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I.  Benthic/Pelagic Coupling— Nutrients and Particulates A.  Background Suspension feeders, such as oysters, mussels, and other bivalve mol- luscs, have been shown to influence the nutrient, organic, and materials coupling of benthic and pelagic systems in a broad range of habitats (Dame, 1996). Oysters feed by filtering particulates from the water col- umn and when populations are abundant they can depress turbidity in their local vicinity and help graze down algal blooms in estuaries (Her- man and Scholten, 1990; Haamer, 1996; Rice, 2000; Smaal et al., 2001; Landry, 2002; Newell, 2004). Epifaunal shellfish such as oysters have a very plastic response to increasing levels of phytoplankton and detritus in water, increasing their filtration rate and production of pseudofeces. This adaptability is not observed in infaunal shellfish (clams and cockles); they stop filtering when suspended particulate levels exceed their tolerance (Foster-Smith, 1975; Prins et al., 1991). Because oysters and other bivalves can filter so much material from the water, producing a large quantity of pseudofeces and feces, they function in the transfer of organic and inor- ganic particulates from the water column to the sediments—a process referred to as benthic-pelagic coupling (Dame, 1996; see review in Dame and Olenin, 2005). The deposition of feces and pseudofeces can modify sediments in the vicinity of high abundances of bivalves, increasing concentrations of fine particles and organic content and altering sediment biogeochemistry (e.g., Newell et al., 2002). Under circumstances of limited physical flushing and transport of these biodeposits, high rates of transfer of organics from the 25

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26 SHELLFISH MARICULTURE IN DRAKES ESTERO water column to the bottom can result in sedimentary anoxia, diminish- ing the capacity of the sediments to sustain benthic invertebrates. On the other hand, low rates of organic enrichment from pseudofeces and feces may fertilize eelgrass and benthic macro- and microalgae, thereby increas- ing benthic primary production (Asmus and Asmus, 1991; Reusch et al., 1994; Peterson and Heck, 1999; Carroll et al., 2008). B.  What is the Body of Scientific Studies on the Impact of the Oyster Farm on Drakes Estero? There are few and limited studies of sedimentation and nutrient inputs in Drakes Estero. Anima (1990, 1991) presents results from stud- ies on sedimentation and pollution in Drakes Estero funded by NPS. In another study funded by NPS, researchers provided a preliminary inven- tory and assessment of the effects of the oyster farm on some of the biota in the estero, including analysis of sediment cores for benthic infauna, organic content, and particle size (Harbin-Ireland, 2004; summarized in Elliott-Fisk et al., 2005). Anima (1990, 1991) conducted a survey of the sedimentation rate and composition of sediments in Drakes Estero in 1984–1986. Sedimenta- tion appeared to increase over the past 150 years, potentially a response to changing land use as the population increased. In the report to NPS, Anima (1990) noted a few potential impacts associated with oysters or oyster farm activities on sedimentation in the estero. First, he observed that the Schooner Bay channel appears to be artificially maintained by boat traffic associated with oyster operations. Propeller action was inferred to maintain the navigation channel and prevent sedimentary in-filling from the adjacent, extensive eelgrass beds. In addition, Anima speculated on the role of oysters in deposition of fine sediments in the estero, based predominantly on studies of oyster biodeposition rates in other systems. Noting that the flushing rate in the upper reaches seems insufficient to transport fine sediments out of the estero, Anima (1990, 1991) concluded that “more research is needed to ascertain what amount of silt-sized mate- rial is being produced by oysters in the lagoon.” Anima (1990, 1991) also reported results from a study of nutrient inputs to the estero based on the monitoring of streams in areas with or without agricultural land use (cited as Hagar, 1990 [unpublished]). From short-term monitoring of nutrients (phosphorus and nitrogen) in the vari- ous streams, it appeared that the estero was unlikely to experience excess nutrient loading from the watershed (Anima, 1990, 1991). This report also asserted that there is low risk of eutrophication due to the high rate of tidal flushing relative to stream inputs. In January and October 2003, Harbin-Ireland (2004) sampled sedi-

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BENTHIC/PELAGIC COUPLING—NUTRIENTS AND PARTICULATES 27 ments below oyster racks and 10 m away from the racks in eelgrass habi- tat and found that the sediments were slightly but significantly sandier immediately below the racks, appeared to be oxygenated to a depth of at least 10 cm in all locations, and did not exhibit a significant difference in the organic content among sampling locations. The report attributed the lack of a detectable difference in organic content beneath the racks to the already high inputs of detritus from eelgrass and concluded that the strong tidal flux appeared sufficient to prevent oxygen depletion in the sediments of eelgrass beds near oyster racks (Harbin-Ireland, 2004). C.  What Effects Can Be Directly Demonstrated by Research Conducted in Drakes Estero Itself? The relatively small, low-flow watershed and high-energy hydrogra- phy of Drakes Estero, dominated by strong tidal flux (Anima, 1991; John Largier, unpublished data), appears to be sufficient to produce low risk of eutrophication in most of Drakes Estero. Even though these properties endow the estero with excellent water quality, filtration by the cultured oysters could provide additional benefits to eelgrass production by lower- ing turbidity and adding nutrients because these limit eelgrass distribu- tion and production even in relatively oligotrophic estuaries (Carroll et al., 2008). In addition, the oysters in Drakes Estero could add ecosystem resilience in the event of a phytoplankton bloom or a high-turbidity event like sedimentation during run-off of stormwaters (Jackson et al., 2001). Also, the strong tidal currents and shallow water depths help maintain the oxygenation of sediments even under oyster racks where biodeposi- tion (feces and pseudofeces) is expected to be highest. Thus, sedimentary anoxia induced by DBOC shellfish is unlikely. D.  What Effects Can Reasonably Be Inferred from Research Conducted in Similar Ecosystems? Studies have shown that oyster reefs and oyster mariculture installa- tions can contribute to the transfer of suspended material into the sedi- ments (Mazouni et al., 1996; Nugues et al., 1996). These dense aggrega- tions of oysters also release dissolved nutrients that can support new growth of algae or seagrasses (Asmus and Asmus, 1991; Reusch et al., 1994; reviewed in Dame and Olenin, 2005). To varying degrees, suspen- sion feeders enhance benthic–pelagic coupling, nutrient remineralization, primary productivity, sediment transfer from water column to the bottom, and habitat complexity. Kaiser (2001) reviewed the effects of shellfish cultivation on estuarine ecosystems and identified a similar set of mecha- nistic influences, concluding that such processes have a generally positive

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28 SHELLFISH MARICULTURE IN DRAKES ESTERO influence on the overall water quality of a system. Oyster enhancement and oyster reef restoration is a major and expanding component of estua- rine restoration throughout the United States (Coen and Luckenbach, 2000; Lotze et al., 2006), now widely promoted by several environmental organizations (M. Beck, The Nature Conservancy, Feb 2009). Several reviews have highlighted the positive and negative feedback mechanisms observed in aquatic systems as a consequence of nutrient dynamics mediated by shellfish (Dame, 1996; Prins et al., 1998; Newell et al., 2005). Concentrated bivalve assemblages have been documented to play a role in regulating the abundance of phytoplankton in shallow seas (Newell et al., 2005; McKindsey et al., 2006). In summary, large popula- tions of filter-feeding molluscs provide the system with a capacity to buf- fer episodic influxes of suspended materials such as turbidity after storms or excess phytoplankton blooms (De Angelis, 1986), thus enhancing and sustaining water clarity. In their review, McKindsey et al. (2006) maintain that bivalve shellfish facilitate the cycling of nutrients both by direct excretion and through remineralization of organic biodeposits in the sediments. Nutrient regen- eration in aquatic systems may be governed by flushing rates and water residence times as well as the abundance and location of bivalves in the systems (i.e., shallow versus deep water) (Dame, 1996; Newell et al., 2005). Subsequent primary production is therefore influenced by the degree of internal cycling of nutrients such as phosphorus, silicon, and nitrogen, as well as the degree of import and export from the systems, as deter- mined by flushing rate (Dame and Prins, 1998). For example, some mea- surements of phosphorous budgets in and around shellfish assemblages have indicated a considerable removal of phosphorous from the system through biodeposition (reviewed in Dame, 1996; Newell et al., 2005). In relation to the cycling of silicon, Prins and Smaal (1994) concluded that the majority of silicon, a structural component of diatoms, was transferred to the sediment with little being released by bivalves. Most nutrient studies have focused upon the fate of nitrogen because this nutrient is generally considered to be the most limiting for primary production in marine and estuarine systems. Benthic bivalves play an important role in nitrogen cycling in both subtidal and intertidal systems, usually through the release of ammonium (NH4+). Nixon et al. (1976) con- cluded that nitrogen flux across oyster reefs was highly variable and was heavily influenced by tidal flow. Dame (1986) reviewed a body of work relating to nutrient fluxes induced by Crassostrea gigas filtration and biode- position in northern France and concluded that 15–40% of nitrogen input to the water column was recycled from oysters and that the measured values were always higher than the estimated values, probably enhanced by mineralization occurring in adjacent sediments containing oyster

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BENTHIC/PELAGIC COUPLING—NUTRIENTS AND PARTICULATES 29 biodeposits. However, Dame and Libes (1993) contended that nitrogen is retained within the water column through direct recycling of nitrogen from shellfish (Crassostrea virginica) to phytoplankton. Newell et al. (2002) showed that oyster biodeposits can also serve as sites for the removal of nitrate from the ecosystem through the conversion of nitrate to nitrogen gas by anaerobic bacterially mediated processes (denitrification). Although no specific study relating oysters to nutrient dynamics, sediment deposition, and water quality has been conducted in Drakes Estero, it is reasonable to assume that processes identified here apply under similar conditions (i.e., oyster production levels, and hydrological flushing and water residence times).