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Nonnative Oysters in the Chesapeake Bay 1 Executive Summary Are nonnative oysters a potential solution or problem? This simplistic question frames the extremes of opinion over a complex and controversial issue that has embroiled the Chesapeake Bay region ever since the state of Virginia proposed introducing a nonnative oyster from Asia to revive the oyster industry. Crassostrea ariakensis, commonly known as the Suminoe oyster, is native to regions in China and Japan but is mostly unfamiliar to oyster growers and consumers in North America. Relatively little is known about the Suminoe oyster, and this has made it difficult for scientists and resource managers to decide whether this oyster has the potential to help or to hurt conditions in the Chesapeake Bay, either for the watermen or for the bay ecosystem. Hence, opinions range from the hope that the Suminoe oyster will revive a threatened industry and restore some of the filtering capacity of the original oyster population to the fear that it will be an invader that outgrows the commercial demand for oysters and upsets the ecology of the Chesapeake Bay. EXPECTATIONS AND PERSPECTIVE Declines in the quality and quantity of natural resources in the Chesapeake Bay have taken place over at least the past 150 years. Today, we stand at an unprecedented crossroads, facing a conscious decision to introduce or not to introduce a nonnative oyster in the hope that this action will improve prospects for both the fisheries and the environment. It is unrealistic to
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Nonnative Oysters in the Chesapeake Bay expect that this long-term degradation in the Chesapeake Bay could be reversed in 10 years or less through any single management action. The degradation of water quality, increased sedimentation, loss of habitats such as sea grass beds and oyster reefs, and changes in the abundances of many plant and animal species not only serve as indicators of change but also act as barriers to restoration. Improvements in the natural resources of the bay will require a multifaceted approach and sustained commitment from communities throughout the watershed toward the goal of reestablishing some of the ecological functions that have been valued for generations. Loss of the Native Oyster The indigenous oyster C. virginica has been depleted to less than 1% of its original abundance in the Chesapeake Bay through a combination of heavy fishing pressure during the 19th and 20th centuries and the recent high mortalities due to the spread of two parasites, Haplosporidium nelsoni and Perkinsus marinus, that cause the diseases MSX and Dermo, respectively. Additionally, nutrient and toxic pollutants, increased sedimentation, and loss of shell bed habitat have made the environment in the bay less conducive to recovery of the oyster population. This combination of factors has threatened the survival of the oyster industry in Virginia and Maryland. As a possible means to address this problem, Virginia has been exploring the option of introducing a nonnative Asian oyster (C. ariakensis) into the state’s coastal waters, including the Chesapeake Bay. Opinions on the likely risks and benefits of introducing a nonnative oyster differ among the states and federal agencies that participate in regional agreements through the Chesapeake Bay Program (CBP). Because of the high stakes associated with the decision to introduce a nonnative species, the Chesapeake Bay Commission (a tristate commission that serves as the legislative arm of the CBP) requested that the National Research Council undertake a study of the pros and cons of introducing C. ariakensis either as an infertile triploid (triploid oysters contain three rather than the normal two sets of chromosomes and cannot reproduce normally) for use in aquaculture or as a reproductive diploid that could either augment or supplant the diseased populations of the native oyster (see Box 1.1). In the past, introductions of nonnative species were not subjected to this level of scrutiny, but rising awareness of the potential ecological and economic problems associated with invasive nonnative species has made resource managers more cautious. Thus, this study presents a landmark opportunity to identify concerns that should be addressed by decision makers when the introduction of a nonnative marine species is under consideration.
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Nonnative Oysters in the Chesapeake Bay BOX 1.1 Statement of Task This study will examine the ecological and socioeconomic risks and benefits of open-water aquaculture or direct introduction of the nonnative oyster Crassostrea ariakensis in the Chesapeake Bay. The committee will address how C. ariakensis might affect the ecology of the bay, including effects on native species, water quality, habitat, and the spread of human and oyster diseases. Possible effects on recovery of the native oyster C. virginica will be considered. The potential range and effects of the introduced oyster will be explored, both within the bay and in neighboring coastal areas. The study will investigate the adequacy of existing regulatory and institutional frameworks to monitor and oversee these activities. The committee will assess whether the breadth and quality of existing research, on oysters and other introduced species, are sufficient to support risk assessments of three management options: (1) no use of nonnative oysters, (2) open-water aquaculture of triploid oysters, and (3) introduction of reproductive diploid oysters. Where current knowledge is inadequate, the committee will recommend additional research priorities. How Might C. ariakensis Affect the Ecology of the Chesapeake Bay? The potential effects of the Suminoe oyster on the ecology of the Chesapeake Bay may be evaluated based on past experiences with introduced species, both deliberate and accidental, and on a comparison of the biological characteristics of the nonnative oyster with the native oyster. The Pacific oyster C. gigas is the most frequently introduced oyster species. C. gigas is native to Japan, China, and Korea but is now the principal oyster harvested worldwide, having been introduced to all continents except Antarctica. Most of the problems associated with previous introductions of nonnative oysters arose from the cointroduction of other marine pest species. Shipments of Pacific oysters contained oyster parasites, pathogens, and predators as well as aquatic plants used as packing material. The risk of introducing a harmful “hitchhiking” species can be greatly reduced through application of protocols adopted by the International Council for the Exploration of the Sea (ICES). The ICES protocols require that imported aquatic organisms be maintained in quarantined facilities as brood stock. The first generation progeny of the brood stock may be transplanted into the environment if they appear to be free of parasites and disease agents. CONCLUSION: Strict application of the ICES protocols reduces the risk of cointroduction of undesirable organisms, including most pathogens and parasites. Oversight of the importation and deployment of the new species and prevention of a rogue introduction (an unsanctioned,
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Nonnative Oysters in the Chesapeake Bay illegal, direct release of reproductive nonnative oysters) will be required to prevent release of “hitchhiking” species. There remains some risk that a nonnative oyster by itself will cause serious ecological problems. The Pacific oyster C. gigas has not been an invasive species in the United States, Canada, and Europe, but in New South Wales, Australia, and northern New Zealand, it spread rapidly and depressed or eliminated active fisheries based on the indigenous rock oysters. The mixed outcomes observed with C. gigas introductions suggest that it is difficult to predict whether or not a species will be invasive. Another way to assess the potential behavior of a nonnative species in a new habitat is to compare its biological characteristics with similar endemic species. The Suminoe oyster has a range of environmental tolerances comparable to the Eastern oyster C. virginica and based on smallscale field trials it grows rapidly in the estuarine waters of the Chesapeake. The most notable characteristic of C. ariakensis is its resistance to the two diseases that currently plague the native oyster. Not much is known about the disease susceptibility of the Suminoe oyster in its home range, although there have been reports of disease problems in China. In France, C. ariakensis was found to be unsuitable because it is susceptible to a disease caused by Bonamia ostrea that also infects the European flat oyster. CONCLUSION: Based on the limited data available, it appears that C. ariakensis has environmental tolerances that make it well suited for growth and reproduction in the Chesapeake Bay and in other similar estuarine habitats on the Atlantic and Gulf coasts. It is likely to compete with the native oyster, although differences in environmental tolerances might result in these two species occupying different habitats if C. ariakensis becomes established in the bay. Research Recommendations: Develop a better understanding of C. ariakensis biology in the Chesapeake Bay under various temperature and salinity regimes, particularly its growth rate, reproductive cycle, larval behavior, and settlement patterns in different hydrodynamic regimes; size-specific, postsettlement mortality rates; and susceptibility to native parasites, pathogens, and predators. Determine the ecological interactions of C. ariakensis and C. virginica at all life stages, including interspecific competition and reef-building capacity. Determine the genetic and phenotypic diversity of different geographic populations of C. ariakensis and other closely related Asian
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Nonnative Oysters in the Chesapeake Bay species of the genus Crassostrea and the extent to which they might respond differently to the Chesapeake Bay environment. Develop an integrated approach to understanding the responses of native and nonnative oysters to environmental change and multiple stressors, including naturally occurring or introduced diseases, climate change, land use, nutrient loading, sedimentation, pollutants, and the interactions of these factors. Develop a model of oyster larval dispersion based on a detailed circulation model for the Chesapeake Bay and incorporating information about differences in the larval behavior or physiology of native and nonnative oysters to predict their dispersal patterns. What Are the Potential Economic and Social Impacts of a Nonnative Oyster? As recently as 1980 the Chesapeake Bay accounted for roughly 50% of the U.S. oyster harvest. The harvest dropped by 55% from 1991 to 2001, and the real price of Chesapeake oysters declined by 24% over the same period. The combined effect of reduced landings and reduced price resulted in a roughly 90% decrease in the value of Chesapeake oyster landings from 1980 to 2001. With this severe decline in oyster harvests, the industry’s interest in the nonnative Suminoe oyster has intensified, even if Suminoe production is limited to contained aquaculture. Because production costs are higher, containerized aquaculture is unlikely to replace wild harvest as a significant source of oysters for the shucking houses. Most intensively cultured oysters are targeted for the higher-value half-shell market. Significant price declines might occur if growth in the oyster supply occurs very rapidly, either as a result of recovery of the native oyster or through establishment of a large reproductive population of Suminoe oysters. Oystering constitutes an important part of the cultural heritage of watermen communities in both Virginia and Maryland. Even at the muchreduced harvest levels of recent years, oysters continue to provide small amounts of much-needed income during periods when watermen have no other fishing income. As winter approaches, watermen shift to the oyster harvest and thereby decrease pressure on the fall harvest of blue crabs. Virginia and Maryland differ in the structure of their oyster fisheries; during the 1990s, more than 96% of the oyster harvest in Maryland came from public beds, while over 60% of Virginia’s harvest came from private leased beds. This places Virginia in a better position to take advantage of the introduction of a new oyster that at least initially will
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Nonnative Oysters in the Chesapeake Bay require hatchery production of triploid spat and containerized aquaculture production methods. CONCLUSION: Although communities in both states value the oyster fishery, policy differences regarding the relative distribution of public grounds and privately leased submerged oyster beds in Maryland and Virginia will have a significant effect on the ease with which the industry in each state adapts to dependence on hatchery production. Research Recommendations: Examine Public versus Leased Oyster Beds. The mix of publicand leased-bottom oyster fisheries has been evolving. A better understanding of the institutional differences, their consequences, and their possible evolution will be critical for predicting the outcome of the management options, the ability of managers to oversee and control production practices, and the potential for Maryland and Virginia oystermen to compete with producers in other regions. Establish an Ongoing Economic and Sociocultural Data Collection Program. The ability of social scientists to predict or evaluate the outcomes of potential management actions is impaired by the lack of both baseline and postimplementation data necessary to evaluate the effects of management action separately from the effects of unrelated changes in the fishery. This research program could be organized through Sea Grant or through a multistate entity but should be designed and budgeted for a full 5- to 10- year period. Examine Economic Feasibility of Alternative Production Systems. Estimates should be developed for the profitability of public grounds versus private leased-bottom fisheries in Virginia and Maryland for different production modes. Triploid nonnative aquaculture estimates should account for the costs of antipredator strategies and biocontainment safeguards. Develop Models of Community and Household Impacts of Alternative Production Systems. The impacts of shifting traditional fisheries into aquaculture-based production will depend on the economic consequences and effects on local sociocultural norms. Data for building these models should be collected from both comparable case studies of traditional fisheries shifting into aquaculture-based production and structured interviews with watermen and coastal community members to solicit their perceptions of the likely effects of the various management options.
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Nonnative Oysters in the Chesapeake Bay Adequacy of Regulatory and Institutional Structures The regulatory framework that addresses the deliberate introduction of nonnative species into marine waters presents a patchwork of state, regional, federal, and international legislation and directives that leave significant gaps in the ability to monitor and oversee the use of exotic organisms. In the Chesapeake Bay, nonnative introductions are covered by the 1993 Policy for the Introduction of Non-Indigenous Aquatic Species through the region’s CBP, but the recommendations made by the program are not legally binding. At the federal level there is limited regulation of nonnative introductions under the Lacey Act, which prohibits the importation of certain species found to be injurious. Species not named on this “black list” are regulated under authority delegated to the states. The U.S. Army Corps of Engineers has permitting authority over aquaculture operations that use in-water structures or fill. Under this authority, the Corps reviews the entire proposal for compliance with other federal statutes such as the Clean Water Act and the Endangered Species Act. CONCLUSION: The existing regulatory and institutional framework is not adequate for monitoring or overseeing the interjurisdictional aspects of open-water aquaculture or direct introduction of C. ariakensis. There is no federal legislation that gives specific criteria for regulating the introduction of a nonnative marine species. States may set their own criteria, but when an introduction is likely to affect neighboring states, there is no statutory mechanism for resolving differences among the interests of affected states. Research Recommendation: Although the CBP is well positioned to air the concerns of the participating state and federal agencies, its decisions are non-binding. The program should be evaluated as a potential venue for interjurisdictional decision making. Also, the review should identify institutional changes that would be required for the CBP, or other regional body, to assume binding authority over management decisions that will potentially affect coastal areas of more than one state. MANAGEMENT OPTIONS The committee was asked to evaluate whether the breadth and quality of existing research are sufficient to support risk assessments of three management options: (1) no use of nonnative oysters, (2) open-water aquaculture of triploid oysters, and (3) introduction of reproductive diploid oysters. The risks and benefits associated with the three management options are discussed individually below. The major concern and greatest uncertainty relates to the likelihood that C. ariakensis will become an inva-
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Nonnative Oysters in the Chesapeake Bay sive nuisance species and potentially threaten the ecological integrity of the Chesapeake Bay and adjacent waters along the Atlantic coastline or in the Gulf of Mexico. Option 1: Prohibit Introduction of Nonnative Oysters Under the first management option, introduction of any nonnative oyster would be prohibited even if the oysters were reproductively sterile. This option precludes risks associated with the introduction of a nonnative species. Another benefit is preservation of the cultural value associated with native species and natural habitats. The main risk identified with pursuing this option would be a continued failure of native oyster restoration efforts with continued decline of the oyster fishery and erosion of the traditional economies and cultures of Chesapeake Bay watermen. Under this option there are additional risks that would arise if the native oyster population failed to rebound, including an erosion of confidence in the ability of managers to address resource problems and continued loss of the ecological functions associated with healthy oyster beds, such as habitat and filtering capacity. An additional risk under this option could arise if frustration with the slow pace of restoration leads to the importation and illegal release of Suminoe oysters. Suminoe oysters could be imported for seafood markets, but if they were released into open waters they could carry oyster pathogens or harbor other undesirable marine species. Introduction of an oyster pathogen or nonnative pest species is generally irreversible. The threat of a rogue introduction could be reduced by identification and vigilant monitoring of likely routes of importation and critical points where interdiction might be achieved. Review and enforcement of regulations against rogue introductions by the responsible state agencies would help avoid a situation in which the states were faced with developing burdensome programs for eradication of nonnative oysters and associated organisms. Public education on the high risks associated with a rogue introduction could be used to increase awareness and vigilance. CONCLUSION: The long-term risk of an outright prohibition on the use of nonnative oysters (either for controlled aquaculture or for deliberate release into open waters) depends on the potential success of restoration programs for the native Eastern oyster. Research Recommendations: Development of an integrated science-based approach to restoration of the native oyster. This would include a selective breeding
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Nonnative Oysters in the Chesapeake Bay program focused on building genetically diverse, native oyster stocks less susceptible to Dermo and MSX diseases. Determination of the causes of recruitment success or failure for C. virginica and evaluation of the success of oyster sanctuaries. Determination of the genetic and physiological bases for disease susceptibility, tolerance, and resistance. Assessment of the native oyster restoration program for probable level of success and the near- and intermediate-term economic consequences posed for watermen. This should include expected net benefits and variance of expected net benefits for harvesting and processing sectors in Maryland and Virginia with probable levels of recovery for each year of the program. Option 2: Open-Water Aquaculture of Triploid Oysters Aquaculture of sterile triploid C. ariakensis in controlled settings, as proposed by the Virginia Seafood Council, may result in the establishment of a diploid, self-reproducing population in the Chesapeake Bay because the process of generating mated triploids is not 100% effective and some triploid oysters may become reproductive as they age. The risk of establishment of a reproductive population of Suminoe oysters will increase with an increase in the scale of the commercial aquaculture operations. Many of the risks associated with the use of triploid nonnatives for aquaculture can be identified, quantified, and managed, as elaborated in Chapter 9 of this report. Aside from the hazard of establishing a self-reproducing population of a nonnative oyster, potential short- and long-term negative impacts of triploid aquaculture include continued or accelerated declines in the traditional oyster fishery, economic exclusion of some harvesters due to the high investment costs required for converting to aquaculture production, potential introduction of pathogens not excluded by adherence to ICES protocols, and conflicts with the cultural value placed on conservation of native species. Managers could face a considerable burden for monitoring aquaculture operations and surveying the bay to detect stray nonnative oysters. Expenses would increase if reproductive oysters were found and it became necessary to eradicate them. Some of the short- and long-term benefits of this option include regulatory and management control over most aspects of the use of nonnative oysters; improved viability of oyster aquaculture; increased employment in the aquaculture sector; and possibly reduced harvest pressure on sanctuaries established for restoration of the native oyster. A major benefit of the controlled use of triploid C. ariakensis would be increased potential for research relevant to assessing the risk of introducing a reproductive popu-
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Nonnative Oysters in the Chesapeake Bay lation in the Chesapeake Bay. For example, the likelihood of ecological harm or benefit of widespread triploid-based aquaculture or direct introduction 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) and the susceptibility of C. ariakensis to native pathogens and parasites. One potential short-term benefit might be the community’s perception of progress with respect to resource management, especially if this perception were to reduce the risk of a rogue introduction. This option also buys time for recovery of the native oyster, with either a reduction in the severity of oyster diseases because of more favorable climate conditions or through breakthroughs in the restoration of the native oyster, such as the development of disease-resistant populations. Revival of the native oyster would likely reduce the pressure for nonnative introduction. CONCLUSION: Contained aquaculture of triploid C. ariakensis provides an opportunity to research the potential effects of extensive triploidbased aquaculture or introduction of reproductive nonnative oysters on the ecology of the bay and offers some additional economic opportunities for the oyster industry and the watermen. Research Recommendations: To fully assess the risks associated with the larger-scale and longer-term aquaculture of triploid C. ariakensis requires research in the areas listed below. Determination of the susceptibility of C. ariakensis to the parasite B. ostreae through challenge experiments and comparison of the DNA sequence of the Bonamia-like organism associated with a C. ariakensis mortality event that occurred in France (archived material from IFREMER, La Tremblade) with known B. ostreae sequences. Development of sufficient data on the fidelity, stability, and fertility of mated triploid C. ariakensis to permit estimates of means and variances in parameters such as the proportions of triploids, diploids, or mosaics in lots of mated triploid seed. Determination of the proportion of triploid individuals undergoing gametogenesis, the fecundity of triploids, the types and proportions of gametes produced by triploids, and the fertility of these gametes. Determination of the maximum proportion of reproductive oysters that can be raised in containers of triploids without successful spawning (i.e., fertilization) under various conditions of water flow.
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Nonnative Oysters in the Chesapeake Bay Option 3: Introduction of Reproductive Diploid Oysters This management option has strong support in some sectors because of fear that the native oyster will never recover and the belief that introduction of a nonnative oyster that is resistant to disease is the only option for sustaining the traditional fishery and lifestyle of the watermen in the Chesapeake Bay. Underlying this support is the assumption that a purposeful introduction will yield a large population of Suminoe oysters after a few years with little or no adverse effects on the native oyster or other species. Potential short- and long-term risks of introducing reproductive C. ariakensis into the Chesapeake Bay include the introduction of a new disease (greatly reduced but not eliminated if ICES protocols are followed); competition with C. virginica or fouling of boats, marinas, and other marine structures; dispersal of nonnative oysters outside the bay where competitive displacement of robust native oyster populations might occur; low market demand for nonnative oysters; susceptibility to endemic pathogens, parasites, or fouling organisms or to lower consumer acceptance; abandonment of attempts to restore native oyster; and conflicts with the conservation ethic for maintaining native species. The potential benefits of a deliberate introduction of reproductive nonnative oysters, if successful, would be similar to those expected from recovery of the native oyster population. Some of these benefits may only be realized over the long term and only if the Suminoe oyster withstands environmental stresses of low water quality, limited habitat, and high sedimentation. With a deliberate introduction, the likelihood of a rogue introduction should be reduced. A successful introduction could improve the profitability of the traditional oyster fishery. Establishment of a dense population of nonnative oysters could improve water clarity in shallow embayments due to the oysters’ filtering activity. Also, Suminoe oysters may form additional reef structures that provide habitat for fish and other invertebrates. The potential ecological impacts of a reproductive Suminoe oyster population will depend on as yet uncharacterized attributes of this species (e.g., temperature and salinity preferences for spawning and larval development, reef-forming capacity, susceptibility to predators and parasites, substrate preferences for larval settlement) that will affect the size of the population in any given area and hence the magnitude of the ecological effects. CONCLUSION: It is not possible to predict if a controlled introduction of reproductive C. ariakensis will improve, further degrade, or have no impact on either the oyster fishery or the ecology of the Chesapeake Bay.
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Nonnative Oysters in the Chesapeake Bay Research Recommendation: Further research for assessing the risks of establishing a reproductive population of Suminoe oysters in the Chesapeake Bay should include: determination of the oyster’s capacity to survive and reproduce; analysis of the Suminoe’s reef-building capacity; investigation of competitive interactions with the native Eastern oyster; and assessment of the marketability of naturally spawned, nonnative oysters harvested with tongs, rakes, or dredges or taken by divers. Choosing Among the Management Alternatives Development of a quantitative risk assessment model would require a great deal of additional research over a long period of time. Because of the dire circumstances faced by the oyster industry, resource managers are under pressure to make a decision about whether or not to proceed with the use of the nonnative oyster despite uncertainty in the type and magnitude of the potential risks. This is a particularly difficult decision due to the uncertainty of all options and the perceptions on all sides that a decision either way will have lasting and serious consequences. Option 3, introduction of diploid, reproductively competent, nonnative oysters may or may not increase the abundance of oysters in the Chesapeake Bay or have a detrimental impact on the ecology of the bay and adjacent waters. This option would be essentially irreversible and would be ill advised given current knowledge. Option 1 is ecologically reversible, since the nonnative oyster could always be introduced at a later time. However, the economic decline of watermen and fishery-dependent communities may become irreversible if oyster abundance remains extremely low. Under Option 1 the threat of a rogue introduction must be addressed because of the high risk of introducing other potentially harmful species or disease-causing organisms to the bay and midAtlantic region. Rogue introductions also threaten the region’s fisheries because of the risk of introducing a new predator or disease. Option 2, aquaculture of triploid, nonnative oysters is unlikely to solve the fishery crisis, but it is reversible, at least in its early stages, and offers more opportunity for adapting management to changing circumstances. Over the long term, the risk of establishment of a nonnative oyster population increases due to the risk of diploid production from triploid stocks. Adoption of triploid C. ariakensis aquaculture may be perceived as progress in reversing the decline of the fishery, possibly reducing the incentive to pursue a rogue introduction. Option 2 has already received considerable
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Nonnative Oysters in the Chesapeake Bay scrutiny by the CBP and its member states and federal agencies. Limited field trials have been completed in Virginia and North Carolina and larger trials are in advanced planning stages. The risks of proceeding with triploid aquaculture in a responsible manner, using best management practices, are low relative to some of the risks posed under the other management options. Strict standards and protocols are required to reduce risks and enhance benefits of this course of action. CONCLUSIONS: Option 2 should be considered a short-term or interim action that provides an opportunity for researchers to obtain critical biological and ecological information on the nonnative oyster required for risk assessment. This option also allows for more management flexibility in the future depending on the status of the native oyster and the success of restoration efforts. Stringent regulations will be necessary to ensure that aquaculture of triploid C. ariakensis does not result in the establishment of a self-reproducing population in the Chesapeake Bay region. Recommendations for Establishing Standards for Nonnative Oyster Aquaculture Before the commencement of open-water aquaculture (or pilot-scale field trials) of triploid nonnative oysters, the committee recommends developing a protocol to minimize and monitor the unintentional release of reproductive C. ariakensis, similar to the Hazard Analysis Critical Control Point protocol currently used to ensure seafood safety. This protocol should establish: acceptable limits for a variety of biological parameters to prevent release of reproductive nonnative oysters from the culture system; disease and quarantine certification of brood stock; confinement and accounting of nonnatives at all life stages; fidelity of triploid induction and the stability and sterility of triploids; and parameters of growth, survival, reproductive maturation, and fecundity of cultivated triploids. Monitoring systems for ensuring these limits at each control point should be established. The protocol for controlled introduction of triploid nonnative oysters should identify corrective actions when monitoring re-
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Nonnative Oysters in the Chesapeake Bay veals that a critical limit has been exceeded. Parties responsible for corrective actions and for record keeping should be identified. An independent verification of the effectiveness of the protocol and means of assessing failures should be established. For instance, genetic identification of hatchery stock could be used to track the source of any nonnatives discovered outside containment.
Representative terms from entire chapter: