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Early reproductive stages in the crustose coralline alga Phymatolithon lenormandii are strongly affected by mild ocean acidification

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Abstract

Coralline algae (Corallinales, Rhodophyta) are predicted to be negatively impacted by near-future ocean acidification. The effect of low pH/high pCO2 on early life stages of Phymatolithon lenormandii (Areschoug) Adey was studied in a perturbation experiment. Several parameters including mortality, calcification (calcein staining) and development (growth and abnormalities) have been monitored for a month under experimental conditions ranging from pHT = 8.00 (pCO2 = 398 μatm) and pHT = 7.55 (pCO2 = 1,261 μatm). Our results demonstrate that survival and development of P. lenormandii early life stages can be impacted by small pH changes (ΔpH < −0.1 pH unit). A negative impact of decreasing pH was observed including an increased mortality and a higher rate of abnormalities. Growth and calcification were still observed at the lowest pH (ΔpH = −0.45). Growth rate was similar at all tested pH, but the maintenance of the skeleton under low pH was only possible through a persistent dynamic dissolution/calcification process, an energetically costly mechanism potentially draining resources from other vital processes.

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References

  • Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol 2011: 1–14 Article ID 473615, doi:10.1155/2011/473615

  • Andersson AJ, Mackenzie FT, Bates NR (2008) Life in the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser 373:265–273

    Article  CAS  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci 45:17442–17446

    Article  Google Scholar 

  • Ballesteros E, Torras X, Pinedo S, García M, Mangialajo L, de Torres M (2007) A new methodology based on littoral community cartography for the implementation of the European water framework directive. Mar Pollut Bull 55:172–180

    Article  CAS  Google Scholar 

  • Basso D (2012) Carbonate production by calcareous red algae and global change. Geodiversitas 34(1):13–33

    Article  Google Scholar 

  • Bilan MI, Usov AI (2001) Polysaccharides of calcareous algae and their effect on the calcification process. Russ J Bioorg Chem 27:2–16

    Article  CAS  Google Scholar 

  • Borowitzka MA (1977) Algal calcification. Oceanogr Mar Biol Ann Rev 15:189–223

    CAS  Google Scholar 

  • Borowitzka MA (1982) Mechanisms of algal calcification. Prog Phycol Res 1:137–177

    CAS  Google Scholar 

  • Bressan G, Ghirardelli L (1993) General features and calcification in the Corallinales: a survey. Giornale Botanico Italiano 27:474–483

    Article  Google Scholar 

  • Büdenbender J, Riebesell U, Form A (2011) Calcification of the Arctic coralline red algae Lithothamnion glaciale in response to elevated CO2. Mar Ecol Prog Ser 441:79–87. doi:10.3354/meps09405

    Article  Google Scholar 

  • Cumani F (2011) Fisiologia della calcificazione nelle Corallinaceae (Rhodophyta): effetti dell’ocean acidification su Lithophyllum incrustans Philippi, PhD dissertation, University of Trieste. http://hdl.handle.net/10077/4581

  • Cumani F, Di Pascoli A, Bressan G (2008) Phenotypic observations of bioindicators in laboratory culture: Pneophyllum fragile Kützing and Hydrolithon boreale (Foslie) Chamberlain (Corallinales, Rhodophyta). Biol Mar Mediterr 15(1):260–261

    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 

  • Dickson AG (2010) The carbon dioxide system in seawater: equilibrium chemistry and measurements. In: Riebesell U, Fabry V, Hansson L, Gattuso JP (eds) Guide for best practices in ocean acidification research and data reporting. Office for Official Publications of the European Communities, Luxembourg, pp 17–40

    Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Oceanogr Res Pap 34:1733–1743

    Article  CAS  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(8):2388–2398

    Article  Google Scholar 

  • Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993) 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 

  • Giraud G, Cabioch J (1979) Ultrastructural and elaboration of calcified cell-wall in the Coralline algae (Rhodophyta, Cryptonemiales). Biol Cell 36:81–86

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Harvey A, Woelkerling W, Farr T, Neill K, Nelson W (2005) Coralline algae of central New Zealand. An identification guide for common “crustose” species. NIWA Information Series N. 57, Wellington

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

    Article  CAS  Google Scholar 

  • Irvine LM, Chamberlain YM (1994) Seaweeds of the British Isles: I, Rhodophyta, 2B, Corallinales, Hildenbrandiales. Ed. Nat. Hist. Mus. London

  • Johansen HW (1981) Coralline algae. A first synthesis. CRC Press, Boca Raton

    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 

  • Kleypas JA, Buddemeier RW, Archer D, Gattuso JP, Langdon C, Bradley NO (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  CAS  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434. doi:10.1111/j.1461-0248.2010.01518.x

    Article  Google Scholar 

  • Kroeker KJ, Micheli F, Gambi MC (2012) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Chang: 1–4, doi: 10.1038/NCLIMATE1680

  • 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, Broecker WS, Hammond DE, Glenn E, Fitzsimmons K, Nelson SG, Peng TH, Hajdas I, Bonani G (2003) Effect of elevated CO2 on the community metabolism of an experimental coral reef. Global Biogeochem Cycle 17(1):1011–1025. doi:10.1029/2002GB001941

    Article  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, Tennessee

  • Lüning K, Dring MJ (1979) Continuous underwater light measurement near Helgoland (North Sea) and its significance for characteristic light limits in the sublitoral region. Helgoländer Meeresun 32:403–424

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Martin S, Castets MD, Clavier J (2006) Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquat Bot 85:121–128

    Article  CAS  Google Scholar 

  • Martin S, Clavier J, Chauvaud L, Thouzeau G (2007) Community metabolism in temperate maerl beds. I. Carbon and carbonate fluxes. Mar Ecol Prog Ser 335:19–29

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400(1–2):278–287

    Article  CAS  Google Scholar 

  • Price NN, Martz TR, Brainard RE, Smith JE (2012) Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS One 7(8): 1–9. e43843, doi:10.1371/journal.pone.0043843

  • Ragazzola F, Foster LC, Form A, Anderson PSL, Hansteen TH, Fietzke J (2012) Ocean acidification weakens the structural integrity of coralline algae. Glob Chang Biol 18:2804–2812. doi:10.111/J.1365-2846.2012.02756.x

    Article  Google Scholar 

  • Riebesell U, Fabry V, Hansson L, Gattuso JP (eds) (2010) Guide for best practices in ocean acidification research and data reporting. Office for Official Publications of the European Communities, Luxembourg

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sarazin G, Michard G, Prevot F (1999) A rapid and accurate spectroscopic method for alkalinity measurement in sea water samples. Water Res 33(1):290–294

    Article  CAS  Google Scholar 

  • Semesi IS, Kangwe J, Bjork M (2009) Alterations in seawater pH and CO2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta). Estuar Coast Shelf Sci 84(3):337–341

    Article  CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Smith AD, Roth AA (1979) Effect of carbon dioxide concentration on calcification in the red coralline alga Bossiella orbigniana. Mar Biol 52:217–225

    Article  CAS  Google Scholar 

  • Smith AM, Sutherland JE, Kregting L, Farr TJ, Winter DJ (2012) Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny. Phytochemistry 81:97–108

    Article  CAS  Google Scholar 

  • Steneck RS (1986) The ecology of coralline algal crusts: convergent patterns and adaptative strategies. Ann Rev Ecol Syst 17:273–303

    Article  Google Scholar 

  • Suneson S. (1943) The structure, life history and taxonomy of the Swedish Corallinaceae. Lunds Universitets Ärsskrift N.F. Avd 2 Bd. 39 Nr. 9

  • Walker R, Moss B (1984) Mode of attachment of six epilithic crustose Corallinaceae (Rhodophyta). Phycologia 23:321–329

    Article  Google Scholar 

  • Woelkerling WJ (1988) The coralline red algae: an analysis of the genera and subfamilies of nongeniculate Corallinaceae. Oxford University Press: 1–268

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Acknowledgments

The authors are very grateful to Prof. Mike Thorndyke and the two reviewers for excellent comments and suggestions on a previous version of this manuscript. This work was supported by an ASSEMBLE grant to FB. SD is funded by the Linnaeus Centre for Marine Evolutionary Biology at the University of Gothenburg (http://www.cemeb.science.gu.se/) and supported by a Linnaeus grant from the Swedish Research Councils VR and Formas.

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Correspondence to F. Bradassi or S. Dupont.

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Communicated by H.-O. Pörtner.

Fulvia Bradassi and Sam Dupont contributed equally to this manuscript.

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Bradassi, F., Cumani, F., Bressan, G. et al. Early reproductive stages in the crustose coralline alga Phymatolithon lenormandii are strongly affected by mild ocean acidification. Mar Biol 160, 2261–2269 (2013). https://doi.org/10.1007/s00227-013-2260-2

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