Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

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Unexpected results from direct measurement, with a torsion microbalance in a closed system, of calcification rates of the coral Agaricia agaricites (Scleractinia:Agariicidae) and concomitant changes in seawater pH
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Keywords

coral calcification
CO2
pH
organic matrix
carbonic anhydrase
Ca(HCO3)2
coral
calcificación
CO2
pH
matriz orgánica
anhidrasa carbónica
Ca (HCO3)2

How to Cite

Sandeman, I. M. (2014). Unexpected results from direct measurement, with a torsion microbalance in a closed system, of calcification rates of the coral Agaricia agaricites (Scleractinia:Agariicidae) and concomitant changes in seawater pH. Revista De Biología Tropical, 62(S3), 25–38. https://doi.org/10.15517/rbt.v62i0.15899

Abstract

Ocean acidification is impacting the calcification of corals, but the mechanisms of calcification are still unclear. To explore the relationship between calcification and pH, small pieces of coral were suspended from a torsion microbalance in gently stirred, temperature controlled, seawater in a closed chamber. Net calcification rate and pH were continuously monitored while light, temperature or pH could be manipulated. The coral pieces were from the edges of thin plates of Agaricia agaricites and were studied alive and freshly collected. Unexpectedly, when calcification was taking place (n=9, 0.082 mg.hr-1.cm-2), as determined by weight increase, the pH of the surrounding seawater medium changed little (n=10, -0.0047 pH units.hr-1.cm-2). When calcification was not taking place the decrease of seawater pH was an order of magnitude higher, -0.013 pH units.hr-1.cm-2. This is the opposite of what is expected when calcium carbonate (CaCO3) forms. Similarly, fresh skeleton initially showed no change of pH in the seawater medium although the rates of weight gain were high (upto 1.0 mg hr-1.cm-2). After 10 hours, as the rate of deposition decreased following a generalized Michaelis-Menten growth curve, the pH began to decrease dramatically indicating an increase of CO2 in the seawater. These unexpected results can be explained if unstable calcium bicarbonate (Ca(HCO3)2) is formed in the organic matrix/carbonic anhydrase surface and slowly transforms later to CaCO3. Pieces of living coral monitored in the chamber for 30 hours gained weight during the day and loss it at night. The loss would be consistent with the transformation of Ca(HCO3)2 to CaCO3 with the release of CO2. The mean calcification rate of live coral was greater (n=8, p=0.0027) in high light (120 μmol.s-1.m-2) at 0.098 mg.hr-1.cm-2, compared to 0.063 mg.hr-1.cm-2 in low light (12 μmol.s-1.m-2). However, at the same time the mean rate of pH change was -0.0076 under low light compared to -0.0030 under high light (n=8, p=0.0001). The difference can be explained by CO2 being used for photosynthesis by zooxanthellae. The deposition rate of live coral was not affected by the addition of phosphate but the rate of weight gain by the freshly collected skeleton was strongly enhanced by phosphate. These results indicate that care should be applied in the application of the alkalinity anomaly technique for the measurement of calcification in corals. Rev. Biol. Trop. 62 (Suppl. 3): 25-38. Epub 2014 September 01.
https://doi.org/10.15517/rbt.v62i0.15899
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References

Al-Horani, F. A., Tambutté E., & Allemand, D. (2007). Dark calcification and the daily rhythm of calcification in the scleratinian coral, Galaxea fascicularis. Coral Reefs, 26, 531-53.

Allemand, D., Ferrier-Pagès, C., Furla, P., Houlbrèque, F., Puverel, S., Reynaud, S., Tambutté, E., Tambutté, S., & Zoccola, D. (2004). Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C R Palévol, 3, 453-467.

Allemand, D., Tambutté, E., Girard, J. P., & Jaubert, J. (1998). Organic matrix synthesis in the scleratinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. Journal of Experimental Biology, 201, 2001-2009.

Allemand, D., Tambutté, É., Zoccola, D., & Tambutté, S. (2011). Coral calcification, cells to reefs, p. 119-150. In Dubinsky, Z., & Stambler, N. (eds). Coral Reefs: an Ecosystem in Transition. Springer Science+Business Media B.V.

Atkinson, M. J., & Bingham, C. (1999). Elemental composition of commercial seasalts. Journal of Aquariculture and Aquatic Sciences, VIII (2), 39-43.

Burton, E. A., & Walter, L. M. (1990). The role of pH in phosphate inhibition of calcite and aragonite precipitation rates in seawater. Geochimica et Cosmochimica Acta, 54, 797-808.

Bryan, W. H., & Hill, D. (1941). Spherulitic crystallization as a mechanism of skeletal growth in the hexacorals. Proceedings of the Royal Society of Queensland, 52, 78–91.

Cohen, A., & McConnaughey, T. A. (2003). Geochemical perspectives on coral mineralization. Reviews in Mineralogy and Geochemistry, 54, 151-187.

Davies, P. S. (1989). Short-term growth measurements of corals using an accurate buoyant weighing technique. Marine Biology, 101, 389-395.

DeCoursey, T. E. (2003). Voltage-gated proton channels and other proton transfer pathways. Physiological Reviews, 83, 475-579.

Erez, J., Reynaud, S., Silverman, J., Schneider, K., & Allemand, D. (2011). Coral calcification under ocean acidification and global change, p. 151-176. In Dubinsky, Z., & Stambler, N. (eds). Coral Reefs: an Ecosystem in Transition. Springer Science+Business Media B.V.

Franzisket, L. (1964). Die Stoffwechselintensität der Riffkorallen und ihre ökologische phylogenetische und soziologische Bedeutung. Zpplogique Vergleich Physiologie, 49, 91-113.

Furla, P., Galgani, I., Durand, I. & Allemand, D. (2000). Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. Journal of Experimental Biology, 203, 3445-3457.

Gattuso, J-P., Allemand, D., & Frankignoulle, M. (1999). Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. American Zoologist, 39, 160-183.

Gischler, E., & Oschmann, W. (2005). Historical climate variation in Belize (Central America) as recorded in scleratinian corals. Palaios, 20, 159-174.

Kawaguti, S., & Sakumoto, D. (1948). The effect of light on the calcium deposition of corals. Bulletin of the Oceanographic Institute of Taiwan , 4, 65-70.

Kitano, Y., Tokuyama, A., & Arakaki, T. (1979). Magnesian calcite synthesis from calcium bicarbonate solution containing magnesium and barium ions. Geochemical Journal, 13, 181-185.

Kleypas, J. A., Buddemeier, R. R., Archer, D., Gattuso, J. P., Langdon, C., & Opdike, B.N. (1999). Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science, 284, 118-120.

Langdon, C. (2000). Review of experimental evidence for effects of CO2 on calcification of reef builders. Proceedings of the 9th International Coral Reef Symposium, 2, 2091-1098.

Langdon, C., & Atkinson, M. J. (2005). Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal of Geophysical Research, 110, CO9S07.

Langdon, C., Broecker, W. S., & Hammond, D. E. (2003). Effect of elevated CO2 on the community metabolism of an experimental coral reef. Global Biogeochemical Cycles, 17, 1101–1114.

Langdon, C., Takahashi, T., Sweeney, C., Chapman, D., Goddard, J., Marubini, F. Aceves, H. Barnett, H., & Atkinson, M.J. (2000). Effect of calcium carbonate saturation state on the rate of calcification of an experimental coral reef. Global Biogeochemical Cycles, 14, 639–654.

Lee, S., Park, J. H., Kwak, D., & Cho, K. (2010). Coral mineralization CaCO3 deposition via CO2 sequestration from the atmosphere. Crystal Growth and Design, 10, 851-855.

Lopez, S., France, J, Gerrits, W. J., Dhanoa, M. S., Humphries, D. J., & Dijkstra, J. (2000). A generalized Michaelis-Menten equation for the analysis of growth. Journal of Animal Science, 78, 1816-1828.

Marsh, J. A. (1970). Primary productivity of reef-building calcareous red algae. Ecology, 51, 255-263.

Marubini, F., & Thake, B. (1999). Bicarbonate addition promotes coral growth. Limnology and Oceanography, 44, 716-720.

McConnaughey, T. A. (1989). 13C and 18O isotopic disequilibrium in biological carbonates. II. In vitro simulation of kinetic isotope effects. Geochimica et Cosmochimica Acta, 53, 163-171.

McConnaughey, T. A. (2000). Community and environmental influences on reef coral calcification. Limnology and Oceanography, 45, 1667-1671.

McConnaughey, T. A. (2012). Zooxanthellae that open calcium channels: implications for coral reef corals. Marine Ecology Progress Series, 460, 277-287.

Morse, J. W. (1974). Dissolution kinetics of calcium carbonate in seawater. V. Effects of natural inhibitors and the position of the chemical lysocline. American Journal of Science, 274, 638-647.

Moya, A., Tambutté, S. Tambutté, E., Zoccola, D., Camaniti, N., & Allemand, D. (2006). Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for ‘light enhanced calcification’. Journal of Experimental Biology, 209, 3413-3419.

Paranawithana, S. R., Tu, C. K., Laipis, P. J., & Silverman, D. N. (1991). Enhancement of the catalytic activity of carbonic anhydrase III by phosphates. Journal of Biological Chemistry, 265 (36), 22270-4.

Pytkpowicz, R. M. (1973). Calcium carbonate retention in supersaturated seawater. American Journal of Science, 273, 515-522.

Puverel, S., Tambutté, E., Pereira-Mouriès, L., Zoccola, D. Allemand, D., & Tambutté, S. (2005). Soluble organic matrix of two scleratinian corals: Partial and comparative analysis. Comparative Biochemical Physiology, 141B, 480-487.

Reddy, M. M., Plummer, L. N., & Busenberg, E. 1981. Crystal growth of calcite from calcium bicarbonate solutions at constant PCO2 and 25°C: a test of a calcite dissolution model. Geochimica et Cosmochemica Acta, 45, 1281-9.

Reynaud, S., Leclercq, N., Romaine-Lioud, S., Ferrier-Pages, C., Jaubert, J., & Gattuso, J. P. (2003). Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biology, 9, 1660– 1668.

Romanek, C. S., Morse, J. W., & Grossman, E. L. (2011). Aragonite kinetics in dilute solutions. Aquatic Geochemistry, 17(4-5), 339-356.

Sandeman, I.M. (2008a). Fine banding in the septa of corals. Proceedings of the 11th International Coral Reef Symposium, 3, 57-61.

Sandeman, I. M. (2008b). Light driven lipid peroxidation of coral membranes and a suggested role in calcification. Revista de Biologia Tropical, 56, 1-9.

Sandeman, I. M. (2012). Preliminary results with a torsion microbalance indicate that carbon dioxide and exposed .carbonic anhydrase in the organic matrix are the basis of calcification on the skeleton surface of living corals. Revista de Biologia Tropical, 60, 103-120.

Smith, S. V., & Key, G. S. (1975). Carbon dioxide and metabolism in marine environments, Limnology and Oceanography, 20, 493– 495

Smith, S., & Kinsey, D. (1978). Calcification and organic carbon metabolism as indicated by carbon dioxide. p. 469–484. In Stoddart, D., & Johannes, R. Coral Reefs. Research Methods. Monographs on Oceanographic Methodology. Paris: UNESCO.

Strickland, J. D. H., & Parsons, T. R. (1965). A manual of sea water analysis. Bulletin No. 125, Fisheries Research Board of Canada. Ottawa.

Tentori, E., & Allemand, D. (2006) Light-enhanced calcification and dark decalcification in isolates of the soft coral Cladiella sp. during tissue recovery. Biological Bulletin, 211, 193-202.

Tokuyama, A., Kitano, Y., & Kanamori, N. (1973). Crystal forms of calcium carbonate formed from calcium bicarbonate solution containing heavy metal ions. Bulletin of Science & Engineering Division, University of Ryukyus. Mathematics & Natural Sciences, 16, 90-108.

Walsh, D., & Mann, S. (1995). Fabrication of hollow porous shells of calcium carbonate from self-organizing media. Nature, 377, 321-3.

Vogel, A. I. (1961). A text-book of quantitative inorganic analysis including elementary instrumental analysis. London: Longmans.

Zeebe, R. E., & Wolf-Gladrow, D. A. (2000). CO2 in Seawater: Equilibrium, Kinetics, Isotopes. Amsterdam: Elsevier.

Zhang, F., Wang, J. Hou, Z., Yu, M., & Xie, L. (2006). Study of growth of calcium carbonate crystals on chitosan film. Materials and Design, 27, 422-426.

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