Farmed Oysters Crassostrea spp., Ostrea spp., Saccostrea spp.

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1 Farmed Oysters Crassostrea spp., Ostrea spp., Saccostrea spp. Image Scandinavian Fishing Yearbook / ww.scandfish.com Worldwide On-Bottom (Seafloor), Suspended Culture (Intertidal/Shallow and Deep Water) October 17, 2014 Kari Heinonen, Consulting Researcher Disclaimer Seafood Watch strives to have all Seafood Reports reviewed for accuracy and completeness by external scientists with expertise in ecology, fisheries science and aquaculture. Scientific review, however, does not constitute an endorsement of the Seafood Watch program or its recommendations on the part of the reviewing scientists. Seafood Watch is solely responsible for the conclusions reached in this report.

2 2 About Seafood Watch Monterey Bay Aquarium s Seafood Watch program evaluates the ecological sustainability of wild-caught and farmed seafood commonly found in the United States marketplace. Seafood Watch defines sustainable seafood as originating from sources, whether wild-caught or farmed, which can maintain or increase production in the long-term without jeopardizing the structure or function of affected ecosystems. Seafood Watch makes its science-based recommendations available to the public in the form of regional pocket guides that can be downloaded from The program s goals are to raise awareness of important ocean conservation issues and empower seafood consumers and businesses to make choices for healthy oceans. Each sustainability recommendation on the regional pocket guides is supported by a Seafood Report. Each report synthesizes and analyzes the most current ecological, fisheries and ecosystem science on a species, then evaluates this information against the program s conservation ethic to arrive at a recommendation of Best Choices, Good Alternatives or Avoid. The detailed evaluation methodology is available upon request. In producing the Seafood Reports, Seafood Watch seeks out research published in academic, peer-reviewed journals whenever possible. Other sources of information include government technical publications, fishery management plans and supporting documents, and other scientific reviews of ecological sustainability. Seafood Watch Research Analysts also communicate regularly with ecologists, fisheries and aquaculture scientists, and members of industry and conservation organizations when evaluating fisheries and aquaculture practices. Capture fisheries and aquaculture practices are highly dynamic; as the scientific information on each species changes, Seafood Watch s sustainability recommendations and the underlying Seafood Reports will be updated to reflect these changes. Parties interested in capture fisheries, aquaculture practices and the sustainability of ocean ecosystems are welcome to use Seafood Reports in any way they find useful. For more information about Seafood Watch and Seafood Reports, please contact the Seafood Watch program at Monterey Bay Aquarium by calling

3 3 Guiding Principles Seafood Watch defines sustainable seafood as originating from sources, whether fished 1 or farmed, that can maintain or increase production in the long-term without jeopardizing the structure or function of affected ecosystems. The following guiding principles illustrate the qualities that aquaculture must possess to be considered sustainable by the Seafood Watch program: Seafood Watch will: Support data transparency and therefore aquaculture producers or industries that make information and data on production practices and their impacts available to relevant stakeholders. Promote aquaculture production that minimizes or avoids the discharge of wastes at the farm level in combination with an effective management or regulatory system to control the location, scale and cumulative impacts of the industry s waste discharges beyond the immediate vicinity of the farm. Promote aquaculture production at locations, scales and intensities that cumulatively maintain the functionality of ecologically valuable habitats without unreasonably penalizing historic habitat damage. Promote aquaculture production that by design, management or regulation avoids the use and discharge of chemicals toxic to aquatic life, and/or effectively controls the frequency, risk of environmental impact and risk to human health of their use. Within the typically limited data availability, use understandable quantitative and relative indicators to recognize the global impacts of feed production and the efficiency of conversion of feed ingredients to farmed seafood. Promote aquaculture operations that pose no substantial risk of deleterious effects to wild fish or shellfish populations through competition, habitat damage, genetic introgression, hybridization, spawning disruption, changes in trophic structure or other impacts associated with the escape of farmed fish or other unintentionally introduced species. Promote aquaculture operations that pose no substantial risk of deleterious effects to wild populations through the amplification and retransmission of pathogens or parasites. Promote the use of eggs, larvae, or juvenile fish produced in hatcheries using domesticated broodstocks thereby avoiding the need for wild capture. 1 Fish is used throughout this document to refer to finfish, shellfish and other invertebrates.

4 4 Recognize that energy use varies greatly among different production systems and can be a major impact category for some aquaculture operations, and also recognize that improving practices for some criteria may lead to more energy-intensive production systems (e.g. promoting more energy-intensive closed recirculation systems). Once a score and rank has been assigned to each criterion, an overall seafood recommendation is developed on additional evaluation guidelines. Criteria ranks and the overall recommendation are color-coded to correspond to the categories on the Seafood Watch pocket guide: Best Choices/Green: Are well managed and caught or farmed in environmentally friendly ways. Good Alternatives/Yellow: Buy, but be aware there are concerns with how they re caught or farmed. Avoid/Red: Take a pass on these. These items are overfished or caught or farmed in ways that harm other marine life or the environment.

5 5 Final Seafood Recommendation Farmed Oysters Crassostrea spp., Ostrea spp., Saccostrea spp. Cultured Worldwide via on-bottom and suspended culture methods in intertidal and subtidal areas Criterion Score (0-10) Rank Critical? C1 Data 8.75 GREEN NO C2 Effluent GREEN NO C3 Habitat 8.13 GREEN NO C4 Chemicals GREEN NO C5 Feed GREEN NO C6 Escapes 4.00 YELLOW NO C7 Disease 8.00 GREEN NO C8 Source 9.00 GREEN NO 3.3X Wildlife mortalities GREEN NO 6.2X Introduced species escape GREEN NO Total Final score 8.06 OVERALL RANKING Final Score 8.06 Initial rank GREEN Red criteria 0 Interim rank GREEN FINAL RANK Critical Criteria? NO GREEN Scoring note scores range from zero to ten where zero indicates very poor performance and ten indicates the aquaculture operations have no significant impact.

6 6 Executive Summary There are few data shortages regarding mussel farming and relevant environmental impacts. Most of the data are of moderate to high or high quality, being reasonably up-to-date, and complete, so as to enable the assessor to obtain a full understanding or reliable representation of mussel farm operations and impacts. Farmed oysters are not provided external feed or nutrient fertilization when culture is entirely sea-based, and from this vantage point there is no effluent concern. Algal feed used in hatcheries or land-based nurseries is also of no concern because of lack of discharge to the environment. There can be a low concern over changes in the sedimentary environment of oyster farms due to biodeposition. These changes are limited to the farm site and are not considered to extend beyond the immediate vicinity of farms. Furthermore, oyster farming has been shown to increase water quality at some farm sites through removal of excess nutrients. Overall, impacts of oyster farming are likely to be minor and unlikely to reach beyond the immediate vicinity of the farm; and because benefits may outweigh such risks, there is no concern regarding resultant effluent or waste impacts. Oyster culture generally occurs on-bottom or in suspension, in coastal intertidal areas or in coastal inshore subtidal areas, which are generally considered to be of moderate to high habitat value; however, the impact of farmed oyster operations on habitat functionality is considered to be minimal, with the main concerns stemming from biodeposition and harvest. Oyster culture is associated with a host of ecosystem services and ecological benefits to water quality, nutrients, provision of habitat and shoreline stabilization that would far outweigh any negative impacts. Minimal habitat impact, coupled with reasonable regulation and enforcement regarding licensing and site selection result in the maintenance of functionality of ecologically valuable habitat. Predator exclusion devices used on oyster farms are usually in the form of a passive nonharmful barrier. Predator exclusion methods would not result in direct or accidental mortality of predators or other wildlife. Dredge harvest techniques result in mortality of wildlife beyond exceptional cases, but due to rapid recovery and some potential benefit to predators, there is no expectation of long-term significant impact to the affected species population size. As such, there is minimal impact to wildlife associated with oyster farms. Recent oyster culture generally does not entail the application of chemicals (i.e., antibiotics, pesticides, herbicides, fertilizers) to control fouling and predators or prevent disease. The amount of chemicals used in mussel culture would be minute, if at all. Further, the water in which chemicals would be used generally is not released to the marine environment. Thus, there is no threat of chemical contamination to adjacent waters or organisms. Oyster culture poses a moderate risk of escape due to that fact that production systems are open to the environment without effective best management practices for design, construction, and management of escapes; and there are no safeguards for larval escape due to

7 7 unrestricted broadcast spawning. While some oysters are cultured within their native ranges, others are cultured in areas where they were introduced by various means (i.e., shipping or escape) more than 10 years ago and are now fully established. Data suggest that recipient ecosystems have been impacted by such introductions, due to competition for resources and habitat modification. The overall score for the escape criterion is low, but not critical. There is a low percentage of trans-waterbody movement of oyster seed at the global level, but there is a high risk of introducing non-native species where it does occur due to the low biosecurity at source locations and farm destinations. This results in an overall minor deduction for the escape of unintentionally introduced species. Despite the fact that oyster growout systems are open to the natural environment increasing the possibility of pathogen exchange, the biosecurity measures that have been put in place at farm, government, and international leels reduce the risk of parasite and pathogen infection to a low level. This is further reinforced by the fact that production practices (especially those of natural settlement) do not increase the likelihood of pathogen amplification compared to natural populations. The source of stock for farmed oysters comes from natural or passive settlement, and hatcheries. Passive collection of oyster spat is much more common and not expected to have any negative impacts on the wild stock. Hatchery production has the impact to modify genetic integrity of wild populations. Due to a large majority of production from natural (passive) settlement, the Source of Stock final score for farmed oysters is 9 (out of 10). Overall, farmed oysters available on the U.S. market get a high overall score of 8.06 out of 10. The analysis of farmed oysters one yellow score and the overall ranking is green. Therefore, the final recommendation is Best Choice.

8 8 Table of Contents About Seafood Watch... 2 Guiding Principles... 3 Final Seafood Recommendation... 5 Executive Summary... 6 Introduction... 9 Analysis Scoring guide Criterion 1: Data quality and availability Criterion 2: Effluents Criterion 3: Habitat Criterion 4: Evidence or Risk of Chemical Use Criterion 5: Feed Criterion 6: Escapes Criterion 7. Disease; pathogen and parasite interactions Criterion 8. Source of Stock independence from wild fisheries Criterion 9X Wildlife and predator score Criterion 10X: Escape of unintentionally introduced species Acknowledgements References Appendix 1: Data points and all scoring calculations... 51

9 9 Introduction Scope of the analysis and ensuing recommendation Species: Farmed oysters available worldwide, including Cassostrea spp., Ostrea spp. and Saccostrea spp. Geographic coverage: Worldwide (namely China, Canada, United States, Brazil, Ecuador, Norway, New Zealand, Australia, South Africa, Europe) Species Overview Production statistics Aquaculture is the fastest growing sector of food production and provides half of the fisheries products consumed worldwide (Shumway 2011). Oyster farming has become an increasingly important global aquaculture activity, accounting for the greatest proportion of molluscan aquaculture production (by quantity, Figure 1). Figure 2 depicts the overwhelming contribution of China to global oyster production. In the United States, the historical oyster market has been dominated by domestic production, but recent data show that the amount of oyster imports have exceeded that of production(figure 3) Quantity (tonnes) Year Clams, cockles, arkshells Mussels Oysters Scallops, pectens Figure 1. The quantity of global mollusk production (FAO 2014)

10 10 Quantity (tonnes) Year France United States Japan China Taiwan Australia Canada Thailand New Zealand Korea Figure 2. The quantity of oyster production in tonnes by country (FAO 2014). FAO data are dependent upon self-report methodology. Lack of a country s contribution in this figure may be due to no report or the manner in which FAO aggregated the data Quantity (tonnes) Year Production Import Export Figure 3. Production and trade of oysters in the United States (FAO 2014) Production Methods: Oyster culture methods include on-bottom and off-bottom techniques, which are chosen based on site suitability (e.g., wave and wind action, salinity, natural food supply, availability of broodstock or seed, water quality, and depth). The different phases of culture are discussed below.

11 11 Recruitment Seed is collected passively via natural settlement of spat on cultch or via hatchery and nursery production. Passive collection techniques have evolved over the years to include different types of material, including metal bars, tiles, slate, oyster and scallop shells placed in bags and strung on wires, and plastic tubes (Héral and Deslous-Paoli 1991). Hatchery production is focused in areas with limited or without natural seed supply, as well as regions previously ravaged by disease. In certain areas, the majority of production is hatchery based (i.e., Washington State and the New England Region in the United States). Broodstock is selected from the field and spawned in the hatchery in order to collect spat (FAO 2004, Wallace et al. 2008). After seed collection, oyster culture may be carried out in two growout phases: pregrowing and maturation, where oysters are left to grow in the seeding area or transferred to a specific growout area (Garrido-Handog 1990, Héral and Deslous-Paoli 1991). Floating upweller systems (FLUPSY) 2 are also used to grow seed from hatchery or nursery to growout size. Growout Oyster growout occurs in open marine and estuarine environments using a variety of techniques, which include plastic or wire-mesh containers, cages, trays, and bags, deployed onbottom, or from floating or fixed structures. Oysters may be grown directly on the bottom of intertidal and subtidal areas as long as there is a hard substrate. This entails sowing the young oysters on the ground, either unattached or attached to collectors for a period of 1-2 years, after which they are scraped from cultch (if applicable) and sown on maturing beds, often surrounded by protective fences in intertidal or shallow subtidal areas. In deeper waters, oysters are often planted only after dredging the area to remove stones, predators, and competitors (Garrido-Handog 1990, Héral and Deslous-Paoli 1991). In areas where there is a lack of hard substrate or significant wave action, oysters may be grown in suspension (i.e., off-bottom) using raft, rack, and stake methods. In raft culture, oysters are suspended from a raft in trays in which single oysters are placed on trays and allowed to grow until a marketable size is reached; or suspended from a raft on strings in which seeds are threaded onto a length of wire, rope, or cord. In rack culture, racks of various materials are used as a superstructure to hold oysters housed in trays or on strings. The racks are typically deployed so that oysters are only exposed to air during a low tide. Stake culture is generally used in lagoons that are too shallow for raft and rack techniques. This method holds oysters in a vertical position and the stakes may also serve as collectors themselves (Garrido- Handog 1990). 2 A Floating Upweller System (FLUPSY) is a floating shellfish seed culturing device that consists of seed containers (silos) attached to a float apparatus sometimes attached to a pier or dock. Young shellfish are placed in the silos and a pump system moves oxygen and nutrient rich water vertically through the 3-dimensional mass of oysters and simultaneously expels seed waste products back to the surrounding water.

12 12 Product forms Oysters can be purchased in many forms, with the most common product forms being fresh shucked oysters (eaten on the half shell; Figure 4) Quantity (tonnes) Year Oyster meat nei, frozen Oyster meat, prepared or preserved, nei Oyster meat, prepared or preserved, nei Oysters, shucked, fresh or chilled Figure 4. Quantity of product forms of cultured oysters available on the U.S. market (FAO 2014) Common Market Names Farmed oysters are available on the U.S. market as oysters. Species include: Ostrea edulis European flat oyster Crassostrea gigas Pacific oyster (also known as the Japanese oyster and giant oyster) Crassostrea virginica cupped Eastern oyster Saccostrea commercialis Sydney rock oyster Species: Ostrea edulis. Natural populations of the European flat oyster are found along the west coast of Europe and Morocco in the northeastern Atlantic. This species was intentionally introduced to North America in the 1940s and 1950s, and can be found on both coasts of the United States. The production of O. edulis has declined on the west coast of the U.S. due to the impacts of disease and the subsequent shift to culture of the Pacific oyster Crassostrea gigas. European flat oysters are available as fresh seafood and generally consumed on the half shell (FAO 2004a- 2014).

13 13 Figure 5. Global aquaculture production of O. edulis (FAO 2004a-2014) Cassostrea gigas. The Pacific oyster is native to Japan, but it has been intentionally introduced to the United States and France. There have been secondary, unintentional and intentional introductions to many other countries. This species is estuarine and occurs at depths ranging from 0 to 40 m. Most of the global supply of C. gigas is obtained from wild seed, but some commercial units operate hatcheries as well. Global production of this species has exceeded that of any other species and continues to expand, with major producing countries including China, Japan, Korea, the United States, France, European states, Australia, New Zealand, and South Africa. Much of the production is consumed by local markets and is only imported when there is a surplus. The preferred product form is fresh and on the half shell, while canned, frozen and vacuum-packed forms are less common (FAO 2005a-2014). Figure 6. Global aquaculture production of the C. gigas (FAO 2005a-2014)

14 14 Crassostrea virginica. The cupped Eastern oyster occurs in estuaries and marine coastal environments, and is cultured in the United States, Canada, and Mexico. This species is marketed fresh on the half shell and frozen, or incorporated into value added products, such as soups and chowders. Most North American jurisdictions do not distinguish between wildcaught and cultured oysters (often because there is a continuum ranging from culture to enhanced fishery), so the quantity of cultured oysters is difficult to track (FAO 2004b-2014). Regardless, the production of C. virginica has been high and consistent in recent years (Figure 7). Figure 7. Global aquaculture production of C. virginica (FAO 2004b-2014) Saccostrea commercialis. The Sydney rock oyster occurs in intertidal estuarine habitats, as well as on natural subtidal dredge beds. The main producer country of this species is Australia. Sydney rock oysters are cultured for the half shell market and are sold in supermarkets and restaurants (FAO 2005b-2014). There has been a gradual and steady decline in the production of this species (Figure 8). Australian oyster growers were in preliminary talks with the U.S. to export this delicacy. In order to be considered, harvest areas must comply with strict criteria set by Australia Quarantine and Inspection services (Townsend 2011).

15 15 Figure 8. Global aquaculture production of S. commercialis (FAO 2005b-2013)

16 16 Analysis Scoring guide With the exception of the exceptional factors (3.3x and 6.2X), all scores result in a zero to ten final score for each criterion and the overall final rank. A zero score indicates lowest performance, while a score of ten indicates highest performance. In contrast, the two exceptional factors result in negative scores from zero to minus ten, and in these cases zero indicates no negative impact. The full Seafood Watch Aquaculture Criteria to which the following scores relate are available here The full data values and scoring calculations are available in Appendix 1 Criterion 1: Data quality and availability Impact, unit of sustainability and principle Impact: poor data quality and availability limits the ability to assess and understand the impacts of aquaculture production. It also does not enable informed choices for seafood purchasers, nor enable businesses to be held accountable for their impacts. Sustainability unit: the ability to make a robust sustainability assessment. Principle: robust and up-to-date information on production practices and their impacts is available to relevant stakeholders. Data Category Relevance (Y/N) Data Quality Score (0-10) Industry or production statistics Yes Effluent Yes Locations/habitats Yes Predators and wildlife Yes Chemical use Yes Feed No Not relevant n/a Escapes, animal movements Yes Disease Yes Source of stock Yes Other (e.g., GHG emissions) No Not relevant n/a Total 70 C1 Data Final Score 8.75 GREEN Brief Summary There are few data shortages regarding mussel farming and relevant environmental impacts. Most of the data are of moderate to high or high quality, being reasonably up-to-date, complete, so as to enable the assessor to obtain a full understanding or reliable representation of mussel farm operations and impacts.

17 17 Justification of Ranking There are few data shortages regarding industry or production statistics relevant to mussel culture. Industry and production statistics available through the FAO (2014) are up-to-date within reason and the data are considered to give a reliable representation of the industry, but there may be some noncritical gaps in the data or data may have been aggregated in a noncritical manner. FAO data are also dependent upon self-report. For this reason, the data quality and availability of industry and production statistics are considered moderate to high, scoring 7.5 out of 10. There is sufficient information on effluent, predator and wildlife mortalities, escapes and disease to make relevant assessments. The majority of the available data in effluent, predator and wildlife mortalities, escapes and disease categories are complete, up-to-date within reason and have been peer reviewed. For this reason, data associated with these categories are considered high quality and receive a score of 10 out of 10.

18 18 Criterion 2: Effluents Impact, unit of sustainability and principle Impact: aquaculture species, production systems and management methods vary in the amount of waste produced and discharged per unit of production. The combined discharge of farms, groups of farms or industries contributes to local and regional nutrient loads. Sustainability unit: the carrying or assimilative capacity of the local and regional receiving waters beyond the farm or its allowable zone of effect. Principle: aquaculture operations minimize or avoid the production and discharge of wastes at the farm level in combination with an effective management or regulatory system to control the location, scale and cumulative impacts of the industry s waste discharges beyond the immediate vicinity of the farm. Effluent Rapid Assessment C2 Effluent Final Score GREEN Rapid assessment used when good quality data clearly defines an appropriate score Brief Summary Farmed oysters are not provided external feed or nutrient fertilization when culture is entirely sea-based, and from this vantage point there is no effluent concern. Algal feed used in hatcheries or land-based nurseries also is of no concern because of lack of discharge to the environment. There can be a low concern over changes in the sedimentary environment of oyster farms due to biodeposition. These changes are limited to the farm site and are not considered to extend beyond the immediate vicinity of farms. Furthermore, oyster farming has been shown to increase water quality at some farm sites through removal of excess nutrients. Overall, impacts of oyster farming are likely to be minor and unlikely to reach beyond the immediate vicinity of the farm; and because benefits may outweigh such risks, there is no concern regarding resultant effluent or waste impacts and the score for the effluent criterion is 10 (out of 10). Key relevant information: For regions in which the supply of natural spat is abundant and reliable, and nursery and growout are entirely sea-based, farmed oysters are not provided external feed or nutrient fertilization; therefore, there is no concern regarding resultant effluent impacts. For regions in which collection of spat is dependent upon hatcheries, and for which nurseries are land-based, there may be a requirement for addition of algal cultures. In hatcheries, both larvae and algae are cultured in closed systems where standing water and wastes are not discharged to the environment (FAO 2004a,b-2014, 2005a-20014, as reviewed in Creswell and McNevin 2008). In land-based nurseries that utilize on-land tank systems rather than barges, juvenile oysters are supplied with algae-rich water pumped from ponds that may be naturally productive or be enriched with artificial or natural fertilizers (FAO 2005a-2014). Such systems do not discharge wastes to the marine environment. Despite the addition of algae for food, and the potential for external fertilization of ponds used to supply land-based nursery tanks, the fact that they do not discharge to the environment results in no effluent concern.

19 19 Active filter feeding by oysters results in the excretion of undigested material (feces or pseudofeces), which can lead to enhanced biodeposition. Enhanced biodeposition has the potential to result in increased organic nutrient load, which leads to enhanced microbial activity that can lead to oxygen depletion in the sediment and sediment porewater beneath the farm (Forrest et al. 2007). Alternatively, some studies have shown that oysters may actually lower ammonium concentrations in sediment porewater, when rapid denitrification occurs at the interface of organic and inorganic sediment layers created by biodeposition (as reviewed in Dumbauld et al. 2009). Other studies have shown that oysters may actually lower ammonium concentrations in sediment porewater when rapid denitrification occurs at the interface of organic and inorganic sediment layers created by biodeposition (as reviewed in Dumbauld et al. 2009). In addition, oysters may be polycultured with other species (i.e., shrimp) to significantly improve water quality of farm effluent (Jones et al. 2000). Overall, data show no evidence that discharges from oyster culture cause or contribute to cumulative impacts beyond the immediate vicinity of the farm. Furthermore, oyster farming may provide increased benefits through their extractive nature when cultured with other species. All impacts considered, the benefits of oyster farming generally outweigh any minimal impacts from effluent. Therefore, the effluent concern is considered of no concern, and the criterion receives a score of 10 (out of 10).

20 20 Criterion 3: Habitat Impact, unit of sustainability and principle Impact: Aquaculture farms can be located in a wide variety of aquatic and terrestrial habitat types and have greatly varying levels of impact to both pristine and previously modified habitats and to the critical ecosystem services they provide. Sustainability unit: The ability to maintain the critical ecosystem services relevant to the habitat type. Principle: aquaculture operations are located at sites, scales and intensities that cumulatively maintain the functionality of ecologically valuable habitats. Habitat parameters Value Score F3.1 Habitat conversion and function 9.00 F3.2a Content of habitat regulations 4.25 F3.2b Enforcement of habitat regulations 3.75 F3.2 Regulatory or management effectiveness score C3 Habitat Final Score 8.13 GREEN Critical? NO Criterion 3 Synthesis Oyster culture generally occurs on-bottom or in suspension, in coastal intertidal areas or in coastal inshore subtidal areas, which are generally considered to be of moderate to high habitat value; however, the impact of farmed oyster operations on habitat functionality is considered to be minimal, with the main concerns stemming from biodeposition and harvest. Oyster culture is associated with a host of ecosystem services and ecological benefits to water quality, nutrients, provision of habitat and shoreline stabilization that would far outweigh any negative impacts. Minimal habitat impact, coupled with reasonable regulation and enforcement regarding licensing and site selection result in an overall high score (8.13). Justification of Ranking Factor 3.1. Habitat conversion and function Habitat conversion is measured by the effect of aquaculture on ecosystem services. Oyster farming, and shellfish farming as a whole, provide valuable ecosystem goods and services, with few negative impacts. The greatest concerns raised about oyster culture on habitat are related to depletion of phytoplankton, enhanced and localized biodeposition, alteration of nutrient exchanges, and broader ecological effects such as the creation of novel habitat (Shumway 2011). Pelagic effects It is recognized that oyster farms remove phytoplankton and organic detritus from the water column through filtration. Reducing the amount of these materials available to other organisms may stimulate trophic cascades, especially if carrying capacity is exceeded, but impact is not quantified beyond the immediate footprint of the aquaculture operation (Dumbauld et al. 2009). Reducing the amount of phytoplankton and detritus in the water

21 21 column may provide a key ecosystem service by reducing primary symptoms of eutrophication (Dumbauld et al. 2009, Burkholder and Shumway 2011). This reduction may result in recognized benefits such as an increase in the amount of underwater light, extending the euphotic zone and potentially benefiting submerged aquatic vegetation (SAV) and macroalgae (as reviewed in Dumbauld et al. 2009). Submerged aquatic vegetation provides further ecosystem services, such as a refuge and nursery for juvenile fish and increased sediment stability (Yamamuro et al. 2006). In addition, reduction of eutrophication symptoms decreases the cycling time of suspended organic matter by removing the opportunity for bacterial remineralization and, therefore, the onset of hypoxia and anoxia. Habitat concerns resulting from the physical [infra]structure associated with on-bottom suspended oyster culture include the alteration of hydrodynamics and current velocities, as well as reduced flow rates (as reviewed in Dumbauld et al and Padilla et al. 2011). Reduced currents may increase sedimentation, but the positive effects (i.e., provision of complex hard substrate for recruitment and refuge) far outweigh those associated with increased sedimentation. Given the dynamic nature of the system, and the fact that pelagic effects are dependent upon the specifics of each study site, it is difficult to compare findings among studies. Furthermore, linking pelagic effects together (removal of phytoplankton and organic detritus with increased sedimentation and turbidity) will not be considered further. Benthic effects Oysters growing in suspended culture often create favorable structures/habitats for other invertebrates and fishes by providing refuges from predation and adverse environmental conditions, as well as providing a food resource (Dumbauld et al. 2009). Aquaculture gear also provides complex habitat structure for other species. Shellfish aquaculture gear used for the growout phase of C. virginica has habitat value equivalent to that of SAV (Dealteris et al. 2004). In addition to habitat, oyster reefs also act as a natural coastal buffer or breakwater that mitigate shoreline loss (Scyphers et al. 2011). Oysters may compete with other benthic species that occupy the same space, but effects of competition would not occur outside of the farm footprint (Dumbauld et al. 2009) and would not outweigh the fact that oysters also provide food for fish, crabs and birds. Biodeposition of fecal matter from oyster culture is a habitat concern because biodeposition from oysters in suspension may be considerable. The build-up of biodeposits under or within oyster production areas reduces grain size and increases organic content, which can reduce oxygen content and can have important consequences for nitrogen cycling (Dumbauld et al. 2009). Two additional factors to consider are that there is a data gap regarding the redistribution of biodeposits among environments with different hydrodynamic regimes, and alteration of biochemical pathways are challenging to measure in the field due to the presence of other nutrient generators (as reviewed in Dumbauld et al. 2009). Alternatively, biodeposition creates conditions suitable for denitrification and it has been demonstrated that oyster reef restoration (parallel to oyster farms) can increase denitrification rates and enhance nutrient sequestration by assimilation into oyster shells (Kellogg et al. 2013). This can be especially beneficial for systems impaired by nutrient overloads.

22 22 Harvest Oysters grown off-bottom are typically harvested by hand, unless the strings or trays employed in raft and rack culture are too heavy and require some form of industrial mechanism. In this case, marketable oysters are harvested by small vessels equipped with mechanical washing and grading equipment (FAO 2004b-2014, 2005a-2014). Oysters grown on-bottom are generally harvested by hand (raking or picking) or dredge (Garrido-Handog 1990, Deslous-Paoli 1991). The typical oyster dredge is operated by a winch and is approximately 3.5 to 4 m wide and 2 m deep with 3-5 cm teeth (FAO 2004a-2014, Creswell and McNevin 2008, Mercado-Allen and Goldberg 2011); however, those used on farms may be smaller (e.g., 1 m wide). Dredge teeth penetrate soft sediments to remove oysters and shell directly from the surface. In the collection of seed oysters, the speed and duration of dredge tows are often modified to improve harvest efficiency on differing bottom types (Getchis et al. 2006). Additionally, suction dredges have been used to collect juvenile oysters and cultch and can be more efficient than traditional oyster dredges because they act as a large vacuum cleaner that pumps water from the seafloor into a hose and efficiently lifts shellfish. Suction dredges are sometimes used to transplant oysters for growout, to relocate shell and cultch material, and to clean leased grounds of predators (Creswell and McNevin 2008, as reviewed in Mercado-Allen and Goldberg 2011). Oyster harvest by dredging can result in an immediate and initial decline in abundance and biomass for all species (i.e., predators, target species and other benthic organisms) that occur on and in oyster cultivation areas, but the decline is often followed by rapid benthic recovery (Mercaldo-Allen and Goldberg 2011). Oyster habitats are generally found in high energy shallow waters, and the organisms that reside in them are well adapted to frequent disturbances (i.e., storms; Stokesbury et al. 2011). While dredging may initially damage or reduce certain organisms, scavengers and opportunistic predators may also benefit from the effects of dredging by feeding on exposed prey or by colonizing newly exposed seafloor. For example, predatory fish and crustaceans increase in density in the vicinity of clam dredges (as reviewed by Mercaldo-Allen and Goldberg 2011). In addition, changes in sediment structure associated with oyster dredging are reversible or dissipate over short periods of time, although time periods may be variable (as reviewed in Dumbauld 2009 and Mercado-Allen and Goldberg 2011). Replanting shell and spatted shell following harvest is a common practice and has the capacity to improve or restore habitat and biodiversity. Habitats in which oysters are farmed may be improved through filtration and maintain full functionality if harvested by hand. Habitats in which oysters are farmed and then harvested by dredge are subject to changes in sediment structure and reduction in species diversity and biomass; harvest impacts are shown to be local, reversible and of low impact in areas well adapted to frequent disturbance (Stokesbury et al. 2011).

23 23 Overall, the effects to habitat function and services from oyster culture are expected to be minimal and mitigated by the ecosystem services that oysters provide. The habitat remains functional and the score for this factor is 9 (out of 10). Factor 3.2. Habitat and farm siting management effectiveness (appropriate to the scale of the industry) China accounts for the majority of global oyster culture, but there are many other contributing countries (Figure 2). Oysters are consumed in many forms (Figure 4), but are only imported live to the U.S. from Canada. Fresh imports must meet water quality standards that are subject to convention and international agreements, as well as health certificates. Each country regulates aquaculture and enforces aquaculture policies differently, but often with the same goal of minimizing environmental impact. The following is an overview of habitat and farm management effectiveness in several countries with significant oyster aquaculture production. In the U.S., the U.S. Army Corps of Engineers issues aquaculture permits before a farm can be established, which often require consultation with the National Marine Fisheries Service and the U.S. Fish and Wildlife Service, as well as approval by states that the farm is consistent with the coastal zone management programs. Additionally, environmental best management practices (BMP) are also employed to reduce, minimize, or mitigate the effects of farming practices on aquatic (or terrestrial) resources and interactions with other users of marine resources (Dewey et al. 2011, Getchis and Rose 2011). Canada is party to international agreements with implications for the regulation of aquaculture, but all aspects of aquaculture in Canada are federally or provincially regulated, or both. The federal government has jurisdiction over the regulation of fish products marketed in export and inter-provincial trade, the conservation and protection of wild fish stocks and fish habitat and research and development. Federal authority to regulate the aquaculture industry is shared among 17 departments and agencies, with the Department of Fisheries and Oceans Canada (DFO) as the lead. Transport Canada grants authorizations for aquaculture facility plans affecting navigation under the Navigable Waters Protection Act. DFO or Transport Canada manages the environmental assessment process in coordination with Environment Canada and the Canadian Environmental Assessment Agency under the Canadian Environmental Assessment Act. Specific responsibilities for aquaculture have been delegated by the federal to the provincial level through memoranda of understanding. Provinces are responsible for aquaculture planning, site leasing, licenses and approvals for aquaculture sites, aquaculture training and education, the collection of statistics, the promotion of fish and aquaculture products, and the management of the industry's day-to-day operations. The provinces also regulate the food safety of aquaculture processing, while the regulation of food safety for export purposes remains under the exclusive jurisdiction of the federal government. All the provinces and territories have legislation to regulate aquaculture industries, either by way of proclaimed acts dealing with aquaculture or zoning bylaws (FAO 2007 to 2013). In China, the use of the aquatic and terrestrial environment is regulated by different laws such as the Fisheries Law, the Regulation Law for Sea Area Usage, and the Environmental Impact

24 24 Assessment Law, but site selection for aquaculture has no specific legislation (FAO 2004c-2014, Chen et al. 2011). Use of state owned land and water areas is required to meet the local functional zoning scheme set by the Land Administration Law, including conservation areas, industry, aquaculture, etc. (FAO , Chen et al. 2011). Most farms are family operated and shellfish leases are managed by local communities (personal communication with X. Guo, November 29, 2012). Environmental Impact Assessments (EIA) are required by different environmental laws, and while there is no specific referral to aquaculture, EIA are required for construction projects that include large-scale aquaculture. Additionally, the Environmental Impact Assessment Law expands EIA requirements from individual construction projects to government planning for the development of agriculture, aquaculture, animal husbandry, forestry, water conservation and natural resources (FAO ). At the local level, licenses may only be granted in state-owned waters if natural spawning, breeding and feeding grounds and migration pathways of fish, shrimp, crab, shellfish and algae are protected and not used as the aquaculture site. Licenses can be revoked if water surfaces and tidal flats are neglected for a period of 1 year (FAO ). Water quality is monitored on lease grounds to ensure that it is suitable and remains suitable for aquaculture; however, monitoring may not be strictly enforced (personal communication with X. Guo, November 29, 2012). Overall, enforcement of aquaculture regulations is often weak as aquaculture is favored by the government as an important economic activity (Chen et al. 2011). In Australia, all states or territories have fisheries or aquaculture legislation that regulates aquaculture production. The Australian Aquaculture Code of Conduct, initiated by the Australian Aquaculture Forum, provides principles aimed at maintaining ecological and economic sustainability for the aquaculture industry. The South Australia Aquaculture Act is the main piece of legislation governing the management, control and development of the aquaculture sector. The act includes provisions giving the South Australian Minister for Agriculture, Food and Fisheries the power to grant aquaculture licenses and the power to make decisions on license conditions, as well as conditions and terms of leases. An aquaculture license can be suspended or cancelled if the licensee obtained the license improperly, the licensee has failed to comply with a condition of the license, or the licensee has committed an offense against any other law relating to aquaculture, fishing or environmental protection. The act also endorses the Aquaculture Environmental Management Framework Policy which forms the basis for license and lease conditions, including aquaculture license assessment, environmental management and monitoring, site management and indemnity, site rehabilitation and remediation (FAO 2005c-2014). Overall, the content of habitat regulations surrounding oyster culture or aquaculture generally takes into account environmental impacts and ecosystem function and services and Criterion 3.2a receives a score of 4.25 (out of 5). Similarly, enforcement organizations are identifiable, permitting processes are based on zoning plans, and the process appears relatively transparent; thus Criterion 3.2b receives a score of 3.75 (out of 5). Regarding the available information it is not clear if all regulations in all locations are effective or well-enforced (see example of weak enforcement in China above). If general statements are available, they appear to rely on opinion rather than data, and therein lies uncertainty. As such, regulation and management of

25 25 farm siting and licensing across all locations resulted in an overall habitat and farm siting management effectiveness score of out of 10. When combined with the Factor 3.1 score (9 out of 10), the final numerical score for Criterion 3 Habitat is 8.13 out of 10, indicating that although there are some variations in the effectiveness of the management regimes, the fundamental nature of the production system means that oyster farming is unlikely to have substantial habitat impacts.

26 26 Criterion 4: Evidence or Risk of Chemical Use Impact, unit of sustainability and principle Impact: Improper use of chemical treatments impacts non-target organisms and leads to production losses and human health concerns due to the development of chemical-resistant organisms. Sustainability unit: non-target organisms in the local or regional environment, presence of pathogens or parasites resistant to important treatments. Principle: aquaculture operations by design, management or regulation avoid the discharge of chemicals toxic to aquatic life, and/or effectively control the frequency, risk of environmental impact and risk to human health of their use. Chemical Use parameters Score C4 Chemical Use Score C4 Chemical Use Final Score GREEN Critical? NO Brief Summary Recent oyster culture generally does not entail the application of chemicals (i.e., antibiotics, pesticides, herbicides, fertilizers) to control fouling and predators or to prevent disease. The amount of chemicals used in mussel culture would be minute, if any. Further, the water in which chemicals would be used generally is not released to the marine environment. Thus, there is no threat of chemical contamination to adjacent waters or organisms. Justification Key relevant information: The purpose of chemical treatment in oyster farming would be to prevent predators, fouling, and infection by disease-causing bacteria in oyster hatcheries. Predators The use of chemical substances (i.e., copper sulfate, calcium oxide, sand coated with trichloroethylene, and insecticides) to control predators of mollusks was pioneered in the 1930s in the U.S. (Loosanoff 1960, Jory et al. 1984, Shumway et al. 1988). While such chemicals proved effective, the concern for potential environmental and public health risks of copper sulfate, trichloroethylene, and insecticides far outweighed the benefits. The use of many chemicals (e.g., pesticides) in the marine environment for aquaculture, or otherwise, have been banned (Creswell and McNevin 2008, Sapkota 2008), hence the chemicals are no longer used to control predators at oyster farms. However, calcium oxide has no environmental impact and is approved by government for use in the environment (personal communication with S. Shumway). Furthermore, a review of predator controls in bivalve culture conducted by Jory et al. (1984) revealed that the installation of exclusionary devices (i.e., netting) was more successful than chemical treatment for control of bivalve predators.

27 27 Fouling Fouling is a significant problem in off-bottom oyster culture, because physical structures are prone to fouling. Constant cleaning is required to remove fouling organisms. There have been many attempts to prevent fouling in bivalve culture through the use of chemicals such as Victoria Blue B, copper sulfate, quicklime, saturated salt solutions, chlorinated hydrocarbon insecticides, and other pesticides (Loosanoff 1960, MacKenzie 1979, Shumway et al. 1988; Brooks 1993); however, chemicals to control fouling may release potentially toxic constituents into the marine environment that pose a threat not only to the species being cultured, but to other non-target organisms. Even antifoulants commonly used in finfish culture are not applied to shellfish gear. This is because the antifoulants approved for finfish culture have not been approved for shellfish culture, and the antifoulants currently available do not adhere to the plastics from which shellfish gear is made (Bishop 2004). Experiments are being conducted on netting but they are inconclusive to date, and the East Coast Shellfish Growers Association Best Management Practices (Flimlin et al. 2010) caution against the use of chemicals to control fouling. Air drying, brine or freshwater dips, power washing, and manual control are not only more successful, but environmentally friendly antifouling methods (Creswell and McNevin 2008, Watson et al. 2009). In a presentation by Gill (2011), 24 hour exposure to air functioned to control fouling in oyster aquaculture operations on Prince Edward Island. Antibiotics in oyster hatcheries The use of antibiotics or therapeutics in U.S. aquaculture is overseen by the U.S. Food and Drug Administration (FDA) and regulations are quite stringent regarding use of unapproved chemicals. The U.S. Environmental Protection Agency (EPA) also regulates the use of nonpharmaceutical chemicals used in shellfish culture 3 ; laws are strict and shellfish producers typically do not use unapproved chemicals. Bacteria that may cause disease in hatchery-reared larvae and spat can be controlled with antibiotics (Ford 2001); however, hatchery operators are concerned with the development of antibiotic resistance, and instead rely on improved animal husbandry and regular cleaning of hatchery equipment (Ford 2001, Creswell and McNevin 2008, Flimlin et al. 2010). Dilute hypochlorite (bleach) solutions often are used for disinfection of equipment, but they are disposed of in the municipal sewer system instead of the marine environment (Creswell and McNevin 2008, Flimlin et al. 2010). Furthermore, the use of hatcheries in mussel culture is fairly uncommon and antibiotics are not used in the natural environment where mussels are farmed (British Columbia Shellfish Growers Association 2012). In Australia, the majority of chemicals used by the oyster farming industry are found on land at service areas or in hatcheries. They usually include maintenance chemicals for machinery (fuel, oil and grease) and cleaning chemicals (bleach). The Environmental Protection Agency requires that all waste-containing chemicals are removed by the appropriate authority and treated at the appropriate facility 4, thus there is no concern over chemical use. In China, chemicals (including antibiotics) have been detected in aquatic products, but supervision and testing of chemicals in such products is improving and the use of most antibiotics for aquaculture is