Access

You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:

login

Log in to your personal account or through your institution.

Praeger Review: Effects on marine algae of changed seawater chemistry with increasing atmospheric CO 2

J.A. Raven
Biology and Environment: Proceedings of the Royal Irish Academy
Vol. 111B, No. 1 (May 2011), pp. 1-17
Published by: Royal Irish Academy
Stable URL: http://www.jstor.org/stable/23033877
Page Count: 17
  • Download PDF
  • Cite this Item
Praeger Review: Effects on marine algae of changed seawater chemistry with increasing atmospheric CO
          2
We're having trouble loading this content. Download PDF instead.

Abstract

The acid—base relations of plant (including algal) environments are complex, comprising geological processes as modified by biology including, especially over the last 200 years, man. Some habitats (e.g. high intertidal rockpools and some freshwater bodies) have pH variations of up to three units over a diel cycle as a result of photosynthesis and respiration. Other habitats, e.g. nutrient-poor open ocean habitats, have diel variations that are more than an order of magnitude smaller. Anthropogenic influences on acid—base relations of different habitats include the input to the atmosphere of gases that dissolve to produce acidic solutions. The quantitatively predominant gas is CO 2 , but SO 2 , NO x and NH y (via nitrification) can also be significant. The influence of the acidic gases in aquatic habitats (including the upper layers of peat bogs) and on terrestrial photosynthetic organisms alters the inorganic carbon speciation and pH around the photosynthetic cells. The calcified coralline marine red macroalgae, with benthic and unattached (maerl) life forms, have extracellular calcification; their calcification rate will decline in the future, with a more CO 2 -rich ocean and decreasing CO 3 2- concentrations. The marine planktonic coccolithophores have intracellular calcification, though the coccoliths themselves occur externally. While many coccolithophores show decreased calcification with increasing external CO 2 and the attendant decrease in external CO 3 2- , this is not universal. For both coralline red algae and coccolithophores the external CaCO 3 will dissolve when seawater becomes undersaturated with respect to the relevant crystal form of CaCO 3 . Overall, the effects of increased CO 2 alone are negligible or result in increased growth of non-calcified algae, while there is most generally a decreased growth of calcified algae.

Notes and References

This item contains 159 references.

REFERENCES
  • Adamczyk, K., Prement-Schwartz, M., Pines, D., Pines, E. and Nibbering, E.T.J. 2009 Real- time observations of carbonic acid formation in aqueous solution. Science 326, 1690—4.
  • Anning, K., Nimer, N.A., Merrett, M.J. and Brownlee, C. 1996 Costs and benefits of calcification in coccolithophorids. Journal of Marine Systems 9, 45-56.
  • Balch, W.H., Holligan, P.H. and Kilpatrick, K.A. 1992 Calcification, photosynthesis and growth of the bloom-forming coccolithophore, Emiliana huxleyi. Continental Shelf Research 12, 1353-74.
  • Balch, W.H., Fritz, J. and Fernandez, E. 1996 Decoupling calcification and photo- synthesis in the coccolithophore Emiliania huxleyi under steady-state light-limited growth. Marine Ecology Progress Series 142, 87-97.
  • Balch, W., Drapeau, D., Bowler, B. and Booth, E. 2007 Prediction of pelagic calcification rates using satellite measurements. Deep-Sea Research Part II Current Topics in Oceanography 54, 478-95.
  • Barcelos e Ramos, J., Miiller, M.N. and Riebesell, U. 2010 Short-term response of the cocco- lithophore Emiliamia huxleyi to an abrupt change in seawater CO , concentrations. Biogeoscience 7, 177-86.
  • Battarbee, R.K. 2010 Are our acidified upland waters are recovering? Freshwater Biological Association News 52, 4-5.
  • Beard, D.A. and Qian, H. 2007 Relationship between thermodynamic driving force and one way fluxes in reversible processes. PLoS ONE 2, el44. doi:10.1371/journal.pone.000144
  • Beman, A.M., Chow, C.E., King, A.L.K., Fend, Y., Fuhrman, J.A., Bates, N.R., Popp, B.N. and Hutchins, D.A. 2011 Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proceedings of the National Academy of Science USA 108, 208-13. doi:10.1073/ pnas.1011053108
  • Berge, T., Daugbjerg, N., Andersen, B.B. and Hansen, P.J. 2010 Effect of lowered pH on marine phytoplankton. Marine Ecology Progress Series 416, 79-91.
  • Berner, E.K. and Berner, R.A. 1996 Water, air and geochemical cycles. Old Tappan, NJ, USA. Prentice Hall.
  • Bethman, B. and Schonknecht, G. 2009 pH regu- lation in an acidophilic green alga - a quantitative analysis. New Phytologist 183, 327-39.
  • Bierman, A. and Engel, A. 2010 The effect of CO , on the properties and sinking velocity of aggre- gates of the coccolithophore Emiliania huxleyi. Biogeosciences 7, 1017—29.
  • Blake, C. and Maggs, C.A. 2003 Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from Northern Europe. Phycologia 42, 606—12.
  • Blinks, L.R. 1963 The effect of pH on the photo- synthesis of littoral marine algae. Protoplasma 57, 126-36.
  • Blunden, G., Campbell, S.A., Smith, J.R., Guiry, M.D., Hession, C.C. and Griffin, R.J. 1997 Chemical and physical characterization of calcified red algal deposits known as maerl. Journal of Applied Phycology 9, 11-7.
  • Borowitzka, M.A. 1981 Photosynthesis and calci- fication in the articulated coralline red algae Amphiroa anceps and A.foliacea. Marine Biology 62, 17-23.
  • Bosence, D.W. 1976 Ecological studies on two unattached coralline algae from Western Ireland. Palaeontology 19, 365—95.
  • Bosence, D. and Wilson, J. 2003 Maerl growth, carbonate production rates and accumulation rates in the northeast Atlantic. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S21—31.
  • Boyce, D.G., Lewis, M.R. and Worm, B. 2010 Global productivity decline over the last century. Nature 466, 591—6.
  • Breitbarth, E., Bellerby, R.J., Neill, C.C., Ardelan, M.V., Meyerhofer, M., Zollner, E., Croot, P.L. and Riebesell, U. 2010 Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7, 1063-73.
  • Broecker, W. and Clark, E. 2009 Ratio ofcocco- lith CaCO , to foraminifera CaCO ^ in late Holocene deep sea sediments. Paleoceanography 24, PA3205.
  • Buitenhuis, E.I., de Baar, H.J.W. and Veldhuis, M.J.W. 1999 Photosynthesis and calcifica- tion by Emiliania huxleyi (Prymnesiophyceae) as a function of inorganic carbon. Journal of Phycology 35, 949-59.
  • Butterfield, N.J. 2000 Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicelularity and the Mesoproterozic/ Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386—404.
  • Chierichi, M. and Fransson, A. 2009 Calcium carbonate saturation in the surface water of the Arctic Ocean: undersaturation in freshwater influenced shelves. Biogeosciences 6, 2421—32.
  • Chisholm, J.R.M. 2000 Calcification by crustose coralline algae on the Northern Great Barrier Reef, Australia. Limnology and Oceanography 45, 1476-84.
  • Cuvellier, M.L., Allen, A.E., Maren, A., McCrow, J.P., Messie, M., Tringe, S.G., Woyke, T., Welsh, R.M., Ishoey, T., Less, J-H., Binder, B.J., Dupont, C.L., Latasa, M., Guigard, C., Back, K.C., Dupont, C.L., Latasa, M., Caleo, E., Read, B., Lasken, R.S., Chavez, F.P. and Worden, A.T. 2010 Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Procedings of the National Academy of Sciences USA 107, 14679-84.
  • Davis, K.J., Dove, P.H. and De Yoreo, J.J. 2000 The role of magnesium as an impurity in calcite growth. Science 290, 1134-7.
  • DEFRA 2005 Ammonia in the UK. Available at http://www.defra.gov.uk/environment/quality/ air/airquali ty/publications/am monia/docu- ments/ammonia-in-uk.pdf (accessed 18 March 2011).
  • De Grave, S. and Whitaker, A. 1999 A census of maerl beds in Irish waters. Aquatic Conservation: Marine and Freshwater Ecosystems 9, 303—11.
  • Doney, S.C., Mahowald, N., Lima, I., Feely, R.A., Mackenzie, F.T., Lamarque, J.-F. and Rasch, P.J. 2007 Impact of anthrogenic atmospheric nitrogen and sulphur deposition in ocean acidifi- cation and the inorganic carbon system. Proceedngs of the National Academy of Sciences USA 104, 14580-5.
  • Doney, S.C., Fabry, V.J., Feeley, R.A. and Kleypas, J.A. 2009 Ocean acidification: the other CO , problem. Annual Review of Marine Science 1, 169-92.
  • Dore, J.E., Lukas, R., Sadler, D.W., Church, M.J. and Karl, D.M. 2009 Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proceedings of the National Academy of Sciences USA 106, 12235-40.
  • Dupont, S., Dorey, N. and Thorndyke, M. 2010 What meta-analyses tell us about the vulnerability of marine biodiversity to ocean acidification. Estuarine, Coastal and Shelf Science 89, 182-5.
  • Engel, A., Szlosek, J., Abrahamson, L., Liu, Z.F. and Lee, C. 2009a Investigating the effect of ballasting by CaCO , in Emiliania huxleyi: I. Formation, settling velocities and physical prop- erties of the aggregates. Deep-Sea Research Part II - Topical Studies in Oceanography 56, 1396- 1407.
  • Engel, A., Abrahamson, L., Szlosek, J., Liu, Z.F., Stewart, G., Hirschberg, D. and Lee, C. 2009b Investigating the effect of ballasting by CaCO , in Emiliania huxleyi: II. Decomposition of particulate organic matter. Deep-Sea Research Part II — Topical Studies in Oceanography 56, 1408-19.
  • Fernandez, E., Boyd, P., Holligan, P.M. and Harbour, D.S. 1993 Production of organic and inor- ganic carbon within large-scale coccolithophore bloom in the northeast Atlantic Ocean. Marine Ecology Progress Series 97, 271—87.
  • Fowler, D., Smith, R., Muller, J., Cape, J.N., Sutton, M., Erisman, J.W. and Fagerli, H. 2007 Long term trends in sulphur and nitrogen deposition in Europe and the cause of non-linearities. Water, Air and Soil Pollution Focus 7, 41—7.
  • Francis, St.P., Bunker, D., Brodie, J.A., Maggs, C.A. and Bunker, A.R. 2010 Seasearch guide to the seaweeds of Britain and Ireland. Ross-on-Wye, UK. Marine Conservation Society.
  • Gao, K., Aruga, Y., Asada, K., Ishihara, T., Akaro, T. and Kiyahara, M. 1993 Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO , . Marine Biology 117, 129-32.
  • Garrels, R.M. and Lerman, A. 1981 Phanerozoic cycles of sedimentary carbon and sulphur. Proceedings of the National Academy of Sciences of the USA 78, 4652-6.
  • Gattuso, J.-P., Frankignoule, M. and Wollast, R. 1998 Carbon and carbonate metabolism in coastal aquatic ecosystems. Annual Review of Ecology and Systematics 29, 405-34.
  • Giordano, M., Beardall, J. and Raven, J. A. 2005 CO , concentrating mechanisms in algae: mechanisms, environmental modulation and evolution. Annual Review of Plant Biology 56, 99—131.
  • Giordano, M., Norici, A., Ratti, S. and Raven, J.A. 2008 Role for sulphur for algae: acquisi- tion, metabolism, ecology and evolution. In R. Hell, C. Dahl, D. Knaff and T. Leustek (eds), Sulphur metabolism in phototrophic organisms, 405-23.
  • Dordrecht. Springer, Godoi, R.H.H., Aerts, K., Harley, J., Kaegi, R., Ro, C-U., Chou, L. and Van Grieken, R. 2009 Organic surface coating on cocco- lithophores - Emiliania huxleyi: its determination and implication in the marine carbon cycle. Microchemical Journal 91, 593-6.
  • Goldman, J.C. and Brewer, P.G. 1980 Effect of nitrogen source and growth rate on phytoplank- ton-linked changes in alkalinity. Limnology and Oceanography 25, 352-7.
  • Gravot, A., Dittami, S.M., Rousvoal, I.S., Lugier, R., Eggert, A., Collen, J., Boyen, C., Bouchereau, A. and Tonon, C. 2010 Diurnal oscillations of metabolite abundance and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytologist 188, 98-110.
  • Green, J.C. and Leadbeater, B.S.C. (eds) 1994 The haptophyte algae. Systematics Association Special Volume no. 51. Oxford. Oxford University Press.
  • Guan, W.C. and Gao, K.S. 2010a Impacts of UV radiation on photosynthesis and growth of the coccolithophore Emiliania huxleyi (Haptophyceae). Environmental and Experimental Botany 67, 502-8.
  • Guan, W.C. and Gao, K.S. 2010b Enhanced calci- fication ameliorates the negative effects of UV radiation on photosynthesis in the calcifying phytoplankter Emiliania huxleyi. Chinese Science Bulletin 55, 588—93.
  • Gurevitch, J. and Hedges, L.V. 1999 Statistical issues in ecological meta-analyses. Ecology 80, 1142-9.
  • Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransone, E., Fine, M., Turner, S.M., Rowley, S.J., Tedesco, D. and Buia, M.-C. 2008 Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 354, 96-9.
  • Harris, R.P. 1994 Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Marine Biology 119, 431—9.
  • Harris, G.N., Scanlan, D.J. and Geider, R.J. 2005 Acclimation of Emiliania huxleyi (Prymnesiophyceae) to photon flux density. Journal of Phycology 41, 851-62.
  • Hedges, L.V., Gurevitch, J. and Curtis, P.S. 1999 The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150—6.
  • Hendriks, I.E. and Duarte, C.M. 2010 Ocean acid- ification: separating evidence from judgement - a reply to Dupont et al. Estuarine, Coastal and Shelf Science 89, 186—94.
  • Hendriks, I.E., Duarte, C.M. and Alvarez, M. 2010 Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal and Shelf Science 86, 157—64.
  • Herfort, L., Loste, E., Meldrum, F. and Thake, B. 2004 Structural and physiological effects of calcium and magnesium in Emiliania huxleyi (Lohman) Hay and Mohler. Journal of Structural Biology 148, 307-14.
  • Ho, T.-Y., Quigg, A., Finkel, Z.V., Milligan, A.J., Wyman, K., Falkowski, P.G. and Morel, F.M.M. 2003 The elemental composition of some marine phytoplankton. Journal of Phycology 39, 1145-59.
  • Hofmann, G.E., Barry, J.P., Edmunds, P.J., Gates, R.D., Hutchins, D.A., Klinger, T. and Sewell, M.A. 2010 The effects of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annual Review of Ecology, Evolution and Systematics 41, 127-47.
  • Hurd, C.L., Hepburn, C.D., Currie, K.I., Raven, J.A. and Hunter, K.A. 2009 Testing the effects of ocean acidification on algal metabolism: consider- ations for experimental design.Journal of Phycology 45, 1030-51. doi:10.1111/j.1529.8817.2009. 00768.x
  • Hutton, J. 1795 Theory of the Earth, with proofs and illustrations, Volumes I and II. Edinburgh. Creech. Hutton, J. 1889 Theory of the Earth, with proofs and illustrations, Volume III. Edited by Sir Archibald Geikie. London. Geological Society, Burlington House.
  • Hyde, P.B., Carton, O.T., O'Toole, P. and Musselbrook, T.H. 2003 A new inventory of ammonia emissions from Irish agriculture. Atmospheric Environment 37, 55—62.
  • Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, D.R.M., Tyrrell, T., Gibbs, S.J., von Passow, P., Rehm, E., Armbrust, E.V. and Boessenkoot, K.P. 2008a Phytoplankton calcification in a high-CO , world. Science 320, 336-40.
  • Iglesias-Rodriguez, M.D., Buitenhuis, E.J., Raven, J.A., Schofield, O., Poulton, A.J., Gibbs, M., Halloran, P.R. and de Baar, H.J.W. 2008b Comment on response to "Phytoplankton calcification in a high-CO , world". Science 322, 1466.
  • Irie, T., Bessho, K., Findlay, H.S. and Calosi, P. 2010 Increasing costs due to ocean acidi- fication drives phytoplankton to be more heavily calcified: optimal growth strategy of cocco- lithophores. PLoS ONE 5 (10), el3436.
  • Irvine, L.M. and Chamberlain, Y.M. 1994 Seaweeds of the British Isles. Volume I Rhodophyta. Part 2B Corallinales, Hildenbrandiales. London: Natural History Museum.
  • Jardiller, L., Zubkov, M.V., Pearman, J. and Scanlan, D.J. 2010 Significant CO , fixation by small Prymnesiophyceae in the subtropical and trop- ical Northeast Atlantic Ocean. ISME Journal 4, 1180-92.
  • Johnston, A.M., Maberly, S.C. and Raven, J. A. 1992 The acquisition of inorganic carbon by four red macroalgae from different habitats. Oecologia 92, 317—26.
  • Jones, M.R., Leith, I.D., Fowler, D., Raven, J.A., Sutton, M.A., Nemiz, E., Cape, J.N., Sheppard, L.J., Smith, R.I. and Theobald, M.R. 2007a Concentration-dependent NH; deposition processes for mixed moorland semi- natural vegetation. Atmospheric Environment 41, 2049-60.
  • Jones, M.R., Leith, I.D., Fowler, D., Raven, J.A., Sutton, M.A., Nemiz, E., Cape, J.N., Sheppard, L.J. and Smith, R.I. 2007b Concentration- dependent NH 1 deposition processes for stomatal and non-stomatal moorland species. Atmospheric Environment 41, 8980-94.
  • Katchalsky, A.K. and Curran, P.F. 1965 Non-equilibrium thermodynamics in biophsics. Cambridge, Mass, USA: Harvward University Press.
  • Kevekordes, K., Holland, D., Haubner, N., Jenkins, S., Kos, R., Roberts, S., Raven, J.A., Scrimgeour, C.M., Shelly, K., Stojkovic, S. and Beardall, J. 2006 Inorganic carbon acquisition by eight species of Caulerpa (Caulerpaceae, Chlorophyta). Phycologia 45, 442-9.
  • Kroeker, K.J., Kordas, R.L., Crim, R.N. and Singh, G.G. 2010 Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13, 1419—34.
  • Kubler, J.E., Johnston, A.M. and Raven, J. A. 1999 The effects of reduced and elevated CO , and O , on the seaweed, Lomentaria articulata. Plant, Cell and Environment 22, 1303—10.
  • Kuffner, I.B., Andersson, A.J., Jokiel, P.L., Rodgers, K.S. and Mackenzie, F.T. 2008 Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geosciences 1, 114-7.
  • Langer, G., Geisen, M., Baumann, K.H., Klas, J., Riebesell, U., Thoms, S. and Young, J.R. 2006 Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochemistry Geophysics Geosystems 7, art. no. Q09006.
  • Langer, G., Nehrke, G., Probert, J., Ly, J. and Ziveri, P. 2009 Strain-specific response of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6, 2637-46.
  • Langner, U., Jakob, T., Shehfest, K. and Wilhelm, C. 2008 An energy balance from absorbed photons to new biomass for Chlamydomonas rein- hardtii and Chlamydomonas acidophila under neutral and extremely acid growth conditions. Plant, Cell and Environment 32, 250—8.
  • Leonardos, N., Read, B., Thake, B. and Young, J.R. 2009 No mechanistic dependence of photosynthesis on calcification in Emiliania huxleyi (Haptophyta). Journal ofPhycology 45, 1046—51.
  • Littler, M.M., Littler, D.S. and Hanisak, M.D. 1991 Deep-water rhodolith distribu- tion, productivity, and growth history at sites of formation and subsequent degradation. Journal of Experimental Marine Biology and Ecology 150, 163-82.
  • Littler, M.M., Littler, D.S., Blair, S.M. and Norris, J.N. 1985 Deepest known plant life discovered on an uncharted seamount. Science 227, 57—9.
  • Liu, H., Probert, I., Uitz, J., Claustre, H., Aris- Broseau, S., Froda, M., Not, F. and de Vargas, C. 2009 Haptophytes rule the waves: extreme oceanic biodiversity in non-calcifying prymne- siophytes explains the 19-Hex paradox. Proceedings of the National Academy of Sciences USA 106, 12803-8. doi: 10.1073/pnas/0905841106.
  • Luther, H. 1947 Vorschlag zu einer okologische Grundeinteilung der Hydrophyten. Acta Botanica Fennica 44, 1-15.
  • Maberly, S.C. 1990 Exogenous inorganic carbon sources for photosynthesis by marine macroalgae. Journal of Phycology 26, 434—41.
  • Maberly, S.C. 1992 Carbonate ions appear to neither inhibit nor stimulate the use of bicar- bonate ions in photosynthesis by Ulva lactuca. Plant, Cell and Environment 15, 255-60.
  • Maberly, S.C. 1996 Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biology 38, 579-98.
  • Maberly, S.C., Raven, J.A. and Johnston, A.M. 1992 Discrimination between l2 C and ,3 C by marine plants. Oecologia 91, 481-92.
  • Mackinder, L., Wheeler, G., Schroeder, D., Riebesell, U. and Brownlee, C. 2010 Molecular mechanisms underlying calcification in coccco- lithophores. Geomicrobiology Journal 27, 583—95.
  • Mantone, P.T. 2010 Quantifying growth and calcium carbonate deposition in Calliarthron cheilosporoides (Corallinales, Rhodophyta) in the field using a persistent vital stain. Journal of Phycology 46, 13—7.
  • Marba, N., Duarte, C.M. and Agusti, S. 2007 Allometric scaling of plant life history. Proceedings of the National Academy of Sciences USA 104, 15777-80. doi: 10.1073/pnas.0703476104.
  • Messerli, M.A., Amaral-Zettler, L.A., Zettler, E., Jung, S.-K., Smith, P.J.S. and Sogin, M.L. 2005 Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile. Journal of Experimental Biology 208, 2569-79.
  • Middelboe, A.L. and Hansen, P.J. 2007 High pH in shallow water macroalgal habitats. Marine Ecology Progress Series 338, 107—17.
  • Milligan, A.J., Varela, D.E., Brzezinski, M.A. and Morel, F.M.M. 2004 Dynamics of silicon metabolism and silicon isotope discrimination in a marine diatom as a function of pCO,. Limnology and Oceanography 49, 322-9.
  • Miiller, M.N., Schulz, K.G. and Riebesell, U. 2010 Effects of long-term high CO, exposure on two species of cocolithophores. Biogeosciences 7, 1109—16.
  • Natori, Y., Haned, A. and Suzuki, Y. 2006 Vertical and seasonal differences in biogenic silica disso- lution in natural seawater in Suruga Bay, Japan: effects of temperature and organic matter. Marine Chemistry 102, 230—41.
  • Neilsen, L.T., Jakobsen, H.H., and Hansen, P.J. 2010 High resilience of two coastal plankton communities to twenty-first century seawater acidification: evidence from microcosm studies. Marine Biology Research 6, 542—55.
  • Nobel, P.S. 2005 Physicochemical and environmental plant physiology. 3rd edn. Burlingtom, MA, USA. Academic Elsevier.
  • O'Boyle, S. and Silke, J. 2010 A review of phyto- plankton ecology in estuarine and coastal waters around Ireland. Journal of Plankton Research 32, 99-118.
  • Odum, H.T. and Pinkerton, R.C. 1955 Time's speed regulator: the optimum efficiency for maximum power output in physical and biological systems. American Scientist 43, 331— 43.
  • Paasche, E. 1964 A tracer study of the inorganic carbon uptake during coccolith formation and photosynthesis in the coccolithophid Coccolithus huxleyi (Prymnesiophycea). Physiologia Plantarum 3 (supplement), 5-82.
  • Paasche, E. 1965 The effect of3-(p-chlorophenyl)- 1,1-dimethylurea on photosynthesis and light-dependent coccolith formation in Coccolithus huxleyi. Physiologia Plantarum 18, 138-45.
  • Paasche, E. 1996a Adjustment to light and dark rates of coccolith formation. Physiologia Plantarum 19, 271-8.
  • Paasche, E. 1996b Action spectrum of coccolith formation. Physiologia Plantarum 19, 770—9.
  • Paasche, E. 2001 A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) with particular reference to growth, coccolith forma- tion and calcification-photosynthesis interactions. Phycologia 40, 503-29.
  • Paerl, H.W. 1997 Coastal eutrophication and harmful algal blooms: importance of atmo- spheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnology and Oceanography 42, 1154-65.
  • Poole, L.J. and Raven, J.A. 1997 The biology of Enteromorpha. Progress in Phycological Research 12, 1-148.
  • Poulton, A.J., Adey, T.R., Balch, W.M. and Holligan, P.M. 2007 Relating coccolithophore calcifi- cation to phytoplankton community dynamics: Regional differences and implications for carbon export. Deep-Sea Research Part II Current Topics in Oceanography 54, 538-57.
  • Raven, J.A. 1976 Transport in algal cells. In U. Liittge and M.G. Pitman (eds), Transport in cells and tissues, 129-188. Encyclopedia of Plant Physiology, New Series vol. 2. Berlin. Springer-Verlag.
  • Raven, J.A. 1980 Nutrient transport in micro- algae. Advances in Microbial Physiology 21, 47—226.
  • Raven, J. A. 1993 Carbon: a phycocentric view. In G.T. Evans and M.J.R. Fasham (eds), Towards a model of ocean biogeochemical processes. NATO. ASI Series, Series I, Global Environmental Change vol. 10, 123-52. Berlin. Springer Verlag.
  • Raven, J.A. 2010 Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynthesis Research 106, 123-34. doi: 10.1007/ si 1120-010-9563-7
  • Raven, J.A. 2011 Carbon. In B. Whitton (ed.), Ecology of cyanobacteria, 2nd edn. Berlin. Springer. In press.
  • Raven, J.A. and Cockell, C.S. 2006 Influence on photosynthesis of starlight, moonlight, planetlight and light pollution (reflections on photosyntheti- cally active radiation in the universe). Astrobiology 6, 668-75.
  • Raven, J.A. and Farquhar, G.D. 1990 The influ- ence of N metabolism and organic acid synthesis on the natural abundance of C isotopes in plants. New Phytologist 116, 505-29.
  • Raven, J.A. andjohnston, A.M. 1991 Photosynthetic carbon assimilation by Prasiola stipitata (Prasiolales, Chlorophyta) under emersed and submersed conditions: relationship to the taxonomy of Prasiola. British Phycological Journal 26, 247—57.
  • Raven, J.A. and Smith, F.A. 1974 Significance of hydrogen ion transport in plant cells. Canadian Journal of Botany 52, 1035—48.
  • Raven, J.A. and Smith, F.A. 1976 Nitrogen assim- ilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytologist 76, 415-31.
  • Raven, J.A. and Smith, F.A. 1980 Intracellular pH regulation in the giant-celled marine alga Chaetomorpha darwinii. Journal of Experimental Botany 31, 1357-71.
  • Raven, J.A. and Waite, A. 2004 Tansley Review: The evolution of silicification in diatoms: inescap- able sinking and sinking as escape? New Phytologist 162, 45-61.
  • Raven, J.A., Ball, L.A., Beardall, J., Giordano, M. and Maberly, S.C. 2005 Algae lacking carbon concentrating mechanisms. Canadian Journal of Botany 83, 879-90.
  • Raven, J.A., Beardall, J., Giordano, M. and Maberly, S.C. 2011 Algal and aquatic plant carbon concentrating mechanisms in relation to environ- mental change. Photosynthesis Research, in press, doi: 10.1007/sl 1120-011-9632-6.
  • Raven, J.A., Caldeira, K., Enderfield, H., Hoegh- Guldberg, O., Liss, P., Riebesell, U., Shepherd, J., Turley, C., Watson, A., Heap, R., Banes, R. and Quinn, R. 2005 Ocean acidification due to increasing carbon dioxide. The Royal Society of London report 12/05.
  • Raven, J.A., Johnston, A.M., Kiibler, J.E., Korb, R.E., Mclnroy, S.G., Handley, L.L., Scrimgeour, C.M., Walker, D.I., Beardall, J., Vanderklift, M., Fredricksen, J. and Dunton, K.H. 2002a Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Functional Plant Biology 29, 355-78.
  • Raven, J.A., Johnston, A.M., Kiibler, J.E., Korb, R.E., Mclnroy, S.G., Handley, L.L., Scrimgeour, C.M., Walker, D.I., Beardall, J., Clayton, M.N., Vanderklift, M., Fredriksen, S. and Dunton, K.H. 2002b Seaweeds in cold seas: evolu- tion and carbon acquisition. Annals of Botany 90, 525-36.
  • Raven, J. A., Kiibler, J.I. and Beardall, J. 2000 Put out the light, and then put out the light. Journal of the Marine Biological Association of the United Kingdom 80, 1-25.
  • Reinfelder, J.R. 2011 Carbon concentrating mech- anisms in eukaryotic marine phytoplankton. Annual Review of Marine Sciences 3, 291—315.
  • Ridgwell, A., Schmidt, D.N., Turley, C., Brownlee, C., Maldonado, M.T., Tortell, P. and Young, J.R. 2009 From laboratory manipulations to Earth System models. Scaling calcification impacts on ocean acidification. Biogeosciences 6, 2611-23.
  • Riebesell, U., Bellerby, R.G.J., Engel, A., Fabry, V.J., Hutchins, D.A., Reusch, T.B.H., Schulz, K.G. and Morel, F.M.M. 2008 Comment on "Phytoplankton calcification in a high-CO , world". Science 322, 1466. doi: 10.1126/ science.1161096
  • Riebesell, U., Fabry, V.J., Nansson, L.N. and Gattuso, J.-P (eds) 2010 Guide to best practices for ocean acidification research and data reporting. 260 pp. Luxembourg. Publications Office of the European Union, http://www.epoca-project.eu/index.php/ guide-to-best-practices-for-ocean-acidification- research-and-data-reporting.html (accessed 18 March 2011).
  • Ries, J.B. 2006 High Mg calcite in crustose coralline algae: geochemical, biological and sedi- mentological implications of secular variations in the Mg/Ca ratio of seawater. Geochimica et Cosmochimica Acta 70, 891-900.
  • Ries, J.13., Cohen, A.L. and McCorkle, D.C. 2009 Marine calcifiers exhibit mixed response to CO , -induced ocean acidification. Geology 37, 1131-4.
  • Schulz, K.G., Ramos, J.B.E., Zeebe, R.E. and Riebesell, U. 2009 CO , perturbation experi- ments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeosciences 6, 2145—53.
  • Semesi, I.S., Kangira, J. and Bjork, M. 2009 Alteration in seawater pH and CO , affect calci- fication and photosynthesis in tropical coralline alga, Hydrolithon sp. Rhodophyta. Estuarine, Coastal and Marine Science 84, 337—41.
  • Shi, D., Xu, Y. and Morel, F.M.M. 2009 Effects of the pH/^CO , control method on medium chem- istry and phytoplankton growth. Biogeosciences 6, 1199-207.
  • Shi, D., Hopkinson, B.M. and Morel, F.M.M. 2010 Effect of ocean acidification in iron avail- ability to marine phytoplankton. Science 327, 676-9. doi: 10.1126/science.ll83517
  • Sikes, C.S. and Wilbur, K.M. 1982 Function of coccoliths. Limnology and Oceanography 27, 18-26.
  • Sikes, C.S., Roer, R.D. and Wilbur, K.M. 1980 Photosynthesis and coccolith formation: inorganic carbon sources and net reaction of deposition. Limnology and Oceanography 25, 248—61.
  • Small, J. 1946 pH and Plants. London. Bailliere, Tyndall and Cox.
  • Small, J. 1954 Modern aspects ofpH (with special refer- ence to soil and plants. London. Bailliere, Tyndall and Cox.
  • Small, J. 1955 The pH of plant cells. In L.V. Heilbrunn and F. Weber (eds), Protoplasmatologia, 1—116. Cytoplasma, Band II B2C. Vienna. Springer-Verlag.
  • Smith, F.A. and Raven, J.A. 1979 Intracellular pH and its regulation. Annual Review of Plant Physiology 30, 289-311.
  • Stanley, S.M., Ries, J.B. and Hardie, L.A. 2002 Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proceedings of the National Academy of Sciences USA 99, 15323-6.
  • Stanley, S.M., Ries, J.B. and Hardie, L.A. 2005 Seawater chemistry, coccolithophore popula- tion growth, and the origin of Cretaceous chalk. Geology 33, 593—6.
  • Steinacher, M., Joos, F., Frolicher, T.L., Bopp, L., Cadule, P., Cocco, V., Doney, S.C., Gehlen, M., Lindsay, K., Moore, J.K., Schneider, B. and Segschneider, J. 2010 Projected 21 st century decrease in marine primary productivity: a multi- model analysis. Biogeosciences 7, 979-1005.
  • Steneck, R.S. 1983 Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9, 44-61.
  • Steneck, R.S. 1986 The ecology of coralline algal crusts: converging patterns and adaptive strate- gies. Annual Review of Ecology and Systematics 17, 273-303.
  • Suffrian, K., Schulz, K.G., Riebesell, U. and McCorkle, D.C. 2011 Cellular pH measurements in Emiliania huxleyi reveal pronounced membrane proton permeability. New Phytologist, in press, doi: 10.1111/j.1469.8137.2010.03633.x
  • Taylor, A.R., Chrachri, A., Wheeler, G.L., Goddard, H. and Brownlee, C. 2011 A proton channel underlies intracellular pH regulation in calcifying coccolithophores. PLoS Biology, in press.
  • Thierstein, H.R. and Young, J.R. (eds) 2004 Coccolithophores: from molecular mechanisms to global impacts. Heidelberg and Berlin. Springer.
  • Trimborn, S., Langer, G. and Rost, B. 2007 Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi. Limnology and Oceanography 52, 2285-93.
  • Tyrrell, T. 2011 Anthropogenic modification of the oceans. Philosophical Transactions of the Royal Society of London A 369, 887-908.
  • Tyrrell, T. and Merico, A. 2004 Emiliania huxleyi: bloom observation and the conditions that induce them. In H.R. Thierstein and J.R. Young (eds), Coccolithophores: from molecular mechanisms to global impacts, 75-97. Heidelberg and Berlin. Springer.
  • Uitz, H., Claustre, H., Gentoli, B. and Stramski, D. 2010 Phytoplankton class-specific primary production in the world's oceans; seasonal and interannual variability from satellite observations. Global Biogeochemical Cycles 24 (3), GB 2016. doi: 10.1029/2009GB003680
  • Walker, N.A. 1976 Membrane transport: theoret- ical background. In U. Liittge and M.G. Pitman (eds), Transport in cells and tissues. Encyclopedia of Plant Physiology, New Series vol. 2, part B, 36—52. Berlin. Springer-Verlag.
  • Wilson, S., Blake, C., Berges, J.A. and Maggs, C.A. 2004 Environmental tolerances of free-living coralline algae (maerl): implications for European marine conservation. Biological Conservation 120, 279-89.
  • Yamamoto, M.Y., McLaughlin, F.A., Carmack, E.C., Nishino, S. and Shimada, K. 2009 Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326, 1098-100.
  • Young, J.R. 1994 Functions of coccoliths. In A. Winter and W.G. Siesser (eds), Coccolithophores, 63-83. Cambridge, UK. Cambridge University Press.
  • Zeebe, R.E. and Wolf-Gladrow, D. 2001 C0 2 in seawater: equilibrium, kinetics, isotopes. Elsevier Oceanography Series Volume 65. Amsterdam. Elsevier.