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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 Author(s): Brett R. Dumbauld, Bruce E. Kauffman, Alan C. Trimble and Jennifer L. Ruesink Source: Journal of Shellfish Research, 30(1):71-83. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.030.0111 URL: http://www.bioone.org/doi/full/10.2983/035.030.0111

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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

BRETT R. DUMBAULD,1,* BRUCE E. KAUFFMAN,2 ALAN C. TRIMBLE3 AND JENNIFER L. RUESINK3 1U.S. Department of Agriculture, Agriculture Research Service, Hatﬁeld Marine Science Center, 2030 S.E. Marine Science Drive, Newport, OR 97365; 2Washington Department of Fish and Wildlife, Willapa Bay Field Station, PO Box 190, Ocean Park, WA 98640; 3Department of Biology, Box 351800, University of Washington, Seattle, WA 98195

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 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 oyster reserves currently represent the Washington state reserve system, but these totals were about 4,400 ha (10,873 acres) of tidelands that were originally reduced to about 3,995 ha and 405 ha, respectively, as tidelands set aside by the first territorial legislature in 1890 to preserve were sold to private shellfish growers. Although native oysters stocks of the native oyster (Ostrea lurida, Carpenter 1864) for are currently rebounding on portions of the Puget Sound re- oyster farmers under the direction of the Washington State serves in Oakland Bay, and there has been renewed interest in Department of Fisheries (now the Washington Department of recreational, tribal, and commercial clam fisheries therein, they Fish and Wildlife (WDFW)) (Woelke 1969, Westley et al. 1985). were generally reduced to small parcels of some of the least Since that time, the state legislature has periodically reviewed productive lands, and use has been limited since 1927 (Westley the laws and modified them to fit the current nature of the et al. 1985). We focus, instead, on the Willapa Bay oyster re- fishery. The fishery for native oysters paralleled numerous serves, where a sustainable and important fishery for Pacific others around the world, starting out as a capture fishery that oysters has been maintained. Furthermore, because these re- ultimately overexploited the oyster stock, leaving only remnant serves represent a relatively large portion of the habitat in this populations in most areas where they were abundant along the estuary, the ecosystem role of both native and introduced west coast of the United States (Baker 1995, Kirby 2004, Beck bivalves can be evaluated, and management for both conserva- et al. 2009, Polson & Zacherl 2009, White et al. 2009). However, tion and sustainable harvest considered. it has now become a large-scale commercial farming operation The history of the Willapa Bay oyster reserves is intimately and a much smaller scale recreational fishery for the Pacific associated with the history of the oyster industry and tideland oyster (Crassostrea gigas, Thunberg 1794), which was intro- ownership in Washington state (Woelke 1969). At the time of duced to Washington state waters in 1920 (Steele 1964, Chew the 1849 gold rush in California, the native or ‘‘Olympia’’ 1990, Lindsay & Simons 1997, Ruesink et al. 2005, White et al. oyster, O. lurida, was harvested in a true open-access fishery in 2009). Recent legislative changes in 2001 and 2007 involved Willapa Bay, which involved hand tonging and moving small creating two advisory committees and setting aside funds oysters from natural beds to other intertidal areas, where they generated from shellfish sales on the reserves to cover expenses, were held until shipment, usually by sailing schooners to mar- assist with research, and establish a shellfish onsite sewage grant kets in San Francisco (Baker 1995, White et al. 2009). From the outset, harvest was extensive, and the lack of knowledge about *Corresponding author. E-mail: [email protected] the life cycle of the native oyster by these early fishers, combined DOI: 10.2983/035.030.0111 with harvest techniques used, contributed to depletion of the

71 72 DUMBAULD ET AL. native oyster stocks and lack of renewal, because oysters were proportion of their volume in empty shells to provide substrate moved to higher intertidal areas and shell was not returned to for natural oyster sets and, therefore, future harvest. The third, the low intertidal and subtidal areas where these oysters were and last, activity includes updating, surveying, and policing abundant and where they would survive after setting. The reserve boundaries. Finally, WDFW also supervises separate Washington State Territorial Legislature passed the first oyster oyster seed-catching operations on the reserves and, since 1989, laws in 1877, which made it possible to own up to 20 acres of has charged a cultching fee for placing shell on reserve grounds. tidelands not covered by natural oysters for development of We provide an update on the current status of the Willapa oyster lands. The new act prohibited private ownership of Bay oyster reserves, including results of an intertidal habitat natural oyster beds but gave rights to discoverers of these beds survey conducted in 2006 and 2007. The current fishery for to use 4.47 ha for 5 y. A winter freeze in 1888 reportedly killed Pacific oysters on the reserves and its management, including 60% of the oysters above low tide (Townsend 1892). In 1890, shell return to the reserves and an annual assessment of oyster the first state legislature revisited the issue and set the natural settlement, are described. Current status is contrasted with oyster beds aside as reserves to be retained in the public domain historical condition by comparing an 1892 map of native oyster and to provide juvenile oysters, called ‘‘seed,’’ for the ‘‘oyster harvest areas with results of the current habitat survey. Last, we farmer’’ and an exploitable stock for the ‘‘fisherman.’’ They outline a plan for research and continued sustainable harvest further defined the principles of private tideland ownership and and management of Pacific oysters, conservation of existing development of tidelands for ‘‘oystering.’’ The Bush Act of 1895 habitat, and the potential for restoring native oysters to the expanded tideland ownership and provided for survey, platting, reserves. filing, and purchasing those lands not included in the reserves. Nonetheless, adequate guidelines for preservation were MATERIALS AND METHODS weak, and by 1900, the reserves in Willapa Bay had already witnessed serious depletion of native oyster stocks, and the Study Site and Intertidal Survey industry was approaching extinction. As a result, in part, of this decline, the U.S. Commissioner of Fisheries visited the bay in The Willapa Bay oyster reserves consist of approximately 1893 and was impressed with the potential for importing and 4,033 ha of intertidal and subtidal land divided into five sep- growing the Eastern oyster Crassostrea virginica (Gmelin, arate reserves located predominantly in the southern portion of 1791). With approval of the state fisheries commissioner, 80 Willapa Bay, the second largest estuary along the west coast of the barrels of Eastern oysters were planted in the Palix River area of United States (46°40# N, 124°0# W; Fig. 1). Because the reserves Willapa Bay (Townsend 1896). These oysters survived, grew were originally set aside to preserve areas where the native oyster well, and contributed to a resurgence of the oyster industry from thrived, the majority of land consists of either subtidal channel or 1895 to 1917. The industry relied on annual shipments of oyster low intertidal ground. We assessed the current status of intertidal seed delivered by trainload from the east coast, because these habitats (aquaculture, eelgrass, burrowing shrimp, and bare oysters rarely spawned successfully in Willapa Bay. In 1919, tideflat) on the reserves as part of a larger survey to map these Eastern oysters in Willapa Bay began to die. Although attrib- habitats in the entire estuary from 2006 to 2007. uted to red tide, no documented account of the cause for this Sampling was conducted on a grid with stations located at catastrophic event exists. The industry did not recover until 200-m intervals across the intertidal. Each accessible location introduction of the Pacific oyster, C. gigas, from Japan in 1928 was visited at low tide by hovercraft. Locations within com- (Sayce 1976). Pacific oysters have continued to be the mainstay mercial Pacific oyster beds or harvest areas were generally not of the industry. Although the Pacific oyster reproduced suc- visited because they were impossible to traverse by hovercraft, cessfully in Willapa Bay, growers found it easier to import seed and because oysters were viewed as a temporally variable from Japan, resulting in little activity on the oyster reserves habitat, only the boundaries of these areas were assessed (as through the 1930s. By the 1940s, a considerable stock of Pacific noted later). At each station, data were recorded into a Trimble oysters had naturally set and accumulated on the reserves. GeoXT mapping-grade GPS system (Trimble, Sunnyvale, CA). When oysters became impossible to obtain from Japan during A photograph of a 0.25-m2 quadrat was taken at most locations World War II, there was renewed interest in the reserves and the to verify visual assessments. At each station, we recorded the laws were changed in 1947 to protect Pacific oyster stocks on the presence and density of two eelgrass species (native Zostera reserves. In 1949, the goals of the reserve management system marina and introduced Zostera japonica), macroalgae, live were broadened to include providing seed and ‘‘stocking public oysters, and shell in a 10-m2 area; the number of burrows beaches.’’ From 1949 to 1967, WDFW used two people to within a 0.25-m2 quadrat; and burrow occupants (clams, poly- manage the Willapa Bay reserves and has used one person since chaetes, and thalassinid burrowing shrimp); as well as basic that time (Woelke 1969, Tufts 1987). Reserve management then sediment characteristics. Density of each eelgrass species, and now involves three basic activities. The first activity is macroalgae (classified loosely into brown, green, or red), oyster, supervising an annual sale of oysters to the highest bidder. and shell was classified into four categories: absent; present, Buyers are typically shellfish growers, because each bidder is minor (<25% cover); present, medium (25–75% cover); and required to sign a contract to harvest all oysters on a tract. present, major (>75% cover). A pilot survey suggested these Furthermore, most of the oysters must be moved or trans- categories related directly to quantified assessments using planted to better growing areas where they can obtain enough smaller quadrats, but the larger 10-m2 scale was more useful food to fatten before they can be sold commercially (closer to to classify vegetation signatures in aerial photographs. Burrow the mouth of the estuary (Banas et al. 2007)). The second ac- occupants were determined by extraction with a shrimp pump tivity includes a shell return program in which the buyer is or by expert opinion, taking into consideration sediment type, required to replace the amount of oysters harvested with a feces, burrow lining, burrow diameter, and burrow density. At AN EVALUATION OF THE WILLAPA BAY OYSTER RESERVES 73

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 Pa- ciﬁc 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

Figure 1. Location of the 5 Willapa Bay oyster reserves (intertidal areas An annual sale of oysters from the reserves involves a call for are shaded light gray) and current sales areas that are actively being bids on individual tracts within the reserves, acceptance and harvested (dark gray; see Table 1 for descriptions of area and current use). opening of bids from interested parties, and awards to the Also shown are the oyster condition or fattening line, the area north of which highest bidder. Buyers then sign a contract to harvest all oysters has long been known to reflect good fattening ground for oyster harvest. The present on the tract and replenish shell. Buyers pay by the location of sampling stations where oyster recruitment has been monitored bushel (1 bushel ¼ 0.035 m3) of oysters harvested. The sale is are also shown: MC, Mill Channel; P, Peterson; ST3, Station III. monitored by a reserve manager, and data on sales are recorded. A shell return program was instigated in 1958 to require growers each station, we recorded elevation relative to height above who harvested oysters to return a percentage of the volume ellipsoid using an L1 Trimble ProXR (Trimble, Sunnyvale, CA) harvested (initially one half of the purchase volume) as empty mounted at a fixed position on the hovercraft to create shell back to the reserves. Because of staff reductions, WDFW a complete digital elevation model by combining our low- was unable to handle shell return from 1970 to 1974, but in 1975 resolution elevation model with a LiDAR data set previously began requiring purchasers to return shell to the beds. The collected for the upper intertidal. amount of shell required to be returned was reduced to 40% of Data were downloaded, postprocessed, and exported to the volume harvested in 1977 and has remained at that level using GPS Pathfinder Office (version 4.2; Trimble, Inc., Sun- since. Shell is generally returned to the same area where harvest nyvale, CA). In ArcMap (version 9.3; ESRI, Redlands, CA), the occurred. density classification for each factor was assigned an integer Some local settlement of Pacific oyster larvae (spatfall) has value (0–4) and interpolated using inverse distance weighted to occurred nearly every year since these oysters were introduced produce a continuous raster image. These raster images were to Willapa Bay in the 1920s. In 1942, WDFW and the Univer- then reclassified into integer values (0–0.5 ¼ 0, 0.5–1.5 ¼ 1, and sity of Washington began a sampling program to determine the so on) and converted to polygons. Calculations of area include magnitude and timing of these recruitment events. Each week polygons designated as level 3 (present, medium) and level 4 2 sets of 20 Pacific oyster shells were strung together on a wire (present, major) only. Elevation data from the ProXR were with the inner face down, and anchored just above the substrate 74 DUMBAULD ET AL. at several locations in the estuary. One set was retrieved a week oyster grounds from which oysters were harvested are now at later (weekly shell strings) and the other set was left until early least 1 m lower in the intertidal on average than areas noted as fall to obtain cumulative spatfall information (seasonal shell cultivated (areas where harvesters moved oysters before ship- string). Data collected (1956 to 1983) were compiled from var- ping; Table 2). Current Pacific oyster culture is generally also at ious sources and reported previously (Trimble et al. 2009). Here this higher tidal elevation. Areas denoted historically as native we reanalyzed the seasonal shell string data for three locations oysters coincide reasonably well with intertidal areas now set (Peterson, Station III, and Mill Channel; Fig. 1) for which data aside as reserves (58% of the areas noted as native harvest areas were most complete. We also include information on relative are now within the reserves; Fig. 2). Yet, these areas of the re- abundance of spat (noncommercial, <3 spat per shell; commer- serves that once harbored native oysters are now covered by cial, 3–25 spat per shell; good, 25–50 spat per shell; and ex- extensive areas of eelgrass (1,309 ha; Fig. 2, Table 2), most of cellent, >50 spat per shell) for 1936 to 1955 (Lindsay et al. (1959) which is native Z. marina (roughly 77% calculated from ground and for 1984 to 2001 (from larval data and discussion with survey data). Thirty-one percent of the slightly higher cultivated Dennis Tufts). Shell string sampling was reinitiated in 2002. We areas that were once used for holding oysters are now privately relate results to natural seed production in the south end of the owned and cultivated for Pacific oysters. These areas are also estuary, and particularly to sales and continued cultching ef- vegetated with eelgrass (92% Z. marina from ground survey forts on the Willapa Bay oyster reserves. WDFW allowed oyster data). A much smaller portion of the historical area where growers to construct racks on the state oyster reserves that sup- native oysters were harvested and cultivated are currently port strings or bags of oyster shell (cultch) on which the oyster occupied by burrowing shrimp (535 ha and 355 ha, respectively, larvae set. Reserve areas that have been used to obtain natural Table 2). Burrowing shrimp mostly reside at higher tidal oyster seed are primarily located along the Naselle River elevations on the Nemah reserve (294 ha; Table 2). channel in the Long Island Slough Reserve (LISOR) or the Long Island Reserve (LIOR). Sales

RESULTS The intertidal ground that constitutes the oyster reserves in Willapa Bay has, in general, proved to be good for Paciﬁc oyster Current Habitat Survey and Historical Map seed production; but, except for small portions, does not produce a market-quality harvestable oyster resulting, in large part, A total of 4,238 grid stations were visited throughout from the majority of the currently used ground being located in Willapa Bay in 2006 and 2007; of these, 783 were located on the southern half of the estuary beyond what is known as the oyster reserves. About 40% of the reserve area (1,587 ha) is fattening or condition line (Fig. 1) (Chapman & Esveldt 1943, subtidal and much of the rest is very low intertidal, so a large Banas et al. 2007). A relatively small portion (453 ha) of in- portion of the reserve lands were not directly assessed in this tertidal ground is currently being used for oyster production habitat survey (Table 1). Although tidal elevations have likely (Fig. 1, Table 1), and this ground averages about +0.4 m mean changed substantially since the late 1800s, an analysis of the lower low water (Table 2). Since the 1930s, the location and historical map overlaid on current elevation suggests that native extent of oyster sales and harvest has depended on the success of

TABLE 1. Area, general characteristics, and current use of Willapa Bay oyster reserves.

Total Area Intertidal Estuary Reserve (ha) Area (ha) Tideﬂat (%) Estuary (%) Current Use Willapa River 196 56 0.3 0.6 Mostly river channel, no recent sales, but some historical dredge harvest and native oysters likely present Bay Center 111 33 0.1 0.3 Mostly river channel, no sales records Nemah 1,036 919 4.0 2.9 Prime area for sales of transplant oysters Long Island 2,418 1,252 5.5 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 234 148 0.7 0.7 Principle cultching area, some transplant oyster sales Total 3,995 2,408 10.6 11.4 AN EVALUATION OF THE WILLAPA BAY OYSTER RESERVES 75

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 Current Native Oyster Reserves Reserves Commercial Characteristics Beds Cultivated Beds Total Sales Area Culture Area (ha) 3,141 3,259 3,995 453 48,879 Intertidal area (ha) 2,201 2,693 2,408 439 43,338 Subtidal area (ha) 940 566 1,587 14 2,921 Proportion of tideﬂat 9.7 11.9 10.6 1.9 19.1 Proportion of estuary 8.8 9.1 11.2 1.3 13.6 Average tide height (mean lower low water) +0.233 +1.310 nd +0.401 +1.755 Eelgrass Zostera marina area (ha) 1,393 202 nd Eelgrass Zostera japonica area (ha) 403 68 nd Burrowing shrimp area (ha) 294 19 nd nd, no data.

Pacific oyster settlement and recruitment in previous years, as brackets a period of low harvest from the reserves that began in well as shell return to the area. Most tracts have been sold on 1969 and ended in 1979 (Fig. 3) and an extended period of low a 3–5-y cycle since the late 1960s, which allows time for values of the Pacific decadal oscillation, a climate index for the recruitment of new oysters and/or planting by WDFW staff. northeast Pacific (Hare & Mantua 2000). Although records are Initially, both intertidal and subtidal tracts were sold and incomplete, recruitment of Pacific oysters in Willapa Bay from harvested by dredge or picked by hand. With the exception of 2005 to 2010 has also been minimal, but it is too soon to know some experimental trials in 2005 and 2006 (46.7 m3 harvested whether this represents another shift in the long-term pattern. from the LIOR), oysters have not been dredged since 1979. The Washington state legislature implemented a 10% charge From 1945 through 2001, 87,934 m3 of oysters were harvested or cultching fee for use of racks placed on the reserves in 1989 generating $2,299,290, which was deposited into the Washing- (10% of the shell placed on the reserves to obtain seed by ton state general fund. From 2002 to 2009, an additional 27,027 growers needed to be returned to the reserves). The oyster seed m3 were sold generating $1,854,758, which was deposited in the obtained from this fee was returned to the state reserves and it newly created Oyster Reserves Land Account. Sales averaged has contributed to increased yields and revenues since the early 1,685 m3/y (47,865 bushels) at an annual return of $64,342, 1990s. WDFW also supplemented the return to reserves by but a clear increase in both the quantity of oysters and the price constructing a state-owned seed rack in the LISOR, which was obtained began during the early 1990s, and the average sales operational from 1990 to 1998. This rack produced an addi- since 1992 have been 2,991 m3 (84,972 bushels) with a return of tional 7,000 seed bags of oysters, most of which were also $167,618, with substantial sales from the Nemah Reserve where planted on the reserves and contributed to increased sales dur- enhancement took place (Fig. 3). No sales of oysters from the ing these years. Introduction of remote setting of Pacific oysters Willapa Oyster Reserves took place in 1984, because growers from hatcheries has reduced the dependence of most growers on who historically bought reserve oysters participated in a trans- natural seed catch. The LISOR was, for many years, the best plant program with one of the major oyster growers in Willapa area for obtaining oyster seed in Willapa Bay. During the past Bay and did not bid. 15 y, setting areas seemed to have shifted and many growers Hard-shell clams (the Manila clam, Ruditapes philippinarum who once exclusively used the reserves for obtaining seed have (Deshayes 1853), and the native littleneck, Leucoma staminea found that tidelands that they own or lease along the west side Conrad 1837) have also been intermittently sold from the of Long Island now get better seed sets. Cultching effort on the Willapa Bay oyster reserves. Sales held in 1979, 1981, 1982, reserves has therefore declined, resulting in part from the and 1984 produced 6,241 kg of clams; recent sales in 2003, 2006, cultching fee, but mostly because oysters did not routinely set 2007, and 2009 produced 45,234 kg. These sales were all located in the LISOR on the east side of the bay. on LIOR, where suitable areas for hard-shell clam settlement and survival are present. DISCUSSION

Oyster Larval Sets and Shell Return Oysters have been an important resource in Washington state since before statehood, and they have defined the recent Seasonal recruitment and survival of Pacific oysters to shell history of the Willapa Bay estuary, as they have much larger strings averaged 8.3 recruits per shell, although the range was U.S. east coast systems like Chesapeake Bay (Sayce 1976, high (0–90 recruits per shell), and commercial sets (>3 recruits Haven et al. 1978, MacKenzie 1997, Keiner 2009, Trimble per shell) occurred in more than half (44 of 73) the years mon- et al. 2009). Problems associated with an open-access fishery for itored (Fig. 4). More consistently high recruitment occurred the native oyster O. lurida, such as overfishing and lack of from the late 1930s through about 1959, after which recruitment knowledge about returning shell to the system, are also similar was low through 1981 and then increased and was generally to those that have befallen wild oyster fisheries elsewhere better through 2005. The period of low recruitment roughly (Ruesink et al. 2005, Beck et al. 2009, White et al. 2009). The 76 DUMBAULD ET AL.

Figure 2. (A) Historical 1892 map of Willapa Bay overlain with the reserves showing native oyster harvest areas and ‘‘cultivated’’ areas where native oysters were held for shipment to markets elsewhere. (B) Results of intertidal surveys for eelgrass, both native Zostera marina and the introduced eelgrass Zostera japonica, with reserve boundaries (see Table 2 for areas). early fishery for native oysters resulted in stock declines governing reserves were altered to reflect the importance of this that followed a similar trajectory as that for C. virginica in new oyster, and a potentially sustainable fishery was ultimately Chesapeake Bay, although other factors like disease signifi- established by creating a shell return program and rotating cantly affected Chesapeake Bay oysters over time, and addi- harvests among reserve areas. tional factors continue to influence recovery of both stocks Willapa Bay is only a fraction of the size of most U.S. east (Kennedy & Breisch 1983, Mann et al. 1991, Rothschild et al. coast estuaries (the entire bay is roughly the size of the James 1994, NRC 2004, Powers et al. 2009, Trimble et al. 2009). As River subestuary within Chesapeake Bay, for example), yet it is a result of the timing of the fishery collapse of native oysters and the second largest estuary along the open west coast of the the choice at statehood to privatize tidelands, jurisdictional United States and produces the largest share of the oysters from differences and cultural and political events that erupted into this coast. Oyster sales are only conducted on 11% of the culture wars between scientists, politicians, and watermen Willapa Bay reserves, and harvests from the reserves currently involved in Chesapeake Bay oyster management (Keiner represent a relatively small fraction of oysters landed in 2009), did not occur in Willapa Bay. Oyster fishers and industry Washington state (equivalent of 1% of 27,669,135 kg landed members were also much more receptive to the advice of in 2008), but this level has been sustained over time since at least biologists and scientists who advised planting first Eastern 1950, and recent harvests have increased (Fig. 3). This is unlike oysters (C. virginica) and then Pacific oysters (C. gigas)to harvest levels in many if not most other ‘‘wild’’ fisheries, which resurrect their industry. Pacific oysters became the industry have leveled off or declined (Kirby 2004, Ruesink et al. 2005, mainstay and at the same time also proliferated on the Willapa Jackson 2008), and is a result, at least in part, of the privatiza- Bay oyster reserves, because they began reproducing naturally tion of land and substantial growth of the aquaculture industry in the estuary, with the first reported set in 1936. The laws in this estuary. Recent advances and success of shellfish AN EVALUATION OF THE WILLAPA BAY OYSTER RESERVES 77

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 3- dimensional 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 nu- trients 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 Figure 3. (A, B) Annual Willapa Bay oyster reserve sale totals in cubic meters or bushels of oysters (A) and dollar value received from 1945 to that local circulation was important and that oceanic water 2009 (B). (C) Oyster sales from 1967 to 2009 are broken down by the rarely spent enough time over the intertidal flats to be fully individual reserve from which they were harvested. 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 hatcheries with corresponding availability of eyed larvae and documented (Dumbauld et al. 2009, Wheat & Ruesink, unpubl. remote setting facilities have changed the face of the industry, manuscript), even though chlorophyll could increase over and resulted in complete control over the life cycle and put-and- ungrazed tidal flats (probably as a result of resuspension of take commercial aquaculture operations. This advance and benthic microalgae). This suggests that native oysters probably even a move toward privatization are now leading to imple- had less of an impact on phytoplankton clearance in the broader mentation of aquaculture as a potential solution to the contin- estuary because they were located predominantly in the south- ued decline of wild fisheries for C. virginica in Chesapeake Bay, ern areas, and especially because native oysters have lower fil- more than 200 y after the inception of large-scale oyster fisheries tration rates than Pacific oysters (Couch & Hassler 1989). there (Keiner 2009, Fincham 2010). Although the Willapa Bay A second highly valued ecosystem function is the provision oyster reserves have persisted and still rely on natural oyster of estuarine habitat. The Willapa reserves represent 11.2% of production, the latest seed crisis and lack of commercial oyster the intertidal portion of the estuary, and our surveys suggest sets will require persistence and ingenuity to sustain the effort. that they contribute substantially to estuarine habitat for other Oysters and other shellfish have been shown to provide a species. As such, they should also be viewed in the context of suite of ecosystem functions and services in addition to direct new efforts to create marine reserves and to conduct spatial harvest for human consumption (Lenihan & Peterson 1998, planning (Fraschetti et al. 2009, Lester et al. 2009, Foley et al. Piazza et al. 2005, Coen et al. 2007, Grabowski & Peterson 2010). The marine habitat most widely recognized to be 2007). Probably the most studied of these is their ability to important is submerged aquatic vegetation, but oysters them- influence water quality by removing seston from the water via selves act as ecosystem engineers and have been shown to filter feeding and subsequently contribute to benthic pelagic provide structured habitat for many aquatic invertebrates and coupling by depositing feces and pseudofeces to the substrate fish (Zimmerman et al. 1989, Jones et al. 1997, Breitberg 1999, (Newell 2004). This ecosystem role clearly depends on the quan- Posey et al. 1999, Bruno & Bertness 2001, Grabowski et al. tity and location of bivalves present, and numerous aspects of 2005, Coen & Grizzle 2007). Submerged aquatic vegetation in the system itself that contribute to its carrying capacity for these Willapa Bay takes the form of the eelgrass Z. marina (Linnaeus filter feeders. A growing amount of work has recently been 1785), the introduced eelgrass Z. japonica (Ascherson & conducted on quantifying carrying capacity, particularly for Graebner), and several species of macroalgae (both indigenous bivalve aquaculture, by developing an array of models that and nonindigenous; Hansen unpubl. data). Although native attempt to predict the responses of systems to the addition of oysters historically covered most of the reserves, and therefore 78 DUMBAULD ET AL.

Figure 4. (A) Oyster larval sets on seasonal shell strings deployed at 3 stations in Willapa Bay (see Fig. 1 for locations). Values from 1936 to 1954 (Lindsay et al. 1959) and from 1984 to 2001 (examination of larval data and discussions with D. Tufts) are reported as midpoints in each category (open symbols; noncommercial, <3 spat per shell; commercial, 3–25 spat per shell; good, 25–50 spat per shell; and excellent, >50 spat per shell). (B) Also shown are mean values of the Pacific decadal oscillation for the oyster spawning months (June to August) using data from http://jisao.washington.edu/pdo/ (accessed August 23, 2010). about 11% of the intertidal area in the estuary, eelgrass now presence of structure, life history stage and location in the covers about 1,796 ha of the reserves and thus represents a very estuary are important considerations. For example, 0 + Dung- significant portion (8%) of this habitat in the estuary. As eness crab clearly preferred the structure provided by oysters a result of the low tidal elevation of the reserves, the majority and eelgrass, but having reached a predation threshold, older (78%) of this eelgrass is native Z. marina, which has been 1 + crab used open mud habitat for foraging (Holsman et al. shown to be a valuable habitat for many invertebrates and fish 2006). Although juvenile flatfish have been shown to associate in Willapa Bay and other U.S. west coast estuaries, as well as with structure for protection but forage in open habitat other estuaries worldwide (Simenstad et al. 1982, Simenstad & elsewhere (Laffargue et al. 2006), studies to date have not Fresh 1995, Bostrom et al. 2006, Hosack et al. 2006, Ferraro & distinguished function, and juvenile English sole were captured Cole 2007). Both oysters and eelgrass provide structured in equal density over oysters, eelgrass, and open mudflats in habitat that is usually contrasted with open unstructured Willapa Bay (Hosack et al. 2006). This was also true for juvenile sediment in these comparisons. We found less open unstruc- Chinook salmon, but they were more abundant at locations tured intertidal habitat than structured habitat on the reserves, closer to the estuary mouth, and they appeared to use eelgrass also presumably a result of their low intertidal elevation and over oysters and open habitat when individually tracked in a location in the estuary (estimate of 22% based on 2,939 large field enclosure and laboratory tanks (Semmens 2008, ha dominated by burrowing shrimp and difference of 2,433 Dumbauld et al. 2009). Other structure-oriented fish like ha of open habitat not covered with oysters or either species of gunnels, tube-snouts, perch, and some juvenile rockfish have eelgrass). also been shown to use eelgrass and oysters in west coast Predation is viewed as the strongest influence on soft- estuaries (Matthews 1990, Weschler 2004, Hosack et al. 2006, sediment tideflat communities, and structure-forming species Dauble 2010). Structure, including both species of eelgrass and like oysters and eelgrass greatly influence these communities by oysters, also provides a substrate on which Pacific herring have providing refuge and also by influencing recruitment (Posey been shown to deposit their eggs in Willapa Bay (D. Pentilla, et al. 1995, Peterson et al. 2000, Lenihan & Micheli 2001). In unpubl. data). Egg survival has not been measured, however, Willapa Bay, oysters and eelgrass have been shown to support and it seems likely that eggs deposited on the larger blades of the equally and more diverse communities of benthic infauna than native eelgrass in low intertidal habitat would be less subject to unstructured open tideflats, which are often dominated by desiccation and would survive better than those found on the thalassinid burrowing shrimp (Posey et al. 1991, Dumbauld much smaller blades of introduced Japanese eelgrass in upper et al. 2001, Hosack et al. 2006, Ferraro & Cole 2007). Larger fish areas (Jones 1972). and invertebrates, including juvenile Dungeness crab, English Last, structured habitat and particularly eelgrass are used sole, and salmon, have also been shown to use these estuarine heavily and valued as foraging areas for waterfowl, waders, and habitats, but studies to date have shown that in addition to the shorebirds. Brant geese in particular graze heavily on eelgrass, AN EVALUATION OF THE WILLAPA BAY OYSTER RESERVES 79 and use Willapa Bay and other estuaries as stopovers on their Written Washington state legislation covering the oyster trek to arctic breeding grounds (Wilson & Atkinson 1995, reserves states that ‘‘it is the policy of the state to improve the Moore et al. 2004). Willapa Bay ranks sixth among estuaries reserves so that they are productive and yield revenue sufficient as a staging area for these geese, and at least 1 area on the LIOR for their maintenance’’ (Washington State Administration is heavily used and serves as a monitoring location for annual Code RCN 75.25.060). Furthermore, it is also the policy of abundance surveys. This area was clearly dominated by native the state ‘‘to maintain the oyster reserves to furnish shellfish to oysters in the 1800s and it is unclear whether geese would have growers and processors and to stock public beaches.’’ An used it as heavily then. Dabbling ducks also feed on eelgrass and economic evaluation prepared by Woelke (1969) pointed out have been shown to alter their foraging habits and switch to 2 policy constraints suggested by the commercial oyster in- nonnative Z. japonica in areas where it has become abundant dustry that were considered in the past: (1) the reserves should (Baldwin & Lovvorn 1994, Lovvorn & Baldwin 1996). Like fish not be sold unless each grower has an equitable chance at and invertebrates, shorebird use of structured habitats is species procuring them and (2) reserve sales should not compete with specific (Luckenbach 1984, Connolly & Colwell 2005), but they the industry and the reserves should not be overpopulated with are more likely to use upper intertidal areas that are available oysters, because this might cause a general decline in oyster for longer periods of time and also available on less extreme condition throughout the estuary. A later revision to the reserve tides. Nonetheless, fairly extensive areas of the reserves are now laws in Washington requested that WDFW periodically in- relatively undisturbed by humans, which are known to decrease ventory the state reserves and assign reserve lands into several use (Yasue 2006), and the value of these areas for feeding by all management categories—including native Olympia oyster 3 types of birds should be considered. broodstock areas, commercial shellfish harvesting zones, com- Seagrasses are a declining resource in many eutrophic mercial shellfish propagation zones designated for long-term estuaries such as Chesapeake Bay and other locations world- leasing to private aquaculturists, public recreational harvesting wide (Orth et al. 2006, Hughes et al. 2009, Waycott et al. 2009, zones, and unproductive land—and that WDFW should de- Orth et al. 2010). This is not the case in Willapa Bay, however, velop a reserve management plan in coordination with the in- where eelgrass is relatively stable and even increasing (Dumbauld dustry. Onsite surveys were conducted for each Puget Sound et al. 2009, Ruesink et al. 2010). Four mechanisms of disturbance reserve in 1985, and a final report was submitted to the leg- and interactions between eelgrass and oyster aquaculture have islature (Westley et al. 1985), whereas only a draft report was been actively researched in Willapa Bay: (1) competition be- prepared on the Willapa Reserves (Tufts 1987). Our survey tween oysters and plants for space, (2) nutrient supplementa- represents the first quantitative attempt at achieving this ob- tion to eelgrass from oyster biodeposits, (3) increased light to jective. Issues surrounding reserve management resurfaced in eelgrass from increased filter feeding by oysters and (4) com- 2001, and an industry advisory committee was granted author- plete or partial removal of plants by oyster harvest activity. ity to make recommendations regarding management practices Results to date suggest that the most significant impacts are the on oyster reserve lands. The new legislation again suggested result of simple competition for space and direct removal via goals that would increase revenue through production of high- shellfish harvest (Wisehart et al. 2007, Dumbauld et al. 2009, value shellfish, not be detrimental to the market for shellfish Tallis et al. 2009, Ruesink et al. unpub. msp., Wagner et al. grown on nonreserve lands, and that would avoid negative unpub. msp.). In the case of oyster reserve operations, oysters impacts to existing shellfish populations. are most likely to compete directly for space, because harvest Our review suggests that Pacific oyster harvest from the activities are generally conducted by hand, which has been Willapa reserves is sustainable as long as ‘‘natural’’ oyster set is shown to have less affect than mechanical harvest (Tallis et al. maintained, but this clearly fluctuates with environmental con- 2009). At the landscape scale, current Pacific oyster culture on ditions. Thus, very low recruitment of oysters from the early the reserves represents a relatively small fraction (11%) of the 1960s through the early 1980s roughly coincided with a shift in reserve area and an even smaller portion (2%) of the intertidal the Pacific decadal oscillation (Fig. 4) (Hare & Mantua 2000) in area of the estuary. Furthermore, we found substantial eelgrass, the northeast Pacific, with cold years typically resulting in fewer Z. marina, comingling with oysters (Z. marina covered 44% of spawning and setting events. This translated to reduced oyster the reserve sales area; Table 2). sales from the reserves. Recent lack of recruitment in 2006 to 2009 and a potential decline in sales may be related to such a Management History and Recommendations climate shift as well, but it is too early to tell. Current sales areas seem appropriately scaled to prevent overpopulation of the re- Willapa Bay oyster reserve management to date has focused serves and, because of their location in the southern portion of almost exclusively on yield of Pacific oysters, with the annual the estuary (predominantly south of the fattening line), the oyster sale and attendant seeding operations being the focus oysters present on them are less likely to influence the condition of activity. Although even this goal has and continues to be of other commercially grown oysters on fattening and harvest controversial at times, our habitat survey results suggest that beds closer to the estuary mouth. These currently cultivated additional goals that take a broader landscape and ecosystem- areas on the reserves represent a reasonably small fraction based perspective should be considered. Although de facto con- (10%) of the total area of the reserves and only 2% of the servation of those areas not set aside for oyster production has tideflat in the estuary, compared with the 20% occupied by arguably occurred, active consideration could be particularly commercial aquaculture operations (Fig. 1). Both quantity of fruitful in light of information now in hand and numerous re- oysters and, in particular, revenue generated from these reserves cent calls for marine ecosystem-based management and spatial sales escalated from the mid 1990s onward as a result of active planning (USCOP 2004, Granek et al. 2005, Leslie & McLeod consideration of larval spawning and setting, and some expan- 2007, Foley et al. 2010). sion of planted areas utilizing this set, particularly those on the 80 DUMBAULD ET AL.

Nemah Reserve, which often generate higher value (Fig. 3). A they influence the environment and presence of other species tradeoff clearly exists between expanding sales in this area to when they are abundant. These engineers are considered con- generate funds and to maintain reserve operations, and poten- servation targets because they can ameliorate degraded habitats tially overstocking the estuary and affecting commercial oper- for other species (Crain & Bertness 2006), and engineering feed- ations elsewhere, because this is one of the only reserve areas backs can lead to persistent or stable states. We suspect that north of the fattening line and is also an area where oysters and burrowing shrimp lead to one alternative stable state, whereas other habitats like eelgrass should be evaluated for their the presence of oysters and/or eelgrass may dominate another, importance to fish and invertebrates that use the estuary as a given that burrowing shrimp have been shown to interact nursery. Dungeness crab, which use oyster habitat, are more negatively with both eelgrass (Dumbauld & Wyllie-Echeverria likely to recruit as juveniles to the Nemah Reserve than those to 2003, Siebert & Branch 2005, Siebert & Branch 2006, Berkenbusch the south, and this area has already been used as a site for et al. 2007) and oysters (Dumbauld et al. 1997). Although burrow- creating oyster habitat to mitigate losses of these crab resulting ing shrimp destabilize the sediment, eelgrass and oysters can from dredging elsewhere in the estuary (Dumbauld & Kauffman stabilize the sediment. Burrowing shrimp are currently only 1999). Juvenile English sole and salmon may also be more likely present in large numbers on the Nemah Reserve, but they are to recruit and use estuarine habitat on this reserve than those declining in abundance throughout Willapa Bay and other located farther away from the ocean (Dumbauld et al. 2009). estuaries along the coast of the Pacific Northwest. The mech- Habitat values and tradeoffs for these species should continue to anism behind this shift between alternative states is unknown, be evaluated on this reserve and at the estuarine landscape scale. but such shifts seem likely to have occurred historically as well, The Willapa Bay oyster reserves were originally set aside to resulting in the need for the oyster industry to treat these shrimp protect native oyster populations, and broodstock maintenance as pests beginning during the late 1950s (Dumbauld et al. 2006). remains a stated goal in governing legislation. Although exist- Native oysters are likely even more susceptible to bioturbation ing population levels are unknown, the current O. lurida pop- from shrimp, but it is unclear whether they formed reefs before ulation is only a miniscule fraction of what the bay historically they were harvested and how stable these were in the face of supported. In response to concern over the reduced populations burrowing shrimp invasions. of this species in Puget Sound and Willapa Bay, WDFW de- The Willapa Bay oyster reserves provide an excellent place veloped an Olympia oyster restoration plan (Cook et al. 2000). to continue to preserve and, potentially, to study multiple con- This restoration plan was approved by the WDFW commission servation targets (native oysters, aquaculture species, eelgrass, in 1998, but no funding was allocated. Nonetheless, studies were and burrowing shrimp), the ecosystem functions and services conducted in Willapa Bay that indicated that several factors they provide, possible mechanisms for shifts between stable influencing postsettlement survival currently prevent this oyster states, and ways to maintain resilience to such shifts (Carpenter from greatly expanding its distribution and attaining preexploi- et al. 2001, Folke et al. 2004). The outlook is particularly tation status in the estuary (Buhle & Ruesink 2009, Trimble favorable now that some of the funds generated from reserve et al. 2009). These factors included a combination of recruit- sales are designated for research. Although the recent legisla- ment preference to Pacific oyster reefs located higher in the tion emphasizes research on aquatic nuisance species and intertidal where aerial exposure causes mortality, competition burrowing shrimp, the advisory committee has voiced sup- with fouling organisms including introduced species of tuni- port for a plan based on broader ecosystem goals for coastal cates and bryozoans after settlement, and predation by two estuaries. introduced species of drills and a flatworm. Recruitment lim- ACKNOWLEDGMENTS itation resulting from lack of broodstock did not appear to be an issue. This broodstock is believed to be predominantly lo- We thank our numerous predecessors at the University of cated in very low intertidal areas or subtidal areas of the reserves Washington, Washington Department of Fish and Wildlife and, although surveys have been proposed, they have not yet (then Fisheries), and Willapa Bay oyster industry for having the been completed. Portions of the LIOR and particularly the Bay foresight to encourage and continue to collect data on oyster Center and Willapa River reserves, which are almost entirely spawning and setting in Willapa Bay. These include but are not subtidal, would be of particular interest. Preliminary investiga- limited to Trevor Kincaid, Cedric Lindsay, Ron Westley, Clyde tions (Trimble, unpubl. data) suggest that substrate limitation Sayce, Dennis Tufts, and Lee Weigardt. Funding for the current may constrain recruitment of native oysters in subtidal areas study was provided by the Andrew Mellon Foundation, where they are less subjected to fouling issues present in the low Washington Department of Fish and Wildlife (both directly intertidal, and that these areas of the reserves could potentially and via a grant to the Olympic Natural Resources Center be used to enhance stocks directly and to be used as a source of (ONRC) from the oyster reserve research account) and USDA- material for low intertidal areas if other factors like outplanting ARS. Lee McCoy was instrumental in designing and setting up techniques (perhaps using small clumps) are also considered. the field survey, processing and analyzing data, and producing Shellfish harvest has been an important activity supporting maps in GIS. Miranda Wecker and Keven Bennett at ONRC local coastal economies in Washington state for at least 150 y. completed extensive work, particularly on the bathymetry layer, Clearly, societal goals will continue to include this activity, and but also compiling existing Willapa GIS layers. We also thank the Willapa Bay oyster reserves should contribute to this goal. A Roy Hildenbrand, Katelyn Cassidy, and Cara Fritz for assis- broader perspective suggests that the reserves have and will tance in collecting data. Last, we thank Dick Olsen, Brian continue to contribute to other ecosystem functions and services Pickering, Kevin Soule, and Travis Haring for data collection as well. Native oysters, Pacific oysters, eelgrass, and burrowing and contributions as oyster reserve managers, and members of shrimp can all be considered foundation species or ecosystem the Willapa Bay Oyster Reserve Advisory Committee for their engineers (sensu Jones et al. 1997, Bruno & Bertness 2001), and guidance. AN EVALUATION OF THE WILLAPA BAY OYSTER RESERVES 81

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