Advertisement

Coral Reefs

pp 1–12 | Cite as

Seasonal calcification of the coral Acropora digitifera from a subtropical marginal Okinawa reef under ocean acidification

  • Haruko KuriharaEmail author
  • Judith Wouters
  • Naoko Yasuda
Report

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.

Keywords

Ocean acidification Coral Seasonality Physiology Subtropics Marginal reef 

Notes

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.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2019_1794_MOESM1_ESM.pptx (233 kb)
Supplementary material 1 (PPTX 233 kb)

References

  1. 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 10:6747–6758CrossRefGoogle Scholar
  2. 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 142:419–426CrossRefGoogle Scholar
  3. 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 3:453–467CrossRefGoogle Scholar
  4. 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 34:479–490CrossRefGoogle Scholar
  5. 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 105:17442–17446CrossRefGoogle Scholar
  6. 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 74:1083–1091Google Scholar
  7. 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 7:2509–2530CrossRefGoogle Scholar
  8. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  9. Chalker BE (1981) Simulating light-saturation curves for photosynthesis and calcification by reef-building corals. Mar Biol 63:135–141CrossRefGoogle Scholar
  10. Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290CrossRefGoogle Scholar
  11. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216CrossRefGoogle Scholar
  12. 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 453:28–35CrossRefGoogle Scholar
  13. 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 1:663–667Google Scholar
  14. 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 15:135–140CrossRefGoogle Scholar
  15. Davies PS (1989) Short-term growth measurements of coral using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  16. 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 216:1570–1577CrossRefGoogle Scholar
  17. 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 359:908–911CrossRefGoogle Scholar
  18. 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 461:133–143CrossRefGoogle Scholar
  19. 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 39:160–183CrossRefGoogle Scholar
  20. 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 116:239–250CrossRefGoogle Scholar
  21. 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:GB3012Google Scholar
  22. 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 22:551–558CrossRefGoogle Scholar
  23. 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 159–228CrossRefGoogle Scholar
  24. 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:e28983CrossRefGoogle Scholar
  25. 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 9:29–39CrossRefGoogle Scholar
  26. 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, USAGoogle Scholar
  27. 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:GB3015CrossRefGoogle Scholar
  28. Kinsey DW (1977) Seasonality and zonation in coral reef productivity and calcification. Proc Int Coral Reef Symp 2:383–388Google Scholar
  29. Kleypas JA, McManus JW, Menez LAB (1999a) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159CrossRefGoogle Scholar
  30. 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 284:118–120CrossRefGoogle Scholar
  31. 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, StGoogle Scholar
  32. 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 165:38CrossRefGoogle Scholar
  33. 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 14:639–654CrossRefGoogle Scholar
  34. 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:C09S07CrossRefGoogle Scholar
  35. Lewis E, Wallace D (1998) Program developed for CO2 system calculations. http://cdiac.esd.ornl.gov/oceans/co2rprtnbk.html
  36. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  37. 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 105:10450–10455CrossRefGoogle Scholar
  38. Manzello DP (2010) Ocean acidification hotspots: Spatiotemporal dynamics of the seawater CO2 system of eastern Pacific coral reefs. Limnol Oceanog 55:239–248CrossRefGoogle Scholar
  39. 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 20:153–162CrossRefGoogle Scholar
  40. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  41. Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224Google Scholar
  42. 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 18:897–907CrossRefGoogle Scholar
  43. Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Amer J Sci 283:780–799CrossRefGoogle Scholar
  44. Ohde S, van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65:559–576Google Scholar
  45. Parsons TR, Maita Y, Lalli CM (1984) A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, p 173Google Scholar
  46. 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 53:215–295Google Scholar
  47. 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 9:1660–1668CrossRefGoogle Scholar
  48. 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 7:289–300CrossRefGoogle Scholar
  49. Ross CL, Falter JL, Schoepf V, McCulloch MT (2015) Perennial growth of hermatypic corals at Rottnest Island, Western Australia (32°S). Peer J 3:e781CrossRefGoogle Scholar
  50. 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 285:20180215CrossRefGoogle Scholar
  51. 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 305:367–371CrossRefGoogle Scholar
  52. 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 35:1371–1382CrossRefGoogle Scholar
  53. 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 127:64–75CrossRefGoogle Scholar
  54. Silverman J, Lazar B, Erez J (2007) Community metabolism of coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82CrossRefGoogle Scholar
  55. Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:L05606CrossRefGoogle Scholar
  56. Shaw EC, McNeil BI, Tilbrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res 117:C03038CrossRefGoogle Scholar
  57. Smith SV (1973) Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol Oceanog 18:106–120CrossRefGoogle Scholar
  58. Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanog 20:493–495CrossRefGoogle Scholar
  59. Smith SV (1981) The Houtman Abrolhos Islands: Carbon metabolism of coral reefs at high latitude. Limnol Oceanog 26:612–621CrossRefGoogle Scholar
  60. Smith SV, Buddemeier RW (1992) Global change and coral reef ecosystems. Ann Review Ecol System 23:89–118CrossRefGoogle Scholar
  61. 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 32:327–337CrossRefGoogle Scholar
  62. 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 32:305–314CrossRefGoogle Scholar
  63. 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 20:103–112CrossRefGoogle Scholar
  64. 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 33:979–997CrossRefGoogle Scholar
  65. Yates K, Halley RB (2006) Diurnal variation in rates of calcification and carbonate sediment dissolution in Florida Bay. Est Coasts 29:24–39CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.University of the RyukyusOkinawaJapan

Personalised recommendations