References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-11-929-2014

Changes in calcification of coccoliths under stable atmospheric CO2

Berger

¹ Meier

K. J. S.

¹ Kinkel

² Baumann

K.-H.

https://orcid.org/0000-0003-2109-5179

Christian-Albrechts-Universität zu Kiel, Institute of Geosciences, Ludewig-Meyn-Str. 10, 24118 Kiel, Germany

University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark

Universität Bremen, Department of Geosciences, 28334 Bremen, Germany

20 02 2014

11 4 929 944

2014

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

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The full text article is available as a PDF file from https://bg.copernicus.org/articles/11/929/2014/bg-11-929-2014.pdf

The response of coccolithophore calcification to ocean acidification has been studied in culture experiments as well as in present and past oceans. The response, however, is different between species and strains, and for the relatively small carbonate chemistry changes observed in natural environments, a uniform response of the entire coccolithophore community has not been documented so far. Moreover, previous palaeo-studies basically focus on changes in coccolith weight due to increasing CO2 and the resulting changes in the carbonate system, and only few studies focus on the influence of other environmental factors. In order to untangle changes in coccolithophore calcification due to environmental factors such as temperature and/or productivity from changes caused by increasing pCO2 and decreasing carbonate ion concentration, we here present a study on coccolith calcification from the Holocene North Atlantic Ocean. The pre-industrial Holocene, with its predominantly stable atmospheric CO2, provides the conditions for such a comprehensive analysis. For an analysis on changes in major components of Holocene coccolithophores under natural conditions, the family Noelaerhabdaceae was selected, which constitutes the main part of the assemblage in the North Atlantic. Records of average coccolith weights from three Holocene sediment cores along a north–south transect in the North Atlantic were analysed. During the Holocene, mean weight (and therefore calcification) of Noelaerhabdaceae (Emiliania huxleyi and Gephyrocapsa) coccoliths decreased at the Azores (Geofar KF 16) from around 7 to 6 pg, but increased at the Rockall Plateau (ODP site 980) from around 6 to 8 pg, and at the Vøring Plateau (MD08-3192) from 7 to 10 pg. The amplitude of average weight variability is within the range of glacial–interglacial changes that were interpreted to be an effect of decreasing carbonate ion concentration. By comparison with SEM assemblage counts, we show that weight changes are not only partly due to variations in the coccolithophore assemblage but also an effect of a change in calcification and/or morphotype variability within single species. Our results indicate that there is no single key factor responsible for the observed changes in coccolith weight. A major increase in coccolith weight occurs during a slight decrease in carbonate ion concentration in the late Holocene at the Rockall Plateau and Vøring Plateau. Here, more favourable productivity conditions apparently lead to an increase in coccolith weight, either due to the capability of coccolithophore species, especially E. huxleyi, to adapt to decreasing carbonate ion concentration or due to a shift towards heavier calcifying morphotypes.

References 1

Andersson, C., Pausata, F. S. R., Jansen, E., Risebrobakken, B., and Telford, R. J.: Holocene trends in the foraminifer record from the Norwegian Sea and the North Atlantic Ocean, Clim. Past, 6, 179–193, <a href="http://dx.doi.org/10.5194/cp-6-179-2010">https://doi.org/10.5194/cp-6-179-2010</a>, 2010.

Andruleit, H.: Coccolithophoriden im Europäischen Nordmeer: Sedimentation und Akkumulation; sowie ihre Entwicklung während der letzten 15 000 Jahre, Berichte aus dem Sonder-forschungsbereich, 313, Christian-Albrechts-Universität, Kiel, 59, 1995.

Andruleit, H.: A filtration technique for quantitative studies of coccoliths, Micropaleontology, 42, 403– 406, 1996.

Andruleit, H. A. and Baumann, K.-H.: History of the Last Deglaciation and Holocene in the Nordic Seas as revealed by coccolithophore assemblages, Mar. Micropaleontol., 35, 179–201, 1998.

Bach, L. T., Bauke, C., Meier, K. J. S., Riebesell, U., and Schulz, K. G.: Influence of changing carbonate chemistry on morphology and weight of coccoliths formed by Emiliania huxleyi, Biogeosciences, 9, 3449–3463, <a href="http://dx.doi.org/10.5194/bg-9-3449-2012">https://doi.org/10.5194/bg-9-3449-2012</a>, 2012.

Bassinot, F. C. and Labeyrie, L. D.: Shipboard Scientific Party (1996): IMAGES MD101 Brest- Marseille 29/05/95–11/07/95 – A coring cruise of the R/V Marion Dufresne in the North Atlantic Ocean and Norwegian Sea, Les rapports de campagnes à la mer, Institut Français pour la Recherche et la Technologie Polaires, Technopole de Brest-lroise, BP75–29280 Plouzane, Francee de Brest-lroise, BP75–29280 Plouzane, France, 96, 217 pp., 1996.

Baumann, K.-H., Andruleit, H., Böckel, B., Geisen, M. and Kinkel, H.: The significance of extant coccolithophores as indicators of ocean water masses, surface water temperature, and palaeoproductivity: a review, Paläontologische Zeitschrift, 79, 93–112, 2005.

Beaufort, L.: Weight estimates of coccoliths using the optical properties (birefringence) of calcite, Micropaleontology, 51, 289–297, 2005.

Beaufort, L. and Heussner, S.: Seasonal dynamics of calcareous nannoplankton on a West European continental margin: the Bay of Biscay, Mar. Micropaleontol., 43, 27–55, 2001.

Beaufort, L. and Dollfus, D.: Automatic recognition of coccoliths by dynamical neural networks, Mar. Micropaleontol., 51, 57–73, <a href="http://dx.doi.org/10.1016/j.marmicro.2003.09.003">https://doi.org/10.1016/j.marmicro.2003.09.003</a>, 2004.

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, <a href="http://dx.doi.org/10.1029/2006GC001493">https://doi.org/10.1029/2006GC001493</a>, 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, <a href="http://dx.doi.org/10.1038/nature10295">https://doi.org/10.1038/nature10295</a>, 2011.

Berner, K., Koç, N., Godtliebsen, F., and Divine, D.: Holocene climate variability of the Nor-wegian Atlantic Current during high and low solar insolation forcing, Paleoceanography, 26, PA2220, <a href="http://dx.doi.org/10.1029/2010PA002002">https://doi.org/10.1029/2010PA002002</a>, 2011.

Birks, C. and Koç, N.: A high-resolution diatom record of late-Quaternary sea-surface tempera- tures and oceanographic conditions from the eastern Norwegian Sea, Boreas, 31, 323–344, 2002.

Blindheim, J. and Østerhus, S.: The Nordic Seas, main oceanographic features, in: The Nordic Seas, An Integrated Perspective, edited by: Drange, H., Dokken, T., Furevik, T., Gerdes, R., and Berger, W., Geophysical Monograph Series 158, American Geophysical Union, Washington DC, 11–38, 2005.

Boeckel, B., Baumann, K.-H., Henrich, R., and Kinkel, H.: Coccolith distribution patterns in South Atlantic and southern Ocean surface sediments in relation to environmental gradients, Deep-Sea Res. Pt. I, 53, 1073–1099, <a href="http://dx.doi.org/10.1016/j.dsr.2005.11.006">https://doi.org/10.1016/j.dsr.2005.11.006</a>, 2006.

Bollmann, J.: Morphology and biogeography of Gephyrocapsa coccoliths in Holocene sediments, Mar. Micropaleontol., 29, 319–350, 1997.

Bollmann, J. and Herrle, J.: Morphological variation of Emiliania huxleyi and sea surface salinity, Earth Planet. Sc. Lett., 255, 273–288, <a href="http://dx.doi.org/10.1016/j.epsl.2006.12.029">https://doi.org/10.1016/j.epsl.2006.12.029</a>, 2007.

Bollmann, J., Herrle, J. O., Cortés, M. Y., Fielding, S. R.: The effect of sea water salinity on the morphology of Emiliania huxleyi in plankton and sediment samples, Earth Planet. Sc. Lett., 284, 320–328, <a href="http://dx.doi.org/10.1016/j.epsl.2009.05.003">https://doi.org/10.1016/j.epsl.2009.05.003</a>, 2009.

Calvo, E., Grimalt, J., and Jansen, E.: High resolution U37K sea surface temperature recon- struction in the Norwegian Sea during the Holocene, Quaternary Sci. Rev., 21, 1385–1394, 2002.

Colmenero-Hidalgo, E., Flores, J. A., and Sierro, F. J.: Biometry of Emiliania huxleyi and its biostratigraphic significance in the eastern North Atlantic Ocean and western Mediterranean Sea in the last 20 000 years, Mar. Micropaleontol., 46, 247–263, 2002.

De Bodt, C., Van Oostende, N., Harlay, J., Sabbe, K., and Chou, L.: Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite pro- duction, the coccolith morphology and the coccosphere size, Biogeosciences, 7, 1401–1412, <a href="http://dx.doi.org/10.5194/bg-7-1401-2010">https://doi.org/10.5194/bg-7-1401-2010</a>, 2010.

Doney, S., Fabry, V., Feely, R., and Kleypas, J.: Ocean acidification: the other CO2 problem, Annual Review of Marine Science, 1, 169–192, 2009.

Duplessy, J. C., Labeyrie, L., Juillet-Leclerc, A., Maitre, F., Duprat, J., and Sarnthein, M.: Surface salinity reconstruction of the North Atlantic Ocean during the last glacial maximum, Oceanol. Acta, 14, 311–324, 1991.

Duplessy, J. C., Cortijo, E., and Kallel, N.: Marine records of Holocene climatic variations, C. R. Geosci., 337, 87–95, <a href="http://dx.doi.org/10.1016/j.crte.2004.08.007">https://doi.org/10.1016/j.crte.2004.08.007</a>, 2005.

Engel, A., Zondervan, I., Aerts, K., Beaufort, L., Benthien, A., Chou, L., Delille, B., Gattuso, J. P., Harlay, J., Heemann, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M. D., Rochelle- Newall, E., Schneider, U., Terbrueggen, A., Riebesell, U.: Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments, Limnol. Oceanogr., 50, 493–507, 2005.

Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C.: Impacts of ocean acidification on marine fauna and ecosystem processes, ICES J. Mar. Sci., 65, 414–432, <a href="http://dx.doi.org/10.1093/icesjms/fsn048">https://doi.org/10.1093/icesjms/fsn048</a>, 2008.

Feely, R. A., Sabine, C. L., Kitack, L., Berelson, W., Kleypas, J., Fabry, V. J., and Millero, F. J.: Impact of anthropogenic CO2 on the CaCO3 system in the ocean, Science, 305, 362–366, 2004

Fielding, S. R., Herrle, J. O., Bollmann, J., Worden, R. H., and Montagnes, D. J. S.: Assessing the application of Emiliania huxleyi coccolith morphology as a sea-surface salinity proxy, Limnol. Oceanogr., 54, 5, 1475–1480, 2009.

Flores, J. A., Colmenero-Hidalgo, E., Mejía-Molina, A. E., Baumann, K.-H., Henderiks, J., Lars- son, K., Prabhu, C. N., Sierro, F. J., and Rodrigues, T.: Distribution of large Emiliania huxleyi in the Central and Northeast Atlantic as a tracer of surface ocean dynamics during the last 25 000 years, Mar. Micropaleontol., 76, 53–66, <a href="http://dx.doi.org/10.1016/j.marmicro.2010.05.001">https://doi.org/10.1016/j.marmicro.2010.05.001</a>, 2010.

Flores, J.-A., Filippelli, G. M., Sierro, F. J., and Latimer, J.: The "white ocean" hypothesis: a late pleistocene southern ocean governed by coccolithophores and driven by phosphorus, Front. Microbiol., 3, 233, <a href="http://dx.doi.org/10.3389/fmicb.2012.00233">https://doi.org/10.3389/fmicb.2012.00233</a>, 2012.

Gattuso, J., Frankignoulle, M., Bourge, I., Romaine, S., and Buddemeier, R.: Effect of calcium carbonate saturation of seawater on coral calcification, Global Planet. Change, 18, 37–46, 1998.

Giraudeau, J., Monteiro, P., and Nikodemus, K.: Distribution and malformation of living coccolithophores in the northern Benguela upwelling system off Namibia, Mar. Micropaleontology, 22, 93–110, 1993

Giraudeau, J., Grelaud, M., Solignac, S., Andrews, J., Moros, M., and Jansen, E.: Millennial-scale variability in Atlantic water advection to the Nordic Seas derived from Holocene coccolith concentration records, Quaternary Sci. Rev., 29, 1276–1287, <a href="http://dx.doi.org/10.1016/j.quascirev.2010.02.014">https://doi.org/10.1016/j.quascirev.2010.02.014</a>, 2010.

Grelaud, M., Schimmelmann, A., and Beaufort, L.: Coccolithophore response to climate and surface hydrography in Santa Barbara Basin, California, AD 1917–2004, Biogeosciences, 6, 2025–2039, <a href="http://dx.doi.org/10.5194/bg-6-2025-2009">https://doi.org/10.5194/bg-6-2025-2009</a>, 2009.

Hagino, K., Okada, H., and Matsuoka, H.: Coccolithophore assemblages and morphotypes of Emiliania huxleyi in the boundary zone between the cold Oyashio and warm Kuroshio currents off the coast of Japan, Mar. Micropaleontol., 55, 19–47, 2005.

Hagino, K., Bendif, E. M., Young, J. R., Kogame, K., Probert, I., Takano, Y., Horiguchi, T., de Vargas, C., and Okada, H.: New evidence for morphological and genetic variation in the cosmopolotan coccolithophore Emiliania huxleyi (Prymnesiophyceae) from the COX1b-ATP4 GENES1, J. Phycol., 47, 1164–1176, <a href="http://dx.doi.org/10.1111/j.1529-8817.2011.01053.x">https://doi.org/10.1111/j.1529-8817.2011.01053.x</a>, 2011.

Hansen, B. and Østerhus, S.: North Atlantic-nordic seas exchanges, Prog. Oceanogr., 45, 109–208, 2000.

Henderiks, J., Winter, A., Elbrächter, M., Feistel, R., Plas, der, A., Nausch, G., and Barlow, R.: Environmental controls on Emiliania huxleyi morphotypes in the Benguela coastal upwelling system (SE Atlantic), Mar. Ecol.-Prog. Ser., 448, 51–66, <a href="http://dx.doi.org/10.3354/meps09535">https://doi.org/10.3354/meps09535</a>, 2012.

Indermühle, A., Stocker, T. F., Joos, F., Fischer, H., Smith, J., Wahlen, M., DeCk, B., Mastroianni, D., Tschumi, J., and Blunier, T.: Holocene carbon-cycle dynamics based on CO2 trapped in ice at Taylor Dome, Antarctica, Nature, 398, 121–126, 1999.

IPCC (Intergovernmental Panel on Climate Change): Global Climate Projections, edited by: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M., and Miller, H. L. , Climate Change 2007: The Physical Science Basis, Contribution of Working Group I to the Fourth Assessment of the Intergovernmental Panel on Climate Change, Cambridge and New York: Cambridge University, 747–845, 2007.

Jansen, E., Raymo, M. E., Blum, P., Anderson, E. S., Austin, W. E. N., Baumann, K-H., Bout- Roumazeilles, V., Carter, S. J., Channell, J. E. T., Cullen, J. L., Flower, B., Higgins, S., Hodell, D. A., Hood, J. A., Hyun, S., Ikehara, M., King, T., Larter, R., Lehman, B., Locker, S., Mclntyre, K., McManus, J., Meng, L. B., O'Commell, S., Ortiz, J. D., Rack, F. R., Solheim, A., and Wei, W.: Proceedings of the ODP Initial Reports, 162, College Station, TX (Ocean Drilling Program), 1182 pp., 1996.

Jansen, E., Blum, P., and Party, S. S.: Gamma-ray attenuation measurements of bulk density using whole-core multi-sensing track on Hole, 162, 980B, <a href="http://dx.doi.org/10.1594/PANGAEA.259998">https://doi.org/10.1594/PANGAEA.259998</a>, 2005.

Kayano, K. and Shiraiwa, Y.: Physiological regulation of coccolith polysaccharide production by phosphate availability in the coccolithophorid Emiliania huxleyi, Plant Cell Physiol., 50, 1522–1531, <a href="http://dx.doi.org/10.1093/pcp/pcp097">https://doi.org/10.1093/pcp/pcp097</a>, 2009.

Kissel, C., Kleiven, K., and Morin, X.: Les rapports de champagnes à la mer – MD 168/AMOCINT IMAGES XVII on board R/V Marion Dufresne, Inst. Polaire Fr., Plouzané, France, 1–104, 2009.

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, 1116, <a href="http://dx.doi.org/10.1029/2001GB001765">https://doi.org/10.1029/2001GB001765</a>, 2002.

Kleijne, A., Kroon, D., and Zevenboom, W.: Phytoplankton and foraminiferal frequencies in northern Indian Ocean and Red Sea surface waters, Neth. J. Sea Res., 24, 531–539, <a href="http://dx.doi.org/10.1016/0077-7579(89)90131-2">https://doi.org/10.1016/0077-7579(89)90131-2</a>, 1989.

Klein, B. and Siedler, G.: On the Origin of the Azores Current, J. Geophys. Res., 94, 6159– 6168, 1989.

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, <a href="http://dx.doi.org/10.5194/bg-8-771-2011">https://doi.org/10.5194/bg-8-771-2011</a>, 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, <a href="http://dx.doi.org/10.1029/2005GC001227">https://doi.org/10.1029/2005GC001227</a>, 2006.

Langer, G., Gussone, N., Nehrke, G., Riebesell, U., Eisenhauer, A., and Thoms, S.: Calcium isotope fractionation during coccolith formation in Emiliania huxleyi: independence of growth and calcification rate, Geochem. Geophys. Geosys., 8, Q05007, <a href="http://dx.doi.org/10.1029/2006GC001422">https://doi.org/10.1029/2006GC001422</a>, 2007.

Lee, K., Tong, L. T., Millero, F. J., Sabine, C. L., Dickson, A. G., Goyet, C., Park, G. H., Wan- ninkhof, R., Feely, R. A., and Key, R. M.: Global relationships of total alkalinity with salinity and temperature in surface waters of the world's oceans, Geophys. Res. Lett., 33, L19605, <a href="http://dx.doi.org/10.1029/2006GL027207">https://doi.org/10.1029/2006GL027207</a>, 2006.

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 37831-6290, USA, 1998.

Lohbeck, K. T., Riebesell, U., and Reusch, T. B. H.: Adaptive evolution of a key phytoplankton species to ocean acidification, Nat. Geosci., 5, 346–351, <a href="http://dx.doi.org/10.1038/ngeo1441">https://doi.org/10.1038/ngeo1441</a>, 2012.

Lototskaya, A., Ziveri, P., Ganssen, G. M., and van Hinte, J. E.: Calcareous nannofloral response to Termination II at 45 N, 25 W (northeast Atlantic), Mar. Micropaleontol., 34, 47–70, 1998.

Marchal, O., Cacho, I., Stocker, T. F., Grimalt, J. O., Calvo, E., Martrat, B., Shackleton, N., Vautravers, M., Cortijo, E., van Kreveld, S., Andersson, C., Koç, N., Chapman, M., Sbaffi, L., Duplessy, J. C., Sarnthein, M., Turon, J. L., Duprat, J., and Jansen, E.: Apparent long-term cooling of the sea surface in the northeast Atlantic and Mediterranean during the Holocene, Quaternary Sci. Rev., 21, 455–483, 2002.

Medlin, L. K., Barker, G., Campbell, L., Green, J. C., Hayes, P. K., Marie, D., Wrieden, S., and Vaulot, D.: Genetic characterisation of Emiliania huxleyi (Haptophyta), J. Marine Syst., 9, 13–31, 1996.

Meier, K. J. S., Beaufort, L., Heussner, S., and Ziveri, P.: The role of ocean acidification in Emiliania huxleyi coccolith thinning in the Mediterranean Sea, Biogeosciences Discuss., 10, 19701–19730, <a href="http://dx.doi.org/10.5194/bgd-10-19701-2013">https://doi.org/10.5194/bgd-10-19701-2013</a>, 2014.

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

Müller, M. N., Beaufort, L., Bernard, O., Pedrotti, M. L., Talec, A., Sciandra, A.: Influence of CO2 and nitrogen limitation on the coccolith volume of Emiliania huxleyi (Haptophyta), Biogeosciences 9, 4155–4167, <a href="http://dx.doi.org/10.5194/bg-9-4155-2012">https://doi.org/10.5194/bg-9-4155-2012</a>, 2012.

Nielsen, J. E. Ø.: Variability at Ocean Weather Station M in the Norwegian Sea, ICES Mar. Sc., 219, 371–374, 2003.

Okada, H. and McIntyre, A.: Seasonal distribution of modern coccolithophores in the western North Atlantic Ocean, Mar. Biol., 54, 319–328, 1979.

Okada, H. and Wells, P.: Late Quaternary nannofossil indicators of climate change in two deep-sea cores associated with the Leeuwin Current off Western Australia, Palaeogeogr. Palaeocl., 131, 413–432, 1997.

Oppo, D., McManus, J., and Cullen, J.: Evolution and demise of the last interglacial warmth in the subpolar North Atlantic, Quaternary Sci. Rev., 25, 3268–3277, <a href="http://dx.doi.org/10.1016/j.quascirev.2006.07.006">https://doi.org/10.1016/j.quascirev.2006.07.006</a>, 2006.

Paillard, D., Labeyrie, L., and Yiou, P.: Macintosh program performs time-series analysis, EOS, Transactions of the American Geophysical Union, USA, 77, 379 pp., 1996.

Ploug, H., Hvitfeldt Iversen, H., Koski, M., and Buitenhuis, E. T.: Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: direct measurements of ballasting by opal and calcite, Limnol. Oceanogr., 53, 469–476, 2008.

Pollard, R. T., Read, J. F., Holliday, N. P., and Leach, H.: Water masses and circulation pathways through the Iceland Basin during Vivaldi 1996, J. Geophys. Res, 109, C04004, <a href="http://dx.doi.org/10.1029/2003JC002067">https://doi.org/10.1029/2003JC002067</a>, 2004.

Poulton, A. J., Young, J. R., Bates, N. R., Balch, W. M.: Biometry of detached Emiliania huxleyi coccoliths along the Patagonian Shelf, Marine Ecology Progress Series, 433, 1–17, <a href="http://dx.doi.org/10.3354/meps09445">https://doi.org/10.3354/meps09445</a>, 2011.

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, The Royal Society, Policy Document 12/05, 60 pp., 2005.

Read, J. F.: CONVEX-91: water masses and circulation of the Northeast Atlantic subpolar gyre, Prog. Oceanogr., 48, 461–510, 2001.

Read, B. A., Kegel, J., Klute, M. J., Kuo, A., Lefebvre, S. C., Maumus, F., Mayer, C., Miller, J., Monier, A., Salamov, A., Young, J., Aguilar, M., Claverie, J.-M., Frickenhaus, S., Gonzales, K., Herman, E. K., Lin, Y.-C., Napier, J., Ogata, H., Sarno, A. F., Shmutz, J., Schroeder, D., de Vargas, C., Verret, F., von Dassow, P., Valentin, K., Van de Peer, Y., Wheeler, G., Dacks, J. B., Delwiche, C. F., Dyhrman, S. T., Glöckner, G., John, U., Richards, T., Worden, A. Z., Zhang, X., and Grigoriev, I. V.: Pan genome of the phytoplankton Emiliania underpins its global distribution, Nature, 499, 209–213, <a href="http://dx.doi.org/10.1038/nature12221">https://doi.org/10.1038/nature12221</a>, 2013.

Richter, T.: Sedimentary fluxes at the Mid-Atlantic Ridge: sediment sources, accumulation rates, and geochemical characterization, GEOMAR Rep. 73, GEOMAR Res. Cent. for Mar. Geosci., Christian Albrechts Univ., Kiel, Germany, 1998.

Rickaby, R., Bard, E., Sonzogni, C., Rostek, F., Beaufort, L., Barker, S., Rees, G., and Schrag, D. P.: Coccolith chemistry reveals secular variations in the global ocean carbon cycle?, Earth Planet. Sc. Lett., 253, 83–95, <a href="http://dx.doi.org/10.1016/j.epsl.2006.10.016">https://doi.org/10.1016/j.epsl.2006.10.016</a>, 2007.

Riebesell, U., Zondervan, I., Rost, B. \`E., Tortell, P. D., Zeebe, R. E., and Morel, F. M. M.: Re- duced calcification of marine plankton in response to increased atmospheric CO2, Nature, 407, 364–367, 2000.

Rios, A. F., Pérez, F. F., Álvarez, M., Mintrop, L., González-Dávila, M., Santana Casiano, J. M., Lefèvre, N., Watson, A. J.: Seasonal sea-surface carbon dioxide in the Azores area, Marine Chemistry, 96, 35–51, doi10.1016/j.marchem.2004.11.001, 2005.

Risebrobakken, B., Jansen, E., Andersson, C., Mjelde, E., and Hevrøy, K.: A high-resolution study of Holocene paleoclimatic and paleoceanographic changes in the Nordic Seas, Paleoceanography, 18, 1017, <a href="http://dx.doi.org/10.1029/2002PA000764">https://doi.org/10.1029/2002PA000764</a>, 2003.

Rogerson, M., Rohling, E. J., Weaver, P., and Murray, J. W.: The Azores front since the last glacial maximum, Earth Planet. Sc. Lett., 222, 779–789, <a href="http://dx.doi.org/10.1016/j.epsl.2004.03.039">https://doi.org/10.1016/j.epsl.2004.03.039</a>, 2004.

Satoh, M., Iwamoto, K., Suzuki, I., and Shiraiwa, Y.: Cold stress stimulates intracellular calcification by the coccolithophore, Emiliania huxleyi (Haptophyceae) under phosphate-deficient conditions, Mar. Biotechnol., 11, 327–333, 2009.

Schwab, C., Kinkel, H., Weinelt, M., and Repschläger, J.: Coccolithophore paleoproductivity and ecology response to deglacial and Holocene changes in the Azores Current System, Paleoceanography, 27, PA3210, <a href="http://dx.doi.org/10.1029/2012PA002281">https://doi.org/10.1029/2012PA002281</a>, 2012.

Sigman, D. M. and Haug, G. H.: The Biological Pump in the Past, Treatise on Geochemistry, 6, 491–528, 2003.

Smith, H. E. K., Tyrrell, T., Charalampopoulou, A., Dumousseaud, C., Legge, O. J., Birchenough, S., Pettit, L. R., Garley, R., Hartman, S. E., Hartman, M. C., Sagoo, N., Daniels, C. J., Achterberg, E. P., and Hydes, D. J.: Predominance of heavily calcified coccolithophores at low CaCO3 saturation during winter in the Bay of Biscay, P. Natl. Acad. Sci. USA, 109, 8845–8849, <a href="http://dx.doi.org/10.1073/pnas.1117508109">https://doi.org/10.1073/pnas.1117508109</a>, 2012.

Solignac, S., Grelaud, M., de Vernal, A., Giraudeau, J., Moros, M., McCave, I. N., and Hoogakker, B.: Reorganization of the upper ocean circulation in the mid-Holocene in the northeastern Atlantic, Can. J. Earth Sci., 45, 1417–1433, <a href="http://dx.doi.org/10.1139/E08-061">https://doi.org/10.1139/E08-061</a>, 2008.

Stolz, K. and Baumann, K.-H.: Changes in palaeoceanography and palaeoecology during Marine Isotope Stage (MIS) 5 in the eastern North Atlantic (ODP Site 980) deduced from calcareous nannoplankton observations, Palaeogeography, Palaeoclimatology, Palaeoecology, 292, 295–305, <a href="http://dx.doi.org/10.1016/j.palaeo.2010.04.002">https://doi.org/10.1016/j.palaeo.2010.04.002</a>, 2010.

Takahashi, T. Sutherland, S. C., Sweeney, C., Poisson, A., Metzl, N., Tilbrook, B., Bates, N., Wanninkhof, R., Feely, R. A., Sabine, C., Olafsson, J., and Nojiri, Y.: Global sea-air CO2 flux based on climatological surface ocean pCO2, and seasonal biological temperature effects, Deep-Sea Res. Pt. II, 49, 1601–1622, 2002.

Tans, P. P. and Conway, T. J.: Monthly Atmospheric CO2 Mixing Ratios from the NOAA CMDL Carbon Cycle Cooperative Global Air Sampling Network, 1968-2002. In Trends: A Compendium of Data on Global Change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tenn., USA, 2005.

Triantaphyllou, M., Dimiza, M., Krasakopoulou, E., Malinverno, E., Lianou, V., and Souvermezoglou, E.: Seasonal variation in Emiliania huxleyi coccolith morphology and calcification in the Aegean Sea (Eastern Mediterranean), Geobios, 43, 99–110, <a href="http://dx.doi.org/10.1016/j.geobios.2009.09.002">https://doi.org/10.1016/j.geobios.2009.09.002</a>, 2010.

Van Kreveld, S., Knappertsbusch, M., Ottens, J., Ganssen, G. M., and Van Hinte, J. E.: Biogenic carbonate and ice-rafted debris (Heinrich layers) accumulation in deep-sea sediments from a Northeast Atlantic piston core, Mar. Geol., 131, 21–46, 1996.

Waelbroeck, C., Labeyrie, L., Michel, E., Duplessy, J., McManus, J., Lambeck, K., Balbon, E., and Labracherie, M.: Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records, Quaternary Sci. Rev., 21, 295–305, 2002.

Weaver, P. P. E. and Pujol, C.: History of the last deglaciation in the alboran sea (western Mediterranean) and adjacent north Atlantic as revealed by coccolith floras, Palaeogeogr. Palaeocl., 64, 35–42, <a href="http://dx.doi.org/10.1016/0031-0182(88)90140-X">https://doi.org/10.1016/0031-0182(88)90140-X</a>, 1988.

Westbroek, P., Brown, C. W., Bleijswijk, J., Brownlee, C., Brummer, G. J., Conte, M., Egge, J., Fernández, E., Jordan, R., Knappertsbusch, M., Stefels, J., Veldhuis, M., van der Wal, P., and Young, J.: A model system approach to biological climate forcing, The example of Emiliania huxleyi, Global Planet. Change, 8, 27–46, 1993.

Young, J. 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.

Young, J., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., and Østergaard, J.: A guide to extant coccolithophore taxonomy, Journal of Nannoplankton Research, 1, 1–125, 2003.

Zeebe, R. E. and Wolf-Gladrow, D.: CO2 in Seawater: Equilibrium, Kinetics, Isotopes: Equilibrium, Kinetics, Isotopes, Elsevier Science, Amsterdam, 2001.

Zeebe, R. E.: History of Seawater Carbonate Chemistry, Atmospheric CO2 and Ocean Acidification, Annu. Rev. Earth Planet. Sci., 40, 141–165, 2012.

Ziveri, P. and Thunell, R.: Coccolithophore export production in Guaymas Basin, Gulf of California: response to climate forcing. Deep-Sea Res. Pt. II, 47, 2073–2100, 2000.

Ziveri, P., Baumann, K., Böckel, B., Bollmann, J., and Young, J.: Biogeography of selected Holocene coccoliths in the Atlantic Ocean, Coccolithophores – from Molecular Processes to Global Impact, Springer, Berlin, 403 pp., 2004.

Ziveri, P., de Bernardi, B., Baumann, K.-H., Stoll, H., and Mortyn, P.: Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean, Deep-Sea Res. Pt. II, 54, 659–675, <a href="http://dx.doi.org/10.1016/j.dsr2.2007.01.006">https://doi.org/10.1016/j.dsr2.2007.01.006</a>, 2007.

Zondervan, I., Zeebe, E., Rost, B., Riebesell., U.: Decreasing marine biogenic calcification: A negative feedback on rising atmospheric pCO2, Global Biogeochem. Cy., 15, 507–516, 2001.

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

100

Zondervan, I.: The effect of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores – A review, Deep-Sea Res. Pt. II, 54, 521–537, 2007.