Seaweed Responses to Ocean Acidification

  • Michael Y. Roleda
  • Catriona L. Hurd
Part of the Ecological Studies book series (ECOLSTUD, volume 219)


Ocean acidification (OA) is the decline in seawater pH caused by the sustained absorption by the oceans of anthropogenically produced atmospheric CO2. The consequences of OA to seaweed-based coastal ecosystems range from organismal to community levels of biological organization. Organismal responses can be species specific, depending on their carbon physiology, mode of calcification, and morphology (functional form). At the community scale, changes in community structure and function can have severe consequences on trophic dynamics. Biologically driven fluctuations in seawater carbonate chemistry are observed from micro- (diffusion boundary layer, DBL) to mesoscales (e.g., within a kelp forest), and such fluctuations may be exacerbated by OA. The synergistic effects of elevated CO2 with other human-induced environmental stressors (e.g., warming, eutrophication, and UVR) could make the primary producers of coastal ecosystems vulnerable to global climate change; some species may perform better than others under “greenhouse” conditions, leading to community phase shifts.


Ocean Acidification Crassulacean Acid Metabolism Crustose Coralline Alga Diffusion Boundary Layer Organic Carbon Assimilation 
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.



The authors were funded by the Royal Society of New Zealand Marsden Fund (UOO0914). We thank the two anonymous reviewers for their helpful comments.


  1. Adey WH, Steneck RS (2001) Thermography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae. J Phycol 37:677–698Google Scholar
  2. Axelsson L, Larsson C, Ryberg H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant Cell Environ 22:969–978Google Scholar
  3. Axelsson L, Mercado JM, Figueroa FL (2000) Utilization of HCO3 at high pH by the brown macroalgae Laminaria saccharina. Eur J Phycol 35:53–59Google Scholar
  4. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071Google Scholar
  5. Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot Mar 41:113–123Google Scholar
  6. Beer S (1994) Mechanisms of inorganic carbon acquisition in marine macroalgae (with special reference to the Chlorophyta). Prog Phycol Res 10:179–207Google Scholar
  7. Beman JM, Chow CE, King AL, Feng YY, Fuhrman JA, Andersson A, Bates NR, Popp BN, Hutchins DA (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc Natl Acad Sci USA 108:208–213. doi: 10.1073/pnas.1011053108 PubMedCentralPubMedGoogle Scholar
  8. Bensoussan N, Gattuso J-P (2007) Community primary production and calcification in a NW Mediterranean ecosystem dominated by calcareous macroalgae. Mar Ecol Prog Ser 334:37–45Google Scholar
  9. Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166. doi: 10.1007/s11157-006-002-3 Google Scholar
  10. Björk M, Haglund K, Ramazanov Z, Garcia-Reina G, Pedersen M (1992) Inorganic-carbon assimilation in the green seaweed Ulva rigida C. Ag. (Chlorophyta). Planta 187:152–156PubMedGoogle Scholar
  11. Björk M, Haglund K, Ramazanov Z, Pedersen M (1993) Inducible mechanisms for HCO3 utilization and repression of photorespiration in protoplasts and thalli of three species of Ulva (Chlorophyta). J Phycol 29:166–173Google Scholar
  12. Björk M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rock pools along the Swedish Atlantic coast? Mar Ecol Prog Ser 284:109–116Google Scholar
  13. Black CC, Bender MM (1976) δ13C values in marine organisms from the Great Barrier Reef. Aust J Plant Physiol 3:25–32Google Scholar
  14. Bode A, Alvarez-Ossorio MT, Varela M (2006) Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Mar Ecol Prog Ser 318:89–102Google Scholar
  15. Borowitzka MA (1987) Calcification in algae: mechanisms and the role of metabolism. CRC Cr Rev Plant Sci 6:1–45Google Scholar
  16. Borowitzka MA, Larkum AWD (1976) Calcification in the green alga Halimeda. 3. sources of inorganic carbon for photosynthesis and calcification and a model of mechanism of calcification. J Exp Bot 27:879–893Google Scholar
  17. Borowitzka MA, Larkum AWD (1986) Reef algae. Oceanus 29:49–54Google Scholar
  18. Boyd P, Doney SC, Strzepek R, Dusenberry J, Lindsay K, Fung I (2008) Climate-mediated changes to mixed-layer properties in the Southern Ocean: assessing the phytoplankton response. Biogeosciences 5:847–864Google Scholar
  19. Brownlee C, Taylor A (2004) Calcification in coccolithophores: A cellular perspective. In: Thierstein HR, Young JR (eds) Coccolithophores: from cellular processes to global impact. Springer, Berlin, pp 31–49Google Scholar
  20. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Science 425:365–365. doi: 10.1038/425365a Google Scholar
  21. Cao L, Caldeira K (2008) Atmospheric CO2 stabilization and ocean acidification. Geophys Res Lett. doi: 10.1029/2008GL035072
  22. 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 forest. Proc R Soc B-Biol Sci 227:1409–1415. doi: 10.1098/rspb.2009.2069 Google Scholar
  23. Corbisier TN, Soares LSH, Petti MAV, Muto EY, Silva MHC, McClelland J, Valiela I (2006) Use of isotopic signatures to assess the food web in a tropical shallow marine ecosystem of Southeastern Brazil. Aquat Ecol 40:381–390. doi: 10.1007/s10452-006-9033-7 Google Scholar
  24. Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, Hunter KA, Hurd CL (2012) Carbon use-strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48:137–144. doi: 10.1111/j.1529-8817.2011.01085.x Google Scholar
  25. De Beer D, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24:1209–1217Google Scholar
  26. Delille B, Delille D, Fiala M, Prevost C, Frankignoulle M (2000) Seasonal changes of pCO2 over a subantarctic Macrocystis kelp bed. Polar Biol 23:706–716Google Scholar
  27. Delille B, Borges AV, Delille D (2009) Influence of giant kelp beds (Macrocystis pyrifera) on diel cycles of pCO2 and DIC in the Sub-Antarctic coastal area. Estuar Coast Shelf S 81:114–122. doi: 10.1016/j.ecss.2008.10.004 Google Scholar
  28. Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2012) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J Phycol 48:32–39. doi: 10.1111/j.1529-8817.2011.01084.x Google Scholar
  29. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192. doi: 10.1146/annurev.marine.010908.163834 Google Scholar
  30. Dromgoole FI (1978) The effects of pH and inorganic carbon on photosynthesis and dark respiration of Carpophyllum (Fucales, Phaeophyceae). Aquat Bot 4:11–22. doi: 10.1016/0304-3770(78)90003-7 Google Scholar
  31. Dunton KH (2001) δ15N and δ13C measurements of Antarctic peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99–112Google Scholar
  32. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas JA, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366. doi: 10.1126/science.1097329 PubMedGoogle Scholar
  33. Feely RA, Alin SR, Newton J, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci 88:442–449. doi: 10.1016/j.ecss.2010.05.004 Google Scholar
  34. Fischer G, Wiecke C (1992) Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region. Polar Biol 12:341–348Google Scholar
  35. Gao K, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60Google Scholar
  36. Gao KS, Zheng YQ (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Change Biol 16:2388–2398. doi: 10.1111/j.1365-2486.2009.02113.x Google Scholar
  37. Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentration. J Appl Phycol 3:355–362Google Scholar
  38. Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993a) Calcification in the articulated coralline alga Corallina pulifera with special reference to the effect of elevated CO2. Mar Biol 117:129–132Google Scholar
  39. Gao K, Aruga Y, Asada K, Kiyohara M (1993b) Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. & G. chilensis. J Appl Phycol 5:563–571Google Scholar
  40. Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytol 188:674–695. doi: 10.1111/j.1469-8137.2010.03441.x PubMedGoogle Scholar
  41. Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81:534–539Google Scholar
  42. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131. doi: 10.1146/annurev.arplant.56.032604.144052 PubMedGoogle Scholar
  43. Gordillo FJL, Niell FX, Figueroa FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64–70PubMedGoogle Scholar
  44. Graham MH, Vásquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol 45:39–88Google Scholar
  45. Hall-Spencer J, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99. doi: 10.1038/nature07051 PubMedGoogle Scholar
  46. 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. Global Change Biol 17:2488–2497. doi: 10.1111/j.1365-2486.2011.02411.x Google Scholar
  47. Holbrook GP, Beer S, Spenser WE, Reiskind J, Davis JS, Bowes G (1988) Photosynthesis in marine macroalgae: evidence for carbon limitation. Can J Bot 66:577–582Google Scholar
  48. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472Google Scholar
  49. Hurd CL, Pilditch CA (2011) Flow-induced morphological variations affect diffusion boundary-layer thickness of Macrocystis pyrifera (Heterokontophyta, Laminariales). J Phycol 47:341–351. doi: 10.1111/j.1529-8817.2011.00958.x Google Scholar
  50. 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 45:1236–1251Google Scholar
  51. Hurd CL, Cornwall CE, Currie K, Hepburn CD, McGraw CM, Hunter KA, Boyd PW (2011) Metabolically-induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility? Glob Change Biol doi:10.1111/j.1365-2486.2011.02473.xGoogle Scholar
  52. IPCC (2007) Climate Change 2007: The physical science basis. Summary for policymakers. Contribution of working group I to the fourth assessment report. The International Panel on Climate Change,
  53. Jiang ZJ, Huang X-P, Zhang J-P (2010) Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J Integr Plant Biol 52:904–913. doi: 10.1111/j.1744-7909.2010.00991.x PubMedGoogle Scholar
  54. Johnston AM (1991) The acquisition of inorganic carbon by marine macroalgae. Can J Bot 69:1123–1132Google Scholar
  55. Johnston AM, Raven JA (1991) Effects of culture in high CO2 on the photosynthetic physiology of Fucus serratus. Br Phycol J 25:75–82Google Scholar
  56. Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia 92:317–326Google Scholar
  57. Kang C-K, Choy EJ, Son Y, Lee J-K, Kim JK, Kim Y, Lee K-S (2008) Food web structure of a restored macroalgal bed in the eastern Korean peninsula determined by C and N stable isotope analyses. Mar Biol 153:1181–1198. doi: 10.1007/s00227-007-0890-y Google Scholar
  58. Kevekordes K, Holland D, Häubner N, Jenkin S, Koss R, Roberts S, Raven JA, Scrimgeour CM, Shelly K, Stojkovic S, Beardall J (2006) Inorganic carbon acquisition by eight species of Caulerpa (Caulerpaceae, Chlorophyta). Phycologia 45:442–449. doi: 10.2216/05-55.1 Google Scholar
  59. Kremer BP (1981) Aspects of carbon metabolism in marine macroalgae. In: Barnes HB, Barnes M (eds) Oceanography and marine biology: an annual review, 19. Aberdeen University Press, Aberdeen, UK, pp 41–94Google Scholar
  60. Kübler JE, Raven JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Mar Ecol Prog Ser 110:203–209Google Scholar
  61. Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310Google Scholar
  62. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117. doi: 10.1038/ngeo100 Google Scholar
  63. Laurand S, Riera P (2006) Trophic ecology of the supralittoral rocky shore (Roscoff, France): a dual stable isotope (δ13C, δ15N) and experimental approach. J Sea Res 56:27–36. doi: 10.1016/j.seares.2006.03.002 Google Scholar
  64. Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449Google Scholar
  65. Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12 C and 13 C by marine plants. Oecologia 91:481–492Google Scholar
  66. Magnusson G, Larsson C, Axelsson L (1996) Effects of high CO2 treatment on nitrate and ammonium uptake by Ulva lactuca grown in different nutrient regimes. Sci Mar 60(Supplement 1):179–189Google Scholar
  67. Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100. doi: 10.1111/j.1365-2486.2009.01874.x Google Scholar
  68. Mathis JT, Cross JN, Bates NR (2011) Coupling primary production and terrestrial runoff to ocean acidification and carbonate mineral suppression in the eastern Bering Sea. J Geophys Res-Oceans. doi: 10.1029/2010JC006453
  69. McGraw CM, Cornwall CE, Reid MR, Currie KI, Hepburn CD, Boyd P, Hurd CL, Hunter KA (2010) An automated pH-controlled culture system for laboratory-based ocean acidification experiments. Limnol Oceanogr Meth 8:686–694. doi: 10:4319/lom.2010.8.686 Google Scholar
  70. McNeil BI, Matear RJ (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864. doi: 10.1073/pnas.0806318105 PubMedCentralPubMedGoogle Scholar
  71. Mercado JM, Niell FX, Gil-Rodríquez MC (2001) Photosynthesis might be limited by light, not inorganic carbon availability, in three intertidal Gelidiales species. New Phytol 149:431–439Google Scholar
  72. Mercado JM, Andria JR, Pérez-Llorens JL, Vergara JJ, Axelsson L (2006) Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina. Photosynth Res 88:259–268. doi: 10.1007/s11120-006-9039-y PubMedGoogle Scholar
  73. Merzouk A, Johnson LE (2011) Kelp distribution in the northwest Atlantic Ocean under a changing climate. J Exp Mar Biol Ecol 400:90–98. doi: 10.1016/j.jembe.2011.02.020 Google Scholar
  74. Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259. doi: 10.1128/EC.00064-07 PubMedCentralPubMedGoogle Scholar
  75. Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845. doi: 10.1111/j.1529-8817.2004.03182.x Google Scholar
  76. Nelson WA (2009) Calcified macroalgae- critical to coastal ecosystems and vulnerable to change: a review. Mar Freshwater Res 60:787–801. doi: 10.1071/MF08335 Google Scholar
  77. Pinnegar JK, Polunin NVC (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409Google Scholar
  78. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287. doi: 10.1016/j.jembe.2011.02.011 Google Scholar
  79. Raven JA (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynth Res 106:123–134. doi: 10.1007/s11120-010-9563-7 PubMedGoogle Scholar
  80. Raven JA, Giordano M (2009) Biomineralization by photosynthetic organisms: evidence of coevolution of the organisms and their environment? Geobiology 7:140–154. doi: 10.1111/j.1472-4669.2008.00181.x PubMedGoogle Scholar
  81. Raven JA, Walker DI, Johnston AM, Handley LL, Kübler JE (1995) Implications of 13C natural abundance measurements for photosynthetic performance by marine macrophytes in their natural environment. Mar Ecol Prog Ser 123:193–205Google Scholar
  82. Raven JA, Johnston AM, Kübler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift M, Fredriksen S, Dunton KH (2002a) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90:525–536. doi: 10.1093/aob/mcf171 PubMedGoogle Scholar
  83. Raven JA, Johnston AM, Kübler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002b) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378. doi: 10.1071/PP01201 Google Scholar
  84. Raven JA, Ball LA, Beardall J, Giordana M, Maberly SC (2005) Algae lacking carbon-concentrating mechanisms. Can J Bot 83:879–890. doi: 10.1139/B05-074 Google Scholar
  85. Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc B 363:2641–2650. doi: 10.1098/rstb.2008.0020 Google Scholar
  86. Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, LuxembourgGoogle Scholar
  87. Ries JB (2009) Effects of secular variation in seawater Mg/Ca ratio (calcite-aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udotea – evidence from recent experiments and the geological record. Terra Nova 21:323–339. doi: 10.1111/j.1365-3121.2009.00899.x Google Scholar
  88. Ries JB (2010) Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effects of marine biological calcification. Biogeosciences 7:2795–2849. doi: 10.5194/bg-7-2795-2010 Google Scholar
  89. Roleda MY, Wiencke C, Hanelt D, Bischof K (2007) Sensitivity of the early life history stages of macroalgae from the Northern Hemisphere to ultraviolet radiation. Photochem Photobiol 83:851–862. doi: 10.1562/2006-08-17-IR-1005 PubMedGoogle Scholar
  90. Roleda MY, Campana GL, Wiencke C, Hanelt D, Quartino ML, Wulff A (2009) Sensitivity of Antarctic Urospora penicilliformis (Ulotrichales, Chlorophyta) to ultraviolet radiation is life-stage dependent. J Phycol 45:600–609. doi: 10.1111/j.1529-8817.2009.00691.x Google Scholar
  91. Roleda MY, Morris JN, McGraw CM, Hurd CL (2012) Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Global Change Biol 18:854–864. doi: 10.1111/j.1365-2486.2011.02594.x
  92. Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05 Royal Society, London. The Clyvedon press Ltd, CardiffGoogle Scholar
  93. Runcie JW, Gurgel CFD, McDermid KJ (2008) In situ photosynthetic rates of tropical marine macroalgae at their lower depth limit. Eur J Phycol 43:377–388. doi: 10.1080/09670260801979303 Google Scholar
  94. Russell BD, Connell SD (2009) Eutrophication science: moving into the future. Trends Ecol Evol 24:527–528. doi: 10.1016/j.tree.2009.06.001 PubMedGoogle Scholar
  95. Russell BD, Thompson JAI, 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 15:2153–2162. doi: 10.1111/j.1365-2486.2009.01886.x Google Scholar
  96. Russell BD, Passarelli CA, Connell SD (2011) Forecasted CO2 modifies the influence of light in shaping subtidal habitat. J Phycol doi:10.1111/j.1529-8817.2011.01002.xGoogle Scholar
  97. Semesi IS, Beer S, Bjork M (2009a) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Mar Ecol Prog Ser 382:41–47. doi: 10.3354/meps07973 Google Scholar
  98. Semesi IS, Kangwe J, Björk M (2009b) Alterations in seawater pH and CO2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta). Estuar Coast Shelf Sci 84:337–341. doi: 10.1016/j.ecss.2009.03.038 Google Scholar
  99. Sherlock DJ, Raven JA (2001) Interactions between carbon dioxide and oxygen in the photosynthesis of three species of marine red algae. Bot J Scotl 53:33–43Google Scholar
  100. Smith RG, Bidwell RGS (1989) Inorganic carbon uptake by photosynthetically active protoplast of the red macroalga Chondrus crispus. Mar Biol 102:1–4Google Scholar
  101. Stanley SM (2008) Effects of global seawater chemistry on biomineralization: past, present and future. Chem Rev 108:4483–4498. doi: 10.1021/cr800233u PubMedGoogle Scholar
  102. Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78:97–105Google Scholar
  103. Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in intertidal and normally submersed members of the Fucales and Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80Google Scholar
  104. Thoms S, Pahlow M, Wolf-Gladrow DA (2001) Model of the carbon concentrating mechanism in chloroplasts of eukaryotic algae. J Theor Biol 208:295–313. doi: 10.1006/jtbi.2000.2219 PubMedGoogle Scholar
  105. Turley C (2008) Impacts of changing chemistry in a high-CO2 world. Mineral Mag 72:359–362. doi: 10.1180/minmag.2008.072.1.359 Google Scholar
  106. van de Waal D, Verschoor AM, Verspagen JMH, van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystem. Front Ecol Environ 8:145–152. doi: 10.1890/080178 Google Scholar
  107. Vizzini S, Mazzola A (2006) The effects of anthropogenic organic matter inputs on stable carbon and nitrogen isotopes in organisms from different trophic levels in a southern Mediterranean coastal area. Sci Total Environ 368:723–731. doi: 10.1016/j.scitotenv.2006.02.001 PubMedGoogle Scholar
  108. Wang W-L, Yeh H-W (2003) δ13C values of marine macroalgae from Taiwan. Bot Bull Acad Sin 44:107–112Google Scholar
  109. Ward JK (2005) Evolution and growth of plants in a low CO2 world. In: Ehleringer JR, Cerling TE, Dearing MD (eds) A history of atmospheric CO2 and its effects on plants, animals, and ecosystem, vol 177, Ecological Studies. Springer, New York, pp 232–257Google Scholar
  110. Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Natl Acad Sci USA 105:18848–18853. doi: 10.1073/pnas0810079105 PubMedCentralPubMedGoogle Scholar
  111. Wozniak AS, Roman CT, Wainright SC, McKinney RA, James-Pirri M-J (2006) Monitoring food web changes in tide-restored salt marshes: a carbon stable isotope approach. Estuar Coast 29:568–578Google Scholar
  112. Zachos JC, Rohl U, Schellenberg SA, Sluijs A, Hodell DA, Kelly DC, Thomas E, Nicolo M, Raffi I, Lourens LJ, McCarren H, Kroon D (2005) Rapid acidification of the ocean during the Paleocene-Eocene thermal maximum. Science 308:1611–1615. doi: 10.1126/science.1109004 PubMedGoogle Scholar
  113. Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics. Isotopes. Elsevier Science B.V, AmsterdamGoogle Scholar
  114. Zou D, Gao K (2002) Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. Eur J Phycol 37:587–592. doi: 10.1017/S0967026202003876 Google Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of BotanyUniversity of OtagoDunedinNew Zealand

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