Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 8 2009 10.5194/bg-6-1811-2009 http://www.biogeosciences.net/6/1811/2009/ http://www.biogeosciences.net/6/1811/2009/bg-6-1811-2009.html http://www.biogeosciences.net/6/1811/2009/bg-6-1811-2009.pdf 1811 1823 2009-08-27 Net Loss of CaCO₃ from a subtropical calcifying community due to seawater acidification: mesocosm-scale experimental evidence A. J. Andersson andreas.andersson@bios.edu I. B. Kuffner F. T. Mackenzie P. L. Jokiel K. S. Rodgers A. Tan Bermuda Institute of Ocean Sciences, St. George's, Bermuda, UK US Geological Survey, Florida Integrated Science Center, St. Petersburg, FL, USA Department of Oceanography, University of Hawaii, Honolulu, HI, USA Hawaii Institute of Marine Biology, Kaneohe, HI, USA Acidification of seawater owing to oceanic uptake of atmospheric CO₂ originating from human activities such as burning of fossil fuels and land-use changes has raised serious concerns regarding its adverse effects on corals and calcifying communities. Here we demonstrate a net loss of calcium carbonate (CaCO₃) material as a result of decreased calcification and increased carbonate dissolution from replicated subtropical coral reef communities (<i>n</i>=3) incubated in continuous-flow mesocosms subject to future seawater conditions. The calcifying community was dominated by the coral <i>Montipora capitata</i>. Daily average community calcification or Net Ecosystem Calcification (NEC=CaCO₃ production – dissolution) was positive at 3.3 mmol CaCO₃ m^&minus;2 h^&minus;1 under ambient seawater <i>p</i>CO₂ conditions as opposed to negative at &minus;0.04 mmol CaCO₃ m^&minus;2 h^&minus;1 under seawater conditions of double the ambient <i>p</i>CO₂. These experimental results provide support for the conclusion that some net calcifying communities could become subject to net dissolution in response to anthropogenic ocean acidification within this century. Nevertheless, individual corals remained healthy, actively calcified (albeit slower than at present rates), and deposited significant amounts of CaCO₃ under the prevailing experimental seawater conditions of elevated <i>p</i>CO₂. % vor jede Referenz Agegian, C. R.: The biogeochemical ecology of Porolithon gardineri (foslie), Ph.D. dissertation, Univ. of Hawaii, Honolulu, 1985. Alexandersson, E. T.: Etch patterns on calcareous sediment grains: petrographic evidence of marine dissolution of carbonate minerals, Science, 189, 47–48, 1975a. Alexandersson, E. T.: Marks of unknown carbonate-decomposing organelles in cyanophyte borings, Nature, 254, 212–238, 1975b. Andersson, A. J., Bates, N. R., and Mackenzie, F. T.: Dissolution of carbonate sediments under rising $p$CO₂ and ocean acidification: observations from Devil's Hole, Bermuda, Aquat. Geochem., 13, 237–264, 2007. Andersson, A. J., Mackenzie, F. T., and Ver, L. M.: Solution of shallow-water carbonates: an insignificant buffer against rising atmospheric CO₂, Geology, 31, 513–516, 2003. Andersson, A. J., Mackenzie, F. T., and Lerman, A.: Coastal ocean and carbonate systems in the high CO₂ world of the Anthropocene, Am. J. Sci., 305, 875–918, 2005. Andersson, A. J., Mackenzie, F. T., and Lerman, A.: Coastal ocean CO₂-carbonic acid-carbonate sediment system of the Anthropocene, Global Biogeochem. Cy., 20, GB1S92, doi:10.1029/2005GB002506, 2006. Andersson, A. J., Mackenzie, F. T., and Bates, N. R.: Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers, Mar. Ecol. Prog. Ser., 373, 265–273, 2008. Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S., and Hoegh-Guldberg, O.: Ocean acidification causes bleaching and productivity loss in coral reef builders, P. Natl. Acad. Sci., 105, 17442–17446, 2008. Bates, N. R.: Seasonal variability of the effect of coral reefs on seawater CO₂ and air-sea CO₂ exchange, Limnol. Oceanogr., 47, 43–52, 2002. Boucher, G., Clavier, J., Hily, C., and Gattuso, J.-P.: Contribution of soft-bottoms to the community metabolism (primary production and calcification) of a barrier reef flat (Moorea, French Polynesia), J. Exp. Mar. Biol. Ecol., 225, 269–283, 1998. Caldeira, K. and Wickett, M. E.: Anthropogenic carbon and ocean pH, Nature, 425, 365–365, 2003. Cohen, A. L. and McConnaughey, T. A.: Geochemical perspectives on coral mineralization, in: Biomineralization, Reviews in Mineralogy and Geochemistry, vol. 54, edited by: Dove, P. M., De Yoreo, J. J., and Weiner, S., Mineralogical Society of America, 151–187, 2003. Dickson, A. and Millero, F. J.: A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media, Deep-Sea Res., 38, 1733–1743, 1987. DOE: Handbook of Methods for the Analysis of the Various Parameters of the Carbon Dioxide System in Sea Water, v. 2, edites by: Dickson, A. G. and Goyet, C., ORNL/CDIAC-74, 1994. Frankignoulle, M., Gattuso, J.-P., Biondo, R., Bourge, I., Copin-Montégut, and Pichon, M.: Carbon fluxes in coral reefs. II. Eularian study of inorganic carbon dynamics and measurement of air-sea CO₂ exchanges, Mar. Ecol. Prog. Ser., 145, 123–132, 1996. Gao, K., Aruga, Y., Asada, K., Ishihara, T., Akano, T., and Kiyohara, M.: Calcification in the articulated coralline alga \textitCoralline pilulifera, with special reference to the effect of elevated CO₂ concentration, Mar. Biol., 117, 129–132, 1993. Gattuso, J.-P., Allemand, P. D., and Frankignoulle, M.: Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry, Am. Zool., 39, 160–183, 1999. Gattuso, J.-P., Pichon, M., Delesalle, B., Canon, C., and Frankignoulle, M.: Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air-sea CO₂ disequilibrium, Mar. Ecol. Prog. Ser., 145, 109–121, 1996. Gazeau, F., Quiblier, C., Jansen, J. M., Gattuso, J.-P., Middelburg, J. J., and Heip, C. H. R.: Impact of elevated CO₂ on shellfish calcification, Geophys. Res. Lett., 34, L07603, doi:10.1029/2006GL028554, 2007. Grasshoff, K., Kremling, K., and Ehrhardt, M. (Eds.): Methods of Seawater Analysis, 2nd ed., Verlag Chemie, Weinheim, Germany, 1983. Hoegh-Guldberg, O.: Low coral cover in a high-CO₂ world, J. Geophys. Res., 110, C09S06, doi:10.1029/2004JC002528, 2005. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E.: Coral reefs under rapid climate change and ocean acidification, Science, 318, 1737–1742, 2007. IPCC: Climate change 2001: The scientific basis, Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change, edited by: Houghton, J. T., Ding, Y., Griggs, D. J., Noguer, M., van der Linden, P. J., Dai, X., Maskell, K., and Johnson, C. A., Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. Jokiel, P. L., Rodgers, K. S., Kuffner, I. B., Andersson, A. J., Cox, E. F., and Mackenzie, F. T.: Ocean acidification and calcifying reef organisms: a mesocosm investigation, Coral Reefs, 27, 473–483, doi:10.1007/s00338-008-0380-9, 2008. Kayanne, H., Suzuki, A., and Saito, H.: Diurnal changes in the partial pressure of carbon dioxide in coral reef water, Science, 269, 214–216, 1995. Kinsey, D. W.: Alkalinity changes and coral reef calcification, Limnol. Oceanogr., 23, 989–991, 1978. Kleypas, J. A., Buddemeier, R. W., Archer, D., Gattuso, J.-P., Langdon, C., and Opdyke, B. N.: Geochemical consequences of increased atmospheric carbon dioxide on coral reefs, Science, 284, 118–120, 1999. Kleypas, J. A., Feely, R. A., Fabry, V. J., Langdon, C., Sabine, C. L., and Robbins, L. L.: 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 US Geological Survey, 2006. Kuffner, I. B. and Paul, V. J.: Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic cyanobacteria from Cocos Lagoon, Guam, Mar. Ecol. Prog. Ser., 222, 63–72, 2001. Kuffner, I. B., Andersson, A. J., Jokiel, P., Rodgers, K. S., and Mackenzie, F. T.: Decreased abundance of crustose coralline algae due to ocean acidification, Nature Geosci., 1, 114–117, 2008. Langdon, C. and Atkinson, M.: Effect of elevated $p$CO₂ on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment, J. Geophys. Res., 110, C09S07 doi:10.1029/2004JC002576, 2005. Langdon, C., Takahashi, T., Sweeney, C., Chipman, D., Goddard, J., Marubini, F., Aceves, H., Barnett, H., and Atkinson, M.: Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef, Global Biogeochem. Cy., 14, 639–654, 2000. Leclercq, N., Gattuso, J.-P., and Jaubert, J.: Primary production, respiration, and calcification of a coral reef mesocosm under increased CO₂ partial pressure, Limnol. Oceanogr., 47, 558–564, 2002. Lewis, E. and Wallace, D. W. R.: Program Developed for CO₂ System Calculations, ORNL/CDIAC-105: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee, 1998. Mackenzie, F. T., Lerman A., and Ver, L. M.: Recent past and future of the global carbon cycle, in: Geological Perspectives of Global Climate Change, AAPG Studies in Geology, edited by: Gerhard, L. C., Harrison, W. E., and Hanson, B. M., The American Association of Petroleum Geologists, Tulsa, 47, 51–82, 2001. Martin, S. and Gattuso, J.-P.: Response of Mediterranean coralline algae to ocean acidification and elevated temperature, Glob. Change Biol., 15, 2089–2100, 2009. Marubini, F., Ferrier-Pagés, C., and Cuif, J.-P.: Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison, P. Roy. Soc. London B, 270, 179–184, 2003. McDonald, M. R., McClintock, J. B., Amsler, C. D., Rittschof, D., Angus, R. A., Orihuela, B., and Lutostanski, K.: Effects of ocean acidification over the life history of the barnacle \textitAmphibalanus amphitrite, Mar. Ecol. Prog. Ser., 385, 179–187, 2009. McNeil, B. I., Matear, R. J., and Barnes, D. J.: Coral reef calcification and climate change: the effect of ocean warming, Geophys. Res. Lett., 31, L22309, doi:10.1029/2004GL021541, 2004. Mehrbach, C., Culberson, C. H., Hawley, J. E., and Pytkowicz, R. M.: Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure, Limnol. Oceanogr., 18, 897–907, 1973. Milliman, J. D.: Production and accumulation of calcium carbonate in the ocean: Budget of a nonsteady state, Global Biogeochem. Cy., 7, 927–957, 1993. Milliman, J. D. and Droxler, A. W.: Neritic and pelagic carbonate sedimentation in the marine environment: ignorance is not bliss, Geol. Rundsch., 85, 496–504, 1996. Morse, J. W., Andersson, A. J., and Mackenzie, F. T.: Initial responses of carbonate-rich shelf sediments to rising atmospheric $p$CO₂ and ocean acidification: role of high Mg-calcites, Geochim. Cosmochim. Acta, 70, 5814–5830, 2006. Morse, J. W. and Mackenzie, F. T.: Geochemistry of sedimentary carbonates, Elseiver Science Publishing Co., 1990. Ohde, S. and van Woesik, R.: Carbon dioxide flux and metabolic processes of a coral reef, Okinawa, B. Mar. Sci., 65, 559–576, 1999. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G. K., Rodgers, K. B., Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M. F., Yamanaka, Y., and Yool, A.: Anthropogenic ocean acidification over the twenty-first century and its impacts on calcifying organisms, Nature, 437, 681–686, 2005. Reynaud, S., Leclercq, N., Romaine-Lioud, S., Ferrier-Pagès, C., and Gattuso, J.-P.: Interacting effects of CO₂ partial pressure and temperature on photosynthesis and calcification in a scleractinian coral, Glob. Change Biol., 9, 1660–1668, 2003. Sabine, C. L., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J. L., Wanninkhof, R., Wong, C. S., Wallace, D. W. R., Tilbrook, B., Millero, F. J., Peng, T. -H., Kozyr, A., Ono, T., and Rios, A.: The oceanic sink for anthropogenic CO₂, Science, 305, 367–371, 2004. Schneider, K. and Erez, J.: The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral \textitAcropora eurystoma, Limnol. Oceanogr., 51, 1284–1293, 2006. Silverman, J., Lazar, B., and Erez, J.: Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef, J. Geophys. Res., 112, C05004, doi:10.1029/2006JC003770, 2007. Silverman, J., Lazar, B., Cao, L., Caldeira, K., and Erez, J.: Coral reefs may start dissolving when atmospheric CO₂ doubles, Geophys. Res. Lett., 36, L05606, doi:10.1029/2008GL036282, 2009. Smith, A. D. and Roth, A. A.: Effect of carbon dioxide concentration on calcification in the coralline alga \textitBossiella orbigniana, Mar. Biol., 52, 217–225, 1979. Smith, S. V, Jokiel, P. L., Key, G. S., and Guinther, E. B.: Metabolic responses of shallow tropical benthic microcosm communities to perturbation, Environmental Protection Agency, Narragansett, Rhode Island, Final report of contract R800906, onlina available at: http://CRAMP.wcc.hawaii.edu/, 1977. Smith, S. V. and Key, G. S.: Carbon dioxide and metabolism in marine environments, Limnol. Oceanogr., 20, 493–495, 1975. Smith, S. V. and Kinsey, D. W.: Calcification and organic carbon metabolism as indicated by carbon dioxide, in: Coral reefs: research methods edited by: Stoddart, D. R. and Johannes, R. E., Monogr. Oceanogr. Methodol. 5. UNESCO, 469–484, 1978. Tribollet, A.: The boring microflora in modern coral reef ecosystems: a review of its roles, in: Current Developments in Bioerosion, edited by: Wisshak, M. and Tapanila, L., Springer-Verlag Berlin Heidelberg, 2008. Tribollet, A., Godinot C., Atkinson, M., and Langdon, C.: Effects of elevated $p$CO₂ on dissolution of carbonates by microbial euendoliths, Global Biogeochem. Cy., 23, GB3008, doi:10.1029/2008GB003286, 2009. Yates, K. K. and Halley, R. B.: CO$_3^2-$ concentration and $p$CO₂ thresholds for calcification and dissolution on the Molokai reef flat, Hawaii, Biogeosciences, 3, 357–369, 2006. Zeebe, R. E. and Wolf-Gladrow, D.: CO₂ in seawater: equilibrium, kinetics, isotopes, Elseiver Science, 2003.