Skip to main content

Advertisement

SpringerLink
Log in

Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Future atmospheric CO2 levels will most likely have complex consequences for marine organisms, particulary photosynthetic calcifying organisms. Corallina officinalis L. is an erect calcifying macroalga found in the inter- and subtidal regions of temperate rocky coastlines and provides important substrate and refugia for marine meiofauna. The main goal of the current study was to determine the physiological responses of C. officinalis to increased CO2 concentrations expected to occur within the next century and beyond. Our results show that growth and production of inorganic material decreased under high CO2 levels, while carbonic anhydrase activity was stimulated and negatively correlated to algal inorganic content. Photosynthetic efficiency based on oxygen evolution was also negatively affected by increased CO2. The results of this study indicate that C. officinalis may become less competitive under future CO2 levels, which could result in structural changes in future temperate intertidal communities.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akioka H, Baba M, Masaki T, Johansen HW (1999) Rocky shore turfs dominated by Corallina (Corallinales, Rhodophyta) in northern Japan. Phycol Res 47:199–206

    Google Scholar 

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142(3):419–426

    CAS  Google Scholar 

  • Andrake W, Johansen HW (1980) Alizarin red dye as a marker for measuring growth in Corallina officinalis L. (Corallinaceae, Rhodophyta). J Phycol 16:620–622

    Article  Google Scholar 

  • Axelsson L, Ryberg H, Beer S (1995) Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ 18:439–445

    Article  CAS  Google Scholar 

  • Beer S, Axelsson L (2004) Limitations in the use of PAM fluorometry for measuring photosynthetic rates of macroalgae at high irradiances. Eur J Phycol 39(1):1–7

    Article  Google Scholar 

  • Belliveau SA, Paul VJ (2002) Effects of herbivory and nutrients on the early colonization of crustose coralline and fleshy algae. Mar Ecol Prog Ser 232:105–114

    Article  Google Scholar 

  • Bischof K, Hanelt D, Wiencke C (1999) Acclimation of maximal quantum yield of photosynthesis in the brown alga Alaria esculenta under high light and UV radiation. Plant Biol 1:435–444

    Article  CAS  Google Scholar 

  • Bischof K, Kräbs G, Hanelt D, Wiencke C (2000) Photosynthetic characteristics and mycosporine-like amino acids under UV radiation: a competitive advantage of Mastocarpus stellatus over Chondrus crispus at the Helgoland shoreline? Helgol Mar Res 54:47–52

    Article  Google Scholar 

  • Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166

    Article  CAS  Google Scholar 

  • Borowitzka MA (1981) Photosynthesis and calcification in the articulated coralline red algae Amphiroa anceps and A. foliacea. Mar Biol 62:17–23

    Article  CAS  Google Scholar 

  • Borowitzka MA, Larkum AWD (1976a) Calcification in the green alga Halimeda. II. The exchange of Ca2+ and the occurrence of age gradients in calcification and photosynthesis. J Exp Bot 27:864–878

    Article  CAS  Google Scholar 

  • Borowitzka MA, Larkum AWD (1976b) Calcification in the green alga Halimeda. III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27:879–893

    Article  CAS  Google Scholar 

  • Borowitzka MA, Larkum AWD (1976c) Calcification in the green alga Halimeda. IV. The action of metabolic inhibitors on photosynthesis and calcification. J Exp Bot 27:894–907

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:1–12

    Article  Google Scholar 

  • Colthart BJ, Johansen HW (1973) Growth rates of Corallina officinalis (Rhodophyta) at different temperatures. Mar Biol 18:46–49

    Article  Google Scholar 

  • Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B 277:1409–1415

    Article  Google Scholar 

  • Coull BC, Wells JBJ (1983) Refuges from fish predation: experiments with phytal meiofaunan from the New Zealand rocky intertidal. Ecol 64(6):1599–1609

    Article  Google Scholar 

  • De Beer D, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24:1209–1217

    Article  Google Scholar 

  • Digby PSB (1977) Photosynthesis and respiration in the coralline algae, Clathromorphum circumscriptum and Corallina officinalis and the metabolic basis of calcification. J Mar Biol Assoc 57:1111–1124

    Article  CAS  Google Scholar 

  • Drechsler Z, Sharkia R, Cabantchik ZI, Beer S (1993) Bicarbonate uptake in the marine macroalga Ulva sp. is inhibited by classical probes of anion exchange by red blood cells. Planta 191:34–40

    Article  CAS  Google Scholar 

  • 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 

  • Gao K, Zheng Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Chang Biol 16:2388–2398

    Article  Google Scholar 

  • 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 3:355–362

    CAS  Google Scholar 

  • Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993a) Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar Biol 117:129–132

    Article  CAS  Google Scholar 

  • Gao K, Aruga Y, Asada K, Kiyohara M (1993b) Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5:563–571

    Article  CAS  Google Scholar 

  • 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 

  • Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81:534–539

    Article  Google Scholar 

  • Haglund K, Björk M, Ramazanov Z, García-Reina G, Pedersén M (1992) Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187:275–281

    Article  CAS  Google Scholar 

  • Hanelt D, Nultsch W (1995) Field studies of photoinhibition show non-correlations between oxygen and fluorescence measurements in the arctic red alga Palmaria palmata. J Plant Physiol 145:31–38

    Article  CAS  Google Scholar 

  • Hicks GRF (1986) Meiofauna associated with rocky shore algae. In: Moore PG, Seed R (eds) The ecol of rocky coasts. Columbia University Press, New York, pp 36–56

    Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in n, n-dimethylformamide and 80% acetone. Plant Physiol 77:483–485

    Article  CAS  Google Scholar 

  • 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 Chang Biol 8:831–840

    Article  Google Scholar 

  • 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 

  • Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483

    Article  Google Scholar 

  • Kelaher BP (2002) Influence of physical characteristics of coralline turf on associated macrofaunal assemblages. Mar Ecol Prog Ser 232:141–148

    Article  Google Scholar 

  • Kelaher BP (2003) Changes in habitat complexity negatively affect diverse gastropod assemblages in coralline algal turf. Oecologia 135:431–441

    CAS  Google Scholar 

  • Kingsley RJ, Watabe N (1987) Role of carbonic anhydrase in calcification in the gorgonian Leptogorgia virgulata. J Exp Zool 241(2):171–180

    Article  CAS  Google Scholar 

  • Krief S, Hendy EJ, Fine M, Yam R, Meibom A, Foster GL, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74(17):4988–5001

    Article  CAS  Google Scholar 

  • 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 

  • Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117

    Article  CAS  Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effect of elevated CO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:1–16

    Article  Google Scholar 

  • Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Glob Biogeochem Cycles 14(2):639–654

    Article  CAS  Google Scholar 

  • Langdon C, Broecker WS, Hammond DE, Glenn E, Fitzsimmons K, Nelson SG, Peng T-H, Hajdas I, Bonani G (2003) Effect of elevated CO2 on the community metabolism of an experimental coral reef. Glob Biogeochem Cycles 17(1):1011

    Article  Google Scholar 

  • Larsson C, Axelsson L, Ryberg H, Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur J Phycol 32(1):49–54

    Article  Google Scholar 

  • LaVelle JM (1979) Translocation in Calliarthron tuberculosum and its role in the light-enhancement of calcification. Mar Biol 55:37–44

    Article  CAS  Google Scholar 

  • Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. U.S. Department of Energy, Oak Ridge

    Google Scholar 

  • Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116(1):25–44

    Article  Google Scholar 

  • Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Chang Biol 15:2089–2100

    Google Scholar 

  • Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia M-C, Gattuso J-P, Hall-Spencer J (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4(6):689–692

    Article  Google Scholar 

  • McConnaughey TA, Falk RH (1991) Calcium-proton exchange during algal calcification. Biol Bull 180:185–195

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mercado JM, Figueroa FL, Niell FX (1997) A new method for estimating external carbonic anhydrase activity in macroalgae. J Phycol 33:999–1006

    Article  CAS  Google Scholar 

  • Nelson EB, Cenedella A, Tolbert NE (1969) Carbonic anhydrase levels in Chlamydomonas. Pergamon Press 8:2305–2306

    CAS  Google Scholar 

  • Nimer NA, Guan Q, Merrett MJ (1994) Extra- and intra-cellular carbonic anhydrase in relation to culture algae in a high-calcifying strain of Emiliana huxleyi. New Phytol 126:601–607

    Article  CAS  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437(29):681–686

    Article  CAS  Google Scholar 

  • Pearse VB (1972) Radioisotopic study of calcification in the articulated coralline alga Bossiella orbigniana. J Phycol 8(1):88–97

    Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Cultures and collections of algae. Proceedings of the US-Japan Conference, Hakone, September 1966, 63–75, 1968 Jpn Soc Plant Physiol

  • Pueschal EM, Eichelberger HH, Trick HN (1992) Specialized calciferous cells in the marine alga Rhodogorgon carriebowensis and their implications for models of red algal calcification. Protoplasma 166:89–98

    Article  Google Scholar 

  • Quader H (1985) Tunicamycin prevents cellulose microfibril formation in Oocystis solitaria. Plant Physiol 75:534–538

    Article  Google Scholar 

  • Ragazzola F (2009) Carbon acquisition mechanisms in Corallina elongata Ellis & Solander and Corallina officinalis L. Dissertation. University of Pisa, Pisa

  • Rahman MA, Oomori T, Uehara T (2007) Carbonic anhydrase in calcified endoskeleton: novel activity in biocalcification in Alcyonarian. Mar Biotechnol 10:31–38

    Article  Google Scholar 

  • Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagès C, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668

    Article  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  Google Scholar 

  • Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367

    Article  CAS  Google Scholar 

  • Ries JB, Cohen AL, McKorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geol 37(12):1131–1134

    Article  CAS  Google Scholar 

  • Rost B, Riebesell U, Burkhardt S (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48(1):55–67

    Article  Google Scholar 

  • Russell BD, Thompson J-AI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Chang Biol 15:2153–2162

    Article  Google Scholar 

  • Russell BD, Passarelli CA, Connell SD (2011) CO2 modifies the influence of light in shaping subtidal habitat. J Phycol 47:744–752

    Article  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  Google Scholar 

  • Stewart JG (1982) Anchor species and epiphytes in intertidal algal turf. Pac Sci 36(1):45–59

    Google Scholar 

  • Tambutté S, Tambutté E, Zoccola D, Caminiti N, Lotto S, Moya A, Allemand D, Adkins J (2007) Characterization and role of carbonic anhydrase in the calcification process of the azooxanthellate coral Tubastrea aurea. Mar Biol 151:71–83

    Article  Google Scholar 

  • Thierstein HR, Young JR (2004) Coccolithophores: from molecular processes to global impact. Springer-Verlag, Berlin

    Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Elke Woelken from the University of Hamburg for algal sample preparation and providing excellent transmission electroscopy images used in this study. We also thank the manuscript reviewers for providing very detailed and constructive comments. Funding for this project was provided by the German Federal Ministry of Education and Research (BMBF) through the cooperative research project Biological Impacts of Ocean Acidification (BIOACID).

Author information

Authors and Affiliations

  1. Department of Marine Botany, University of Bremen, Leobener Straße NW2, 28359, Bremen, Germany

    Laurie C. Hofmann & Kai Bischof

  2. Department of Biology, Faculty of Science and Arts, Uludag University, 16059, Bursa, Turkey

    Gamze Yildiz

  3. Department of Cell Biology and Phycology, University of Hamburg, Ohnhorststraße 18, 22609, Hamburg, Germany

    Dieter Hanelt

Authors
  1. Laurie C. Hofmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gamze Yildiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dieter Hanelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Bischof
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laurie C. Hofmann.

Additional information

Communicated by F. Bulleri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hofmann, L.C., Yildiz, G., Hanelt, D. et al. Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol 159, 783–792 (2012). https://doi.org/10.1007/s00227-011-1854-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1854-9

Keywords

Search

Navigation