Brett R. Dumbauld

Historical ecology with real numbers: past and present extent and biomass of an imperilled estuarine habitat

Historic baselines are important in developing our understanding of ecosystems in the face of rapid global change. While a number of studies have sought to determine changes in extent of exploited habitats over historic timescales, few have quantified such changes prior to late twentieth century baselines. Here, we present, to our knowledge, the first ever large-scale quantitative assessment of the extent and biomass of marine habitat-forming species over a 100-year time frame. We examined records of wild native oyster abundance in the United States from a historic, yet already exploited, baseline between 1878 and 1935 (predominantly 1885–1915), and a current baseline between 1968 and 2010 (predominantly 2000–2010). We quantified the extent of oyster grounds in 39 estuaries historically and 51 estuaries from recent times. Data from 24 estuaries allowed comparison of historic to present extent and biomass. We found evidence for a 64 per cent decline in the spatial extent of oyster habitat and an 88 per cent decline in oyster biomass over time. The difference between these two numbers illustrates that current areal extent measures may be masking significant loss of habitat through degradation.

Oysters, Crabs, and Burrowing Shrimp: Review of an Environmental Conflict Over Aquatic Resources and Pesticide Use in Washington State's (USA) Coastal Estuaries

Washington State’s coastal estuaries are productive shallow water environments that support commercial fisheries for Dungeness crabs (Cancer magister) and English sole (Parophrys vetulus) by providing 0+(settlement to age l) populations with critical refuge and foraging habitats until subadults migrate to the nearshore coast. Intertidalmudflats also constitute prime areas for commercial oyster (Crassostrea gigas) culture, an, important industry for the coastal communities of Willapa Bay and Grays Harbor that supply much of the nations oysters. Conflicts over natural resources and estuarine utilization have arisen over the last 37 yr due to the use of carbaryl (an organo carbamate pesticide) by oyster growers on their grounds to control populations of burrowing thalassinidean shrimp (Neotrypaea californiensis and Upogebia pugettensis). Burrowing shrimp, which have an indirect negative effect on oyster survival and growth through bioturbation and sediment destabilization, are killed by carbaryl, as are 0+ and subadult Dungeness crabs, 0+English sole, and other non-target species prsent on the tideflats at the time of application. The pesticide is delivered at 9 kg ha−1 directly to the mudflat as a wetable powder during low tides in July and August. Commercial crabbers and other groups who have economic, recreational, and environmental interests in the estuaries have generally opposed use of the chemical that oyster growers maintain is essential to sustain production levels. For years, government natural resource agencies that regulate the use of carbaryl lacked critical information needed to effectively manage the program. An Environmental Impact Statement (EIS) and Supplemental EIS have provided much of that data and helped shape management decisions with regard to establishing carbaryl concentration rates and total allowable spray area. Additional research is needed to develop more economically and environmentally sound policies for shrimp control based on burrowing shrimp-oyster interactions on an estuarine-wide scale. In this paper we review issues pertaining to oyster culture, the use of carbaryl to control burrowing shrimp populations, and effects on non-target species, drawing upon research from, published articles as well as unpublished data collected by the authors. We also discuss what is known of burrowing shrimp life history and ecology and emphasize the importance of integrating information on shrimp, such as timing of recruitment, variability in year class strength, and patterns of habitat use, into carbaryl control policies or alternative strategies that may be developed in the future. We recommend controlled experimentation be done to examine the ecological effects of delaying carbaryl application to some ghost shrimp beds until October after peak recruitment of 0+ ghost shrimp has occurred, allowing the number of hectares treated each year to vary based on fluctuations in pest population densities, and modifying the substrate by applying a dense layer of oyster shell to the mudflat (shell pavement) to reduce recruitment of ghost shrimp.

Habitat Associations of Estuarine Species: Comparisons of Intertidal Mudflat, Seagrass (Zostera marina), and Oyster (Crassostrea gigas) Habitats

The complexity of habitat structure created by aquatic vegetation is an important factor determining the diversity and composition of soft-sediment coastal communities. The introduction of estuarine organisms, such as oysters or other forms of aquaculture, that compete with existing forms of habitat structure, such as seagrass, may affect the availability of important habitat refugia and foraging resources for mobile estuarine fish and decapods. Fish and invertebrate communities were compared between adjacent patches of native seagrass (Zostera marina), nonnative cultured oyster (Crassostrea gigas), and unvegetated mudflat within a northeastern Pacific estuary. The composition of epibenthic meiofauna and small macrofaunal organisms, including known prey of fish and decapods, was significantly related to habitat type. Densities of these epifauna were significantly higher in structured habitat compared to unstructured mudflat. Benthic invertebrate densities were highest in seagrass. Since oyster aquaculture may provide a structural substitute for seagrass being associated with increased density and altered composition of fish and decapod prey resources relative to mudflat, it was hypothesized that this habitat might also alter habitat preferences of foraging fish and decapods. The species composition of fish and decapods was more strongly related to location within the estuary than to habitat, and fish and decapod species composition responded on a larger landscape scale than invertebrate assemblages. Fish and decapod species richness and the size of ecologically and commercially important species, such as Dungeness crab (Cancer magister), English sole (Parophrys vetulus), or lingcod (Ophiodon elongatus), were not significantly related to habitat type.

Growth and persistence of a recent invader Carcinus maenas in estuaries of the northeastern Pacific

During the summer of 1998 a new year class of the invasive European green crab, Carcinus maenas, appeared in Oregon and Washington estuaries as well as in northern California, USA, and on Vancouver Island, Canada. This invader was first discovered in San Francisco Bay almost a decade earlier and by 1995 it had spread to northern California. The coast-wide colonization event we studied in 1998 (El Niño cohort) was correlated with unusually strong north flowing coastal currents from September 1997 to April 1998. Larval transport by ocean currents from established populations to the south appeared to be the mechanism for the colonization. Crabs from the 1998-year class grew faster than counterparts from Maine and Europe, averaging 14 mm in carapace width in June, and 46 mm by September 1998. By the end of their second summer, males ranged from 52 to 80 mm in carapace width, and by fall of 2000 some males attained a carapace width of over 90 mm. The life span for C. maenasit in Oregon, Washington and British Columbia is estimated to be similar as in Europe and Maine: 4–6 years. Even though the initial colonists (98-year class) are dying of senescence, and coastal currents have not been favorable for larval transport from source populations in California, green crabs do persist in Oregon and Washington estuaries. It appears that local reproduction and recruitment in some years is high enough to keep this population from going extinct.

Factors Preventing the Recovery of a Historically Overexploited Shellfish Species, Ostrea lurida Carpenter 1864

ABSTRACT The Olympia oyster, Ostrea lurida Carpenter 1864,† in estuaries along the Pacific coast of North America, experienced overexploitation throughout its range in the late 1800s, resulting in commercial extinction before 1930. Significant harvest restrictions and marine reserves were established in Washington State by 1897 to protect new recruits, and harvest pressure has been negligible for the past 80 y. Nevertheless, O. lurida remains locally rare. This study focuses on the contemporary dynamics of the remnant population of O. lurida in Willapa Bay, Washington, historically home to the largest native oyster fishery on the coast, with a broad focus on factors preventing recovery. Failed recovery could be because of reproductive limitation, or to poor postrecruitment performance. In this case, reproductive limitation seems unlikely, because historical (1947 to 1983) and modern (2002 to 2006) records reveal 5-fold higher annual spatfall for O. lurida than introduced Pacific oysters (Crassostrea gigas.) However, O. lurida remains rare and C. gigas is commercially exploited from natural recruitment. To evaluate the effects of abundant C. gigas in intertidal areas on O. lurida settlement patterns, strings of C. gigas shell were placed at two tidal elevations in three habitat types—open mud, eelgrass beds of Zoster a marina, and C. gigas reefs. Settlement of O. lurida was significantly higher on the shell strings placed in the C. gigas reefs at both tidal heights. To evaluate postrecruitment demography, juvenile O. lurida were outplanted at three tidal elevations at five sites, and fouling organisms were manipulated to test for competition. Short emersion times (8% greater exposure) reduced survival by 80% relative to subtidal treatments, but did not affect growth rates of survivors. Naturally-setting competitors, mostly nonindigenous, depressed survival by 50% and growth by 20%. In a third experiment, manipulating the density and stability of shell substrate, O. lurida was easily moved or buried when outplanted in a thin, unconsolidated layer. These results indicate that recovery has been hampered by the removal of dense subtidal native oyster shell accumulations during exploitation, by direct competition from exotic species, and by the appearance of novel introduced oyster shell settlement substrate in the intertidal zone. This altered web of interactions influencing O. lurida serves as a model for beginning to explore the failed recovery of overfished species in rapidly changing coastal systems.

Oysters and Aquaculture Practices Affect Eelgrass Density and Productivity in a Pacific Northwest Estuary

ABSTRACT The presence of bivalves and bivalve aquaculture can have positive and negative impacts on seagrass and associated benthic communities. Some oyster (Crassostrea gigas) aquaculture methods recently have been restricted to reduce benthic disturbance and protect native eelgrass (Zostera manna) in West coast (USA) estuaries. We argue that aquaculture, like all food production systems, involves tradeoffs with natural systems, but that the magnitude of those tradeoffs depends on the ecological details of the production system. Capitalizing on oyster aquaculture farms as large scale “manipulations” in Willapa Bay, WA (USA), we explored three different oyster aquaculture methods (mechanical harvest or “dredged” on-bottom, hand-picked on-bottom and long line off-bottom). We found that both the biological (oyster-eelgrass interactions) and physical (disturbance or structure) components of aquaculture led to changes in the eelgrass population. Eelgrass density declined with oyster density in all aquaculture areas, likely as a result of direct competition for space. Eelgrass relative growth rate, plant size, and production did not change with oyster density. However, all eelgrass measures were affected by aquaculture, and the type and magnitude of impacts varied among eelgrass measures and aquaculture methods. Throughout the bay, eelgrass in long line areas occurred at densities indistinguishable from nearby uncultivated areas, but in 2004, eelgrass in long line areas was smaller (32%) and had lower production per area (70%). Cultivating oysters in dredged or hand picked beds increased eelgrass growth rates slightly, but led to lower eelgrass density (70% and 30%, respectively), plant size (32%, both cases), and production (70%, both cases). In a large scale simulated mechanical harvest experiment, the temporal response of eelgrass density varied dramatically by site, ranging from 1 to >4 y. If eelgrass impact reduction, rather than avoidance, is identified as the management goal, the degree of tradeoff between eelgrass habitat and oyster production can be minimized by managing aquaculture methods or oyster planting densities, depending on the eelgrass measure of interest. Explicit management goals and appropriate eelgrass habitat indicators must be developed before our findings can be used to suggest best management practices for intertidal aquaculture in the Pacific Northwest.

Contributions of Coastal and Watershed Energy Sources to Secondary Production in a Northeastern Pacific Estuary

We examined the relationship between variation in origin of organic matter and benthic secondary production in a shallow, macrotidal estuary on the United States Pacific Northwest coast, Willapa Bay, Washington. Spatial variation in energy sources and benthic productivity were investigated at both local (vertical height and cross-bank components) and regional (sites within the bay) scales. We determined the stable carbon isotope ratios of oysters (Crassostrea gigas) to evaluate marine versus terrestrial energy sources, compared growth rates of oysters, and made time series measurements of physical variablest at estuarine channel and intertidal stations. The stable carbon isotope ratios of oysters ranged from −22‰ in inner portions of the estuary to −18‰ near the mouth and oysters grown on the substrate surface were enriched in δ13C relative to those grown in the water column. These patterns are consistent with terrigenous inputs away from the estuary mouth and benthic microalgae in the diets of on-bottom oysters. The highest oyster growth was found at an inner estuary site where riverine inputs are relatively high and coincided, with high ammonium in the water column. However, for most sites in Willapa Bay, oyster growth actually declined away from the estuary mouth. Reducing the time available for feeding by transplanting oysters higher in the intertidal zone had significant negative effects on growth(e.g., a reduction of 27–35% over 0.5 m). Despite the fact that oysters grown on-bottom had access to different resources than those in the water column, their growth was slower at amy given tidal elevation, which may be due to on-bottom competition with other suspension feeders, boundary layer effects, or interference from turbidity. In a practical sense, oyster growers have been adjusting to allochthonous energetic support of food webs in Willapa Bay for more than a century, because they have traditionally moved oysters from southern parts of the bay where recruitment is relatively high to beds where market-size oysters can be grown closer to the mouth. This study provides mechanistic support for these practices and suggests that climatic events on a variety of temporal scales (Pacific Decadal Oscillation, upwelling events) could have economic consequences for aquaculture.

An introduced Asian parasite threatens northeastern Pacific estuarine ecosystems

The introduced Asian parasitic bopyrid isopod, Orthione griffenis, was first discovered on the Pacific coast of North America in Washington in 1988 and next in California in 1992. The range of Orthione presently extends from British Columbia to Baja California, where it infests at least two species of the native estuary mud shrimp, Upogebia. Intense Orthione infestations are associated with the apparent demise of many local populations of Upogebia pugettensis yet nonindigenous origins of Orthione in North America and thus the ecological significance of its impacts have remained in doubt. Six criteria reveal that Orthione is introduced to North America: its conspecificity with disjunct Asian populations, its earliest (1950s) collections in Asia, its late discovery among symbiotic species associated with Upogebia, its historical absence, and its appearance in North America coincident with extensive new ballast water traffic from Asia. Orthione is the first recognized bopyrid isopod invasion globally. Coexistence of U. pugettensis, which are ecosystem engineers, with its newly acquired parasite cannot be assumed. Orthione threatens eastern Pacific estuary ecosystems where Upogebia were previously abundant.

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.

Do sturgeon limit burrowing shrimp populations in Pacific Northwest Estuaries

Green sturgeon, Acipenser medirostris, and white sturgeon, Acipenser transmontanus, are frequent inhabitants of coastal estuaries from northern California, USA to British Columbia, Canada. An analysis of stomach contents from 95 green sturgeon and six white sturgeon commercially landed in Willapa Bay, Grays Harbor, and the Columbia River estuary during 2000–2005 revealed that 17–97% had empty stomachs, but those fish with items in their guts fed predominantly on benthic prey items and fish. Burrowing thalassinid shrimp (mostly Neotrypaea californiensis) were important food items for both white and especially for green sturgeon taken in Willapa Bay, Washington during summer 2003, where they represented 51% of the biomass ingested (84.9% IRI). Small pits observed in intertidal areas dominated by these shrimp, are likely made by these sturgeon and we present evidence from exclusion studies and field observation that the predator making the pits can have a significant cumulative negative effect on burrowing shrimp density. These burrowing shrimp present a threat to the aquaculture industry in Washington State due to their ability to de-stabilize the substrate on which shellfish are grown. Despite an active burrowing shrimp control program in these estuaries, it seems unlikely that current burrowing shrimp abundance and availability as food is a limiting factor for threatened green sturgeon stocks. However, these large predators may have performed an important top down control function on shrimp populations in the past when they were more abundant.