Abstract
Coral calcification is affected by the decrease in aragonite saturation state (Ωarag) caused by ocean acidification (OA). However, OA effects are modulated by other environmental factors such as seawater temperature, light intensity and nutrients. Considering that in subtropical coral reefs all these factors vary seasonally, it can be hypothesized that the magnitude of OA effects on coral physiology will also vary seasonally. We evaluated the seasonal coral calcification rate of a subtropical reef-building coral under OA conditions. We approached this aim by culturing Acropora digitifera under three different CO2 partial pressure (pCO2) conditions in three different seasons (summer, autumn and winter) under natural light and temperature conditions. Additionally, to predict future coral net G, the year-round seawater carbonate chemistry was measured on the coast of Okinawa Island, and the annual coral CaCO3 production amount assessed considering seasonal changes in environmental conditions. Coral A. digitifera net calcification (net G) significantly differed among seasons, and summer net G was 1.7 and 2.7 times higher than autumn and winter, respectively. However, the impact of OA did not differ among seasons and the rate of net G decrease per unit Ωarag was 11.1%, 17.4% and 18.7% for summer, autumn and winter, respectively. The regression model indicated that net G of A. digitifera is primarily affected by temperature, secondly by seawater Ωarag, while light intensity was not selected as an explanatory factor, and there was no interactive effect among the factors. The model predicts that the present annual A. digitifera net G in Okinawa Island reef (present mean annual pCO2: 382 μatm and Ωarag: 3.49) is about 0.3 g CaCO3 cm−2 y−1, and it will decrease by 20% with an increase of 500 μatm seawater pCO2 than the present condition. As reefs in high-latitude regions already have marginal positive net G, further decrease in annual CaCO3 production would be detrimental for the reef under conditions of climate change.
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References
Albright R, Langdon C, Anthony KRN (2013) Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, central Great Barrier Reef. Biogeosciences 10:6747–6758
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 142:419–426
Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté É, Tambutté S, Zoccola D (2004) Biomineralization in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467
Anderson KD, Heron SF, Pratchett MS (2015) Species-specific declines in the linear extension of branching corals at a subtropical reef, Lord Howe Island. Coral Reefs 34:479–490
Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. PNAS 105:17442–17446
Bahr K, Jokiel PL, Rodgers KS (2017) Seasonal and annual calcification rates of the Hawaiian reef coral, Montipora capitata, under present and future climate change scenarios. ICES J Mar Sci 74:1083–1091
Bates NR, Amat A, Andersson AJ (2010) Feedbacks and responses of coral calcification on the Bermuda reef system to seasonal changes in biological processes and ocean acidification. Biogeosciences 7:2509–2530
Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365
Chalker BE (1981) Simulating light-saturation curves for photosynthesis and calcification by reef-building corals. Mar Biol 63:135–141
Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290
Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216
Comeau S, Carpenter RC, Edmunds PJ (2014) Effects of irradiance on the response of the coral Acropora pulchra and the calcifying alga Hydrolithon reinboldii to temperature elevation and ocean acidification. J Exp Mar Biol Ecol 453:28–35
Crossland CJ (1981) Seasonal growth of Acropora cf. formosa and Pocillopora damicornis on a high latitude reef (Houtman Abrolhos, Western Australia). Proc Fourth Int Coral Reef Symp 1:663–667
Crossland CJ (1984) Seasonal variations in the rates of calcification and productivity in the coral Acropora formosa on a high-latitude reef. Mar Ecol Prog Ser 15:135–140
Davies PS (1989) Short-term growth measurements of coral using an accurate buoyant weighing technique. Mar Biol 101:389–395
Dufault AM, Ninokawa A, Bramanti L, Cumbo VR, Fan T-Y, Edmunds PJ (2013) The role of light in mediating the effects of ocean acidification on coral calcification. J Exp Biol 216:1570–1577
Eyre BD, Cyronak T, Drupp P, De Carlo EH, Sachs JP, Andersson AJ (2018) Coral reefs will transition to net dissolving before end of century. Science 359:908–911
Foster T, Short JA, Falter JL, Ross C, McCulloch MT (2014) Reduced calcification in Western Australian corals during anomalously high summer water temperatures. J Exp Mar Biol Ecol 461:133–143
Gattuso J-P, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interaction and control by carbonate chemistry. Am Zool 39:160–183
Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 116:239–250
Gray SE, DeGrandpre MD, Langdon C, Corredor JE (2012) Short-term and seasonal pH, pCO2 and saturation state variability in a coral-reef ecosystem. Glob Biochem Cycles 26:GB3012
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
Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of Seawater Analysis, 3rd edn. Wiley-VCH, Weinheim, pp 159–228
Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. Plos ONE 6:e28983
Holocomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39
Intergovernmental Panel on Climate Change (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge Univ. Press, New York, NY, USA
Kayanne H, Hata H, Kudo S, Yamano H, Watanabe A, Ikeda Y, Nozaki K, Kato K, Negishi A, Saito H (2005) Seasonal and bleaching-induced changes in coral reef metabolism and CO2 flux. Glob Biogeochem Cycles 19:GB3015
Kinsey DW (1977) Seasonality and zonation in coral reef productivity and calcification. Proc Int Coral Reef Symp 2:383–388
Kleypas JA, McManus JW, Menez LAB (1999a) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159
Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999b) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120
Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: A guide for future research, report of a workshop held 18-20 April 2005. Petersburg, FL, sponsored by NSF, NOAA, and the U.S. Geological Survey, St
Kurihara H, Takahashi A, Reyes-Bermudez A, Hidaka M (2018) Intraspecific variation in the response of the scleractinian coral Acropora digitifera to ocean acidification. Mar Biol 165:38
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 14:639–654
Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09S07
Lewis E, Wallace D (1998) Program developed for CO2 system calculations. http://cdiac.esd.ornl.gov/oceans/co2rprtnbk.html
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and losers. Ecol Lett 4:122–131
Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world. PNAS 105:10450–10455
Manzello DP (2010) Ocean acidification hotspots: Spatiotemporal dynamics of the seawater CO2 system of eastern Pacific coral reefs. Limnol Oceanog 55:239–248
Marubini F, Barnett H, Langdon C, Atkinson MJ (2001) Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar Ecol Prog Ser 20:153–162
Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263
Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224
Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constant of carbonic acid in seawater at atmospheric pressure. Limnol Oceanog 18:897–907
Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Amer J Sci 283:780–799
Ohde S, van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65:559–576
Parsons TR, Maita Y, Lalli CM (1984) A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, p 173
Pratchett MS, Anderson KD, Hoogenboom MO, Widman E, Baird AH, Pandolfi JM, Edmunds PJ, Lough JM (2015) Spatial, temporal and taxonomic variation in coral growth-implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol Annu Rev 53:215–295
Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagès C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Change Biol 9:1660–1668
Rodolfo-Metalpa R, Martin S, Ferrier-Pagès C, Gattuso J-P (2010) Response of temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289–300
Ross CL, Falter JL, Schoepf V, McCulloch MT (2015) Perennial growth of hermatypic corals at Rottnest Island, Western Australia (32°S). Peer J 3:e781
Ross CL, Schoepf V, DeCarlo TM, McCulloch MT (2018) Mechanisms and seasonal drivers of calcification in the temperate coral Turbinaria reniformis at its latitudinal limits. Proc R Soc B 285:20180215
Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371
Samiei JV, Saleh A, Shirvani A, Fumani NS, Hashtroudi M, Pratchett MS (2016) Variation in calcification rate of Acropora downingi relative to seasonal changes in environmental conditions in the northeastern Persian Gulf. Coral Reefs 35:1371–1382
Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75
Silverman J, Lazar B, Erez J (2007) Community metabolism of coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82
Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:L05606
Shaw EC, McNeil BI, Tilbrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res 117:C03038
Smith SV (1973) Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol Oceanog 18:106–120
Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanog 20:493–495
Smith SV (1981) The Houtman Abrolhos Islands: Carbon metabolism of coral reefs at high latitude. Limnol Oceanog 26:612–621
Smith SV, Buddemeier RW (1992) Global change and coral reef ecosystems. Ann Review Ecol System 23:89–118
Suggett DJ, Dong LF, Lawson T, Lawrenz E, Torres L, Smith DJ (2013) Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32:327–337
Takahashi A, Kurihara H (2013) Ocean acidification does not affect the physiology of the tropical coral Acropora digitifera during a 5-week experiment. Coral Reefs 32:305–314
van Hooidonk RV, Maynard JA, Manzello D, Planes S (2014) Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Global Change Biol 20:103–112
Venti A, Andersson A, Langdon C (2014) Multiple driving factors explain spatial and temporal variability in coral calcification rates on the Bermuda platform. Coral Reefs 33:979–997
Yates K, Halley RB (2006) Diurnal variation in rates of calcification and carbonate sediment dissolution in Florida Bay. Est Coasts 29:24–39
Acknowledgements
We are grateful to all the staff of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, for their support. We also thank Izumi Mimura and Asami Tsugi for laboratory assistance. This work was supported by funding from the Japan Society for the Promotion of Science (JSPS) KAKENHI, Grant Number: 15H04536, and Japan Science and Technology (JST) CREST program, Grant Number: 140401.
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Kurihara, H., Wouters, J. & Yasuda, N. Seasonal calcification of the coral Acropora digitifera from a subtropical marginal Okinawa reef under ocean acidification. Coral Reefs 38, 443–454 (2019). https://doi.org/10.1007/s00338-019-01794-9
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DOI: https://doi.org/10.1007/s00338-019-01794-9