Advertisement

Marine Biology

, Volume 160, Issue 8, pp 1813–1824 | Cite as

Responses of marine benthic microalgae to elevated CO2

  • V. R. Johnson
  • C. Brownlee
  • R. E. M. Rickaby
  • M. Graziano
  • M. Milazzo
  • J. M. Hall-SpencerEmail author
Original Paper
First Online:

Abstract

Increasing anthropogenic CO2 emissions to the atmosphere are causing a rise in pCO2 concentrations in the ocean surface and lowering pH. To predict the effects of these changes, we need to improve our understanding of the responses of marine primary producers since these drive biogeochemical cycles and profoundly affect the structure and function of benthic habitats. The effects of increasing CO2 levels on the colonisation of artificial substrata by microalgal assemblages (periphyton) were examined across a CO2 gradient off the volcanic island of Vulcano (NE Sicily). We show that periphyton communities altered significantly as CO2 concentrations increased. CO2 enrichment caused significant increases in chlorophyll a concentrations and in diatom abundance although we did not detect any changes in cyanobacteria. SEM analysis revealed major shifts in diatom assemblage composition as CO2 levels increased. The responses of benthic microalgae to rising anthropogenic CO2 emissions are likely to have significant ecological ramifications for coastal systems.

Keywords

Benthic Diatom Amphora Prochlorococcus Carbonate Chemistry Benthic Microalgae 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

VJ is carrying out a PhD funded by the Marine Institute, University of Plymouth (UoP) and thanks are due to the staff at the Marine Biological Association, UK and the SEM unit at UoP for laboratory support. We also thank C. Totti and T. Romagnoli at Università Politecnica delle Marche, Ancona, Italy for assistance with diatom identification, R. Lee at the Department of Earth Sciences at Oxford University for help with fieldwork, Y. Olsen and L. Basso at IMEDEA, Spain for providing light data and A. Beesley at Plymouth Marine Laboratory for performing total alkalinity analysis. This article contributes to the EU FP7 project on ‘Mediterranean Sea Acidification under a changing climate’ (MedSeA grant agreement no. 265103) and to the UK Ocean Acidification Research Programme, with additional funding for JHS from Save Our Seas Foundation and for RR from ERC grant SP2-GA-2008-200915.

References

  1. Anderson MJ (1995) Variations in biofilms colonising artificial surfaces: seasonal effects and effects of grazers. J Mar Biol Assoc UK 75:705–714CrossRefGoogle Scholar
  2. Azim ME, Verdegem MCJ, van Dam AA, Beveridge MCM (eds) (2005) Periphyton: ecology, exploitation and management. CABI, OxfordGoogle Scholar
  3. Badger MR, Price GD (2002) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622CrossRefGoogle Scholar
  4. Barcelos e Ramos J, Biswas H, Schulz KG, La Roche J, Riebesell U (2007) Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Glob Biogeochem Cycles 21:1–6CrossRefGoogle Scholar
  5. Barry JP, Tyrell T, Hansson L, Plattner G-K, Gattuso J-P (2010) Atmospheric CO2 targets for ocean acidification perturbation experiments. In: Riebsel U, Fabry VJ, Hansson L, Gattusso J-P (eds) Guide to best practises for ocean acidification research and data reporting. Publications Office of the European Union, LuxembourgGoogle Scholar
  6. Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms and their regulation. Funct Plant Biol 29:335–347CrossRefGoogle Scholar
  7. Beardall J, Raven JA (2004) The potential effects of global climate change in microalgal photosynthesis, growth and ecology. Phycologia 43:31–45CrossRefGoogle Scholar
  8. Bianchi CN, Dando PR, Morri C (2011) Increased diversity of sessile epibenthos at subtidal hydrothermal vents: seven hypotheses based on observations at Milos Island, Aegean Sea. Adv Limnol Oceangr 2:1–31CrossRefGoogle Scholar
  9. Burkhardt S, Riebesell U (1997) CO2 availability affects elemental composition (C:N:P) of the marine diatom Skeletonema costatum. Mar Ecol Prog Ser 155:67–76CrossRefGoogle Scholar
  10. Burkhardt S, Zondervan I, Riebesell U (1999) Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: a species comparison. Limnol Oceanogr 44:683–690CrossRefGoogle Scholar
  11. Burkhardt S, Amoroso G, Riebsell U, Sültemeyer D (2001) CO2 and HCO3 − uptake in marine diatoms acclimatised to different CO2 concentrations. Limnol Oceanogr 46:1378–1391CrossRefGoogle Scholar
  12. Bustamante RH, Branch GM, Eekhout S, Robertson B et al (1995) Gradients of intertidal primary productivity around the coast of South Africa and their relationships with consumer biomass. Oecologia 102:189–201CrossRefGoogle Scholar
  13. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  14. Chisholm SW (1992) Phytoplankton size. In: Falkowski PG, Woodhead AD (eds) Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York, pp 213–237CrossRefGoogle Scholar
  15. Cigliano M, Gambi MC, Rodolfo-Metalpa R, Patti FP, Hall-Spencer JM (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502CrossRefGoogle Scholar
  16. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc London B 277:1409–1415CrossRefGoogle Scholar
  17. Couto RP, Neto AI, Rodrigues AS (2010) Metal concentration and structural changes in Corallina elongata (Corallinales, Rhodophyta) from hydrothermal vents. Mar Pollut Bull 60:509–514CrossRefGoogle Scholar
  18. Dias BB, Hart MB, Smart CW, Hall-Spencer JM (2010) Modern seawater acidification: the response of foraminifers to high-CO2 conditions in the Mediterranean Sea. J Geol Soc London 167:1–4CrossRefGoogle Scholar
  19. Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162CrossRefGoogle Scholar
  20. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication, 3, Sidney, CanadaGoogle Scholar
  21. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  22. Edyvean EGJ, Terry IA, Picken GB (1985) Marine fouling and its effects on offshore structures in the North Sea-a review. Int Biodeterior 21:227–284Google Scholar
  23. Engel A, Zondervan I, Aerts K, Beaufort L, Benthien A, Chou L, Delille B, Gattuso J-P, Harlay J, Heemann C, Hoffman L, Jacquet S, Nejstgaard J, Pizay M-D, Rochelle-Newall E, Schneider U, Terbrueggen A, Riebsell U (2005) Testing the direct effect of CO2 concentration on a bloom of the coccolithphorid Emiliania huxleyi in mesocosm experiments. Limnol Oceanogr 50:493–507CrossRefGoogle Scholar
  24. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim Chang 1:165–169CrossRefGoogle Scholar
  25. Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth and elemental ratios of Synechococcus and Prochlorococcus (cyanobacteria). J Phycol 43:485–496CrossRefGoogle Scholar
  26. Fu F-X, Mulholland MR, Garcia NS, Beck A, Bernhardt PW, Warner ME, San˜udo-Wilhelmy SA, Hutchins DA (2008a) Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol Oceanogr 53:2472–2484CrossRefGoogle Scholar
  27. Fu F-X, Zhang Y, Warner ME, Feng Y, Sun J, Hutchins DA (2008b) A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7:76–90CrossRefGoogle Scholar
  28. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanism, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131CrossRefGoogle Scholar
  29. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Dine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99CrossRefGoogle Scholar
  30. Hawkins SJ, Watson DC, Hill AS, Harding SP, Kyriakides MA, Hutchinson S, Norton TA (1989) A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. J Molluscan Stud 55:151–165CrossRefGoogle Scholar
  31. Hawkins SJ, Hartnoll RG, Kain JM, Norton TA (1992) Plant–animal interactions on hard substrata in the north-east Atlantic. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos. Oxford University Press, Oxford, pp 1–32Google Scholar
  32. Hein M, Sand-Jensen K (1997) CO2 increases oceanic primary production. Nature 388:526–527CrossRefGoogle Scholar
  33. Hendriks IE, Duarte CM, Alvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coastal Shelf Sci 86:157–164CrossRefGoogle Scholar
  34. Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 Ocean. Glob Change Biol 17:2488–2497CrossRefGoogle Scholar
  35. Hill AS, Hawkins SJ (1990) An investigation of methods for sampling microbial films on rocky shores. J Mar Biol Assoc UK 70:77–88CrossRefGoogle Scholar
  36. Hill AS, Hawkins SJ (1991) Seasonal and spatial variation of epilithic microalgal distribution and abundance and its ingestion by Patella vulgata on a moderately exposed rocky shore. J Mar Biol Assoc UK 71:403–423CrossRefGoogle Scholar
  37. Hinga KR (2002) Effects of pH on coastal marine phytoplankton. Mar Ecol Prog Ser 238:281–300CrossRefGoogle Scholar
  38. Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Nat Acad Sci 108:3830–3837CrossRefGoogle Scholar
  39. Hoppe CJM, Langer G, Rokitta SD, Wolf-Gladrow DA, Rost B (2010) On CO2 perturbation experiments: over-determination of carbonate chemistry reveals inconsistencies. Biogeosci Discuss 7:1707–1726CrossRefGoogle Scholar
  40. Huang R, Boney AD (1984) Growth interactions between littoral diatoms and juvenile marine algae. J Exp Mar Biol Ecol 81:21–45CrossRefGoogle Scholar
  41. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J Phycol 45:1236–1251CrossRefGoogle Scholar
  42. Hutchins DA, Fu F-X, ZhangY WarnerME, Feng Y, Portune K, Bernhardt PW, Mullholland MR (2007) CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates and elemental ratios: implications for past, present and future ocean biogeochemistry. Limnol Oceanogr 52:1293–1304CrossRefGoogle Scholar
  43. Hutchins DA, Mulholland MR, Fu F-X (2009) Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22:128–145CrossRefGoogle Scholar
  44. Iglesias-Rodriguez MD, Halloran RP, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRH, Tyrrell T, Gibbs S, von Dassow P, Rehm E, Armbrust V, Boessenkoolm KP (2008) Phytoplankton calcification in a high CO2 world. Science 320:320–336CrossRefGoogle Scholar
  45. IPCC (Intergovernmental Panel on Climate Change) (2007) Working group 1 report, the physical science basis. http://ipcc-wg1.ucar.edu/wg1/wg1-report.html
  46. Jenkins SR, Arenas F, Arrontes J, Bussell J, Castro J, Coleman RA, Hawkins SJ, Kay S, Martinez B, Oliveros J, Roberts MF, Sousa SJ, Thompson RC, Hartnoll RG (2001) European-scale analysis of seasonal variability in limpet grazing activity and microalgal abundance. Mar Ecol Prog Ser 211:193–203CrossRefGoogle Scholar
  47. Kerrison P, Hall-Spencer JM, Suggett D, Hepburn LJ, Steinke M (2011) Assessment of pH variability at a coastal CO2 vent for ocean acidification studies. Estuar Coastal Shelf Sci 94:129–137CrossRefGoogle Scholar
  48. Kim J-M, Lee K, Shin K, Kang J-H, Lee H-W, Kim M, Jang P-G, Jang M-C (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol Oceanogr 51:1629–1636CrossRefGoogle Scholar
  49. Kiørboe T (1993) Turbulence, phytoplankton cell size and the structure of pelagic food webs. Adv Mar Biol 29:1–72CrossRefGoogle Scholar
  50. Kleypas JA, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 22:108–117CrossRefGoogle Scholar
  51. Kranz SA, Sültemeyer D, Richter KU, Rost B (2009) Carbon acquisition in Trichodesmium: diurnal variation and effect of pCO2. Limnol Oceanogr 54:548–559CrossRefGoogle Scholar
  52. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefGoogle Scholar
  53. Langer G, Nehrke G, Probert I, Ly J, Ziveri P (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences Discuss 6:4361–4383CrossRefGoogle Scholar
  54. Levitan O, Rosenberg G, Setlik I, Setlikova E, Grigel J, Klepetar J, Prasil O, Berman-Frank I (2007) Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob Change Biol 13:531–538CrossRefGoogle Scholar
  55. Lewis E, Wallace WR (1998) Program developed for CO2 system calculations. Carbon dioxide information analysis center, Oak Ridge National Laboratory. US Department of Energy, Oak RidgeGoogle Scholar
  56. Liu J, Weinbauer MG, Maier C, Dai M, Gattuso J-P (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol 61:291–305CrossRefGoogle Scholar
  57. Lombardi C, Rodolfo-Metalpa R, Cocito S, Gambi MC, Taylor PD (2010) Structural and geochemical alterations in the Mg calcite bryozoans Myriapora truncata under elevated seawater pCO2 simulating ocean acidification. Mar Ecol 32:211–221CrossRefGoogle Scholar
  58. Lu Z, Jiao N, Zhang H (2006) Physiological changes in marine picocyanobacterial Synechococcus strains exposed to elevated CO2 and partial pressure. Mar Biol Res 2:424–430CrossRefGoogle Scholar
  59. Mak YM, Williams GA (1999) Littorinids control high intertidal biofilm abundance on tropical, Hong Kong rocky shores. J Exp Mar Biol Ecol 233:81–94CrossRefGoogle Scholar
  60. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100CrossRefGoogle Scholar
  61. Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia M-C, Gattuso J-P, Hall-Spencer JM (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4:689–692CrossRefGoogle Scholar
  62. Matsumoto M, Yohida E, Takeyama H, Matsunaga T (2000) Floating cultivation of marine cyanobacteria using coal fly ash. Appl Biochem Biotech 84–86:51–57CrossRefGoogle Scholar
  63. McNamara AE, Hill WR (2000) UV-B irradiance gradient affects photosynthesis and pigments but not food quality of periphyton. Freshwater Biol 43:649–662Google Scholar
  64. Meadows PS, Williams GB (1963) Settlement of Spirorbis borealis Daudin larvae on surfaces bearing films of micro-organisms. Nature 198:610–611Google Scholar
  65. Munda IM (2005) Seasonal fouling by diatoms on artificial substrata at different depths near Piran (Gulf of Trieste, Northern Adriatic). Acta Adriat 46:137–157Google Scholar
  66. Nagarkar S, Williams GA (1997) Comparative techniques to quantify cyanobacteria dominated epilithic biofilms on tropical rocky shores. Mar Ecol Prog Ser 154:281–291CrossRefGoogle Scholar
  67. Nakićenović N, Swart R (2000) Special report on emissions scenarios: a special report of Working Group III of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 599Google Scholar
  68. National Research Council (2010) Ocean acidification: a national strategy to meet the challenges of a changing ocean. The National Academies Press, Washington. http://www.nap.edu/catalog/12904.html
  69. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686CrossRefGoogle Scholar
  70. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287CrossRefGoogle Scholar
  71. Raven JA (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: Relation to increased CO2 and temperature. Plant Cell Environ 14:779–794CrossRefGoogle Scholar
  72. Raven JA, Beardall J (2003) CO2 acquisition mechanisms in algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms: In Photosynthesis in the algae. Larkum AWW, Raven JA, Douglas S (eds). Advances in photosynthesis and respiration. Series editor, GovindjeeGoogle Scholar
  73. Raven JA, Giordano M, Beardall J, Maberly S (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosyn Res 109:281–296CrossRefGoogle Scholar
  74. Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60:719–729CrossRefGoogle Scholar
  75. Riebesell U (2008) Acid test for marine biodiversity. Nature 454:46–47CrossRefGoogle Scholar
  76. Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361:249–251CrossRefGoogle Scholar
  77. Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–1126CrossRefGoogle Scholar
  78. Rodolfo-Metalpa R, Lombardi C, Cocito S, Hall-Spencer JM, Gambi MC (2010) Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar Ecol 31:447–456Google Scholar
  79. Rodolfo-Metalpa R, Tambutté É, Houlbrèque F, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Clim Change 1:308–312CrossRefGoogle Scholar
  80. Rost B, Riebesell U, Burkhardt S (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67CrossRefGoogle Scholar
  81. Rost B, Zondervan I, Wolf-Gladrow D (2008) Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar Ecol Prog Ser 373:227–237CrossRefGoogle Scholar
  82. Round FE, Crawford RM, Mann DG (1990) The diatoms—biology & morphology of the genera. Cambridge University Press, CambridgeGoogle Scholar
  83. Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45 °C. Mar Chem 4:249–267Google Scholar
  84. Russell BD, Thompson J-A I, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15:2153–2162CrossRefGoogle Scholar
  85. Sekar R, VenugopalanVP SatpathyKK, Nair KVK, Rao VNR (2004) Laboratory studies on adhesion of microalgae to hard substrates. Hydrobiologia 512:109–116CrossRefGoogle Scholar
  86. Shannon CE, Weaver W (1949) A mathematical theory of communication. University of Illinois Press. ISBN 0-252-72548-4Google Scholar
  87. Simpson EH (1949) Measurement of diversity. Nature 163:688CrossRefGoogle Scholar
  88. Stafford R, Davies MS (2005) Spatial patchiness of epilithic biofilm caused by refuge-inhabiting high shore gastropods. Hydrobiologia 545:279–287CrossRefGoogle Scholar
  89. Stanley PM (1983) Factors affecting the irreversible attachment of Pseudomonas aeruginosa to stainless steel. Can J Microbiol 29:1493–1499CrossRefGoogle Scholar
  90. Thompson RC, Hawkins SJ, Norton TA (1998) The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids—a comparison between laboratory and field experiments. Hydrobiologia 375(376):203–216CrossRefGoogle Scholar
  91. Thompson RC, Tobin ML, Hawkins SJ, Norton TA (1999) Problems in extraction and spectrophotometric determination of chlorophyll from epilithic microbial biofilms: towards a standard method. J Mar Biol Assoc UK 79:551–558CrossRefGoogle Scholar
  92. Thompson RC, Norton TA, Hawkins SJ (2004) Physical stress and biological control regulate the producer-consumer balance in intertidal biofilms. Ecology 85:1372–1382CrossRefGoogle Scholar
  93. Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Kürtzinger AK, Wahl M, Melzner F (2010) Calcifying invertebrates succeed in a naturally CO2 enriched coastal habitat but are threatened by high levels of future acidification. Biogeosci Discuss 7:5119–5156CrossRefGoogle Scholar
  94. Torstensson A, Chierici M, Wulff A (2011) The influence of increased temperature and carbon dioxide levels on the benthic/sea ice diatom Navicula directa. Polar Biol. doi: 10.1007/s00300-011-1056-4
  95. Tortell PD, Reinfelder JR, Morel FMM (1997) Active uptake of bicarbonate by diatoms. Nature 390:243–244CrossRefGoogle Scholar
  96. Tortell PD, Rau GH, Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45:1485–1500CrossRefGoogle Scholar
  97. Tortell PD, DiTullio GR, Sigman DM, Morel FMM (2002) CO2 effects on taxonomic composition and nutrient utilisation in an Equatorial Pacific phytoplankton assemblage. Mar Ecol Prog Ser 236:37–43CrossRefGoogle Scholar
  98. Tortell PD, Payne CD, Li Y, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RB, Sedwick DiTullioGR (2008) CO2 sensitivity of southern ocean phytoplankton. Geophys Res Lett 35:L04605. doi: 10.1029/2007GL032583 CrossRefGoogle Scholar
  99. Tribollet A, Atkinson MJ, Langdon C (2006) Effects of elevated pCO2 on epilithic and endolithic metabolism on reef carbonates. Glob Change Biol 12:2200–2208CrossRefGoogle Scholar
  100. Trimborn S, Wolf-Gladrow D, Ritcher K-L, Rost B (2009) The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. J Exp Mar Biol Ecol 376:26–36CrossRefGoogle Scholar
  101. Tuchman ML, Blinn DW (1979) Comparison of attached algal communities on natural and artificial substrates along a thermal gradient. Br Phycol J 14:243–251CrossRefGoogle Scholar
  102. Underwood AJ (1984) The vertical distribution and seasonal abundance of intertidal microalgae on a rocky shore in New South Wales. J Exp Mar Biol Ecol 78:199–220CrossRefGoogle Scholar
  103. Vanhaecke E, Remon J-P, Moors M, Raes F, De Rudder D, Peteghem Van (1990) Kinetics of Pseudomonas aeruginosa adhesion to 304 and 326-L stainless steel: role of cell surface hydrophobicity. Appl Environ Microbiol 56:788–795Google Scholar
  104. Vizzini S, Tomasello A, Maida GD, Pirrotta M, Mazzola A, Calvo S (2010) Effect of explosive shallow hydrothermal vents on δ13C and growth performance in the seagrass Posidonia oceanica. J Ecol 98:1284–1291CrossRefGoogle Scholar
  105. Witt V, Wild C, Anthony KRN, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol. doi: 10.1111/j.1462-2920.2011.02571.x
  106. Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates—but at a cost. Proc Royal Soc B 275:1767–1773CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • V. R. Johnson
    • 1
  • C. Brownlee
    • 2
  • R. E. M. Rickaby
    • 3
  • M. Graziano
    • 4
    • 5
  • M. Milazzo
    • 5
  • J. M. Hall-Spencer
    • 1
    Email author
  1. 1.Marine Biology and Ecology Research Centre, Marine InstituteUniversity of PlymouthPlymouthUK
  2. 2.The Marine Biological Association of the United Kingdom (MBA), The LaboratoryPlymouthUK
  3. 3.Department of Earth SciencesUniversity of OxfordOxfordUK
  4. 4.CNR-Institute of Atmospheric Pollution Research, UNICAL-PolifunzionaleRendeItaly
  5. 5.Dipartimento di Scienze della Terra e del MareUniversity of PalermoPalermoItaly

Personalised recommendations

Cite article

Buy options