Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 5 2009 10.5194/bg-6-877-2009 http://www.biogeosciences.net/6/877/2009/ http://www.biogeosciences.net/6/877/2009/bg-6-877-2009.html http://www.biogeosciences.net/6/877/2009/bg-6-877-2009.pdf 877 885 2009-05-20 Primary production during nutrient-induced blooms at elevated CO₂ concentrations J. K. Egge jorun.egge@bio.uib.no T. F. Thingstad A. Larsen A. Engel J. Wohlers R. G. J. Bellerby U. Riebesell Department of Biology, University of Bergen, 5020 Bergen, Norway Alfred Wegener Institute (AWI) for Marine and Polar Research, Am Handelshafen 12, 27570 Bremerhaven, Germany Bjerknes Centre for Climate Research, University of Bergen, Allégaten 55, 5007 Bergen, Norway IFM-GEOMAR, Leibniz Institute of Marine Sciences, Kiel University, Düsternbrooker Weg 20, 24105 Kiel, Germany A CO₂ enrichment experiment (PeECE III) was carried out in 9 mesocosms in which the seawater carbonate system was manipulated to achieve three different levels of <i>p</i>CO₂. At the onset of the experimental period, nutrients were added to all mesocosms in order to initiate phytoplankton blooms. Primary production rates were measured by in-vitro incubations based on ¹⁴C-incorporation and oxygen production/consumption. Size fractionated particulate primary production was also determined by ¹⁴C incubation and is discussed in relation to phytoplankton composition. Primary production rates increased in response to nutrient addition and a net autotrophic phase with ¹⁴C-fixation rates up to 4 times higher than initial was observed midway through the 24 days experiment before net community production (NCP) returned to near-zero and ¹⁴C-fixation rates dropped below initial values. No clear heterotrophic phase was observed during the experiment. Based on the ¹⁴C-measurements we found higher cumulative primary production at higher <i>p</i>CO₂ towards the end of the experiment. CO₂ related differences were also found in size fractionated primary production. The most noticeable responses to CO₂ treatments with respect to primary production rates occurred in the second half of the experiment when phytoplankton growth had become nutrient limited, and the phytoplankton community changed from diatom to flagellate dominance. This opens for two alternative hypotheses that the effects are either associated with mineral nutrient limited growth, and/or with a change in phytoplankton species composition. The lack of a clear net heterotrophic phase in the last part of the experiment supports the idea that a substantial part of production in the upper layer was not degraded locally, but either accumulated or exported vertically. 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. Bellerby, R. G. J., Schulz. K. G., Riebesell, U., Neil, C., Nondal, G., Johannessen, T., and Brown, K. R.: Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences,~5,~1517–1527,~2008. Brett, M. T. and Goldman, C. R.: A meta-analysis of the freshwater trophic cascade, Proc. Natl. Acad. Sci, USA, 93, 7723–7726, 1996. Burkhardt S., Amoroso, G., Riebesell, U., and Sültemeyer, D.: CO₂ and HCO$_3^-$ uptake in marine diatoms acclimated to different CO₂ concentrations, Limnol. Oceanogr., 46, 1378–1391, 2001. Børsheim, K.I., Vadstein, O., Myklestad S.M., Reinertsen, H., Kirkvold, K., Olsen, Y.: Photosynthetic algal production, accumulation and realease of phytoplankton storage carbohydrates and bacterial production in a gradient in daily nutrient supply, J. Plank. Res., 27, 743–745, 2005. Carpenter, S. R.: Microcosm experiments have limited relevance for community and ecosystem ecology, Ecology, 77, 677–680, 1996. Clark, D. R. and Flynn, K. J.: The relationship between the dissolved inorganic carbon concentration and growth rate in marine phytoplankton, Proc. R. Soc. Lond., 267, 953–959, 2000. Delille, B., Harley, 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 $p$CO₂ during experimental blooms of the coccolithophorid Emiliania huxleyi, Global Biogeochem. Cy., 19, GB2023, doi:10.1029/2004GB002318, 2005. Dugdale, R. C. and Goering, J. J.: Uptake of new and regenerated forms of nitrogen in primary productivity, Limnol. Oceanogr., 12, 196–206, 1967. Egge, J. K.: Nutrient control of phytoplankton growth: Effects of macronutrients composition (N, P, Si) on species succession. Dr. Scient thesis, University of Bergen, Norway, ISBN: 82-7744-007-3, 1994. Egge, J. K. and Heimdal, B. R.: Blooms of phytoplankton including Emiliania huxleyi (Haptophyta). Effects of nutrient supply in different N:P ratios, Sarsia, 79, 333–348, 1994. Engel, A.: Direct relationship between CO₂ uptake and transparent exopolymer particles production in natural phytoplankton, J. Plank. Res., 24, 49–53, 2002. Engel, A.: Distribution of transparent exopolymer particles (TEP) in the northeast Atlantic Ocean and their potential significance for aggregation processes, Deep Sea Res., 51, 83–92, 2004. Engel, A., Delille, B., Jacquet, S., Riebesell, U., Rochelle-Newall, E., Terbrüggen, A., and Zondervan, I.: Transparent exopolymer particles and dissolved organic carbon production by Emiliania huxleyi exposed to different CO₂ concentrations: a mesocosm experiment, Aquat. Microb. Ecol., 34, 93–104, 2004. Engel, A., Zondervan, I., Aerts, K., Baufort, L., Benthien, A. Chou, L., Delille, B., Gattuso, J. P., Harley, J., Heeman, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M. D., Rochelle-Newall, E., Schneider, U., Terbrueggen, A., and Riebesell, U.: Testing the direct effect of CO₂ concentration on a bloom of the coccolithophorid Emiliania huxley$i$ in mesocosm experiment, Limnol. Oceanogr., 50, 493–507, 2005. Engel, A., Schulz, K., Riebesell, U., Bellerby, R., Delille, B., and Schartau, M.: Effects of CO₂ on particle size and phytoplankton abundance during a mesocosm bloom experiment (PeECE II), Biogeosciences, 5, 509–521, 2008. Gargas, E.: A manual for phytoplankton primary production studies in the Baltic, The Baltic Marine Biologists, Publication No. 2, The Danish Agency of Environmental Protection, Hørsholm, 1–88, 1975. Gazeau, F, Gattuso, J. P., Middleburg, J. J., Brion, N., Schiettecatte, L. S., Frankignoulle, M., and Borges, A. V.: Planktonic and whole system metabolism in a nutrient-rich estuary (the Scheldt estuary), Estuaries, 28, 868–833, 2005. Gazeau, F., Middelburg, J. J., Loijens, M., Vanderborght J.-H., Pizay, M.-D., and Gattuso, J.-P.: Planktonic primary production in estuaries: comparison of $^14$C, O₂ and $^18$O methods, Aquat. Microb. Ecol., 46, 95–106, 2007. Giordano, M., Beardall, J., and Raven, J. A.: CO₂ concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution, Annu. Rev. Plant. Biol., 56, 99–131, 2005. Grossart, H. P., Allgaier, M., Passow, U., and Riebesell, U.: Testing the effect of CO₂ concentration on the dynamics of marine heterotrophic bacterioplankton, Limnol. Oceanogr., 51, 1–11, 2006. Hare, C. E., Leblanc, K., DiTullio, G. R., Kudela, R. M., Zhang, Y., Lee, P. A., Risman, S., Hutchins, D. A.: Consequences of increased temperature and CO₂ for phytoplankton community in Bering Sea, Mar. Ecol. Prog. Ser., 352, 9–16, 2007. Hein, M. and Sand-Jensen, K.: CO₂ increases oceanic primary production, Nature, 338, 526–527, 1997. Joassin, P., Delille, B., Soetaert, K., Borges, A. V., Chou, L. Engel, A., Gattuso, J.-P., Harlay, J., Riebesell, U., Suykens, K., and Gregoire, M.: A mathematical modelling of bloom of the coccolithophore Emiliania huxleyi in a mesocosm experiment, Biogeosciences Discuss., 5, 787–840, 2008. Karl, D. M., Hebel, D. V., and Björmann, K.: The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific Ocean, Limol. Oceanogr. 43, 1270–1286, 1998. Kim, J.-M., Lee, K., Shin, K., Kang, J.-H., Lee, H.-W., Kim, M., Jang, P.-G., and Jang, M.-C.: The effect of seawater CO₂ concentration on growth of natural phytoplankton assemblage in a controlled mesocosm experiment, Limnol. Oceanogr. 51, 1629–1636, 2006. Marra, J.: Approches to the Measuremrnt of Plankton Production: Chapter 4 edited by: Williams, P. J. le B., Thomas, D. N., Reynolds, C. S., in: Primary Productivity. Carbon assimilation in marine and freshwater ecosystems, Blackwell Science, Oxford, 78–108, 2002. Leonardos, N. and Geider, R. J.: Elevated atmospheric carbon dioxide increases organic carbon fixation by Emiliania huxleyi (Haptophyta), under nutrient-limited high-light conditions, J. Phycol., 41, 1196–1203, 2005. Li, W. K. W.,and Irwin, B. D., and Dickie, P. M.: Variation related to biomass and productivity of phytoplankton and bacteria, Limnol. Oceanogr., 38, 483–494, 1993. Lizon, F. and Lagadeuc, Y.: Comparisons of primary production values estimated from different incubation times in a coastal sea, J. Plank. Res. 2, 371–381, 1998. Passow, U.: Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton, Mar. Ecol. Prog. Ser. 236, 1–12, 2002. Passow, U. and Alldredge, A. L.: A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP), Limnol. Oceanogr., 40, 1326–1335, 1995. 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. Pringault, O., Tassas, V., and Rochelle-Newall, E.: Consequences of respiration in the light on the determination of production in pelagic systems, Biogeosciences, 4, 105–114, 2007. Raven, J. A.: Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO₂ and temperature, Plant. Cell. Environ., 14, 779–774, 1991. Raven, J. A. and Johnston, A. M.: Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other recourses, Limnol. Oceanogr. 36, 1701–1714, 1991. Riebesell, U., Wolf-Gladrow, D., and Smetacek, V.: Carbon dioxide limitation of marine phytoplankton growth rates, Nature, 361, 249–251, 1993. Riebesell, U.: Effects of CO₂ enrichment on marine phytoplankton, J. Oceanogr. 60, 719–729, 2004. Riebesell, U., Schulz, K. G., Bellerby, R. G. J., Botros, M., Fritsche, P., Meyerhöfer, M., Neil, C., Nondal, G., Oschies, A., Wohlers, J., and Zöllner, E.: Enhanced biological carbon consumption in a high CO₂ ocean, Nature, 450, 545–548, doi:10.1038/nature06267, 2007. Rochelle-Newall, E., Delille, B., Frankignoulle, M., Gattuso, J. P., Jacquet, S., Riebesell, U., Terbruggen, A., and Zondervan, I.: Chromophoric dissolved organic matter in experimental mesocosms maintained under different $p$CO₂ levels, Mar. Ecol. Prog. Ser., 272, 25–31, 2004. Rost, B., Riebesell, U., Burkhardt, S. and Sültemeyer, D.: Carbon acquisition of bloom-forming phytoplankton, Limnol. Oceanogr., 48, 55–67, 2003. Savidge, G., Boyd, P., Pomroy, A., Harbour, D., and Joint, I.: Phytoplankton production and biomass estimates in the northeast Atlantic Ocean, May–June 1990, Deep-Sea Res., 42, 599–617, 1995. Sciandra, A., Harley, J., Lefèvre, D., Lemée, R., Rimmelin, P., Denis, M., and Gattuso, J. P.: Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO₂ under nitrogen limitation, Mar. Ecol. Prog. Ser., 261, 111–122, 2003. Schippers, P., Lürling, M., and Scheffer, M.: Increase of atmospheric CO₂ promotes phytoplankton productivity, Ecological Lett., 446–451, 2004. 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, Biogeosciences,~5,~707–718,~2008. Sobrino, C. S., Ward, M. L., and Neale, P. J.: Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom \textitThalassiosira pseudonana: Effects on growth, photosynthesis, and spectral sensitivity of photoinhibition, Limnol. Oceanogr., 53, 494–505, 2008. Sokal, R. R. and Rohlf, F. J.: Biometry, the principles and practice of statistics in biological research, 3rd Ed., 7th Printing, W. H. Freeman and Company, 887 pp., 2001. Steemann Nielsen, E.: The use of radioactive ($^14$C) for measuring organic production in the sea, J. Cons. Perm. Int. Expl. Mer., 18, 117–140, 1952. Tanaka, T., Thingstad, T. F., Løvdal, T., Grossart, H.-P., Larsen, A., Schulz, K., and Riebesell, U.: Availability of phosphate for phytoplankton and bacteria and of labile organic carbon for bacteria at different $p$CO₂ levels in mesocosm study, Biogeosciences,~5,~669–687,~2008. Thingstad, T. F., Hagstrom, A., and Rassoulzadegan, F.: Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop?, Limnol. Oceanogr., 42, 398–404, 1997. Tortell, P. D.: Evolutionary and ecological perspectives on carbon acquisition in phytoplankton, Limnol. Oceanogr., 45, 744–750, 2000. Tortell, P. D., DiTullino, G. R., Sigman, D. M., and Morel, F. M. M.: CO₂ effects on taxonomic composition and nutrient utilization in an Equatorial Pacific phytoplankton assemblage, Mar. Ecol. Prog. Ser., 236, 37–43, 2002. Wang, Z. A., Cai, W. J., Wang, Y. C., and Ji, H. W.: The southeastern continental shelf of the United States as an atmospheric CO₂ source and an exporter of inorganic carbon to the ocean, Continental Shelf Res, 25, 1917–1941, 2005. Williams, P. J. le B. and Lefèvre, D.: An assessment of the measurement of phytoplankton respiration rates from dark 14C incubations, Limnol. Oceanogr. Methods, 6, 1–11, 2008. Wolf-Gladrow, D., Riebesell, U., Burkhardt, S., and Bijma, J.: Direct effects of CO₂ concentration on growth and isotopic composition of marine plankton, Tellus, 51B, 461–476, 1999. Zondervan, I., Zeebe, R. E., Rost, B., and Riebesell, U.: Decreasing marine biogenic calcification: a negative feedback on rising atmospheric $p$CO₂, Global Biogeochem. Cy., 15, 507–516, 2001.