Impacts of Coastal Acidification on the Pacific Northwest Shellfish Industry and Adaptation Strategies Implemented in Response

Barton, A., Waldbusser, G. G., Feely, R. A., Weisberg, S. B., Newton, J. A., Hales, B., ... & McLaughlin, K. (2015). Impacts of coastal acidification on the Pacific Northwest shellfish industry and adaptation strategies implemented in response. Oceanography, 28(2), 146-159. doi:10.5670/oceanog.2015.38

10.5670/oceanog.2015.38 Oceanography Society

Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse EMERGING THEMES IN OCEAN ACIDIFICATION SCIENCE

Impacts of Coastal Acidification

on the Pacific Northwest Shellfish Industry and Adaptation Strategies Implemented in Response

By Alan Barton, George G. Waldbusser, Richard A. Feely, Stephen B. Weisberg, Jan A. Newton, Burke Hales, Sue Cudd, Benoit Eudeline, Chris J. Langdon, Ian Jefferds, Teri King, Andy Suhrbier, and Karen McLaughlin

Photo credit: Sandra Barton Vickers

146 Oceanography | Vol.28, No.2 ABSTRACT. In 2007, the US west coast shellfish industry began to feel the effects at optimal levels, but the chemistry of of unprecedented levels of larval mortality in commercial hatcheries producing incoming seawater varies (Barton et al., the Pacific oyster Crassostrea gigas. Subsequently, researchers at Whiskey Creek 2012). Subsequent work, in part the result Shellfish Hatchery, working with academic and government scientists, showed a of monitoring larval oysters in shellfish

high correlation between aragonite saturation state (Ωarag) of inflowing seawater and hatcheries, documents a mechanism for

survival of larval groups, clearly linking increased CO2 to hatchery failures. This work direct Ωarag sensitivity in early shell forma- led the Pacific Coast Shellfish Growers Association (PCSGA) to instrument shellfish tion of bivalve larvae (Waldbusser et al., on the Pacific Northwest hatcheries and coastal waters, establishing a monitoring network in collaboration with 2013; 2015), responses previously thought university researchers and the US Integrated Ocean Observing System. Analytical to be related solely to changes in the

developments, such as the ability to monitor Ωarag in real time, have greatly improved organisms’ acid-base chemistry (Pörtner, Shellfish Industry the industry’s understanding of carbonate chemistry and its variability and informed 2008). These findings have immediate the development of commercial-scale water treatment systems. These treatment implications for the Pacific Northwest systems have generally proven effective, resulting in billions of additional oyster shellfish industry, which has experienced larvae supplied to Pacific Northwest oyster growers. However, significant challenges significant seed shortages since 2007. remain, and a multifaceted approach, including selective breeding of oyster stocks, In nearshore California Current sur- expansion of hatchery capacity, continued monitoring of coastal water chemistry, and face waters off the coast of Oregon, the

improved understanding of biological responses will all be essential to the survival of increase in atmospheric CO2 has shifted

the US west coast shellfish industry. the median Ωarag from approximately 2.5 to 2.0 (Feely et al., 2008; Harris et al.,

INTRODUCTION sensitive to the effects of ocean acidifi- 2013), and values of Ωarag less than 2.0 are The coastal ocean along the west coast cation (OA), such as reduced saturation already common throughout the spring of the United States supports some of state (Fabry et al., 2008; Hofmann et al., and summer across major sections of the most productive fisheries in the 2010; Hettinger et al., 2012; Bednaršek US Pacific coastal waters and Puget Sound world, including the 120-year-old Pacific et al., 2012, 2014; Gazeau et al., 2013; (Feely et al., 2008, 2010, 2012b; Hauri Northwest shellfish industry. Seasonal Kroeker et al., 2010, 2013; Gaylord et al., et al., 2009). OA has contributed signifi- coastal upwelling, which annually sup- 2014), including many commercially cantly to shoaling of Pacific Northwest plies nutrient-rich water to the inner con- important shellfish species (Kurihara aragonite and calcite saturation horizons tinental shelf from late spring to early et al., 2007; Green et al., 2009; Miller (Feely el al., 2012b), and recent observa- fall, drives this productivity. However, et al., 2009; Talmage and Gobler, 2011; tions along the Oregon/Washington coast

the same upwelling that fuels the indus- Barton et al., 2012; Hettinger et al., 2012; have recorded Ωarag <1.0 in upwelled water try also threatens it. Decomposition of Waldbusser et al., 2013, 2015). Organisms at the surface, a condition not expected in organic matter at depth naturally raises that deposit calcareous shells or skele- the open ocean for decades (Feely et al.,

CO2 in upwelled seawater, and increasing tons may respond to decreasing Ωarag at 2008). Modeling of the California Current

atmospheric CO2 concentrations have values as high as 2, and are expected to System predicts that this trend will con- raised the baseline, leading to increased encounter increasing physiological chal- tinue and accelerate relative to the open intensity, magnitude, and duration of lenges as carbonate saturation decreases oligotrophic ocean, with undersaturated acidified water over the continental shelf in the ocean (Fabry et al., 2008; Barton conditions in surface waters predicted to (Feely et al., 2008; Hauri et al., 2009, 2013; et al., 2012; Bednaršek et al., 2012, 2014; be the norm more than 50% of the time Gruber et al., 2012). Waldbusser et al., 2015). Except for a few during summer by 2050 (Gruber et al.,

When gaseous CO2 dissolves in sea- studies at underwater seeps that vent 2012; Hauri et al., 2011, 2013).

water, it reacts with the water to form CO2, this research has almost exclusively These changes in Pacific Northwest

a weak acid (H2CO3), which dis- been carried out in laboratories, where ocean conditions have already resulted

sociates to release a hydrogen ion saturation states were reduced with CO2 in major oyster seed production declines + – (H2CO3 H + HCO3) or reacts and held constant to match the expected (Barton et al., 2012; Washington directly to consume carbonate ions changes in surface ocean chemistry sev- State Blue Ribbon Panel on Ocean 2– – (H2CO3 + CO3 2HCO3 ). This acid- eral decades in the future. Acidification, 2012), and the shellfish ification process decreases the satura- Recent research shows a clear link industry has adopted a comprehensive

tion state of aragonite (Ωarag) and calcite between natural variability in seawater strategy to understand, and mitigate, fur-

(Ωcal), the two mineral forms of calcium Ωarag along the Oregon coast and com- ther impacts on commercial production carbonate that most bivalves use to form mercial production of Pacific oyster lar- (Washington State Blue Ribbon Panel on their shells. A variety of shell-forming vae in a hatchery setting, where food Ocean Acidification, 2012). Using fund- organisms have been shown to be highly and water temperatures are maintained ing from state, federal, and industry

Oceanography | June 2015 147 groups, shellfish hatcheries have forged academia, federal and state scientists, and seed became prohibitively expensive, and partnerships with university research- the local management community flour- it became clear that growers could not ers, and are now some of the best instru- ished in ways that benefited all sectors; rely solely on inconsistent natural spawn- mented monitoring stations for collecting and the industry’s strategy to adapt as OA ing events (Dumbauld et al., 2011) to sup- carbonate chemistry measurements in the continues to advance globally. port their burgeoning industry (Gordon coastal zone. Industry uses these mon- and Blanton, 2001). itoring data as a real-time management PACIFIC NORTHWEST By the late 1970s, successful commer- tool to optimize water treatment systems SHELLFISH INDUSTRY cial hatcheries were established in the and improve commercial production of Shellfish have been harvested in the Pacific Northwest and began supplying oyster larvae. Additionally, hatcheries Pacific Northwest for thousands of years, billions of “eyed” (setting size) larvae to provide a perfect environment for mon- and commercial oyster farming has been growers each year. The three major com- itoring biological responses, given that an important cultural and economic part mercial hatcheries that currently supply typical hatchery protocols require rou- of coastal communities in the Northwest larvae to the West Coast shellfish indus- tine tracking and measurement of larval since the late 1800s. Today, shellfish farm- try are Whiskey Creek Shellfish Hatchery cohorts. The industry has capitalized on ing supports over $270 million in eco- (Netarts Bay, OR), Taylor Shellfish this by forging relationships with phys- nomic activity and over 3,000 family Hatchery (Dabob Bay, WA), and Coast iologists and geneticists to determine wage jobs in rural areas throughout the Seafoods Hatchery (Quilcene Bay, WA). the mechanisms behind larval mortality region. Although shellfish farms can be These hatcheries combine with smaller events and develop long-term strategies found throughout Oregon, Washington, hatcheries in Washington and Hawaii to adapt to further declines in water qual- Alaska, California, and Hawaii, most to produce 40–60 billion eyed larvae ity predicted for the coming decades. of the oysters harvested in the Pacific each year, and their 30 years of consis- More importantly, the shellfish farm- Northwest are produced in Washington. tent production has helped build today’s ing industry has become a catalyst for Large farms in Willapa Bay and southern $270 million per year shellfish industry change. The partnerships industry mem- Puget Sound make up the majority of the (http://pcsga.org/shellfish-initiative). bers have developed with the scientific industry, and have existed in these areas community helped shift the focus of OA for several generations (http://pcsga.org/ Hatchery Failures research from oceanic to coastal environ- shellfish-initiative). High levels of larval mortality at the ments, where there are many additional Shellfish species farmed in the Whiskey Creek Shellfish Hatchery began drivers and more complex natural tempo- Pacific Northwest include Manila clams in July 2007 and persisted to the end of ral patterns (Hinga, 1992; Frankignoulle (Venerupis philippinarum), geoduck clams the growing season in October. Some et al., 1998; Ringwood and Keppler, 2002; (Panopea generosa), mussels (Mytilus month-to-month variability in hatch- Wootton et al., 2008; Juranek et al., 2009; trossulus and M. galloprovincialis), and ery production is normal, but the magni- Hofmann et al., 2010; Alin et al., 2012; several species of oysters. Although tude and duration of the 2007 mortality Harris et al., 2013; Feely et al., 2012a; Kumamoto oysters (Crassostrea sikamea), events were unprecedented in the hatch- Waldbusser and Salisbury, 2014). In eastern oysters (Crassostrea virginica), ery’s 30-year history. Hatchery manag- addition, the shellfish industry’s chal- and the native Olympia oyster (Ostrea ers initially attributed the mortality to a lenges helped refocus OA management conchaphila) represent important niche large bloom of Vibrio tubiashii in Netarts away from solely pursuing global carbon markets, the Pacific oyster (Crassostrea Bay, a bacterium pathogenic to oyster lar- reduction, and encouraged managers to gigas) is the predominant species farmed vae (Elston et al., 2008). However, larval pursue actions that can be taken locally in the region, comprising >80% of the mortality persisted even after success- to mitigate OA effects on coastal waters industry’s total annual shellfish produc- ful elimination of the pathogen, forcing throughout the Pacific Northwest (Kelly tion by live weight (Table 1). managers to search for another explana- et al., 2011; Washington State Blue Ribbon Pacific oysters from Japan were first tion for the die-offs. Panel on Ocean Acidification, 2012). In brought to the United States in the early By early summer of 2008, hatchery per- 2013, Washington became the first state twentieth century, and naturalized popu- sonnel shifted their focus away from bio- to develop a comprehensive management lations became established in portions of logical pathogens and for the first time strategy to protect its resources from Puget Sound and in Willapa Bay. Natural began investigating seawater chemis- OA effects, largely in response to con- recruitment of seed oysters from these try as a potential explanation for the per- cerns raised by the shellfish industry. This spawning populations helped support the sistent summertime mortality events. A paper describes the factors that drew the industry for several decades, supplement- large mortality event in July 2008 trig- shellfish industry into this issue; how the ing the supply of imported seed from gered these investigations, which coin- partnerships established among industry, Japan. In the 1970s, the cost of importing cided with a large upwelling event along

148 Oceanography | Vol.28, No.2 the Washington-Oregon coast. This growers across the entire West Coast monitoring included continuous mea- strong upwelling event brought seawater shellfish industry. surement of pH, dissolved oxygen, tem- undersaturated with respect to aragonite The annual growers meeting held in perature, salinity, and pressure, as well to the surface and across the continental September 2008 represented an import- as weekly discrete samples for bacteria, shelf into Netarts Bay, and hatchery man- ant turning point for the industry, when nutrient concentrations, and total car- agers recorded pH values as low as 7.6 the keynote speaker, Richard Feely, intro- bonate chemistry. Carbonate chemistry near hatchery intakes. Preliminary exper- duced oyster growers to the potential samples were sent for analysis to the lab- iments conducted in July and August 2008 impacts of OA on shellfish. Combined oratory of author Hales at Oregon State showed a marked improvement in the sur- with preliminary indications from University (http://ceoas.oregonstate.edu/ vival and growth of larval cohorts when Whiskey Creek that acidified seawater profile/hales), establishing an import- pH was adjusted by adding sodium car- played a major role in the hatchery’s pro- ant connection between the shell- bonate, providing the first clear evidence duction problems that summer, the meet- fish industry and the chemical oceano- that carbonate chemistry had affected ing served as a call to action for the entire graphic community. hatchery production. industry, and provided an initial forum Data collected throughout summer These findings came too late in the for researchers, hatchery managers, and 2009 were then correlated against pro- 2008 production season to be of imme- growers to discuss the problem face- duction metrics routinely recorded at the diate commercial benefit, however, and to-face and propose a strategy to better hatchery, and the results showed a clear overall production at Whiskey Creek in understand OA’s impacts on the industry. link between Ωarag and the survival and 2008 was approximately 2.5 billion eyed growth of larval cohorts in the hatch- larvae, about 25% of a normal season’s INSTRUMENTING THE ery. In particular, these data showed production. Whiskey Creek is the pri- HATCHERIES that Ωarag during first-shell develop- mary supplier of larvae to many inde- First Attempts at Monitoring ment (the first 24–48 hours after fertil- pendent growers throughout the Pacific (2009) ization of eggs) was critical to the ulti- Northwest, and the shortage of larvae In spring 2009, Whiskey Creek Shellfish mate survival and growth of larval groups from the hatchery, combined with sev- Hatchery initiated a comprehensive (Figure 1), and Ωarag > 1.7 represented the eral consecutive years of poor natu- water quality monitoring program, “break-even” point for commercial pro- ral recruitment of larvae from spawning funded by the Pacific Coast Shellfish duction at Whiskey Creek (Barton et al., populations in Willapa Bay (Dumbauld Growers Association (PCSGA) and the 2012). These findings offered the first et al., 2011), generated concern among Willapa Bay Reserve Fund. This initial clear evidence of OA impacts on larval

TABLE 1. US West Coast shellfish production estimates for 2009 (the most recent data available) compiled by the Pacific Coast Shellfish Growers Association (PCSGA). Shellfish sales are divided by species and by state, and when available, total sales are shown both by live weight and economic value. Data for this table were compiled by Ted Kuiper and Jim Gibbons.

Oysters Clams Mussels Geoduck All Shellfish Total Current* Current* Current* Current* Larvae and Seed Current Pounds 61,000,000 9,520,000 2,750,000 1,650,000 74,920,000 Washington Sales $57,750,000 $19,550,000 $3,162,500 $20,100,00 $7,000,000 $107,562,500 Pounds 9,270,995 741,463 315,000 10,327,458 California Sales $12,361,326 $830,000 $945,000 $2,300,000 $16,436,326 Pounds 2,379,988 2,379,988 Oregon Sales $2,253,135 $750,000 $3,003,135 Pounds 206,709 7,839 1,988 216,536 Alaska Sales $441,781 $24,841 $6,610 $126,000 $599,232 Pounds 72,857,692 10,269,302 3,066,988 1,650,000 87,843,982 Total Sales $72,806,242 $20,404,841 $4,114,110 $20,100,000 $117,425,193

*All pounds converted to live weight/in the shell Compiled by the Pacific Coast Shellfish Growers Association. All production data represent most recent info available from: Alaska Dept of Fish and Game (2009) Oregon Dept of Agriculture (2009) Powell, Seiler and Co, Certified Public Accountants for Willapa (2008) Shellfish companies in California (2008) and Washington (2008, 2009)

Oceanography | June 2015 149 organisms in the natural environment spawning to coincide with afternoon important to seed production and, ulti- under naturally fluctuating conditions photosynthetic activity, which raised mately, to the economic resiliency of the that have been magnified by increasing saturation states outside the hatchery. Pacific Northwest shellfish industry; and atmospheric CO2 (Barton et al., 2012; Although not a perfect strategy, manag- (2) simple pH measurements are inade- Waldbusser et al., 2013). ers saw immediate improvements in the quate for developing a full understanding Subsequent research confirmed that survival and growth of larval cohorts, of the impacts of shifting carbonate chem-

Ωarag values significantly >1.0 are required and using real-time monitoring to “pick istry on larvae, and measurement of Ωarag to support proper development of their moments” allowed Whiskey Creek is necessary for determining the impact Pacific oyster larvae (Barton et al., 2012; to significantly improve summertime of water chemistry on the initial devel- Waldbusser et al., 2013, 2015). Pacific oys- larval production in 2009 and 2010. In opment and ultimate survival of oyster ter larvae develop from an egg (0% shell) 2011, large-scale buffering systems were larvae (Waldbusser et al., 2013, 2015). to D-hinge oyster larvae (~80% shell) installed in Whiskey Creek Hatchery, In the winter of 2009–2010, PCSGA in a period of less than 24 hours (and it and in 2012, hatcheries shifted produc- growers submitted a proposal to Senator appears to be closer to a six-hour window; tion cycles earlier in the year to increase Maria Cantwell’s (WA) office, request- Waldbusser et al., 2015), representing a seed production before upwelling begins. ing funds to build a monitoring network tremendous energetic bottleneck due to in areas of commercial importance to the rapid rate of calcification (Waldbusser Development of the Pacific the industry. This proposal stressed the et al., 2013). During this rapid shell devel- Coastal Shellfish Growers immediacy of the industry’s seed sup- opment, analysis of stable C isotopes Association Monitoring Program ply problems, and the potential for high-​ indicates that the shell is precipitated in Whiskey Creek’s initial success with resolution, real-time data to improve seed greater contact with surrounding water, water quality monitoring in 2009 pro- supply for the entire industry. With Senator increasing susceptibility to ambient water duced two important findings for the Cantwell’s support, National Oceanic and saturation state (Waldbusser et al., 2013; entire shellfish industry: (1) understand- Atmospheric Administration (NOAA) Figure 2). Recent experiments show that ing, and adapting to, water chemistry funds were allocated in early 2010, and

Ωarag, not pH or pCO2, is the primary in commercial hatcheries is extremely PCSGA monitoring stations were quickly variable impacting larval development and growth(A) during these early stages (B)

(Waldbusser1.5 et al., 2015). )

–1 1,024 Knowing that the first two days of 10 1.0 development are critical to the survival 5 1,020 0 of larval0.5 groups, managers timed their 1,016 –5 Pressure (hPa) 0.0 –10 1,012 (A) N Wind Velocity (m s 34 (B) 18 –0.5 33 1.5 ) 16 –1 1,024 1032 Relative Larval Producation –1.0 31 14 1.0 5 1,020 30 –1.5 Salinit y 12 290 0.50.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 1,016 28–5 10 Temperature (° C) Ωarag in Initial Water Pressure (hPa) 0.0 –1027 1,012

N Wind Velocity (m s 8.234 18 –0.5 33 16 8.032 SW S

Relative Larval Producation –1.0 31 14 pH 7.8 30 –1.5 Salinit y 12 29 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 7.6 28 10 Temperature (° C) Ω in Initial Water 3.0 arag 27 2.5 FIGURE 1. (A) Relative production of Pacific Oyster larvae at the 8.2

Netarts Bay Whiskey Creek Shellfish Hatchery as a function of ara- arag 2.0 Ω gonite saturation state (Ωarag). (B) Wind speed, atmospheric pres- 8.0

SW S 1.5 sure, salinity, temperature, pH, and aragonite saturation state in Netarts Bay during summer 2009. The solid red line shows the pH 1.07.8 threshold aragonite saturation state for no viable commercial pro- duction. After Barton et al. (2012) 7.6 160 170 180 190 200 210 3.0 Day of Year 2009 2.5 150 Oceanography | Vol.28, No.2 arag 2.0 Ω 1.5 1.0

160 170 180 190 200 210 Day of Year 2009 established to characterize water chemis- systems was installed at Whiskey Creek and Taylor Shellfish hatcheries (and for try at Whiskey Creek Shellfish Hatchery, in April 2010, and by spring 2011, sen- growers utilizing monitoring data to Taylor Shellfish Hatchery, the Lummi sors were operational at Taylor Shellfish improve commercial sets), the PCSGA Nation Shellfish Hatchery, and at three Hatchery and in Willapa Bay, with sup- Monitoring Program put the proverbial sites in Willapa Bay (Tokeland, Bay plementary funding from the Educational “headlights on the car.” Access to real- Center, and Nahcotta) (Figure 3; Table 2). Foundation of America (EFA). time carbonate chemistry data provides These funds allowed PCSGA to expand The ability to observe carbonate chem- a clear connection between OA and lar- the model originally adopted at Whiskey istry data in real time has fundamentally val mortality as well as an explanation Creek, and continuous data (pH, tem- altered the way shellfish hatchery manag- for the recent decline in commercial perature, salinity, and dissolved oxygen) ers view seawater chemistry in the Pacific larval production. from the monitoring sites were combined Northwest. The data streams generated with routine discrete sampling for bacte- at commercial hatcheries and distrib- Turning on the High Beams: ria, nutrient concentrations, and total car- uted through the US Integrated Ocean Interactions with C-CAN, bonate chemistry. The award also sup- Observing System (IOOS) regional the Burke-O-Lator 3000, and ported construction of three continuous Northwest Association of Networked New IOOS Sensor Development

(1 Hz) pCO2 monitoring systems that Ocean Observing Systems (NANOOS) Although real-time measurement of were designed and constructed at Oregon data portal serve as an important man- pCO2 provided essential data to commer-

State University (http://ceoas.oregonstate. agement tool for growers throughout cial hatchery managers, pCO2 is, like pH, edu/profile/hales). The first of these the industry. For both Whiskey Creek a proxy for seawater Ωarag, the parameter

Recovery from early development Preparation for at e

R metamorphosis and n

o settlement ti Embryological a c

fi &Prodissoconch I i c

a l shell development C

) % (

s d i p i L

n o b

l a r l C e

h c i S

n a n i g r o n I

Calcification initiated D-Hinged Energetic low Seed size ( 4-8 days) (~10 hrs) Feeding initiated (~16 hrs) ~ (~2-3 weeks)

~3 hours ~10 hours ~14 hours ~16 hours ~48 hours ~8 days ~16 days FIGURE 2. Trends in relative biochemistry and shell morphology in Pacific oyster larvae raised in the Whiskey Creek Shellfish Hatchery. Bottom axis is time on a nonlinear scale, relating to stages of larval ontology from hours after fertilization to settlement two to three weeks later. Shell diameters in scanning electron microscope images increase from ~75 mm to ~320 mm at settlement size. Panels for calcification rate, % lipids, and inorganic carbon in shell are in relative scales to highlight the changes occurring in the early shell development stage (yellow), when the primary energy source is mater- nally derived lipids. During this initial period, there is high incorporation of seawater inorganic carbon and high sensitivity to saturation state effects. Even if larvae manage to develop under moderate saturation state stress, they are smaller at the completion of this period (Waldbusser et al., 2015), and fewer proceed to metamorphosis (Barton et al., 2012).

Oceanography | June 2015 151 most closely associated with initial shell to valuable commercial fisheries across This workshop ultimately resulted formation and survival of oyster lar- the Pacific Northwest and the need for in formation of the California Current vae (Waldbusser et al., 2015). Gaining a a coordinated regional approach to the Acidification Network (C-CAN), true understanding of carbonate chem- problem. The workshop led to a partner- a unique partnership dedicated to: istry variability and its effects on shell- ship among these groups and recognition (1) encouraging development of an OA fish larvae therefore required another that coastal zone acidification represents monitoring network for the West Coast, technological leap forward for both new scientific and management chal- (2) understanding the linkages between the shellfish industry and the chemical lenges compared to acidification stud- oceanographic conditions and biological oceanographic community. ies in the open ocean. Until then, lim- responses, (3) encouraging development A workshop held in Costa Mesa, CA, ited work on OA had been conducted in of causal, predictive, and economic mod- in July 2010 facilitated this next step, nearshore environments (e.g., Ringwood els that characterize these linkages and and concern from shellfish growers and and Keppler, 2002: Green et al., 2009), forecast effects, and (4) facilitating com- wild harvest fisherman alike helped bring with most oceanographic research munication and resource/data sharing together a diverse group of scientists, focused on decadal-scale changes in the among the many organizations that par- shellfish industry representatives, com- open ocean (Feely et al., 2008, 2012b). ticipate in C-CAN in collaboration with mercial fishermen, and resource manag- The workshop illustrated that coastal US IOOS (http://c-can.msi.ucsb.edu). ers from local, state, federal, and tribal effects operate around tidal, diurnal, In subsequent workshops, C-CAN groups (Southern California Coastal and seasonal patterns that were not well helped define the parameters most Water Research Project, 2010). These understood, requiring additional mon- important to monitor in coastal sys- parties recognized the threat OA poses itoring and analysis. tems and developed a detailed set of Core Monitoring Principles (McLaughlin et al., 2015, in this issue) to help indus- try representatives obtain research qual- ity data from their monitoring systems. A major outcome of these workshops was definition of a benchmark that requires

Ωarag to be measured within ±0.2 in order to be biologically relevant, based on vari- ance often seen in experimental stud- ies of species responses. Although this level of accuracy is generally attainable in open-ocean systems, the complexi- ties of dynamic coastal estuaries make it a more challenging task in these envi- ronments (Feely et al., 2010; Harris et al., 2013). C-CAN’s Core Monitoring Principles provide specific direction to assist industry personnel in optimiz- ing data quality, including recommen- dations on available instrumentation, protocols for proper calibration of equip- ment, and recommendations for routine Quality Assurance/Quality Control with outside laboratories. Additionally, C-CAN provided a forum for face-to-face interactions between FIGURE 3. Monitoring sites established in 2011 by the Pacific Coast industry personnel and researchers and Shellfish Growers Association (PCSGA). Main map: LSH = Lummi Shellfish extended these interactions beyond the Hatchery, Bellingham, WA. TSH = Taylor Shellfish Hatchery, Dabob Bay, WA. hatcheries to a wider audience of shell- WCSH = Whiskey Creek Shellfish Hatchery, Netarts Bay, OR. Inset of Willapa Bay: TK = Tokeland. BC = Bay Center (Ekone Oyster Co.). NC = Nahcotta (Jolly Roger fish growers and commercial fishermen. Oyster Co). Three new sites were added in 2014, in Alaska and California, as part- These conversations allowed growers nerships between shellfish growers and NOAA, and additional sites are planned. throughout the industry to obtain a basic

152 Oceanography | Vol.28, No.2 TABLE 2. Summary of monitoring sites of the Pacific Coast Shellfish Growers Association, insights gained from monitoring, and associated mitigation strategies.

Site Location Site Characteristics Insights Gained from Monitoring Mitigation Strategies Buffered tanks using sodium carbonate

Increased frequency of spawning Identified large-scale shifts in immediately after strong north winds seawater chemistry associated with began (because 24–48 hours of the intrusion/relaxation of upwelled sustained north winds are required seawater into Netarts Bay (2009) to advect upwelled water across the Oregon continental shelf and into Netarts Bay) to create large groups of larvae prior to intrusion of Whiskey Creek is a shallow (< 10 m upwelled water into Netarts Bay deep), largely oceanic bay with little Whiskey freshwater input Revealed large diel pH/O variability 2 “Picked their moments” to utilize Creek Netarts Bay, associated with photosynthetic afternoon (high pH, high O ) water Shellfish OR Strongly influenced by offshore activity of eelgrass and algae in 2 for spawning Hatchery conditions including direct intrusions the bay (2009) and the estuary’s of high salinity (>33 ppt) upwelled dynamic responses to these forcings water during summertime Provided hatchery with an understanding of how carbonate Shifted production season earlier chemistry and oxygen levels evolve each year to place less reliance in the bay throughout the growing on late season (August–October) season. Conditions deteriorate in production late summer/fall due to prolonged periods of upwelling and associated Refined treatment systems to oxidize decomposition of high volumes of incoming seawater Additional work organic matter, both within Netarts is required to address late season Bay (eelgrass, etc.) and offshore over conditions at the hatchery the Oregon continental shelf Monitoring revealed a marked Provided an explanation for poor difference in pCO concentrations 2 survival commonly observed when from shallow (5–15 m) and deep deep water was used for rearing Dabob Bay is a deep (>100 m) bay (100 m) water intakes at the hatchery. oyster larvae (Figure 4) off Hood Canal Deep water has persistently high Taylor pCO2 (generally >800 µatm) Dabob Bay, Strongly influenced by local Shellfish WA processes within Hood Canal due to Monitoring revealed that periodic, Hatchery wind-driven mixing of the entire long residence times once offshore Developed treatment systems similar water column in Dabob Bay leads water intrudes into the canal over a to those at Whiskey Creek to buffer to a significant increase in the pCO shallow (~25 m) sill at Admiralty Inlet 2 and improve oxidation state of water of surface waters outside the incoming seawater hatchery, with potential negative impacts on larval production Willapa Bay is a large coastal Growers use real-time data from Monitoring has shown that Ω bay with long residence times in arag NANOOS to time filling of setting during the summer often falls the southern portion of the bay tanks well below the optimal threshold (Banas et al., 2007) and significant (of Ω > 1.7) for larval development freshwater input from coastal rivers, arag Some farms are now buffering Bay Center which may complicate or overwhelm setting tanks with carbonate As OA advances in coming decades, the signal from an offshore the window of opportunity for upwelling event After seven to eight years of sub- Willapa Bay, spawning events to coincide with Nahcotta par commercial sets (recruitment of WA favorable water chemistry will Unlike hatcheries, larvae in the naturally occurring larvae to shell continue to shrink (Rykaczewski and natural environment face wide bags placed in the bay (Dumbauld Dunne, 2010; Gruber et al., 2012; Tokeland variations in temperature, salinity, et al., 2011), many growers who relied Hauri et al., 2011, 2013; recent work and food availability, and any of on natural spawning events to seed of author Hales and colleagues), these factors may play important their farms for decades have instead adding a significant stressor to the roles in determining the success begun purchasing shell bags seeded list of factors impacting the survival or failure of a larval cohort with hatchery larvae, increasing of shellfish larvae in natural systems (Ruesink et al., 2003) overall demand for larvae Monitoring has revealed significant The Lummi hatchery draws seawater The pond may act as a buffer/ Lummi Bellingham, differences between pond water and from a large (700 acre) sea pond off refuge against extreme events in the Hatchery WA waters of the outer sound, where Puget Sound surrounding ocean conditions are more variable

Oceanography | June 2015 153 understanding of how carbonate chemis- Ωarag can be calculated from any two of recorded simultaneously. Although pH sen- try is measured and how those measure- four measurable parameters in the carbon- sors are readily available, many are unable ments can be used to calculate Ωarag, the ate system (pH, pCO2, total alkalinity, and to achieve the level of precision required quantity of interest to shellfish farmers. dissolved inorganic carbon [DIC]), if they to calculate Ωarag within ±0.2; selection of These discussions helped greatly in refin- are measured within a required level of pre- appropriate pH sensors, along with proper ing the direction of PCSGA’s monitoring cision and accuracy, and if accurate tem- calibration, is therefore essential if they are effort, and can be summarized as follows: perature and salinity measurements are to be used in calculating Ωarag. Instruments

to measure pCO2 are costly, but are com-

mercially available, making pH and pCO2 an obvious pair of parameters for shell-

fish growers to use in calculating Ωarag.

However, pH and pCO2 covary and can both be highly dynamic in coastal systems, introducing error into the calculation of

Ωarag. Therefore, it is preferable to use one of these quantities, paired with either DIC or total alkalinity (both of which are less variable in coastal environments), to have

the best chance of reliably measuring Ωarag in coastal bays and estuaries.

Following C-CAN advice, PCSGA monitoring stations upgraded their pH sensor technology after the 2010 work-

shop. Combined with the pCO2 sen- sors installed at Whiskey Creek, Taylor Shellfish Hatchery, and in Willapa Bay, growers were for the first time able to

generate real-time Ωarag estimates, albeit

from measurements of pH and pCO2 only (or through use of emerging relationships between total alkalinity and salinity). At the same time, the shellfish indus- try began working toward measur-

ing DIC and pCO2 in near-real time to obtain the best possible measurement

of Ωarag. Using funds provided under the NOAA/Cantwell award, Oregon State University oceanographers modi-

fied the existing pCO2 monitoring sys- tem at Whiskey Creek into a combined

pCO2/tCO2 system, and by the end of 2013, the Burke-O-Lator 3000 emerged as a robust sensor for real time calculation of

Ωarag, capable of meeting the C-CAN pre- cision standard of ±0.2 for extended peri- FIGURE 4. Pacific oyster larvae from the same spawn, raised by the Taylor Shellfish Hatchery in nat- ods of continuous use. The robustness ural waters of Dabob Bay, WA, exhibiting favorable (shallow intake, left column, pCO2 = 403 ppm, of this system stems largely from recog- Ωarag = 1.64, and pHT = 8.00) and unfavorable (deep intake, right column, pCO2 = 1418 ppm, nizing that sensors will ultimately fail in Ωarag = 0.47, and pHT = 7.49) carbonate chemistry during the spawning period. Scanning Electron Microscopy (SEM) images show representative larval shells from each condition at one, two, and dynamic coastal environments. Therefore, four days post-fertilization. Under more acidified conditions, shell development is impaired; arrows rather than relying solely on measurement show defects (creases) and features (light patches on shell) suggestive of dissolution. of pCO2 and DIC to calculate Ωarag, the

154 Oceanography | Vol.28, No.2 Whiskey Creek system also measures pH Dubbed “turning the headlights on high,” exposed to artificially acidified conditions using a Durafet III sensor, ensuring that this project seeks to improve and institu- in laboratory trials but rather showed OA three of the four parameters in the carbon- tionalize the partnerships and successes impacts when grown in seawater drawn ate system are measured continuously. In to date, while commercializing a more directly from Netarts Bay (Barton et al., addition, five years of routine data collec- stable and less costly pCO2 sensor desired 2012). Such collaborative work illustrates tion at Whiskey Creek have provided suf- by shellfish growers. the role that the PCSGA Monitoring ficient data for oceanographers to define Program can play in engaging research- the local relationship between total alka- EXPANDING THE PARTNERSHIP ers to work in important shellfish grow- linity and salinity, allowing salinity to be WITH OA SCIENTISTS ing areas and the mutual benefits to all used a proxy measurement for alkalinity. The PCSGA Monitoring Program’s insis- parties as they attempt to understand, Thus, the carbonate system can be fully tence on a high level of precision has and adapt to, coastal acidification in the constrained at Whiskey Creek. had an immediate synergistic effect. Pacific Northwest. This oversampling allows for calcula- When researchers developed the capa- Similar partnerships have devel- tion of Ωarag from several different pairs of bility to actively monitor time series and oped between researchers and shellfish carbonate system measurements, which maximize the overall quality of the data growers throughout Washington State. can be compared against one another. stream, the monitoring program became The relocation of a NOAA buoy within Currently, the Whiskey Creek system is not only a sophisticated tool for helping Dabob Bay to waters adjacent to Taylor capable of calculating, and displaying in shellfish hatcheries but also a resource Shellfish Hatchery represents an exam- real time, five calculated values for Ωarag for high quality, publishable carbonate ple of the responsiveness of NOAA and

(from pH/DIC, pCO2/DIC, pCO2/TA, chemistry data from coastal locations University of Washington researchers to

DIC/TA, pH/pCO2). By adding the capa- previously undocumented in efforts to the needs of shellfish growers and the bility for remote access to the system, the monitor the coastal ocean. mutual benefits of comparing buoy data Hales laboratory can view data, make These data are particularly valuable to instrumentation at the hatchery. These adjustments as needed, and quickly iden- for quantifying the impacts of OA on industry/research partnerships have tify the need for system maintenance if coastal estuaries throughout the Pacific spawned research in additional shellfish any discrepancies arise between the inde- Northwest because the chemical moni- growing areas important to the industry pendent calculations of Ωarag. toring stations were co-located with bio- (http://www.pacshell.org/about-us.asp; This capability is key to the success logical monitoring systems (i.e., hatchery http://www.ocean.washington.edu/home/ of any monitoring partnership between production records; Table 2). This co- Simone+Alin), and helped identify shellfish growers and oceanographers. location allowed researchers to develop a potential sites for future expansion of the Most growers lack the familiarity with better understanding the response of biota monitoring network. carbonate chemistry to identify errors to the chemical parameters and at what in a time series quickly, and budgetary thresholds. Moreover, the continuous Making Data Available to the constraints limit the amount of time that chemistry data helped refine laboratory- Larger Community Through researchers can spend traveling to and based acidification exposure studies. Interactions with NANOOS from commercial hatcheries. Remote Whereas most physiological experiments Early on in the development of the access to the data allows researchers prior to that time focused on changes in PCSGA Monitoring Program, the shell- to identify sensor failures quickly and steady-state conditions, as might occur fish industry began to interact with deploy technicians as needed to optimize in the open ocean, the new temporally IOOS, and in particular with NANOOS, the overall quality of the time series. intensive data provided information on the regional IOOS authority responsible A newly awarded grant from US IOOS episodic exposures relating to the diur- for the Pacific Northwest. NANOOS rec- and the NOAA OA Program’s “Ocean nal and tidal changes encountered by ognized the potential value of PCSGA’s Technology Transition” competition will biota in nearshore habitats. program in monitoring coastal locations allow the Hales laboratory to develop As an example, the work conducted not previously represented in the larger new lower cost and higher accuracy at Whiskey Creek by researchers from effort to monitor ocean conditions in the pCO2 sensor technology for OA mon- Oregon State University has greatly Pacific Northwest, and became an essen- itoring, with expansion to new sites as increased scientific understanding of tial partner in the effort to display these advised by PCSGA. It will also strengthen early shell formation in Pacific oyster lar- data streams online. existing regional partnerships through vae (Waldbusser et al., 2013), in addition The shellfish industry is very inter- IOOS regional associations along the to providing valuable insights to hatchery ested in sharing data online so that it is Pacific coast to implement and provide managers (Figures 2 and 3). Importantly, accessible to as many growers as pos- quality-assured tests of the new sensors. the larvae used in these studies were not sible. In areas like Willapa Bay, coastal

Oceanography | June 2015 155 monitoring has become a valuable tool DEVELOPMENT OF collaboratively with Whiskey Creek, for growers with commercial setting sta- COMMERCIAL-SCALE and ongoing research at MBP contin- tions because it helps them maximize the TREATMENT SYSTEMS IN ues to inform treatment system devel- quality of water used to fill setting tanks. HATCHERIES opment at both Whiskey Creek and This can have dramatic impact on setting Research at Whiskey Creek Shellfish Taylor Shellfish hatcheries. success and seed survival, and ultimately, Hatchery has identified Ωarag >1.7 as the Although buffering systems have the “bottom line” for shellfish growers. minimum threshold for development greatly improved production at Whiskey The partnership with NANOOS makes of commercially viable larvae groups Creek, they are insufficient to completely these data widely available to growers (Barton et al., 2012), although higher sat- repair water chemistry issues impacting throughout the Northwest, as well as to uration states are preferred by hatchery commercial hatcheries. Just as OA affects the scientists involved. managers. Monitoring at Whiskey Creek larvae in the hatchery setting, it also has

Based on the success of the PCSGA has shown that Ωarag now rarely exceeds a potential impact on biology in coastal Monitoring Program, the NOAA Ocean this minimum threshold throughout waters throughout the Pacific Northwest Acidification Program (OAP) subse- the growing season, although nearshore (Bednaršek et al., 2014). The link quently worked with IOOS to provide California Current waters were likely at between persistent summertime upwell- three new pCO2/DIC combined sys- least 0.5 units higher prior to large-scale ing and low oxygen/high carbon dioxide tems, which were recently installed in CO2 emissions from fossil fuels (Harris regions over the inner continental shelf California and Alaska. These instru- et al., 2013). Even in the spring, before has been well documented (Hales et al., ments significantly increase the number the summertime upwelling season, 2005, 2006; Chan et al., 2008; Feely et al., of shellfish growing areas represented in Ωarag is less than optimal, and the hatch- 2008). These oceanic waters are advected coastal monitoring programs and greatly ery has responded by installing chemi- into the many small estuaries along the extend the geographic extent of near- cal buffering systems that modify Ωarag Pacific Northwest coast and can result in shore carbonate chemistry monitoring in in the hatchery year-round. These sys- decreased estuarine oxygen conditions the Pacific Northwest. These data should tems have been quite effective, restor- (Brown and Power, 2011). In Netarts Bay, enhance understanding of OA impacts on ing 30–50% of productivity lost in pre- local natural processes add to the oceanic coastal estuaries throughout the region. vious seasons and resulting in billions signal, and as large amounts of seagrass In 2013, a Blue Ribbon panel of experts of additional eyed larvae supplied to and benthic micro- and macro-algae gen- in Washington State recommended that growers each year. Discovering the link erated through the summer season begin the state provide funding to continue between acidification and seed produc- to decay in August–October each year, the PCSGA Monitoring Program and tion, and installation of buffering sys- carbon dioxide is increased and oxy- provided a detailed set of recommen- tems to correct the problem, has kept the gen decreased. Although there was no dations to combat OA at the state level hatchery in business, maintaining seed regular water chemistry monitoring in (Washington State Blue Ribbon Panel on supply to dozens of growers in Oregon, Netarts Bay prior to 2009, conditions at Ocean Acidification, 2012). The result- Washington, and California. the hatchery were historically conducive ing funding, along with an Oregon leg- Commercial treatment system devel- to larvae growth in September and early islature award to support monitoring at opment at Whiskey Creek has ben- October. Since 2007, however, September Whiskey Creek, ensures that the mon- efited greatly from close collabora- and October have been characterized by itoring network will continue to pro- tion with Chris Langdon and the poor water quality in the bay, forcing an vide essential information to the shellfish Molluscan Broodstock Program (MBP) early end to the growing season. industry. This funding also supported at Oregon State University’s Hatfield Treatment systems designed to com- an upgrade of the existing pCO2 mon- Marine Science Center in Newport, bat these secondary effects of OA have itoring system at Taylor Shellfish to a OR (http://fw.oregonstate.edu/content/ met with some limited success and are system capable of measuring pCO2 and chris-langdon). MBP has been an indus- undergoing further development both DIC. The improvement in data quality try partner since its inception in 1996, at Whiskey Creek and at Taylor Shellfish should facilitate better collaboration, as developing high-yield Pacific oyster Hatchery. However, shellfish growers both hatcheries attempt to understand, stocks for industry use. To produce these throughout the Pacific Northwest have and mitigate, OA effects on commercial stocks, MBP operates a small research much more work ahead to first under- production. The new IOOS-OAP award, hatchery in Yaquina Bay, where pro- stand, and then correct, the late sea- leveraged with support from Washington duction failures began as early as 2005, son deterioration of water conditions and Oregon state funds, should extend prior to the major production fail- in coastal bays. the monitoring effort at least several ures first observed at Whiskey Creek years into the future. in 2007. Since 2007, MBP has worked

156 Oceanography | Vol.28, No.2 LONGER-TERM STRATEGIES than sites in the Pacific Northwest. OA is a seed mortality in commercial nurser- TO COMBAT THE IMPACTS OF global problem, however, so these efforts ies become more widespread each sea- COASTAL OA ON THE INDUSTRY at best represent a short-term solution to son and are likely related to the challeng- Selective Breeding for carry the industry forward for the next ing conditions seed experience once they OA Tolerance few decades. Shellfish growers are aware leave the protected waters of commer- One strategy to combat the advance- of this fact, and the sheer amount of cap- cial hatcheries. While building capacity ment of OA in the Pacific Northwest ital investment going into these adap- for buffering of remote setting tanks at involves the use of selective breeding to tation strategies speaks volumes about commercial farms should provide some develop resistant stocks. Selective breed- the level of concern felt among growers resiliency, as early post-metamorphic ing of Pacific oysters in the Northwest throughout the Northwest. stages of bivalves appear to be more sen- began in 1996 with creation of the MBP. sitive to acidification than later juveniles Selected broodstock, from both MBP EMERGENCE OF THE SHELLFISH (Waldbusser et al., 2010), at some point and industry-​based breeding programs, INDUSTRY AS A SPOKESGROUP demands for algal production and infra- is now commonly used in commercial FOR THE EFFECTS OF OA ON structure require out-planting. The Pacific hatcheries. Although these existing stocks THE COASTAL OCEAN Northwest shellfish industry cannot treat were not specifically selected for OA Shellfish growers are, by definition, envi- the entire coastal ocean, and the general resistance, they have been reared in the ronmentalists, because their livelihood deterioration of coastal water quality is a coastal waters of the Pacific Northwest depends entirely on the health of the pressing concern for the entire industry. for four to five generations and may have coastal ocean. However, a cross section of Growers understand that development developed some natural resistance to oyster farmers is unlikely to reveal a num- of treatment systems and new hatchery acidification stress. At Whiskey Creek ber of outspoken environmental activists. capacity are only stopgap measures, and Shellfish Hatchery, managers have elected Rather, the industry is typified by ded- the only real solution to OA is to address to use only MBP-selected broodstock, icated businessmen who would much its causes. This puts shellfish farmers in based on anecdotal evidence that these rather put their heads down and work a unique position, as business owners stocks perform better even in early larval than participate in environmental advo- depend on fossil fuels to maintain their stages. Ongoing research, supported by cacy. However, OA has leapt suddenly out livelihood, yet also heavily depend on both the Oregon and Washington legisla- of hypothetical discussions for the future the health of the coastal ocean to pro- tures, is specifically focused on selecting and into the day-to-day life of shell- duce sensitive shellfish species. A visit stocks that perform well when exposed fish growers—who now recognize a very to any shellfish hatchery in the Pacific to reduced saturation state, with particu- clear and immediate threat to their indus- Northwest will reveal thousands of gal- lar emphasis on exposing oysters to low try and possess a fairly advanced level of lons of diesel or propane fuel on site,

Ωarag in early larval stages. These breeding understanding of acidification and the used to heat seawater for larvae produc- efforts are unlikely to identify larvae that coastal processes affecting it (Mabardy, tion. Hatchery managers work within a are totally resistant to OA, but the exist- 2014). A recent survey found that over paradox of simultaneously releasing CO2 ing gene pool may produce larvae with 50% of the those in the West Coast indus- into the atmosphere, which exacerbates some tolerance, representing another try have personal experience with effects OA, and adding carbonate to seawater to valuable tool for hatcheries to employ in of OA, and 75% were very or extremely repair it. However, the fact that shellfish combating acidification impacts on com- concerned about OA (Mabardy, 2014). growers live and work in the real, fossil- mercial larval production. There is hope among the industry, how- fuel-dominated world makes the indus- ever, in that 59% of respondents indi- try an important voice in the discussion Expansion of Hatchery cated they believed they were definitely to slow the advance of OA worldwide. Capacity in Locations Outside or somewhat able to adapt to OA. Industry representatives now devote a the Pacific Northwest The direct effects of OA on shell- great deal of time and energy to discuss- Another strategy adopted by the shellfish fish larval shell formation are troubling ing coastal OA’s impacts on the Pacific industry to deal with OA in the Pacific to shellfish growers, wild harvest fisher- Northwest shellfish industry (Bill Dewey, Northwest involves expansion of exist- men, and to many other groups con- Taylor Shellfish Farms, pers. comm., ing hatchery facilities and construction cerned about the health of shell-forming December 4, 2014). Industry involve- of new facilities in remote locations. In organisms. However, the more com- ment has helped expand the discus- particular, hatchery operations in Hawaii plex, and indirect, effects of OA on the sion of acidification management from have expanded dramatically in the past general health of coastal systems are the single issue of global carbon reduc- three to four years, with the hope that even more disconcerting to the Pacific tion to include practical actions that can these sites will be less impacted by OA Northwest shellfish industry. Reports of be taken at the local level to reduce and

Oceanography | June 2015 157 mitigate acidification effects. These local the importance of coastal monitoring to West Coast Dumbauld, B.R., B.E. Kauffmann, A.C. Trimble, shellfish growers, and their continued support for and J.L. Ruesink. 2011. The Willapa Bay oys- decision makers are fundamentally dif- OA monitoring in the Pacific Northwest. We owe ter reserves in Washington State: Fishery col- ferent entities, with fundamentally dif- special thanks to the Oregon Coastal Caucus, and lapse, creating a sustainable replacement, and Sen. Betsy Johnson, for their tenacious support of the potential for habitat conservation and resto- ferent science questions, than the groups Whiskey Creek Shellfish Hatchery, the Molluscan ration. Journal of Shellfish Research 30:71–83, interested in international-scale discus- Broodstock Program, and the Oregon shellfish indus- http://dx.doi.org/10.2983/035.030.0111. try at large. We would like to recognize Brad Warren, Elston, R.A., H. Hasegawa, K.L. Humphrey, sions of carbon inputs to the atmosphere. Todd Capson, and Amy Grondin from the Sustainable I.K. Polyak, and C.C. Häse. 2008. Re-emergence The direct involvement of shellfish indus- Fisheries Partnership for their role in raising awareness of Vibrio tubishii in bivalve shellfish aquaculture: of OA’s impacts on shellfish in the Pacific Northwest Severity, environmental drivers, geographic try representatives has contributed sig- and for building a bridge between hatchery managers, extent and management. Diseases of Aquatic nificantly to a growing body of literature commercial fishermen, and resource managers across Organisms 82:119–134, http://dx.doi.org/10.3354/ the United States and around the globe. We acknowl- dao01982. that outlines strategies by which man- edge the efforts of Diane Pleschner-Steele and Fabry, V.J., B.A. Seibel, R.A. Feely, and J.C. Orr. 2008. agement actions can be targeted toward Bruce Steele for their role in broadening the discussion Impacts of ocean acidification on marine fauna to include OA’s impacts on valuable wild fisheries, and and ecosystem processes. ICES Journal of Marine reducing the effects of OA at the local in helping to bring together scientists, shellfish grow- Science 65:414–432, http://dx.doi.org/10.1093/ level (e.g., Kelly et al., 2011; Washington ers, commercial fishermen, and resource managers to icesjms/fsn048. form and sustain the California Current Acidification Feely, R.A., S.R. Alin, J. Newton, C.L. Sabine, State Blue Ribbon Panel on Ocean Network (C-CAN). We would like to express thanks M. Warner, A. Devol, C. Krembs, and C. Maloy. Acidification, 2012; Strong et al., 2014). to Bill Robertson (Seattle Aquarium, retired) for his 2010. The combined effects of ocean acidifica- practical insight into the design of commercial scale tion, mixing, and respiration on pH and carbon- Shellfish industry outreach efforts have water treatment systems. We acknowledge funding ate saturation in an urbanized estuary. Estuarine, paired effectively with regional not-for- support from the National Oceanic and Atmospheric Coastal, and Shelf Science 88:442–449, Administration (NOAA)’s Ocean Acidification Program http://dx.doi.org/10.1016/j.ecss.2010.05.004. profit organizations (http://sustainable- and NOAA’s Pacific Marine Environmental Laboratory Feely, R.A., C.L. Sabine, J.M. Hernandez-Ayon, fish.org/global-programs/global-ocean- (PMEL contribution number 4268). D. Ianson, and B. Hales. 2008. Evidence for health), with the primary focus of making upwelling of corrosive “acidified” water onto REFERENCES the continental shelf. Science 320:1,490–1,492, http://dx.doi.org/10.1126/science.1155676. direct contact with shellfish growers and Alin, S.R., R.A. Feely, A.G. Dickson, J.M.Hernández- Feely, R.A., T. Klinger, J.A. Newton, and M. Chadsey. Ayón, L.W. Juranek, M.D. Ohman, and R. Goericke. fishermen, not only in the Northwest but 2012a. Scientific Summary of Ocean Acidification 2012. Robust empirical relationships for esti- in Washington State Marine Waters. NOAA OAR also on the US East Coast and through- mating the carbonate system in the southern Special Report. California Current System and application to out the world. Recent workshops regard- Feely, R.A., C.L. Sabine, R.H. Byrne, F.J. Miller, CalCOFI hydrographic cruise data (2005–2011). A.G. Dickson, R. Wanninkhof, A. Murata, ing the Gulf of Maine, Chesapeake Bay, Journal of Geophysical Research 117, C05033, L.A. Miller, and D. Greeley. 2012b. Global http://dx.doi.org/10.1029/2011JC007511. Mexico, and New Zealand have brought Biogeochemical Cycles 26(3), GB3001, Banas, N.S., B.M. Hickey, J.A. Newton, and http://dx.doi.org/10.1029/2011GB004157. together industry representatives, policy- J.L. Rueslink. 2007. Tidal exchange, bivalve graz- Frankignoulle, M., G. Abril, A. Borges, I. Bourge, ing, and patterns of primary production in Willapa makers, and researchers, and have yielded C. Canon, B. DeLille, E. Libert, and J.M. Theate. Bay, Washington, USA. Marine Ecology Progress 1998. Carbon dioxide emission from similar results: growers and fishermen Series 341:123–139, http://dx.doi.org/10.3354/ European estuaries. Science 282:434–436, meps341123. throughout all these regions are very con- http://dx.doi.org/10.1126/science.282.5388.434. Brown, C.A., and J.H. Power. 2011. Historic and Gaylord, B., K.J. Kroeker, J.M. Sunday, K.M. Anderson, cerned about potential impacts of OA on recent patterns of dissolved oxygen in the J.P. Barry, N.E. Brown, S.D. Connell, S. Dupont, Yaquina estuary (Oregon, USA): Importance of their industry and are universally inter- K.E. Fabricius, J.M. Hall-Spencer, and others. 2014. anthropogenic activities and oceanic conditions. Ocean acidification through the lens of ecolog- ested in the role water quality monitor- Estuarine, Coastal, and Shelf Science 92:446–455, ical theory. Ecology 96:3–15, http://dx.doi.org/​ http://dx.doi.org/10.1016/j.ecss.2011.01.018. ing can play in helping their industry face 10.1890/14-0802.1. Barton, A., B. Hales, G.G. Waldbusser, C. Langdon, Gazeau, F., L.M. Parker, S. Comeau, J.-P. Gattuso, these challenges. In this way, the shell- and R.A. Feely. 2012. The Pacific oyster, W.A. O’Connor, S. Martin, H.-O. Pörtner, and Crassostrea gigas, shows negative correla- fish industry acts as a bridging organi- P.M. Ross. 2013. Impacts of ocean acidifi- tion to naturally elevated carbon dioxide lev- cation on marine shelled molluscs. Marine zation between scientists, policymakers, els: Implications for near-term ocean acidification Biology 160:2,207–2,245, http://dx.doi.org/10.1007/ effects. Limnology and Oceanography 57:698–710, and other stakeholders. By building con- s00227-013-2219-3. http://dx.doi.org/10.4319/lo.2012.57.3.0698. Gordon, D.G., and N.E. Blanton. 2001. Heaven on the sensus among those who work around Bednaršek, N., R.A. Feely, J.C.P. Reum, B. Peterson, Half Shell: The Story of the Northwest’s Love Affair J. Menkel, S.R. Alin, and B. Hales. 2014. Limacina and depend on a healthy ocean for their with the Oyster. Washington Sea Grant, Seattle, helicina shell dissolution as an indicator of declin- WA, and WestWinds Press, Portland, OR. livelihood and the urban diners who con- ing habitat suitability due to ocean acidification Green, M.A., G.G. Waldbusser, S.L. Reilly, K. Emerson, in the California Current Ecosystem. Proceedings sume their products, shellfish growers and S. O’Donnell. 2009. Death by dissolu- of the Royal Society B, http://dx.doi.org/10.1098/ tion: Sediment saturation state as a mortal- can contribute a powerful voice to dis- rspb.2014.0123. ity factor for juvenile bivalves. Limnology and Bednaršek, N., G.A. Tarling, D.C.E. Bakker, S. Fielding, cussions of OA and influence the difficult Oceanography 54:1,037–1,047, http://dx.doi.org/​ E.M. Jones, H.J. Venables, P. Ward, A. Kuzirian, 10.4319/lo.2009.54.4.1037. decisions necessary to halt its advance in B. Lézé, R.A. Feely and E.J. Murphy. 2012. Gruber, N., C. Hauri, Z. Lachkar, D. Loher, Extensive dissolution of live pteropods in the the global ocean. T.L. Frölicher, and G.-K. Plattner. 2012. Rapid pro- Southern Ocean. Nature Geoscience 5:881–885, gression of ocean acidification in the California http://dx.doi.org/10.1038/ngeo1635. ACKNOWLEDGEMENTS. The authors would like current system. Science 337:220–223, Chan, F., J.A. Barth, J. Lubchenko, A. Kirincich, to acknowledge the determination of Robin Downey, http://dx.doi.org/10.1126/science.1216773. H. Weeks, W.T. Peterson, and B.A. Menge. 2008. Bill Dewey, Margaret Barrette, and Connie Smith Hales, B., L. Karp-Boss, A. Perlin, and P. Wheeler, Emergence of anoxia in the California cur- in finding, and maintaining, funding for the PCSGA 2006. Oxygen production and carbon seques- rent large marine ecosystem. Science 319:920, Monitoring Program. We thank the Washington gov- tration in an upwelling coastal margin. http://dx.doi.org/10.1126/science.1149016. ernor’s office and state legislature, and in particular Global Biogeochemical Cycles 20, GB3001, Sen. Maria Cantwell, for their vision in understanding http://dx.doi.org/10.1029/2005GB002517.

158 Oceanography | Vol.28, No.2 Hales, B., T. Takahashi, and L. Bandstra. 2005. Network: Linking chemistry, physics, and eco- multi-year dataset. Proceedings of the National

Atmospheric CO2 uptake by a coastal upwelling logical effects. Oceanography 28(2):160–169, Academy of Sciences of the United States of system. Global Biogeochemical Cycles 19, GB1009, http://dx.doi.org/10.5670/oceanog.2015.39. America 105:18,848–18,853, http://dx.doi.org/​ http://dx.doi.org/10.1029/2004GB002295. Miller, A.W., A.C. Reynolds, C. Sobrino, and 10.1073/pnas.0810079105. Harris, K.E., M.D. DeGrandpre, and B. Hales. G.F. Riedel. 2009. Shellfish face uncertain future in 2013. Aragonite saturation state dynamics in a high CO world: Influence of acidification on oys- 2 AUTHORS. Alan Barton (alan_barton22@ coastal upwelling zone. Geophysical Research ter larvae calcification and growth in estuaries. yahoo.com) is Production Manager and Research Letters 40:2,720–2,725, http://dx.doi.org/10.1002/ PLoS ONE 4:e5661, http://dx.doi.org/10.1371/journal. Coordinator, Whiskey Creek Shellfish Hatchery, grl.50460. pone.0005661. Tillamook, OR, USA. George G. Waldbusser is Hauri, C., N. Gruber, C.-K. Plattner, S. Alin, R.A. Feely, Pörtner, H.O. 2008. Ecosystem effects of ocean acidi- Assistant Professor, Oregon State University, Corvallis, B. Hales, and P.A. Wheeler. 2009. Ocean acid- fication in times of ocean warming: A physiologist’s OR, USA. Richard A. Feely is Senior Scientist, National ification in the California Current System. view. Marine Ecology Progress Series 373:203–217, Oceanic and Atmospheric Administration, Pacific Oceanography 22(4):60–71, http://dx.doi.org/​ http://dx.doi.org/10.3354/meps07768. Marine Environmental Laboratory, Seattle, WA, USA. 10.5670/oceanog.2009.97. Ringwood, A.H., and C.J. Keppler. 2002. Water Stephen B. Weisberg is Executive Director, Southern Hauri, C., N. Gruber, A.M.P. McDonnell, and M. Vogt. quality variation and clam growth: Is pH really a California Coastal Water Research Project Authority, 2013. The intensity, duration, and severity of non-issue in estuaries? Estuaries 25:901–907, Costa Mesa, CA, USA. Jan A. Newton is Affiliate low aragonite saturation state events on the http://dx.doi.org/​10.1007/BF02691338. Assistant Professor, University of Washington, Seattle, California continental shelf. Geophysical Research Ruesink, J.L., C. Roegner, B.R. Dumbauld, J. Newton, WA, USA. Burke Hales is Professor, Oregon State Letters 40:3,424–3,428, http://dx.doi.org/10.1002/ and D.A. Armstrong. 2003. Contributions of University, Corvallis, OR, USA. Sue Cudd is Owner, grl.50618. coastal and watershed energy sources to second- Whiskey Creek Shellfish Hatchery, Tillamook, OR, Hettinger, A., E. Sanford, T.M. Hill, A.D. Russell, ary production in a northeastern Pacific estuary. USA. Benoit Eudeline is Chief Hatchery Scientist, K.N.S. Sato, J. Hoey, M. Forsch, H.N. Page, and Estuaries 26:1,079–1,093, http://dx.doi.org/10.1007/ Taylor Shellfish Hatchery, Quilcene, WA, USA. B. Gaylord. 2012. Persistent carry-over effects BF02803365. Chris J. Langdon is Professor, Oregon State University, of planktonic exposure to ocean acidification Rykaczewski, R.R., and J.P. Dunne. 2010. Enhanced Newport, OR, USA. Ian Jefferds is General Manager, in the Olympia oyster. Ecology 93:2,758–2,768, nutrient supply to the California Current Ecosystem Penn Cove Shellfish, Coupeville, WA, USA.Teri King http://dx.doi.org/10.1890/12-0567.1. with global warming and increased stratifica- is Marine Water Quality Specialist, Washington Sea Hinga, K. R. 1992. Co-occurrence of dinoflagellate tion in an earth system model. Geophysical Grant, Shelton, WA, USA. Andy Suhrbier is Senior blooms and high pH in marine enclosures. Marine Research Letters 37, L21606, http://dx.doi.org/​ Biologist, Pacific Shellfish Institute, Olympia, WA, Ecology Progress Series 86:181–187, http://www.int- 10.1029/2010GL045019. USA. Karen McLaughlin is Biogeochemist, Southern res.com/articles/meps/86/m086p181.pdf. Southern California Coastal Water Research Project. California Coastal Water Research Project Authority, Hofmann, G.E., J.P. Barry, P.J. Edmunds, 2010. Ocean Acidification Impacts on Shellfish Costa Mesa, CA, USA. R.D. Gates, D.A. Hutchins, T. Klinger, and Workshop: Findings and Recommendations. M.A. Sewell. 2010. The effect of ocean acidifi- Technical Report 624, Southern California Coastal cation on calcifying organisms in marine eco- Water Research Project, Costa Mesa, CA. ARTICLE CITATION systems: An organism-to-ecosystem perspec- Strong, A.L., K.J. Kroeker, L.T. Teneva, L.A. Mease, Barton, A., G.G. Waldbusser, R.A. Feely, S.B. Weisberg, tive. Annual Review of Ecology, Evolution, and and R.P. Kelly. 2014. Ocean acidification 2.0: J.A. Newton, B. Hales, S. Cudd, B. Eudeline, Systematics 41:127–147, http://dx.doi.org/10.1146/ Managing our changing coastal ocean chemistry. C.J. Langdon, I. Jefferds, T. King, A. Suhrbier, and annurev.ecolsys.110308.120227. BioScience 64:581–592, http://dx.doi.org/10.1093/ K. McLaughlin. 2015. Impacts of coastal acidifica- Juranek, L.W., R.A. Feely, W.T. Peterson, S.R. Alin, biosci/biu072. tion on the Pacific Northwest shellfish industry and B. Hales, J. Peterson, K. Lee, and C.L. Sabine. Talmage, S.C., and C.J. Gobler. 2011. Effects of ele- adaptation strategies implemented in response. 2009. A novel method for determination of ara- vated temperature and carbon dioxide on the Oceanography 28(2):146–159, http://dx.doi.org/​ 10.5670/oceanog.2015.38. gonite saturation state on the continental shelf growth and survival of larvae and juveniles of of central Oregon using multi-parameter rela- three species of Northwest Atlantic bivalves. tionships with hydrographic data. Geophysical PLoS ONE 6(10):e26941, http://dx.doi.org/10.1371/ Research Letters 37, L01601, http://dx.doi.org/​ journal.pone.0026941. 10.1029/2009GL040778. Waldbusser, G.G., H. Bergschneider, and M.A. Green. Kelly, R.P., M.M. Foley, W.S. Fisher, R.A. Feely, 2010. Size-dependent pH effect on calcifica- B.S. Halpern, G.G. Waldbusser, and M.R. Caldwell. tion in post-larval hard clam Mercenaria spp. 2011. Mitigating local causes of ocean acidifica- Marine Ecology Progress Series 417:171–182, tion with existing laws. Science 332:1,036–1,037, http://dx.doi.org/10.3354/meps08809. http://dx.doi.org/10.1126/science.1203815. Waldbusser, G.G., E.L. Brunner, B.A. Haley, B. Hales, Kroeker, K.J., R.L. Kordas, R. Crim, I.E. Hendriks, C.J. Langdon, and F.G. Prahl. 2013. A developmen- L. Ramajo, G.S. Singh, C.M. Duarte, and tal and energetic basis linking larval oyster shell J.-P. Gattuso. 2013. Impacts of ocean acidifica- formation to acidification sensitivity. Geophysical tion on marine organisms: Quantifying sensitivi- Research Letters 40:2,171–2,176, http://dx.doi.org/​ ties and interaction with warming. Global Change 10.1002/grl.50449. Biology 19:1,884–1,896, http://dx.doi.org/10.1111/ Waldbusser, G.G., and J.E. Salisbury. 2014. Ocean gcb.12179. acidification in the coastal zone from an organ- Kroeker, K.J., R.L. Kordas, R.N. Crim, and G.G. Singh. ism’s perspective: Multiple system parameters, fre- 2010. Meta-analysis reveals negative yet variable quency domains, and habitats. Annual Review of effects of ocean acidification on marine organisms. Marine Science 6:221–247, http://dx.doi.org/10.1146/ Ecology Letters 13:1,419–1,434, http://dx.doi.org/​ annurev-marine-121211-172238. 10.1111/j.1461-0248.2010.01518.x. Waldbusser, G.G., B. Hales, C.J. Langdon, B.A. Haley, Kurihara, H., S. Kato, and A. Ishimatsu. 2007. Effects P. Schrader, E.L. Brunner, M.W. Gray, C.A. Miller,

of increased seawater pCO2 on early develop- and I. Gimenez. 2015. Saturation-state sensitivity of ment of the oyster Crassostrea gigas. Aquatic marine bivalve larvae to ocean acidification. Nature Biology 1:91–98, http://dx.doi.org/10.3354/ Climate Change 5:273–280, http://dx.doi.org/​ ab00009. 10.1038/nclimate2479. Mabardy, R. 2014. Exploring perceptions and expe- Washington State Blue Ribbon Panel on Ocean riences of the U.S. West Coast shellfish industry Acidification. 2012. Ocean Acidification: From dealing with ocean acidification. Master’s Thesis, Knowledge to Action, Washington State’s Strategic Oregon State University, Corvallis, OR. Response. H. Adelsman and L. Whitely Binder, McLaughlin, K., S.B. Weisberg, A.G. Dickson, eds, Washington Department of Ecology, Olympia, G.E. Hofmann, J.A. Newton, D. Aseltine- Washington, Publication no. 12-01-015. Neilson, A. Barton, S. Cudd, R.A. Feely, Wootton, J.T., C.A. Pfister, and J.D. Forester. 2008. I.W. Jefferds, and others. 2015. Core princi- Dynamic patterns and ecological impacts ples of the California Current Acidification of declining ocean pH in a high-resolution

Oceanography | June 2015 159