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Biological control of marine pests.


Some species, often those that are introduced from elsewhere, are "pests" to the extent that efforts have been made to control them in terrestrial and freshwater environments. Prior to the advent of chemical pesticides, use of natural enemies of these pests was an important area of applied research, particularly in agriculture. We now recognize the unfortunate environmental damage caused by some of these pesticides and we have repeatedly witnessed the development of genetic resistance of pests. Hence, interest in biological control has been renewed. We now have an extensive body of practical and theoretical knowledge concerning biological control, and a track record that includes many successful applications interspersed with some notable failures. Biological control for these pest problems has involved the deployment of herbivores, predators, parasites, or diseases.

In marine environments, introductions are also common and damaging (Carlton 1987, 1989, Zibrowius 1991), but efforts at pest control have been limited to conventional pesticides. Recent studies on mechanisms of transport and establishment indicate that ballast water, as a larval conveyance, is the most important means of dissemination (Carlton 1985, 1989). Since most such introductions arrive as larvae, they generally come free of natural enemies (parasitic castrators, specialized predators, and pathogens of adults) that might normally control their abundance in their native regions (Lafferty and Kuris 1994). The resultant, extremely high population densities attained by alien species is what usually leads to economic damage (Nichols et al. 1990).

There have been several recent calls for research on biological control of marine pests (Miller 1985, Moyle 1991, Buttermore et al. 1994, Lafferty and Kuris 1994). Australia's CSIRO (Commonwealth Scientific and Industrial Research Organization) Division of Fisheries has recently taken the lead in marine pest problems by establishing the Centre for Research on Introduced Marine Pests (CRIMP) in Hobart, Tasmania. CRIMP plans a pro-active approach to marine pests in the style of Australia's historically aggressive and innovative use of terrestrial biological control. To stimulate further dialogue on control of marine pests, particularly introduced species, we first briefly consider some marine pests in U.S. waters. We illustrate the highly diverse nature of these pests and focus on the type of damage they cause and on considerations for their control. The heart of our paper contrasts the general nature of marine vs. terrestrial pest control, and we provide some guidelines for the adaptation of existing biological control strategies to the unique challenges of the marine environment. Finally, we present a case study of the introduced European green crab, Carcinus maenas. Since this has been recognized as a serious pest and is a well-studied animal, we outline a general approach to its control.


The introduction of marine pests to new habitats is as old as nautical experience. Recall that Sir Francis Drake had to rebuild the Golden Hind in California in 1579, probably because it was riddled with (mostly) Atlantic shipworms. It is quite possible that this first ship served to introduce a marine pest to California. So it is not surprising that introduced species such as Mytilus galloprovincialis and the western Atlantic populations of the European green crab have planted themselves so firmly on our shores that most ecologists accept them, without concern, as a naturalized part of the biota. Many other introductions, particularly polychaetes and amphipods, are cryptic and have been considered species with natural cosmopolitan distributions (Chapman 1988). The following subsections describe and discuss a series of well-known marine pests.

Red and brown tides. - Red tides result from blooms of marine dinoflagellates. For many years, these dinoflagellates have been considered cosmopolitan, and the increasing frequency of blooms a result of coastal eutrophication. Now it appears that some species have been transported by ballast water (Hallegraeff 1993) or with shellfish for mariculture (Shumway 1989). Red tides can cause massive fish mortality, with consequent pollution of beaches and losses to fisheries. When algal toxins build up in edible shellfish, humans can die of paralytic shellfish poisoning. Massive brown-tide blooms caused by chrysophytes have also caused heavy mortalities of invertebrates and eel grass beds and have severely impacted scallop fisheries. Algal consumers, such as planktonic ciliates and heterotrophic dinoflagellates, might act as control agents (Jeong and Latz 1994). Viral outbreaks have been implicated as important controls for algal blooms and offer potential for prevention or attenuation of such blooms (Sieburth et al. 1988, Suttle et al. 1990, Milligan and Cosper 1994).

Red algae. - Two species of introduced red algae affect community structure of Hawaiian coral reefs. Acanthophora spicifera came to Hawaii in the 1950s (Doty 1961), possibly attached to ships or with aquarium fishes. A highly adaptable alga, it became well established and is currently the most widespread exotic alga in Hawaii (Russell 1992). Hypnea musciformis invaded Hawaii in 1974 (Abbott 1987) and became a dominant species at several reefs on Oahu by 1977. Both exotic algae have rapid growth rates, high reproductive capacities, and compete with the native Hypnea cervicornis (A. spicifera also competes with the native Laurencia nidifica). Both species resist herbivory, which may complicate the use of grazers as natural enemies. The high productivity of these introduced species on some reefs raises drag and causes the eventual loss of reef material (Russell 1992). On a positive note, both species are now significant food sources for globally endangered green sea turtles, Chelonia mydas (Russell and Balazs 1994).

Jellyfish. - Although it is apparently native, the summer jellyfish, Chrysaora quinquecirrha, becomes periodically abundant in the Chesapeake Bay region, reaching pest proportions. Its relatively powerful stinging nematocysts are responsible for intense burning reactions among swimmers and those who must work around the water. Its presence has a negative but unmeasured impact on tourism in that area, as swimming is often avoided. Jellyfish have sometimes become so abundant that they clog nets and block water-intake pipes (Ruppert and Fox 1988). Hyperiid amphipods might be possible control agents. These generally host-specific amphipods act as parasitoids, parasites, or parasitic castrators on gelatinous zooplankton (Kuris 1974). However, biological control in this case may have risks. In Chesapeake Bay, C. quinquecirrha preys on, and may control, the ctenophore Mnemiopsis leidyi (Feigenbaum and Kelly 1984). The cascading release of M. leidyi from predation could lead to the sorts of problems that occur now in the Black Sea, where M. leidyi was introduced in 1982 (Vinogradov et al. 1989). Achieving incredible densities there, it has altered the food chain and led to the collapse of fisheries by consuming a large proportion of the zooplankton (Harbison and Volovik 1994). Ironically, two jellyfish from the Black Sea have recently invaded San Francisco Bay (Mills and Sommer 1995).

Nemerteans. - Egg predators in the genera Carcinonemetres and Pseudocarcinonemertes can cause very substantial mortality of eggs in the clutches of Dungeness crabs (Cancer magister), red king crabs (Paralithodes camtschatica), and American lobsters (Homarus americanus) (reviewed in Kuris [1991]). This mortality is sometimes so substantial that it has been implicated as the cause of the non-recovery of the Central California Dungeness crab fishery and the collapse of some red king crab stocks (Hobbs and Botsford 1988), Kuris et al. 1991). Models of brood mortality and parasitic castration in crustacean fisheries suggest that adaptive management strategies, such as intensive fishing of both sexes in heavily infected localities, may be able to break the threshold of nemertean transmission without reducing yield to the fishery (Kuris and Lafferty 1992). This represents an instance where the ability to fish a pest (in this case, along with its host) might lead to its removal.

Snails. - Snails introduced with oyster culture have been quite successful in bays and estuaries. The oyster drill, Urosalpinx cinerea, has sometimes become an established pest even where introduced oyster culture has failed (Carlton 1975). In San Francisco Bay, Ilynassa obsoleta (from the East Coast) is able to out-compete the native mud snail, Cerithidea californica, by preying on its egg masses (Race 1982). The Japanese snail Battilaria attramentaria may also be competitively superior to C. californica (Whitlatch and Obrebski 1980; S. McDermott, unpublished manuscript). Interestingly, the latter two introduced species are castrated by native larval trematodes (K. D. Lafferty, personal observation). Unlike the oyster drill, the primary consequence of these grazers is the replacement of a functionally similar competitor. Thus, alterations to the ecosystem are likely to be relatively subtle.

Bivalves. - The oyster industry has paid a price for its frequent and inadequately monitored spread of new species for culture. Introduced oyster diseases have caused severe mortality in several new culture areas (Farley 1992). The Asian clam, Potamocorbula amurensis, invaded San Francisco Bay and became abundant in the late 1980s, reaching phenomenal densities ([greater than] 10 000 individuals/[m.sup.2]) (Carlton et al. 1990). It may cause major alterations in this estuarine system, including displacing other suspension and filter feeders, altering diets of fish and birds, reducing phytoplankton, and altering substrate stabilization. Another bivalve, the brown mussel (Perna perna) from South Africa, has appeared in large numbers on the Texas coast where it has crowded out other organisms, becoming the dominant organism on pier pilings (Hicks and Tunnell 1993). As most of the hard-substrate habitat (piers, breakwaters, jetties) in Texas is not natural, it might not seriously affect native fauna. Mussels, in general, may increase the drag on subsurface pilings to the extent that they must be removed (the same is true of a wide range of fouling organisms on ships).

Sea urchins. - The destructive impact of sea urchins, Strongylocentrotus spp., on kelp forests was a major, inshore, marine environmental concern from the 1950s to the 1970s. Dense aggregations of urchins ([greater than]100 individuals/[m.sup.2]), termed "barrens," prevented the re-colonization of kelp (Ebeling et al. 1985). A protozoan parasite, Paramoeba invadens, was recommended and tested in the laboratory as a biological control agent because natural outbreaks of this ameba greatly reduced sea urchin abundance (Jones 1985, Jones and Scheibling 1985, Miller 1985). Fatal to this control scheme was the emergence of sea urchins as a major U.S. fishery in the 1980s (with the highest landings value among California fisheries, Parker and Kalvass 1992). Not surprisingly, there are now no control efforts against sea urchins. Instead, research efforts aim to protect dwindling stocks.

Polychaetes. - Spionid polychaete worms in the genus Polydora are shell borers, inhabiting many commercially important marine molluscs (Lauckner 1983). High infestations inhibit normal growth of the host, weaken the shell, and can kill the animal. Classification as a "pest" dates back to 1940, following large mortalities of east coast oysters due to Polydora websteri (Lunz 1940, 1941, Loosanoff and Engle 1943). The worm is likely native and is found naturally at low densities, but mariculture apparently provides host densities conducive for high worm densities (Wargo and Ford 1993). In addition, substantial damage to mussels (Kent 1979, 1981) and scallops (Evans 1969, Bergman et al. 1981, Mori et al. 1985) has been attributed to P. websteri and P. ligni. Infestations of abalone (Blake and Evans 1973, Hahn 1989) and other intertidal gastropods (Blake 1971, Blake and Evans 1973) also occur. Because worms are prevalent in mariculture operations, some control methods exist (reviewed by Lauckner [1983]). Most control is chemical, killing many existing individuals but allowing rapid re-infestation. In 1993 an undescribed species of sabellid polychaete was recognized as the causative agent of marked shell deformations and cessation of growth in cultured abalone in California. The worm is a South African species (K. Fitzhugh and G. Rouse, unpublished manuscript). Outflow from culture facilities and release of infested abalone in outplanting programs threaten to introduce this pest into California waters (A. Kuris, C. Culver, and K. Fitzhugh, unpublished manuscript).

Burrowing shrimps. - The native ghost shrimp (Callianassa californiensis) and mud shrimp (Upogebia pugettensis) disturb and suspend sediments in bays and estuaries, negatively affecting some filter-feeding organisms. The oyster industry in Washington State initiated chemical control with carbaryl to reduce bioturbation by shrimps. Since 1990 the Burrowing Shrimp Committee has been developing an integrated pest management plan. The Committee ranked biological control agents second among research priority areas and specifically recommended the use of oyster shell as refuge for juvenile Dungeness crab that prey on the shrimps (B. Dumbauld, personal communication). Although, as yet, there has been no search for potential parasites and pathogens of the shrimps, research on natural enemies continues while Washington and Oregon try to develop non-chemical means of control. Cooperation with the mudshrimp bait fishery might also help reduce densities.

Crabs. - Several species of crab are pests or potential pests. The European green crab, Carcinus maenas, became established in California around 1990 and has received much attention. We will discuss it at length below (see A case study: the green crab). McDermott (1991) noticed a shore crab from the western Pacific, Hemigrapsus sanguineus, in New Jersey in 1988. It presently ranges from at least Chesapeake Bay to Cape Cod. Its widely dispersing larval stages may help expand its range further. It is difficult to predict what impact H. sanguineus will have. It lives higher up in the intertidal than other east coast crabs and, therefore, may not compete much with the native fauna. An even more recently observed introduction (1994) is the Chinese mitten crab (Eriocheir japonicus) into San Francisco Bay and the Sacramento-San Joaquin Delta region. This species has clear potential for damage. It burrows into banks and could further weaken levees in the Delta. Mitten crabs invaded Germany in the 1920s where they caused substantial erosion in the Lower Rhine Valley. The Germans eventually extirpated them with an intensive trapping program. An additional concern surrounding the introduction of the Chinese mitten crab in California is that it is an important second intermediate host for Oriental lung fluke (Paragonimus westermani), a trematode that causes substantial pathology in Asia. Since many infected people from Asia have already immigrated to California (Burton et al. 1982), the arrival of E. japonicus closes a further link in the life cycle of the lung fluke. If the mitten crab becomes abundant, it may also serve as a suitable host for native North American lung flukes P. kellicotti and P. mexicanus (Pachucki et al. 1984, Markell et al. 1992: 216), increasing the potential for zoonoses (infection of humans by normally sylvatic parasites).

Tunicates. - Following the regrettable release of the compound tunicate, Botrylloides sandiegensis, by a developmental biologist in the vicinity of Woods Hole, Massachusetts, this orange tunicate, known now as Freeman's blight, has spread along the southern New England coast, coating rocks, piers, and other hard substrates with a layer of orange gelatinous slime. It has replaced other encrusting organisms and is a nuisance in harbors. No attempt to control this species has been made and it is likely to continue its rapid spread to the south.

Fishes. - The yellowfin goby, Acanthogobius flavimanus, is an estuarine fish that turned up in the lower Sacramento Delta region of California around 1963 (Brittan et al. 1970). Although it probably invaded as a result of the transport of oysters from Japan, it could also have arrived in ballast water or as a discard from live shipments meant for food (McGinnis 1984). The goby has successfully dispersed from estuary to estuary in a southward expansion along the coast. It grows to large sizes for a goby ([greater than]25 cm) and feeds on invertebrates and small fish. This is of concern in areas where it overlaps with the federally endangered tidewater goby (Lafferty et al. 1996). Yellowfin gobies are considered a delicacy in Japan and, although difficult to seine, are relatively easy to trap (McGinnis 1984). Encouraging a trap fishery for Asian American markets or export might be one method for control.


The absence of studies on the control of introduced marine and estuarine pests approaches fatalism. Occasional forlorn cries for solutions (e.g., MacPhail et al. 1955) have yielded little response from researchers and management agencies. This is odd, considering that the use of natural enemies in classical biological control is a robust approach with a long track record of remarkable successes in agriculture. Since the successful scientific application of biological control to an insect pest in the 1880s (the cottony cushion scale in California by the Vidalia beetle and parasitoid wasps), its use against many insect pests has become well established and analyzed. Clearly, one of the most efficient approaches to the control of marine pests is to carefully examine the use of biological control against terrestrial insect pests for appropriate analogous tactics. A 100-yr head start provides a vast source of insight. With similarities and differences more clearly in view, we can then use the terrestrial experience as an ample source of guidance for the control of marine pests ([ILLUSTRATION FOR FIGURE 1 OMITTED] for a proposed general strategy).

Certain biological and economic features made the use of natural enemies highly desirable in terrestrial systems. Firstly, successful natural enemies are able to either track pest populations or to locate new pest populations as they eradicate others. Secondly, because natural enemies can evolve, they largely evade development of resistance on the part of the pests (by co-evolving). Thirdly, when well chosen, and carefully tested on native hosts, they usually have sufficient specificity to be environmentally safe. When successful, they provide either a long-term or a permanent solution to a pest problem. Thus, use of natural enemies will generally produce a low-cost solution to pest problems.

The underlying question for the biological control of an introduced species is, "What controlled its abundance in its native region and why is it a problem in its introduced locale if it is not a problem where it is native?" The extensive practical success of the insect pest biological-control approach demonstrates how to answer these questions. Natural enemies generally control insect populations and these enemies are more likely to be available in the native regions of the pests (Huffaker 1971, DeBach 1974, Kuris and Norton, 1985). In essence, biological control strategies are seemingly paradoxical: seek the solution where there may be no apparent problem. Therefore, to use natural enemies as a biological control, it is clearly necessary to survey introduced populations for parasites and predators and compare them with the types and abundance of such natural enemies where the pest is native. Most of the successfully introduced natural enemies that achieve good (economic) control in terrestrial systems without deleterious side effects are parasitoids. Parasitoids are like parasites in that they permanently feed on a single host, but they are like predators in that a single parasitoid will always ultimately kill its host. Pathology is not intensity dependent; more parasitoids do not cause more damage than does a sole parasitoid (Kuris 1974).

Several criteria define a good biological control agent (Kuris 1973, DeBach 1974). The agent should respond numerically to host outbreaks. At low host densities it should either be able to find the host and persist so that pest outbreaks do not occur after pest density drops, or be able to rapidly and efficiently locate pest patches so that outbreaks do not occur (although some have argued that this overemphasizes the importance of stabilizing factors at local scales [Murdoch et al. 1985, Waage 1990]). The agent should also have the physiological capacity to survive in the target area. The ability to culture the biological control agent is important for implementing a control strategy. Most importantly, biological control agents should be host specific so that they do not damage valued native organisms.

Special considerations in marine environments

Marine systems have some important features that contrast with terrestrial biological control paradigms and require special consideration. To develop a protocol for the biological control of a marine pest, it is first necessary to precisely consider what qualifies as "control." Eradication is certainly not possible once a pest has become well established. The potential to use natural enemies against marine pests enjoys, in principle, a significant advantage compared to their use against terrestrial agricultural pests. In agriculture, farmers must cut pest populations to very low levels to maximize the economic yield of their crops. For many crops, merely maximizing tonnage is insufficient; the cosmetic condition of the produce is also important. In contrast, for marine pests, it seems probable that it will not be economically nor culturally necessary to achieve such an exquisite degree of control. Damage due to marine pests occurs at outbreak densities. There is usually no reason to reduce pest populations to very low levels, and relatively modest reductions in pest abundance will usually provide a successful outcome.

Another important difference between terrestrial and marine systems is the general nature of recruitment (Gaines and Lafferty 1995). In terrestrial habitats, recruitment of most species is relatively closed; offspring mostly live in the vicinity of the parents. Recruitment to a distant suitable patch is a rarity, and biological control using natural enemies is effective because control agents either reduce and persist in local patches or can disperse and efficiently locate more distant pest patches (Murdoch et al. 1985). In marine environments recruitment is generally open; planktonic larval stages disperse widely, and offspring rarely settle and live near their parents. Oceanic and local abiotic factors drive recruitment, and numerical responses to a locally high pest density may not occur. Biological control may not have been sought because actions taken against adults at a particular location are intuitively deemed to have no impact on future recruitment. Approaches aimed at reducing the reproductive output of a pest population with parasitic castrators or egg predators might appear even more futile. In this case, efforts would neither reduce pest densities nor prevent subsequent recruitment. However, these limitations are scale-dependent phenomena that require a new frame of reference. In other words, the perspective of terrestrial crop damage or disease transmission with localized impacts has traditionally dominated pest control, in both theory and practice. To devise and implement biological control in marine systems requires a vision of a much broader spatial scale. Therefore, large-scale institutional efforts may be needed for success.

Control agents for marine systems include parasitic castrators as well as predators, competitors, and diseases. Parasitic castrators are more typical of marine systems than parasitoids and deserve special attention. Unfortunately, in comparison with insect parasitoids (see Murdoch and Briggs 1996), there has been little attention paid to the ability of parasitic castrators to control host populations. Like parasitoids, parasitic castrators do not cause intensity-dependent pathology (Kuris 1974); a single parasitic castrator blocks the reproductive capability of its host. Also, like the parasitoid-infected host, the reproductive potential of the parasitically castrated host is nil. However, the castrated host continues to exert intraspecific competitive effects against unparasitized individuals (Lafferty 1993). It also continues to be a pest. Other differences of parasitic castrators include an inability to attack more than one host and limited abilities to search out dense host patches. Kuris (1974) postulated that, analogous to parasitoids, parasitic castrators may be able to control host populations. Analytical models (Blower and Roughgarden 1987, Lafferty 1991, Kuris and Lafferty 1992, Gaines and Lafferty 1995) and experimental evidence from field studies (Blower and Roughgarden 1989, Lafferty 1993) support this. Other effective control agents include some predators (Van den Bosch et al. 1982, Hofkin et al. 1991) and, for control of freshwater snails, competitors (Jobin et al. 1977, Nassi et al. 1979, Pointier 1983, Pointier et al. 1991).

A potential disadvantage when using natural enemies in marine environments compared to their use in terrestrial counterparts concerns safety. It would seem that our society cares little about native insects such as aphids or scale. In contrast, most people would consider a natural enemy used against a marine pest, such as the green crab, to be unsafe if it were to significantly reduce Dungeness crab populations, even if the natural enemy was effective against the targeted pest. Thus, environmental safety of natural enemies used against marine pests must meet a high safety threshold to conserve our native fauna.

In addition to biological control in its classic mode (introducing an exotic natural enemy to control an exotic pest), we also consider aspects of control suitable for an integrated pest management approach. These may include: pesticides, mechanical removal, fisheries, and the enhancement of native natural enemies [ILLUSTRATION FOR FIGURE 1 OMITTED]. Chemical controls (in the form the anti-fouling agent tributyltin or penta-impregnated pressure-treated pilings) are effective but, like many pesticides used on terrestrial pests, have collateral effects on non-target species. Mechanical removal of pests has been used to clear fouling organisms from offshore oil platforms. In recent years, it was realized that the fouling community was dominated by mussels, an increasingly valuable seafood commodity. A substantial fishery has replaced mechanical removal (R. Meek, personal communication). Enhancing native predators, such as increasing the abundance of Dungeness crabs to control burrowing shrimps, is a relatively safe form of biological control because it does not involve introducing exotic control agents. We next provide a case study that recommends a combination of introducing a parasite and initiating a fishery.


The European green crab makes an interesting test case because it is likely to prove to be a truly bad introduction. Establishing in San Francisco Bay in 1990 (Cohen et al. 1995), it is euryhaline and extends up estuaries to low-salinity conditions (1.4%) (Williams 1984). On the West Coast the green crab lives in protected bays, on soft bottoms, from the intertidal zone to 6 m deep. On the Atlantic coast, and where native in Europe, it also occurs on semi-protected rocky outer coasts. Since its discovery, Carcinus maenas has spread north to Bolinas Lagoon, Drake's Estero, Tomales Bay, Bodega Harbor, and Humboldt Bay and south to Elkhorn Slough (T. Carlton, A. Cohen, E. Grosholz, personal communications). It now encompasses a latitudinal range of over 500 km in California. As it has also invaded South Africa and Australia (mainland and Tasmania) international cooperation is likely to aid the development of control over the next several years.

The green crab is a well-studied species. The literature of the past 25 yr has emphasized the feeding habits of the green crab as this provides the most direct evidence of its economic impact on shellfish prey (Glude 1955, Moulton and Gustafson 1956, Ropes 1968, Elner 1981, Le Roux et al. 1990). In their native range, green crabs are voracious predators of many benthic invertebrates (Scherer and Reise 1981, Klein Breteler 1983, Sanchez-Salazar et al. 1987). For example, in Britain they each consume up to forty 15-mm-long cockles per day. After its introduction to the western Atlantic, the green crab had a devastating impact on shellfish fisheries. The demise of the softshell clam fishery in northern New England and Nova Scotia is associated with Carcinus maenas (Glude 1955, Moulton and Gustafson 1956, Ropes 1968). They have destroyed artificial shellfish beds and consumed large numbers of young oysters and Cancer crabs (MacPhail et al. 1955, Ropes 1968, Elner 1981).

Virtually all groups listed by Nichols and Thompson (1985) as the predominant macrohenthic species (introduced and native) of South San Francisco Bay are known prey types for the green crab (Ropes 1968). It is unlikely that native shellfish will exhibit useful defensive preadaptations to this voracious generalist, eurytopic, euryhaline predator. The green crab is likely to alter the distribution, abundance, and species interactions of intertidal and subtidal faunas, both native and non-native, wild and cultured (Cohen et al. 1995, Grosholz and Ruiz 1995).

Based on the history of Carcinus maenas after its introduction elsewhere (Ropes 1968, Le Roux et al. 1990), the crab is likely to devastate the intertidal and subtidal beds of the softshell clam, Mya arenaria, the Japanese cockle, Tapes japonica, several Macoma species, and the marsh mussel Geukensia demissa in San Francisco. If population densities increase in the substantial shellfish mariculture industry of nearby Tomales Bay and Drakes Estero, it may heavily impact young shellfish. So far, measures taken to reduce predation (mesh enclosures) seem to have been successful for clam and oyster seeding operations in Tomales Bay (T. Sawyer, personal communication).

Although predicting the ultimate range of the green crab on the Pacific Coast is speculative, temperature regimes seem suitable from southern California north to Puget Sound. The spread is mostly likely to come in spurts (Grosholz 1996). The large volume of commercial shipping along the Pacific Coast is very likely to introduce green crabs in ballast water to most of its major harbors. This would threaten the nation's largest oyster-rearing industry in Washington state. Green crabs could also reduce commercial stocks of Dungeness crab in Washington and Oregon and of rock crabs to the south. Since Dungeness crabs use bays for nursery areas, juveniles would be exposed to both competition for a similar food base of small epibenthic [TABULAR DATA FOR TABLE 1 OMITTED] invertebrates, and direct predation by green crabs (Grosholz and Ruiz 1995).

Although the impact of the green crab on West Coast fisheries is potentially very considerable, there is, as yet, no damage assessment. Potentially, the green crab introduction could cause direct losses of all or part of the oyster, mussel, and clam mariculture industries in Tomales Bay and Drakes Estero, a 1993 harvest value of about U.S.$2.5 x [10.sup.6], as well as losses to the Dungeness fishery, and impact on bait fisheries and sports fisheries (Table 1). Beyond this direct economic impact, the ability of C. maenas to burrow extensively in marshes (Berill and Berill 1981) suggests that bioerosion and destabilization of marsh channel banks, levees, and dikes may occur.

The only potential control agent known to infect green crabs in California is a nemertean egg predator, Carcinonemertes epialti, that normally infests the shore crab Hemigrapsus oregonensis (Torchin et al. 1996). At this point, it is unlikely that the nemertean alone will affect green crab abundance because infestation rates are apparently low. The predators and parasites of the green crab in Europe are relatively well known (Crothers 1968, Williams 1984). In particular, in-depth studies of two parasitic castrators, Sacculina carcini and Portunion maenadis, are available. These document their life cycles and effects on host growth, reproduction, and behavior, and provide some information on their prevalence in different populations (Day 1935, Veillet 1945, Rasmussen 1959, Crothers 1968, Heath 1971, Lutzen 1984, Hoeg and Lutzen 1985).

The parasitic barnacle Sacculina carcini presently seems the best candidate for biological control as the Rhizocephala are highly host-specific parasitic castrators that can theoretically control host populations. Hoeg and Lutzen (1985) recently reviewed the host range of S. carcini. All valid records are for portunid crabs (including Carcinus maenas) or for the related Pirimelidae. Fortunately, the native crab fauna of central California lacks representatives of these families (Schmitt 1921, Carlton and Kuris 1980, Garth and Abbott 1980). Further, the family Cancridae seems to be remarkably unsusceptible to rhizocephalans. Only the European Cancer pagurus is parasitized by the distinctive host-specific species, S. triangularis (Hoeg and Lutzen 1985). It is likely that host specificity is even stronger than currently recognized. Karyological analyses of morphologically similar sacculinids from different species of crabs demonstrate species-level differences in chromosome number and organization (Fratello 1968). Although the present information strongly suggests that S. carcini would be a safe control agent, the documentation of rhizocephalans with broader host specificity (e.g., Loxothylacus panopaei infects seven xanthid crabs [Grosholz and Ruiz 1995]) underscores the need for carefully controlled experiments to determine if native species are refractory to infections of the parasite.

Following safety determination, techniques to raise the biocontrol agent would need development. Improved barnacle culture technology would be required for infecting large numbers of green crabs for release. Determination of the geographic origin of the introduced crabs using genetic techniques would allow better selection of an appropriate source of parasites. Technological advancements in the early detection of infected crabs would increase the efficiency of the program and decrease delays. Implementation of biological control might comprise a sustained program of trapping and infecting crabs. This would also serve as a means to monitor the success of the control effort.

In addition to this rather classical biological control program, it might be useful to integrate a subsidized fishery for green crabs. After all, fisheries are a proven way to eradicate a species. Although the green crab is too small for traditional seafood markets, it is a tasty crab (A. M. Kuris, personal observation) and should be acceptable to several ethnic groups with sizable communities around San Francisco Bay. In the Tokyo Bay area of Japan, the introduced Mediterranean green crab is split in two and adds flavor to miso soup (M. Takeda, personal communication). So far, it is not a pest in Japan.


It is absolutely certain that more deleterious invasions are yet to come (we predict, for example, that the Asiatic seastar, Asterias amurensis, will invade the West Coast just as it has invaded Tasmania). Shipping will continue to expand as our national economy inexorably integrates into the global economy. This will intensify the rate of ballast-water introductions. Management of ballast water continues to be a minimally regulated, controversial issue. Mariculture of imported species has always included unwanted hitchhikers that accompany the shipments of commercial species. This second major source of new pests is also expanding as we struggle to replace declining fisheries. Beyond the obvious need to protect our waters from unwanted introductions, ecologists can help predict new arrivals, study the basic biology of these probable new arrivals, and work on biological controls. We cannot overemphasize that, as has been long evident in the management of agricultural pests, early detection and a rapid response afford the greatest opportunity to control pest invasions.


Special thanks to C. Culver for help with research and development of these ideas. We also thank T. Bellows, C. Briggs, J. Carlton, J. Chapman, R. Collins, R. Day, Y. Hayakawa, J. Hoeg, R. Luck, R. Martin, E Nichols, S. Rainer, M. Takeda, R. Thresher, and M. Torchin for helpful discussion and information. This paper is funded in part by Saltonstall-Kennedy Grant NA46FDO493 and a grant from the National Sea Grant College Program, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, under grant number NA36RGO537 (project numbers R/C-22-16-PD and R/F-23-1-PD) through the California Sea Grant College, and in part by the California State Resources Agency. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its sub-agencies. The U.S. Government is authorized to reproduce and distribute this paper for governmental purposes.


Abbott, I. A. 1987. There are aliens among the algae, too - or limu malihini. Newsletter of the Hawaiian Botanic Society 26:60-63.

Basson, M. 1994. A preliminary investigation of the possible effects of rhizocephalan parasitism on the management of the crab fishery around South Georgia. CCAMLR [Commission for the Conservation of Antarctic Marine Living Resources] Science 1:175-192.

Bergman, K. M., R. W. Elner, and M. J. Risk. 1981. The influence of Polydora websteri on the strength of the shell of the sea scallop, Placopecten magellanicus. Canadian Journal of Zoology 60:2551-2556.

Berrill, M., and N. Berrill. 1981. The North Atlantic coast. Sierra Club Books, New York, New York, USA.

Blake, J. A. 1971. Revision of the genus Polydora from the East Coast of North America (Polychaeta: Spionidae). Smithsonian Contributions in Zoology 75:1-32.

Blake, J. A., and J. W. Evans. 1973. Polydora and related genera as borers in mollusk shells and other calcareous substrates (Polychaeta: Spionidae). Veliger 15:235-249.

Blower, S., and J. Roughgarden. 1987. Population dynamics and parasitic castration: a mathematical model. American Naturalist 129:730-753.

Blower, S., and J. Roughgarden. 1989. Parasites detect host spatial pattern and density: a field experiment analysis. Oecologia 78:138-141.

Brittan, M. R., J. D. Hopkirk, J. D. Conners, and M. Martin. 1970. Explosive spread of the oriental goby Acanthogobius flavimanus in the San Francisco Bay-Delta region of California. Proceedings of the California Academy of Sciences 38:207-214.

Burton, K., R. Yogev, N. London, K. Boyer, and S. T. Shulman. 1982. Pulmonary paragonimiasis in Laotian refugee children. Pediatrics 70:246-248.

Buttermore, R. E., E. Turner, and M. G. Motrice. 1994. The introduced northern Pacific seastar, Asterias amurensis in Tasmania. Memoirs of the Queensland Museum 36:21-25.

Campbell, F. T. 1993. Legal avenues for controlling exotics. Pages 243-250 in B. N. McKnight, editor. Biological pollution: the control and impact of invasive exotic species. Indiana Academy of Sciences, Indianapolis, Indiana, USA.

Carlton, J. T. 1975. Introduced intertidal invertebrates. Pages 17-25 in J. T Carlton and R. I. Smith, editors. Light's manual: intertidal invertebrates of the Central California coast. Third edition. University of California Press, Berkeley, California, USA.

-----. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology Annual Review 23: 313-371.

-----. 1987. Mechanisms and patterns of transoceanic marine biological invasions in the Pacific Ocean. Bulletin of Marine Science 41:467-499.

-----. 1989. Man's role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conservation Biology 3:452465.

Carlton, J. T., and A. M. Kuris. 1980. Keys to decapod Crustacea. Pages 385-412 in J. T. Carlton and R. I. Smith, editors. Light's manual: intertidal invertebrates of the Central California coast. Third edition. University of California Press, Berkeley, California, USA.

Carlton, J. T., J. K. Thompson, L. E. Schemel, and F. H. Nichols. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. II. Introduction and dispersal. Marine Ecology Progress Series 66:81-94.

Chapman, J. W. 1988. Invasions of the northeast Pacific by Asian and Atlantic gammaridean amphipod crustaceans, including a new species of Corophium. Journal of Crustacean Biology 8:364-382.

Cohen, A. N., J. T. Carlton, and M. C. Fountain. 1995. Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Marine Biology 122:225-237.

Cook, James R. 1993. The role of biological control in pest management in the 21st century. Pages 10-20 in R. D. Lumsden and J. L. Vaughn, editors. Pest management: biologically based technologies. American Chemical Society, Washington, D.C., USA.

Crothers, J. H. 1968. The biology of the shore crab Carcinus maenas (L.). 2. The life of the adult crab. Field Studies 2: 579-614.

Day, J. H. 1935. The life-history of Sacculina. Quarterly Journal of Microscopical Science 77:549-583.

DeBach, P. 1974. Biological control by natural enemies. Cambridge University Press, London, England.

Doty, M. S. 1961. Acanthophora, a possible invader of the marine flora of Hawaii. Pacific Science 15:547-552.

Drea, J. J. 1993. Classical biological control - an endangered discipline? Pages 215-222 in B. N. McKnight, editor. Biological pollution: the control and impact of invasive exotic species. Indiana Academy of Sciences, Indianapolis, Indiana, USA.

Ebeling, A. W., D. R. Laur, and R. J. Rowley. 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. Marine Biology 84:287-294.

Elner, R. W. 1981. Diet of green crab Carcinus maenas (L.) from Port Hebert, southwestern Nova Scotia. Journal of Shellfish Research 1:89-94.

Evans, J. W. 1969. Borers in the shell of the sea scallop, Placopecten magellanicus. American Zoologist 9:775-782.

Farley, C. A. 1992. Mass mortalities and infectious lethal diseases in bivalve molluscs and associations with geographic transfers of populations. Pages 139-154 in A. Rosen field and R. Mann, editors. Dispersal of living organisms into aquatic ecosystems. Maryland Sea Grant Publications, College Park, Maryland, USA.

Feigenbaum, D., and M. Kelly. 1984. Changes in the lower Chesapeake Bay food chain in the presence of the sea nettle Chrysaora quinquecirrha (Scyphomedusa). Marine Ecology Progress Series 19:39-47.

Fratello, B. 1968. Cariologia e tassonomia dei Sacculinidae (Cirripedi, Rizocefali). Caryologia 21:359-367.

Gaines, S. D., and K. D. Lafferty. 1995. Modeling the dynamics of marine species: the importance of incorporating larval dispersal. Pages 389-412 in L. McEdward, editor. Ecology of marine invertebrate larvae. CRC Press, Boca Raton, Florida, USA.

Garth, J. S., and D. P. Abbott. 1980. Brachyura: the true crabs. Pages 594-630 in B. H. Morris, D. P. Abbott, and E. C. Haderlie, editors. Intertidal invertebrates of California. Stanford University Press, Stanford, California, USA.

Glude, J. B. 1955. The effects of temperature and predators on the abundance of the soft-shell clam, Mya arenaria, in New England. Transactions of the American Fisheries Society 84:13-26.

Grosholz, E. D. 1996. Contrasting rates of spread for introduced species in terrestrial and marine systems. Ecology 77:1680-1686.

Grosholz, E. D., and G. M. Ruiz. 1995. Does spatial heterogeneity and genetic variation in populations of the xanthid crab Rhithropanopeus harrisii (Gould) influence the prevalence of an introduced parasitic castrator? Journal of Experimental Marine Biology and Ecology 187:129-145.

Grosholz, E. D., and G. M. Ruiz. 1995. Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Marine Biology 122:239-247.

Hahn, K. O. 1989. Handbook of culture of abalone and other marine gastropods. CRC Press, Boca Raton, Florida, USA.

Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 33:79-99.

Harbison, G. R., and S. P. Volovik. 1994. The ctenophore, Mnemiopsis leidyi, in the Black Sea: a holoplanktonic organism transported in the ballast water of ships. Pages 25-36 in D. Cottingham, editor. Proceedings of the Conference and Workshop on Nonindigenous Estuarine and Marine Organisms. 1994-300-566/03051. U.S. Department of Commerce, NOAA Office of the Chief Scientist, U.S. Government Printing Office, Washington, D.C., USA.

Heath, J. R. 1971. Seasonal changes in a population of Sacculina carcini Thompson (Crustacea: Rhizocephala) in Scotland. Journal of Experimental Marine Biology and Ecology 6:15-22.

Hicks, D. W., and J. W. Tunnell, Jr. 1993. Invasion of the South Texas coast by the edible brown mussel Perna perna. Veliger 36:92-97.

Hobbs, R. C., and L. W. Botsford. 1989. Dynamics of an age-structured prey with density-, and predator-dependent recruitment: the Dungeness crab and a nemertean egg predator worm. Theoretical Population biology 36:1-22.

Hoeg, J., and J. Lutzen. 1985. Crustacea rhizocephala. Norwegian University Press, Oslo, Norway.

Hofkin, B. V., D. K. Koech, J. Ouma, and E. S. Loker. 1991. The North American crayfish Procambarus clarkii and the biological control of schistosome-transmitting snails in Kenya: laboratory and field investigations. Biological Control 1:183-187.

Huffaker, C. B. 1971. The phenomenon of predation and its roles in nature. Pages 327-343 in P. J. den Boer and G. R. Gradwell, editors. Dynamics of populations. Center for Agricultural Publications and Documentation, Wageningen, The Netherlands.

Jeong, H. J., and M. I. Latz. 1994. Growth and grazing rates of the heterotrophic dinoflagellates Protoperidinium spp. on red tide dinoflagellates. Marine Ecology Progress Series 106:173-185.

Jobin, W. R., R. A. Brown, S. P. Velez, and F. F. Ferguson. 1977. Biological control of Biomphalaria glabrata in major reservoirs of Puerto Rico. American Journal of Tropical Medicine and Hygiene 26:1018-1024.

Jones, G. M. 1985. Paramoeba invadens n. sp. (Amoebida, Paramoebidae), a pathogenic amoeba from the sea urchin Strongylocentrotus droebachiensis, in Eastern Canada. Journal of Protozoology 32:564-569.

Jones, G. M., and R. E. Scheibling. 1985. Paramoeba sp. (Amoebida, Paramoebidae) as the possible causative agent of sea urchin mass mortality in Nova Scotia. Journal of Parasitology 71:559-565.

Kent, R. M. L. 1979. The Effect of Polydora ciliata on the shell strength of Mytilus edulis. Journal du Conseil International pour l'Exploration de la Met 39:252-255.

-----. 1981. The influence of heavy infestations of Polydora ciliata on the flesh content of Mytilus edulis. Journal of the Marine Biological Association of the United Kingdom 59:289-297.

Klein Breteler, W. C. M. 1983. The shore crab Carcinus maenas. Pages 119-122 in W. J. Wolff, editor. Ecology of the Wadden Seas. Volume 1. A.A. Balkema, Rotterdam, The Netherlands.

Kuris, A. M. 1973. Analogy between the trophic interactions of insect pest-parasitoid and snail-trematode system: implication for biological control. Experimental Parasitology 33:365-379.

-----. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. Quarterly Review of Biology 49: 129-148.

-----. 1991. A review of patterns and causes of crustacean brood mortality. Crustacean Issues 7:117-141.

Kuris, A.M., S. F. Blau, A. J. Paul, J. D. Shields, and D. E. Wickham. 1991. Infestation by brood symbionts and their impact on egg mortality of the red king crab, Paralithodes camtschatica, in Alaska: geographic and temporal variation. Canadian Journal of Fisheries and Aquatic Sciences 48:559-568.

Kuris, A. M., and K. D. Lafferty. 1992. Modeling crustacean fisheries: effects of parasites on management strategies. Canadian Journal of Fisheries and Aquatic Sciences 49: 327-336.

Kuris, A. M., and S. P. Norton. 1985. Evolutionary importance of overspecialization: insect parasitoids as an example. American Naturalist 126:387-391.

Lafferty, K. D. 1991. Effects of parasitic castration on the salt marsh snail, Cerithidea californica. Dissertation. University of California, Santa Barbara, California, USA.

-----. 1993. Effects of parasitic castration on growth, reproduction and population dynamics Cerithidea californica. Marine Ecology Progress Series 96:229-237.

Lafferty, K. D., and A. M. Kuris. 1994. Potential uses for biological control of alien marine species. Pages 97-102 in D. Cottingham, editor. Proceedings of the Conference and Workshop on Nonindigenous Estuarine and Marine Organisms. 1994-300-566/03051. U.S. Department of Commerce, NOAA Office of the Chief Scientist, U.S. Government Printing Office, Washington, D.C., USA.

Lafferty, K. D., R. O. Swenson, and C. C. Swift. 1996. Threatened fishes of the world: Eucyclogobius newberryi Girard, 1857 (Gobiidae). Environmental Biology of Fishes 46, in press.

Lassuy, D. R. 1994. Aquatic nuisance report overview. Fisheries 19:14-23.

Lauckner, G. 1983. Diseases of Mollusca: Bivalvia. Pages 477-978 in O. Kinne, editor. Diseases of marine animals. Volume II, Bivalvia to Scaphopoda. John Wiley and Sons, New York, New York, USA.

Le Roux, P. J., G. M. Branch, and M. A. P. Joska. 1990. On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African coast. South African Journal of Marine Science 9: 85-93.

Leet, W. S., C. M. Dewees, and C. W. Haugen. 1992. California's living marine resources and their utilization. UCSGEP-92-12. University of California Sea Grant Extension, La Jolla, California, USA.

Lodge, D. M. 1993. Biological invasions: lessons for ecology. Trends in Ecology and Evolution 8:133-137.

Loosanoff, V. L., and J. B. Engle. 1943. Polydora in oysters suspended in the water. Biological Bulletin of Marine Biology 85:69-78.

Lunz, G. R., Jr. 1940. The annelid worm, Polydora, as an oyster pest. Science 92:310.

-----. 1941. Polydora, a pest in South Carolina oysters. Journal of the Elisha Mitchell Scientific Society 57:273-283.

Lutzen, J. 1984. Growth, reproduction and life span in Sacculina carcini Thompson (Crustacea: Rhizocephala) in the Isefjord, Denmark. Sarsia 69:91-106.

MacPhail, J. S., E. I. Lord, and L. M. Dickie. 1955. The green crab - a new clam enemy. Fisheries Research Board of Canada, Atlantic Progress Report 63:3-12.

Markell, E. K., M. Voge, and D. T. John. 1992. Medical parasitology. Seventh edition. Saunders, Philadelphia, Pennsylvania, USA.

McDermott, J. J. 1991. A breeding population of the Western Pacific crab Hemigrapsus sanguineus (Crustacea, Decapoda, Grapsidae) established on the Atlantic coast of North America. Biological Bulletin 181:195-198.

McGinnis, S. M. 1984. Freshwater fishes of California. University of California Press, Berkeley, California, USA.

Miller, R. F. 1985. Sea urchin pathogen: a possible tool for biological control. Marine Ecology Progress Series 21: 169-174.

Milligan, K. L., and E. M. Cosper. 1994. Isolation of virus capable of lysing the brown tide microalga, Aureococcus anophagefferens. Science 266:805-807.

Mills, C. E., and F. Sommer. 1995. Invertebrate introductions in marine habitats: two species of hydromedusae (Cnidaria) native to the Black Sea, Maeotias inexspectata and Blackfordia virginica, invade San Francisco Bay. Marine Biology 122:279-288.

Mori, K., W. Sato, T. Nomura, and M. Imajima. 1985. Infestation of the Japanese scallop Patinopecten yessoensis by the boring polychaetes, Polydora, on the Okhotsk sea coast of Hokkaido, especially in Abashiri waters. Bulletin of the Japanese Society of Scientific Fisheries 51:371-380.

Moulton, J. M., and A. H. Gustafson. 1956. Green crabs and the redistribution of quahogs. Science 123:992.

Moyle, P. B. 1991. Ballast water introductions. Fisheries 16: 4-6.

Murdoch, W. W., and C. J. Briggs. 1996. Theory for biological control: recent developments. Ecology 77:2001-2013.

Murdoch, W. W., J. Chesson, and P. L. Chesson. 1985. Biological control in theory and practice. American Naturalist 125:343-366.

Nassi, H., J. P. Pointier, and Y. J. Golvan. 1979. Bilan d'un essai de controle de Biomphalaria glabrata en Guadeloupe a l'aide d'un Trematode sterilisant. Annales de Parasitologie Humain et Comparee 54:185-192.

Nichols, F. H., and J. K. Thompson. 1985. Persistence of an introduced mudflat community in South San Francisco Bay, California. Marine Ecology Progress Series 24:83-97.

Nichols, F. H., J. K. Thompson, and L. E. Schemel. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensts. II. Displacement of a former community. Marine Ecology Progress Series 66:95-101.

Pachuki, C. T., R. A. Levandowski, V. A. Brown, B. H. Sonnenkalb, and M. J. Vruno. 1984. American paragonimiasis treated with praziquantal. New England Journal of Medicine 311:582-583.

Parker, D., and P. Kalvass. 1992. Sea urchins Pages 41-43 in W. S. Leet, C. M. Dewees, and C. W. Haugen, editors. California's living marine resources and their utilization. UCSGEP-92-12. University of California Sea Grant Extension, La Jolla, California, USA.

Pointier, J. P. 1983. La lutte biologique contre les Mollusques hotes intermediares des bilharzioses a l'aide de mollusques competiteurs. Symbioses 15:85-91.

Pointier,J. P., A. Theron, D. Imbert-Establet, and G. Borel. 1991. Eradication of a sylvatic focus of Schistosoma mansoni using biological control by competitor snails. Biological Control 1:244-247.

Race, M. S. 1982. Competitive displacement and predation between introduced and native mud snails. Oecologia 34: 337-347.

Rasmussen, E. 1959. Behaviour of sacculinized shore crabs (Carcinus maenas Pennant). Nature 183:479-480.

Ropes, J. W. 1968. The feeding habits of the green crab, Carcinus maenas (L). Fisheries Bulletin 67:183-203.

Ruppert, E. E., and E. S. Fox. 1988. Seashore animals of the Southeast. University of South Carolina Press, Columbia, South Carolina, USA.

Russell, D. J. 1992. The ecological invasion of Hawaiian reefs by two marine red algae, Acanthophora spicifera (Vahl) Boerg. and Hypnea musciformis (Wulfen) J. Ag., and their association with two native species, Laurencia nidifica J. Ag. and Hypnea cervicornis J. Ag. ICES [International Council for Exploration of the Sea] Marine Science Symposium 194:110-125.

Russell, D. J., and G. H. Balazs. 1994. Colonization by the alien marine alga Hypnea musciformis (Wulfen) J. Ag. (Rhodophyta: Gigartinales) in the Hawaiian Islands and its utilization by the green turtle, Chelonia mydas L. Aquatic Botany 47:3-60.

Sanchez-Salazar, M. E., C. L. Griffiths, and R. Seed. 1987. The effect of size and temperature on the predation of cockles Cerastoderma edule (L.) by the shore crab Carcinus maenas (L.). Journal of Experimental Marine Biology and Ecology 111:181-193.

Scherer, B., and K. Reise. 1981. Significant predation on micro- and macrobenthos by the crab Carcinus maenas (L.) in the Wadden Sea. Kieler Meeresforschungen Sonderheft 5:490-500.

Schmitt, W. L. 1921. The marine decapod Crustacea of California. University of California Publications in Zoology 23.

Shumway, S. E. 1989. Toxic algae a serious threat to shellfish aquaculture. World Aquaculture 20:65-74.

Sieburth, J. McN., P. W. Johnson, and P. E. Hargraves. 1988. Ultrastructure and ecology of Aureococcus anophagefferens gert. et sp. nov. (Chrysophyceae): the dominant pico-plankton during a bloom in Narragansett Bay, Rhode Island, summer 1985. Journal of Pbycology 24:416-425.

Suttle, C. A., A. M. Chan, and M. T. Cottrell. 1990. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467-469.

Torchin, M. E., K. D. Lafferty, and A. M. Kuris. 1996. Infestation of an introduced host, the European green crab, Carcinus maenus, by a native symbiotic nemertean egg predator, Carcinornertes epialti. Journal of Parasitology 82: 449-453.

Van den Bosch, R., P. S. Messenger, and A. P. Gutierrez. 1982. An introduction to biological control. Plenum, New York, New York, USA.

Veillet, A. 1945. Recherches sur le parasitisme des Crabes et des Galathees par les Rhizocephales et les Epicarides. Annales de l'Instut oceanographique Monaco 22:193-341.

Vinogradov, M. E., E. A. Shushkina, E. I. Musayeva, and P. Yu. Sorokin. 1989. A newly acclimated species in the Black Sea: ctenophore Mnemiopsis leidyei (Ctenophora: Lobata). Oceanology 29:200-224.

Waage, J. 1990. Ecological theory and the selection of biological control agents. Pages 135-157 in M. Mackauer, L. E. Ehler, and J. Roland, editors. Critical issues in biological control. VCH Publishers, New York, New York, USA.

Wargo, R. N., and S. E. Ford. 1993. The effect of shell infestation by Polydora sp. and infection by Haplosporidium nelsoni (MSX) on the tissue condition of oysters, Crassostrea virginica. Estuaries 16:229-234.

Whitlatch, R. B., and S. Obrebski. 1980. Feeding selectivity and coexistence in two deposit feeding gastropods. Marine Biology 58:219-225.

Williams, A. B. 1984. Shrimps, lobsters and crabs of the Atlantic coast of the eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, USA.

Zibrowius, H. 1991. Ongoing modifications of the Mediterranean marine fauna and flora by the establishment of exotic species. Mesogee 51:83-107.
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Date:Oct 1, 1996
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