References

BGD

Biogeosciences Discussions

BGD

1810-6285

Copernicus GmbH

Göttingen, Germany

10.5194/bgd-9-4979-2012

Influence of CO2 and nitrogen limitation on the coccolith volume of Emiliania huxleyi (Haptophyta)

Müller

M. N.

¹ Beaufort

² Bernard

³ Pedrotti

M. L.

⁴ ⁵ Talec

⁴ ⁵ Sciandra

⁴ ⁵

Institute for Marine and Antarctic Studies (IMAS), Private Bag 129, Hobart, TAS 7001, Australia

CNRS/Université Aix-Marseille, CEREGE, 13545 Aix-en-Provence, Cedex 4, France

INRIA (French National Institute for Research in Computer Science and Automatic Control), BIOCORE, 2004 Route des Lucioles, 06902 Sophia-Antipolis, France

UPMC Univ. Paris 06, UMR7093, LOV, Observatoire océanologique, 06234 Villefranche/mer, France

CNRS, UMR7093, LOV, Observatoire océanologique, 06234 Villefranche/mer, France

25 04 2012

9 4 4979 5010

This is an open-access article ditributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

This article is available from http://www.biogeosciences-discuss.net/9/4979/2012/bgd-9-4979-2012.html

The full text article is available as a PDF file from http://www.biogeosciences-discuss.net/9/4979/2012/bgd-9-4979-2012.pdf

Coccolithophores, a key phytoplankton group, are one of the best studied organisms with regard to the response to ocean acidification/carbonation. The biogenic production of calcareous coccoliths has made coccolithophores a promising group for paleoceanographic research aiming to reconstruct past environmental conditions. Recently, geochemical and morphological analyses of fossil coccoliths have gained increased interest in regard to changes in seawater carbonate chemistry. The cosmopolitan coccolithophore Emiliania huxleyi (Lohm.) Hay and Mohler was cultured over a range of pCO2 levels in controlled laboratory experiments under nutrient replete and nitrogen limited conditions. Measurements of photosynthetic activity and calcification revealed, as previously published, an increase in organic carbon production and a moderate decrease in calcification from ambient to elevated pCO2. The enhancement in particulate organic carbon production was accompanied by an increase in cell diameter. Coccolith volume was best correlated with the coccosphere/cell diameter and no significant correlation was found between coccolith volume and particulate inorganic carbon production rate. The conducted experiments revealed that the coccolith volume of E. huxleyi is variable with aquatic CO2 concentration within the tested range but appears to be a primary function of the coccosphere/cell diameter both under nitrogen limited and nutrient replete conditions. Comparing coccolith morphological and geometrical parameters like volume, mass and size to physiological parameters under controlled laboratory conditions is an important step to understand variations in fossil coccolith geometry.

References 1

Bach, L T., Schulz, K G., and Riebesell, U.: Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore \textitEmiliania huxleyi, Limnol. Oceanogr., 55, 2040–2050, 2011.

Barcelos e Ramos, J., Müller, M. N., and Riebesell, U.: Short-term response of the coccolithophore \textitEmiliania huxleyi to an abrupt change in seawater carbon dioxide concentrations, Biogeosciences, 7, 177–186, http://dx.doi.org/10.5194/bg-7-177-2010doi:10.5194/bg-7-177-2010, 2010.

Beaufort, L., Probert, I., and Buchet, N.: Effects of acidification and primary production on coccolith weight: Implications for carbonate transfer from the surface to the deep ocean, Geochem. Geophy. Geosy., 8, Q08011, http://dx.doi.org/10.1029/2006GC001493doi:10.1029/2006GC001493, 2007.

Beaufort, L., Probert, I., de~Garidel-Thoron, T., Bendif, E M., Ruiz-Pino, D., Metzl, N., Goyet, C., Buchet, N., Coupel, P., Grelaud, M., Rost, B., Rickaby, R. E M., and de~Vargas, C.: Sensitivity of coccolithophores to carbonate chemistry and ocean acidification, Nature, 476, 80–83, http://dx.doi.org/10.1038/nature10295doi:10.1038/nature10295, 2011.

Borchard, C., Borges, A V., Händel, N., and Engel, A.: Biogeochemical response of \textitEmiliania huxleyi (PML B92/11) to elevated CO2 and temperature under phosphorous limitation: A chemostat study, J. Exp. Mar. Biol. Ecol., 410, 61–71, http://dx.doi.org/10.1016/j.jembe.2011.10.004doi:10.1016/j.jembe.2011.10.004, 2011.

Cubillos, J C., Wright, S W., Nash, G., de~Salas, M F., Griffiths, B., Tilbrook, B., Poisson, A., and Hallegraeff, G M.: Calcification morphotypes of the coccolithophorid \textitEmiliania huxleyi in the Southern Ocean: changes in 2001 to 2006 compared to historical data, Mar. Ecol.-Prog. Ser., 348, 47–54, 2007.

Davey, M., Tarran, G A., Mills, M M., Ridame, C., Geider, R J., and LaRoche, J.: Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic, Limnol. Oceanogr., 53, 1722–1733, 2008.

De Bodt, C., Van Oostende, N., Harlay, J., Sabbe, K., and Chou, L.: Individual and interacting effects of $p$CO2 and temperature on \textitEmiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size, Biogeosciences, 7, 1401–1412, http://dx.doi.org/10.5194/bg-7-1401-2010doi:10.5194/bg-7-1401-2010, 2010.

Dickson, A.: An exact definition of total alkalinity and a procedure for the estimation of alkalinity and total inorganic carbon from tritration data, Deep-Sea Res., 28, 609–623, 1981.

Ehrhardt, M. and Koeve, W.: Determination of particulate organic carbon and nitrogen, in: Methods of seawater analysis, edited by: Grasshoff, K., Kremling, K., and Erhardt, M., 3rd Edn., WILEY-VCH, 1999.

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, http://dx.doi.org/10.5194/bg-5-509-2008doi:10.5194/bg-5-509-2008, 2008.

Feng, Y., Warner, M., Zhang, Y., Sun, J., Fu, F.-X., Rose, J., and Hutchins, D.: Interactive effects of increased $p$CO2, temperature and irradiance on the marine coccolithophore \textitEmiliania huxleyi (Prymnesiophyceae), Eur. J. Phycol., 43, 87–98, 2008.

Feng, Y., Hare, C E., Leblanc, K., Rose, J M., Zhang, Y., DiTullio, G R., Lee, P A., Wilhelm, S W., Rowe, J M., Sun, J., Nemcek, N., Gueguen, C., Passow, U., Benner, I., Brown, C., and Hutchins, D.: Effects of increased $p$CO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response, Mar. Ecol.-Prog. Ser., 388, 13–25, 2009.

Findlay, H S., Calosi, P., and Crawfurd, K.: Determinants of the PIC:POC response in the coccolithophore \textitEmiliania huxleyi under future ocean acidification scenarios, Limnol. Oceanogr., 56, 1168–1178, 2011.

Finkel, Z V., Beardall, J., Flynn, K J., Quigg, A., Rees, T. A V., and Raven, J A.: Phytoplankton in a changing world: cell size and elemental stoichiometry, J. Plankton Res., 32, 119–137, 2010.

Fukuda, R., Ogawa, H., Nagata, T., and Koike, I.: Direct determination of carbon and nitrogen contents environments, Appl. Environ. Microb., 64, 3352–3358, 1998.

Guillard, R R.: Culture of phytoplankton for feeding marine invertebrates, in: Culture of marine invertebrates, edited by: Smith, W. and Chanley, M., Plenum, 1975.

Hansen, H P. and Koroleff, F.: Determination of nutrients, in: Methods of seawater analysis, edited by: Grasshoff, K., Kremling, K., and Erhardt, M., 3rd Edn., WILEY-VCH, 1999.

Henderiks, J.: Coccolithophore size rules – Reconstructing ancient cell geometry and cellular calcite quota from fossil coccoliths, Mar. Micropaleontol., 67, 143–154, 2008.

Herrmann, S., Weller, A F., Henderiks, J., and Thierstein, H R.: Global coccolith size variability in Holocene deep-sea sediments, Mar. Micropaleontol., 82–83, 1–12, 2012.

Hoppe, C. J M., Langer, G., and Rost, B.: \textitEmiliania huxleyi shows identical responses to elevated $p$CO2 in TA and DIC manipulations, J. Exp. Mar. Biol. Ecol., 406, 54–62, 2011.

Iglesias-Rodriguez, M D., Buitenhuis, E T., Raven, J A., Schofield, O., Poultan, A J., Gibbs, S., Halloran, P R., and de~Baar, H. J W.: Phytoplankton Calcification in a High-CO2 World (Response to technical comment), Science, 322, 336–340, http://dx.doi.org/10.1126/science.1154122doi:10.1126/science.1154122, 2008.

Koroleff, F.: Determination of total phosphorus, WILEY-VCH, Weinheim, 3rd Edn., 159–228, 1999.

Krug, S. A., Schulz, K. G., and Riebesell, U.: Effects of changes in carbonate chemistry speciation on Coccolithus braarudii: a discussion of coccolithophorid sensitivities, Biogeosciences, 8, 771–777, http://dx.doi.org/10.5194/bg-8-771-2011doi:10.5194/bg-8-771-2011, 2011.

Langer, G., Geisen, M., Baumann, K.-H., Kläs, J., Riebesell, U., Thoms, S., and Young, J R.: Species-specific responses of calcifying algae to changing seawater carbonate chemistry, Geochem. Geophy. Geosy., 7, Q09006, http://dx.doi.org/10.1029/2005GC001227doi:10.1029/2005GC001227, 2006.

Langer, G., Nehrke, G., Probert, I., Ly, J., and Ziveri, P.: Strain-specific responses of \textitEmiliania huxleyi to changing seawater carbonate chemistry, Biogeosciences, 6, 2637–2646, http://dx.doi.org/10.5194/bg-6-2637-2009doi:10.5194/bg-6-2637-2009, 2009.

Leonardos, N. and Geider, R J.: Elevated atmospheric carbon dioxide increases organic carbon fixation by \textitEmiliania huxleyi (Haptophyta), under nutrient-limited high-light conditions, J. Phycol., 41, 1196–1203, 2005.

Malara, G. and Sciandra, A.: A multiparameter phytoplanktonic culture system driven by microcomputer, J. Appl. Phycol., 3, 235–241, 1991.

Moore, C M., Mills, M M., Langlois, R., Milne, A., Achterberg, E P., LaRoche, J., and Geider, R J.: Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean, Limnol. Oceanogr., 53, 291–305, 2008.

Müller, M N., Antia, A N., and LaRoche, J.: Influence of cell cycle phase on calcification in the coccolithophore \textitEmiliania huxleyi, Limnol. Oceanogr., 53, 506–512, 2008.

Müller, M. N., Schulz, K. G., and Riebesell, U.: Effects of long-term high CO2 exposure on two species of coccolithophores, Biogeosciences, 7, 1109–1116, http://dx.doi.org/10.5194/bg-7-1109-2010doi:10.5194/bg-7-1109-2010, 2010.

Paasche, E.: Roles of nitrogen and phosphorus in coccolith formation in \textitEmiliania huxleyi (Prymnesiophyceae), Eur. J. Phycol., 33, 33–42, 1998.

Paasche, E.: Reduced coccolith calcite production under light-limited growth: a comparative study of three clones of \textitEmiliania huxleyi (Prymnesiophyceae), Phycologia., 38, 508–516, 1999.

Paasche, E.: A review of the coccolithophorid \textitEmiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions, Phycologia, 40, 503–529, 2002.

Porter, K G. and Feig, Y S.: The use of DAPI for identifying and counting aquatic microflora, Limnol. Oceanogr., 25, 943–948, 1980.

Poulton, A J., Yound, J R., Bates, N R., and Balch, W M.: Biometry of detached \textitEmiliania huxleyi coccoliths along the Patagonian Shelf, Mar. Ecol.-Prog. Ser., 443, 1–17, 2011.

Ridgwell, A., Schmidt, D. N., Turley, C., Brownlee, C., Maldonado, M. T., Tortell, P., and Young, J. R.: From laboratory manipulations to Earth system models: scaling calcification impacts of ocean acidification, Biogeosciences, 6, 2611–2623, http://dx.doi.org/10.5194/bg-6-2611-2009doi:10.5194/bg-6-2611-2009, 2009.

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., Bellerby, R. G J., Engel, A., Fabry, V J., Reusch, T. B H., Schulz, K G., and Morel, F. M M.: Phytoplankton Calcification in a High CO2 World (technical comment), Science, 322, 5907, http://dx.doi.org/10.1126/science.1161096doi:10.1126/science.1161096, 2008.

Riegmann, R., Noordeloos, A., and Cadee, G.: \textitPhaeocystis blooms and eutrophication of the continental coastal zones of the North Sea, Mar. Biol., 112, 479–484, 1992.

Riegmann, R., Stolte, W., Noordeloos, A., and Slezak, D.: Nutrient uptake and alkaline phosphatase (EC 3:1:3:1) activity of \textitEmiliania huxleyi (Prymnesiophyceae), J. Phycol., 36, 87–96, 2000.

Roy, R., Roy, L., Vogel, K., Porter-Moore, C., Pearson, T., Good, C., Millero, F., and Campbell, D.: The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45 °C, Mar. Chem., 44, 249–267, 1993.

Sciandra, A., Harlay, J., Lefèvre, D., Lemée, R., Rimmelin, P., Denis, M., and Gattuso, J.-P.: Response of coccolithophorid \textitEmiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation, Mar. Ecol.-Prog. Ser., 261, 111–122, 2003.

Shi, D., Xu, Y., and Morel, F. M. M.: Effects of the pH/$p$CO2 control method on medium chemistry and phytoplankton growth, Biogeosciences, 6, 1199–1207, http://dx.doi.org/10.5194/bg-6-1199-2009doi:10.5194/bg-6-1199-2009, 2009.

Young, J R. and Ziveri, P.: Calculation of coccolith volume and its use in calibration of carbonate flux estimates, Deep-Sea Res. Pt. II, 47, 1679–1700, 2000.

Zondervan, I., Rost, B., and Riebesell, U.: Effect of CO2 concentration on the PIC/POC ratio in the coccolithophore \textitEmiliania huxleyi grown under light-limiting conditions and different daylengths, J. Exp. Mar. Biol. Ecol., 272, 55–70, 2002.