Aquaculture, Methods of Sustainable

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1 9174 hellfish Aquaculture, Methods of ustainable Books and Reviews Bossart G (2006) Marine mammals as sentinel species for oceans and human health. Oceanography 19: Boyd IL, Bowen WD, Iverson J (eds) (2010) Marine mammal ecology and conservation, a handbook of techniques. Oxford University Press, New York Gulland FM (1999) tranded seals: important sentinels. J Am Vet Med Assoc 214:1191 cotch ML, Odofin PR (2009) Linkages between animal and human health sentinel data. BMC Vet Res 5:15 hellfish Aquaculture, Methods of ustainable FRANCI X. O BEIRN 1,CHRITOPHER W. MCKINDEY 2, THOMA LANDRY 3,BARRY A. COTA-PIERCE 4 1 Marine Institute, Galway, Ireland 2 Ocean and Environmental ciences Division, Fisheries and Oceans Canada, Institut Maurice-Lamontagne Fisheries and Oceans Canada, Mont-Joli, Québec, Canada 3 Fisheries and Oceans Canada, Gulf Fisheries Centre, Moncton, NB, Canada 4 Graduate chool of Oceanography, Rhode Island ea, Grant College Program, University of Rhode Island, URI Bay Campus, Narragansett, RI, UA Article Outline Glossary Definition of the ubject Introduction Interactions of hellfish Culture Evolution of ustainability for hellfish Culture Measuring ustainability: The Development of Indicators Progressing ustainability in hellfish Aquaculture Future Directions Bibliography Glossary Azoic conditions Conditions that prevail when no organisms or their remains are found in a system as a consequence of stress on a system. Biodeposition Organic matter deriving from (shellfish) species that falls to the seafloor. The matter can take the form of feces, pseudofeces, or the shellfish themselves. Far-field effects The effects of impacts of activities measured at a predefined distance or time from the location of the pressure. The effects may or may not be distinguishable from other effects in the system leading to cumulative impacts. Ecological aquaculture The implementation of aquaculture practices whose design and implementation result in economically viable and socially responsible aquaculture systems. Integrated coastal zone management (ICZM) The management of activities in marine environments in a coherent and practical fashion so as to result in the most efficient use of resources and avoid conflicting claims on space and missed opportunities for more sustainable coastal development. Performance standards Defined expectations represented by some measurable variable which reflects the impact an activity will have on the marine environment. Best management practices A series of operating procedures, schedules of activities, and other management practices that aquaculture operations can use to prevent or reduce impact on the marine environment while retaining an economically viable operation. Definition of the ubject Worldwide aquaculture production of finfish and shellfish species is an ever-increasing sector of food production and now represents nearly half (48%) of all aquatic species intended for human consumption [1]. It is thought that the increased aquaculture production is driven primarily by the vacuum created as a consequence of the static (or declining) status of wild capture fisheries allied to an overall greater demand for fishfood products [1]. This generalization is broadly accepted as the primary driver for increased aquaculture production; however, more specific drivers may be, increased profit as a consequence of targeted marketing allied with development of new species in developing countries and as a means of providing more self-sufficient mechanisms to grow fishfood and provide a regular income in developing countries. Typically, aquaculture production has been dominated by the culture of

2 hellfish Aquaculture, Methods of ustainable 9175 finfish species; however, shellfish production has shown a steady increase in production over the last number of decades [1] and represents 27% by weight and 15% by value of worldwide aquaculture production. The culture of shellfish in aquaculture is comprised primarily of species of crustaceans (e.g., shrimp and crab) and molluscs (e.g., oysters, clams, mussels). A major distinction between the crustaceans and molluscs is that crustaceans, as omnivores, typically require the input into their culture system of feed, usually derived from external sources (e.g., fish protein or oils). Consequently, issues surrounding the sustainability of crustacean culture as activities are more akin to those encountered with finfish aquaculture. Molluscs, particularly those identified above, are filter feeders. Filter-feeding organisms, for the most part, feed at the lowest trophic level, usually relying primarily on ingestion of phytoplankton. The process in extractive in that it does not rely on the input of feedstuffs in order to produce growth. The steady increase in world aquaculture production over the last number of decades allied with greater environmental awareness has resulted in an increased level of scrutiny of these activities in relation to their interactions with the environment. The increased focus on environmental issues in the marine environment (driven by consumer demands and/or regulatory requirements) has resulted in a concomitant increase in efforts to identify methods to culture shellfish that are considered sustainable. Consequently, there is a move toward rearing aquatic shellfish species in the marine environment such that negative interactions are minimized. In addition, it has also become apparent that there are considerable marketing benefits that will accrue as a consequence of food being reared in an environmentally acceptable fashion. These efforts (to identify and activate more sustainable method of culture) have been driven both by industry and environmental nongovernmental organisations (e.g., Pacific hellfish Growers Association and World Wildlife Fund) as well as regulatory drivers (e.g., Natura 2000 Legislation in the European Union). Notwithstanding the efforts to carry out shellfish aquaculture activities in a more sustainable fashion, there is still some confusion relating to the definition of sustainability and how an activity might be carried out in a sustainable fashion. At first, identifying if an activity and its consequences in the marine environment is acceptable or not will help define whether the activity is sustainable. Clarifying or clearing defining some of the terms utilized in this subject area will lend itself to a clearer and understandable of how the culture of shellfish can be managed to achieve sustainability goals. Introduction Worldwide aquaculture production has increased steadily since 1980 [1]. Production of aquatic products in 1980 accounted for 7% of food fish supply (five million tons), in 2007 this quantity had risen to 50 million tons. Based upon current trends, it is apparent that production of shellfish will continue to increase at a stable rate (6.5% per annum since 2002). This increase is fueled by an increase in market demand, adoption of more efficient and effective culture methods, and the financial rewards associated with the production of value-added products to higher end markets. Notwithstanding the important differences between finfish production and the majority of shellfish production methods, i.e., the introduction of feedstuffs into the environment, which has led to well-documented resource demands and impacts on the marine environment, shellfish aquaculture also has the potential to impact on the marine environment in a negative fashion if not carried out in a responsible manner. This is underpinned by a background of greater environmental awareness and increased legislative drivers toward maintaining biodiversity and minimizing negative interactions between a range of conservation goals and development activities. ome authors [2] correctly highlight that aquaculture cannot be considered as one single monolith, which can be tarnished with the single level of criticism, as it reflects a diverse array of species, methods, and potential interactions. In addition to the differences highlighted above between those culture methods reliant on input of feedstuffs necessary for the culture of some species (finfish and crustaceans), the degree of structural input and environmental alteration is also highly varied among the different species cultured and the method employed. In short, this entry will identify some of the issues associated with sustainability of shellfish aquaculture and whether or not the efforts directed to date are considered to be on a trajectory toward sustainability [3].

3 9176 hellfish Aquaculture, Methods of ustainable Interactions of hellfish Culture Early incarnations of shellfish culture are considered not far removed from wild fisheries in that the activities were broadly extensive with only small-scale manipulation of stocks (e.g., movement of wild seed to production areas; an activity still practiced today with on-bottom mussel and oyster culture). Over time, the industry has evolved with the development of more contained systems. With such intensification, the risk of detrimental environmental interactions increased, e.g., disease risks or greater deposition of organic matter beneath structures, as a consequence of higher holding densities of culture organisms. Notwithstanding density-related issues, in many instances, it is not the presence of the culture organisms that result in largely negative interactions but the activities associated with the culture mechanisms, e.g., dredging extensive culture systems, pesticides, or chemotheraputents in pond systems. The culture of shellfish (bivalve molluscs) as distinct from finfish and crustaceans, for the most part, requires no input of feed to the culture process. Given this difference, this entry will focus primarily on the culture of molluscan shellfish (primarily bivalves). Under certain circumstances, e.g., hatchery production of shellfish, the input of feed in the form of phytoplankton is required to produce seed [4]. Thereafter, for the majority of their life cycle, shellfish consume at the lowest trophic level, feeding largely as herbivores and relying on ambient seston [5]. This distinction is important in that it highlights the fact the culture of shellfish, upon harvest, is considered a process that facilitates the net export of carbon (and other nutrients) from marine systems. While this may be considered an exploitation of a resource and detrimental to the system, there are situations where this is also inherently beneficial to the ecosystem. The impacts of shellfish culture have been well documented in research literature where specific interactions are described and quantified (Table 1). In addition, this topic has been a subject of numerous reviews highlighting similarities and differences inherent in culture methods and considers the factors governing any differences observed. The extent of the interactions between shellfish culture and the environment are primarily a function of the type of species being cultured, the system of culture, and the properties of the receiving environment. Table 1 provides a summary of the interactions identified between shellfish culture practices and the environment. The interactions are summarised as the mechanism which acts on the system. For example, the dredging associated with the collection of mussel seed for aquaculture practices can have the effect of physically disturbing the seafloor and the organisms therein (the impact indicator). It has been demonstrated empirically that this activity can have an impact at the community level of marine ecosystems. The culture of shellfish species using structures presents a number of likely interactions. The use of structures, i.e., bags and trestles, longlines with droppers will increase the density of culture organisms above the seafloor, thus influencing the flux of material and nutrients to the seafloor and into suspension. This higher density can also modify water flow in and around the culture system. These and other more general interactions are discussed below. Nutrients Bivalve shellfish can function in the ecosystem by filtering seston and releasing nutrients in solid or dissolved forms. They are responsible for deposition onto the seafloor of particulate matter (as either feces or pseudofeces), thus influencing benthic-pelagic coupling of organic matter and nutrients. The deposition of organic matter by molluscs has been demonstrated to impact on the infauna organisms and communities found in sedimentary environments. The changes have broadly reflected the Pearson Rosenberg [6] pattern of community development whereby moderate increases in organic matter stimulate species richness and abundance. Further increases in organic matter could result in a reduction in species richness and abundance such that excesses result in azoic conditions as a consequence of protracted anoxic conditions. The effects of biodeposition are exacerbated by the increase in density of culture organisms above the seafloor. The use of bags on trestles (e.g., oyster culture) and longlines (with mussels) will increase the density of culture organisms over a particular point and increase the risk of impact due to biodeposition. While effects of organic loading have been demonstrated with shellfish

4 hellfish Aquaculture, Methods of ustainable 9177 hellfish Aquaculture, Methods of ustainable. Table 1 Interactions between shellfish culture methods and the environment identifying the interaction route and indicator Culture type (species) Interactions Indicator References Off-bottom uspended culture (e.g., mussels, oysters) using longlines, rafts, floating bags On-bottom (Mussels, oysters, clams) Water flow alteration Depostion of organic matter (feces and pseudofeces) hading Habitat creation/fouling eston filtration Nutrient exchange Introduction of exotic species with culture organisms Physical alteration, dredging, intertidal picking ediment particle size analysis (PA) increase in fine sediment composition due increased sediment deposition or increase in coarse sediment complement due to scouring Benthic infauna adjustment in species composition and abundance; community composition [7, 79 85, 163] [86 89] Increase in sulfide reduction, Decrease in REDOX [84, 88, 90 93] depth; ediment biogeochemistry changes Benthic infauna [81, 86, 87, 94, 95] Condition of light-sensitive species (macroalgae, [96, 97] maerl, eel grass) econdary production on culture organisms or structures. Increased nekton species Alteration of phytoplankton communities, impact on production/ecological carrying capacity; changes in zooplankton assemblages Ammonium, DIN increased primary production, N2 removal via harvest or denitrification [22, ] [80, ] [93, ] Presence of non-endemic or exotic species [22, 112, 151] Benthic infauna [86, 114, 115] Monoculture Epifuana community alteration: PA alteration [52, 86, 89, 91, 96, ] Depostion of organic matter (feces and pseudofeces) hading Habitat creation/fouling eston filtration Nutrient exchange Introduction of exotic species with culture organisms Increase sulfide reduction, Decrease in REDOX depth; sediment biogeochemistry changes [ ] Benthic infauna [8, 127] Condition of light-sensitive species (macroalgae, [11] maerl, eel grass) econdary production on culture organisms or structures Alteration of phytoplankton communities, impact on production/ecological carrying capacity; increased light penetration Increased primary production, N 2 removal via harvest or denitrification; alteration of N:P ratios [78, 79, 89, 115, ] [11, 91, 106, 107, 109, ] [109, 110, ] Presence of non-endemic of exotic species [112, 113]

5 9178 hellfish Aquaculture, Methods of ustainable culture activities, the impacts are considered relatively small when compared with other culture systems where externally derived organic matter, i.e., food, is inputted directly to the system, e.g., finfish culture. A number of factors mediate the level of impact on the seafloor. In addition to density of culture organisms, the hydrography of the system including residence time, tidal range, and residual flow will all dictate the likely influence the extent of an impact on the seafloor. The greater the residual flow and/or tidal regime, the risk of accumulation of organic material is reduced [7, 8] due to the dispersive regime. imilarly, the high density of structures can result in the impediment of water flow (baffling effect), slow it down, and cause localized deposition of suspended material on the seafloor. Depending on the extent of the structures, the effect can be localized or extensive [9] with concomitant impacts on sedimentary infauna. Organic deposition by shellfish on the seabed can also influence the remineralization of nutrients in marine systems. This process as well as normal excretion (of ammonium NH 4 + ) demonstrates that shellfish in both their natural state and in culture can influence nutrient dynamics in marine systems. In fact, in a coastal bay in France it has been estimated that between 15% and 40% of nitrogen in the system is derived from oysters in culture [10]. Notwithstanding the factors that govern extent of impacts on systems, molluscs are considered net consumers of particulate and dissolved nutrients, and, by virtue of the movement of product to market the nutrients are exported from the system. The area required to assimilate material is generally confined to the production area and as such the area required to assimilate material is less with culture than without. Filtration Bivalve shellfish (oysters and mussels) have a high filtration capacity and can respond rapidly to changes in phytoplankton abundance (as a result of eutrophication) in marine systems. In nearshore marine environments, the presence of large numbers of bivalve shellfish has provided the system with the ability to buffer the effects of large phytoplankton blooms. This phenomenon applies equally to shellfish in culture which likewise provides the system with resilience against natural or anthropogenically derived fluctuations in phytoplankton numbers (blooms) [11 14]. As a consequence of this phenomenon, the subsequent removal of natural bivalve populations from marine systems (e.g., by fishing) has resulted in welldocumented ecological shifts in system processes. The dramatic reduction of oyster numbers in the Chesapeake Bay (UA) has coincided with a deterioration in water quality of the Bay; this situation was exacerbated by increased athropogenic pressures [15 17]. hellfish in culture while having demonstrable localized effects do also appear to have the ability to moderate the effects of nutrients more broadly in marine systems [9, 18]. Exotic pecies The importance of aquaculture as a vector for the introduction and spread of exotic species has been well documented [19 23]. There are two broad classes of introductions that may result from bivalve aquaculture. First, there is the establishment and spread of nonendemic species that have been intentionally introduced into an area for aquaculture purposes, the target species. Classic examples of this include the establishment of the Pacific oyster (Crassostrea gigas) on the Pacific coast of North America [24] and in various countries throughout Europe [25 27] and of the Mediterranean mussel (Mytilus galloprovincialis)in outh Africa [28]. More recently, the large expansion of C. gigas in the Oosterschelde and the Dutch and German Wadden ea have been a cause of concern in both countries from a fisheries, ecological, and human health perspective. Wild populations of the Pacific oysters have expanded from 15 ha in 1980 to 750 ha in 2005 in the Oosterschelde [29]. They have become a competitor (for space and food) with the commercially important mussel industry [25, 30]. In addition, they have become an increasing health risk associated with human encounters given the sharp nature of the shell [31]. Efforts to remove wild Pacific oysters from the Oosterschelde in the Netherlands are ongoing (Aad maal, IMARE, NL personnel communication). It is important to note that in the Netherlands, Pacific oysters were first introduced by broadcast spreading in an uncontained fashion on the seabed under the assumption that the summer temperatures were such that they

6 hellfish Aquaculture, Methods of ustainable 9179 would not successfully complete gametogenesis, spawn, and most importantly recruit. econd, there is the establishment and spread of species that are associated with the introduced bivalves [32, 33]. These species may include both hitchhiking species animals, plants that grow associated with the bivalves and diseases or parasites that may cause outbreaks in the same or other species [34]. This acts at two spatial scales: at an interregional or international scale with respect to the initial introduction of hitchhiking species and also at a regional scale, where the transfer of stock among sites may be very important to the spread of established exotic species locally [35]. The provision of novel habitat by the species being cultured may also allow for the establishment or amplification of exotic species that may be introduced through other vectors or of native species that thrive in the novel habitat [36 38]. Introductions of the C. gigas, and to a lesser extent C. virginica and other oyster species, outside of their native range for aquaculture have been suggested to be one of the greatest single modes of introduction of exotic species worldwide [19, 39]. For example, transfer of organisms with bivalves has been suggested to be the most important source of exotic species in northern Europe [17, 40] and among the most important vectors elsewhere in that continent [17, 41, 42]. In the northeast Pacific, some authors suggest that oyster (C. gigas) introductions have even been the major source of introduction of exotic molluscs [14] and invertebrates in general [43], historically contributing at least as many of the exotic species in that area as has international shipping. The slipper limpet (Crepidula fornicata), originally introduced into England with C. virginica, has had great impacts on some benthic communities in Europe, particularly in France [44] and the UK [45]. It has displaced important commercial bivalves, such as the great scallop (Pecten maximus) in some areas and native oysters beds in Normandy [46] and the south coast of England [39]; however, in other areas where it has not proliferated as much, it appears to have had little effect on overall macrobenthic community diversity [47]. Introductions have not just been confined to macrofaunal species. Oyster introductions have also been strongly implicated in the introduction of parasitic organisms and macroalgal species into novel regions [48 50]. Notwithstanding the records of aquaculture-mediated introductions of nonnative species into marine systems, there still appears to be a paucity of information and experimental evidence quantifying the impacts of nonnative oyster introductions on the receiving environment [13]. The structures associated with shellfish culture (e.g., ropes, bags, floats) in some areas provide novel habitat for the colonization and proliferation of exotic species [18]. In addition to the likely effects on system function, the colonization of structures associated with shellfish culture also presents practical problems for the aquaculturists from a husbandry perspective. Biodiversity The physical presence of large numbers of shellfish in culture can result in a monoculture which has a finite period of time in the system as a consequence of husbandry practices, e.g., thinning or harvesting. Given this constraint, the development of communities associated with the cultured shellfish will be restricted and hence biodiversity is likely to be reduced. This is particularly true if the culture period is short (i.e., approximately 1 year). The activities associated with shellfish culture can also be impacting. For example, dredging associated with on-bottom culture of mussels and oysters can cause damage to seabed (and organisms therein) and cause sediment plumes to be distributed beyond the culture environs [51, 52]. tructures The culture of shellfish species using structures presents a number of likely interactions with the environment. The use of structures, i.e., bags and trestles, longlines with droppers will increase the density of culture organisms above the seafloor, thus influencing the flux of materials and nutrients to the seafloor and into suspension. The physical presence of the structures can also modify water flow in and around the culture system resulting in increased deposition of material or scouring in areas of higher flow. Either way there is a potential to impact on the sediment structure and associated communities. As stated above, shellfish aquaculture can also provide structures that can provide for the proliferation of individual (fouling)

7 9180 hellfish Aquaculture, Methods of ustainable organisms in a system. ome of which might be new to the system. Finally, the physical presence of the structures and culture animals can have the effect of shading the seafloor and thus potentially impacting on species reliant on light (e.g., maerl or seagrasses). The interaction of shellfish culture activities with the marine environment can be considered from the perspective of near-field and far-field impacts. While near-field effects are more easily measured (using many standard near-field impact indicators identified in Table 1) and mitigated, the measurement of far-field effects is more difficult to achieve, although some of the impacts might be lessened if near-field activities are reduced or mitigated. Other far-field effects may not be as easily measured and assigned to a specific causative activity (as there may be multiple causative factors) yet they all must be considered when managing marine systems. To this end, a number of authors (e.g., Tucker and Hargraves [163]; Costa-Pierce and Page [3]) have provided a good contextual presentation on the issues surrounding sustainability of aquaculture activities. They acknowledge that sustainability solutions can extend from ecological, technical, and socioeconomic and cover very small spatial scales to adjusting broader societal values. It is important to appreciate that in order to manage activities in marine systems, it is imperative that there is a good understanding linking the culture practice to a specific environmental response. These interactions are important in order to coordinate management responses between regulatory agents and aquaculture operators, in order to minimize negative environmental effects while maintaining production returns and hence, profits. Evolution of ustainability for hellfish Culture It is widely accepted that most human activities in the marine environment will have some effect on marine species and habitats. The scale of these impacts depends on the nature of the activity, its intensity, and the sensitivity of the receiving environment. The degree of change that is considered permissible depends on a number of factors, not the least of which is public perception. Empirical data demonstrating change or impact is the most obvious basis on which to justify management actions or inactions. Equally important is linking the change observed directly to the process under consideration (e.g., bivalve molluscan mariculture). Best management practices (BMPs) and performance standards have been adopted as means of mitigating against unacceptable environmental interactions. The major categories of practices and standards include the following: Regulatory standards governing molluscan mariculture BMPs (or design standards or specifications) for bivalve growers, mariculture regulators, and managers Certification standards for molluscan products (e.g., organic, sustainable, fair trade, domestically or even locally grown) Other innovations, Integrated Multi-Trophic Aquaculture (IMTA) Legislative Drivers Toward ustainable Practices As in many countries there is much national and internationally derived legislation governing the production and placement of aquaculture-derived food products on the market. These regulations consider the product primarily from a food safety perspective with the goal of protecting the consumer. In European Union member states, Regulation (EC) No 854/2004 [53] of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organization of official controls on products of animal origin intended for human consumption was implemented to ensure that consumers of shellfish products are not exposed to toxins that might have accumulated in shellfish flesh as a consequence of filtering phytoplankton species responsible for producing these toxins. hellfish are effective bioaccumulators. uch regulation requires continual monitoring of shellfish products derived from marine waters. In the event of an excess of defined thresholds, the product is not placed on the market and monitoring continues. The broader environmental benefits of this legislation are that it can identify areas of risk (for harmful algal blooms) and has spawned research to identify factors governing the causes of bloom events including anthropogenic sources. How this impacts on sustainability of shellfish aquaculture? The persistence of HAB and toxic events can dictate the

8 hellfish Aquaculture, Methods of ustainable 9181 feasibility of locating or developing shellfish culture these areas. If areas are subject to prolonged closures, the product is generally restricted from being removed and can result in overload and subsequent impact on system processes. The Water Framework Directive [54] is a legislative driver designed to improve surface and groundwater quality throughout the European Union. Allied with a full-risk assessment, each waterbody will be assessed for its condition in terms of ecological quality elements. This monitoring program focuses on a range of ecological quality elements (e.g., benthic invertebrates, phytoplankton, macroalgae, fish in transitional waters) for which a series of standards have been developed. The waterbodies included in the monitoring program were selected on the basis of no obvious pressures and site for which some pressure has been identified, e.g., aquaculture activities. The goal of the WFD is to ensure that all waterbodies achieve good ecological status by The Habitats and Birds Directive [55] in EU member states is considered the cornerstone of Europe s nature conservation policy. The Directive requires that certain areas are designated as conservation sites (Natura sites) and that the conservation features therein managed such that they are preserved in a natural state. In many EU member states, licensed aquaculture activities take place in Natura sites. The designation does not preclude licensing activities in Natura sites but the licensing process must ensure that the proposed activities do not pose a significant risk to the conservation objectives of the site. In this regard, the licensing authority must be seen to carry out and appropriate assessment on the likelihood of these activities significantly impacting on the conservation features. If the activity is considered impacting, then the licensing authority or the applicant can mitigate with a view to reducing the significance of the impacts and still fulfill both conservation and aquaculture objectives. imilarly, in the UA, the Magnuson- tevenson Fishery Conservation and Management Act, provides for the protection of essential fish habitat and the restoration of coastal habitats. Both objectives can cause the relocation of shellfish aquaculture operations to less ecologically sensitive areas (e.g., away from seagrass beds). However, the act also provides some opportunity for shellfish aquaculturists from the perspective of the benefits shellfish aquaculture can provide specifically as it relates to habitat restoration goals. The worldwide depletion of natural populations of shellfish in nearshore coastal areas has been well documented (reviewed in National Research Council [18]). The ability of aquaculture to fill the ecological niche previously provided by native populations has been postulated. At a minimum aquaculture has provided stock for the implementation of restoration projects in Chesapeake Bay in Virginia and Maryland [56]. The International Council Exploration of the ea Code of Practice on the Introductions and Transfers of Marine Organisms [57] is not legislation per se; however, it is cited in legislation and is considered a good example of a guide/code of practice developed in response to particular pressures or risks identified with human activities including, inter alia, shellfish aquaculture. The ICE Code of Practice recommends a series of protocols with a view to mitigating any negative risks associated with intentional introductions and transfers of marine organisms and is targeted at individuals or organization that engages in such activities. As an example of specific legislation citing the ICE Code is the European Union regulation concerning use of alien and locally absent species in aquaculture (708/2007/EC). pecifically, the legislation is designed to avoid alterations to ecosystems, prevent negative biological interactions (including genetic change) with indigenous populations, and restrict the spread of nontarget species and detrimental impacts on natural habitats. This legislation directs member states to ensure that a full-risk assessment is carried out prior to the introduction of a nonnative species for aquaculture purposes. In order to facilitate any introduction, the regulator must ensure that the operator mitigate fully any negative interactions identified as a consequence of the risk assessment. The protocols identified in the ICE Code can provide an avenue toward this mitigation. The Code is aimed at a broad audience since it applies to both public (commercial and governmental) and private (including scientific) interests. In short, any persons engaged in activities that could lead to the intentional or accidental release of exotic species should be aware of the procedures covered by the Code of Practice.

9 9182 hellfish Aquaculture, Methods of ustainable Notwithstanding the potential for regulation to positively guide the development and practice of shellfish aquaculture activities, there is also the risk that regulation can result in constraint of bivalve aquaculture development. This has been demonstrated in the UA where a range of local, state, and federal ordinances govern the licensing of activities in nearshore waters (i.e., areas conducive to bivalve aquaculture). For example, while some coordination has occurred between state and federal agencies in the UA, it still requires up to 30 permits to establish a shellfish culture operation (National Research Council [18]). The complexity can result in a protracted and expensive application process on the part of the aquaculturist that can end with the permit application being refused. The conflict inherent in the regulatory processes is also reflected by conflicts of users in the coastal areas, e.g., wild fishery and aquaculture interests. As a solution to such conflicts, some jurisdictions have implemented zoning of activities where certain activities are only permitted. For example, in an effort to mitigate the conflicts between shellfish culturists and fisherman, some states (Massachusetts and North Carolina) allow shellfish culture in areas where bivalves do not naturally grow. While this offers a somewhat artificial solution to user conflicts, it would appear to favor fishermen, as shellfish typically grow best where they are found naturally in the wild and the availability of approved growing areas might be hard to locate if shellfish are ubiquitous. Industry olutions Toward ustainable Practices There have been a number of industry-led initiatives that have directly or indirectly led to the implementation of more sustainable practices relating to shellfish culture. As already stated, an important realization among promoters of aquaculture and/or regulatory bodies is that a good understanding of the likely interactions between culture practices and environmental concerns is paramount in order to structure management responses. From the industry perspective, these responses are structured with a view to minimizing the negative environmental interactions while maximizing profits. Integrated Multi-Trophic Aquaculture Integrated Multi-Trophic Aquaculture (IMTA) is based upon the principle that the coculture of aquaculture products in carried out in sequence and that one species production is dependent upon the outputs of another [58]. Integration at larger scales may address the optimization of shared resources among various aquaculture users (e.g., shellfish or seaweed culture near fish farms), but assumes that the integrated components (species) are situated within the influence of the system component upon which it directly depends for waste/energy transfer and utilization. In a wellbalanced system this relationship provides the environmental benefits associated with polyculture, and is the basis of definitions such as sustainable, or ecological, aquaculture. Initiatives on the east coast of Canada (New Brunswick) have recently evaluated the performance of mussels (Mytilus trossulus) and large macrophytes (Laminaria) cultured within the infrastructure of an open net-cage salmon (almo salar) aquaculture facility (see IMTA chapter) [58]. To date, there have been mixed results in terms of performance of secondary species, i.e., shellfish species in demonstration projects for IMTA; however, there are a number of other perceived benefits of location shellfish operations in the influence of finfish farms. Most notably is the effect of the shellfish on diseases and parasites of the fish species. Concern has been raised about the ability of the shellfish species of retaining and/or transmitting disease-causing organisms to fish species. The counterargument to these concerns is that the shellfish species is likely endemic to the area and may form part of fouling community on structures such that the risk is not magnified by the presence of the species in culture. In addition, a demonstrated benefit is that the blue mussel (Mytilus edulis) has been shown to destroy the virus for infectious salmon anemia (IA) [59]. Furthermore, the blue mussel has also been demonstrated to eat copepodids (the larval stage of the sea louse, a parasite of salmon) [60] and represents a potential alternative control mechanism to sea lice to chemical treatment which have limited efficacy due to a buildup of resistance in the louse. The environmental benefits of MTA are not constrained solely to the direct assimilation of waste constituents among the cocultured species, but will also be achieved indirectly through the physical design/ configuration and orientation of such a system with respect to adjacent, and potentially sensitive marine

10 hellfish Aquaculture, Methods of ustainable 9183 habitats. Furthermore, there are a number of perceived social benefits associated with the development of marine integrated aquaculture including: (1) optimizing culture opportunities where space is constrained; (2) the provision of development opportunities in remote coastal regions; and/or (3) improving public awareness of aquaculture or aquaculture subsequent environmental accountability. To this end, in the European Union, the Common Agriculture Policy and Common Fishery Policy requires primary users of the natural resources (e.g., agriculturists, fishermen, aquaculturists) to implement an ecosystem approach in the management and conservation of the environment and landscape. It considers polyculture (MTA) as a viable utilization approach for these areas that could provide restoration at a lower cost for society. Certification chemes The increasing demand from consumers for information pertaining to the products they are consuming has been the primary driver for the development of aquaculture certification schemes. The schemes operate on the principal that aquaculture products are produced in fashion that considers a range of factors including, inter alia: ocial responsibility and comply with laws such that they are produced in a legal, safe, and fair manner Environmentally responsible manner such that any negative impacts on the system are minimized That all food safety and quality standards are complied with in the member states That all animal health issues are considered and managed consistent with legislative requirements To date, the most prominent schemes are overseen by the Global Aquaculture Alliance (GAA) [61], which is responsible for the development of best aquaculture standards for mostly fed aquaculture products, including shrimp hatchery and farm standards. It would appear that there are currently no plans for the GAA to develop standards for bivalve shellfish culture. The Aquaculture tewardship Council is an association founded jointly by the WWF and Dutch ustainable Trade Initiative with a view to ensuring aquaculture is carried out in an environmentally and socially sustainable fashion. The AC has developed standards for the culture of bivalve shellfish products (on foot of the Bivalve Aquaculture Dialogues [62]). The standards are governed by a range of broad principles for addressing the environmental and social issues associated with bivalve aquaculture. These principles are consistent with those identified above. The principles provided the framework for developing the criteria, indicators, and standards applicable to bivalve farming. The standards attempt to provide quantitative performance levels that determine whether a principle is achieved or not. The ultimate goal of AC is to have comprehensive participation in the certification scheme by shellfish aquaculturists, which is planned to be certified by a third party. In addition to bivalves (clams, oysters, mussels, and scallops) standards have also been established for abalone. In summary, certification standards have been developed by buyers, public agencies, nongovernmental organizations, or marketing groups as a means of providing consumers with information about a product. The ultimate goal of certification schemes is to persuade growers to modify culture practices by influencing consumer choice and market forces. However, pursuit of certification is voluntary for growers. Best Management Practices The origin of Best Management Practices (BMPs) dealing specifically with environmental interactions is primarily from broader land-based agricultural practices used to mitigate the effects of soil erosion and nutrient loading. imilarly, mariculture BMPs have been developed with a view to minimizing effects resulting from aquaculture culture practices (see Table 2). Best management practices often are developed or strongly supported by the industry group (e.g., oyster growers) to which they apply and as such, adoption of and adherence to these codes is usually voluntary. As with other practices (cited above) the adoption of BMPs tend to have multiple objectives including, for example, reducing the likelihood that shellfish farming will have unacceptable ecological effects. These effects relate primarily to changes in the ecology of the system and interactions with other stakeholders in the system. As highlighted in Table 2, some examples of BMPs relating to shellfish culture consist of outreach brochures on

11 9184 hellfish Aquaculture, Methods of ustainable hellfish Aquaculture, Methods of ustainable. Table 2 Examples of best management practices and environmental standards for the farming of bivalve molluscs produced by a range of organizations, demonstrating the range of topics and the variety of subjects covered. Ecosystem Concepts for ustainable Bivalve Mariculture by Committee on Best Practices for hellfish Mariculture and the Effects of Commercial Activities in Drakes Estero, Pt. Reyes National eashore, California Reproduced with permission of National Academies Press Author Affiliation cope cale References U.. Agency for International Development World Wildlife Fund U.. Department of Agriculture tate of Virginia Pacific Coast hellfish Growers Association eafish (UK) tate of Massachusetts Maryland Aquaculture Coordinating Council Ireland Florida Department of Agriculture and Consumer ervices International Council for the Exploration of the ea Maine Aquaculture Association National Oceanic and Atmospheric Administration Creswell and McNevin (2008) Regulator, nongovernmental organization, and academia Nongovernmental organization Regulator Advisory agency, regulator, and industry Industry Regulator, industry, and advisory agency Industry, regulatory, and advisory agency Industry, regulatory, and advisory agency Industry and advisory agency Regulator Generic guidelines and environmental interactions International [151] Environmental interactions International [72] Policy on organic certification and environmental interactions Environmental interactions and permitting Policy and environmental interactions National [152] tate [153] Regional [154] Alien species interactions National [155] Environmental interactions, permitting, and husbandry Environmental interactions, permitting, and husbandry advice Generic environmental interactions Permitting and environmental interactions tate (local) [156] tate [157] National [158] tate [159] International convention Alien species Interactions International [56] Industry Regulatory Academia ource: From National Research Council [18] Environmental interactions and permitting Environmental interactions and policy Generic guidelines, environmental interactions, and husbandry tate [160] National [161] International [162] husbandry techniques (e.g., Washington ea Grant, 2002; Alaska ea Grant, 2009; University of Maryland, 2009) to identify the optimal ways to culture bivalve molluscs. While these publications focus on methodologies to maximize production, they can still be considered as rudimentary BMPs, in that they require, of the culturists or advisors, a good understanding of the likely interactions between the specific

12 hellfish Aquaculture, Methods of ustainable 9185 culture methods and the environment (e.g., performance in light of productivity). The development of BMPs with a view to managing environmental interactions should be considered a fluid or transitory process that should allow for feedback and subsequent modification of culture practices to mitigate negative effects associated with the shellfish culture. ome BMPs are usually nontechnical wherein they identify a range of issues and present a framework of general principles and solutions and as such, are unlikely to address the range of detailed and local in aspect, issues that present to regulatory agencies and the producers. Other BMPs do deal with more regional issues, and yet others specifically consider the day-today operations at farms and their interactions. These guidelines can provide important advice on pertinent laws and ordinances and focus on important local issues (e.g., environmental interactions, stakeholder interactions, community relationships). In addition, they can identify solutions that range from farm- or small-scale measures to broader societal solutions focusing upon competing uses and values. Toward this end, there are a number of general principles that have applied to the development of BMPs that have directed the practice of shellfish aquaculture toward producing molluscs under the broader umbrella of sustainability. These principles can be broadly categorized under the following headings [50, 63]: 1. Promote a good understanding of environmental and ecological processes, with the broader view of generating carrying capacity models for production areas. This can be further expanded including important socioeconomic considerations also (i.e., ecological and socioeconomic sustainability). 2. Utilize the BMP as a means of promoting the product, i.e., a marketing tool to target a niche market and/or premium price (i.e., economic sustainability). 3. Allow a staged increase in production and reduce uncertainty in terms of environmental interactions (i.e., ecological sustainability). 4. Provide an important communication tool to highlight issues and benefits of shellfish culture to relevant regulatory authorities as well other stakeholders (e.g., nongovernmental organizations) (i.e., social sustainability). While a goal of implementing BMPs will undoubtedly be the improvement of environmental conditions or mitigation of negative effects caused by the aquaculture activity, there still remains a question of how the effects of the BMP are measured. There can be a sharp distinction between BMPs and performance standards. On the face of it, both schemes are broadly designed to limit risk of undesirable environmental impacts. ome authors [15, 64] correctly note, however, that BMPs are not a proxy for performance and that they may have little or no impact in terms of measurable environmental improvements. Typically there are no measures associated with BMPs to validate the claims about mitigating environmental effects. BMPs, in effect, are akin to design standards, whereby procedures and practices are strictly defined (e.g., number of longlines per hectare) which are relatively easily verified. BMPs, therefore, will have a lower administrative burden for demonstrating compliance by identifying easily measured metrics, but have the drawback that there is no guarantee of environmental benefit. Performance standards, on the other hand, measure specific environmental objectives, i.e., the effect on the activity on some aspect of the environment (e.g., free sulfide concentration in sediments). Performance standards relate more specifically to objectives focusing upon ecological integrity of a system [15]. However, performance standards have resource implications in terms of monitoring and enforcement; they are likely more expensive to administer and implement that BMPs. Notwithstanding with distinction highlighted between BMPs and performance standards, it is still possible for managers to align husbandry practices with some measure of performance. For example, it is possible for managers to identify the carrying capacity of a system and subsequently advise on the design of husbandry systems. The process must be fluid and allow for changes in practices and standards as more information on effects is gathered and uncertainty is reduced. It also should allow for stakeholder participation to inform management decisions. In this regard, the science underpinning management actions is communicated concisely to all with an interest in the subject matter and that the views and experience of stakeholders are brought to bear on the process.

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