Skip to main content

Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta

Abstract

Ocean acidification affects with special intensity Arctic ecosystems, being marine photosynthetic organisms a primary target, although the consequences of this process in the carbon fluxes of Arctic algae are still unknown. The alteration of the cellular carbon balance due to physiological acclimation to an increased CO2 concentration (1300 ppm) in the common Arctic brown seaweeds Desmarestia aculeata and Alaria esculenta from Kongsfjorden (Svalbard) was analysed. Growth rate of D. aculeata was negatively affected by CO2 enrichment, while A. esculenta was positively affected, as a result of a different reorganization of the cellular carbon budget in both species. Desmarestia aculeata showed increased respiration, enhanced accumulation of storage biomolecules and elevated release of dissolved organic carbon, whereas A. esculenta showed decreased respiration and lower accumulation of storage biomolecules. Gross photosynthesis (measured both as O2 evolution and 14C fixation) was not affected in any of them, suggesting that photosynthesis was already saturated at normal CO2 conditions and did not participate in the acclimation response. However, electron transport rate changed in both species in opposite directions, indicating different energy requirements between treatments and species specificity. High CO2 levels also affected the N-metabolism, and 13C isotopic discrimination values from algal tissue pointed to a deactivation of carbon concentrating mechanisms. Since increased CO2 has the potential to modify physiological mechanisms in different ways in the species studied, it is expected that this may lead to changes in the Arctic seaweed community, which may propagate to the rest of the food web.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Amthor JS (1991) Respiration in a future, higher CO2 world. Plant Cell Environ 14:13–20

    CAS  Article  Google Scholar 

  2. Andría JR, Brun FG, Pérez-Lloréns JL, Vergara JJ (2001) Acclimation responses of Gracilaria sp. (Rhodophyta) and Enteromorpha intestinalis (Chlorophyta) to changes in the external inorganic carbon concentration. Bot Mar 44:361–370

    Article  Google Scholar 

  3. Axelsson L, Mercado J, Figueroa F (2000) Utilization of HCO3 at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59

    Article  Google Scholar 

  4. Azcón-Bieto J, González-Meler M, Dougherty W, Drake B (1994) Acclimation of respiratory O2 uptake in green tissues of field-grown native species after long-term exposure to elevated atmospheric CO2. Plant Physiol 106:1163–1168

    Article  PubMed  PubMed Central  Google Scholar 

  5. Beer S, Larsson C, Poryan O, Axelsson L (2000) Photosynthetic rates of Ulva (Chlorophyta) measured by pulse amplitude modulated (PAM) fluorescence. Eur J Phycol 35:69–74

    Article  Google Scholar 

  6. Bischoff B, Wiencke C (1993) Temperature requirements for growth and survival of macroalgae from Disko Island (Greenland). Helgoländer Meeresunters 47:167–191

    Article  Google Scholar 

  7. Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall, Inc., Englewood Cliffs

    Google Scholar 

  8. Borchard C, Engel A (2012) Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeosciences 9:3405–3423

    CAS  Article  Google Scholar 

  9. Brown DL, Tregunna EB (1967) Inhibition of respiration during photosynthesis by some algae. Can J Bot 45:1135–1143

    Article  Google Scholar 

  10. Bunce J, Caulfield F (1991) Reduced respiratory carbon dioxide efflux during growth at elevated carbon dioxide in three herbaceous perennial species. Ann Bot 67:325–330

    CAS  Google Scholar 

  11. Burkhardt S, Amoroso G, Riebesell U, Sültemeyer D (2001) CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46:1378–1391

    CAS  Article  Google Scholar 

  12. Chapman ARO, Lindley JE (1980) Seasonal growth of Laminaria solidungula in the high Arctic in relation to irradiance and dissolved nutrient concentration. Mar Biol 57:1–5

    CAS  Article  Google Scholar 

  13. Chen SW, Beardall J, Gao KS (2014) A red tide alga grown under ocean acidification up-regulates its tolerance to lower pH by increasing its photophysiological functions. Biogeosci Discuss 11:6303–6328

    Article  Google Scholar 

  14. 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

    CAS  Article  PubMed  Google Scholar 

  15. Davey PA, Hunt S, Hymus GJ, DeLucia EH, Drake BG, Karnosky DF, Long SP (2004) Respiratory oxygen uptake is not decreased by an instantaneous elevation of [CO2], but is increased with long-term growth in the field at elevated [CO2]. Plant Physiol 134:520–527

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192

    Article  PubMed  Google Scholar 

  17. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215

    Article  Google Scholar 

  18. Feikema WO, Marosvölgyi MA, Lavaud J, van Gorkom HJ (2006) Cyclic electron transfer in photosystem II in the marine diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1757:829–834

    CAS  Article  Google Scholar 

  19. Fogg GE (1983) The ecological significance of extracelular products of phytoplankton. Bot Mar 26:3–14

    CAS  Article  Google Scholar 

  20. García-Sánchez MJ, Fernández JA, Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194:55–61

    Article  Google Scholar 

  21. Genty B, Briantais J, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Article  Google Scholar 

  22. Giordano M, Davis S, Bowes G (1994) Organic carbon release by Dunaliella salina (Chlorophyta) under different growth conditions of CO2, nitrogen and salinity. J Phycol 30:249–257

    CAS  Article  Google Scholar 

  23. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Ann Rev Plant Biol 56:99–131

    CAS  Article  Google Scholar 

  24. Gordillo FJL, Jiménez C, Figueroa FL, Niell FX (1999) Effects of increased atmospheric CO2 and N supply on photosynthesis, growth and cell composition of the cyanobacterium Spirulina platensis (Arthrospira). J Appl Phycol 10:461–469

    Article  Google Scholar 

  25. 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 213:64–70

    CAS  Article  PubMed  Google Scholar 

  26. Gordillo FJL, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322

    CAS  Article  PubMed  Google Scholar 

  27. Gordillo FJL, Aguilera J, Jimenez C (2006) The response of nutrient assimilation and biochemical composition of Arctic seaweeds to a nutrient input in summer. J Exp Bot 57:2661–2671

    CAS  Article  PubMed  Google Scholar 

  28. Gran G (1952) Determination of the equivalence point in potentiometric titrations. Part II. Analyst 77:661–671

    CAS  Article  Google Scholar 

  29. Gutow L, Rahman MM, Bartl K, Saborowski R, Bartsch I, Wiencke C (2014) Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90

    CAS  Article  Google Scholar 

  30. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents reveal ecosystem effects of ocean acidification. Nature 454:96–99

    CAS  Article  PubMed  Google Scholar 

  31. Henley WJ, Dunton KH (1997) Effects of nitrogen supply and continuous darkness on growth and photosynthesis of the Arctic kelp Laminaria solidungula. Limnol Oceanogr 42:209–216

    CAS  Article  Google Scholar 

  32. Hennon GMM, Quay P, Morales RL, Swanson LM, Armbrust EV (2014) Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J Phycol 50:243–253

    CAS  Article  PubMed  Google Scholar 

  33. Hop H, Pearson T, Hegseth EN, Kovacs KM, Wiencke C, Kwasniewski S, Eiane K, Mehlum F, Gulliksen B, Wlodarska-Kowalczuk M, Lydersen C, Weslawski JM, Cochrane S, Gabrielsen GW, Leakey RJG, Lønne OJ, Zajaczkowski M, Falk-Petersen S, Kendall M, Wängberg S-A, Bischof K, Voronkov AY, Kovaltchouk NA, Wiktor J, Poltermann M, di Prisco G, Papucci C, Gerland S (2002) The marine ecosystem of Kongsfjorden, Svalbard. Polar Res 21:167–208

    Article  Google Scholar 

  34. Hop H, Wiencke C, Vögele B, Kovaltchouk NA (2012) Species composition, zonation and biomass of marine benthic macroalgae in Kongsfjorden, Svalbard. Bot Mar 55:399–414

    Article  Google Scholar 

  35. Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnol Oceanogr 55:2011–2024

    CAS  Article  Google Scholar 

  36. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: recommendations for experimental designs. J Phycol 45:1236–1251

    CAS  Article  PubMed  Google Scholar 

  37. IPCC (2013) The intergovernmental panel on climate change. Climate change 2013: the physical science basis. summary for policymakers. Cambridge University Press, Cambridge, pp 24–25

  38. Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Change Biol 8:831–840

    Article  Google Scholar 

  39. Israel A, Katz S, Dubinsky Z, Merrill JE, Friedlander M (1999) Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta). J Appl Phycol 11:447–453

    Article  Google Scholar 

  40. Korb RE, Gerard VA (2000) Effects of concurrent low temperature and low nitrogen supply on polar and temperate waters. Mar Ecol Prog Ser 198:73–82

    Article  Google Scholar 

  41. Kremer BP, Küppers U (1977) Carboxylating enzymes and pathway of photosynthetic carbon assimilation in different marine algae–evidence for the C4 pathway? Planta 133:191–196

    CAS  Article  PubMed  Google Scholar 

  42. Kristensen E, Andersen F (1987) Determination of organic carbon in marine sediments: a comparison of two CHN-analyzer methods. J Exp Mar Bio Ecol 109:15–23

    CAS  Article  Google Scholar 

  43. Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310

    Article  Google Scholar 

  44. Lüning K (1985) Meeresbotanik. Verbreitung, Ökophysiologie und Nutzung der marinen Makroalgen. Thieme Verlag Stuttgart, pp 375

  45. Lüning K (1991) Circannual growth rhythm in a brown alga, Pterygophora californica. Bot Acta 104:157–162

    Article  Google Scholar 

  46. Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492

    Article  Google Scholar 

  47. Mague TH, Friberg E, Hughes DJ, Morris I (1980) Extracellular release of carbon by marine phytoplankton: a physiological approach. Limnol Oceanogr 25:262–279

    CAS  Article  Google Scholar 

  48. Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom Phaeodactylum tricornutum. Plant Cell Environ 24:611–620

    CAS  Article  Google Scholar 

  49. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    CAS  Article  Google Scholar 

  50. Mercado JM, Gordillo FJL, 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 11:455–461

    Article  Google Scholar 

  51. Mercado JM, de los Santos CB, Pérez-Lloréns JL, Vergara JJ (2009) Carbon isotopic fractionation in macroalgae from Cádiz Bay (Southern Spain): comparison with other bio-geographic regions. Estuar Coast Shelf Sci 85:449–458

    CAS  Article  Google Scholar 

  52. Moulin P, Andria 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 95:31–38

    CAS  Article  Google Scholar 

  53. O’Leary MH, Madhavan S, Paneth P (1992) Physical and chemical basis of carbon isotope fractionation in plants. Plant Cell Environ 15:1099–1104

    Article  Google Scholar 

  54. Olabarria C, Arenas F, Viejo RM, Gestoso I, Vaz-Pinto F, Incera M, Rubal M, Cacabelos E, Veiga P, Sobrino C (2012) Response of macroalgal assemblages from rockpools to climate change: effects of persistent increase in temperature and CO2. Oikos 122:1065–1079

    Article  Google Scholar 

  55. 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 64:5587–5597

    Article  PubMed  Google Scholar 

  56. Ormerod JG (1983) The carbon cycle in aquatic ecosystems. In: Slater JH, Whittenbury R, Wimpenny JWT (eds) Microbes in their natural environments. Cambridge University Press, Cambridge, pp 463–482

    Google Scholar 

  57. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and Collections of Algae. Proceedings of the U.S.-Japan Conference, Hakone 1966. Japanese Society for Plant Physiology, Tokyo, pp 63–75

    Google Scholar 

  58. Raven JA, Beardall J (2003) Carbon acquisition mechanisms of algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum AW, Douglas SE, Raven JA (eds) Photosynthesis in algae. Advances in photosynthesis and respiration. Vol. Kluwer Academic Publishers, The Netherlands, pp 225–244

    Google Scholar 

  59. Raven JA, Johnston AM, Kübler JE, Korb R, Mcinroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:335–378

    Article  Google Scholar 

  60. Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zöllner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–549

    CAS  Article  PubMed  Google Scholar 

  61. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc—a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone), U.S. Geological Survey Open-File Report 2010–1280, p 17

  62. Roleda MY, Hurd CL (2012) Seaweed responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed biology, ecological studies 219. Springer, Berlin, pp 407–431

    Google Scholar 

  63. 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

    Article  Google Scholar 

  64. Satoh A, Kurano N, Senger H, Miyachi S (2002) Regulation of energy balance in photosystems in response to changes in CO2 concentrations and light intensities during growth in extremely high-CO2-tolerant green microalgae. J Plant Cell Physiol 43:440–451

    CAS  Article  Google Scholar 

  65. Schaffelke B, Lüning K (1994) A circannual rhythm controls seasonal growth in the kelps Laminaria hyperborea and Laminaria digitata from Helgoland (North Sea). Eur J Phycol 29:49–56

    Article  Google Scholar 

  66. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    CAS  Article  PubMed  Google Scholar 

  67. Sharp JH (1977) Excretion of organic matter by marine phytoplankton: do healthy cells do it? Limnol Oceanogr 22:381–399

    CAS  Article  Google Scholar 

  68. Sobrino C, Segovia M, Neale P, Mercado JM, García-Gómez C, Kulk G, Lorenzo MR, Camarena T, Van de Poll W, Spilling K (2014) Interactive effects of solar radiation, CO2 and nutrient enrichment on cell viability and organic carbon excretion of coastal phytoplankton. Aquat Biol. doi:10.3354/ab00590

    Google Scholar 

  69. Steeman-Nielsen E (1952) The use of radioactive carbon (14C) for measuring organic production in the sea. J Cons Int Explor Mer 18:117–140

    Article  Google Scholar 

  70. Steinacher M, Joos F, Frölicher TL, Plattner G-K, Doney SC (2009) Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6:515–533

    CAS  Article  Google Scholar 

  71. Suárez-Álvarez S, Gómez-Pinchetti JL, García-Reina G (2012) Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). J Appl Phycol 24:815–823

    Article  Google Scholar 

  72. Swanson AK, Fox CH (2007) Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs. Glob Change Biol 13:1696–1709

    Article  Google Scholar 

  73. Wassmann P, Duarte CM, Agustí S, Sejr MK (2011) Footprints of climate change in the Arctic marine ecosystem. Glob Change Biol 17:1235–1249

    Article  Google Scholar 

  74. Weiss RF (1974) Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Mar Chem 2:203–215

    CAS  Article  Google Scholar 

  75. Wiencke C, Vögele B, Kovaltchouk NA, Hop H (2004) Species composition and zonation of marine benthic macroalgae at Hansneset in Kongsfjorden, Svalbard. Ber Polarforsch Meeresforsch 492:55–62

    Google Scholar 

  76. Wiencke C, Clayton MN, Gómez I, Iken K, Lüder UH, Amsler CD, Karsten U, Hanelt D, Bischof K, Dunton K (2007) Life strategy, ecophysiology and ecology of seaweeds in polar waters. Rev Environ Sci Biotechnol 6:95–126

    Article  Google Scholar 

  77. Wiencke C, Gómez I, Dunton K (2011) Phenology and seasonal physiological performance in polar seaweeds. In: Wiencke C (ed) Biology of polar benthic algae. de Gruyter, Berlin, pp 181–194

    Google Scholar 

  78. Wood AM, Van Valen LM (1990) Paradox lost? On the release of energy-rich compounds by phytoplankton. Mar Microb Food Webs 4:103–116

    Google Scholar 

  79. Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7:2915–2923

    CAS  Article  Google Scholar 

  80. Xu ZG, Zou DH, Gao KS (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–9

  81. Yang G, Gao K (2012) Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity. Mar Environ Res 79:142–151

    Article  PubMed  Google Scholar 

  82. Zou DH (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250:726–735

    CAS  Article  Google Scholar 

  83. Zou D, Gao K (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517

    CAS  Article  Google Scholar 

  84. Zou D, Gao K, Luo H (2011a) 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 47:87–97

    CAS  Article  PubMed  Google Scholar 

  85. Zou D, Gao K, Xia J (2011b) Dark respiration in the light and in darkness of three marine macroalgal species grown under ambient and elevated CO2 concentrations. Acta Oceanol 30:106–112

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was performed at the International Arctic Environmental Research and Monitoring Facility at Ny-Ålesund, Spitsbergen, Norway. It was financed by the project CTM2011-24007/ANT from the Spanish Ministry for Science and Innovation. Concepcion Iñiguez and M. Rosario Lorenzo were supported by a FPU grant from the Spanish Ministry for Education. Finally, we thank the AWI diving team and Elisabeth Helmke (AWI) for assistance with 14C counting.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Concepción Iñiguez.

Additional information

This article belongs to the special issue on the “Kongsfjorden ecosystem—new views after more than a decade of research”, coordinated by Christian Wiencke and Haakon Hop.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Iñiguez, C., Carmona, R., Lorenzo, M.R. et al. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta . Polar Biol 39, 1979–1991 (2016). https://doi.org/10.1007/s00300-015-1724-x

Download citation

Keywords

  • Carbon concentrating mechanisms
  • Growth
  • Macroalgae
  • Ocean acidification
  • Photosynthesis
  • Respiration