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The Willapa Bay oyster reserves in Washington state: fishery collapse, creating a sustainable replacement, and the potential for habitat conservation and restoration.

ABSTRACT Oysters have been an important resource in Washington state since the mid 1800s and are intimately associated with recent history of the Willapa Bay estuary, just as they have defined social culture around much larger U.S. east coast systems. The Willapa Bay oyster reserves were set aside in 1890 to preserve stocks of the native oyster Ostrea lurida in this estuary, but these stocks were overfished and replaced with the introduced Pacific oyster Crassostrea gigas during the late 1920s. Pacific oysters have spawned and set naturally in this estuary on a fairly regular basis since that time, and have formed the basis of a sustainable fishery established on state oyster reserves. The fishery is managed as an annual sale of oysters to private aquaculture interests. Oysters are harvested mostly by hand from intertidal tracts, usually moved to better growing areas closer to the estuary mouth, and shell is required to be returned to the reserves to perpetuate the fishery. Although oyster harvest for human consumption will remain an important social management goal, these bivalves have been shown to provide a suite of other ecosystem functions and services. A survey of the reserves suggests that they represent 11.2% of the intertidal habitat in Willapa Bay and cover substantial subtidal areas as well. A comparison with historical maps suggests that most of the low intertidal area in the reserves formerly populated by native oysters is now covered primarily with eelgrass (Zostera marina), which potentially serves as important habitat for numerous other organisms, including juvenile salmon, Dungeness crab, and migratory waterfowl like black Brant. Native oysters can still potentially be restored to some of these areas, but the value of both introduced oysters and eelgrass as habitat and ecosystem engineers also deserves attention, and the reserves provide an excellent place to elucidate the role of these additional conservation targets at the landscape scale.

KEY WORDS: oyster reserves, Ostrea lurida, Crassostrea gigas, Washington, oysters, habitat, eelgrass, recruitment

INTRODUCTION

The Washington state oyster reserves currently represent about 4,400 ha (10,873 acres) of tidelands that were originally set aside by the first territorial legislature in 1890 to preserve stocks of the native oyster (Ostrea lurida, Carpenter 1864) for oyster farmers under the direction of the Washington State Department of Fisheries (now the Washington Department of Fish and Wildlife (WDFW)) (Woelke 1969, Westley et al. 1985). Since that time, the state legislature has periodically reviewed the laws and modified them to fit the current nature of the fishery. The fishery for native oysters paralleled numerous others around the world, starting out as a capture fishery that ultimately overexploited the oyster stock, leaving only remnant populations in most areas where they were abundant along the west coast of the United States (Baker 1995, Kirby 2004, Beck et al. 2009, Polson & Zacher12009, White et al. 2009). However, it has now become a large-scale commercial farming operation and a much smaller scale recreational fishery for the Pacific oyster (Crassostrea gigas, Thunberg 1794), which was introduced to Washington state waters in 1920 (Steele 1964, Chew 1990, Lindsay & Simons 1997, Ruesink et al. 2005, White et al. 2009). Recent legislative changes in 2001 and 2007 involved creating two advisory committees and setting aside funds generated from shellfish sales on the reserves to cover expenses, assist with research, and establish a shellfish onsite sewage grant program. Originally, 4,548 ha (11,238 acres) in Willapa Bay and 1,821 ha (4,500 acres) in South Puget Sound were included in the Washington state reserve system, but these totals were reduced to about 3,995 ha and 405 ha, respectively, as tidelands were sold to private shellfish growers. Although native oysters are currently rebounding on portions of the Puget Sound reserves in Oakland Bay, and there has been renewed interest in recreational, tribal, and commercial clam fisheries therein, they were generally reduced to small parcels of some of the least productive lands, and use has been limited since 1927 (Westley et al. 1985). We focus, instead, on the Willapa Bay oyster reserves, where a sustainable and important fishery for Pacific oysters has been maintained. Furthermore, because these reserves represent a relatively large portion of the habitat in this estuary, the ecosystem role of both native and introduced bivalves can be evaluated, and management for both conservation and sustainable harvest considered.

The history of the Willapa Bay oyster reserves is intimately associated with the history of the oyster industry and tideland ownership in Washington state (Woelke 1969). At the time of the 1849 gold rush in California, the native or "Olympia" oyster, O. lurida, was harvested in a true open-access fishery in Willapa Bay, which involved hand tonging and moving small oysters from natural beds to other intertidal areas, where they were held until shipment, usually by sailing schooners to markets in San Francisco (Baker 1995, White et al. 2009). From the outset, harvest was extensive, and the lack of knowledge about the life cycle of the native oyster by these early fishers, combined with harvest techniques used, contributed to depletion of the native oyster stocks and lack of renewal, because oysters were moved to higher intertidal areas and shell was not returned to the low intertidal and subtidal areas where these oysters were abundant and where they would survive after setting. The Washington State Territorial Legislature passed the first oyster laws in 1877, which made it possible to own up to 20 acres of tidelands not covered by natural oysters for development of oyster lands. The new act prohibited private ownership of natural oyster beds but gave rights to discoverers of these beds to use 4.47 ha for 5 y. A winter freeze in 1888 reportedly killed 60% of the oysters above low tide (Townsend 1892). In 1890, the first state legislature revisited the issue and set the natural oyster beds aside as reserves to be retained in the public domain and to provide juvenile oysters, called "'seed," for the "oyster farmer" and an exploitable stock for the "fisherman.'" They further defined the principles of private tideland ownership and development of tidelands for "oystering." The Bush Act of 1895 expanded tideland ownership and provided for survey, platting, filing, and purchasing those lands not included in the reserves.

Nonetheless, adequate guidelines for preservation were weak, and by 1900, the reserves in Willapa Bay had already witnessed serious depletion of native oyster stocks, and the industry was approaching extinction. As a result, in part, of this decline, the U.S. Commissioner of Fisheries visited the bay in 1893 and was impressed with the potential for importing and growing the Eastern oyster Crassostrea virginica (Gmelin, 1791). With approval of the state fisheries commissioner, 80 barrels of Eastern oysters were planted in the Palix River area of Willapa Bay (Townsend 1896). These oysters survived, grew well, and contributed to a resurgence of the oyster industry from 1895 to 1917. The industry relied on annual shipments of oyster seed delivered by trainload from the east coast, because these oysters rarely spawned successfully in Willapa Bay. In 1919, Eastern oysters in Willapa Bay began to die. Although attributed to red tide, no documented account of the cause for this catastrophic event exists. The industry did not recover until introduction of the Pacific oyster, C. gigas, from Japan in 1928 (Sayce 1976). Pacific oysters have continued to be the mainstay of the industry. Although the Pacific oyster reproduced successfully in Willapa Bay, growers found it easier to import seed from Japan, resulting in little activity on the oyster reserves through the 1930s. By the 1940s, a considerable stock of Pacific oysters had naturally set and accumulated on the reserves. When oysters became impossible to obtain from Japan during World War II, there was renewed interest in the reserves and the laws were changed in 1947 to protect Pacific oyster stocks on the reserves. In 1949, the goals of the reserve management system were broadened to include providing seed and "stocking public beaches." From 1949 to 1967, WDFW used two people to manage the Willapa Bay reserves and has used one person since that time (Woelke 1969, Tufts 1987). Reserve management then and now involves three basic activities. The first activity is supervising an annual sale of oysters to the highest bidder. Buyers are typically shellfish growers, because each bidder is required to sign a contract to harvest all oysters on a tract. Furthermore, most of the oysters must be moved or transplanted to better growing areas where they can obtain enough food to fatten before they can be sold commercially (closer to the mouth of the estuary (Banas et al. 2007)). The second activity includes a shell return program in which the buyer is required to replace the amount of oysters harvested with a proportion of their volume in empty shells to provide substrate for natural oyster sets and, therefore, future harvest. The third, and last, activity includes updating, surveying, and policing reserve boundaries. Finally, WDFW also supervises separate oyster seed-catching operations on the reserves and, since 1989, has charged a cultching fee for placing shell on reserve grounds.

We provide an update on the current status of the Willapa Bay oyster reserves, including results of an intertidal habitat survey conducted in 2006 and 2007. The current fishery for Pacific oysters on the reserves and its management, including shell return to the reserves and an annual assessment of oyster settlement, are described. Current status is contrasted with historical condition by comparing an 1892 map of native oyster harvest areas with results of the current habitat survey. Last, we outline a plan for research and continued sustainable harvest and management of Pacific oysters, conservation of existing habitat, and the potential for restoring native oysters to the reserves.

MATERIALS AND METHODS

Study Site and Intertidal Survey

The Willapa Bay oyster reserves consist of approximately 4,033 ha of intertidal and subtidal land divided into five separate reserves located predominantly in the southern portion of Willapa Bay, the second largest estuary along the west coast of the United States (46[degrees]40' N, 124[degrees]0' W; Fig. 1). Because the reserves were originally set aside to preserve areas where the native oyster thrived, the majority of land consists of either subtidal channel or low intertidal ground. We assessed the current status of intertidal habitats (aquaculture, eelgrass, burrowing shrimp, and bare tideflat) on the reserves as part of a larger survey to map these habitats in the entire estuary from 2006 to 2007.

Sampling was conducted on a grid with stations located at 200-m intervals across the intertidal. Each accessible location was visited at low tide by hovercraft. Locations within commercial Pacific oyster beds or harvest areas were generally not visited because they were impossible to traverse by hovercraft, and because oysters were viewed as a temporally variable habitat, only the boundaries of these areas were assessed (as noted later). At each station, data were recorded into a Trimble GeoXT mapping-grade GPS system (Trimble, Sunnyvale, CA). A photograph of a 0.25-[m.sup.2] quadrat was taken at most locations to verify visual assessments. At each station, we recorded the presence and density of two eelgrass species (native Zostera marina and introduced Zostera .japonica), macroalgae, live oysters, and shell in a 10-[m.sup.2] area; the number of burrows within a 0.25-[m.sup.2] quadrat; and burrow occupants (clams, polychaetes, and thalassinid burrowing shrimp); as well as basic sediment characteristics. Density of each eelgrass species, macroalgae (classified loosely into brown, green, or red), oyster, and shell was classified into four categories: absent; present, minor (<25% cover); present, medium (25-75% cover); and present, major (>75% cover). A pilot survey suggested these categories related directly to quantified assessments using smaller quadrats, but the larger 10-[m.sup.2] scale was more useful to classify vegetation signatures in aerial photographs. Burrow occupants were determined by extraction with a shrimp pump or by expert opinion, taking into consideration sediment type, feces, burrow lining, burrow diameter, and burrow density. At each station, we recorded elevation relative to height above ellipsoid using an LI Trimble ProXR (Trimble, Sunnyvale, CA) mounted at a fixed position on the hovercraft to create a complete digital elevation model by combining our low-resolution elevation model with a LiDAR data set previously collected for the upper intertidal.

[FIGURE 1 OMITTED]

Data were downloaded, postprocessed, and exported to using GPS Pathfinder Office (version 4.2; Trimble, Inc., Sunnyvale, CA). In ArcMap (version 9.3; ESRI, Redlands, CA), the density classification for each factor was assigned an integer value (04) and interpolated using inverse distance weighted to produce a continuous raster image. These raster images were then reclassified into integer values (0-0.5 = 0, 0.5-1.5 = 1, and so on) and converted to polygons. Calculations of area include polygons designated as level 3 (present, medium) and level 4 (present, major) only. Elevation data from the ProXR were downloaded and postprocessed using GPS Pathfinder Office.

The data were corrected using a Trimble L1 5700 base station or NGS-CORS station (P415, Trimble, Sunnyvale, CA). These data were sent to the GIS group at the Olympic Natural Resources Center, University of Washington, for processing. They extracted, interpolated, and aligned the data with the high intertidal LiDAR data set to create a digital elevation model referenced to mean lower low water that covered the entire intertidal area of Willapa Bay. In addition, we created a map of the intertidal areas by creating polygons of the exposed tideflats visible in orthorectified and georeferenced aerial photography taken at low tide in 2005.

Reserve Boundaries, Current Pacific Oyster Sales Areas, and Historical Map Comparison

Reserve boundaries have been surveyed and marked historically with pilings and monuments. An oyster reserve layer for Willapa Bay was created by collecting monument and piling positions when possible, and estimating boundaries and corners from historical survey descriptions where monuments and pilings are now missing. We also confirmed some of these piling and monuments during our intertidal mapping survey. Data from the larger survey were cropped to the reserves to calculate coverage, density, and distribution of habitats, elevation, and sediment characteristics. Similarly, coordinates of current Pacific oyster sales areas were recorded on handheld GPS units and used to create a data layer in ArcMap. We created a GIS layer of historical "natural" and "cultured" native oyster (O. lurida) beds by georeferencing a map created by the U.S. Fisheries Commission (Collins 1892) and drawing polygons around the relevant beds. Native oysters were occasionally observed in our survey; however, their numbers were low and distribution was patchy, making our 200-m grid inadequate for creating a meaningful map.

Pacific Oyster Sales, Larval Sets, and Shell Return

An annual sale of oysters from the reserves involves a call for bids on individual tracts within the reserves, acceptance and opening of bids from interested parties, and awards to the highest bidder. Buyers then sign a contract to harvest all oysters present on the tract and replenish shell. Buyers pay by the bushel (1 bushel = 0.035 [m.sup.3]) of oysters harvested. The sale is monitored by a reserve manager, and data on sales are recorded. A shell return program was instigated in 1958 to require growers who harvested oysters to return a percentage of the volume harvested (initially one half of the purchase volume) as empty shell back to the reserves. Because of staff reductions, WDFW was unable to handle shell return from 1970 to 1974, but in 1975 began requiring purchasers to return shell to the beds. The amount of shell required to be returned was reduced to 40% of the volume harvested in 1977 and has remained at that level since. Shell is generally returned to the same area where harvest occurred.

Some local settlement of Pacific oyster larvae (spatfall) has occurred nearly every year since these oysters were introduced to Willapa Bay in the 1920s. In 1942, WDFW and the University of Washington began a sampling program to determine the magnitude and timing of these recruitment events. Each week 2 sets of 20 Pacific oyster shells were strung together on a wire with the inner face down, and anchored just above the substrate at several locations in the estuary. One set was retrieved a week later (weekly shell strings) and the other set was left until early fall to obtain cumulative spatfall information (seasonal shell string). Data collected (1956 to 1983) were compiled from various sources and reported previously (Trimble et al. 2009). Here we reanalyzed the seasonal shell string data for three locations (Peterson, Station III, and Mill Channel; Fig. 1) for which data were most complete. We also include information on relative abundance of spat (noncommercial, <3 spat per shell; commercial, 3-25 spat per shell; good, 25-50 spat per shell; and excellent, >50 spat per shell) for 1936 to 1955 (Lindsay et al. (1959) and for 1984 to 2001 (from larval data and discussion with Dennis Tufts). Shell string sampling was reinitiated in 2002. We relate results to natural seed production in the south end of the estuary, and particularly to sales and continued cultching efforts on the Willapa Bay oyster reserves. WDFW allowed oyster growers to construct racks on the state oyster reserves that support strings or bags of oyster shell (cultch) on which the oyster larvae set. Reserve areas that have been used to obtain natural oyster seed are primarily located along the Naselle River channel in the Long Island Slough Reserve (LISOR) or the Long Island Reserve (LIOR).

RESULTS

Current Habitat Survey and Historical Map

A total of 4,238 grid stations were visited throughout Willapa Bay in 2006 and 2007; of these, 783 were located on oyster reserves. About 40% of the reserve area (1,587 ha) is subtidal and much of the rest is very low intertidal, so a large portion of the reserve lands were not directly assessed in this habitat survey (Table 1). Although tidal elevations have likely changed substantially since the late 1800s, an analysis of the historical map overlaid on current elevation suggests that native oyster grounds from which oysters were harvested are now at least 1 m lower in the intertidal on average than areas noted as cultivated (areas where harvesters moved oysters before shipping; Table 2). Current Pacific oyster culture is generally also at this higher tidal elevation. Areas denoted historically as native oysters coincide reasonably well with intertidal areas now set aside as reserves (58% of the areas noted as native harvest areas are now within the reserves; Fig. 2). Yet, these areas of the reserves that once harbored native oysters are now covered by extensive areas of eelgrass (1,309 ha; Fig. 2, Table 2), most of which is native Z. marina (roughly 77% calculated from ground survey data). Thirty-one percent of the slightly higher cultivated areas that were once used for holding oysters are now privately owned and cultivated for Pacific oysters. These areas are also vegetated with eelgrass (92% Z. marina from ground survey data). A much smaller portion of the historical area where native oysters were harvested and cultivated are currently occupied by burrowing shrimp (535 ha and 355 ha, respectively, Table 2). Burrowing shrimp mostly reside at higher tidal elevations on the Nemah reserve (294 ha; Table 2).

Sales

The intertidal ground that constitutes the oyster reserves in Willapa Bay has, in general, proved to be good for Pacific oyster seed production; but, except for small portions, does not produce a market-quality harvestable oyster resulting, in large part, from the majority of the currently used ground being located in the southern half of the estuary beyond what is known as the fattening or condition line (Fig. 1) (Chapman & Esveldt 1943, Banas et al. 2007). A relatively small portion (453 ha) of intertidal ground is currently being used for oyster production (Fig. 1, Table l), and this ground averages about +0.4 m mean lower low water (Table 2). Since the 1930s, the location and extent of oyster sales and harvest has depended on the success of Pacific oyster settlement and recruitment in previous years, as well as shell return to the area. Most tracts have been sold on a 3-5-y cycle since the late 1960s, which allows time for recruitment of new oysters and/or planting by WDFW staff. Initially, both intertidal and subtidal tracts were sold and harvested by dredge or picked by hand. With the exception of some experimental trials in 2005 and 2006 (46.7 [m.sup.3] harvested from the LIOR), oysters have not been dredged since 1979. From 1945 through 2001, 87,934 [m.sup.3] of oysters were harvested generating $2,299,290, which was deposited into the Washington state general fund. From 2002 to 2009, an additional 27,027 [m.sup.3] were sold generating $1,854,758, which was deposited in the newly created Oyster Reserves Land Account. Sales averaged 1,685 [m.sup.3]/y (47,865 bushels) at an annual return of $64,342, but a clear increase in both the quantity of oysters and the price obtained began during the early 1990s, and the average sales since 1992 have been 2,991 [m.sup.3] (84,972 bushels) with a return of $167,618, with substantial sales from the Nemah Reserve where enhancement took place (Fig. 3). No sales of oysters from the Willapa Oyster Reserves took place in 1984, because growers who historically bought reserve oysters participated in a transplant program with one of the major oyster growers in Willapa Bay and did not bid.

Hard-shell clams (the Manila clam, Ruditapes philippinarum (Deshayes 1853), and the native littleneck, Leucoma staminea Conrad 1837) have also been intermittently sold from the Willapa Bay oyster reserves. Sales held in 1979, 1981, 1982, and 1984 produced 6,241 kg of clams; recent sales in 2003, 2006, 2007, and 2009 produced 45,234 kg. These sales were all located on LIOR, where suitable areas for hard-shell clam settlement and survival are present.

Oyster Larval Sets and Shell Return

Seasonal recruitment and survival of Pacific oysters to shell strings averaged 8.3 recruits per shell, although the range was high (0 90 recruits per shell), and commercial sets (>3 recruits per shell) occurred in more than half (44 of 73) the years monitored (Fig. 4). More consistently high recruitment occurred from the late 1930s through about 1959, after which recruitment was low through 1981 and then increased and was generally better through 2005. The period of low recruitment roughly brackets a period of low harvest from the reserves that began in 1969 and ended in 1979 (Fig. 3) and an extended period of low values of the Pacific decadal oscillation, a climate index for the northeast Pacific (Hare & Mantua 2000). Although records are incomplete, recruitment of Pacific oysters in Willapa Bay from 2005 to 2010 has also been minimal, but it is too soon to know whether this represents another shift in the long-term pattern.

The Washington state legislature implemented a 10% charge or cultching fee for use of racks placed on the reserves in 1989 (10% of the shell placed on the reserves to obtain seed by growers needed to be returned to the reserves). The oyster seed obtained from this fee was returned to the state reserves and it has contributed to increased yields and revenues since the early 1990s. WDFW also supplemented the return to reserves by constructing a state-owned seed rack in the LISOR, which was operational from 1990 to 1998. This rack produced an additional 7,000 seed bags of oysters, most of which were also planted on the reserves and contributed to increased sales during these years. Introduction of remote setting of Pacific oysters from hatcheries has reduced the dependence of most growers on natural seed catch. The LISOR was, for many years, the best area for obtaining oyster seed in Willapa Bay. During the past 15 y, setting areas seemed to have shifted and many growers who once exclusively used the reserves for obtaining seed have found that tidelands that they own or lease along the west side of Long Island now get better seed sets. Cultching effort on the reserves has therefore declined, resulting in part from the cultching fee, but mostly because oysters did not routinely set in the LISOR on the east side of the bay.

DISCUSSION

Oysters have been an important resource in Washington state since before statehood, and they have defined the recent history of the Willapa Bay estuary, as they have much larger U.S. east coast systems like Chesapeake Bay (Sayce 1976, Haven et al. 1978, MacKenzie 1997, Keiner 2009, Trimble et al. 2009). Problems associated with an open-access fishery for the native oyster O. lurida, such as overfishing and lack of knowledge about returning shell to the system, are also similar to those that have befallen wild oyster fisheries elsewhere (Ruesink et al. 2005, Beck et al. 2009, White et al. 2009). The early fishery for native oysters resulted in stock declines that followed a similar trajectory as that for C. virginica in Chesapeake Bay, although other factors like disease significantly affected Chesapeake Bay oysters over time, and additional factors continue to influence recovery of both stocks (Kennedy & Breisch 1983, Mann et al. 1991, Rothschild et al. 1994, NRC 2004, Powers et al. 2009, Trimble et al. 2009). As a result of the timing of the fishery collapse of native oysters and the choice at statehood to privatize tidelands, jurisdictional differences and cultural and political events that erupted into culture wars between scientists, politicians, and watermen involved in Chesapeake Bay oyster management (Keiner 2009), did not occur in Willapa Bay. Oyster fishers and industry members were also much more receptive to the advice of biologists and scientists who advised planting first Eastern oysters (C. virginica) and then Pacific oysters (C. gigas) to resurrect their industry. Pacific oysters became the industry mainstay and at the same time also proliferated on the Willapa Bay oyster reserves, because they began reproducing naturally in the estuary, with the first reported set in 1936. The laws governing reserves were altered to reflect the importance of this new oyster, and a potentially sustainable fishery was ultimately established by creating a shell return program and rotating harvests among reserve areas.

[FIGURE 2 OMITTED]

Willapa Bay is only a fraction of the size of most U.S. east coast estuaries (the entire bay is roughly the size of the James River subestuary within Chesapeake Bay, for example), yet it is the second largest estuary along the open west coast of the United States and produces the largest share of the oysters from this coast. Oyster sales are only conducted on 11% of the Willapa Bay reserves, and harvests from the reserves currently represent a relatively small fraction of oysters landed in Washington state (equivalent of 1% of 27,669,135 kg landed in 2008), but this level has been sustained over time since at least 1950, and recent harvests have increased (Fig. 3). This is unlike harvest levels in many if not most other "wild" fisheries, which have leveled off or declined (Kirby 2004, Ruesink et al. 2005, Jackson 2008), and is a result, at least in part, of the privatization of land and substantial growth of the aquaculture industry in this estuary. Recent advances and success of shellfish hatcheries with corresponding availability of eyed larvae and remote setting facilities have changed the face of the industry, and resulted in complete control over the life cycle and put-and-take commercial aquaculture operations. This advance and even a move toward privatization are now leading to implementation of aquaculture as a potential solution to the continued decline of wild fisheries for C. virginica in Chesapeake Bay, more than 200 y after the inception of large-scale oyster fisheries there (Keiner 2009, Fincham 2010). Although the Willapa Bay oyster reserves have persisted and still rely on natural oyster production, the latest seed crisis and lack of commercial oyster sets will require persistence and ingenuity to sustain the effort.

[FIGURE 3 OMITTED]

Oysters and other shellfish have been shown to provide a suite of ecosystem functions and services in addition to direct harvest for human consumption (Lenihan & Peterson 1998, Piazza et al. 2005, Coen et al. 2007, Grabowski & Peterson 2007). Probably the most studied of these is their ability to influence water quality by removing seston from the water via filter feeding and subsequently contribute to benthic pelagic coupling by depositing feces and pseudofeces to the substrate (Newel12004). This ecosystem role clearly depends on the quantity and location of bivalves present, and numerous aspects of the system itself that contribute to its carrying capacity for these filter feeders. A growing amount of work has recently been conducted on quantifying carrying capacity, particularly for bivalve aquaculture, by developing an array of models that attempt to predict the responses of systems to the addition of cultured molluscs (McKindsey et al. 2006, Ferreira et al. 2009, NRC 2010). In the case of the Willapa Bay oyster reserves, it is interesting to note that shellfish growers have voiced concern for some time about exceeding the capacity of the estuary to produce oysters, or at least to fatten oysters on their beds, and therefore did not want oysters on the reserves to become "overpopulated" (Woelke 1969). Hedgepeth and Obrebski (1981) speculated that oysters near the mouth of the estuary are most likely to have this effect on oysters in the southern part of the bay, and Banas et al. (2007) explored this using a 3dimensional circulation model and a series of measurements of phytoplankton biomass and productivity along a north south or mouth-to-river axis. Results suggested that the source of nutrients and resulting phytoplankton production in Willapa Bay is almost entirely the ocean, especially during summer months, and this primary production enters the estuary at all depths via strong tidal mixing. The plume of highly productive water extends into the bay as far as horizontal advection takes it on flood tides; therefore the fattening line that the growers have observed is likely a real phenomenon limiting oyster growth in the south end of the estuary where water residence time is more than 40 d and new production is limited. Thus, it is unlikely that oysters found south of this line (which includes most of the reserves) would limit growth of oysters to the north; however, oysters found on the majority of the commercial fattening and harvest beds (and perhaps portions of the Nemah Reserve) may limit growth of oysters farther south. They concluded that oysters in Willapa Bay appear to be within an order of magnitude of their carrying capacity, but their model also showed that local circulation was important and that oceanic water rarely spent enough time over the intertidal flats to be fully grazed and often left the bay on the next tidal cycle. Since then, measurable depletion of chlorophyll from the water by oysters over these commercial beds at realistic local scales has been documented (Dumbauld et al. 2009, Wheat & Ruesink, unpubl. manuscript), even though chlorophyll could increase over ungrazed tidal flats (probably as a result of resuspension of benthic microalgae). This suggests that native oysters probably had less of an impact on phytoplankton clearance in the broader estuary because they were located predominantly in the southern areas, and especially because native oysters have lower filtration rates than Pacific oysters (Couch & Hassler 1989).

A second highly valued ecosystem function is the provision of estuarine habitat. The Willapa reserves represent 11.2% of the intertidal portion of the estuary, and our surveys suggest that they contribute substantially to estuarine habitat for other species. As such, they should also be viewed in the context of new efforts to create marine reserves and to conduct spatial planning (Fraschetti et al. 2009, Lester et al. 2009, Foley et al. 2010). The marine habitat most widely recognized to be important is submerged aquatic vegetation, but oysters themselves act as ecosystem engineers and have been shown to provide structured habitat for many aquatic invertebrates and fish (Zimmerman et al. 1989, Jones et al. 1997, Breitberg 1999, Posey et al. 1999, Bruno & Bertness 2001, Grabowski et al. 2005, Coen & Grizzle 2007). Submerged aquatic vegetation in Willapa Bay takes the form of the eelgrass Z. marina (Linnaeus 1785), the introduced eelgrass Z. japonica (Ascherson & Graebner), and several species of macroalgae (both indigenous and nonindigenous; Hansen unpubl, data). Although native oysters historically covered most of the reserves, and therefore about 11% of the intertidal area in the estuary, eelgrass now covers about 1,796 ha of the reserves and thus represents a very significant portion (8%) of this habitat in the estuary. As a result of the low tidal elevation of the reserves, the majority (78%) of this eelgrass is native Z. marina, which has been shown to be a valuable habitat for many invertebrates and fish in Willapa Bay and other U.S. west coast estuaries, as well as other estuaries worldwide (Simenstad et al. 1982, Simenstad & Fresh 1995, Bostrom et al. 2006, Hosack et al. 2006, Ferraro & Cole 2007). Both oysters and ee[grass provide structured habitat that is usually contrasted with open unstructured sediment in these comparisons. We found less open unstructured intertidal habitat than structured habitat on the reserves, also presumably a result of their low intertidal elevation and location in the estuary (estimate of 22% based on 2,939 ha dominated by burrowing shrimp and difference of 2,433 ha of open habitat not covered with oysters or either species of eelgrass).

[FIGURE 4 OMITTED]

Predation is viewed as the strongest influence on soft-sediment tideflat communities, and structure-forming species like oysters and eelgrass greatly influence these communities by providing refuge and also by influencing recruitment (Posey et al. 1995, Peterson et al. 2000, Lenihan & Micheli 2001). In Willapa Bay, oysters and eelgrass have been shown to support equally and more diverse communities of benthic infauna than unstructured open tideflats, which are often dominated by thalassinid burrowing shrimp (Posey et al. 1991, Dumbauld et al. 2001, Hosack et al. 2006, Ferraro & Cole 2007). Larger fish and invertebrates, including juvenile Dungeness crab, English sole, and salmon, have also been shown to use these estuarine habitats, but studies to date have shown that in addition to the presence of structure, life history stage and location in the estuary are important considerations. For example, 0 + Dungeness crab clearly preferred the structure provided by oysters and eelgrass, but having reached a predation threshold, older 1 + crab used open mud habitat for foraging (Holsman et al. 2006). Although juvenile flatfish have been shown to associate with structure for protection but forage in open habitat elsewhere (Laffargue et al. 2006), studies to date have not distinguished function, and juvenile English sole were captured in equal density over oysters, eelgrass, and open mudflats in Willapa Bay (Hosack et al. 2006). This was also true for juvenile Chinook salmon, but they were more abundant at locations closer to the estuary mouth, and they appeared to use eelgrass over oysters and open habitat when individually tracked in a large field enclosure and laboratory tanks (Semmens 2008, Dumbauld et al. 2009). Other structure-oriented fish like gunnels, tube-snouts, perch, and some juvenile rockfish have also been shown to use eelgrass and oysters in west coast estuaries (Matthews 1990, Weschler 2004, Hosack et al. 2006, Dauble 2010). Structure, including both species ofeelgrass and oysters, also provides a substrate on which Pacific herring have been shown to deposit their eggs in Willapa Bay (D. Pentilla, unpubl, data). Egg survival has not been measured, however, and it seems likely that eggs deposited on the larger blades of the native eelgrass in low intertidal habitat would be less subject to desiccation and would survive better than those found on the much smaller blades of introduced Japanese eelgrass in upper areas (Jones 1972).

Last, structured habitat and particularly eelgrass are used heavily and valued as foraging areas for waterfowl, waders, and shorebirds. Brant geese in particular graze heavily on eelgrass, and use Willapa Bay and other estuaries as stopovers on their trek to arctic breeding grounds (Wilson & Atkinson 1995, Moore et al. 2004). Willapa Bay ranks sixth among estuaries as a staging area for these geese, and at least 1 area on the LIOR is heavily used and serves as a monitoring location for annual abundance surveys. This area was clearly dominated by native oysters in the 1800s and it is unclear whether geese would have used it as heavily then. Dabbling ducks also feed on eelgrass and have been shown to alter their foraging habits and switch to nonnative Z. japonica in areas where it has become abundant (Baldwin & Lovvorn 1994, Lovvorn & Baldwin 1996). Like fish and invertebrates, shorebird use of structured habitats is species specific (Luckenbach 1984, Connolly & Colwell 2005), but they are more likely to use upper intertidal areas that are available for longer periods of time and also available on less extreme tides. Nonetheless, fairly extensive areas of the reserves are now relatively undisturbed by humans, which are known to decrease use (Yasue 2006), and the value of these areas for feeding by all 3 types of birds should be considered.

Seagrasses are a declining resource in many eutrophic estuaries such as Chesapeake Bay and other locations worldwide (Orth et al. 2006, Hughes et al. 2009, Waycott et al. 2009, Orth et al. 2010). This is not the case in Willapa Bay, however, where eelgrass is relatively stable and even increasing (Dumbauld et al. 2009, Ruesink et al. 2010). Four mechanisms of disturbance and interactions between eelgrass and oyster aquaculture have been actively researched in Willapa Bay: (1) competition between oysters and plants for space, (2) nutrient supplementation to eelgrass from oyster biodeposits, (3) increased light to eelgrass from increased filter feeding by oysters and (4) complete or partial removal of plants by oyster harvest activity. Results to date suggest that the most significant impacts are the result of simple competition for space and direct removal via shellfish harvest (Wisehart et al. 2007, Dumbauld et al. 2009, Tallis et al. 2009, Ruesink et al. unpub, msp., Wagner et al. unpub, msp.). In the case of oyster reserve operations, oysters are most likely to compete directly for space, because harvest activities are generally conducted by hand, which has been shown to have less affect than mechanical harvest (Tallis et al. 2009). At the landscape scale, current Pacific oyster culture on the reserves represents a relatively small fraction (11%) of the reserve area and an even smaller portion (2%) of the intertidal area of the estuary. Furthermore, we found substantial eelgrass, Z. marina, comingling with oysters (Z. marina covered 44% of the reserve sales area; Table 2).

Management History and Recommendations

Willapa Bay oyster reserve management to date has focused almost exclusively on yield of Pacific oysters, with the annual oyster sale and attendant seeding operations being the focus of activity. Although even this goal has and continues to be controversial at times, our habitat survey results suggest that additional goals that take a broader landscape and ecosystem-based perspective should be considered. Although de facto conservation of those areas not set aside for oyster production has arguably occurred, active consideration could be particularly fruitful in light of information now in hand and numerous recent calls for marine ecosystem-based management and spatial planning (USCOP 2004, Granek et al. 2005, Leslie & McLeod 2007, Foley et al. 2010).

Written Washington state legislation covering the oyster reserves states that "it is the policy of the state to improve the reserves so that they are productive and yield revenue sufficient for their maintenance" (Washington State Administration Code RCN 75.25.060). Furthermore, it is also the policy of the state "to maintain the oyster reserves to furnish shellfish to growers and processors and to stock public beaches." An economic evaluation prepared by Woelke (1969) pointed out 2 policy constraints suggested by the commercial oyster industry that were considered in the past: (l) the reserves should not be sold unless each grower has an equitable chance at procuring them and (2) reserve sales should not compete with the industry and the reserves should not be overpopulated with oysters, because this might cause a general decline in oyster condition throughout the estuary. A later revision to the reserve laws in Washington requested that WDFW periodically inventory the state reserves and assign reserve lands into several management categories--including native Olympia oyster broodstock areas, commercial shellfish harvesting zones, commercial shellfish propagation zones designated for long-term leasing to private aquaculturists, public recreational harvesting zones, and unproductive land and that WDFW should develop a reserve management plan in coordination with the industry. Onsite surveys were conducted for each Puget Sound reserve in 1985, and a final report was submitted to the legislature (Westley et al. 1985), whereas only a draft report was prepared on the Willapa Reserves (Tufts 1987). Our survey represents the first quantitative attempt at achieving this objective. Issues surrounding reserve management resurfaced in 2001, and an industry advisory committee was granted authority to make recommendations regarding management practices on oyster reserve lands. The new legislation again suggested goals that would increase revenue through production of high-value shellfish, not be detrimental to the market for shellfish grown on nonreserve lands, and that would avoid negative impacts to existing shellfish populations.

Our review suggests that Pacific oyster harvest from the Willapa reserves is sustainable as long as "natural" oyster set is maintained, but this clearly fluctuates with environmental conditions. Thus, very low recruitment of oysters from the early 1960s through the early 1980s roughly coincided with a shift in the Pacific decadal oscillation (Fig. 4) (Hare & Mantua 2000) in the northeast Pacific, with cold years typically resulting in fewer spawning and setting events. This translated to reduced oyster sales from the reserves. Recent lack of recruitment in 2006 to 2009 and a potential decline in sales may be related to such a climate shift as well, but it is too early to tell. Current sales areas seem appropriately scaled to prevent overpopulation of the reserves and, because of their location in the southern portion of the estuary (predominantly south of the fattening line), the oysters present on them are less likely to influence the condition of other commercially grown oysters on fattening and harvest beds closer to the estuary mouth. These currently cultivated areas on the reserves represent a reasonably small fraction (10%) of the total area of the reserves and only 2% of the tideflat in the estuary, compared with the 20% occupied by commercial aquaculture operations (Fig. 1). Both quantity of oysters and, in particular, revenue generated from these reserves sales escalated from the mid 1990s onward as a result of active consideration of larval spawning and setting, and some expansion of planted areas utilizing this set, particularly those on the Nemah Reserve, which often generate higher value (Fig. 3). A tradeoff clearly exists between expanding sales in this area to generate funds and to maintain reserve operations, and potentially overstocking the estuary and affecting commercial operations elsewhere, because this is one of the only reserve areas north of the fattening line and is also an area where oysters and other habitats like eelgrass should be evaluated for their importance to fish and invertebrates that use the estuary as a nursery. Dungeness crab, which use oyster habitat, are more likely to recruit as juveniles to the Nemah Reserve than those to the south, and this area has already been used as a site for creating oyster habitat to mitigate losses of these crab resulting from dredging elsewhere in the estuary (Dumbauld & Kauffman 1999). Juvenile English sole and salmon may also be more likely to recruit and use estuarine habitat on this reserve than those located farther away from the ocean (Dumbauld et al. 2009). Habitat values and tradeoffs for these species should continue to be evaluated on this reserve and at the estuarine landscape scale.

The Willapa Bay oyster reserves were originally set aside to protect native oyster populations, and broodstock maintenance remains a stated goal in governing legislation. Although existing population levels are unknown, the current O. lurida population is only a miniscule fraction of what the bay historically supported. In response to concern over the reduced populations of this species in Puget Sound and Willapa Bay, WDFW developed an Olympia oyster restoration plan (Cook et al. 2000). This restoration plan was approved by the WDFW commission in 1998, but no funding was allocated. Nonetheless, studies were conducted in Willapa Bay that indicated that several factors influencing postsettlement survival currently prevent this oyster from greatly expanding its distribution and attaining preexploitation status in the estuary (Buhle & Ruesink 2009, Trimble et al. 2009). These factors included a combination of recruitment preference to Pacific oyster reefs located higher in the intertidal where aerial exposure causes mortality, competition with fouling organisms including introduced species of tunicates and bryozoans after settlement, and predation by two introduced species of drills and a flatworm. Recruitment limitation resulting from lack of broodstock did not appear to be an issue. This broodstock is believed to be predominantly located in very low intertidal areas or subtidal areas of the reserves and, although surveys have been proposed, they have not yet been completed. Portions of the LIOR and particularly the Bay Center and Willapa River reserves, which are almost entirely subtidal, would be of particular interest. Preliminary investigations (Trimble, unpubl, data) suggest that substrate limitation may constrain recruitment of native oysters in subtidal areas where they are less subjected to fouling issues present in the low intertidal, and that these areas of the reserves could potentially be used to enhance stocks directly and to be used as a source of material for low intertidal areas if other factors like outplanting techniques (perhaps using small clumps) are also considered.

Shellfish harvest has been an important activity supporting local coastal economies in Washington state for at least 150 y. Clearly, societal goals will continue to include this activity, and the Willapa Bay oyster reserves should contribute to this goal. A broader perspective suggests that the reserves have and will continue to contribute to other ecosystem functions and services as well. Native oysters, Pacific oysters, eelgrass, and burrowing shrimp can all be considered foundation species or ecosystem engineers (sensu Jones et al. 1997, Bruno & Bertness 2001), and they influence the environment and presence of other species when they are abundant. These engineers are considered conservation targets because they can ameliorate degraded habitats for other species (Crain & Bertness 2006), and engineering feedbacks can lead to persistent or stable states. We suspect that burrowing shrimp lead to one alternative stable state, whereas the presence of oysters and/or eelgrass may dominate another, given that burrowing shrimp have been shown to interact negatively with both eelgrass (Dumbauld & Wyllie-Echeverria 2003, Siebert & Branch 2005, Siebert & Branch 2006, Berkenbusch et al. 2007) and oysters (Dumbauld et al. 1997). Although burrowing shrimp destabilize the sediment, eelgrass and oysters can stabilize the sediment. Burrowing shrimp are currently only present in large numbers on the Nemah Reserve, but they are declining in abundance throughout Willapa Bay and other estuaries along the coast of the Pacific Northwest. The mechanism behind this shift between alternative states is unknown, but such shifts seem likely to have occurred historically as well, resulting in the need for the oyster industry to treat these shrimp as pests beginning during the late 1950s (Dumbauld et al. 2006). Native oysters are likely even more susceptible to bioturbation from shrimp, but it is unclear whether they formed reefs before they were harvested and how stable these were in the face of burrowing shrimp invasions.

The Willapa Bay oyster reserves provide an excellent place to continue to preserve and, potentially, to study multiple conservation targets (native oysters, aquaculture species, eelgrass, and burrowing shrimp), the ecosystem functions and services they provide, possible mechanisms for shifts between stable states, and ways to maintain resilience to such shifts (Carpenter et al. 2001, Folke et al. 2004). The outlook is particularly favorable now that some of the funds generated from reserve sales are designated for research. Although the recent legislation emphasizes research on aquatic nuisance species and burrowing shrimp, the advisory committee has voiced support for a plan based on broader ecosystem goals for coastal estuaries.

ACKNOWLEDGMENTS

We thank our numerous predecessors at the University of Washington, Washington Department of Fish and Wildlife (then Fisheries), and Willapa Bay oyster industry for having the foresight to encourage and continue to collect data on oyster spawning and setting in Willapa Bay. These include but are not limited to Trevor Kincaid, Cedric Lindsay, Ron Westley, Clyde Sayce, Dennis Tufts, and Lee Weigardt. Funding for the current study was provided by the Andrew Mellon Foundation, Washington Department of Fish and Wildlife (both directly and via a grant to the Olympic Natural Resources Center (ONRC) from the oyster reserve research account) and USDAARS. Lee McCoy was instrumental in designing and setting up the field survey, processing and analyzing data, and producing maps in GIS. Miranda Wecker and Keven Bennett at ONRC completed extensive work, particularly on the bathymetry layer, but also compiling existing Willapa GIS layers. We also thank Roy Hildenbrand, Katelyn Cassidy, and Cara Fritz for assistance in collecting data. Last, we thank Dick Olsen, Brian Pickering, Kevin Soule, and Travis Haring for data collection and contributions as oyster reserve managers, and members of the Willapa Bay Oyster Reserve Advisory Committee for their guidance.

LITERATURE CITED

Baker, P. 1995. Review of ecology and fishery of the Olympia oyster, ] Ostrea lurida, with annotated bibliography. J. Shellfish Res. 14: 501-518.

Baldwin, J. R. & J. R. Lovvorn. 1994. Habitats and tidal accessibility of i the marine foods of dabbling ducks and Brant in Boundary Bay, British Columbia. Mar. Biol. 120:627 638.

Banas, N. S., B. M. Hickey, J. A. Newton & J. L. Ruesink. 2007. Tidal exchange, bivalve grazing, and patterns of primary production in Willapa Bay, Washington, USA. Mar. Ecol. Prog. Ser. 341:123-139.

Beck, M. B., R. D. Brumbaugh, L. Airoldi, A. Carranza, L. D. Coen, C. Crawford, O. Defeo, G. J. Edgar, B. Hancock, M. Kay, M. W.

Luckenbach, C. L. Toropova & G. Zhang. 2009. Shellfish reefs at risk: a global analysis of problems and solutions. Arlington, VA: The Nature Conservancy. 52 pp.

Berkenbusch, K., A. A. Rowden & T. E. Myers. 2007. Interactions between seagrasses and burrowing ghost shrimps and their influence on infaunal assemblages. J. Exp. Mar. Biol. Ecol. 341:70-84.

Bostrom, C., E. L. Jackson & C. A. Simenstad. 2006. Seagrass landscapes and their effects on associated fauna: a review. Estuar. Coast. Shelf Sci. 68:383403.

Breitberg, D. L. 1999. Are three dimensional structure and healthy oyster populations the keys to an ecologically interesting and important fish community? In: M. W. Luckenbach & J. Wesson, editors. Oyster reef habitat restoration: a synopsis of approaches. Williamsburg, VA: Virginia Institute of Marine Sciences Press. pp. 239-250.

Bruno, J. F. & M. D. Bertness. 2001. Habitat modification and facilitation in benthic marine communities. In: M. D. Bertness, S. D. Gaines & M. E. Hay, editors. Marine community ecology. Sunderland, MA: Sinauer Associates. pp. 201-219.

Buhle, E. R. & J. L. Ruesink. 2009. Impacts of invasive oyster drills on Olympia oyster (Ostrea lurida Carpenter) recovery in Willapa Bay, Washington, USA. J. Shellfish Res. 28:87-96.

Carpenter, S., B. Walker, J. M. Anderies & N. Abel. 2001. From metaphor to measurement: resilience of what to what? Ecosystems (NY) 4:765-781.

Chapman, W. M. & G. D. Esveldt. 1943. The spawning and setting of the Pacific oyster (Ostrea gigas Thunberg) in the state of Washington in 1942. Biological report. Seattle, WA: Washington Department of Fisheries. 40 pp.

Chew, K. K. 1990. Global bivalve shellfish introductions. Worm Aquacult. 21:9-22.

Coen, L. D., R. D. Brumbaugh, D. Bushek, R. Grizzle, M. W.

Luckenbach, M. H. Posey, S. P. Powers & S. G. Tolley. 2007. Ecosystem services related to oyster restoration. Mar. Ecol. Prog. Ser. 341:303-307.

Coen, L. & R. E. Grizzle. 2007. The importance of habitat created by molluscan shellfish to managed species along the Atlantic coast of the United States. Habitat management series. Washington, DC: Atlantic States Marine Fisheries Commission. 108 pp.

Collins, J. W. 1892. Report on the fisheries of the Pacific coast of the United States. Report of the Commissioner for 1888. Washington, DC: United States Commission of Fish and Fisheries. 209 pp.

Connolly, L. M. & M. A. Colwell. 2005. Comparative use of longline oysterbeds and adjacent tidal flats by waterbirds. Bird Conserv. Int. 15:237-255.

Cook, A. E., J. A. Shaffer, B. R. Dumbauld & B. E. Kauffman. 2000. A plan for rebuilding stocks of Olympia oysters (Ostreola conchaphila, Carpenter 1857) in Washington state. J. Shellfish Res. 19:409-412.

Couch, D. & T. J. Hassler. 1989. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest), Olympia oyster. Biological report. Vicksburg, MS: U.S. Fish and Wildlife Service, U.S. Army Corps of Engineers. 8 pp.

Crain, C. M. & M. D. Bertness. 2006. Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211-218.

Dauble, A. 2010. Young of the year rockfish (Sebastes spp.) settlement dynamics in Oregon estuaries. MS thesis, Oregon State University. 91 pp.

Dumbauld, B. R., D. A. Armstrong & J. R. Skalski. 1997. Efficacy of the pesticide carbaryl for thalassinid shrimp control in Washington state oyster (Crassostrea gigas, Thunberg, 1793) aquaculture. J. Shellfish Res. 16:503-518.

Dumbauld, B. R., S. Booth, D. Cheney, A. Suhrbier & H. Beltran. 2006. An integrated pest management program for burrowing shrimp control in oyster aquaculture. Aquaculture 261:976-992.

Dumbauld, B. R., K. M. Brooks & M. H. Posey. 2001. Response of an estuarine benthic community to application of the pesticide carbaryl and cultivation of Pacific oysters (Crassostrea gigas) in Willapa Bay, Washington. Mar. Pollut. Bull. 42:826-844.

Dumbauld, B. R. & B. E. Kauffman. 1999. Mitigation for estimated juvenile Dungeness crab loss due to dredging in Willapa Bay, Washington: long-term establishment of oyster shell reefs. Report to the Seattle district, U.S. Army Corps of Engineers. Ocean Park, WA.: Washington Department of Fish and Wildlife. 21 pp.

Dumbauld, B. R., J. L. Ruesink & S. S. Rumrill. 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in west coast (USA) estuaries. Aquaculture 290:196-223.

Dumbauld, B. R. & S. Wyllie-Echeverria. 2003. The influence of burrowing thalassinid shrimps on the distribution of intertidal seagrasses in Willapa Bay, Washington, USA. Aquat. Bot. 77:2742.

Ferraro, S. P. & F. A. Cole. 2007. Benthic macrofauna habitat associations in Willapa Bay, Washington, USA. Estuar. Coast. ShelfSci. 71:491-507.

Ferreira, J. G., A. Sequeira, A. J. S. Hawkins, A. Newton, T. D. Nickell, R. Pastres, J. Forte, A. Bodoy & S. B. Bricker. 2009.

Analysis of coastal and offshore aquaculture: application of the FARM model to multiple systems and shellfish species. Aquaculture 289:32-41.

Fincham, M. W. 2010. Up from the bottom: oysters for the 21st century. Chesapeake Quarterly 9:2-5.

Foley, M. M., B. S. Halpern, F. Micheli, M. H. Armsby, M. R. Caldwell, C. M. Crain, E. Prahler, N. Rohr, D. Sivas, M. W. Beck, M. H. Carr, L. B. Crowder, J. E. Duffy, S. D. Hacker, K. L. McLeod, S. R. Palumbi, C. H. Peterson, H. M. Regan, M. H. Ruckelshaus, P. A. Sandifer & R. S. Steneck. 2010. Guiding ecological principles for marine spatial planning. Mar. Policy 34:955-966.

Folke, C., S. Carpenter, B. Walker, M. Scheffer, T. Elmqvist, L. Gunderson & C. S. Holling. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst. 35:557-581.

Fraschetti, S., P. D'Ambrosio, F. Micheli, F. Pizzolante, S. Bussotti & A. Terlizzi. 2009. Design of marine protected areas in a human-dominated seascape. Mar. Ecol. Prog. Ser. 375:13-24.

Grabowski, J. H., R. A. Hughes, D. L. Kimbro & M. A. Dolan. 2005. How habitat setting influences restored oyster reef conmmnities. Ecology 86:1926-1935.

Grabowski, J. & C. H. Peterson. 2007. Restoring oyster reefs to recover ecosystem services. In: K. Cuddington, J. E. Byers, W. Wilson & A. Hastings, editors. Ecosystem engineers: plants to protists. New York: Academic Press. pp. 281-298.

Granek, E. F., D. R. Brumbaugh, S. A. Heppell, S. S. Heppell & D. Secord. 2005. A blueprint for the oceans: implications of two national commission reports for conservation practitioners. Conserv. Biol. 19:1008-1018.

Hare, S. R. & N. J. Mantua. 2000. Empirical evidence for North Pacific regime shifts in 1977 and 1989. Prog. Oceanogr. 47:103-145.

Haven, D. S., W. J. Hargis, Jr. & P. C. Kendall. 1978. The oyster industry of Virginia: its status, problems and promise: a comprehensive study of the oyster industry of Virginia. VIMS special papers in marine science. Gloucester, VA: Virginia Institute of Marine Science. 1024 pp.

Hedgepeth, J. & S. Obrebski. 1981. Willapa Bay: a historical perspective and a rationale for research. FWS/OBS-81/03. Washington, DC: U.S. Fish and Wildlife Service, Office of Biological Services. 52 pp.

Holsman, K. K., P. S. McDonald & D. A. Armstrong. 2006. Intertidal migration and habitat use by subadult Dungeness crab Cancer magister in a NE Pacific estuary. Mar. Ecol. Prog. Ser. 308:183-195.

Hosack, G. R., B. R. Dumbauld, J. L. Ruesink & D. A. Armstrong. 2006. Habitat associations of estuarine species: comparisons of intertidal mudflat, seagrass (Zostera marina), and oyster (Crassostrea gigas) habitats. Estuaries Coasts 29:1150-1160.

Hughes, A. R., S. L. Williams, C. M. Duarte, K. L. Heck & M. Waycott. 2009. Associations of concern: declining seagrasses and threatened dependent species. Front. Ecol. Environ 7:242-246.

Jackson, J. B. C. 2008. Ecological extinction and evolution in the brave new ocean. Proc. Natl. Acad. Sci. USA 105:11458 11465.

Jones, B. C. 1972. Effect of intertidal exposure on survival and embryonic development of Pacific herring spawn. J. Fish. Res. Board Can. 29:1119-1124.

Jones, C. G., J. H. Lawton & M. Shackak. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946-1957.

Keiner, C. 2009. The oyster question: scientists, watermen, and the Maryland Chesapeake Bay since 1880. Athens, GA, University of Georgia Press. 331 pp.

Kennedy, V. S. & L. L. Breisch. 1983. 16 Decades of political management of the oyster fishery in Maryland's Chesapeake Bay. J. Environ. Manage. 16:153-171.

Kirby, M. X. 2004. Fishing down the coast: historical expansion and collapse of oyster fisheries along continental margins. Proc. Natl. Acad. Sci. USA 101:13096-13099.

Laffargue, P., M. L. Begout & F. Eagardere. 2006. Testing the potential effects of shellfish farming on swimming activity and spatial distribution of sole (Solea solea) in a mesocosm. ICES J. Mar. Sci. 63:1014-1028.

Lenihan, H. S. & F. Micheli. 2001. Soft-sediment communities. In: M. D. Bertness, S. D. Gaines & M. E. Hay, editors. Marine community ecology. Sunderland, MA: Sinauer Associates. pp. 253-287.

Lenihan, H. S. & C. H. Peterson. 1998. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecol. Appl. 8:128-140.

Leslie, H. M. & K. L. McLeod. 2007. Confronting the challenges of implementing marine ecosystem-based management. Front. Ecol. Environ 5:540-548.

Lester, S. E., B. S. Halpern, K. Grorud-Colvert, J. Lubchenco, B. I. Ruttenberg, S. D. Gaines, S. Airame & R. R. Warner. 2009. Biological effects within no-take marine reserves: a global synthesis. Mar. Ecol. Prog. Ser. 384:33-46.

Lindsay, C. E. & D. Simons. 1997. The fisheries for Olympia oysters, Ostreola conchaphila; Pacific oysters, Crassostrea gigas; and Pacific razor clams, Siliqua patula; in the state of Washington. In: C. L. J. MacKenzie, V. G. J. Burrell, A. Rosenfield & W. L. Hobart, editors. The history, present condition, and future of the molluscan fisheries of North and Central America and Europe. Vol. 2. Pacific coast and supplemental topics. Seattle, WA: NOAA, U.S. Department of Commerce. pp. 89-113.

Lindsay, C., R. E. Westley & C. S. Sayce. 1959. Prediction of oyster setting in the state of Washington. Proc. Natl. Shellfish. Assoc. 49:59-70.

Lovvorn, J. R. & J. R. Baldwin. 1996. Intertidal and farmland habitats of ducks in the Puget Sound region: a landscape perspective. Biol. Conserv. 77:97-114.

Luckenbach, M. W. 1984. Biogenic structure and foraging by five species of shorebirds (Charadrii). Estuar. Coast. Shelf Sci. 19:691-696.

MacKenzie, C. L. J. 1997. The molluscan fisheries of Chesapeake Bay. In: C. L. J. MacKenzie, V. G. J. Burrell, A. Rosenfield & W. L. Hobart, editors. The history, present condition, and future of the molluscan fisheries of North and Central America and Europe. Vol. 1. Atlantic and Gulf coasts. Seattle, WA: NOAA, U.S. Department of Commerce. pp. 141-169.

Mann, R., E. M. Burreson & P. K. Baker. 1991. The decline of the Virginia oyster fishery in Chesapeake Bay: considerations for introduction of a non-endemic species, Crassostrea gigas (Thunberg, 1793). J. Shellfish Res. 10:379-388.

Matthews, K. 1990. A comparative study of habitat use by young of the year rockfish on four habitat types in Puget Sound. Fish Bull. 88:223-240.

McKindsey, C. W., H. Thetmeyer, T. Landry & W. Silvert. 2006. Review of recent carrying capacity models for bivalve culture and recommendations for research and management. Aquaculture 261:451-462.

Moore, J. E., M. A. CoIwell, R. L. Mathis & J. M. Black. 2004. Staging of Pacific flyway Brant in relation to eelgrass abundance and site isolation, with special consideration of Humboldt Bay, California. Biol. Conserv. 115:475-486.

Newell, R. I. E. 2004. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J. Shellfish Res. 23:51-62.

NRC. 2004. Nonnative oysters in the Chesapeake Bay. Washington, DC: National Academies Press. 325 pp.

NRC. 2010. Ecosystem concepts for sustainable bivalve mariculture. Washington, DC: National Academies Press. 179 pp.

Orth, R. J., T. J. B. Carruthers, W. C. Dennison, C. M. Duarte, J. W. Fourqurean, K. L. Heck, A. R. Hughes, G. A. Kendrick, W. J. Kenworthy, S. Olyarnik, F. T. Short, M. Waycott & S. L. Williams. 2006. A global crisis for seagrass ecosystems. Bioscience 56:987-996.

Orth, R. J., S. R. Marion, K. A. Moore & D. J. Wilcox. 2010. Eelgrass (Zostera marina L.) in the Chesapeake Bay region of mid-Atlantic coast of the USA: challenges in conservation and restoration. Estuaries Coasts 33:139-150.

Peterson, C. H., H. C. Summerson, E. Thomson, H. S. Lenihan, J. Grabowski, L. Manning, F. Micheli & G. Johnson. 2000. Synthesis of linkages between benthic and fish communities as a key to protecting essential fish habitat. Bull. Mar. Sci. 66:759-774.

Piazza, B. P., P. D. Banks & M. K. La Peyre. 2005. The potential for created oyster shell reefs as a sustainable shoreline protection strategy in Louisiana. Restor. Ecol. 13:499-506.

Polson, M. P. & D. C. Zacherh 2009. Geographic distribution and intertidal population status for the Olympia oyster, Ostrea lurida Carpenter 1864, from Alaska to Baja. J. Shellfish Res. 28:69-77.

Posey, M. H., T. D. Alphin, C. M. Powell & E. Townsend. 1999. Oyster reefs as habitat for fish and decapods. In: M. W. Luckenbach & J. Wesson, editors. Oyster reef habitat restoration: a synopsis of approaches. Williamsburg, VA: Virginia Institute of Marine Sciences Press. pp. 229-237.

Posey, M. H., B. R. Dumbauld & D. A. Armstrong. 1991. Effects of a burrowing mud shrimp, Upogebia pugettensis (Dana), on abundances of macro-infauna. J. Exp. Mar. Biol. Ecol. 148:283 294.

Posey, M., C. Powell, L. Cahoon & D. Lindquist. 1995. Top down vs. bottom up control of benthic community composition on an intertidal tideflat. J. Exp. Mar. Biol. Ecol. 185:19-31.

Powers, S. P., C. H. Peterson, J. H. Grabowski & H. S. Lenihan. 2009. Success of constructed oyster reefs in no-harvest sanctuaries: implications for restoration. Mar. Ecol. Prog. Ser. 389:159-170.

Rothschild, B. J., J. S. Ault, P. Goulletquer & M. Herah 1994. Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Mat'. Ecol. Prog. Ser. 111:29-39.

Ruesink, J. L., J. S. Hong, L. Wisehart, S. D. Hacker, B. R. Dumbauld, M. Hessing-Lewis & A. C. Trimble. 2010. Congener comparison of native (Zostera marina) and introduced (Z. japonica) eelgrass at multiple scales within a Pacific Northwest estuary. Biol. Invasions 12:1773-1789.

Ruesink, J. L., H. S. Lenihan, A. C. Trimble, K. W. Heiman, F. Micheli, J. E. Byers & M. C. Kay. 2005. Introduction of non-native oysters: ecosystem effects and restoration implications. Annu. Rev. Ecol. Syst. 36:643-689.

Sayce, C. S. 1976. The oyster industry of Willapa Bay. In: R.D. Andrews, editor. Proceedings of a symposium on terrestrial and ecological studies of the Northwest. Cheney, WA: Eastern Washington State College Press. pp. 347-356.

Semmens, B. X. 2008. Acoustically derived fine-scale behaviors of juvenile Chinook salmon associated with intertidal benthic habitats in an estuary. Can. J. Fish. Aquat. Sci. 65:2053-2062.

Siebert, T. & G. M. Branch. 2005. Interactions between Zostera capensis, Callianassa kraussi and Upogebia africana: deductions from field surveys in Langebaan Lagoon, South Africa. Afr. J. Mar. Sci. 27:345-356.

Siebert, T. & G. M. Branch. 2006. Ecosystem engineers: interactions between eelgrass Zostera capensis and the sandprawn Callianassa kraussi and their indirect effects on the mudprawn Upogebia africana. J. Exp. Mar. Biol. Ecol. 338:253-270.

Simenstad, C. A. & K. L. Fresh. 1995. Influence of intertidal aquaculture on benthic communities in Pacific Northwest estuaries: scales of disturbance. Estuaries 18:43-70.

Simenstad, C. A., K. L. Fresh & E. A. Salo. 1982. The role of Puget Sound and Washington coastal estuaries in the life history of Pacific salmon: an unappreciated function. In: V. S. Kennedy, editor. Estuarine comparisons. New York: Academic Press. pp. 343-364.

Steele, E. N. 1964. The immigrant oyster (Ostrea gigas) now known as the Pacific oyster. Olympia, WA: Warren's Quick Print. 179 pp.

Tallis, H. M., J. L. Ruesink, B. R. Dumbauld, S. D. Hacker & L. M. Wisehart. 2009. Oysters and aquaculture practices affect eelgrass density and productivity in a Pacific Northwest estuary. J. Shellfish Res. 28:251-261.

Townsend, C. H. 1893. Report of observations respecting the oyster resources and oyster fishery of the Pacific coast of the United States. Report of Commissioner of Fish and Fisheries. U.S. Fisheries Commission. 641 pp.

Townsend, C. H. 1896. The transplanting of eastern oysters to Willapa Bay, Washington with notes on the native oyster industry. Report of Commissioner of Fish and Fisheries. U.S. Fisheries Commission. 584 pp.

Trimble, A. C., J. L. Ruesink & B. R. Dumbauld. 2009. Factors preventing the recovery of a historically overexploited shell fish species, Ostrea lurida Carpenter 1864. J. Shellfish Res. 28:97-106.

Tufts, D. F. 1987. The Willapa Bay oyster reserves: a history and inventory with recommendations for the future. Report to the Washington state legislature. Olympia, WA: Washington Department of Fisheries. 22 pp.

USCOP. 2004. An ocean blueprint for the 21st century. Washington, DC: U.S. Commission on Ocean Policy. 36 pp.

Waycott, M., C. M. Duarte, T. J. B. Carruthers, R. J. Orth, W. C. Dennison, S. Olyarnik, A. Calladine, J. W. Fourqurean, K. L. Heck, Jr., A. R. Hughes, G. A. Kendrick, J. W. Kenworthy, F. T. Short & S. L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Acad. Nat. Sci. Phila. 106: 12377-12381.

Weschler, J. F. 2004. Assessing the relationship between the ichthyofauna and oyster mariculture in a shallow embayment, Drakes Estero, Point Reyes National Seashore. MS thesis, University of California at Davis. 42 pp.

Westley, R. E., A. J. Scholz & R. T. Burge. 1985. The Puget Sound oyster reserves: a history and inventory with recommendations for the future. Report to the Washington state legislature. Olympia, WA: Washington State Department of Fisheries. 25 pp.

White, J., J. L. Ruesink & A. C. Trimble. 2009. The nearly forgotten oyster: Ostrea lurida Carpenter 1864 (Olympia oyster) history and management in Washington state. J. Shellfish Res. 28:43-49.

Wilson, U. W. & J. B. Atkinson. 1995. Black Brant winter and spring-staging use at two Washington coastal areas in relation to eelgrass abundance. Condor 97:91-98.

Wisehart, L. M., J. L. Ruesink, S. D. Hacker & B. R. Dumbauld. 2007. Importance of eelgrass early life history stages in response to oyster aquaculture disturbance. Mar. Ecol. Prog. Ser. 344:71-80.

Woelke, C. E. 1969. A history and economic evaluation of Washington state oyster reserves. Research division report. Olympia, WA: Washington State Department of Fisheries. 17 pp.

Yasue, M. 2006. Environmental factors and spatial scale influence shorebirds' responses to human disturbance. Biol. Conserv. 128:47-54.

Zimmerman, R., T. Minello, T. Baumer & M. Castiglione. 1989. Oyster reef as habitat for estuarine macrofauna. NOAA technical memorandum NMFS-SEFC-249. Silver Springs, MD: U.S. Department of Commerce, NOAA. 16 pp.

BRETT R. DUMBAULD, (1), * BRUCE E. KAUFFMAN, (2) ALAN C. TRIMBLE (3) AND JENNIFER L. RUESINK (3)

(1) U.S. Department of Agriculture, Agriculture Research Service, Hatfield Marine Science Center, 2030 S.E. Marine Science Drive, Newport, OR 97365; (2) Washington Department of Fish and Wildlife, Willapa Bay Field Station, PO Box 190, Ocean Park, WA 98640; (3) Department of Biology, Box 351800, University of Washington, Seattle, WA 98195

* Corresponding author. E-mail: brett.dumbauld@ars.usda.gov

DOI: 10.2983/035.030.0111
TABLE 1.
Area, general characteristics, and current use of Willapa Bay oyster
reserves.

                     Total Area   Intertidal     Estuary
Reserve                 (ha)      Area (ha)    Tideflat (%)

Willapa River           196           56           0.3
Bay Center              111           33           0.1
Nemah                 1,036          919           4.0
Long Island           2,418        1,252           5.5
Long Island Slough      234          148           0.7
Total                 3,995        2,408          10.6

Reserve              Estuary (%)   Current Use

Willapa River            0.6       Mostly river channel, no
                                     recent sales, but some
                                     historical dredge harvest
                                     and native oysters likely
                                     present
Bay Center               0.3       Mostly river channel, no
                                     sales records
Nemah                    2.9       Prime area for sales of
                                     transplant oysters
Long Island              6.8       Sales of transplant oysters
                                     especially along Naselle
                                     River channel and north
                                     end of Long Island; native
                                     oysters still present in low
                                     areas
Long Island Slough       0.7       Principle cultching area,
                                     some transplant oyster
                                     sales
Total                   11.4

TABLE 2.
Size and coverage characteristics of historical 1889 native oyster
grounds and "cultivated" beds, and current Willapa Bay state oyster
reserves and sale areas based on overlays with 2005 to 2007 habitat
survey.
                                                    Historical

                                    Native Oyster   Cultivated
Characteristics                         Beds           Beds

Area (ha)                           3,141           3,259
Intertidal area (ha)                2,201           2,693
Subtidal area (ha)                    940             566
Proportion of tideflat                  9.7            11.9
Proportion of estuary                   8.8             9.1
Average tide height (mean lower        +0.233          +1.310
  low water)
Eelgrass Zostera marina area (ha)
Eelgrass Zostera japonica area
  (ha)
Burrowing shrimp area (ha)

                                                Current

                                    Reserves    Reserves    Commercial
Characteristics                      Total     Sales Area    Culture

Area (ha)                           3,995      453          48,879
Intertidal area (ha)                2,408      439          43,338
Subtidal area (ha)                  1,587       14           2,921
Proportion of tideflat                 10.6      1.9            19.1
Proportion of estuary                  11.2      1.3            13.6
Average tide height (mean lower        nd       +0.401           $
  low water)
Eelgrass Zostera marina area (ha)   1,393      202              nd
Eelgrass Zostera japonica area        403       68              nd
  (ha)
Burrowing shrimp area (ha)            294       19              nd

nd, no data.
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Article Details
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Author:Dumbauld, Brett R.; Kauffman, Bruce E.; Trimble, Alan C.; Ruesink, Jennifer L.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1U9WA
Date:Apr 1, 2011
Words:11766
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