Marine Biology

, 165:38 | Cite as

Intraspecific variation in the response of the scleractinian coral Acropora digitifera to ocean acidification

  • Haruko Kurihara
  • Asami Takahashi
  • Alejandro Reyes-Bermudez
  • Michio Hidaka
Original paper


To examine the possible variation in responses of corals to ocean acidification (OA) among populations, we compared the sensitivity of two Okinawan populations (Sesoko and Bise) of the scleractinian coral Acropora digitifera to high pCO2. We found that both light and dark calcification rates of Sesoko corals did not change with an increase in seawater pCO2, while the calcification rates of Bise corals significantly decreased. Additionally, calcification rate of Sesoko corals was significantly lower than Bise corals at control conditions. Expressions of two putative calcification-related genes (BAT: bicarbonate transporter and galaxin) were up-regulated at high CO2 compared to the control and expression of the BAT gene was significantly higher in Sesoko compared to Bise corals. Consequently, differences in the calcification rate between populations and differences in the expression of genes related to inorganic carbon transport regulation could be reasons that explain the difference in the response to OA between the two populations. Furthermore, taking into account that Sesoko corals were located in relatively nearshore areas where the environmental conditions are more variable, while Bise corals were located in the forereef which shows more stable conditions, plasticity for coral calcification in response to different environmental conditions and/or acclimation response to changes such as seawater pCO2 may lead to differences in sensitivity between the two populations to high seawater pCO2. Studies considering the potential variability in corals sensitivity to OA among local populations from different habitats are important to predict the potential effects of climate change on reef ecosystems.



We are grateful to all the staff of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus for their support. We also thank Hideyuki Yamashiro for help with lipid content analysis.


This work was conducted with the support of funding from the Japan Society for the Promotion of Science (JSPS), and JST, CREST program.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest.

Ethical approval

The manuscript has not been submitted to more than one journal for simultaneous consideration. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

227_2018_3295_MOESM1_ESM.pdf (166 kb)
Supplementary material 1 (PDF 165 kb)


  1. 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
  2. Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 119–150Google Scholar
  3. Anthony KRN (2006) Enhanced energy status of corals on coastal, high-turbidity reefs. Mar Ecol Prog Ser 319:111–116CrossRefGoogle Scholar
  4. Bertucci A, Moya A, Tambutté S, Allemand D, Supuran CT, Zoccola D (2013) Carbonic anhydrases in anthozoan corals—a review. Bioorg Med Chem 21:1437–1450CrossRefGoogle Scholar
  5. Castillo KD, Ries JB, Weiss JM (2011) Declining coral skeleton extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, southern Belize. PLoS ONE 6:e14615CrossRefGoogle Scholar
  6. Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290CrossRefGoogle Scholar
  7. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Rev Mineral Geochem 54:151–187CrossRefGoogle Scholar
  8. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014a) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory experiments. Limnol Oceanogr 59:1081–1091CrossRefGoogle Scholar
  9. Comeau S, Carpenter RC, Nojiri Y, Putman HM, Sakai K, Edmunds PJ (2014b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc B 281:20141339CrossRefGoogle Scholar
  10. Davis PS (1989) Short-term growth measurements of coral using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  11. De Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2011) The impact of seawater saturation state and biocarbonate ion concentration in calcification by new recruits of two Atlantic corals. Coral Reefs 30:321–328CrossRefGoogle Scholar
  12. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2013) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169CrossRefGoogle Scholar
  13. Fukuda I, Ooki S, Fujita T, Murayama E, Nagasawa H, Isa Y, Watanabe T (2003) Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton. Biochem Biophys Res Commun 304:11–17CrossRefGoogle Scholar
  14. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457Google Scholar
  15. Goiran C, Al-Moghrabi S, Allemand D, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association I. Photosynthetic performances of symbionts and dependence on sea water biocarbonate. J Exp Mar Biol Ecol 199:207–225CrossRefGoogle Scholar
  16. Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull 116:59–75CrossRefGoogle Scholar
  17. Grasso LC, Maindonald J, Rudd S, Hayward DC, Saint R, Miller DJ, Ball EE (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genom 9:540CrossRefGoogle Scholar
  18. Hayward DC, Hetherington S, Behm CA, Grasso LC, Foret S, Miller DJ, Ball EE (2011) Differential gene expression at coral settlement and metamorphosis—a subtractive hybridization study. PLoS ONE 6:e26411CrossRefGoogle Scholar
  19. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, GreenWeld P, Gomez E, Harvell CD, Sale PF et al (2007) Coral reef under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefGoogle Scholar
  20. Holcomb M, Venn AA, Tambutté E, Tambutté S, Allemand D, Trotter J, McCulloch M (2014) Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep 4:5207CrossRefGoogle Scholar
  21. Iguchi A, Ozaki S, Nakamura T, Inoue M, Tanaka Y, Suzuki A, Kawahata H, Sakai K (2012) Effects of acidified seawater on coral calcification and symbiotic algae on the massive coral Porites australiensis. Mar Environ Res 73:32–36CrossRefGoogle Scholar
  22. Inoue S, Kayanne H, Yamamoto S, Kurihara H (2013) Spatial community shift from hard to soft corals in acidified water. Nat Clim Change 3:683–687CrossRefGoogle Scholar
  23. Isa Y, Yamazato K (1984) The distribution of carbonic anhydrase in a staghorn coral Acropora hebes (Dana). Galaxea 3:25–36Google Scholar
  24. Jokiel PL, Rodgers KS, Kuffner LB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483CrossRefGoogle Scholar
  25. Jury CP, Whitehead RF, Szmant AM (2010) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973): biocarbonate concentrations best predict calcification rates. Glob Change Biol 16:1632–1644CrossRefGoogle Scholar
  26. Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O (2012) Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS ONE 7:e34659CrossRefGoogle Scholar
  27. Kavousi J, Reimer JD, Tanaka Y, Nakamura T (2015) Colony-specific investigations reveal highly variable responses among individual corals to ocean acidification and warming. Mar Environ Res 109:9–20CrossRefGoogle Scholar
  28. Kavousi J, Tanaka Y, Nishida K, Suzuki A, Nojiri Y, Nakamura T (2016) Colony-specific calcification and mortality under ocean acidification in the branching coral Montipora digitata. Mar Environ Res 119:161–165CrossRefGoogle Scholar
  29. 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, St. Petersburg, FL, sponsored by NSF, NOAA, and the U.S. Geological SurveyGoogle Scholar
  30. 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
  31. 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 RidgeGoogle Scholar
  32. Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868CrossRefGoogle Scholar
  33. McConnaughey TA, Falk RH (1991) Calcium–proton exchange during algal calcification. Biol Bull 180:185–195CrossRefGoogle Scholar
  34. 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
  35. Movilla J, Calvo E, Pelejero C, Coma R, Serrano E, Fernández-Vallejo P, Ribes M (2012) Calcification reduction and recovery in native and non-native Mediterranean corals in response to ocean acidification. J Exp Mar Biol Ecol 438:144–153CrossRefGoogle Scholar
  36. Moya A, Huisman L, Ball EE, Hayward DC, Grasso LC, Chua CM, Woo HN, Gattuso J-P, Foret S, Miller DJ (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol Ecol 21:2440–2454CrossRefGoogle Scholar
  37. Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Am J Sci 283:780–799CrossRefGoogle Scholar
  38. Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2010) Gene flow and genetic diversity of a broadcast spawning coral in northern peripheral populations. PLoS ONE 5:e11149CrossRefGoogle Scholar
  39. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422CrossRefGoogle Scholar
  40. Parker LM, Ross PM, O’Connor WA (2011) Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Mar Biol 158:689–697CrossRefGoogle Scholar
  41. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefGoogle Scholar
  42. Range P, Chícharo MA, Ben-Hamadou R, Pilo D, Fernandez-Reiriz MJ, Labarta U, Marin MG, Bressan M, Matozzo V, Chinellato A, Munari M, El Menif NT, Dellali M, Chícharo L (2014) Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Reg Environ Change 14:19–30CrossRefGoogle Scholar
  43. Reyes-Bermudez A, Lin Z, Hayward DC, Miller DJ, Ball EE (2009) Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora. BMC Evol Biol 9:178CrossRefGoogle Scholar
  44. 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
  45. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535CrossRefGoogle Scholar
  46. Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293CrossRefGoogle Scholar
  47. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with new type of modulation fluorometer. Photosynth Res 10:51–62CrossRefGoogle Scholar
  48. Shaw EC, Carpenter RC, Lantz CA, Edmunds PJ (2016) Intraspecific variability in the response to ocean warming and acidification in the scleractinian coral Acropora pulchra. Mar Biol 163:210CrossRefGoogle Scholar
  49. Smith SV (1973) Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol Oceanogr 18:106–120CrossRefGoogle Scholar
  50. Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495CrossRefGoogle Scholar
  51. Smith LW, Barshis D, Birkeland C (2007) Phenotypic plasticity for skeleton growth, density and calcification of Porites lobata in response to habitat type. Coral Reefs 26:559–567CrossRefGoogle Scholar
  52. Souter P, Bay LK, Andreakis N, Császár N, Seneca FO, Van Oppen MJH (2010) A multilocus, temperatures stress-related gene expression profile assay in Acropora millepora, a dominant reef-building coral. Mol Ecol Resour 11:328–334CrossRefGoogle Scholar
  53. Stimson JS (1987) Location, quantity and rate of change in quantity of lipid in tissue of Hawaiian hermatypic corals. Bull Mar Sci 21:889–904Google Scholar
  54. Strahl J, Stolz I, Uthicke S, Vogel N, Noonan SHC, Fabricius KE (2015) Physiological and ecological performance differs in four coral taxa at a volcanic carbon dioxide seep. Comp Biochem Physiol A 184:170–186CrossRefGoogle Scholar
  55. Sunday JM, Crim RN, Harley DG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS ONE 6:e22881CrossRefGoogle Scholar
  56. 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
  57. Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté E, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408:58–78CrossRefGoogle Scholar
  58. Tanaka K, Holcomb M, Takahashi A, Kurihara H, Asami R, Shinjo R, Sowa K, Rankenburg K, Watanabe T, McCulloch M (2015) Response of Acropora digitifera to ocean acidification: constraints from δ11B, Sr, Mg, and Ba compositions of aragonitic skeletons cultured under variable seawater pH. Coral Reefs 34:1139–1149CrossRefGoogle Scholar
  59. Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Körtzinger A, Wahl M, Melzner F (2010) Calcifying invertebrates succeed in naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7:3879–3891CrossRefGoogle Scholar
  60. Vidal-Dupiol J, Zoccola D, Tambutté E, Grunau C, Cosseau C, Smith KM, Freitag M, Dheilly NM, Allemand D, Tambutté S (2013) Genes related to ion-transport and energy production are upregulated in response to CO2-driven pH decrease in corals: new insights from transcriptome analysis. PLoS ONE 8:e58652CrossRefGoogle Scholar
  61. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawa corals. Comp Biochem Physiol Part B Biochem Mol Biol 122:397–407CrossRefGoogle Scholar
  62. Zoccola D, Tambutté E, Kulhanek E, Puverel S, Scimeca J-C, Allemand D, Tambutté S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta 1663:1–27CrossRefGoogle Scholar
  63. Zoccola D, Ganot P, Bertucci A, Caminiti-Segonds N, Techer N, Voolstra CR, Aranda M, Tambutté E, Allemand D, Casey JR, Tambutté S (2015) Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification. Sci Rep 5:09983CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Chemistry, Biology, and Marine Science, Faculty of ScienceUniversity of the RyukyusNishiharaJapan
  2. 2.School of Biology, Faculty of Natural SciencesUniversidad de la AmazoniaFlorenciaColombia

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