Skip to main content

Advertisement

SpringerLink
Log in

Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The effects of elevated CO2 and temperature on photosynthesis and calcification of two important calcifying reef algae (Halimeda macroloba and Halimeda cylindracea) were investigated with O2 microsensors and chlorophyll a fluorometry through a combination of two pCO2 (400 and 1,200 μatm) and two temperature treatments (28 and 32 °C) equivalent to the present and predicted conditions during the 2100 austral summer. Combined exposure to pCO2 and elevated temperature impaired calcification and photosynthesis in the two Halimeda species due to changes in the microenvironment around the algal segments and a reduction in physiological performance. There were no significant changes in controls over the 5-week experiment, but there was a 50–70 % decrease in photochemical efficiency (maximum quantum yield), a 70–80 % decrease in O2 production and a threefold reduction in calcification rate in the elevated CO2 and high temperature treatment. Calcification in these species is closely coupled with photosynthesis, such that a decrease in photosynthetic efficiency leads to a decrease in calcification. Although pH seems to be the main factor affecting Halimeda species, heat stress also has an impact on their photosystem II photochemical efficiency. There was a strong combined effect of elevated CO2 and temperature in both species, where exposure to elevated CO2 or temperature alone decreased photosynthesis and calcification, but exposure to both elevated CO2 and temperature caused a greater decline in photosynthesis and calcification than in each stress individually. Our study shows that ocean acidification and ocean warming are drivers of calcification and photosynthesis inhibition in Halimeda. Predicted climate change scenarios for 2100 would therefore severely affect the fitness of Halimeda, which can result in a strongly reduced production of carbonate sediments on coral reefs under such changed climate conditions.

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
Fig. 4
Fig. 5
Fig. 6

References

  • Al-Horani FA (2005) Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral Galaxea fascicularis, measured with O2, Ca2+ and pH microsensors. Sci Mar 69:347–354

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  PubMed  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 USA 105:17442–17446

    Article  PubMed  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Physiol 59:89–113

    CAS  Google Scholar 

  • Blaxter JHS, Russel FS, Young M (eds) (1980) Ecology and taxonomy of Halimeda: primary producer of coral reefs. Academic Press, New York

    Google Scholar 

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

    CAS  Google Scholar 

  • Borowitzka MA (1986) Physiology and biochemistry of calcification in the Chlorophyceae. In: Leadbeater B, Riding H (eds) Biomineralization in the lower plants and animals. Oxford University Press, Oxford, pp 107–124

    Google Scholar 

  • Borowitzka MA (1989) Carbonate calcification in algae—initiation and control. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: Chemical and biochemical perspectives. VCH, Weinheim, pp 63–94

    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 (1977) Calcification in the green alga Halimeda. I. An ultrastructure study on thallus development. J Phycol 13:6–16

    Google Scholar 

  • Borowitzka MA, Larkum AWD, Nockolds CE (1974) A scanning electron microscope study of the structure and organization of the calcium carbonate deposits of algae. Phycologia 13:195–203

    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 

  • Diaz-Pulido G, McCook LJ, Larkum AWD, Lotze HK, Raven JA, Schaffelke B, Smith JE, Steneck RS (2007) Vulnerability of macroalgae of the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds) Climate change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia, pp 153–192

    Google Scholar 

  • Drew EA (1983) Halimeda biomass, growth rates and sediment generation on reefs in the Central Great Barrier Reef Province. Coral Reefs 2:101–110

    Article  Google Scholar 

  • Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366

    Article  PubMed  CAS  Google Scholar 

  • Fujita K, Hikami M, Suzuki A, Kuroyanagi A, Sakai K, Kawahata H, Nojiri Y (2011) Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers. Biogeosciences 8:2089–2098

    Article  Google Scholar 

  • 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 5:563–571

    Article  CAS  Google Scholar 

  • Gattuso J-P, Lavigne H (2009) Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121–2133

    Article  CAS  Google Scholar 

  • Glud RN, Gundersen JK, Revsbech NP, Jørgensen BB (1995) Effects on the benthic diffusive boundary layer imposed by microelectrodes. Limnol Oceanogr 39:462–467

    Article  Google Scholar 

  • Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hill R, Larkum AWD, Frankart C, Kühl M, Ralph PJ (2004) Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynth Res 82:59–72

    Article  PubMed  CAS  Google Scholar 

  • Hofmann LC, Yildiz G, Hanelt D, Bischof K (2012) Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol 159:783–792

    Article  CAS  Google Scholar 

  • Houghton J (2009) Global warming: the complete briefing. Cambridge University Press, United Kingdom

    Book  Google Scholar 

  • Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Biol Sci Ser B 271:1757–1763

    Article  CAS  Google Scholar 

  • Jokiel PL, Maracios JE, Franzisket L (eds) (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: Research methods, UNESCO, pp 529–541

  • 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, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 22:108–117

    Article  Google Scholar 

  • Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  PubMed  CAS  Google Scholar 

  • Köhler-Rink S, Kühl M (2000) Microsensor studies of photosynthesis and respiration in larger symbiotic foraminifera. I The physio-chemical microenvironment of Marginopora vertebralis, Amphistegina lobifera and Amphisorus hemprichii. Mar Biol 137:473–486

    Article  Google Scholar 

  • Köhler-Rink S, Kühl M (2005) The chemical microenvironment of the symbiotic planktonic foraminifer Orbulina universa. Mar Biol Res 1:68–78

    Article  Google Scholar 

  • Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2007) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117

    Article  Google Scholar 

  • Kuguru B, Achituv Y, Gruber DF, Tchernov D (2010) Photoacclimation mechanisms of corallimorpharians on coral reefs: photosynthetic parameters of zooxanthellae and host cellular responses to variation in irradiance. J Exp Mar Biol Ecol 394:53–62

    Article  Google Scholar 

  • Langdon C, Gattuso J-P, Anderson A (2010) Measurements of calcification and dissolution of benthic organisms and communities. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting. Publication Office of the European Union, Luxembourg, pp 213–232

    Google Scholar 

  • Larkum AWD, Salih A, Kühl M (2011) Rapid mass movement of chloroplasts during segment formation of the calcifying siphonalean green alga Halimeda macroloba. PLoS One 6. doi:10.1371/journal.pone.0020841

  • Lewis E, Wallace DWR (1998) CO2SYS—Program developed for the CO2 system calculations. Carbon Dioxide Information Analysis Center; Report ORNL/CDIAC-105, Oakridge National Laboratory, Oakridge, TN

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • McConnaughey T (1989) Biomineralization mechanisms. In: Crick RE (ed) Origin, evolution, and modern aspects of biomineralization in plants and animals. Plenum Press, New York, pp 57–73

    Google Scholar 

  • McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev 42:95–117

    Article  CAS  Google Scholar 

  • Palacios SL, Zimmerman RC (2007) Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar Ecol Prog Ser 344:1–13

    Article  Google Scholar 

  • Revsbech NP, Jorgensen BB, Brix O (1981) Primary production of microalgae in sediments measured by oxygen microprofile, H14CO3 − fixation, and oxygen exchange methods. Limnol Oceanogr 26:717–730

    Article  CAS  Google Scholar 

  • Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064

    Article  CAS  Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126

    Article  CAS  Google Scholar 

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Springer, Dordrecht, pp 279–319

    Google Scholar 

  • Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196

    Article  Google Scholar 

  • Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56:1200–1212

    Article  CAS  Google Scholar 

  • Smith SV, Kinsey DW (1976) Calcium carbonate production, coral reef growth, and sea level change. Science 194:937–939

    Article  PubMed  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schimidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012

    Article  PubMed  CAS  Google Scholar 

  • Weyl PK (1959) The change in solubility of calcium carbonate with temperature and carbon dioxide content. Geochim Cosmochim Acta 17:214–225

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Louise Evans and Linda Xiao and the School of Chemistry and Forensic Science, University of Technology, Sydney, for assistance with the autotitrator. Anthony Larkum, Daniel Nielsen, Daniel Wangpraseurt and Ponlachart Chotikarn are thanked for their assistance with microsensor experimental set-ups. This project was supported by the Plant Functional Biology and Climate Change Cluster, School of the Environment, University of Technology, Sydney, an Australian Coral Reef Society student research award (SS), and the Phycological Society of America Grant-in-Aid of Research award (SS). Additional support was due to the Danish Natural Science Research Council (MK). The research was performed under Great Barrier Reef Marine Park Authority permit G09/30853.1.

Author information

Author notes

  1. R. Hill

    Present address: Centre for Marine Bio-Innovation and Sydney Institute of Marine Science, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW, 2052, Australia

Authors and Affiliations

  1. Plant Functional Biology and Climate Change Cluster, School of the Environment, University of Technology Sydney, PO Box 123, Broadway, Sydney, NSW, 2007, Australia

    S. Sinutok, R. Hill, M. A. Doblin, M. Kühl & P. J. Ralph

  2. Marine Biology Section, Department of Biology, University of Copenhagen, Strandpromenaden 5, 3000, Helsingør, Denmark

    M. Kühl

  3. Singapore Centre on Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Nanyang Avenue, Singapore

    M. Kühl

Authors
  1. S. Sinutok
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. A. Doblin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Kühl
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. J. Ralph
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Hill.

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sinutok, S., Hill, R., Doblin, M.A. et al. Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming. Coral Reefs 31, 1201–1213 (2012). https://doi.org/10.1007/s00338-012-0952-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-012-0952-6

Keywords

Search

Navigation