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Biocalcification in the Eastern Oyster (Crassostrea virginica) in Relation to Long-term Trends in Chesapeake Bay pH

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Abstract

Anthropogenic carbon dioxide (CO2) emissions reduce pH of marine waters due to the absorption of atmospheric CO2 and formation of carbonic acid. Estuarine waters are more susceptible to acidification because they are subject to multiple acid sources and are less buffered than marine waters. Consequently, estuarine shell forming species may experience acidification sooner than marine species although the tolerance of estuarine calcifiers to pH changes is poorly understood. We analyzed 23 years of Chesapeake Bay water quality monitoring data and found that daytime average pH significantly decreased across polyhaline waters although pH has not significantly changed across mesohaline waters. In some tributaries that once supported large oyster populations, pH is increasing. Current average conditions within some tributaries however correspond to values that we found in laboratory studies to reduce oyster biocalcification rates or resulted in net shell dissolution. Calcification rates of juvenile eastern oysters, Crassostrea virginica, were measured in laboratory studies in a three-way factorial design with 3 pH levels, two salinities, and two temperatures. Biocalcification declined significantly with a reduction of ∼0.5 pH units and higher temperature and salinity mitigated the decrease in biocalcification.

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References

  • Addadi, L., D. Joester, F. Nudelman, and S. Weiner. 2006. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry-a European Journal 12: 981–987.

    Article  Google Scholar 

  • Blackford, J.C., and F.J. Gilbert. 2007. pH variability and CO2 induced acidification in the North Sea. Journal of Marine Systems 64: 229–241.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Burnett, L.E. 1988. Physiological responses to air exposure: acid-base balance and the role of branchial water stores. American Zoologist 28: 125–135.

    Google Scholar 

  • Cai, W.J., and Y. Wang. 1998. The chemistry, fluxes, and sources of carbon dioxide in the estuarine waters of the Satilla and Altamaha Rivers, Georgia. Limnology and Oceanography 43: 657–668.

    Article  CAS  Google Scholar 

  • Carriker, M.R. 1996. The shell and ligament. In The eastern oyster Crassostrea virginica, ed. V.S. Kennedy, R.I.E. Newell, and A. Eble, 734. College Park: Maryland Sea Grant.

    Google Scholar 

  • Dame, R.F. 1996. Ecology of marine bivalves, an ecosystem approach. Boca Raton: CRC Press.

    Book  Google Scholar 

  • Doney, S.C., N. Mahowald, I. Lima, R.A. Feely, F.T. Mackenzie, J.F. Lamarque, and P.J. Rasch. 2007. Impact of anthropogenic atmospheric nitrogen and sulfur deposition on ocean acidification and the inorganic carbon system. Proceedings of the National Academy of Sciences of the United States of America 104: 14580–14585.

    Article  CAS  Google Scholar 

  • 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 

  • Dove, M.C., and J. Sammut. 2007. Impacts of estuarine acidification on survival and growth of Sydney rock oysters Saccostrea Glomerata (gould 1850). Journal of Shellfish Research 26: 519–527.

    Article  Google Scholar 

  • Edmond, J.M. 1970. High precision determination of titration alkalinity and total carbon dioxide content of sea water by potentiometric titration. Deep-Sea Research 17: 737.

    CAS  Google Scholar 

  • Fan, W.M., C.Z. Li, X. Wang, N.P. Gong, L.P. Xie, and R.Q. Zhang. 2007. Cloning, characterization and expression analysis of calcium channel beta subunit from pearl oyster (Pinctada fucata). Journal of Bioscience and Bioengineering 104: 47–54.

    Article  CAS  Google Scholar 

  • Frankignoulle, M., G. Abril, A. Borges, I. Bourge, C. Canon, B. DeLille, E. Libert, and J.M. Theate. 1998. Carbon dioxide emission from European estuaries. Science 282: 434–436.

    Article  CAS  Google Scholar 

  • Gazeau, F., C. Quiblier, J.M. Jansen, J.P. Gattuso, J.J. Middelburg and C.H.R. Heip. 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34: doi:10.1029/2006GL028554

  • Gillikin, D.P., A. Lorrain, L. Meng, and F. Dehairs. 2007. A large metabolic carbon contribution to the delta C-13 record in marine aragonitic bivalve shells. Geochimica et Cosmochimica Acta 71: 2936–2946.

    Article  CAS  Google Scholar 

  • Green, M.A., G.G. Waldbusser, S.L. Reilly, K. Emerson, and S. O’Donnell. 2009. Death by dissolution: sediment saturation state as a mortality factor for juvenile bivalves. Limnology and Oceanography 54: 1037–1047.

    Article  CAS  Google Scholar 

  • Gutierrez, J.L., C.G. Jones, D.L. Strayer, and O.O. Iribarne. 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101: 79–90.

    Article  Google Scholar 

  • Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950-2001: long-term change in relation to nutrient loading and river flow. Estuaries 27: 634–658.

    Article  CAS  Google Scholar 

  • Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, R. Cooke, J. Erlandson, J.A. Estes, T.P. Hughes, S. Kidwell, C.B. Lange, H.S. Lenihan, J.M. Pandolfi, C.H. Peterson, R.S. Steneck, M.J. Tegner, and R.R. Warner. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–638.

    Article  CAS  Google Scholar 

  • Kemp, W.M., W.R. Boynton, J.E. Adolf, D.F. Boesch, W.C. Boicourt, G. Brush, J.C. Cornwell, T.R. Fisher, P.M. Glibert, J.D. Hagy, L.W. Harding, E.D. Houde, D.G. Kimmel, W.D. Miller, R.I.E. Newell, M.R. Roman, E.M. Smith, and J.C. Stevenson. 2005. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Marine Ecology-Progress Series 303: 1–29.

    Article  Google Scholar 

  • Kennedy, V.S., R.I.E. Newell, and A. Eble. 1996. The eastern oyster, Crassostrea virginica. College Park: Maryland Sea Grant.

    Google Scholar 

  • 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 

  • Kleypas, J.A., R.A. Feely, V.J. Fabry, C. Langdon, C.L. Sabine, and L.L. Robbins, 2006. Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research, report of a workshop held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the U.S. Geological Survey, 88 pp.

  • Kurihara, H., S. Kato, and A. Ishimatsu. 2007. Effects of increased seawater pCO(2) on early development of the oyster Crassostrea gigas. Aquatic Biology 1: 91–98.

    Article  CAS  Google Scholar 

  • Levi-Kalisman, Y., G. Falini, L. Addadi, and S. Weiner. 2001. Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using Cryo-TEM. Journal of Structural Biology 135: 8–17.

    Article  CAS  Google Scholar 

  • Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806–1809.

    Article  CAS  Google Scholar 

  • Mann, R., and E.N. Powell. 2007. Why oyster restoration goals in the Chesapeake Bay are not and probably cannot be achieved. Journal of Shellfish Research 26: 905–917.

    Article  Google Scholar 

  • McConnaughey, T.A., and D.P. Gillikin. 2008. Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters 28: 287–299.

    Article  CAS  Google Scholar 

  • Michaelidis, B., C. Ouzounis, A. Paleras, and H.O. Portner. 2005. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology-Progress Series 293: 109–118.

    Article  Google Scholar 

  • Miller, A.W., A.C. Reynolds, C. Sorbino, and G.F. Riedel. 2009. Shellfish face uncertain future in high CO2 world: influence of acidification on oyster larvae calcification and growth in estuaries. PLoS Biology 4: e5661.

    Google Scholar 

  • Millero, F.J. 1986. The pH of estuarine waters. Limnology and Oceanography 31: 839–847.

    Article  CAS  Google Scholar 

  • Najjar, R.G., C.R. Pyke, M.B. Adams, D. Breitburg, C. Hershner, M. Kemp, R. Howarth, M.R. Mulholland, M. Paolisso, D. Secor, K. Sellner, D. Wardrop, and R. Wood. 2010. Potential climate-change impacts on the Chesapeake Bay. Estuarine Coastal and Shelf Science 86: 1–20.

    Article  CAS  Google Scholar 

  • Newell, R.I.E., G.S. Alspach Jr., V.S. Kennedy, and D. Jacobs. 2000. Mortality of newly metamorphosed eastern oysters (Crassostrea virginica) in mesohaline Chesapeake Bay. Marine Biology 136: 665–676.

    Article  Google Scholar 

  • Newell, R.I.E., V.S. Kennedy, and K.S. Shaw. 2007. Comparative vulnerability to predators, and induced defense responses, of eastern oysters Crassostrea virginica and non-native Crassostrea ariakensis oysters in Chesapeake Bay. Marine Biology 152: 449–460.

    Article  Google Scholar 

  • O’Donnell, M., L. Hammond, and G. Hofmann. 2009. Predicted impact of ocean acidification on a marine invertebrate: elevated CO2 alters response to thermal stress in sea urchin larvae. Marine Biology 156: 439–446.

    Article  Google Scholar 

  • Parker, L.M., P.M. Ross, and W.A. O’Connor. 2009. The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Global Change Biology 15: 2123–2136.

    Article  Google Scholar 

  • Paynter, K.T. 1999. Managing around oyster disease in Maryland and Maryland oyster roundtable strategies. In Oyster reef habitat restoration: a synopsis and synthesis of approaches, ed. M.W. Luckenbach, R. Mann, and J.A. Wesson, 317–328. Gloucester Point: Virgina Institute of Marine Science Press.

    Google Scholar 

  • Pörtner, H.O. 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology-Progress Series 373: 203–217.

    Article  Google Scholar 

  • Pörtner, H.O., M. Langenbuch, and A. Reipschlager. 2004. Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. Journal of Oceanography 60: 705–718.

    Article  Google Scholar 

  • Powell, E.N., and J.M. Klinck. 2007. Is oyster shell a sustainable estuarine resource? Journal of Shellfish Research 26: 181–194.

    Article  Google Scholar 

  • Powell, E.N., J.N. Kraeuter, and K.A. Ashton-Alcox. 2006. How long does oyster shell last on an oyster reef? Estuarine Coastal and Shelf Science 69: 531–542.

    Article  Google Scholar 

  • Ringwood, A.H., and C.J. Keppler. 2002. Water quality variation and clam growth: is pH really a non-issue in estuaries? Estuaries 25: 901–907.

    Article  Google Scholar 

  • Rothschild, B.J., J.S. Ault, P. Goulletquer, and M. Heral. 1994. Decline of the Chesapeake Bay oyster population—a century of habitat destruction and overfishing. Marine Ecology-Progress Series 111: 29–39.

    Article  Google Scholar 

  • Salisbury, J., M.A. Green, C. Hunt, and J. Campbell. 2008. Coastal acidifcation by rivers: a threat to shellfish? EOS, Transactions, American Geophysical Union 89: 513–514.

    Article  Google Scholar 

  • Schulte, D.M., R.P. Burke, and R.N. Lipcius. 2009. Unprecedented restoration of a native oyster metapopulation. Science 325: 1124–1128.

    Article  CAS  Google Scholar 

  • Smith, S.V., and G.S. Key. 1975. Carbon dioxide and metabolism in marine environments. Limnology and Oceanography 20: 493–495.

    Article  CAS  Google Scholar 

  • Smith, G.F., K.N. Greenhawk, D.G. Bruce, E.B. Roach, and S.J. Jordan. 2001. A digital presentation of the Maryland oyster habitat and associated bottom types in the Chesapeake Bay (1974-1983). Journal of Shellfish Research 20: 197–206.

    Google Scholar 

  • Smith, G.F., D.G. Bruce, E.B. Roach, A. Hansen, R.I.E. Newell, and A.M. McManus. 2005. Assessment of recent habitat conditions of eastern oyster Crassostrea virginica bars in mesohaline Chesapeake Bay. North American Journal of Fisheries Management 25: 1569–1590.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Srna, R.F. and A. Baggaley. 1976. Rate of excretion of ammonia by hard clam Mercenaria-Mercenaria and American oyster Crassostrea-Virginica. Marine Biology 36: 251–258.

  • Talmage, S.C., and C.J. Gobler. 2009. The effects of elevated carbon dioxide concentrations on the metamorphosis, size, and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians), and Eastern oysters (Crassostrea virginica). Limnology and Oceanography 54: 2072–2080.

    Article  Google Scholar 

  • Ulanowicz, R.E., W.C. Caplins, and E.A. Dunnington. 1980. The forecasting of oyster harvest in Central Chesapeake Bay. Estuarine and Coastal Marine Science 11: 101–106.

    Article  Google Scholar 

  • Wilber, K.M., and A.S.M. Saleuddin. 1983. Shell formation. In The mollusca: physiology, ed. K.M. Wilber and A.S.M. Saleuddin, 594. New York: Academic Press, Inc.

    Google Scholar 

  • Yates, K.K., C. Dufore, N. Smiley, C. Jackson, and R.B. Halley. 2007. Diurnal variation of oxygen and carbonate system parameters in Tampa Bay and Florida Bay. Marine Chemistry 104: 110–124.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by a National Science Foundation award #OCE-0622999 to MAG and GGW and The Geneva Boone Endowed Award Fund to EPV by St. Mary’s College of Maryland. We thank two anonymous reviewers for helpful and critical feedback on a previous version of this manuscript. We thank M. Luckenbach and S. Bonniwell of the Virginia Institute of Marine Science-Eastern Shore Laboratory for providing juvenile oysters. Components of this research were conducted as an undergraduate senior research thesis by EPV in partial fulfillment of requirements for a B.A. GGW would also like to thank Chesapeake Biological Laboratory, where this work was conducted.

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Correspondence to George G. Waldbusser.

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Waldbusser, G.G., Voigt, E.P., Bergschneider, H. et al. Biocalcification in the Eastern Oyster (Crassostrea virginica) in Relation to Long-term Trends in Chesapeake Bay pH. Estuaries and Coasts 34, 221–231 (2011). https://doi.org/10.1007/s12237-010-9307-0

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