Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 5 6 2008 10.5194/bg-5-1517-2008 http://www.biogeosciences.net/5/1517/2008/ http://www.biogeosciences.net/5/1517/2008/bg-5-1517-2008.html http://www.biogeosciences.net/5/1517/2008/bg-5-1517-2008.pdf 1517 1527 2008-11-10 Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment R. G. J. Bellerby richard.bellerby@bjerknes.uib.no K. G. Schulz U. Riebesell C. Neill G. Nondal E. Heegaard T. Johannessen K. R. Brown Bjerknes Centre for Climate Research, University of Bergen, Allégaten 55, 5007 Bergen, Norway Geophysical Institute, University of Bergen, Allégaten 70, 5007 Bergen, Norway Leibniz Institute for Marine Sciences (IFM-GEOMAR), Dusternbrooker Weg 20, 24105 Kiel, Germany Mohn-Sverdrup Center and Nansen Environmental and Remote Sensing Center, Thormølensgate 47, 5006 Bergen, Norway EECRG, Department of Biology, University of Bergen, Allégaten 41, 5007 Bergen, Norway Changes to seawater inorganic carbon and nutrient concentrations in response to the deliberate CO₂ perturbation of natural plankton assemblages were studied during the 2005 Pelagic Ecosystem CO₂ Enrichment (PeECE III) experiment. Inverse analysis of the temporal inorganic carbon dioxide system and nutrient variations was used to determine the net community stoichiometric uptake characteristics of a natural pelagic ecosystem perturbed over a range of <i>p</i>CO₂ scenarios (350, 700 and 1050 μatm). Nutrient uptake showed no sensitivity to CO₂ treatment. There was enhanced carbon production relative to nutrient consumption in the higher CO₂ treatments which was positively correlated with the initial CO₂ concentration. There was no significant calcification response to changing CO₂ in <i>Emiliania huxleyi</i> by the peak of the bloom and all treatments exhibited low particulate inorganic carbon production (~15 μmol kg^&minus;1). With insignificant air-sea CO₂ exchange across the treatments, the enhanced carbon uptake was due to increase organic carbon production. The inferred cumulative C:N:P stoichiometry of organic production increased with CO₂ treatment from 1:6.3:121 to 1:7.1:144 to 1:8.25:168 at the height of the bloom. This study discusses how ocean acidification may incur modification to the stoichiometry of pelagic production and have consequences for ocean biogeochemical cycling. Allgaier, M., Riebesell, U., Vogt, M., Thyrhaug, R., and Grossart, H.-P.: Coupling of heterotrophic bacteria to phytoplankton bloom development at different $p$CO₂ levels: a mesocosm study, Biogeosciences, 5, 1007–1022, 2008. Anderson, L. and Sarmiento, J.: Redfield ratios of remineralization determined by nutrient data analysis, Global Biogeochem. Cy., 8, 65–80, 1994. Anderson, T. R., Hessen, D. O., Elser, J. J., and Urabe, J.: Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers, Am. Nat., 165(1), 1–11, 2005. Banse, K.: Uptake of inorganic carbon and nitrate by marine plankton and the Redfield ratio, Global Biogeochem. Cy., 8, 81–84, 1994. Bellerby, R. G. J., Olsen, A., Furevik, T., and Anderson, L. A.: Response of the surface ocean CO₂ system in the Nordic Seas and North Atlantic to climate change, in: Climate Variability in the Nordic Seas, edited by: Drange, H., Dokken, T. M., Furevik, T., Gerdes, R., and Berger, W., Geophysical Monograph Series, AGU, 189–198, 2005. Berg, G. M., Glibert, P. M., and Chen, C,-C.: Dimension effects of enclosures on ecological processes in pelagic systems, Limnol. Oceanogr., 44(5), 1331–1340, 1999. Blackford, J. C. and Gilbert, F. J.: pH variability and CO₂ induced acidification in the North Sea, J. Marine Syst., 1–4, 229–241, 2007. Brezinski, M.: The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables, J. Phycol., 21, 347–357, 1985. Broecker, W. S.: Ocean geochemistry during glacial time, Geochimica Cosmochimica Acta, 46, 1689–1705, 1982. Caldeira, K. and Wickett, M. E.: Anthropogenic carbon and ocean pH, Nature, 425, 365–365, 2003. Canadell, J. G., Le Quéré, C., Raupach, M. R., Field, C. B., Buitenhuis, E. T., Ciais, P., Conway, T. J., Gillett, N. P., Houghton, R. A., and Marland, G.: Contributions to accelerating atmospheric CO₂ growth from economic activity, carbon intensity, and efficiency of natural sinks, Proceedings of the National Academy of Science, USA, doi:10.1073/pnas.0702737104, 2007. Carotenuto, Y., Putzeys, S., Simonelli, P., Paulino, A., Meyerhöfer, M., Suffrian, K., Antia, A., and Nejstgaard, J. C.: Copepod feeding and reproduction in relation to phytoplankton development during the PeECE III mesocosm experiment, Biogeosciences Discuss., 4, 3913–3936, 2007. Chen, C.-C., Petersen, J. E., and Kemp, W. M.: Spatial and temporal scaling of periphyton growth on walls of estuarine mesocosms, Mar. Ecol.-Prog. Ser., 155, 1–15, 1997. Delille, B., Harlay, J., Zondervan, I., Jacquet, S., Chou, L.,Wollast, R., Bellerby, R. G. J., Frankignoulle, M., Borges, A. V., Riebesell, U., and Gattuso, J.-P.: Response of primary production and calcification to changes of pCO₂ during experimental blooms of the coccolithophorid Emiliania huxleyi, Global Biogeochem. Cy., 19, GB2023, doi:10.1029/2004GB002318, 2005. Dickson, A. G.: Standard potential of the reaction: AgCl(s) + 1/2 H₂(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO$_4^-$ in synthetic seawater from 273.15 to 318.15 K, J. Chem. Thermodyn., 22, 113–127, 1990a. Dickson, A. G.: Thermodynamics of the dissociation of boric acid in synthetic sea water from 273.15 to 318.15 K, Deep-Sea Res., 37, 755–766, 1990b. Dickson, A. G. and Millero, F. J.: A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media, Deep-Sea Res., 34, 1733–1743, 1987. Egge, J. K., Thingstad, T. F., Engel, A., Bellerby, R. G. J., and Riebesell, U.: Primary production during nutrient-induced blooms at elevated CO₂ concentrations, Biogeosciences Discuss., 4, 4385–4410, 2007. Engel, A.: Direct relationship between CO₂ uptake and transparent exopolymer particles production in natural phytoplankton, J. Plankton Res., 24, 49–53, 2002. Engel, A., Thoms, S., Riebesell, U., Rochelle-Newall, E., and Zondervan, I.: Polysaccharide aggregation as a potenial sink of marine dissolved organic carbon, Nature, 428, 929–932, 2004. Engel, A., Zondervan, I., Aerts, K., Beaufort, L., Benthien, A., Chou, L., Delille, B., Gattuso, J.-P., Harley, J., Heemann, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M.-D., Rochelle-Newall, E., Schneider, U., Terbrüggen, A., and Riebesell, U.: Testing the direct effect of CO₂ concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments, Limnol. Oceanogr., 50, 493–504, 2005. Engel, A., Schulz, K. G., Riebesell, U., Bellerby, R., Delille, B., and Schartau, M.: Effects of CO₂ on particle size distribution and phytoplankton abundance during a mesocosm bloom experiment (PeECE II), Biogeosciences, 5, 509–521, 2008. Falck, E. and Anderson, L.G.: The dynamics of the carbon cycle in the surface water of the Norwegian Sea, Mar. Chem., 94, 43–53, 2005. Gattuso, J.-P., Frankignoulle, M., Bourge, I., Romaine, S., and Buddemeier, R. W.: Effect of calcium carbonate saturation of seawater on coral calcification, Global Planet. Change, 18, 37–46, 1998. Goldman, J. C. and Brewer, P. G.: Effect of nitrogen source and growth rate on phytoplankton-mediated changes in alkalinity, Limnol. Oceanogr., 25(2), 352–357, 1980. Gran, G.: Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid, Oceanologica Acta, 5, 209–218, 1952. Hein, M. and Sand-Jensen, K.: CO₂ Increases Oceanic Primary Production, Nature, 388(6642), 526–527, 1997. Heinze, C.: Simulating oceanic Ca CO₃ export production in the greenhouse, Geophys. Res. Lett., 31, L16308, doi:10.1029/2004GL020613, 2004. Johnson, K. M., Sieburth, J. M., Williams, P. J., and Brändström, L.: Coulometric total carbon analysis for marine studies: automation and calibration, Mar. Chem., 21, 117–133, 1987. Klaas, C. and Archer, D. E.: Association of sinking organic matter with various types of mineral ballast in the deep sea: Implications for the rain ratio, Global Biogeochem. Cy., 16(4), 1116, doi:10.1029/2001GB001765, 2002. Klausmeier, C. A., Litchman, E., Daufresne, T., and Levin, S. A.: Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Nature, 429, 171–174, 2004. 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 sponsored by NSF, NOAA and the USGS, 88 pp., 2006. Koeve, W.: C:N stoichiometry of the biological pump in the North Atlantic: Constraints from climatological data, Global Biogeochem. Cy., 20, GB3018, doi:10.1029/2004GB002407, 2006. Körtzinger, A., Hedges, J. I., and Quay, P. D.: Redfield ratios revisited: removing the biasing effect of anthropogenic CO₂, Limnol. Oceanogr., 46, 964–970, 2001. Kuss, J. and Schneider, B.: Chemical enhancement of the CO₂ gas exchange at a smooth seawater surface, Mar. Chem., 91, 165–174, 2004. Langdon, C., Broecker, W. S., Hammond, D. E., Glenn, E., Fitzsimmons, K., Nelson, S. G., Peng, T.-S., Hajdas, I., and Bonani, G.: Effect of elevated CO₂ on the community metabolism of an experimental coral reef, Global Biogeochem. Cy., 17, 1011, doi:10.1029/2002GB001941, 2003. Langer, G., Geisen, M., Kläs, J., Riebesell, U., Thoms, S., Young, J. R.: Species-specific responses of calcifying algae to changing seawater carbonate chemistry, Geochem. Geophy. Geosy., 7 (9), Q09006, doi:10.1029/2005GC001227, 2006. Larsen, J. B., Larsen, A., Thyrhaug, R., Bratbak, G., and Sandaa, R.-A.: Response of marine viral populations to a nutrient induced phytoplankton bloom at different $p$CO₂ levels, Biogeosciences, 5, 523–533, 2008. 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, U.S. Department of Energy, Oak Ridge, Tennessee, 1998. Merico, A., Tyrrell, T., and Cocakar, T.: Is there any relationship between phytoplankton seasonal dynamics and the carbonate system?, J. Marine Syst., 59, 120–142, 2006. Mintrop, L., Fernández-Pérez, F., González Dávila, M., Körtzinger, A., and Santana Casiano, J. M.: Alkalinity determination by potentiometry- intercalibration using three different methods, Ciencias Marinas, 26, 23–37, 2000. Nielsen, M. V.: Photosynthetic characteristics of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) exposed to elevated concentrations of dissolved inorganic carbon, J. Phycol., 31, 715–719, 1995. Omta, A. W., Bruggeman, J., Kooijman, S. A. L. M., and Dijkstra, H. A.: Biological carbon pump revisited: Feedback mechanisms between climate and the Redfield ratio, Geophys. Res. Lett., 33, L14613, doi:10.1029/2006GL026213, 2006. 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 impact on calcifying organisms, Nature, 437, 7059, 681–686, doi:10.1038/nature04095, 2005. Pahlow, M. and Riebesell, U.: Temporal trends in deep ocean Redfield ratios, Science, 287, 831–833, 2000. Paulino, A. I., Egge, J. K., and Larsen, A.: Effects of increased atmospheric CO₂ on small and intermediate sized osmotrophs during a nutrient induced phytoplankton bloom, Biogeosciences, 5, 739–748, 2008. Petersen, J. E., Cornwell, J. C., and Kemp, W. M.: Implicit scaling in the design of experimental aquatic ecosystems, Oikos, 85, 3–18, 1999. Pinheiro, J. C. and Bates, D. M.: Mixed-Effects Models in S and S-plus, Springer, New York, 527 pp., 2000. Raven, J., Caldeira, K., Elderfield, H., Hoegh-Guldberg, O., Liss, P., Riebesell, U., Shepherd, J., Turley, C., and Watson, A.: Ocean acidification due to increasing atmospheric carbon dioxide, Royal Society Report, 2005. Redfield, A. C., Ketchum, B. M., and Richards, F. A.: The influence of organism on the composition of seawater, in: The Sea, 2. Ed., edited by: Hill, M. N., Wiley, 26–77, 1963. Riebesell, U., Wolf-Gladrow, D. A., and Smetacek, V.: Carbon dioxide limitation of marine phytoplankton growth rates, Nature, 361, 249–251,1993. Riebesell, U., Schulz, K. G., Bellerby, R. G. J., Fritsche, P., Meyerhöfer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J., and Zöllner, E.: Enhanced biological carbon consumption in a high CO₂ ocean, Nature, 545–548, doi:10.1038/nature06267, 2007. Riebesell, U., Zondervan, I., Rost, B., Tortell, P. D., Zeebe, R. E., and Morel, F. M. M.: Reduced calcification of marine plankton in response to increased atmospheric CO₂, Nature, 407, 364–367, 2000. Riebesell, U.: Effects of CO$_2 $ enrichment on marine phytoplankton, J. Oceanogr., 60, 719–729, 2004. Ridgwell, A., Zondervan, I., Hargreaves, J. C., Bijma, J., and Lenton, T. M.: Assessing the potential long-term increase of oceanic fossil fuel CO₂ uptake due to CO₂-calcification feedback, Biogeosciences, 4, 481–492, 2007. Sabine, C. S., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J. L., Wanninkhof, R., Wong, C. S., Wallace, D. W. R., Tillbrook, B., Millero, F. J., Peng, T.-H., Kozyr, A., Ono, T., and Rios, A. F.: The oceanic sink for anthropogenic CO₂, Science, 305, 367–371, 2004. Sambrotto, R. N., Savidge, G., Robinson, C., Boyd, P., Takahashi, T., Karl, D. M., Langdon, C., Chipman, D., Marra, J., and Codispoti, L.: Elevated consumption of carbon relative to nitrogen in the surface ocean, Nature, 363, 248–250, 1993. Schulz, K. G., Riebesell, U., Bellerby, R. G. J., Biswas, H., Meyerhöfer, M., Müller, M. N., Egge, J. K., Nejstgaard, J. C., Neill, C., Wohlers, J., and Zöllner, E.: Build-up and decline of organic matter during PeECE III, Biogeosciences, 5, 707–718, 2008. Schuster, U. and Watson, A. J.: A variable and decreasing sink for atmospheric CO₂ in the North Atlantic, J. Geophys. Res., 112, C11006, doi:10.1029/2006JC003941, 2007. Sterner, R. W. and Elser, J. J.: Ecological Stoichiometry, Princeton University Press, Oxford, UK, 2002. Tanaka, T., Thingstad, T. F., Løvdal, T., Grossart, H.-P., Larsen, A., Allgaier, M., Meyerhöfer, M., Schulz, K. G., Wohlers, J., Zöllner, E., and Riebesell, U.: Availability of phosphate for phytoplankton and bacteria and of glucose for bacteria at different $p$CO₂ levels in a mesocosm study, Biogeosciences, 5, 669–678, 2008. Tortell, P. D., DiTullino, G. R., Sigman, D. M., and Morel, F. M. M.: CO₂ effects on taxonomic composition and nutrient utilisation in an Equatorial Pacific phytoplankton assemblage, Mar. Ecol.-Prog. Ser., 236, 37–43, 2002. Tyrrell, T. and Merico, A.: Emiliania huxleyi: bloom observations and the conditions that induce them, in: Coccolithophores: from molecular processes to global impact, edited by: Thierstein, H. R. and Young, J. R., Berlin, Germany, Springer, 75–97, 2004. Urabe, J., Togari, J., and Elser, J. J.: Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore, Glob. Change Biol., 9, 818–825, 2003. Volk, T. and Hoffert, M. I.: Ocean carbon pumps, analysis of relative strengths and efficiencies in ocean-driven atmospheric CO₂ changes, in: The Carbon Cycle and Atmospheric CO₂: Natural Variations Archean to Present, edited by: Sunquist, E. T. and Broecker, W. S., Geophysical Monograph Series, Vol 32, Washington, DC, 99–110, 1985. Wanninkhof, R. and Thoning, K.: Measurement of fugacity of CO₂ in surface water using continuous and discrete sampling methods, Mar. Chem., 44, 189–205, 1993. Weiss, R. F.: Carbon dioxide in water and seawater: the solubility of a non-ideal gas, Mar. Chem., 2, 203–215, 1974. Zondervan, I., Rost, B., and Riebesell, U.: Effect of CO₂ concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limited conditions and different daylengths, J. Exp. Mar. Biol. Ecol., 272, 55–70, 2002. Zondervan, I.: The effects of light, macronutrients, trace metals and CO₂ on the production of calcium carbonate and organic carbon in coccolithophores – A review, Deep-Sea Res. II, 54, 521–537, doi:10.1016/j.dsr2.2006.12.004, 2007.