9
Elements of Risk Assessment for the Introduction of Crassostrea ariakensis in the Chesapeake Bay

BACKGROUND ON RISK ASSESSMENT

The committee was asked to assess whether the breadth and quality of existing information on oysters and other introduced species are sufficient to support risk assessment of three management options: no use of nonnative oysters, open-water aquaculture of triploid nonnative oysters, and introduction of diploid nonnative oysters. We must begin by identifying an appropriate scope for the risk assessment. Structuring a conceptual or numerical risk assessment highlights what is known and what is not known about the modeled system, breaks complex issues into more understandable problems, and helps to identify critical assumptions. Some previous National Research Council (NRC) studies (e.g., NRC, 1983, 2002b) define risk assessment as the identification and characterization of hazards and the determination of the likelihood that hazards will result in harms. In these studies, risk management is defined as a decision-making process that takes into account the probability distribution of harms given exposure to the hazard and the associated conditional costs and benefits. That is, risk assessment and risk management are reduced to characterizing the branches and conditional probabilities of a decision tree and selecting a strategy based on preferences regarding the conditional net benefits. While this may be workable for well-understood systems with well-defined objectives, complex systems require a more general framework for risk assessment and a closer integration of risk assessment with risk management (NRC, 1993, 1996a, 1996b, 2002b). This closer integration is necessary because the risks that we choose to manage determine the risks that need



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Nonnative Oysters in the Chesapeake Bay 9 Elements of Risk Assessment for the Introduction of Crassostrea ariakensis in the Chesapeake Bay BACKGROUND ON RISK ASSESSMENT The committee was asked to assess whether the breadth and quality of existing information on oysters and other introduced species are sufficient to support risk assessment of three management options: no use of nonnative oysters, open-water aquaculture of triploid nonnative oysters, and introduction of diploid nonnative oysters. We must begin by identifying an appropriate scope for the risk assessment. Structuring a conceptual or numerical risk assessment highlights what is known and what is not known about the modeled system, breaks complex issues into more understandable problems, and helps to identify critical assumptions. Some previous National Research Council (NRC) studies (e.g., NRC, 1983, 2002b) define risk assessment as the identification and characterization of hazards and the determination of the likelihood that hazards will result in harms. In these studies, risk management is defined as a decision-making process that takes into account the probability distribution of harms given exposure to the hazard and the associated conditional costs and benefits. That is, risk assessment and risk management are reduced to characterizing the branches and conditional probabilities of a decision tree and selecting a strategy based on preferences regarding the conditional net benefits. While this may be workable for well-understood systems with well-defined objectives, complex systems require a more general framework for risk assessment and a closer integration of risk assessment with risk management (NRC, 1993, 1996a, 1996b, 2002b). This closer integration is necessary because the risks that we choose to manage determine the risks that need

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Nonnative Oysters in the Chesapeake Bay to be assessed. Following Pratt et al. (1995), we define risk assessment as a decision-making technique that incorporates objective and subjective estimates of the probability of uncertain factors and identifies preferred actions with respect to multiple objectives (see Box 9.1). BOX 9.1 Glossary of Risk Analysis Terms Bayes theorem: a statistical rule for combining relative frequencies and subjective probabilities or prior information about the likelihood of certain future conditions. Conditional costs and benefits: outcomes that can be expected given the occurrence of specific management actions or particular stochastic events. Decision: an active or passive choice. Harm: costs incurred as a consequence of specific hazards; a conditional payoff. For example, some Chesapeake Bay stakeholders would construe the establishment of a self-sustaining population of nonnative oysters as a harm related to exposure to the hazard of reversion. Hazard: an action or event that has the potential to result in an undesired outcome. In the context of this study, a hazard occasioned by open-water aquaculture of triploid nonnative oysters is that reproductively competent oysters are released and the undesired outcome is that the nonnative oysters become invasive. Likelihood: the probability that an outcome will occur given exposure to a hazard. Multiple criteria decision analysis: procedures for evaluating alternative outcomes with respect to multiple objectives. Objectives: goals of stakeholders. Payoffs: conditional outcomes evaluated in terms of management objectives. Probability and probability distributions: statistical descriptions of relative frequencies, often expressed in terms of expected value, variance, skewness, and kurtosis. Relative frequency: the frequency of particular outcomes relative to the frequency of observed outcomes Risk: the possibility of undesired outcomes being realized as a result of management action or natural variability. In the context of this study, a risk associated with openwater aquaculture of triploid nonnative oysters could be defined as the joint probability that some oysters might revert and that their progeny might become established in the Chesapeake Bay. Risk analysis: synonymous with risk assessment. Risk assessment: a decision-making technique that incorporates relative frequencies and subjective probabilities of uncertain factors and identifies preferred actions with respect to one or more objectives. Risk management: the avoidance, mitigation, reduction, shifting, pooling, or buffering of risk. Risk preferences: faced with a choice between an action that leads to a guaranteed payoff and an action that leads to an equal but uncertain payoff, the selection of a particular payoff by a decision maker. Most decision makers in most circumstances will select the certain payoff; they are said to be risk averse. Stakeholder: any person, group, or organization interested in the management decision. Subjective probabilities: estimates of the likelihood of events and their distribution based on expert judgment with limited historical or experimental observations.

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Nonnative Oysters in the Chesapeake Bay The structure and dynamics of the Chesapeake Bay ecological and socioeconomic systems are complex, not well understood, and subject to environmental, social, and political influences beyond the scope of management control. Consequently, decision makers are faced with uncertainty—uncertainty about the structure and dynamics of integrated physical, biological, economic, and sociocultural systems, uncertainty about how the systems will respond to the actions taken, and uncertainty about the merits of alternative outcomes. Decision making under these conditions entails risk to ecological systems, risk to socioeconomic systems and institutions, and risk that implementation of management actions will lead to unanticipated or undesired consequences. Actions taken to minimize one aspect of risk often increase the level of risk in other dimensions. When the consequences of management actions are uncertain, good decision making involves balancing risks and benefits. In order to balance risks and payoffs, it is important to understand the characteristics of risk preferences and approaches to solving multiple criteria decision problems. Although individual risk preferences differ, most decision makers are averse to increased levels of risk unless the risk is offset by increased conditional gains. That is, given a choice between a risk-free payoff and an equal but uncertain payoff, most decision makers will select the risk-free payoff. Risks may be symmetric (equal likelihood of being above or below an expected value) or asymmetric (unequal likelihood of being above or below an expected value). Risk preferences are typically asymmetric (we prefer favorable outcomes) and discordant (we disagree on what is favorable). For example, stakeholders who favor the establishment of nonnative oysters might prefer management actions that increase the likelihood of reproduction, while those who oppose establishment of nonnative oysters might prefer management actions that decrease the likelihood of reproduction, decrease the likelihood of reproduction by reverted oysters, or decrease the likelihood of successful establishment of nonnative populations. Multiple objectives may be balanced through political processes or formally examined using multiple criteria decision analysis methods (e.g., Keeney and Raiffa, 1976; Saaty, 1990). These methods have been used to address a variety of fishery management issues (e.g., Hilborn and Walters, 1977; Bain, 1987; Walker et al., 1983; Healey, 1984; Mackett, 1985; Merritt and Criddle, 1993). Solutions that emerge from the application of multiple criteria decision analysis often favor compromises that minimize maximum losses or maximize minimum benefits. Multiple criteria decision analyses that incorporate multiple stakeholders with overlapping objectives often select management options that enjoy broad support and limited objection. Stakeholders with conflicting objectives may prefer similar options for dissimilar reasons. For example, stakeholders opposed to the

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Nonnative Oysters in the Chesapeake Bay establishment of nonnative oysters might strongly prefer that triploid aquaculture field trials be based on genetic triploids (mated tetraploid-diploid crosses) because of the reduced likelihood of reproduction. Stakeholders interested in commercial-scale aquaculture of triploid nonnatives might favor field trials based on genetic triploids to reduce liability of diploid escape. Risks that cannot be avoided can often be mitigated, reduced, shifted, pooled, or buffered. A policy mandating the early harvest of triploid nonnatives might mitigate the risk of open-water triploid aquaculture by minimizing the number of oysters that would revert from a triploid to diploid condition and reducing the likelihood that reverted oysters would spawn before they are harvested. Risk reduction might entail actions that partially reduce the level of risk. For example, triploids created from tetraploid-diploid crosses have a lower reversion rate than chemically induced triploids. Risk shifting entails a transfer of risk from one individual or stakeholder class to another. For example, oyster farmers may be able to shift the risk and liability associated with broodstock maintenance and larval production to state hatchery facilities. Risk pooling distributes individual risk across a class of stakeholders. Traditional insurance programs are a mechanism for pooling low-frequency risks with severe negative consequences. Buffering consists of actions that increase the resilience of systems to adverse events. For example, oyster farmers may be able to buffer production risk by distributing their oyster beds across a broad geographic region or across salinity gradients. The three management options entail differing arrays of risks and are subject to the diverse objectives of multiple stakeholders. Development of a risk assessment framework for the decision would involve characterizing and developing probability distribution functions for the various risks, evaluating those risks according to the diverse objectives, and balancing those objectives in a multiple criteria decision analysis. At this stage there is insufficient information for a formal risk assessment of management options concerning the introduction of a nonnative oyster into the bay. Moreover, it is not possible to complete a risk assessment because the objectives and goals for the Chesapeake Bay and its dependent communities are not well defined or fully agreed upon. The objectives of state, federal, and local governing agencies are unclear, conflicting, or both. In addition, the objectives of the watermen, environmental groups, aquaculturalists, and other users are also unclear, conflicting, or both. Until these diverse objectives are sorted out, meaningful risk assessment cannot be undertaken. Nevertheless this chapter reviews areas of risk and identifies specific risk factors, indicates relative degrees of risk in the ecological and socioeconomic realms, and evaluates the adequacy of the information available.

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Nonnative Oysters in the Chesapeake Bay Ecological risks associated with the options include the environmental and ecological consequences of continued low native oyster population levels, the risk that nonnative oysters would become established and pervasive or fail to become established or pervasive, the risk of further collapse or impaired recovery of native oyster populations, and the risk of adverse consequences for other stocks of fish, shellfish, and vascular plants. Ecological risks could arise through competitive interactions for food and space through technological interactions (e.g., joint harvesting of scarce stocks of native oysters admixed with abundant stocks of nonnative oysters) or through other interactions (e.g., enhancement of predator, parasite, or disease organisms, or fertilization competition between native and nonnative oyster gametes). An example of a qualitative risk assessment for shellfish farming in Tasmania considered the spread of predators or pests, habitat disturbance, and effects on food resources for other filter feeders (Crawford, et al., 2003). The risk assessment model described by Dew et al. (2003) provides a useful example of a simple model of the likelihood of self-sustaining populations resulting from commercial production of supposed triploid nonnative oysters. Examples of more comprehensive approaches to ecological risk assessment would include models coupling hydrodynamics and larval transport, models assessing age- or size-dependent predator-prey and competitive interactions, and models that incorporate variability in environmental conditions (e.g., salinity, temperature, substrate) to oyster growth, survivorship, and reproduction. The decision to introduce or not introduce C. ariakensis can be expected to generate differing arrays of risk to economic and sociocultural institutions and systems. Economic and sociocultural risks would differ under each of the three management options and would impact, for example, the availability of oysters for public- and leased-bottom fisheries, the opportunity and incentive for consolidating and vertical integrating of harvesting and processing operations, the sustainability of public-and leased-bottom fisheries, household production and the structure of fishery-dependent communities, the net use and option benefits of recreational and amenity services, and non-use benefits. The economic and socioeconomic risks associated with the management options and the adequacy of available data to assess the magnitude and significance of risk to social, cultural, and economic systems and institutions are also examined below. Implementation risk includes the risk of political objection, the consequences of management actions that may differ from the intent of those actions, the possibility that actions taken by one regulatory entity might adversely affect the efficacy of actions taken by another regulatory entity, and the likelihood that the selected management option might spur unau-

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Nonnative Oysters in the Chesapeake Bay thorized introductions. Endangered Species Act Section 7 consultations are an example of an assessment of the risk that implementation of a proposed action could jeopardize the recovery of an endangered species or adversely modify its critical habitat. The adequacy of information available for assessing implementation risks is the final consideration discussed below. RISK FACTORS Ecological Risk Disease The possibility that a new disease-causing organism might be introduced along with C. ariakensis has been one of the major concerns of all agencies and individuals involved in the deliberations about a possible introduction. This fear is not unwarranted since a number of disease outbreaks in oysters have been linked to the introduction and transfer of molluscs for commercial culture (Rosenfield and Kern, 1979; Andrews, 1980). Adherence to the International Council for the Exploration of the Sea protocols, discussed in more detail below, would significantly reduce the risk of bringing in a new disease-causing organism as a consequence of introducing a nonnative oyster. Some of the linkages are more robust than others, and some researchers are more confident of a causal relationship than others. Manifestation of disease following an introduction could result from the concomitant accidental introduction of an exotic pathogen or through the susceptibility of the introduced oyster to an endemic pathogen (Sindermann, 1990). The method mostly commonly envisioned is that the introduced oyster would bring a new pathogen, which would infect the native oyster (or other species). This might occur even though the introduced oyster displayed no disease symptoms. It might be extremely difficult even to detect the pathogen because so few oysters are infected because so few pathogens are present in any individual, or both. Since the native oyster would never have been exposed to the parasite, it would likely be highly susceptible, experience high infection rates, and suffer heavy mortalities. Less frequently considered but equally plausible is the possibility that the introduced oyster would be exposed to an enzootic or “resident” pathogen, which might or might not cause problems in the native oyster (or other) species. In this case it is the introduced oyster that would develop disease. The causative pathogen may never have been recognized simply because it never caused a problem in native species. It must also be stressed that pathogens can be transported by means that are not related to a nonnative introduction for fishery or aquaculture pur-

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Nonnative Oysters in the Chesapeake Bay poses, including water currents, ballast water, other (vector) animals, or discards from restaurants and processing plants. Case studies illustrating various scenarios are presented here. Haplosporidium nelsoni (MSX Disease) When H. nelsoni was first identified in 1958 as the cause of massive oyster mortalities in Delaware Bay, it was a new parasite to the investigators who saw it in tissue sections of the affected oysters. Mortalities of the scale caused by the parasite in Delaware Bay and later in Chesapeake Bay had never before been recorded in those estuaries, and it was assumed that the parasite was new to the region (Ford and Tripp, 1996). Later, two separate investigations (Katkansky and Warner, 1970; Kern, 1976) reported the finding of a parasite that was morphologically identical to H. nelsoni in the tissues of the Pacific oyster, C. gigas, in California and Korea. Friedman and Hedrick (1991) and Friedman (1996) found what appeared to be the same organism in C. gigas from Japan and California. The observed prevalence of H. nelsoni in these samples of C. gigas was low (<2%), and no commercially noticeable mortalities of C. gigas were reported. Burreson et al. (2000) determined that the small subunit ribosomal DNA sequence of H. nelsoni is identical to that of the parasite in C. gigas and concluded that C. gigas was the source of H. nelsoni, which was highly pathogenic in C. virginica even though it caused little damage in the original host. Further, they strongly suggested that the parasite was introduced in shipments of C. gigas for commercial trials. However, they noted a lack of known introductions of C. gigas into the mid-Atlantic in the years immediately preceding the initial outbreaks of H. nelsoni and acknowledged the possibility of other mechanisms of introduction. Subsequent citations of Burreson et al. (2000), including many of the position papers and documents prepared by agencies concerned with the possible introduction of C. ariakensis, state, without qualification, that H. nelsoni was introduced in “unauthorized” oyster shipments. There is little argument that H. nelsoni came from the Pacific where it infects C. gigas, but the pathway of its introduction is simply not known. Introduced C. gigas might well have been the source, but other possibilities must be considered. Particularly noteworthy is the great increase in ship transit between Pacific and Atlantic ports that occurred during and after World War II. Shipping could have introduced H. nelsoni via infected C. gigas attached to ships hulls or via release of H. nelsoni spores in the discharge of ballast water. The spore is a thick-walled stage in the life cycle of H. nelsoni; its role in transmission is not known, but the spore in other species is typically a transmission stage that can remain “dormant” for long periods and is highly tolerant of environmental extremes. MSX must be consid-

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Nonnative Oysters in the Chesapeake Bay ered a disease in which the causative agent was surely introduced but for which the means of introduction is unknown. Perkinsus marinus (Dermo Disease) Although P. marinus was first described and associated with oyster mortalities in the Gulf of Mexico in the late 1940s, it had probably infected oysters in the southern United States for a long time (Mackin and Hopkins, 1962). The parasite was identified in tissue slides of oysters collected in the 1930s, and mortalities similar to those caused by P. marinus were reported in documents dating back to the early part of the 20th century. Further, this parasite was identified in tissues of oysters in the southeastern United States, including the Virginia portion of Chesapeake Bay, as soon as investigators looked in the late 1940s and early 1950s. It was not detected in the northeastern United States, however, and numerous studies documented that the parasite multiplied and killed most readily at elevated water temperatures. However, coincident with large-scale commercial transplanting of infected oysters from Virginia into the New Jersey portion of Delaware Bay for several years in the mid-1950s, the parasite was found in nearby native Delaware Bay oysters, although it caused no mortalities (Ford, 1996). When H. nelsoni began killing oysters in the bay in 1957, an embargo was placed on all imports and exports, and after several years P. marinus was rarely detected in Delaware Bay oysters. It was argued that without repeated introductions of the parasite, Delaware Bay water temperatures were simply too low for the parasite to maintain a self-sustaining population. Nevertheless, in 1990, a severe outbreak of P. marinus infections and consequent oyster mortalities began in the bay, without the concomitant transfer of oysters from outside the estuary. That outbreak and other outbreaks over a 500-km range north to Cape Cod, Massachusetts, which followed over the next 2 years, occurred during a period of unusually warm water temperatures. Although this range extension was not associated with contemporaneous transplantation of oysters, historical transfers of oysters from the south to overfished regions of the north would probably have introduced P. marinus repeatedly over many earlier decades. In this new, colder region the parasite may have persisted at low and undetectable levels until the temperature became warm enough to stimulate an epizootic, as occurred in Delaware Bay. This account of Dermo disease illustrates what appears to be an example of a pathogen that can be present but suppressed by unfavorable environmental conditions (low temperature), then stimulated to become epizootic when conditions become favorable.

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Nonnative Oysters in the Chesapeake Bay Marteilia refringens (Marteiliosis, Aber Disease) M. refringens infects and causes severe disease in the European oyster, Ostrea edulis. Mortalities ascribed to the pathogen were first noted in Brittany, northern France, in 1967 and 1968 and over the next several years, caused mortalities in most Breton culture areas (Balouet et al., 1979). It is now found south along the French coast and into Spain, Portugal, and the Mediterranean. Like H. nelsoni, the mechanism of transmission and origin of M. refringens are unknown, although recent studies indicate that a copepod may be a second host (Audemard et al., 2002). M. refringens was a “new” parasite when first associated with the O. edulis mortalities; neither it nor any similar parasite had been seen before. Some authors (Andrews, 1980; Farley, 1992) have pointed to the propinquity of the marteiliosis outbreak and the inception of C. gigas introductions into France in the mid-1960s (Grizel and Héral, 1991) as a cautionary example of a disease agent brought with an introduced host. Others are less sure of the connection (Grizel and Héral, 1991). The timing of the introduction of C. gigas, which was found to have very low prevalence of a Marteilia-like parasite (Cahour, 1979) and the outbreak of Marteiliosis in O. edulis, may be simply a coincidence. If it does represent a cause-effect situation, the linkage is less strong than in some other instances. Interestingly, the mussels Mytilus edulis and M. galloprovincialis, which inhabit the same European waters as O. edulis, are infected by very similar parasites (Berthe et al., 2000; Le Roux et al., 2001; Longshaw et al., 2001). An alternative explanation for the appearance of M. refringens is that M. maurini “jumped” to a new host, O. edulis, concomitant with a gene mutation. Bonamia ostreae (Bonamiosis) B. ostreae also infects and causes mortality in O. edulis. It came to the attention of molluscan disease specialists when it was implicated as the cause of epizootic mortalities of O. edulis in Brittany, France. The mortalities were first noted at one site in mid-1979 and later during the same year in other Breton oyster farms (Balouet et al., 1983). Within a year or two B. ostreae was found to be causing oyster deaths in Ireland, England, the Netherlands, and Spain. In conjunction with M. refringens, B. ostreae continues to depress European oyster production. The probable movement of B. ostreae through oyster shipments has an interesting history. Although it was described simply as a “microcell” at the time, the same parasite was found in the mid-1960s in O. edulis reared at the Milford Laboratory in Connecticut (Farley et al., 1988). Some of the Milford progeny were shipped to California where the microcell was later observed in dead and dying oysters (Katkansky et al., 1969). Seed oysters

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Nonnative Oysters in the Chesapeake Bay from at least one California hatchery were then transferred to Washington state, Maine, Spain, and France (Katkansky and Warner, 1974; Elston et al., 1987; Figueras, 1991; Friedman and Perkins, 1994). B. ostreae has since been detected in O. edulis grown in California, Washington, and Maine (Elston et al., 1986; Friedman and Perkins, 1994; Zabaleta and Barber, 1996). Since the parasite is directly transmissible between oysters, a case can be made that the source of B. ostreae responsible for the European outbreak was the “large amounts of O. edulis seed transferred to France in the years prior to the detection of the disease there” (Elston et al., 1986). The finding of B. ostreae in O. edulis shipped from the Milford Laboratory to California, where the oysters experienced heavy mortality, and the presence of the same parasite in oysters from the Milford Laboratory held in quarantine at the Oxford, Maryland, National Marine Fisheries Laboratory, suggests that the parasite may have been introduced from the East to the West coasts of North America (Farley et al., 1988). The original shipments of O. edulis to the Milford Laboratory came from the Netherlands, where oyster mortalities caused by B. ostreae were reported only after the French outbreaks. The evidence available thus suggests that the parasite was probably not native to Europe at the time those shipments were made (see Table 3.2). B. ostreae is thus an example of a disease agent that is known to be transmitted directly between oysters, with a relatively welldocumented linkage with the movement of the host oyster for commercial purposes. Vibrio tapetis (Brown Ring Disease) Brown Ring Disease is a disease that has caused mortalities of the Manila clam, Ruditapes philippinarum, in Western Europe (Paillard et al., 1994). It is caused by a marine bacterium, Vibrio tapetis, and is characterized by the deposition of a ring of organic material (periostracum) on the inner edge of each valve. Manila clams were introduced to France from the U.S. West Coast for aquaculture because they grow faster than the native clam, R. decussatus. For several years Manila clams did extremely well in culture and became established in the wild, but in 1987 heavy mortalities associated with the brown ring symptom were reported in culture parks in northern Brittany. The disease spread north and south with Manila clam culture in Europe and is now found in England, Spain, and Portugal as well as France, and it affects naturalized populations of R. philippinarum as well as those under culture. It is not found in the northwestern United States or in the native range of the Manila clam along the Asian Pacific coast. The pathogen Vibrio tapetis can be found in environmental samples and the native clam, R. decussatus, is highly resistant to the disease (Maes and Paillard, 1992). Brown Ring Disease appears to be

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Nonnative Oysters in the Chesapeake Bay an example of an introduced host being highly susceptible to a resident pathogen, which has little effect on the native clam. Quahog Parasite X (QPX Disease) QPX is a newly recognized disease agent in the hard clam, Mercenaria mercenaria (Whyte et al., 1994). Although it has yet to be given a scientific name, QPX is a member of the phylum Labyrinthulomycota, a group of microorganisms that live in marine and estuarine environments on micro and macro algae and detritus. Sometimes they are pathogenic, and they have been associated with mortalities of molluscs in captivity or under culture (Ford, 2001). QPX has been found in clams from Virginia to the Canadian maritime provinces, but it appears to be most serious in the northern culture areas. Recently, it has become evident that serious outbreaks in clams being cultured in New Jersey and Virginia occurred in stocks that had come from South Carolina and Florida and not in those produced locally. This observation is supported by results of an experiment in which brood stock originating in five states from Florida to Massachusetts were spawned in a single hatchery and their offspring grown in side-by-side plots in Virginia and New Jersey (Ragone-Calvo and Burreson, 2002). In both grow-out sites, clams from Florida and South Carolina acquired numerous and heavy QPX infections and suffered high mortalities. Those from Massachusetts and New Jersey had few infections and low mortality. Clams from Virginia exhibited intermediate traits. QPX outbreaks appear to be an example of a disease caused by an enzootic parasite, which may evoke no detectable problems in a resident host but is highly pathogenic to nonlocal stocks of the same species. Considerations for Disease Risk Assessment Implications of Detecting Pathogens in Disease Surveys One of the questions raised about the potential introduction of C. ariakensis is the lack of knowledge of parasites and diseases of the species in its native range. A number of samples have been examined at the Virginia Institute of Marine Science (VIMS) and more are planned (see Chapter 4). So far the only identified pathogen has been a haplosporidian found in one of 155 oysters (0.6%) in a sample from northern China. This very low prevalence is not unusual for parasites that are present in “resistant” hosts but can cause epizootic mortalities when they infect susceptible hosts (e.g., H. nelsoni in C. gigas versus C. virginica). It is worth noting that the prevalence of H. nelsoni in various samples of C. gigas (considered “resistant” to H. nelsoni) from Korea, Japan, and California averaged <1%

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Nonnative Oysters in the Chesapeake Bay of intertidal vegetation that harbor completely different invertebrate faunas than existed previously (Posey, 1988; Carlton, 1989). Another hazard might be the introduction of a nontarget oyster species, caused by lack of care or ability to discriminate among morphologically similar species, subspecies, or physiologically distinct races. The taxonomy of Asian cupped oysters is poorly known and in a state of flux, depending on sporadic studies undertaken for various reasons (e.g., Buroker et al., 1979a, b; Banks et al., 1994; Ó Foighil et al., 1995, 1998; Boudry et al., 1998; Hedgecock et al., 1999; Day et al., 2000). In particular, two distinct geographic races of C. ariakensis have been uncovered through analysis of mitochondrial and nuclear DNA sequences since researchers at VIMS turned their attention to this species as a candidate for nonnative introduction (Francis et al., 2001). A nontarget oyster might not perform as well as the particular strains of C. ariakensis that have been tested to date in Chesapeake Bay field trials. The likelihood of rogue behavior cannot be quantified but is judged to be substantial and depends on which management strategy is chosen (see below). Rogue introductions of the Pacific oyster have occurred previously in the Chesapeake Bay and elsewhere on the East Coast. This led Maryland to adopt legislation against the introduction of this species (see Table 3.2; Andrews, 1980). Hopes for the recovery of the oyster industry have been fueled by reports about the impressive survival and growth of C. ariakensis in experimental trials. The economic motive for carrying out an illegal rogue introduction is present and is likely to build over time if native oyster populations remain depressed. Although human behavior is unpredictable, shipment of live oysters from Asia to the United States would not present an obstacle to a rogue introduction. All life stages of cupped oysters (D-hinge or later larvae, spat, and adults) are readily shipped live via air courier. Adult Asian oysters could be readily obtained and imported live to the region, probably through normal channels of seafood supply. Hundreds of adults can be shipped live in a box no larger than a typical picnic cooler; if kept moist and refrigerated, adults can survive out of water for more than a week. Obtaining larval and seed stages of C. ariakensis would require locating a cooperating hatchery in Asia, but these early life stages are attractive targets for rogue introduction because of the much larger numbers of oysters that could be imported. Commercial oyster hatcheries routinely supply farmers with late pediveliger or eyed larvae in very large numbers for remote setting; when screened from their culture water, for example, 2.5 million eyed larvae constitute a golf-ball-sized mass that is easily shipped in a small package. Eyed larvae remain competent for setting for about a week if kept moist and refrigerated. Remote setting requires little technology and minimum infrastructure.

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Nonnative Oysters in the Chesapeake Bay The likelihood of a rogue introduction resulting in the establishment and spread of a population of nonnative oysters depends on the life stage introduced, the number and density of animals introduced, the spatial scale of introduction, the spawning and recruitment potential at the sites of introduction, and the frequency of introduction. The number of adults that could be shipped and introduced at any one time would likely be limited to a few hundred individuals. A small inoculum of adults could successfully found a population, in principle, owing to the high fecundity of the oyster. Nevertheless, the chances of establishment and spread would be governed by the likelihood that environmental conditions conducive to spawning, larval development, retention in a local area, and recruitment in sufficient density for successful spawning in the next generation were met. The chances of successful spawning and recruitment are classically difficult to predict for most marine animals, including the native oyster. It is noted that successful introduction of the Pacific oyster into France was made possible by massive importation of adults and spat (Chapter 3). Much larger numbers of seed oysters could be introduced via a shipment of eyed larvae. The percentage of eyed larvae that can be successfully set is variable but probably in the range of 10 to 30%; of these, perhaps 10 to 20% might survive to a suitable size of about 8 mm. This means that from 2.5 million eyed larvae 100,000 seed could be reared and planted, of which thousands or tens of thousands might survive to reproductive maturity. With that size of inoculum, the chances of successful recruitment, establishment, and spread would be greatly increased though not guaranteed. MANAGEMENT OPTIONS The biological and social factors likely to be impacted by each of the three management options for introducing the Asian oyster, C. ariakensis into the Chesapeake Bay are listed in Table 9.2. The body of the table contains a qualitative assessment of potential outcomes for each factor under the three management options. Lack of information precludes definitive characterization of every hazard, particularly the ecological ones. Moreover, the very different ecological, economic, and social hazards cannot be weighted with respect to one another or summed to derive an overall relative risk for each management option. Table 9.2 primarily characterizes the various factors likely to be affected by the choice of management options. In the table the likelihood of a particular outcome (listed as positive, negative, or neutral) represents the committee’s assessment for each management option under a short time frame (1 to 5 years). However, there are many uncertainties and potential scenarios that could af-

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Nonnative Oysters in the Chesapeake Bay TABLE 9.2 Assessment of Potential Outcomes Under Each Management Option Biological and Social Factors No Introductiona Triploid Introductionb Diploid Introductionc Ecological       Disease introduction   − − Disease reservoir       Susceptibility to endemic pathogens or parasites   − − Impacts on ecosystem   − − Competition with C. virginica—space, food, habitat   − − Competition with other species (relative to C. virginica) Invasion   − − Dispersal beyond the bay   − − Genetic interactions   − − Water quality − + + Reef structures and services − + + Economic/social/cultural       Human health/pathogen Price     − Viability of traditional fishery − − + Fishery employment − − + Viability of aquaculture + + + Aquaculture employment + + + Tourism, recreational, sports fishery   + + Public institutions       Management effectiveness − − − Employment   + + Watermen communities − − + Watermen culture − − +

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Nonnative Oysters in the Chesapeake Bay Biological and Social Factors No Introductiona Triploid Introductionb Diploid Introductionc Cultural perception of restoration, environment + − − Political impact       Fishery − + + Environmental + − − Restoration efforts + + − Likelihood of rogue introduction + +   Impact of rogue introduction − − − Biological and social factors are likely to be affected by selection of one of the three management options with regard to introducing the Suminoe oyster into the Chesapeake Bay. The assessments given here are developed for short-term (1 to 5 years) outcomes and are listed as +, positive; −, negative; and blank, no effect. The rationale for each of these values is explained in detail in the text. There are large uncertainties associated with each outcome; therefore, these values serve as an illustration, but not a prediction, of how the various management options might compare. aEcological and economic and social outcomes assume no rogue introduction. bOutcomes assume eventual production of diploids and the establishment of small reproducing populations. cOutcomes assume large managed introduction of diploids using ICES protocols.

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Nonnative Oysters in the Chesapeake Bay fect outcomes. The qualitative characterization of risk presented in the table is meant to provide a starting point for reviewing the hazards associated with each of the three management options the committee was charged to consider. Option 1. Status Quo, No Introduction of Nonnative Oysters The first management option is simply to maintain the status quo by forbidding the introduction of all nonnative oysters into the Chesapeake Bay, whether diploid or triploid. The chief consequences likely to be associated with this action, were it successful in maintaining the status quo, would be: continued decline of the oyster fishery and erosion of the traditional economies and cultures of Chesapeake Bay watermen; possible increased pressure in the blue crab fishery; possible further declines in bay water quality, owing to loss of oyster filtering capacity, though scientific evidence that water quality is tightly coupled to oyster abundance is weak; possible continuing or accelerating losses of aquatic vegetation and oyster reef habitats, with cascading effects on the structure and stability of the bay’s estuarine communities, though scientific evidence for these assumptions is lacking; possible reduction of bay acreage protected under the Clean Water Act’s shellfish bed water quality preservation mandates; and erosion of confidence in governmental management of the living marine resources of the Chesapeake Bay. The economic or ecological harm from these hazards can be reasonably extrapolated from recent trends in the fishing sector and in bay water quality and ecology. The chief benefits of maintaining the status quo would be: avoidance of risks identified with either of the alternative options for introducing a nonnative oyster; increased emphasis on aquaculture of native oysters selectively bred for resistance to MSX and Dermo diseases; increased employment in the native oyster aquaculture sector, especially with new strains of disease-tolerant C virginica; and affirmation of cultural value on conserving native species and natural habitats. Simply banning the introduction of nonnative oysters into the Chesapeake Bay, however, will not necessarily maintain the status quo. A no-

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Nonnative Oysters in the Chesapeake Bay introduction policy would increase the likelihood of a rogue introduction, that is, a nonsanctioned direct release of diploid reproductive Asian oysters, executed surreptitiously and without benefit of adherence to ICES protocols. The economic desperation created by the collapse of the traditional oyster fishery of the Chesapeake Bay, coupled with widespread awareness of the performance of triploid C. ariakensis in previous field trials and the ease with which live animals could be acquired through traditional fish markets, makes rogue introduction an easy response to the perception of management inaction. Industry representatives, who addressed the committee, made this hazard explicit. The risks associated with rogue introductions include the risks identified under sanctioned introductions that employ ICES protocols, as well as those incurred by circumventing ICES protocols, and would remain for as long as the population of a native oyster remained depressed. If a self-reproducing population of C. ariakensis were established as the result of a rogue introduction, the resulting harms and benefits would probably increase through time, with an increase in the abundance of the nonnative oyster. Unfortunately, the specific ecological, economic, or cultural harms or benefits of a rogue introduction cannot be specified nor can their magnitudes be predicted. Finally, under this option, management would presumably be burdened with monitoring for rogue introductions and with eradication of diploid nonnative oysters were they detected. Eradication of introduced marine species is extremely difficult or impossible, as recent experiences with the invasive seaweed Caulerpa in the Mediterranean Sea at-test (Thibaut et al., 2001). Any attempt to maintain the status quo should certainly be coupled with scrutiny of why the restoration of native oysters has failed so far. Such an examination was not part of the charge of this study. Clearly, however, successful restoration of native oysters and the traditional fishery would largely have precluded the present controversy over introduction of a nonnative oyster. Option 2. Open-Water Aquaculture of Triploid Oysters Because the fidelity, stability, and sterility of mated triploids are not likely to be 100%, expanding the introduction of mated triploid C. ariakensis in controlled aquaculture settings risks establishing a diploid self-reproducing population in the Chesapeake Bay. This hazard, however, can be broken down into components, most of which can be quantified and modeled, as attempted by Dew et al. (2003), for example, who simulated the population growth and local establishment of nonnative oysters introduced by triploid aquaculture under specified ecological conditions and management strategies. Furthermore, many of the hazards

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Nonnative Oysters in the Chesapeake Bay associated with open-water aquaculture of triploid nonnative oysters can be managed to reduce specific elements of risk. For example, increasing the containment of, and accountability for, planted stock could lessen the risk that triploids would remain in the bay long enough to revert to the diploid state. Likewise, the density of planted stocks could be managed to reduce the risk that gametes released by the small percentage of diploids that might be produced along with mated triploid seed would be able to find and fertilize each other. The number of triploids introduced could be constrained to reduce risk, but this would also reduce potential economic or ecological benefits. Minimizing the duration and scale of the triploid culture effort would minimize the risks of this management option. Indeed, introduction of triploids could be used as a management strategy to buy time for restoration of native oysters, which could result either artificially (from the development of new and more successful approaches to restoration) or naturally (from a return to the more typical conditions of colder winters and wetter summers, which would inhibit parasite proliferation and provide the native oyster with more freshwater refuges from disease). Recovery of native oyster populations would reduce the incentive to introduce a nonnative species or would reduce the scale of any aquaculture sector based on the nonnative relative to the scale of a resuscitated traditional fishery. Aside from the hazard of establishing a self-reproducing population of a nonnative oyster, some short- and long-term negative impacts of this management option are: continued declines in the traditional oyster fishery or possibly accelerated declines as hope for recovery is lost and extraction is maximized; economic hardships for watermen communities, unless they switch from fishing to aquaculture; no marked improvement in bay water quality in the near term, owing to only a marginal increase in oyster filtration capacity from triploid aquaculture; continued threat of rogue introductions of diploid nonnative oysters; potential introduction of pathogens that may not be excluded by adherence to ICES protocols; potential introduction of other pathogens owing to inadvertent breaches of ICES protocols; susceptibility of nonnative oysters to endemic pathogens or parasites; conflicts with cultural value placed on conservation of native species and habitats;

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Nonnative Oysters in the Chesapeake Bay erosion of confidence in resource management; and political resistance or legal challenges by environmentalists or states from outside the Chesapeake Bay. As under the first option, management could face a considerable burden for monitoring bay waters for the establishment of diploid populations or for subsequent eradication of any diploids detected. Genetic markers could be profiled in all tetraploid and diploid stocks used to make triploids, so that the provenance of any diploids that might subsequently be detected or become established could be determined. Some short- and long-term benefits of this option, aside from those attending the establishment of a diploid population, are: management control over most aspects of the authorized introduction; viability of aquaculture; aquaculture employment; possible retention of tourism, recreational, and sports fishery benefits associated with Chesapeake Bay oysters, even though nonnative; and increased incentive for restoring the native oyster, if it serves to rally the political constituents of restoration. One important benefit to the controlled introduction of triploid C. ariakensis could be opportunities for research on the biology of C. ariakensis in the Chesapeake Bay. The likelihood of ecological harm or benefit could be more accurately assessed if basic information were available on the season of reproduction (triploids, though sterile, still go through an annual reproductive cycle), susceptibility to native pathogens and parasites, competition with C. virginica for space, and propensity to sustain old or restored reefs or to build new ones. The risks of expanded industrial trials could be partially offset by the inclusion of parallel ecological experiments designed to generate information critical to evaluating the risk that triploid aquaculture will eventually produce a diploid population. Option 3. Introduction of Reproductive Diploid Oysters This management option has strong local support because introduction of an oyster that can survive and grow in the Chesapeake Bay appears, to many, as the only hope of improving water quality and the bay’s ecosystem, recovering the traditional fishing industry and sustaining watermen culture. Behind the hope is the assumption that purpose-

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Nonnative Oysters in the Chesapeake Bay ful introduction will quickly yield a large viable population of C. ariakensis, with little or no adverse effects on the remnant native oyster population or other species. However, introductions are not always successful. Initial trials with triploid Pacific oysters in the Chesapeake Bay showed, for example, that this nonnative oyster, though resistant to the diseases that kill native oysters, was susceptible to infestation with the shell-boring polychaete worm Polydora, which made them unacceptable in the market. Still, some introductions of oysters and other bivalves have been successful in establishing industries without untoward ecological harm. The introductions of the Pacific oyster to the west coasts of North America and Europe had positive impacts on fishing and farming industries. The Pacific oyster proved noninvasive on the West Coast of North America; hence, there were no pronounced ecological changes, with the important exception of problems stemming from cointroductions (e.g., Spartina alterniflora to the U.S. West Coast; Naylor et al., 2001). The risks of cointroductions, today, would be greatly reduced by the use of ICES protocols. Finally, opponents of diploid introduction can cite counterexamples of negative ecological impacts from introductions of oysters or other bivalves. The Pacific oyster, C. gigas, in New Zealand and Australia threatens endemic oyster species; the zebra mussel, Dreissena polymorpha, has caused widespread fouling problems in the Great Lakes and other regions in North America; and the Asian clam, Potamocorbula, has greatly modified the soft benthic fauna and primary productivity of the San Francisco Bay and delta. What mix of outcomes—no impact, positive impact, or negative impact—would follow a clean introduction of C. ariakensis into the Chesapeake Bay cannot be predicted. Short- and long-term negative impacts of introducing diploid C. ariakensis into the Chesapeake Bay could include: disease introduction, though greatly reduced, would still present an unknown hazard from vertically transmitted pathogens even if ICES protocols are followed and perfectly effective; negative ecological impacts, such as competition with C. virginica or fouling of boats, marinas, and other marine structures; spread of nonnative oysters outside the bay, where competitive displacement of healthy native oyster populations might be possible; susceptibility to endemic pathogens or parasites; decreased management effectiveness; abandonment of attempts to restore the native oyster; conflicts with conservation ethic; and political resistance or legal challenges by environmentalists or states from outside the bay.

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Nonnative Oysters in the Chesapeake Bay The chief benefits of a diploid introduction would ostensibly be the same as those deriving from recovery of the native oyster population, though hard scientific evidence supporting these presumed effects is limited or lacking: possible improvements in water quality; increases in aquatic vegetation; deposition of new reefs and increases in reef habitat for fish and other invertebrates; resuscitation of the traditional oyster fishery and fishery employment; continued viability of aquaculture and increased aquaculture employment; potential increases in tourism, sports fishery, and a recreational economy; maintenance of watermen communities and culture; and reduced likelihood of a rogue introduction. All of these benefits assume that an introduction of diploid C. ariakensis would result in a large population of reef-building oysters, an outcome that is uncertain. FINDINGS The three management options (no introduction of nonnative oysters, introduction of triploids for aquaculture, and introduction of diploids) entail differing arrays of ecological, socioeconomic, institutional, and implementation risks. The risk of a disease outbreak in either the native or nonnative oyster populations following an introduction is not zero, even if ICES protocols are followed. If ICES protocols are applied, the risk of disease outbreak has low probability but potentially high impact if it occurs. Assessing an array of ecological risks is severely constrained by lack of fundamental ecological information on the Suminoe oyster, C. ariakensis, and even by lack of sufficiently detailed ecological information for the native oyster and the Chesapeake Bay. Various ecological risks that can be postulated have unknown probabilities and unknown impacts. No human health risks are apparent. The risk to human health has a very low probability and a low impact. Assessment of the risks to institutions with responsibilities for managing the living resources of the Chesapeake Bay have unknown probabilities and unknown impacts.

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Nonnative Oysters in the Chesapeake Bay The risks of rogue introductions are likely high under the no-introduction management option; may remain high to moderate under the triploid aquaculture option, particularly among the “have not” stakeholders; and are likely low to moderate under the diploid introduction model. The potential impact of a rogue introduction is high, owing to the substantial ecological impacts that have been documented following the unintended cointroduction of other organisms besides the oyster. The breadth and quality of existing information on oysters and other introduced species are not sufficient to support a comprehensive risk assessment of the three management options. Comprehensive risk assessment is also not practicable, owing to the lack of well-defined and/or conflicting objectives and goals among Chesapeake Bay management agencies and users.