Skip to main content

The Carbonate Chemistry of the “Fattening Line,” Willapa Bay, 2011–2014

Abstract

Willapa Bay has received a great deal of attention in the context of rising atmospheric CO2 and the concomitant effects of changes in bay carbonate chemistry, referred to as ocean acidification, and the potential effects on the bay’s naturalized Pacific oyster (Crassostrea gigas) population and iconic oyster farming industry. Competing environmental stressors, historical variability in the oyster settlement record, and the absence of adequate historical observations of bay-water carbonate chemistry all conspire to cast confusion regarding ocean acidification as the culprit for recent failures in oyster larval settlement. We present the first measurements of the aqueous CO2 partial pressure (PCO2) and the total dissolved carbonic acid (TCO2) at the “fattening line,” a location in the bay that has been previously identified as optimal for both larval oyster retention and growth, and collocated with a long historical time series of larval settlement. Samples were collected from early 2011 through late 2014. These measurements allow the first rigorous characterization of Willapa Bay aragonite mineral saturation state (Ωar), which has been shown to be of leading importance in determining the initial shell formation and growth of larval Crassostrea gigas. Observations show that the bay is usually below Ωar levels that have been associated with poor oyster hatchery production and with chronic effects noted in experimental work. Bay water only briefly rises to favorable Ωar levels and does so out of phase with optimal thermal conditions for spawning. Thermal and carbonate conditions are thus coincidentally favorable for early larval development for only a few weeks at a time each year. The limited concurrent exceedance of thermal and Ωar thresholds suggests the likelihood of high variability in settlement success, as seen in the historical record; however, estimates of the impact of elevated atmospheric CO2 suggest that pre-industrial Ωar conditions were more persistently favorable for larval development and more broadly coincident with thermal optima.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Banas, N.S., B.M. Hickey, P. MacCready, and J.A. Newton. 2004. Dynamics of Willapa Bay, Washington: A highly unsteady, partially mixed estuary. Journal of Physical Oceanography 34: 2413–2427.

    Article  Google Scholar 

  2. Banas, N.S., and B.M. Hickey. 2005. Mapping exchange and residence time in a model of Willapa Bay, Washington, a branching, macrotidal estuary. Journal Geophysical Research C 110: C11011. doi:10.1029/2005JC002950.

    Article  Google Scholar 

  3. Banas, N.S., B.M. Hickey, J.A. Newton, and J.L. Ruesink. 2007. Tidal exchange, bivalve grazing, and patterns of primary production in Willapa Bay, Washington. Marine Ecology Progress Series 341: 123–139.

    Article  Google Scholar 

  4. Bandstra, L., B. Hales, and T. Takahashi. 2006. High-frequency measurement of seawater total carbon dioxide. Marine Chemistry. doi:10.1016/j.marchem.2005.10.009.

    Google Scholar 

  5. Barton, A., G.G. Waldbusser, R.A. Feely, S.B. Weisberg, J.A. Newton, B. Hales, S. Cudd, B. Eudeline, C. Langdon, I. Jefferds, T. King, and K. Mclaughlin. 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.

    Article  Google Scholar 

  6. Barton, A., B. Hales, G. Waldbusser, C. Langdon, and R. Feely. 2012. The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: Implications for near-term ocean acidification impacts. Limnology and Oceanography 57: 698–710. doi:10.4319/lo.2012.57.3.0698.

    CAS  Article  Google Scholar 

  7. Bochenek, E.A., J.M. Klinck, E.N. Powell, and E.E. Hofmann. 2001. A biochemically based model of the growth and development of Crassostrea gigas larvae. Journal of Shellfish Research 20: 243–265.

    Google Scholar 

  8. Borges, A.V., and N. Gypens. 2010. Carbonate chemistry in the coastal zone responds more strongly to eutrophication than to ocean acidification. Limnology and Oceanography 55: 346–353.

    CAS  Article  Google Scholar 

  9. Cai, W.-J.X. Hu, W. Huang, M.C. Murrell, J.C. Lehrter, S.E. Lohrenz, W.-C. Chou, W. Zhai, J.T. Hollibaugh, Y. Wang, P. Zhao, X. Guo, K. Gundersen, M. Dai, and G.-C. Gong. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4: 766–770. http://www.nature.com/ngeo/journal/v4/n11/abs/ngeo1297.html#supplementary-information

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

    Google Scholar 

  11. Dickson, A., C. L. Sabine, and J. R. Christian (Eds.) 2007. Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, 191 pp.

  12. Dickson, A.G. 1990. Thermodynamics of the dissociation of boric acid in synthetic sea water from 273.15 to 298.15 K. Deep Sea Research 37: 755–766.

    CAS  Article  Google Scholar 

  13. Doney, S.C., V.J. Fabry, R.A. Feely, and J.A. Kleypas. 2009. Ocean Acidification: The other CO2 problem. Annual Review of Marine Science 1: 169–192.

    Article  Google Scholar 

  14. Dumbauld, B. R., and L. M. McCoy, 2015. The effect of oyster aquaculture on seagrass (Zostera marina) at the estuarine landscape scale in Willapa Bay, Washington (USA). Aquaculture Environment Interactions, in revision.

  15. Dumbauld, B.R., B.E. Kauffmann, A.C. Trimble, and J.L. Ruesink. 2011. The Willapa Bay oyster reserves in Washington State: Fishery collapse, creating a sustainable replacement, and the potential for habitat conservation and restoration. Journal of Shellfish Research 30: 71–83.

    Article  Google Scholar 

  16. Ekstrom, J., L. Suatoni, S. Cooley, L. Pendleton, G.G. Waldbusser, J. Cinner, J. Ritter, C. Langdon, R. van Hooidonk, D. Gledhill, K. Wellman, M. Beck, L. Brander, D. Rittschof, C. Doherty, P. Edwards, and R. Portela. 2015. Vulnerability and adaptation of US shellfisheries to ocean acidification. Nature Climate Change 5: 207–214. doi:10.1038/nclimate2508.

  17. Elston, R.A., H. Hasegawa, K.L. Humphrey, I.K. Polyak, and C.C. Hase. 2008. Re-emergence of Vibrio tubiashii in bivalve shellfish aquaculture: severity, environmental drivers, geographic extent and management. Diseases of Aquatic Organisms 82: 119–134.

    Article  Google Scholar 

  18. Emmett, R., R. Llansó, J. Newton, R. Thom, M. Hornberger, C. Morgan, C. Levings, A. Copping, and P. Fishman. 1999. Geographic signatures of North American west coast estuaries. Estuaries 23: 765–792.

    Article  Google Scholar 

  19. Feely, R.A., C.L. Sabine, K. Lee, W. Berelson, J. Kleypas, V.J. Fabry, and F.J. Millero. 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305(5682): 362–366. doi:10.1126/science.1097329,.

    CAS  Article  Google Scholar 

  20. Feely, R.A., C.L. Sabine, J.M. Hernandez-Ayon, D. Ianson, and B. Hales. 2008. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320: 1490–1492.

    CAS  Article  Google Scholar 

  21. Feely, R.A., S.R. Alin, J. Newton, C.L. Sabine, M. Warner, A. Devol, C. Krembs, and C. Maloy. 2010. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuarine, Coastal. Shelf Science 88: 442–449. doi:10.1016/j.ecss.2010.05.004,.

    CAS  Article  Google Scholar 

  22. Feely, R.A., T. Klinger, J.A. Newton, and M. Chadsey, 2012. Scientific Summary of Ocean Acidification in Washington State Marine Waters. NOAA OAR Special Report, 170 pp.

  23. Feely, R.A., S.R. Alin, B. Carter, N. Bednarsek, B. Hales, F. Chan, T. Hill, B. Gaylord, E. Sanford, R. Byrne, C. Sabine, and D. Greeley. 2016. Chemical and biological impacts of ocean acidification along the west coast of North America.  Estuarine, Coastal, and Shelf Science, revision submitted.

  24. Hales, B., T. Takahashi, and L. Bandstra. 2005. Atmospheric CO2 uptake by a coastal upwelling system. Global Biogeochemical Cycles 19. doi:10.1029/2004GB002295.

  25. Hales, B., D. Chipman, and T. Takahashi. 2004. High-frequency measurement of partial pressure and total concentration of carbon dioxide in seawater using microporous hydrophobic membrane contactors. Limnology and Oceanography: Methods 2: 356–364.

    Article  Google Scholar 

  26. Harris, K.E., M.D. DeGrandpre, and B. Hales. 2013. Aragonite saturation states in a coastal upwelling zone. Geophysical Research Letters. doi:10.1002/grl.50460.

    Google Scholar 

  27. Hauri, C., N. Gruber, M. Vogt, S.C. Doney, R.A. Feely, Z. Lachkar, A. Leinweber, A.M.P. McDonnell, M. Munnich, and G.-K. Plattner. 2013. Spatiotemporal variabiliry and long-term trends of ocean acidification in the California Current System. Biogeosciences 10: 193–216. doi:10.5194/bg-10-193-2013.

  28. Hickey, B.M., and N.S. Banas. 2003. Oceanography of the U. S. Pacific Northwest coastal ocean and estuaries with application to coastal ecology. Estuaries 26: 1010–1031.

    Article  Google Scholar 

  29. Huyer, A., R. Pillsbury, and R. Smith. 1978. Seasonal variation of the alongshore velocity field over the continental shelf off Oregon. Limnology and Oceanography 20: 90–95.

    Article  Google Scholar 

  30. Huyer, A., E. Sobey, and R. Smith. 1979. The spring transition in currents over the Oregon continental shelf. Journal of Geophysical Research 84: 6995–7011.

    Article  Google Scholar 

  31. Kelly, R.P., M.M. Foley, W.S. Fisher, R.A. Feely, B.S. Halpern, G.G. Waldbusser, and M.R. Caldwell. 2011. Mitigating local causes of ocean acidification with existing laws. Science Policy Forum 332. doi:10.1126/science.1203815.

  32. Kennedy, V.S. 1996. Biology of larvae and spat. In The Eastern Oyster, Crassostrea virginica, eds. V.S. Kennedy, R.I.E. Newell, and A. Eble, 371–421. College Park, MD: Maryland Sea Grant.

    Google Scholar 

  33. Kimmel, D.G., and R.I.E. Newell. 2007. The influence of climate variation on eastern oyster (Crassostrea virginica) juvenile abundance in Chesapeake Bay. Limnology and Oceanography 52: 959–965.

    Article  Google Scholar 

  34. Mann, R., E. Burreson, and P.K. Baker. 1991. The decline of the Virginia oyster fishery in Chesapeake Bay: considerations for introduction of a non-endemic species, Crassostrea gigas (Thunberg). Journal of Shellfish Research 10(2): 379–388.

  35. Millero, F.J. 2010. Carbonate constants for estuarine waters. Marine and Freshwater Research 61: 139–142.

    CAS  Article  Google Scholar 

  36. Millero, F.J. 1995. Thermodynamics of the carbon dioxide system in the oceans. Geochimica et Cosmochimica Acta 59: 661–677.

    CAS  Article  Google Scholar 

  37. Mucci, A. 1983. The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. American Journal of Science 283: 780–799.

    CAS  Article  Google Scholar 

  38. Nelson, J. 1903. Report of Biologist: Part I, Experimental studies in oyster propagation. pp 333–369, in Ann. Rep. N.J. Agric. Exp. Sta. 1902. New Brunswick, NJ.

  39. Newton, J.A., and R.A. Horner. 2003. Use of phytoplankton species indicators to track the origin of phytoplankton blooms, Washington. Estuaries 26: 1071–1078.

    Article  Google Scholar 

  40. Portner, H.O. 2008. Effects of ocean acidification on marine ecosystems. Marine Ecology Progress Series 373: 203–217. doi:10.334/meps07868.

  41. Reum, J.C.P., S.R. Alin, R.A. Feely, J. Newton, M. Warner, and P. McElhany. 2014. Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: Implications for the design of ocean acidification experiments. PloS One 9(2): e89619. doi:10.1371/journal.pone.0089619.

    Article  Google Scholar 

  42. Reinsch, C.J. 1967. Smoothing spline functions. Numerische Mathematik 29: 177–283.

    Article  Google Scholar 

  43. Ruesink, J.L., G.C. Roegner, B.R. Dumbauld, J.A. Newton, and D.A. Armstrong. 2003. Contributions of coastal and watershed energy sources to secondary production in a northeastern Pacific estuary. Estuaries 26: 1079–1093.

    Article  Google Scholar 

  44. Ruesink, J.L., S. Yang, and A.C. Trimble. 2015. Variability in carbon availability and eelgrass (Zostera marina) biometrics along an estuarine gradient in Willapa Bay, WA, USA. Estuaries and Coasts 38:1908-1917. doi:10.1007/s12237-014-9933-z.

  45. Rumrill, S.S. 1990. Natural mortality of marine invertebrate larvae. Ophelia 32: 163–198.

    Article  Google Scholar 

  46. Sabine, C.L., and R.A. Feely. 2007. In Greenhouse Gas Sinks, eds. D. Reay, N. Hewitt, J. Grace, K. Smith. Oxfordshire, UK: CABI.

  47. Sabine, C.L., R.A. Feely, N. Gruber, R.M. Key, K. Lee, J.L. Bullister, R. Wanninkhof, C.S. Wong, D.W.R. Wallace, B. Tilbrook, F.J. Millero, T.-H. Peng, A. Kozyr, T. Ono, and A.F. Rios. 2004. The oceanic sink for anthropogenic CO2. Science 305(5682): 367–371. doi:10.1126/science.1097403,.

    CAS  Article  Google Scholar 

  48. Salisbury, J., M. Green, C. Hunt, and J. Campbell. 2008. Coastal acidification by rivers: A threat to shellfish? Eos 89: 513–514.

    Article  Google Scholar 

  49. Sherwood, C.R., and J.S. Creager. 1990. Sedimentary geology of the Columbia River estuary. Progress in Oceanography 25: 15–79.

    Article  Google Scholar 

  50. Soetaert, K., A.F. Hofmann, J.J. Middelburg, F.J.R. Meysman, and J. Greenwood. 2007. The effect of biogeochemical processes on pH. Marine Chemistry 105: 30–51.

    CAS  Article  Google Scholar 

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

    Google Scholar 

  52. Sunda, W.G., and W.J. Cai. 2012. Eutrophication Induced CO2-Acidification of Subsurface Coastal Waters: Interactive Effects of Temperature, Salinity, and Atmospheric PCO2. Environmental Science & Technology 46: 10651–10659.

    CAS  Article  Google Scholar 

  53. Takahashi, T., S.C. Sutherland, C. Sweeney, A. Poisson, N. Metzl, B. Tilbrook, N. Bates, R. Wanninkhof, R.A. Feely, C. Sabine, J. Olafson, and Y. Nojiri. 2002. Global sea–air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects.  Deep-Sea Res II 49: 1601–1622.

  54. Takahashi, T., et al. 2009. Climatological mean and decadal change in surface ocean pCO2, and net sea-air CO2 flux over the global oceans. Deep Sea Research. doi:10.1016/j.dsr2.2008.12.009.

    Google Scholar 

  55. Takahashi, T., S.C. Sutherland, D.W. Chipman, J.G. Goddard, C. Ho, T. Newberger, C. Sweeney, and D.R. Munro. 2014. Climatological distributions of pH, pCO2, total CO2, alkalinity and CaCO3 saturation in the global surface ocean, and temporal changes at selected locations. Marine Chemistry 164: 95–125.

    CAS  Article  Google Scholar 

  56. Waldbusser, G.G., B. Hales, C.J. Langdon, B.A. Haley, P. Schrader, E.L. Brunner, M.W. Gray, C.A. Miller, and I. Gimenez. 2015a. Experimental Evidence for Saturation State Impacts on Early Larval Bivalves. Nature Climate Change. doi:10.1038/NCLIMATE2479.

    Google Scholar 

  57. Waldbusser, G.G., B. Hales, C.J. Langdon, B.A. Haley, P. Schrader, E.L. Brunner, M.W. Gray, C.A. Miller, I. Gimenez, and G. Hutchinson. 2015b. Ocean acidification has multiple modes of action on bivalve larvae. PloS One 10(6): e0128376. doi:10.1371/journal.pone.0128376.

    Article  Google Scholar 

  58. Waldbusser, G.G., and J.E. Salisbury. 2014. Ocean Acidification in the Coastal Zone from an Organism’s Perspective: Multiple System Parameters, Frequency Domains, and Habitats. Annual Review of Marine Science 6: 221–247.

    Article  Google Scholar 

  59. Waldbusser, G.G., E.P. Voigt, H. Bergschneider, M.A. Green, and R.I. Newell. 2011. Biocalcification in the eastern oyster (Crassostrea virginica) in relation to long-term trends in Chesapeake Bay pH. Estuaries and Coasts 34: 221–231.

    CAS  Article  Google Scholar 

  60. Waldbusser, G.G., E. Brunner, B. Haley, B. Hales, F. Prahl, and C. Langdon. 2013. A developmental and energetic basis linking larval oyster shell formation to ocean acidification. Geophysical Research Letters. doi:10.1002/grl.50449.

    Google Scholar 

  61. Wallace, R.B., H. Baumann, J.S. Grear, R.C. Aller, and C.J. Gobler. 2014. Coastal ocean acidification: The other eutrophication problem. Estuarine, Coastal and Shelf Science 148: 1–13. doi:10.1016/j.ecss.2014.05.027.

  62. Washington State Blue Ribbon Panel on Ocean Acidification, 2012. Ocean Acidification: From Knowledge to Action, Washington State’s Strategic Response. H. Adelsman and L. Whitely Binder (eds). Olympia, Washington: Washington Department of Ecology. Publication no. 12-01-015.

  63. Wheatcroft, R.A., M.A. Goni, J.A. Hatten, G.B. Pasternack, and J.A. Warrick. 2010.  The role of effective discharge in the ocean delivery of particulate organic carbon bysmall, mountainous river systems. Limnology and Oceanography 55: 161–171.

Download references

Acknowledgments

Grants to OSU supported BH (NOAA NA14NOS0120151, NA05OAR4311164, NA10OAR4310091, and NA1INOSOI20036; NSF OCE-1041267; and State of Oregon funds under House Bill 5008) and GGW (NSF OCE-1041267) in this work. Water quality monitoring funds supporting secured by Senator Maria Cantwell in 2010 to 2011 and in subsequent years by the Washington State Legislature through a contract from the Washington Ocean Acidification Center to the Pacific Coast Shellfish Growers Association supported AS and the sample collection and analyses. RF was supported by the Pacific Marine Environmental Laboratory and the NOAA Ocean Acidification Program. JN acknowledges the support of the Washington Ocean Acidification Center at the University of Washington, and the Northwest Association of Networked Ocean Observing Systems, NANOOS, which is supported by NOAA Award NA11NOS0120036 and part of US IOOS. Bruce Kaufman and Travis Haring of Washington Department of Fish and Wildlife assisted with collection of carbon chemistry bottle samples. Two anonymous reviewers and R. Osman provided helpful comments on this manuscript. This is PMEL Contribution 4425.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Burke Hales.

Additional information

Communicated by Charles Simenstad

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hales, B., Suhrbier, A., Waldbusser, G.G. et al. The Carbonate Chemistry of the “Fattening Line,” Willapa Bay, 2011–2014. Estuaries and Coasts 40, 173–186 (2017). https://doi.org/10.1007/s12237-016-0136-7

Download citation

Keywords

  • Estuarine carbonate chemistry
  • Oyster settlement
  • Ocean acidification