 in R. Mann, editor. Ex:otic Spe­ Columbia waters. Journal of the Fisheries Research Board uf Canada cies in Mariculture. MIT Press, Cambridge. 21:1155-1181. Levin, D. A., editor. 1979. Hybridization An Evolutionary Perspective. Templeton, A. R. 1989. The meaning of species and speciation: a genetic Dowden, Hutchinson & Ross, Inc., Stroudsburg, Pennsylvania. perspective_ Pages 3-27 in D. Otte and J. A. Endler, editors. Specia­ (Benchmark Papers in Genetics, Volume 1 1.) tion and Its Consequences. Sinauer Associates, Inc., Sunderland, Mas­ Mallet, A. L. & L. E. Haley. 1983. Growth rate and survival in pure sachusetts. Avoiding the Transmission of Disease in Commercial Culture of Molluscs, with Special Reference to Perkinsus marinus (Dermo) and Haplosporidium nelsoni (MSX)

Susan E. Ford

ABSTRACT Epizootic mortalities of oysten. m the United States and Europe over the last several decades have stimulated a great deal of concern over the potential spread of disease-causing agents by introduction or transfer of molluscs in commerce. Whereas there is good evidence for the spread of some pathogens in this manner, especially those that are demonstrably contagious, evidence for others is purely circumstantial. When making decisions concerning shipments of stock>, ;hell fish regulators, managers, biologists, and industry members must critically evaluate such evidence, and add to it all other available information about the disease and its causative agent. Rational decision-making should consider biological information on life cycles and transmission of the pathogens, their distribution patterns in enzootic waters, environmental limit~ to their spread or survival, and a knowledge of the history of the animals to be sh1pped. In the United States, two major oyster pathogens, exhibiting distinctly different biological characteristics, are m.ed to illustrate problems and to provide advice, concerning potential tramfer of disease agents. Perkinsus marmus, cause of Denno disease, is a highly contagious pathogen with a documented history of spread through movement of oysters. Until 1990, it had not become epizootic in northern estuaries (Delaware Bay and north) despite repeated large scale introductions from southern areas (Chesapeake Bay and south). Coincident with abnormally high winter tempemtures from 1990 through 1992, P. marinus was reported as far north as Cape Cod, and caused an epizootic in Delaware Bay, underscoring the probable influence of temperature in control of this parasite. Haplosporidium ne/soni, cause of MSX disease, has not been demonstrated to be contagious and oysters can become parasitized in the absence of nearby infected oysters. Its spread has not been convincingly linked to tr.msfers of oysters. Decision-makers are urged not to dwell solely on the ''unknowns'' in molluscan disease situations, but to make full use of what is known alxtut the diseases, their causes and controls.

KEY WORDS: disease, introduction, mollu>C, oyster, Hapiosporidium neisoni, Perkin.ms marinus

INTRODUCTION In the United States, several conferences have considered the overall problems surrounding the introduction of exotic species The documented, suspected, and potential transfers of disease­ and the movements of shellfish in commerce, and have attempted causing organisms in transplantations and introductions of com­ to standardize regulations of the various states affected. Austin mercially valuable molluscs have received considerable attention Farley and Fredrick Kern of the U.S. National Marine Fisheries over the past two decades (Mann 1979, Rosenfield and Kern Service llave proposed the establishment of shellftsh management 1979, Andrews 1980, Elston et al. 1986). Since the middle of the zones and embargo areas based on the known distribution of in­ twentieth century, concern over possible introduction of disease fectious diseases, parasites, predators, pests, and competitors has been stimulated by epizootic mortalities associated with previ­ (Proceedings of a Shellfi~h Relocation Conference, Marine Bio­ ously undescribed pathogens in several species of oysters on the ea~t logical Laboratory, Woods Hole, MA. February 3-4, 1982). coast of the United States and in western Europe (Andrews 1980). Movement of species between zones would require approval by a In response to these and other disease problems in marine spe­ "controlling authority" and transfers between embargoed areas cies, the Working Group on Disease of the International Council would, in addition, be permitted only after thorough assessment of for the Exploration of the Seas (ICES) established criteria for the the proposed transfer, including a review of the biology of the introduction of exotic species, which are designed to limit the species and associated organisms, and compliance with the ICES spread of disease (Sindermann and Lightner 1988). The guidelines recommendations, including inspection by a certified laboratory. specify that broodstock must be quarantined prior to and during Despite efforts to establish uniform regulations for the transfer spawning, and subsequently destroyed. First generation progeny of native species, shellfish are commonly shipped between areas can be transplanted to the natural environment if no diseases or of the United States without concern for potential disease trans­ parasites be<:ome evident in quarantine. When an introduced or fers-as they have been for centuries. In other instances, it may be transferred species is part of current commercial practice, ICES impractical to follow ICES recommendations because of the ex­ recommends periodic inspection of material (including micro­ pense and time required to provide the needed information. For scopic examination) by the receiving country prior to mass trans­ example, movement of seed stocks from areas of high natural plantation. Each shipment must be inspected upon arrival and setting to other areas for growth and conditioning, or relays from quarantined or disinfected whenever possible or appropriate. Im­ condemned to clean water, are rarely accompanied by inspection portation must be immediately discontinued if inspection reveals for disease agents. Some states have no regulations and many that any introducible pests or diseases. do are lax in enforcement. Some shellfish growers are unaware of the potential risks or willfully ignore the rules. Managers and Contribution No. 90 10 from the ln;titute of Marine and Coastal Sciences, regulators arc often caught between the desire to foster shellfish Rutgers University. industries that rely on transfer of animals and fear of allowing

63 64 MOLLUSCAN INTRODUCTIONS AND TRANSFERS introduction of a pest or pathogen that could result in catastrophe. on the very real and immediate problems caused by these two They almost always are forced to make decisions with too little pathogens. To illustrate some problems commonly faced by these information. individuals, I'd like to cite some specific concerns about potential A decade ago, MaUhiessen (1979) stated that "many decisions spread and control of MSX and Denno diseases. The questions are made by regulatory authorities relating to the importation of shell­ of immediate practical importance and they illustrate what we do fish inevitably will be made on the basis of best guess rather than and do not know concerning these diseases as they impact move­ fact.'' This statement is true today. Some of the guess work is ment of the shellfish: because we don't completely understand the biology of the para­ I. What is the evidence for introduction of Perkinsas marinas sites and their hosts, but some is because individuals making de­ and Haplosporidiam nelsoni by oyster tmnsport? cisions (whether regulator or industry member) are not aware of 2. Can the pathogens be transmitted in hatchery-produced lar­ what is known about them. In this situation, the scientist can be vae or small seed? most helpful by evaluating available information as accurately as 3. Can the pathogens be spread through overboard disposal of feasible, by presenting it as dearly as possible, and by taking pains contaminated meats, shells, or other wastes by processors, to distinguish between fact and speculation (Bowden 1979, Mann dealers, restaurants, or consumers? 1979). 4. Can the pathogens be transmitted to and from other species? Evidence implicating shipments of molluscs in the spread of 5. Are there methods for treating small lots of oysters (brood­ disease is convincing in some cases. For instance, the spread of stock, larvae, small seed) to eliminate pathogens? Bonamia ostrea, a parasite of the flat oyster Ostrea edulis (Lin­ naeus, 1970) (Grizel eta!. 1988), can be followed along a docu­ EXAMPLES mented path tracing introductions of host and parasite from the east coast of the United States to the west coast and then to Europe I. What is the Evidence for Introdw:tion of Per/ansas nuuinus and (Elston eta!. 1986, Farley eta!. 1988). The linkage, however, is Haplosporidiam nelsoni by Oyster Transport? not in itself sufficient evidence. What fortifies this argument is the fact that B. ostrea can be transmitted directly from oyster to oyster One of the well-documented, but unpublished, instances of (Poder et al. 1982). transmission of a disease-causing organism affecting molluscs oc­ Much of the evidence for transmission of disease along with curred in the early and mid 1950s in Delaware Bay. Because the movement of molluscs, however, is circumstantial. The outbreak supply of native seed was low during this period, many Delaware of Malpeque Bay disease of oysters, Crassostrea virginica (Orne­ Bay planters bought "seed" oysters from private leases in the lin, 1791), in Prince Edward Island in 1914--15 was preceded by Hampton Roads area and other higher salinity regions of Chesa­ transplantation of oysters from New England, which first took peake Bay where P. marinas was present and causing heavy losses place on a large scale just before the mortalities occurred (Needler (Andrews 1988). Infected oysters were brought by the shipload for and Logie 1947). Nevertheless, Fraser (1938) reported that direct planting in Delaware Bay (H. Haskin, Haskin Shellfish Research inoculation of material from sick to healthy oysters failed to cause Laboratory, personal communication, 1989). disease symptoms, and the disease was unknown in New England, A survey conducted by Rutgers University in 1955 and 1956 although the oysters there may have been resistant. found evidence that the disease had spread from the imported to Two diseases of oysters appeared in France shortly after the native oysters (Christensen 1956). The highest prevalences of P. introduction of Pacific oyster, Crassostrea gigas, (Thunberg marinas were in the oysters brought from Virginia and in the 1793) seed. Gill disease of the Portuguese oyster, Crassostrea native oysters growing close to them. Prevalences were negligible angalata appeared in late 1966 in an area of southwestern France on the seed beds and on the eastern edge of the planting grounds. where C. gigas had been introduced at approximately the same Prevalences and intensities of infection were low compared to time (Grizel and Hera! 1991). The disease, caused by a virus, those in fully epizootic areas of Virginia and the Gulf of Mexico almost completely destroyed C. angalata culture in France. Aber (Andrews and Hewatt 1957, Mackin 1962) and there were no disease, caused by the protozoan Marteilia refringens (Alderman reports of heavy mortalities in Delaware Bay (Christensen 1956). 1979, Balouet 1979), appeared in Brittany in 1968, in an area Although the proximity of imported oysters to infected native where Pacific oysters were being held, and subsequently caused oysters was highly suggestive of transmission, lack of monitoring extensive losses of the flat oyster, Ostrea edalis (Andrews 1980). for the period before introduction precluded a clear assessment of Marteilia sp. has been found occasionally in C. gigas, (Cahour the origin of P. marinas in native stocks. Within two years of this 1979), but experimental transmission (between or within the two survey (spring 1957), however, the epizootic caused by H. nelsoni oyster species), has never been successful (Balouet eta!. 1979, (MSX) had begun (Haskin et al. 1966) and all imports and exports Figueras and Montes 1988). into and out of Delaware Bay were embargoed. Intensive moni­ Two important protozoan parasites of oysters have been re­ toring in 1958 and 1959 to determine the cause of the epizootic sponsible for catastrophic mortalities of C. virginica on the Gulf failed to show significant presence of P. marinus (unpublished and East Coasts of the United States over the past forty to fifty records of this laboratory). years. The recognition of Perkinsus marinas (Mackin, Owen, Col­ We interpreted these observations as evidence that P. marinas lier 1950) as the cause of Denno disease in southern estuaries and was introduced into Delaware Bay and sustained by importations Haplosporidium nelsoni (Haskin, Stauber, Mackin 1966) as the of infected oysters from lower Chesapeake Bay, but was unable to cause of MSX disease in the mid-Atlantic estuaries has spurred maintain itself once that source was stopped (Ford and Haskin most of the concern over the spread of shellfish disease in the 1982). Andrews (1988) pointed out that P. marinas also disap­ United States. Many of the greatest worries of industry members, peared from major planting areas in the lower Chesapeake after the state regulatory officials, and biologists in the United States center MSX epizootic of 1959-1960 killed most of the oysters there. The DISEASE TRANSMISSION THROUGH INTRODUCED MOLLUSCS 65

same occurrence in Delaware Bay between 1957 and 1959 un­ spat in Virginia in 1976. These observations have led us to con­ doubtedly contributed to the elimination of P. marinus in that sider the possibility that direct transmission from oyster to oyster estuary, but in contrast to Chesapeake Bay, P. marinus never may indeed occur, with the source of infective stages being very reappeared to cause problems in Delaware Bay, even after inten­ young oysters in which spores are produced. sive plantings of native seed resumed in the late 1960s and 1970s For several years before the first MSX epizootic in 1975, Del­ (Haskin and Ford 1983). Rather, low temperature was considered aware Bay planters had been importing large quantities of seed to be the controlling factor in the failure of P. marin us to persist oysters from the seaside bays on the eastern shore of Virginia (N. in Delaware Bay or to become epizootic north of Chesapeake Bay Jeffries Sr., personal communication), as well as from the lower (Christensen 1956, Andrews and Hewatt 1957). Chesapeake. When the first oyster disease survey was initiated in In the summer of 1990, P. marinus was found in oysters at a that region in mid-1959, H. nelsoni was found, although a newly number of sites in Delaware Bay (Ford, unpublished) where it discovered, related species, H. costale (Woods and Andrews caused localized epizootics. In 1991, the disease intensified caus­ 1962) (cause of SSO disease), was more prevalent in these high ing severe mortalities over much of the New Jersey portion of the salinity waters (Andrews et al. 1962, H. Haskin, personal com­ Bay. Coincidentally, temperatures in the Delaware Bay area dur­ munication). Andrews (1968) speculated that a new and virulent ing 1990 and 1991 were among the highest on record (U.S. De­ "race" of H. nelsoni may have developed by "interbreeding" of partment of Commerce, National Oceanic and Atmospheric Ad­ H. costale and H. nelsoni when the imported oysters were moved ministration, Climatological Data for New Jersey). The 1990--91 into the lower salinity waters of Delaware Bay. A simpler hypoth­ epizootic was not linked with large-scale transplants of infected esis also presupposes that H. nelsoni was enzootic to the seaside of oysters and, in fact, an apparent focus of infection appeared on the Virginia, but was masked by the better adapted (to high salinity) New Jersey seed beds where oysters would never have been in­ H. costale. If spores of H. nelsoni were present in the huge num­ troduced. At the same time, infected oysters were found at several bers of young, rapidly growing oysters moved into the Delaware locations on the Atlantic coast of New Jersey, including Raritan Bay, then they, rather than a hybrid strain, might have initiated the and Manasquan Bays (W. 1. Canzonier, Maurice River Oyster epizootic once H. nelsoni was in a more favorable salinity. Culture Foundation, personal communication) where oyster indus­ Outbreaks of MSX disease in at least two areas on Cape Cod tries have not existed for many years. Our current interpretation of have foJlowed importation of seed oysters from areas where H. these data is that pre-existing non-lethal infections in a few native nelsoni was present (Krantz et a!. 1972, Haskin and Andrews oysters, or introductions by transient ships or overboard disposal 1988), but it is equally signiftcant that other outbreaks have oc­ (see below), were stimulated to proliferate and spread by unusu­ curred in the absence of any known importations. Notable among ally warm temperatures. It is significant that the previous incursion these was the initial epizootic in Chesapeake Bay in 1959, which of P. marinus into Delaware Bay in the 1950s, which occurred occurred in the midst of "native [James River] transplants no during a more typical temperature regime, never caused epizootic different from beds in surrounding areas [which did not experience mortalities and disappeared after importation of infected seed was mortalities]" (Andrews 1968). Seed oysters were not moved into stopped. We expect that a return to more normal temperatures will this area from seaside bays (J. D. Andrews, Virginia Institute of attenuate the cycle of parasite proliferation, host death (releasing Marine Science, personal communication). Mortalities caused in infective forms), and reinfection of new hosts, but its effective 1983--85 by MSX in Oyster Bay, Long Island, a location totally disappearance (not causing mortalities or being detectable through controlled by one company, were not associated with imports (D. routine sampling) will probably require unusually low tempera­ Relyea, F. M. Flower and Son Oyster Co., personal communica­ tures. It is not yet clear, however, whether the critical controlling tion to H. Haskin) nor were outbreaks in North Carolina in 1988 temperatures occur in the winter or summer, or both (Ford and (M. Marshall, North Carolina Division of Marine Fisheries, per­ Tripp 1992). sonal communication, 1989). Also relevant is that grounds on the It is much more difficult to evaluate evidence of possible in­ Delaware side of Delaware Bay, heavily planted with Chinco­ troduction of MSX disease because the complete life cycle and teague Bay seed between 1953 and 1957, did not experience losses means of transmission of its etiologic agent, Haplosporidium nel­ due to MSX disease until the spring of 1958, a full year after soni, are not known. Nevertheless, there is information available epizootic mortalities had begun on the New Jersey side (N. Jef­ of use to those making decisions about po~sible introduction of this fries, Sr., personal communication, 1989). disease into non endemic areas. The link between movement of infected oysters and outbreaks After the ftrst outbreaks of MSX disease in Delaware and Ches­ of MSX disease is thus quite tenuous compared to that for P. apeake Bays in the late 1950s, considerable effort was put into marin us. In addition to its introduction into Delaware Bay in the elucidating the life cycle of H. nelsoni and in trying to transmit the 1950s, the latter has been spread around Chesapeake Bay by trans­ parasite experimentally. None of these experiments resulted in plants of infected seed (E. Burreson, personal communication in transmission, but most of them have involved the plasmodial stage (Andrews 1988)). In contrast, there are as many examples of H. of the parasite (Canzonier 1968, 1974). Few have used the spore nelsoni appearing in areas with no known history of introductions stage (Andrews 1979), which is most likely involved in transmis­ or transfers as there are cases with connections, although many sion, but which has been reported only rarely in oysters. Most undocumented transfers of oysters are undoubtedly made. researchers have concluded that another host may be involved in the life cycle (Farley 1965, Andrews 1968, Ford and Haskin 1982, 2. Can the Pathogens bl! Transmitted in Hatchery-produced Larvae or Haskin and Andrews 1988). Recently, Barber et al. (1991) have Smull Seed? found that sporulation may occur regularly in spat (oysters under a year of age) if infections reach the advanced stage. Andrews The ICES measures designed to reduce risk of disease intro­ ( 1979) also reported heavy spore production in a single group of duction involve the quarantine of broodstock. A recent report sug- 66 MOLLUSCAN INTRODUCfiOKS Al'iD TRANSFERS gested that a parasite of bay , , cites a case involving the presumed introduction of a sacculinid which was identified as P. karlssoni and was reported to occur in parasite (Loxothylacus panopaei) into Chesapeake Bay. This par­ scallop eggs, might undergo vertical transmission (McGladdery et asite, which devastated two species of mud crab in the mid 1960s, a!. 1991). Perkinsus marinus has never been reported to occur in may have been introduced in shipments of oysters from the Gulf of oyster eggs, although it does ~urvive intracellularly in hemocytes. Mexico brought "to Virginia for shucking at waterside plants Greater concern exists that larvae could become infected by the where shells and wastes were discarded near native oy~ter beds.'' adults during spawning in a hatchery. Although there is no abso­ We do know that P. marinus can be very easily transmitted in lute reason that larvae could not become infected by P. marin us in a laboratory simply by water splashing from a tank holding in­ this manner, it has never been reported and there are a number of fected animals (W. 1. Canzonier, personal communication, 1989) biological reasons why it is unlikely. The presumed site of infec­ and that any stage is infective (Andrews 1988). We also know that tion by P. marinus is the digestive tract (Mackin 1951) and the oysters with high levels of P. marinus appear glassy and emaci­ spawning stock would normally be removed from contact with the ated, and might well be discarded (overboard) by shuckers, as embryos long before the latter developed into veligers (18-24 hr) would infected gapers (dead oysters). On the other hand, injection with the capacity to feed. If viable infective particles were dis­ experiments with measured numbers of P. marin us cells indicate charged during spawning and survived in sufficient numbers until that a threshold inoculum is required to initiate infection and cause the larvae were capable of ingesting them, the larvae theoretically mortality (Mackin 1962). In the laboratory, a relatively small could become infected. There is, however, no reason to believe number of infective cells may initiate an epizootic because of the that lightly infected oysters would discharge P. marinus cells dur­ limited volume of water and the high density of oysters involved ing spawning, and heavily infected individuals will not spawn making the chance that each infective particle will come into con­ because they do not produce gametes (Mackin 1962). Thus, the tact with an oyster very high. If wastes are disposed of in an areas chances of larval contamination, although possible, are extremely with restricted circulation where oysters are present nearby (within slight. Hatchery operators could minimize the possibility by thor­ several hundred yards) in relatively large numbers, the chance of oughly cleaning the shells of parent stock, including placing the transmission is high. That possibility would be reduced if infective oy~ters in dilute (0.3%) hypochlorite solution for 15-20 minutes to stages from wastes were diluted before they contact a host, either kill epibionts that might harbor P. marinus cells and removing because of flushing patterns or distances of oysters from the dis­ parent oysters from spawning container~ as soon as they have posal site. Andrews (1988) found that isolation of oysters by as spawned. As a further safeguard, broodstock could be screened for little as 15 m substantially delayed the transmission of P. marin us, systemic P. marinus by non-destructive blood diagnosis (A. Far­ although transmission over longer distances is possible. ley, Oxford Cooperative Laboratory, personal communication Between 1986 and 1989, when local oysters were scarce, sev­ 1989; Gauthier and Fisher 1990) before selecting spawners. eral shucking plants bordering the Maurice River, a New Jersey Because of the life cycle and transmission considerations al­ tributary of Delaware Bay, processed oysters from the Gulf of ready discussed, there is no danger that larvae could acquire H. Mexico and the Chesapeake Bay, where P. marinus was enzootic. nelsoni from infected broodstock. The parasite has never been During the initial stages of the 1990 epizootic in Delaware Bay, observed in eggs and, as a matter of fact, is typically extracellular. very high prevalences of P. marinus were found in oysters grow­ Spat, which might be carrying spores capable of producing infec­ ing in the river adjacent to the shucking houses. We do not think tive stages, are hardly likely to be chosen as broodstock, and that P. marinu.1· was necessarily re-introduced into Delaware Bay oyster-to-oyster infection does not occur from plasmodia. As with by this means because of other apparent infection foci in the Bay P. murinus, cleaning of shells (to remove potential alternate or and along the New Jersey Atlantic coast (see above), but the intermediate hosts) and screening for the presence of systemic H. intensity of the early outbreak near the shucking houses suggests nelsoni, would be added ~afety measures. that a combination of waste disposal and suitable temperature may Juvenile oysters (spat) can become infected with either patho­ have stimulated a localized epizootic in the river. gen, but because they "pump" much smaller volumes of water The proximity of processing plants to oyster populations and than do adult oysters, their chances of encountering either of these the characteristics of the water into which they are discharging water-borne parasites is considerably reduced. If the juveniles are wastes should be considered in assessing the potential for trans­ maintained in an on-shore nursery where water flow is restricted mission of P. marinus in this manner, but because of the extremely compared to the field, their chances of becoming infected would contagious nature of this disease, processors should be encouraged be further reduced. The potential for seed being infected is thus a not to dispose of fresh shucking wastes overboard in non-enzootic combination of their size, the length of time they have been ''ex­ areas if oyster populations exist nearby. Additionally, appropriate posed," and the concentration of infective particles in the water means for treating P. marinus-contaminated wastes should be in­ surrounding them. We cannot presently measure the abundance of vestigated (Goggin et al. 1990). either pathogen in water samples, but inferences as to relative Transmis~ion of P. marinus via the movement of shells from abundance can be made based on the history of infections in the shucked infected oysters is less likely, but probably not impossi­ immediate area. ble. Andrews and Hewatt (1957) reported survival of P. marinus (i.e., it could be cultured in fluid thioglycollate) after infected 3. Can the Pathogens be Spread through Overboard Disposal of tissues had been frozen or dried, although the authors did not Contamitwted Meats, Shells, or Other Wmtes by Processors, Dealers, attempt transmission with material that had been subjected to Reswurants, or Consumers? freezing or drying. Also to be considered is the possibility that carriers such as the parasitic snail Boonea impressa (White et aL There is no conclusive evidence of which I am aware that any 1987), crabs, oyster drills, polychaetes, etc. (Table 1) might sur­ molluscan disease-causing organism has been transmitted through vive for extended periods in the interior of shell piles, particularly shucking wastes or shell transplants; however, Andrews ( 1980) during cool weather, and infect oysters when reintroduced into the DISEASE TRANSMISSION THROUGH INTRODUCED MOLLUSCS 67

TABLE I. 1963, White et al. 1987). Most, however, appear to carry related, Organisms in which Perldnsus marinus, or Perldnsus-like cells but not identical, organisms. Ray (1954) and Andrews (1955) culturable in fluid thloglycollate, have been identified. reported finding them in many species, but always in very low abundance. Attempts at cross~species transmission between oys­ ters and Mercenaria mercenaria (Linnaeus, 1758) Macoma bal­ Transmission thica (Linnaeus, 1758), and Mya arenaria (Linnaeus, 1758), by to Oysters CeUs Found Perkinsus-Like direct inoculation or feeding, failed in nearly all cases (Ray 1954, Demonstrated inion Scavengers Cells in BivaJves Andrews and Hewatt 1957). The same techniques easily transmit Boonea impressaw Opsanus tauH Mercenaria merceMriif'­ the parasite between oysters. Apparent invasion of M. mercenaria Gobiosoma bosciH Clwsmodes bosquianul' Macoma balthicaA tissues did occur at the site of injection, but no parasites spread Ostrea lurida(UJR Urosalpinx cinereaH,c M. phenax" from there. Several M. arenaria did become infected when in­ Neopanope texanaH M. tentaA jected with material from infected oysters (Ray 1954). Presently Rhithropanopeus hanisi1

A (Andrews 1955) 5. Are There Methods for Treating Small Lots of0y$ters (Broodstock, c (Christensen 1956) Larvae, SmaU Seed) to Eliminate Pathogens? H (Hoese 1963) M (McGJaddery eta!. 1991) Both P. marinus and H. nelsoni are found primarily in the R (Ray 1954) higher salinity portions of estuaries, where salinities are between (UJR (Ray ]954) 15 and 30 parts per thousand (ppt). At temperatures of 20°C or w (White et a!. 1987) more it has been shown that H. nelsoni can be eliminated from infected oysters if they are submerged for two weeks at salinities water. It is unlikely that more than a few organism would survive below lO ppt (Ford 1985). The use of low-salinity immersion to for long in this environment and, further, Andrews (1988) con­ clear H. nelsoni infections from broodstock or seed would appear siders that scavengers do not carry sufficient infective stages of P. to be a very inexpensive and practical means for reducing the risk mnrinus to make ''major contribution to the high dosage necessary of transmitting this parasite through aquacultural practices. Addi­ tional research is needed, OOwever, to pinpoint the exact time­ to produce infections." The concerns discussed above apply also to overboard disposal temperature-salinity requirements needed to assure complete elim­ of infected oysters, or their remains, by restaurants, seafood mar­ ination of the parasite. kets, or consumers. Such disposal is practically impossible to pre­ P. marinus cannot be cleared under similar conditions as it is vent except by education, but is likely to introduce only a small much more tolerant of low salinity than is H. nelsoni (Andrews amount of infective material. and Ray 1988). There are currently no anti-protozoal agents Transmission of H. nelsoni by this means is far less likely than known to be effective and practical in ridding oysters of P. mnri­ for P. marinus. As mentioned already, H. nelsoni has proved nus. Ray (1966) demonstrated that exposure of infected oysters to impossible to transmit in the laboratory, whereas special care must cycloheximide reduced disease levels, but when the "treatment" be taken to prevent contamination by P. marinus. We are confi­ was stopped, even after 164 days, the parasite recovered and 'lgain dent that plasmodial stages of H. nelsoni, even when injected or started causing deaths. transplanted into recipient oysters, cannot initiate infections (Can­ SUMMARY AND RECOMMENDATIONS zanier 1968, 1974; Ford unpublished). Thus overboard disposal of whole animals or tissues infected with only this stage (which is by Catastrophic losses caused by oyster pathogens over the last far the most common fonn in oysters) could not be a source of several decades have justifiably frightened persons concerned with infective stages for oysters. The fact that most processors, distrib­ shellfish transfers. In attempting to prevent the spread of disease, utors, and consumers would not be dealing with spat minimizes most individuals, particularly regulators, are extremely conserva­ the potential for distributing spore stages from young oysters; on tive. While caution is appropriate, over-reactions, sometime~ ap­ the other hand, shuckers would not open spat on shells of market­ proaching paranoia, can result if those responsible are ignorant of, sized oysters and they might be discarded overboard. or are reluctant to emphasize, biological knowledge in their deci­ sion-making. 4. Can the Pathogen$ be Tran$milted to and from Other Specie$ It is not sufficient to conclude that a disease agent has been Perkinsus-like organisms (i.e., those that culture in fluid thio­ introduced through transfer of the host species simply because it glycollate) have been found in many North American species other has been newly discovered in a particular location (or something than oysters (Table I). Some of these species, like the gastropod resembling a known pathogen has been found in tissue sections or Boonea impressa, carry P. mnrinus that can infect oysters (Hoese culture media). Even when mortalities associated with a parasite 68 MOLLUSCAN INTRODUCTIONS AND TRANSFERS occur suddenly after transfer of host species, there may be alter­ 3. What is known about environmental constraints, especially nate explanations. For instance, review of the vast numbers of salinity and temperature? Is it likely that the pathogen could species moved about the world in ballast water or on the bottom of su!Vive and/or cause damage in the new environment? Per­ ships (Carleton, this volume?) suggests that some potenlial intro­ kinsus murinus was introduced in tremendous quantities ductions may be well out of the imme

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