Journal of Applied Phycology

, Volume 29, Issue 1, pp 381–393 | Cite as

Red alga Palmaria palmata—growth rate and photosynthetic performance under elevated CO2 treatment

  • Stefan SebökEmail author
  • Werner B. Herppich
  • Dieter Hanelt


Marine macroalgae offer a feasible solution for reducing CO2 emissions by fixing CO2 as algal biomass and thus providing a source of renewable energy. The perennial red alga Palmaria palmata was cultivated and supplied with increased CO2 concentrations starting with 22 μmol kg−1 (pH 8.53) to 9770 μmol kg−1 (pH 6.04). Experiments covered test periods of 28 days, 7 days, and 2 h to examine the possible influence of different treatment durations. Biomass productivity over 28 days showed an increased production rate, which continuously declined with increasing CO2 concentration. After 7 days, the productivity was below the controls, suggesting a lag phase or necessary adaptation period to elevated CO2 concentrations of more than 7 days. Concerning the effects on maximum electron transport rate (ETRmax), light-harvesting efficiency (alpha), and light saturation of the photosynthetic electron transport (E k ), a stimulating influence was identified with the effect becoming more significant the shorter the test period was. The treatment with elevated CO2 concentrations for 28 days led to a decrease in photochemical efficiency (Y(II)) and regulated nonphotochemical energy dissipation (Y(NPQ)). In contrast, the treatment duration of 7 days predominantly increased photochemical quenching whereas the 2-h treatment resulted in a significant increase in photochemical quenching and in a significant decrease in nonregulated nonphotochemical energy dissipation. Hence, elevated CO2 concentrations over a prolonged time period interfered more distinctively with the fluorescence quenching ability of P. palmata.


Palmaria palmata Rhodophyta Biomass CO2 Photosynthesis Fluorescence quenching 



S. Sebök thanks Prof. K. Lüning for his constructive suggestions and comments during the course of this research and for his valuable advice during the preparation of this manuscript.


  1. Allen E, Wall DM, Herrmann C, Xia A, Murphy JD (2015) What is the gross energy yield of third generation gaseous biofuel sourced from seaweed? Energy 81:352–360CrossRefGoogle Scholar
  2. Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms and their regulation. Funct Plant Biol 29:335–347CrossRefGoogle Scholar
  3. Bidwell RGS, McLachlan J, Lloyd NDH (1985) Tank cultivation of Irish Moss Chondrus crispus Stackh. Bot Mar 28:87–97CrossRefGoogle Scholar
  4. Bilger W, Björkman O, Thayer SS (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol 91:542–551CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production processing and extractions of biofuels and coproducts. Renew Sust Energ Rev 14:557–577CrossRefGoogle Scholar
  6. Bruhn A, Dahl J, Nielsen HB, Nikolaisen L, Rasmussen MB, Markager S, Olesen B, Arias C, Jensen PD (2011) Bioenergy potential of Ulva lactuca: biomass yield methane production and combustion. Bioresour Technol 102:2595–2604CrossRefPubMedGoogle Scholar
  7. Celis-Plá PSM, Hall-Spencer JM, Horta PA, Milazzo M, Korbee N, Cornwall CE, Figueroa FL (2015) Macroalgal responses to ocean acidification depend on nutrient and light levels. Front Mar Sci 2:26Google Scholar
  8. Chen S, Beardall J, Gao K (2014) A red tide alga grown under ocean acidification upregulates its tolerance to lower pH by increasing its photophysiological functions. Biogeosciences 11:4829–4838CrossRefGoogle Scholar
  9. Chen B, Zou D, Ma J (2016) Interactive effects of elevated CO2 and nitrogen–phosphorus supply on the physiological properties of Pyropia haitanensis (Bangiales, Rhodophyta. J Appl Phycol 28:1235–1243Google Scholar
  10. Chynoweth DP (2005) Colloquium Proceedings: Renewable biomethane from land and ocean energy crops and organic wastes. HortSci 40:283–286Google Scholar
  11. De Paula Silva PH, de Nys R, Paul NA (2012) Seasonal growth dynamics and resilience of the green tide alga Cladophora coelothrix in high-nutrient tropical aquaculture. Aquacult Environ Interact 2:253–266Google Scholar
  12. De Paula Silva PH, Paul NA, De Nys R, Mata L (2013) Enhanced production of green tide algal biomass through additional carbon supply. PLoS One 8:e81164CrossRefPubMedPubMedCentralGoogle Scholar
  13. Demetropoulos CL, Langdon CJ (2004a) Enhanced production of Pacific dulse (Palmaria mollis) for co-culture with abalone in a land-based system: effects of stocking density, light, salinity and temperature. Aquaculture 235:471–488CrossRefGoogle Scholar
  14. Demetropoulos CL, Langdon CJ (2004b) Enhanced production of Pacific dulse (Palmaria mollis) for co-culture with abalone in a land-based system: nitrogen phosphorus and trace metal nutrition. Aquaculture 235:433–455CrossRefGoogle Scholar
  15. Demetropoulos CL, Langdon CJ (2004c) Enhanced production of Pacific dulse (Palmaria mollis) for co-culture with abalone in a land-based system: effects of seawater exchange pH and inorganic carbon concentration. Aquaculture 235:457–470CrossRefGoogle Scholar
  16. Dickson AG (1990) Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Res A 37:755–766CrossRefGoogle Scholar
  17. Dincer I (2000) Renewable energy and sustainable development: a crucial review. Renew Sust Energ Rev 4:157–175CrossRefGoogle Scholar
  18. Engle CR, Balakrishnan R, Hanson TR, Molnar JJ (1997) Economic considerations. In: Egna HS, Boyd CE (eds) Dynamics of pond aquaculture. CRC Press, New York, pp. 377–395Google Scholar
  19. Enríquez S, Borowitzka MA (2010) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences - methods and applications. Springer, Dordrecht, pp. 187–208CrossRefGoogle Scholar
  20. Ernst DH (2000) Aqua Farm: simulation and decision-support software for aquaculture facility design and management planning. Dissertation, Oregon State UniversityGoogle Scholar
  21. Evans F, Langdon CJ (2000) Co-culture of dulse Palmaria mollis and red abalone Haliotis rufescens under limited flow conditions. Aquaculture 185:137–158Google Scholar
  22. Falk S, Palmqvist K (1992) Photosynthetic light utilization efficiency, photosystem II heterogeneity, and fluorescence quenching in Chlamydomonas reinhardtii during the induction of the CO2-concentrating mechanism. Plant Physiol 100:685–691Google Scholar
  23. Figueroa FL, Barufi JB, Malta EJ, Conde-Álvarez R, Nitschke U, Arenas F, Mata M, Connan S, Abreu MH, Marquardt R, Vaz-Pinto F, Konotchick T, Celis-Plá PSM, Hermoso M, Ordoñez G, Ruiz E, Flores P, de los Ríos J, Kirke D, Chow F, Nassar CAG, Robledo D, Pérez-Ruzafa A, Bañares-España E, Altamirano M, Jiménez C, Korbee N, Bischof K, Stengel DB (2014a) Short-term effects of increasing CO2, nitrate and temperature on three Mediterranean macroalgae: biochemical composition. Aquat Biol 22:177–193CrossRefGoogle Scholar
  24. Figueroa FL, Malta EJ, Bonomi-Barufi J, Conde-Álvarez R, Nitschke U, Arenas F (2014b) Short-term effects of increasing CO2, nitrate and temperature on three Mediterranean macroalgae: biochemical composition. Aquat Biol 22:177–193CrossRefGoogle Scholar
  25. Friedlander M, Levy I (1995) Cultivation of Gracilaria in outdoor tanks and ponds. J Appl Phycol 7:315–324CrossRefGoogle Scholar
  26. Fritsche UR, Sims REH, Monti A (2010) Direct and indirect land-use competition issues for energy crops and their sustainable production – an overview. Biofuels Bioprod Biorefin 4:692–704CrossRefGoogle Scholar
  27. Gao K, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60CrossRefGoogle Scholar
  28. 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 concentrations. J Appl Phycol 3:355–362CrossRefGoogle Scholar
  29. Gao K, Aruga Y, Asada K, Kiyohara M (1993) Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5:563–571CrossRefGoogle Scholar
  30. Garcia-Sanchez MJ, Fernandez JA, Niell FX (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194:55–61CrossRefGoogle Scholar
  31. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connel SD, Dupont S, Fabricius KE, Hall-Spencer JH, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan ML, Widdicombe S, Harley CD (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15CrossRefPubMedGoogle Scholar
  32. Gellenbeck KW, Kraemer GP, McMurtry LA, Chapman DJ (1988) An experimental culture system for macroalgae and other aquatic life. Aquaculture 74:385–391CrossRefGoogle Scholar
  33. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation and evolution. Annu Rev Plant Biol 56:99–131CrossRefPubMedGoogle Scholar
  34. 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 213:64–70CrossRefPubMedGoogle Scholar
  35. Hafting JT, Critchley AT, Cornish ML, Hubley SA, Archibald AF (2011) On-land cultivation of functional seaweed products for human usage. J Appl Phycol 24:385–392CrossRefGoogle Scholar
  36. Hahn H, Krautkremer B, Hartmann K, Wachendorf M (2014) Review of concepts for a demand-driven biogas supply for flexible power generation. Renew Sust Energ Rev 29:383–393CrossRefGoogle Scholar
  37. Hanelt D, Wiencke C, Nultsch W (1997) Influence of UV radiation on the photosynthesis of arctic macroalgae in the field. J Photochem Photobiol B 38:40–47CrossRefGoogle Scholar
  38. Herppich WB, Herppich M, von Willert DJ (1998a) Ecophysiological investigations on plants of the genus Plectranthus (Lamiaceae). Influence of environment and leaf age on CAM gas exchange and leaf water relations in Plectranthus marrubioides Benth. Flora 193:99–109Google Scholar
  39. Herppich WB, Herppich M, Tüffers A, von Willert DJ, Midgley GF, Veste M (1998b) Photosynthetic responses to CO2 concentration and photon fluence rates in the CAM-cycling plant Delosperma tradescantioides (Mesembryanthemaceae). New Phytol 138:433–440CrossRefGoogle Scholar
  40. Herppich WB, Flach BM-T, von Willert DJ, Herppich M (1997) Field investigations in Welwitschia mirabilis during a severe drought. II. Influence of leaf age, leaf temperature and irradiance on photosynthesis and photoinhibition. Flora 192:65–174CrossRefGoogle Scholar
  41. Hofmann LC, Bischof K, Baggini C, Johnson A, Koop-Jakobsen K, Teichberg M (2015) CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte. Oecologia 177:1157–1169CrossRefPubMedGoogle Scholar
  42. Huguenin JE (1976) An examination of problems and potentials for future large-scale intensive seaweed culture systems. Aquaculture 9:313–342CrossRefGoogle Scholar
  43. Israel A, Gavrieli J, Glazer A, Friedlander M (2005) Utilization of flue gas from a power plant for tank cultivation of the red seaweed Gracilaria cornea. Aquaculture 249:311–316CrossRefGoogle Scholar
  44. Israel A, Levy I, Friedlander M (2006) Experimental tank cultivation of Porphyra in Israel. J Appl Phycol 18:235–240CrossRefGoogle Scholar
  45. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  46. Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia 92:317–326CrossRefGoogle Scholar
  47. Kirschbaum MUF (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiol 155:117–124CrossRefPubMedGoogle Scholar
  48. Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application. Notes 1:27–35CrossRefGoogle Scholar
  49. Koch M, Bowes G, Ross C, Zhang X (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132CrossRefPubMedGoogle Scholar
  50. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218CrossRefPubMedGoogle Scholar
  51. Kübler JE, Raven JA (1995) The interaction between inorganic carbon acquisition and light supply in Palmaria palmata (Rhodophyta). J Phycol 31:369–375CrossRefGoogle Scholar
  52. Le Gall L, Pien S, Rusig AM (2004) Cultivation of Palmaria palmata (Palmariales, Rhodophyta) from isolated spores in semi-controlled conditions. Aquaculture 229:181–191CrossRefGoogle Scholar
  53. Lewis E, Wallace D (1998) Program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center. Oak Ridge National Laboratory, Oak RidgeGoogle Scholar
  54. Li W, Gao K, Beardall J (2012) Interactive effects of ocean acidification and nitrogen limitation on the diatom Phaeodactylum tricornutum. PLoS One 7:e51590CrossRefPubMedPubMedCentralGoogle Scholar
  55. Li Y, Horsman M, Wu N, Lan CQ, Dubois-Calero N (2008) Biofuels from microalgae. Biotechnol Prog 24:815–820PubMedGoogle Scholar
  56. Lüning K, Pang S (2002) Mass cultivation of seaweeds: current aspects and approaches. J Appl Phycol 15:115–119CrossRefGoogle Scholar
  57. Menendez M, Martınez M, Comin FA (2001) A comparative study of the effect of pH and inorganic carbon resources on the photosynthesis of three floating macroalgae species of a Mediterranean coastal lagoon. J Exp Mar Biol Ecol 256:123–136CrossRefPubMedGoogle Scholar
  58. Mercado JM, Javier F, Gordillo L, Niell FX, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta. J Appl Phycol 11:455–461CrossRefGoogle Scholar
  59. Morgan KC, Simpson FJ (1981a) The cultivation of Palmaria palmata. Effect of light intensity and nitrate supply on growth and chemical composition. Bot Mar 24:273–277Google Scholar
  60. Morgan KC, Simpson FJ (1981b) The cultivation of Palmaria palmata. Effect of high concentrations of nitrate and ammonium on growth and nitrogen uptake. Aquat Bot 11:167–171CrossRefGoogle Scholar
  61. Morgan KC, Shacklock PF, Simpson FJ (1980) Some aspects of the culture of Palmaria palmata in greenhouse tanks. Bot Mar 23:765–770Google Scholar
  62. Mueller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefGoogle Scholar
  63. Murru M, Sandgren DC (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound Washington, USA. J Phycol 40:837–845CrossRefGoogle Scholar
  64. Mussgnug JH, Klassen V, Schlüter A, Kruse O (2010) Microalgae as substrates for fermentative biogas production in a combined biorefinery concept. J Biotechnol 150:51–56CrossRefPubMedGoogle Scholar
  65. Nygård CA, Dring MJ (2008) Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. Eur J Phycol 43:253–262CrossRefGoogle Scholar
  66. Olesen JE, Bindi M (2002) Consequences of climate change for European agricultural productivity, land use and policy. Eur J Agron 16:239–262CrossRefGoogle Scholar
  67. Olischläger M, Wiencke C (2013) Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J Exp Bot 64:5587–5597CrossRefPubMedGoogle Scholar
  68. Pang S, Lüning K (2004) Tank cultivation of the red alga Palmaria palmata: effects of intermittent light on growth rate, yield and growth kinetics. J Appl Phycol 16:93–99CrossRefGoogle Scholar
  69. Pang S, Lüning K (2006) Tank cultivation of the red alga Palmaria palmata: year-round induction of tetrasporangia, tetraspore release in darkness and mass cultivation of vegetative thalli. Aquaculture 252:20–30CrossRefGoogle Scholar
  70. Pang S, Gomez I, Lüning K (2001) The red macroalga Delesseria sanguinea as a UVB-sensitive model organism: selective growth reduction by UVB in outdoor experiments and rapid recording of growth rate during and after UV pulses. Eur J Phycol 36:207–216CrossRefGoogle Scholar
  71. Papazi A, Makridis P, Divanach P, Kotzabasis K (2008) Bioenergetic changes in the microalgal photosynthetic apparatus by extremely high CO2 concentrations induce an intense biomass production. Physiol Plant 132:338–349CrossRefPubMedGoogle Scholar
  72. Poeschl M, Ward S, Owende P (2010) Prospects for expanded utilization of biogas in Germany. Renew Sust Energ Rev 14:1782–1797CrossRefGoogle Scholar
  73. Poorter H (1993) Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104/105:77–97CrossRefGoogle Scholar
  74. Rathmann R, Szklo A, Schaeffer R (2010) Land use competition for production of food and liquid biofuels: an analysis of the arguments in the current debate. Renew Energy 35:14–22CrossRefGoogle Scholar
  75. Roleda MY, Hanelt D, Wiencke C (2006) Exposure to ultraviolet radiation delays photosynthetic recovery in Arctic kelp zoospores. Photosynth Res 88:311–322CrossRefPubMedGoogle Scholar
  76. 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). Glob Chang Biol 18:854–864CrossRefGoogle Scholar
  77. Sagert S, Schubert H (2000) Acclimation of Palmaria palmata (Rhodophyta) to light intensity: comparison between artificial and natural light fields. J Phycol 36:1119–1128CrossRefGoogle Scholar
  78. Sarker M, Bartsch I, Olischläger M, Gutow L, Wiencke C (2012) Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot Mar 56:63–74Google Scholar
  79. Sastre R, Posten C (2010) The variety of microalgae applications as a renewable resource. Chem Ing Tech 82:1925–1939Google Scholar
  80. Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1:20–43CrossRefGoogle Scholar
  81. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulated fluorometer. Photosynth Res 10:51–62CrossRefPubMedGoogle Scholar
  82. Shi D, Xu Y, Morel FMM (2009) Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeosciences 6:1199–1207CrossRefGoogle Scholar
  83. Suárez-Àlvarez S, Gómez-Pinchetti JL, García-Reina G (2011) Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales Rhodophyta). J Appl Phycol 24:815–823CrossRefGoogle Scholar
  84. Takahashi T, Williams RT, Bos DL (1982) Carbonate Chemistry. In: Broecker WS, Spence DW, Craig H (eds) GEOSECS Pacific Expedition Hydrographic Data, Vol. 3, pp 77–82Google Scholar
  85. Titlyanov EA, Titlyanova TV (2010) Seaweed cultivation: methods and problems. Russ J Mar Biol 36:227–242CrossRefGoogle Scholar
  86. Wiley PE, Campbell JE, McKuin B (2011) Production of biodiesel and biogas from algae: a review of process train options. Water Environ Res 83:326–338CrossRefPubMedGoogle Scholar
  87. Wu HY, Zou DH, Gao KS (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro- and macroalgae. Sci China Ser C 51:1144–1150.Google Scholar
  88. Xu Z, Zou D, Gao K (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–129CrossRefGoogle Scholar
  89. Zamalloa C, Vulsteke E, Albrecht J, Verstraete W (2011) The techno-economic potential of renewable energy through the anaerobic digestion of microalgae. Bioresour Technol 102:1149–1158CrossRefPubMedGoogle Scholar
  90. Zou D, Gao K (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517CrossRefGoogle Scholar
  91. Zou D, Gao K (2014) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53:86–94CrossRefGoogle Scholar
  92. Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Stefan Sebök
    • 1
    Email author
  • Werner B. Herppich
    • 2
  • Dieter Hanelt
    • 1
  1. 1.Department of Cell Biology and PhycologyUniversity of HamburgHamburgGermany
  2. 2.Leibniz Institute for Agricultural Engineering Potsdam-Bornim e.VPotsdamGermany

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