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Barton, Alan, Et Al. the Pacific Oyster

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Barton, Alan, Et Al. the Pacific Oyster Limnol. Oceanogr., 57(3), 2012, 698–710 E 2012, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2012.57.3.0698 The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: Implications for near-term ocean acidification effects Alan Barton,a Burke Hales,b,* George G. Waldbusser,b Chris Langdon,c and Richard A. Feelyd a Pacific Coast Shellfish Grower’s Association, Emerald Isle, North Carolina bCollege of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, Oregon c Department of Fisheries and Wildlife and Coastal Marine Experiment Station, Oregon State University, Newport, Oregon dPacific Marine Environmental Laboratory, National Oceanic and Atmospheric Administration, Seattle, Washington Abstract We report results from an oyster hatchery on the Oregon coast, where intake waters experienced variable carbonate chemistry (aragonite saturation state , 0.8 to . 3.2; pH , 7.6 to . 8.2) in the early summer of 2009. Both larval production and midstage growth (, 120 to , 150 mm) of the oyster Crassostrea gigas were significantly negatively correlated with the aragonite saturation state of waters in which larval oysters were spawned and reared for the first 48 h of life. The effects of the initial spawning conditions did not have a significant effect on early-stage growth (growth from D-hinge stage to , 120 mm), suggesting a delayed effect of water chemistry on larval development. Rising atmospheric carbon dioxide (CO2) driven by on the North American Pacific coast takes on the order of anthropogenic emissions has resulted in the addition of decades to transit from the point of subduction to the over 140 Pg-C (1 Pg 5 1015 g) to the ocean (Sabine et al. upwelling locales (Feely et al. 2008), this anthropogenic 2011). The thermodynamics of the reactions between CO2 was added to the water under a substantially lower- carbon dioxide and water require this addition to cause a CO2 atmosphere than today’s, and water already en route decline of ocean pH and carbonate ion concentrations to this location is likely carrying an increasing burden of 5 ([CO 3 ]). For the observed change between current-day and anthropogenic CO2. Understanding the effects of natural preindustrial atmospheric CO2, the surface oceans have lost variations in CO2 in these waters on the local fauna is 5 approximately 16% of their [CO 3 ] and decreased in pH by critical for anticipating how more persistently corrosive 0.1 unit, although colder surface waters are likely to have conditions will affect marine ecosystems. experienced a greater effect (Feely et al. 2009). Projections The responses of organisms to rising CO2 are potentially for the open ocean suggest that wide areas, particularly at numerous and include negative effects on respiration, 5 high latitudes, could reach low enough [CO 3 ] levels that motility, and fertility (Portner 2008). From a geochemical dissolution of biogenic carbonate minerals is thermody- perspective, however, the easiest process to understand namically favored by the end of the century (Feely et al. conceptually is that of solid calcium carbonate (CaCO3,s) 2009; Steinacher et al. 2009), with implications for mineral formation. In nearly all ocean surface waters, commercially significant higher trophic levels (Aydin et al. formation of CaCO3,s is thermodynamically favored by the 2005). abundance of the reactants, dissolved calcium ([Ca2+]), and There is considerable spatial and temporal variability in 5 2+ carbonate ([CO 3 ]) ions. While oceanic [Ca ] is relatively ocean carbonate chemistry, and there is evidence that these constant at high levels that are well described by natural variations affect marine biota, with ecological conservative relationships with salinity, ocean [CO 5] assemblages next to cold-seep high-CO sources having 3 2 decreases as atmospheric CO2 rises, lowering the energetic been shown to be distinct from those nearby but less favorability of CaCO3,s formation. This energetic favor- affected by the elevated CO2 levels (Hall-Spencer et al. ability is proportional to the saturation state, V, defined by 2008). Coastal environments that are subject to upwelling ÂÃÂÃ ~ 2z events also experience exposure to elevated CO2 conditions CO3 Ca Vf ~ where deep water enriched by additions of respiratory CO2 K is brought up from depth to the nearshore surface by sp,f physical processes. Feely et al. (2008) showed that where the subscript f refers to the phase of the mineral upwelling on the Pacific coast of central North America being formed and Ksp,f is the apparent thermodynamic markedly increased corrosiveness for calcium carbonate solubility product of that phase. Precipitation is thermo- minerals in surface nearshore waters. A small but dynamically possible for Vf . 1, and greater values of Vf significant amount of anthropogenic CO2 present in the correspond to greater energetic favorability for precipita- upwelled source waters provided enough additional CO2 to tion. Calcium carbonate exists in a variety of phases cause widespread corrosiveness on the continental shelves distinguished by crystal structure and associated contribu- (Feely et al. 2008). Because the source water for upwelling tions of contaminaxting elements. The most common phases are the low-magnesium phases calcite and aragonite * Corresponding author: [email protected] and high-magnesium calcite. Aragonite is about twice as 698 Ocean acidification and Pacific oyster 699 soluble as calcite, and the solubility of high-Mg calcites natural and hatchery larval production have been severely increases with increased magnesium in the crystal lattice depressed in the Pacific Northwest, and a lack of sufficient (Morse and Mackenzie 1990). Aragonite, in particular, ‘‘seed’’ has threatened an industry with a total economic plays an important role in the calcareous structures value estimated at US$278 million as of 2009 (Pacific Coast produced by corals, pteropods, and early life stages of Shellfish Growers Association 2010). Hatchery problems larval oysters. started in 2006, when high concentrations of the patheno- The CaCO3 shell-forming bivalves, including oysters genic bacterium Vibrio tubiashii were observed, perhaps (Gazeau et al. 2007; Miller et al. 2009; Waldbusser et al. associated with high-nutrient, low-O2 coastal upwelled 2011), mussels (Gazeau et al. 2007; Thomsen et al. 2010), waters (Grantham et al. 2004; Chan et al. 2008) mixing and clams (Green et al. 2009; Talmage and Gobler 2009; with warm late-summer bay waters (Elston et al. 2008). The Waldbusser et al. 2010), show negative responses to Whiskey Creek Shellfish Hatchery in Netarts Bay on the lowered V values, even when those perturbations occur northern Oregon coast (, 45.4uN, 123.9uW) experienced above the V 5 1 thermodynamic threshold for the minerals high concentrations of V. tubiashii and difficulties in seed in question. Larval oysters appear to be particularly production (Elston et al. 2008). However, by the summer of susceptible to the influences of ambient seawater chemistry, 2008, bacterial monitoring indicated that pronounced as they form their larval shell material out of the more mortality events often occurred in the absence of detectable soluble aragonite (Stenzel 1964) and only deposit less V. tubiashii. On the other hand, these larval mortality soluble calcite following settlement. Additionally, some events often coincided with strong coastal upwelling and studies indicate amorphous calcium carbonate (ACC) as an the presence of seawater thermodynamically unstable with even more soluble mineral precursor (Weiss et al. 2002) respect to aragonite in Netarts Bay. during early stages of calcification, although other studies Although the effects of ocean acidification have been question the ubiquity of this finding (Mount et al. 2004; forecast for nearly 30 yr (Feely and Chen 1982), the issue Kudo et al. 2010). has only recently received community-wide interest with Regardless of exact calcification mechanisms, previous workshops (Fabry et al. 2009) and strategy documents studies have shown that oyster larvae respond negatively to (e.g., National Research Council 2010) completed in the more acidic conditions. Kurihara et al. (2007) found a last few years, along with development of large-scale inter- reduction in development success when Crassostrea gigas national integrated projects (http://www.epoca-project.eu) larvae were exposed to acidified conditions (pH 5 7.4). and locally integrated observation networks (http://c-can. Watson et al. (2009) exposed D-hinge (1-d-old) larvae of msi.ucsb.edu). As a result, the chemical signature and the Sydney rock oyster (Saccostrea glomerata) to a range of ecological effects of acidification have been under way long pH conditions (7.6–8.1) over a period of 10 d and showed a before adequate scientific monitoring and classical exper- significant decline in the survival and growth of young imentation could sufficiently be put in place to resolve larvae at lower pH. In a study starting with 5-d-old larvae, either the baseline or the mechanisms of ecosystem Miller et al. (2009) also showed a significant decrease in responses. Because of this known information deficiency, growth rate of C. virginica when exposed to lower pH workshop reports (Fabry et al. 2009) have strongly conditions but relatively little effect on survival. Reduced recommended that the scientific community engage affect- larval growth of C. virginica in response to reduced pH
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