Photosynthesis Research

, Volume 113, Issue 1–3, pp 105–125 | Cite as

Ecophysiology of photosynthesis in macroalgae

Regular Paper
First Online:
Received:
Accepted:

Abstract

Macroalgae occur in the marine benthos from the upper intertidal to depths of more than 200 m, contributing up to 1 Pg C per year to global primary productivity. Freshwater macroalgae are mainly green (Chlorophyta) with some red (Rhodophyta) and a small contribution of brown (Phaeophyceae) algae, while in the ocean all three higher taxa are important. Attempts to relate the depth distribution of three higher taxa of marine macroalgae to their photosynthetic light use through their pigmentation in relation to variations in spectral quality of photosynthetically active radiation (PAR) with depth (complementary chromatic adaptation) and optical thickness (package effect) have been relatively unsuccessful. The presence (Chlorophyta, Phaeophyceae) or absence (Rhodophyta) of a xanthophyll cycle is also not well correlated with depth distribution of marine algae. The relative absence of freshwater brown algae does not seem to be related to their photosynthetic light use. Photosynthetic inorganic carbon acquisition in some red and a few green macroalgae involves entry of CO2 by diffusion. Other red and green macroalgae, and brown macroalgae, have CO2 concentrating mechanisms; these frequently involve acid and alkaline zones on the surface of the alga with CO2 (produced from HCO3 −) entering in the acid zones, while some macroalgae have CCMs based on active influx of HCO3 −. These various mechanisms of carbon acquisition have different responses to the thickness of the diffusion boundary layer, which is determined by macroalgal morphology and water velocity. Energetic predictions that macroalgae growing at or near the lower limit of PAR for growth should rely on diffusive CO2 entry without acid and alkaline zones, and on NH4 + rather than NO3 − as nitrogen source, are only partially borne out by observation. The impact of global environmental change on marine macroalgae mainly relates to ocean acidification and warming with shoaling of the thermocline and decreased nutrient flux to the upper mixed layer. Predictions of the impact on macroalgae requires further experiments on interactions among increased inorganic carbon, increased temperature and decreased nitrogen and phosphorus supply, and, when possible, studies of genetic adaptation to environmental change.

Keywords

CO2 concentrating mechanism Chlorophyta Complementary chromatic adaptation Diffusive CO2 entry Phaeophyceae Photoinhibition Rhodophyta 

Abbreviations

CA

Carbonic anhydrase

CAM

Crassulacean acid metabolism

CCN

Complementary chromatic adaptation

CCM

CO2 Concentrating mechanism

DBL

Diffusion boundary layer

DIDS

4,4′-Diisothiocyano-2,2′stibene disulfonic acid

PAR

Photosynthetically active radiation

PEPc

Phosphoenolpyruvate carboxylase

PEPck

Phosphoenolpyruvate carboxykinase

Rubisco

Ribulose bisphosphate carboxylase oxygenase

UVA

Ultraviolet A

UBB

Ultraviolet B

UVR

Ultraviolet radiation

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

Barry Osmond continues, over more than 40 years, to be a scientific inspiration to JAR. JAR’s understanding of macroalgal photosynthesis has been much improved by collaboration with Mitchell Andrews, Lucy Ball, John Beardall, Rainer Box, Jenny Brenchley, Anthony Cheshire, Kenneth Dunton, Paul Falkowski, Richard Geider, Mario Giordano, Sheila Glidewell, Linda Handley, Howard Griffiths, Andrew Johnston, Beki Korb, Janet Kübler, Tony Larkum, Jeffrey MacFarlane, Shona McInroy, Stephen Maberly, Michele Marconi, Bruce Osborne, Barry Osmond, Lynda Poole, David Raffaelli, Simon Roberts, Goran Samuelsson, Charlie Scrimgeour, Andrew Smith, Misni bin Surif, Becky Taylor, Diana Walker and Alan Walker. Funding to JAR from NERC UK, the Royal Society of London and SERC (now BBSRC) UK is gratefully acknowledged. CLH was funded by Royal Society of New Zealand Marsden grant UOO0914. The University of Dundee is a registered Scottish Charity No SC 015096.

References

  1. Andrews M, Box R, Fyson A, Raven JA (1984) Source-sink characteristics of carbon transport in Chara hispida. Plant Cell Environ 7:683–687Google Scholar
  2. Arens K (1939) Physiologische Multipolaritat der Zelle von Nitella während der Photosynthese. Protoplasma 33:295–300CrossRefGoogle Scholar
  3. Atkinson MJ, Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28:568–574CrossRefGoogle Scholar
  4. Axelsson L, Larsson C, Ryberg H (2002) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant Cell Environ 22:969–978CrossRefGoogle Scholar
  5. Beer S (1996) Photosynthetic utilization of inorganic carbon in Ulva. Sci Mar 60(suppl 1):125–128Google Scholar
  6. Beer S, Björk M, Hellblom F, Axelsson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29:349–354CrossRefGoogle Scholar
  7. Behrendt L, Larkum AWD, Borman A, Qvortrup K, Chen M, Ralph P, Sørensen SJ, Trampe E, Kühl M (2011) Endolithic chlorophyll d-containing phototrophs. ISME J 5:1072–1076PubMedCrossRefGoogle Scholar
  8. Bell G (1997) The evolution of the life cycle of brown algae. Biol J Linn Soc 60:21–38CrossRefGoogle Scholar
  9. Bell G, Mooers AO (1997) Size and complexity among multicellular organisms. Biol J Linn Soc 60:345–363CrossRefGoogle Scholar
  10. Binzer T, Middelboe AL (2005) From thallus to communities: scale effects and photosynthetic performance in macroalgae communities. Mar Ecol Prog Ser 287:65–75CrossRefGoogle Scholar
  11. Binzer T, Sand-Jensen K, Middelboe AL (2006) Community photosynthesis of aquatic macrophytes. Limnol Oceanogr 51:2722–2733CrossRefGoogle Scholar
  12. 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 5:141–166CrossRefGoogle Scholar
  13. Bisson MA, Walker NA (1980) The Chara plasmalemma at high pH: electrical measurements show rapid selective uniport of H+ or OH−. J Membr Biol 56:1–7CrossRefGoogle Scholar
  14. Bjork M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast. Mar Ecol Prog Ser 284:109–116CrossRefGoogle Scholar
  15. Black CC, Burris JE, Everson RG (1976) Influence of oxygen concentration on photosynthesis in marine plants. Aust J Plant Physiol 3:81–86CrossRefGoogle Scholar
  16. Blinks LR (1960) Action spectra of chromatic transients and the Emerson effect in marine algae. Proc Natl Acad Sci USA 46:327–333PubMedCrossRefGoogle Scholar
  17. Blinks LR (1963) The effect of pH on the photosynthesis of littoral marine algae. Protoplasma 57:126–136CrossRefGoogle Scholar
  18. Boller AJ, Thomas PJ, Cavanaugh CM, Scott KM (2011) Low stable carbon isotope fractionation by coccolithophore Rubisco. Geochim Cosmochim Acta 75:7200–7207CrossRefGoogle Scholar
  19. Box R, Andrews M, Raven JA (1984) Intercellular transport and cytoplasmic streaming in Chara hispida. J Exp Bot 35:1016–1021CrossRefGoogle Scholar
  20. Brechignac F, Lucas WJ (1987) Photorespiration and internal CO2 accumulation in Chara coralline as inferred from the influence of dissolved inorganic carbon and O2 on photosynthesis. Plant Physiol 83:163–169PubMedCrossRefGoogle Scholar
  21. Brechignac F, Andre M, Gerbaud A (1986) Preferential photosynthetic uptake of HCO3 − in the marine macroalga Chondrus crispus. Plant Physiol 80:1059–1062PubMedCrossRefGoogle Scholar
  22. Brenchley JL, Raven JA, Johnston AM (1997) Resource acquisition in two intertidal seaweeds: seasonal variations and the effect of reproductive development. Mar Biol 120:367–375CrossRefGoogle Scholar
  23. Brenchley JL, Raven JA, Johnston AM (1998) Carbon and nitrogen allocation patterns in two intertidal fucoids: Fucus serratus and Himanthalia elongata (Phaeophyta). Eur J Phycol 33:307–313CrossRefGoogle Scholar
  24. Bulychev AA, Chenkashin AA, Rubin AA, Vredemberg WJ, Zykov VS, Müller SC (2001) A comparative study of the chloroplasts in acid and alkaline zones of Chara corallina. Bioelectrochemistry 53:225–232PubMedCrossRefGoogle Scholar
  25. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365–367PubMedCrossRefGoogle Scholar
  26. Chapman ARO, Craigie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205CrossRefGoogle Scholar
  27. Chapman ARO, Craigie JS (1978) Seasonal growth in Laminaria longicruris: relations with reserve carbohydrate storage and production. Mar Biol 46:209–213CrossRefGoogle Scholar
  28. Charpy-Roubard C, Sournia A (1990) The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobenthic primary production in the oceans. Mar Microb Food Webs 4:31–57Google Scholar
  29. Charrier B, Coelho SM, Le Bail A, Tonon T, Michel G, Potin P, Kloareg B, Boyen C, Peters AF, Cock JM (2008) Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol 177:319–332PubMedCrossRefGoogle Scholar
  30. Chen H, Dang W, Xie J, Zhao J, Weng Y (2012) Ultrafast energy transfer pathways in R-phycoerythrin from Polysiphonia urceolata. Photosynth Res 111:81–86PubMedCrossRefGoogle Scholar
  31. Clausen J, Junge W (2005) Search for intermediates of photosynthetic water oxidation. Photosynth Res 84:339–345Google Scholar
  32. Clausen J, Junge W (2004) Detection os an intermediate of photosynthetic water oxidation. Nature 430:480–483PubMedCrossRefGoogle Scholar
  33. Clausen J, Beckman K, Junger W, Messinger J (2005a) Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution. Plant Physiol 139:1444–1450PubMedCrossRefGoogle Scholar
  34. Clausen J, Junger W, Dau H, Haumann M (2005b) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 64:12775–12779CrossRefGoogle Scholar
  35. Cock JM, Coelho SM, Brownlee C, Taylor AR (2010) The Ectocarpus genome sequence: insights into brown algal biology and the evolutionary diversity of the eukaryotes. New Phytol 188:1–4PubMedCrossRefGoogle Scholar
  36. Collins S, Bell G (2004) Phenotypic consequences of 1000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569PubMedCrossRefGoogle Scholar
  37. Collins S, Bell G (2006) Evolution of natural algal populations at elevated CO2. Ecol Lett 9:129–135PubMedCrossRefGoogle Scholar
  38. Cooke RRM, Hurd CL, Lord JM, Peake BM, Raven JA (2004) Iron and zinc content of Hormosira banksii in New Zealand. N Z J Mar Freshwater Sci 38:73–85CrossRefGoogle Scholar
  39. Cornelisen CD, Wing SR, Clark KL, Bowman MH, Frew RD, Hurd CL (2007) Patterns in the δ13C and δ 15N signature of Ulva pertusa: interaction between physical gradients and nutrient source pools. Limnol Oceanogr 52:820–832CrossRefGoogle Scholar
  40. 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 48:137–144CrossRefGoogle Scholar
  41. Cardoll P, Franck F (2010) Eukaryotic algae: where lies the diversity of oxygenic photosynthesis. Photosynth Res 106:1–2CrossRefGoogle Scholar
  42. Crossett RN, Drew EA, Larkum AWD (1965) Chromatic adaptation of benthic marine algae. Nature 207:547–548CrossRefGoogle Scholar
  43. de Beer D, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24:1209–1217CrossRefGoogle Scholar
  44. Dillehay TD, Ramirez C, Pino MB, Collins MB, Rossen J, Pino-Navarro JD (2008) Monte Verde: seaweed, food, medicine and the peopling of South America. Science 320:784–786PubMedCrossRefGoogle Scholar
  45. Downton WJS, Bishop DG, Larkum AWD, Osmond CB (1976) Oxygen inhibition of photosynthetic O2 evolution in marine plants. Aust J Plant Physiol 3:73–78CrossRefGoogle Scholar
  46. Dring MJ (1981) Chromatic adaptation of photosynthesis in benthic marine algae: an examination of its ecological significance using a theoretical model. Limnol Oceanogr 26:271–284CrossRefGoogle Scholar
  47. Dring MJ, Lüning K (1985) Emerson enhancement effect and quantum yields of photosynthesis from marine macroalgae in simulated underwater light fields. Mar Biol 87:109–117CrossRefGoogle Scholar
  48. Enríquez S, Rodríguez-Román A (2006) Effect of water flow on the photosynthesis of three marine macrophytes from a fringing reef lagoon. Mar Ecol Prog Ser 323:119–132CrossRefGoogle Scholar
  49. Entwisle TJ (1989) Psilosiphon scoparium gen. et sp. nov (Lemaneaceae) a new red alga from south-east Australian streams. Phycologia 28:469–475CrossRefGoogle Scholar
  50. Erlandson JM, Braje TJ, Graham MH (2008) How old is MVII?—seaweeds, shorelines and the Pre-Clovis chronology of Monte Verde, Chile. J Isl Coast Archaeol 3:277–281CrossRefGoogle Scholar
  51. Fairhead VA, Cheshire AC (2004) Seasonal and depth related variation in the photosynthesis-irradiance response of Ecklonia radiata (Phaeophyta, Laminariales) at West Island, South Australia. Mar Biol 145:415–426Google Scholar
  52. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2 edn. Princeton University Press, Princeton, pp xiii + 484Google Scholar
  53. Fan X, Fang Y, Hu S, Wang G (2007) Generation and analysis of 5318 expressed sequence tags from the filamentous sporophyte of Porphyra haitanensis (Rhodophyta). J Phycol 43:1287–1294CrossRefGoogle Scholar
  54. Field CB, Behrenfeld MJ, Rabderson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240PubMedCrossRefGoogle Scholar
  55. Finkel ZV, Irwin AJ, Schofield O (2004) Resource limitation alters the ¾ power scaling of metabolic rates in phytoplankton. Mar Ecol Prog Ser 273:260–279CrossRefGoogle Scholar
  56. Flynn KJ (2009) Going for the slow burn: why should possessing a low relative growth rate nbe advantageous for microalgae. Plant Ecol Divers 2:179–189CrossRefGoogle Scholar
  57. Franklin L, Forster R (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32:207–232Google Scholar
  58. Franklin G, Levevaseur G, Osmond CB, Henley WJ, Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186:399–408CrossRefGoogle Scholar
  59. Fujii R, Kita M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Cogdell RJ, Hashimoto H (2012a) Isolation and purification of the major photosynthetic antenna, fucoxanthin-Chl a/c protein, from cultured discoid germlings of the brown alga, Cladosiphon okamuranus TOKIDA (Okinawa Mozuku). Photosynth Res 111:157–163PubMedCrossRefGoogle Scholar
  60. Fujii R, Kita M, Doe M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Mizoguchi T, Cogdell RJ, Hashimoto H (2012b) The pigment stoichiometry in a chlorophyll a/c photosynthetic antenna. Photosynth Res 111:165–172PubMedCrossRefGoogle Scholar
  61. Gabriel B, Teissié J (1996) Proton long-range migration along protein monolayers and its consequences on membrane coupling. Proc Natl Acad Sci USA 93:14251–14525Google Scholar
  62. 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. Glob Change Biol 16:2388–2398CrossRefGoogle Scholar
  63. Garbary DJ, Kim KY (2005) Anatomical differentiation and photosynthetic adaptation in brown algae. Algae 20:233–238CrossRefGoogle Scholar
  64. García-Sanchez MJ, Jaime MP, Ramos A, Sanders D, Fernández JA (2000) Sodium-dependent nitrate transport at the plasma membrane of leaf cells of the marine higher plant Zostera marina L. Plant Physiol 122:879–886PubMedCrossRefGoogle Scholar
  65. Geider RJ, DeLucia EH, Falkowski PG, Finzi AC, Grime PC, Grace J, Kana TM, La Roche J, Long SP, Osborne BA, Platt T, Prentice IC, Raven JA, Schlesinger WH, Smetacek V, Stuart V, Sathyendranath S, Thomas RJ, Vogelman TC, Williams P, Woodward FI (2001) Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats. Glob Change Biol 7:849–882CrossRefGoogle Scholar
  66. Gerard VA (1987) Hydrodynamic streamlining of Laminaria saccharina Lamour. in response to mechanical stress. J Exp Mar Biol Ecol 107:237–244CrossRefGoogle Scholar
  67. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation and evolution. Annu Rev Plant Biol 56:99–131PubMedCrossRefGoogle Scholar
  68. Gonen Y, Kimmel E, Friedlander M (1993) Effect of relative water motion on photosynthetic rate of red alga Gracilaria conferta. Hydrobiologia 260(261):493–498CrossRefGoogle Scholar
  69. Gonen Y, Kimmel E, Friedlander M (1995) Diffusion boundary layer transport in Gracilaria conferta (Rhodophyta). J Phycol 31:768–773CrossRefGoogle Scholar
  70. Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122PubMedCrossRefGoogle Scholar
  71. Graham LE, Graham J, Wilcox L (2009) Algae, 2nd edn. Benjamin Cummings (Pearson), San Francisco 720Google Scholar
  72. Granbom M, Pedersén M (1999) Carbon acquisition strategies of the red alga Eucheuma denticulate. Hydrobiologia 398(399):349–354CrossRefGoogle Scholar
  73. Gravot A, Dittami SM, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T (2010) Diurnal oscillations of metabolite abundances gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus silicolosus. New Phytol 188:98–110PubMedCrossRefGoogle Scholar
  74. Greene RH, Gerard VA (1990) Effects of high-frequency light fluctuations on growth and acclimation of the red alga Chondrus crispus. Mar Biol 105:337–344CrossRefGoogle Scholar
  75. Haldall P (1964) Ultraviolet action spectra of photosynthesis and photosynthetic inhibition is a green and a red alga. Physiol Plant 17:414–421CrossRefGoogle Scholar
  76. Haldall P (1968) Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol Bull 134:411–424CrossRefGoogle Scholar
  77. Hellblom F, Beer S, Bjork M, Axelsson L (2001) A buffer sensitive inorganic carbon utilization system in Zostera marina. Aquat Bot 69:55–62CrossRefGoogle Scholar
  78. Henley WJ, Ramus J (1989) Time course of ophysiological response of Ulva rotundata to growth irradiance transients. Mar Ecol Prog Ser 54:171–177CrossRefGoogle Scholar
  79. Henley WJ, Levevasseur G, Franklin LA, Osmond CB, Ramus J (1991) Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184:235–243CrossRefGoogle Scholar
  80. Hepburn CD, Hurd CL (2005) Conditional mutualism between the giant kelp Macrocystis pyrifera and colonial epifauna. Mar Ecol Progr Ser 302:37–48 Google Scholar
  81. Hepburn CD, Hurd CL, Frew RD (2006) Colony structure and seasonal differences in light and nitrogen modify the impact of epifauna on the giant kelp Macrocystis pyrifera (L.) C Agardh. Hydrobiologia 560:373–384CrossRefGoogle Scholar
  82. 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: a window to a high CO2 ocean? Glob Change Biol 17:2488–2497CrossRefGoogle Scholar
  83. Hepburn CD, Frew RD, Hurd CL (2012) Uptake and transport of nitrogen derived from sessile epifauna in the giant kelp Macrocystis pyrifera. Aquat Biol 14:121–128CrossRefGoogle Scholar
  84. Herfort L, Thake B, Roberts J (2002) Acquisition and use of bicarbonate by Emiliania huxleyi. New Phytol 156:427–436CrossRefGoogle Scholar
  85. Hillrichs S, Schmid R (2001) Activation by blue light of inorganic carbon acquisition for photosynthesis in Ectocarpus silicilosus organic acid pools and short-term carbon fixation. Eur J Phycol 36:71–79Google Scholar
  86. Huertas IE, Rouco M, López-Rodas V, Costas E (2011) Warming will affect phytoplankton differently: evidence from a mechanistic approach. Proc R Soc B 278:3534–3543PubMedCrossRefGoogle Scholar
  87. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472CrossRefGoogle Scholar
  88. Hurd CL, Pilditch CA (2011) Flow-induced morphological variations affect diffusion boundary-layer thickness of Macrocystis pyrifera (Heterokontophyta, Laminariales). J Phycol 47:341–351CrossRefGoogle Scholar
  89. Hurd CL, Galvin RS, Norton TA, Dring MJ (1993) Production of hyaline hairs by intertidal species of Fucus (Fucales) and their role in phosphate uptake. J Phycol 29:160–165CrossRefGoogle Scholar
  90. Hurd CL, Harrison PJ, Druehl LD (1996) Effect of seawater velocity on inorganic nitrogen uptake by morphologically distinct forms of Macrocystis integrifolia from wave-sheltered and exposed sites. Mar Biol 126:205–214CrossRefGoogle Scholar
  91. 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
  92. Hurd CL, Cornwall CE, Currie K, Hepburn CD, McGraw CM, Hunter KA, Boyd PW (2011) Metabolically induced pH fluctuations by some coastal calcifiers exceeds projected 22nd century ocean acidification: a mechanism for differential susceptibility? Glob Change Biol 17:3254–3262CrossRefGoogle Scholar
  93. Irwin S, Davenport J (2002) Hyperoxic boundary layers inhabited by the epiphytic meiofauna of Fucus serratus. Mar Ecol Prog Ser 244:73–79CrossRefGoogle Scholar
  94. Johansson G, Snoejis P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72CrossRefGoogle Scholar
  95. Johnson WS, Gigon A, Gulmon SL, Mooney HA (1974) Comparative photosynthetic capacities of intertidal algae under exposed and submerged conditions. Ecology 55:450–453CrossRefGoogle Scholar
  96. Johnston AM (1991) The acquisition of inorganic carbon by marine macroalgae. Can J Bot 69:1123–1132CrossRefGoogle Scholar
  97. Johnston AM, Raven JA (1986a) The analysis of photosynthesis in air and water by Ascophyllum nodosum (L) Le Jol. Oecologia 69:288–295CrossRefGoogle Scholar
  98. Johnston AM, Raven JA (1986b) Dark fixation studies on the intertidal macroalga Ascophyllum nodosum (Phaeophyta). J Phycol 22:78–83CrossRefGoogle Scholar
  99. Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae from different habitats. Oecologia 92:317–326CrossRefGoogle Scholar
  100. Kaspar HF (1992) Oxygen conditions on surfaces of coralline red algae. Mar Ecol Prog Ser 81:97–100CrossRefGoogle Scholar
  101. Keeley JE (1998) CAM photosynthesis in submerged aquatic plants. Bot Rev 64:121–175CrossRefGoogle Scholar
  102. Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310:694–695CrossRefGoogle Scholar
  103. Kevekordes K, Holland D, Häubner N, Jenkins S, Kos 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 45:442–449CrossRefGoogle Scholar
  104. Klaveness D, Lindstram E-A (2011) Hydrurus foetidus (Chromista: Chrysophyceae): a large freshwater chromophyta alga in culture. Phycol Res 59:105–112CrossRefGoogle Scholar
  105. Koehl MAR, Alberte RS (1988) Flow, flapping, and photosynthesis of Nereocystis luetkeana: a functional comparison of undulate and flat blade morphologies. Mar Biol 99:435–444CrossRefGoogle Scholar
  106. Koehl MAR, Silk WK, Liang H, Mahadevan L (2008) How kelp produce blade shapes suited to different flow regimes: a new wrinkle. Integr Comp Biol 48:834–851PubMedCrossRefGoogle Scholar
  107. Koehne B, Elli G, Jennings RC, Wilhem C, Trissl H-W (1999) Spectroscopic and molecular characterisation of a long wavelength absorbing antenna of Ostreobium sp. Biochim Biophys Acta Bioenerg 1412:94–107CrossRefGoogle Scholar
  108. Kolling DR, Brown TS, Ananyev G, Dismukes GC (2009) Photosynthetic oxygen evolution is not reversed at high oxygen pressures: consequences for the water-oxidising complex. Biochemistry 48:1381–1389PubMedCrossRefGoogle Scholar
  109. Kraemer GP, Chapman DJ (1991) Effects of tensile force and nutrient availability on carbon uptake and cell wall synthesis in blades of juvenile Egregia menziesii (Turn.) Aresch. (Phaeophyta). J Exp Mar Biol Ecol 149:267–277CrossRefGoogle Scholar
  110. Kübler JE, Raven JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Mar Ecol Prog Ser 110:203–209CrossRefGoogle Scholar
  111. Kübler JE, Raven JA (1995) The interaction between inorganic carbon supply and light supply in Palmaria palmata (Rhodophyta). J Phycol 31:369–375CrossRefGoogle Scholar
  112. Kübler JE, Raven JA (1996a) Inorganic carbon acquisition by red seaweeds grown under dynamic light regimes. Hydrobiologia 326(327):401–406CrossRefGoogle Scholar
  113. Kübler JE, Raven JA (1996b) Nonequilibrium rates of photosynthesis and respiration under dynamic light supply. J Phycol 32:963–969CrossRefGoogle Scholar
  114. Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed, Lomentaria articulata. Plant Cell Environ 22:1303–1310CrossRefGoogle Scholar
  115. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117CrossRefGoogle Scholar
  116. Langer G, Nehrke G, Probert I, Ly J, Ziveri P (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6:2637–2646CrossRefGoogle Scholar
  117. Lapointe BE, Tenore KR (1981) Experimental outdoor studies with Ulva fasctiata. 1. Interaction of light and nitrogen uptake, growth and biochemical composition. J Exp Mar Biol Ecol 53:128–152CrossRefGoogle Scholar
  118. Larkum AWD, Kuhl M (2005) Chlorophyll d: the puzzle resolved. Trends Plant Sci 10:355–357PubMedCrossRefGoogle Scholar
  119. Larkum AWD, Drew EA, Crossett RN (1967) The vertical zonation of attached marine algae in Malta. J Ecol 55:365–372Google Scholar
  120. Larkum AWD, Koch EW, Kühl M (2003) Diffusive boundary layers and photosynthesis of the epilithic algal community of coral reefs. Mar Biol 142:1073–1082Google Scholar
  121. Larsson C, Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34:79–86CrossRefGoogle Scholar
  122. Littler MM, Littler DS (1999) Blade abandonment: a novel mechanism for rapid epiphyte control in marine macrophytes. Ecology 80:1736–1746CrossRefGoogle Scholar
  123. Littler MM, Littler DS, Blair SM, Norris JN (1985) Deepest known plant life discovered on an unmarked seamount. Science 227:57–59PubMedCrossRefGoogle Scholar
  124. Lobban CS (1978) Translocation of 14C in Macrocystis integrifolia (Phaeophyceae). J Phycol 14:178–182CrossRefGoogle Scholar
  125. Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci. doi:10.10238/NGEO1441
  126. Longstaff BJ, Kildea T, Runcie JW, Cheshire A, Dennison WC, Hurd C, Kana T, Raven JA, Larkum AWD (2002) In situ measurements of marine plant photosynthesis. A comparison of oxygen exchange and electron transport rate methods using the marine macroalga Ulva lactuca (Chlorophyta). Photosynth Res 74:281–293PubMedCrossRefGoogle Scholar
  127. Lucas WJ, Smith FA (1973) The formation of alkaline and acid regions at the surface of Chara corallina cells. J Exp Bot 24:1–14CrossRefGoogle Scholar
  128. Lucas WJ, Keifer DW, Sanders D (1983) Bicarbonate transport in Chara coralline: evidence for cotransport with H+. J Membr Biol 73:263–276CrossRefGoogle Scholar
  129. Lucas WJ, Brechignac F, Mimura T, Gross JW (1989) Charasomes are not essential for photosynthetic utilization of HCO3 − in Chara coralline. Protoplasma 151:106–114CrossRefGoogle Scholar
  130. Lüning K (1990) Seaweeds: their environment, biogeography and ecophysiology. Wiley, New YorkGoogle Scholar
  131. Lüning K, Dring MJ (1985) Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli. Mar Biol 87:119–129CrossRefGoogle Scholar
  132. Lüther H (1949) Vorschlag zu einer Ökologischen Grundeinleitung der Hydrophyten. Acta Bot Fenn 44:1–15Google Scholar
  133. Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449CrossRefGoogle Scholar
  134. Maberly SC, Madsen TV (1990) Contribution of air and water to the carbon balance of Fucus spiralis. Mar Ecol Prog Ser 62:175–183CrossRefGoogle Scholar
  135. Maberly SC, Madsen TV (2002) Freshwater angiosperm varbon concentrating mechanisms: process and patterns. Funct Plant Biol 29:393–405Google Scholar
  136. Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492CrossRefGoogle Scholar
  137. Maberly SC, Ball LA, Raven JA, Sültemeyer D (2009) Inorganic carbon acquisition by chrysophytes. J Phycol 45:1052–1061CrossRefGoogle Scholar
  138. MacFarlane JJ, Raven JA (1985) External and internal CO2 transport in Lemanea: interactions with the kinetics of ribulose bisphosphate carboxylase. J Exp Bot 36:610–622CrossRefGoogle Scholar
  139. MacFarlane JJ, Raven JA (1989) Quantitative determination of the unstirred layer permeability and kinetic parameters of RUBISCO in Lemanea mamillosa. J Exp Bot 40:321–327CrossRefGoogle Scholar
  140. MacFarlane JJ, Raven JA (1990) C, N and P nutrition of Lemanea mamillosa Kutz. (Batrachospermales, Rhodophyta) in the Dighty Burn, Angus, Scotland. Plant Cell Environ 13:1–13CrossRefGoogle Scholar
  141. Manning WM, Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151:1–19Google Scholar
  142. Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography and depth on the δ13C and δ15N variation in a large collection of macroalgae. J Phycol 47:1023–1035CrossRefGoogle Scholar
  143. Markager S, Sand-Jensen K (1992a) Light requirements and depth zonation of marine macroalgae. Mar Ecol Prog Ser 88:83–92CrossRefGoogle Scholar
  144. Markager S, Sand-Jensen K (1992b) Implications of thallus thickness for growth-irradiance relationships of marine macroalgae. Eur J Phycol 31:79–87CrossRefGoogle Scholar
  145. Mass T, Genin A, Shavit U, Grinstein M, Tchernov D (2010) Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. Proc Natl Acad Sci USA 107:2527–2531PubMedCrossRefGoogle Scholar
  146. Matta RJ, Chapman DJ (1991) Photosynthetic responses and daily carbon balance of Colpomenia peregrina: seasonal variations and differences between intertidal and subtidal populations. Mar Biol 108:303–313CrossRefGoogle Scholar
  147. Medvedev ES, Stucebrukhov AA (2011) Proton diffusion along biological membranes. J Phys Condens Matter 23:234103. doi: 10.108/0953-8984/23/23/234103 PubMedCrossRefGoogle Scholar
  148. Mercado JM, Andría JR, Pérez-Llorens JL, Vergara JJ, Axelsson L (2006) Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina. Photosynth Res 88:259–268Google Scholar
  149. Middelboe AL, Binzer T (2004) Importance of canopy structure on photosynthesis in single- and multi-species assemblages of marine macroalgae. Oikos 107:422–432CrossRefGoogle Scholar
  150. Middelboe AL, Hansen PJ (2007a) Direct effects of pH and inorganic carbon on macroalgal photosynthesis and growth. Mar Biol Res 3:134–144CrossRefGoogle Scholar
  151. Middelboe AL, Hnasen PJ (2007b) High pH in shallow macroalgal habitats. Mar Ecol Prog Ser 338:107–117CrossRefGoogle Scholar
  152. Miller SM, Wing SR, Hurd CL (2006) Photoacclimation of Ecklonia radiata (Laminariales, Heterokontophyta) in Doubtful Sound, Fjordland, Southern New Zealand. Phycologia 45:44–52CrossRefGoogle Scholar
  153. Miller SM, Hurd CL, Wing SR (2011) Variations in growth, erosion, productivity and morphology of Ecklonia radiata (Alariaceae; Laminariales) along a fjord in Southern New Zealand. J Phycol 47:505–516CrossRefGoogle Scholar
  154. Moulin P, Andría JR, Axelsson L, Mercado JM (2011) Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer. Aquat Bot 95:31–38CrossRefGoogle Scholar
  155. Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhofophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845CrossRefGoogle Scholar
  156. Newman JR, Raven JA (1993) Carbonic anhydrase in Ranunculus penicillatus ssp. pseudofluitans: activity, location and implications for carbon assimilation. Plant Cell Environ 16:491–500CrossRefGoogle Scholar
  157. Newman JR, Raven JA (1999) CO2 is the main inorganic C species entering photosynthetically active leaf protoplasts of the freshwater macrophyte Ranunculus penicillatus ssp. pseudofluitans. Plant Cell Environ 22:1019–1026CrossRefGoogle Scholar
  158. Nielsen SL, Sand-Jensen K (1990) Allometric scaling pf maximal growth rate to surface/volume ratio. Limnol Oceanogr 25:177–181CrossRefGoogle Scholar
  159. Nielsen JAD, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71CrossRefGoogle Scholar
  160. Osmond CB, Valaane N, Haslam SM, Uotila P, Roksamdic Z (1981) Comparison of δ13C values in leaves of aquatic vascular macrophytes from different habitats in Britain and Finland: some applications for photosynthetic processes in aquatic plants. Oecologia 50:117–124CrossRefGoogle Scholar
  161. Osmond CB, Ramus J, Levevasaeur G, Franklin LA, Henley WJ (1993) Fluorescence quenching during photosynthesis and photoinhibition of Ulva rotundata blid. Planta 190:97–106CrossRefGoogle Scholar
  162. Pöhn M, Vopel K, Grünberger E, Ott J (2001) Microclimate of the brown alga Feldmannia caespitula interstitium under zero-flow conditions. Mar Ecol Prog Ser 210:285–290CrossRefGoogle Scholar
  163. Prats M, Teissié J, Tocanne J-F (1986) Lateral proton conduction at lipid-water interfaces and its implications for the chemiosmotic-coupling hypothesis. Nature 322:756–758CrossRefGoogle Scholar
  164. Price GD, Badger MR (1985) Inhibition by proton buffers of photosynthetic utilization of bicarbonate in Chara corallina. Aust J Plant Physiol 12:257–267CrossRefGoogle Scholar
  165. Price GD, Badger MR, Bassett ME, Whitecross MI (1985) Involvement of plasmalemmasomes and carbonic anhydrase in photosynthetic utilization of bicarbonate in Chara corallina. Aust J Plant Physiol 12:241–256CrossRefGoogle Scholar
  166. Prins MBA, Elzenga JTH (1989) Bicarbonate utilization: function and mechanism. Aquat Bot 34:59–83CrossRefGoogle Scholar
  167. Quigg A, Beardall J (2003) Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae. Plant Cell Environ 26:693–703CrossRefGoogle Scholar
  168. Quigg A, Kevecordes K, Raven JA, Beardall J (2006) Limitations on microalgal growth at very low photon flux rates: the role of energy slippage. Photosynth Res 88:299–310PubMedCrossRefGoogle Scholar
  169. Ramus J (1978) Seaweed anatomy and photosynthetic performance: the ecological significance of light guides, heterogeneous absorption and multiple scatter. J Phycol 14:352–362CrossRefGoogle Scholar
  170. Ramus J (1983) A physiological test of the theory of complementary chromatic adaptation. II. Brown, green and red seaweeds. J Phycol 19:173–178CrossRefGoogle Scholar
  171. Ramus J, Rosenberg G (1980) Diurnal photosynthetic performance of seaweeds measured under natural conditions. Mar Biol 56:21–28CrossRefGoogle Scholar
  172. Ramus J, Van der Meer JP (1983) A physiological test of the theory of complementary chromatic adaptation. II. Color mutants of a red seaweed. J Phycol 19:86–91CrossRefGoogle Scholar
  173. Rascio N, Cuccatop F, Dalle Vecchia F, La Rocca N, Larcher W (1999) Structural and functional characteristics of the leaves of Ranunculus trichophyllous Chaix, a freshwater submerged macrophyte. Plant Cell Environ 22:205–212CrossRefGoogle Scholar
  174. Raven JA (1976) Transport in algal cells. In: Lüttge U, Pitman MG (eds) Transport in cells and tissues encyclopedia of plant physiology, new series. Springer, Berlin, pp 129–188Google Scholar
  175. Raven JA (1981) Nutritional strategies of submerged benthic plants: the acquisition of C, N and P by rhizophytes and haptophytes. New Phytol 88:1–30CrossRefGoogle Scholar
  176. Raven JA (1984a) A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytol 98:593–625CrossRefGoogle Scholar
  177. Raven JA (1984b) Energetics and transport in aquatic plants. A.R. Liss, New York, pp xi + 587Google Scholar
  178. Raven JA (1991) Responses of aquatic photosynthetic organisms to increased solar UV-B. J Photochem Photobiol B 9:239–244CrossRefGoogle Scholar
  179. Raven JA (1992) How benthic algae cope with flowing freshwaters: resource acquisition and retention. J Phycol 28:133–146CrossRefGoogle Scholar
  180. Raven JA (1996) The bigger the fewer: size, taxonomic diversity and range of pigments in marine phototrophs. J Mar Biol Assoc UK 76:211–217CrossRefGoogle Scholar
  181. Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27:85–209CrossRefGoogle Scholar
  182. Raven JA (1998) Review of Kirk DC (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. CUP, pp. xvi + 381. Eur J Phycol 33: 275–278Google Scholar
  183. Raven JA (1999a) The minimum size of seeds and spores in relation to the ontogeny of homoiohydry. Funct Biol 13:5–14CrossRefGoogle Scholar
  184. Raven JA (1999b) The size of cells and organisms in relation to the evolution of embryophytes. Plant Biol 1:2–12CrossRefGoogle Scholar
  185. Raven JA (2003a) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth Res 77:155–171PubMedCrossRefGoogle Scholar
  186. Raven JA (2003b) Long-distance transport in non-vascular plants. Plant Cell Environ 26:73–85CrossRefGoogle Scholar
  187. Raven JA (2010) How have genome studies improved our understanding of organelle evolution and metabolism in red algae? In: Seckbach J, Chapman D, Weber A (eds) Red algae in the genomics age. One of a series of books on “Cellular origins, life in extreme environments and astrobiology”. Springer, Berlin, pp 275–290Google Scholar
  188. Raven JA (2011a) The cost of photoinhibition. Physiol Plant 142:87–104PubMedCrossRefGoogle Scholar
  189. Raven JA (2011b) Effects on marine algae of changed seawater chemistry with increasing CO2. Biol Environ Proc R Irish Acad 111B:1–17CrossRefGoogle Scholar
  190. Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci. doi: 10.1016/j.plantsci.2012.02.010
  191. Raven JA, Smith FA (1978) Effect of temperature on ion content, ion fluxes and energy metabolism in Chara corallina. Plant Cell Environ 1:231–238CrossRefGoogle Scholar
  192. Raven JA, Beardall J (1981a) The intrinsic permeability of biological membranes to H+: significance for low rates of energy transformation. FEMS Lett 10:1–5CrossRefGoogle Scholar
  193. Raven JA, Beardall J (1981b) Carbon dioxide as the exogenous inorganic carbon source for Batrachospermum and Lemanea. Br Phycol 16:165–175CrossRefGoogle Scholar
  194. Raven JA, Beardall J (1982) The lower limit of photon fluence rate for phototrophic growth: the significance of ‘slippage’ reactions. Plant Cell Environ 5:117–124Google Scholar
  195. Raven JA, Richardson K (1984) Dinophyte flagella: a cost-benefit analysis. New Phytol 98:259–276CrossRefGoogle Scholar
  196. Raven JA, Samuelsson G (1988) Ecophysiology of Fucus vesiculosus L. close to its Northern limit in the Gulf of Bothnia. Bot Mar 31:399–410CrossRefGoogle Scholar
  197. Raven JA, Osmond CB (1992) Inorganic C assimilation processes and their ecological significance in inter- and sub-tidal macroalgae of North Carolina. Funct Ecol 6:41–47CrossRefGoogle Scholar
  198. Raven JA, Taylor R (2003) Macroalgal growth in nutrient-enriched estuaries: a biogeochemical and evolutionary perspective. Water Air Soil Pollut Focus 3:7–26CrossRefGoogle Scholar
  199. Raven JA, Waite A (2004) Tansley Review: the evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytol 161:45–61CrossRefGoogle Scholar
  200. Raven JA, Larkum AWD (2007) Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations? Photosynth Res 94:31–42PubMedCrossRefGoogle Scholar
  201. Raven JA, Beardall J, Griffiths H (1982) Inorganic C-sources for Lemanea, Cladophora and Ranunculus in a fast-flowing stream: measurements of gas exchange and of carbon isotope ratio and their ecological implications. Oecologia 53:68–78CrossRefGoogle Scholar
  202. Raven JA, Osborne BA, Johnston A (1985) Uptake of CO2 by aquatic vegetation. Plant Cell Environ 8:417–425CrossRefGoogle Scholar
  203. Raven JA, Beardall J, Roberts S (1989) The ecophysiology of inorganic carbon assimilation by Durvillaea potatorum (Durvillaeales, Phaeophyta). Phycologia 28:429–437CrossRefGoogle Scholar
  204. Raven JA, Wollenweber B, Handley LL (1992) A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytol 121:19–32Google Scholar
  205. Raven JA, Beardall J, Johnston AM, Kübler JE, Geoghegan I (1995) Inorganic carbon acquisition by Hormosira banksii (Phaeophyta: Fucales) and its epiphyte Notheia anomala (Phaeophyta: Fucales). Phycologia 34:267–277CrossRefGoogle Scholar
  206. Raven JA, Beardall J, Johnston AM, Kübler JE, McInroy SG (1996) Inorganic carbon acquisition by Xiphophora chondrophylla (Fucales). Phycologia 35:83–89CrossRefGoogle Scholar
  207. Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149CrossRefGoogle Scholar
  208. Raven JA, Kübler JI, Beardall J (2000) Put out the light, and then put out the light. J Mar Biol Assoc UK 80:1–25CrossRefGoogle Scholar
  209. Raven JA, Beardall J, Chudek JA, Scrimgeour CM, Clayton MN, McInroy SG (2001) Altritol synthesis by Notheia anomala. Phytochemistry 68:389–394CrossRefGoogle Scholar
  210. Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredricksen J, Dunton KH (2002a) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378CrossRefGoogle Scholar
  211. Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift M, Fredriksen J, Dunton KH (2002b) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90:525–536PubMedCrossRefGoogle Scholar
  212. Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005) Algae lacking carbon concentrating mechanisms. Can J Bot 83:879–890CrossRefGoogle Scholar
  213. Raven JA, Giordano M, Beardall J, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos Trans R Soc B 367:493–507CrossRefGoogle Scholar
  214. Ray S, Klenell M, Chen K-S, Pedersén M, Snoeijs P (2003) Carbon acquisition mechanisms in Chara tomentosa. Aquat Bot 76:141–154CrossRefGoogle Scholar
  215. Reiskind JB, Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88:2883–2887Google Scholar
  216. Reynolds CJ (1984) The ecology of freshwater phytoplankton. Cambridge University Press, CambridgeGoogle Scholar
  217. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  218. Roberson LM, Coyer JA (2004) Variation in blade morphology of the kelp Eisenia arborea: incipient speciation due to local water motion? Mar Ecol Prog Ser 282:115–128CrossRefGoogle Scholar
  219. Rodriguez MA, dos Santos CP, Young AJ, Strbac D, Hall DO (2002) A smaller and impaired xanthophyll cycle makes the deeper-sea macroalgae Laminaria abyssalis (Phaeophyceae) highly sensitive to daylight when compared with shallow water Laminaria digitata. J Phycol 28:939–947CrossRefGoogle Scholar
  220. Rubio L, Linres-Rued A, Garcia-Sánchez MJ, Fernández JA (2005) Physiological evidence for a sodium-dependent high affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of Zostera marina L. J Exp Bot 56:613–622PubMedCrossRefGoogle Scholar
  221. Runcie JW, Gunzel CFD, Mcdermid KJ (2008) In situ photosynthetic rates of tropical marine macroalgae at their lower depth limits. Eur J Phycol 43:377–388CrossRefGoogle Scholar
  222. Sand-Jensen KAJ (1977) Effect of epiphytes on ellegrass photosynthesis. Aquat Bot 3:55–83CrossRefGoogle Scholar
  223. Sand-Jensen K, Binzer T, Middelboe AL (2007) Scaling of photosynthetic production in aquatic macrophytes—a review. Oikos 116:280–294Google Scholar
  224. Schaffelke B (1999) Particulate organic matter as a novel nutrient source for tropical macroalgae. J Phycol 35:1150–1157CrossRefGoogle Scholar
  225. Schubert N, García-Mendoza E (2008) Photo-inhibition in red algal species with differents carotenoid profile. J Phycol 44:1437–1446CrossRefGoogle Scholar
  226. Schubert N, García-Mendoza E, Pacheco-Ruiz I (2006) Carotenoid composition of marine red algae. J Phycol 42:1208–1216CrossRefGoogle Scholar
  227. Schubert N, García-Mendoza E, Enríquez S (2011) Is the photo-acclimation response of Rhodophyta conditioned by the species carotenoid profile? Limnol Oceanogr 56:2347–2361CrossRefGoogle Scholar
  228. Shepherd SA (1981) Ecological strategies in a deep-water red algal community. Bot Mar 24:457–463CrossRefGoogle Scholar
  229. Sherlock DJ, Raven JA (2001) Interactions between carbon dioxide and oxygen in the photosynthesis of three species of marine red algae. Bot J Scotl 53:33–43CrossRefGoogle Scholar
  230. Shevela D, Beckmann D, Clausen J, Junge U, Messinger J (2011) Membrane-inlet mass spectrometry reveals a high driving force for oxygen production by photosystem II. Proc Natl Acad Sci USA 108:3602–3607PubMedCrossRefGoogle Scholar
  231. Six C, Sherrard R, Lionard M, Roys S, Campbell DA (2009) Photosystem II dynamics among ecotypes of the green alga Ostreococcus. Plant Physiol 151:379–390PubMedCrossRefGoogle Scholar
  232. Smith SV (1981) Marine macrophytes as a global carbon sink. Science 211:838–840PubMedCrossRefGoogle Scholar
  233. Smith FA, Walker NA (1980) Photosynthesis in aquatic plants: effects on unstirred layers in relation to the assimilation of CO2 and HCO3 − and to carbon isotope discrimination. New Phytol 86:245–259CrossRefGoogle Scholar
  234. Smith JR, Walker NA (1983) Membrane conductance of Chara measured in the acid and alkaline zones. J Membr Biol 73:193–202CrossRefGoogle Scholar
  235. Smith RG, Bidwell RGS (1989) Mechanism of CO2 uptake by the red macroalga, Chondrus crispus. Plant Physiol 89:93–99PubMedCrossRefGoogle Scholar
  236. Smith JR, Walker NA (1985) Effects of pH and light on the Membrane conductance measured in the acid and basic zones of Chara. J Membr Biol 83:193–205CrossRefGoogle Scholar
  237. Smith SME, Morgan D, Musset B, Cherney VV, Place AB, Hastings JW, De Coursey TE (2011) Voltage-gated proton channel in a dinoflagellate. Proc Natl Acad Sci USA 108:18162–18167PubMedCrossRefGoogle Scholar
  238. Spilling K, Titelman J, Greve TM, Kühl M (2010) Microsensor measurements of the external and internal microenvironment of Fucus vesiculosus (Phaeophyceae). J Phycol 46:1350–1355CrossRefGoogle Scholar
  239. Staal M, Elzenga JTM, Prins HBA (1989) 14C fixation by leaves and leaf protoplasts of the submerged aquatic angiosperm Potamogeton lucens: carbon dioixide or bicarbonate. Plant Physiol 90:1035–1040PubMedCrossRefGoogle Scholar
  240. Steinacher M, Joos F, Frolicher TL, Bopp L, Cadule P, Cocco V, Doney SC, Gehlen M, Lindsay K, Moore JK, Schneider B, Segschneider J (2010) Projected 21st century decrease in marine primary productivity: a multi-model analysis. Biogeosciences 7:979–1005CrossRefGoogle Scholar
  241. Suffrian K, Schulz KG, Gutowska MA, Reibesell U, Bleich M (2011) Cellular pH measurements in Emiliania huxleyi reveal pronounced membrane proton permeability. New Phytol 190:595–608PubMedCrossRefGoogle Scholar
  242. Surif MB, Raven JA (1989a) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78:97–105CrossRefGoogle Scholar
  243. Surif MB, Raven JA (1989b) Occurrence of diel changes in titratable acidity of plant cell contents: indication of CAM-like metabolism in plants native to Scotland and comparisons with plants from elsewhere. Trans Bot Soc Edinb 45:235–244CrossRefGoogle Scholar
  244. Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80CrossRefGoogle Scholar
  245. Suzuki Y, Kura K, Kudo I, Matsunaga K (1995) Iron requirements of the brown macroalgae Laminaria japonica, Undaria pinattifida (Phaeophyta) and the crustose coralline alga Lithophyllum yessoenese (Rhodophyta), and their competition in the northern Japan Sea. Phycologia 34:201–205CrossRefGoogle Scholar
  246. Takahashi S, Milward SE, Yamone W, Evans JR, Hiller W, Badger MR (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993PubMedCrossRefGoogle Scholar
  247. Taylor AR, Chrachri A, Wheeler G, Goddard H, Brownlee C (2011) A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. PLoS One 9:e1001085Google Scholar
  248. Tcherkez GCB, Farquhar GB, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly completely optimized. Proc Natl Acad Sci USA 103:1246–1251CrossRefGoogle Scholar
  249. The Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05. The Royal Society, London, p 57Google Scholar
  250. Thornber CS (2006) Functional properties of the isomorphic algal life cycle. Integr Comp Biol 46:605–614PubMedCrossRefGoogle Scholar
  251. Uku J, Beer S, Björk M (2005) Buffer sensitivity of photosynthetic carbon utilization in tropical seagrasses. Mar Biol 147:1085–1090CrossRefGoogle Scholar
  252. Van den Hoek C, Mann DG, Jahns HN (1995) Algae: an introduction. Cambridge University Press, Cambridge 623Google Scholar
  253. Vis ML, Harper JT, Saunders GW (2008) Large subunit rDNA and rbcL gene sequence data place Petrohua baerbaei gen. et sp. Nov in the Batrachospermales (Rhodophyta) but do not provide further resolution among taxa in this order. Phycol Res 55:103–110CrossRefGoogle Scholar
  254. Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438PubMedCrossRefGoogle Scholar
  255. Walker NA (1985) The uptake of inorganic carbon by freshwater plants. Plant Cell Environ 6:323–328Google Scholar
  256. Walker NA, Smith FA, Cathers IR (1980) Bicarbonate assimilation by freshwater charophytes and higher plants. I. Membrane transport of bicarbonate is not proven. J Membr Biol 57:51–58CrossRefGoogle Scholar
  257. Wang C, Fan X, Wang G, Niu J, Zhou B (2011) Differential expression of Rubisco in sporophytes and gametophytes of some marine macroalgae. PLoS One 6:e16351PubMedCrossRefGoogle Scholar
  258. Wangpraseurt D, Weber M, Røy H, Polerecky L, de Beer D, Suharsono, Nugues MM (2012) In situ oxygen dynamics in coral–algal interactions. PLoS ONE 7:e31192. doi: 10.1371/journal.pone.0031192 PubMedCrossRefGoogle Scholar
  259. Wernberg T, Vanderklift MA (2010) Contribution of temporal and spatial components to morphological variation in the kelp Ecklonia (Laminariales). J Phycol 46:153–161CrossRefGoogle Scholar
  260. Wernberg T, Coleman M, Fairhead A, Miller S, Thomsen M (2003) Morphology of Ecklonia radiata (Phaeophyta, Laminariales) along its geographic distribution in south-western Australia and Australasia. Mar Biol 143:47–55CrossRefGoogle Scholar
  261. Weykam G, Gómez I, Wiencke C, Iken K, Klöser H (1995) Photosynthetic characteristics and C:N ratios of macroalgae from King George Island, (Antarctica). J Exp Mar Biol Ecol 204:1–22CrossRefGoogle Scholar
  262. Wheeler WN (1980) Effect of boundary layer transport on the fixation of carbon by the giant kelp Macrocystis pyrifera. Mar Biol 56:103–110CrossRefGoogle Scholar
  263. Williams SL, Dethier MN (2005) High and dry: variation in net photosynthesis of the intertidal seaweed Fucus gardneri. Ecology 86:2373–2379CrossRefGoogle Scholar
  264. Wing SR, Patterson MR (1993) Effects of wave-induced light flecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile (Phaeophyceae). Mar Biol 116:519–525CrossRefGoogle Scholar
  265. Wing SR, Leichter JJ, Denny MW (1993) A dynamic model for wave-induced light fluctuations ion a kelp forest. Limnol Oceanogr 38:396–407CrossRefGoogle Scholar
  266. Wing SR, Leichter JJ, Perrin C, Rutger SM, Bowman MH, Cornelisen CD (2007) Topographic shading and wave exposure influence morphology and ecophysiology of Eckonia radiata (C. Aghard 1817) in Fiordland. N Z Limnol Oceanogr 52:1853–1864CrossRefGoogle Scholar
  267. Xu Z, Gao KS (2009) Impacts of UV radiation on growth, and photosynthetic C acquisition in Gracilaria lemanaeiformis (Rhodophyta) under P-limited and replete conditions. Funct Plant Biol 36:1057–1064CrossRefGoogle Scholar
  268. Xu Z, Zou DH, Gao KS (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake by the marine macroalga Gracilaria lemanaeiformis (Rhodophyta). Bot Mar 63:123–129CrossRefGoogle Scholar
  269. Zechman FW, Verbruggen H, Leliaert F, Ashworth M, Buchheim MA, Fawley MR, Spalding H, Pusechel CM, Buchhem J, Verghese B, Hanisak MD (2010) An unrecognised ancient lineage of green plants persists in deep marine waters. J Phycol 46:1288–1295CrossRefGoogle Scholar
  270. Zou D, Gao K (2009) Effect of elevated CO2 on the red seaweed Gracilaria lemaneformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517CrossRefGoogle Scholar
  271. Zou DH, Gao KS (2010) Acquisition of inorganic carbon by Endaraachne binghamiae (Scytosiphonales, Phaeophyceae). Eur J Phycol 45:117–126CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Division of Plant SciencesUniversity of Dundee at the James Hutton InstituteDundeeScotland, UK
  2. 2.School of Plant BiologyUniversity of Western AustraliaCrawleyAustralia
  3. 3.Department of BotanyUniversity of OtagoDunedinNew Zealand

Personalised recommendations