Responses of coral gastrovascular cavity pH during light and dark incubations to reduced seawater pH suggest species-specific responses to the effects of ocean acidification on calcification

Abstract

Coral polyps have a fluid-filled internal compartment, the gastrovascular cavity (GVC). Respiration and photosynthesis cause large daily excursions in GVC oxygen concentration (O2) and pH, but few studies have examined how this correlates with calcification rates. We hypothesized that GVC chemistry can mediate and ameliorate the effects of decreasing seawater pH (pHSW) on coral calcification. Microelectrodes were used to monitor O2 and pH within the GVC of Montastraea cavernosa and Duncanopsammia axifuga (pH only) in both the light and the dark, and three pHSW levels (8.2, 7.9, and 7.6). At pHSW 8.2, GVC O2 ranged from ca. 0 to over 400% saturation in the dark and light, respectively, with transitions from low to high (and vice versa) within minutes of turning the light on or off. For all three pHSW treatments and both species, pHGVC was always significantly above and below pHSW in the light and dark, respectively. For M. cavernosa in the light, pHGVC reached levels of pH 8.4–8.7 with no difference among pHSW treatments tested; in the dark, pHGVC dropped below pHSW and even below pH 7.0 in some trials at pHSW 7.6. For D. axifuga in both the light and the dark, pHGVC decreased linearly as pHSW decreased. Calcification rates were measured in the light concurrent with measurements of GVC O2 and pHGVC. For both species, calcification rates were similar at pHSW 8.2 and 7.9 but were significantly lower at pHSW 7.6. Thus, for both species, calcification was protected from seawater acidification by intrinsic coral physiology at pHSW 7.9 but not 7.6. Calcification was not correlated with pHGVC for M. cavernosa but was for D. axifuga. These results highlight the diverse responses of corals to changes in pHSW, their varying abilities to control pHGVC, and consequently their susceptibility to ocean acidification.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Agostini S, Suzuki Y, Higuchi T, Casareto BE, Yoshinaga K, Nakano Y, Fujimura H (2012) Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31:147–156

    Article  Google Scholar 

  2. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003a) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Article  Google Scholar 

  3. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003b) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15

    Article  Google Scholar 

  4. Allemand D, Tambutté É, Zoccola D, Tambutté S (2010) Coral calcification, cells to reefs. Springer, Dordrecht

    Google Scholar 

  5. Allemand D, Ferrier-Pages C, Furla P, Houlbreque F, Puverel S, Reynaud S, Tambutte E, Tambutte S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. CR Palevol 3:453–467

    Article  Google Scholar 

  6. Barott KL, Venn AA, Perez SO, Tambutte S, Tresguerres M (2015) Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc Natl Acad Sci USA 112:607–612

    CAS  PubMed  Article  Google Scholar 

  7. Bove C, Ries J, Davies S, Westfield I, Umbanhowar J, Castillo K (2019) Common Caribbean corals exhibit highly variable responses to future acidification and warming. Proc R Soc B Biol Sci 286:1–9

    Google Scholar 

  8. Cai WJ, Ma Y, Hopkinson BM, Grottoli AG, Warner ME, Ding Q, Hu X, Yuan X, Schoepf V, Xu H, Han C, Melman TF, Hoadley KD, Pettay DT, Matsui Y, Baumann JH, Levas S, Ying Y, Wang Y (2016) Microelectrode characterization of coral daytime interior pH and carbonate chemistry. Nat Commun 7:11144

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Chalker BE (1976) Calcium-transport during skeletogenesis in hermatypic corals. Comp Biochem Physiol A Physiol 54:455–459

    CAS  Article  Google Scholar 

  10. Chalker BE, Taylor DL (1975) Light-enhanced calcification, and role of oxidative-phosphorylation in calcification of coral Acropora cervicornis. Proc R Soc B Biol Sci 190:323–331

    CAS  Google Scholar 

  11. Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290

    Article  Google Scholar 

  12. Chen S, Gagnon AC, Adkins JF (2018) Carbonic anhydrase, coral calcification and a new model of stable isotope vital effects. Geochim Cosmochim Acta 236:179–197

    CAS  Article  Google Scholar 

  13. Chou WC, Liu PJ, Chen YH, Huang WJ (2020) Contrasting changes in diel variations of net community calcification support that carbonate dissolution can be more sensitive to ocean acidification than coral calcification. Front Mar Sci 7:3

    Article  Google Scholar 

  14. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Biomineralization 54:151–187

    CAS  Article  Google Scholar 

  15. Cohen I, Dubinsky Z, Erez J (2016) Light enhanced calcification in hermatypic corals: new insights from light spectral responses. Front Mar Sci 2:122

    Article  Google Scholar 

  16. Colombo-Pallotta MF, Rodriguez-Roman A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Article  Google Scholar 

  17. Comeau S, Cornwall CE, McCulloch MT (2017a) Decoupling between the response of coral calcifying fluid pH and calcification to ocean acidification. Sci Rep 7:1–10

    CAS  Article  Google Scholar 

  18. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnol Oceanogr 59:1081–1091

    CAS  Article  Google Scholar 

  19. Comeau S, Tambutte E, Carpenter RC, Edmunds PJ, Evensen NR, Allemand D, Ferrier-Pages C, Tambutte S, Venn AA (2017b) Coral calcifying fluid pH is modulated by seawater carbonate chemistry not solely seawater pH. Proc R Soc B Biol Sci 284:20161669

    Article  CAS  Google Scholar 

  20. Cyronak T, Eyre BD (2016) The synergistic effects of ocean acidification and organic metabolism on calcium carbonate (CaCO3) dissolution in coral reef sediments. Mar Chem 183:1–12

    CAS  Article  Google Scholar 

  21. D’Olivo JP, McCulloch MT, Judd K (2013) Long-term records of coral calcification across the central Great Barrier Reef: assessing the impacts of river runoff and climate change. Coral Reefs 32:999–1012

    Article  Google Scholar 

  22. de Beer D, Kuhl M, Stambler N, Vaki L (2000) A microsensor study of light enhanced Ca2 + uptake and photosynthesis in the reef-building hermatypic coral Favia sp. Mar Ecol Prog Ser 194:75–85

    Article  Google Scholar 

  23. DeCarlo TM, Ross CL, McCulloch MT (2019) Diurnal cycles of coral calcifying fluid aragonite saturation state. Mar Biol 166:28

    Article  CAS  Google Scholar 

  24. DeCarlo TM, Comeau S, Cornwall CE, McCulloch MT (2018) Coral resistance to ocean acidification linked to increased calcium at the site of calcification. Proc R Soc B Biol Sci 285:20180564

    Article  CAS  Google Scholar 

  25. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432

    CAS  Article  Google Scholar 

  26. Gattuso JP, 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. Am Zool 39:160–183

    CAS  Article  Google Scholar 

  27. Goreau Thomas F, Goreau Nora I (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117(2):239–250

    CAS  Article  Google Scholar 

  28. Gregoire V, Schmacka F, Coffroth MA, Karsten U (2017) Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp (Dinophyceae). J Appl Phycol 29:1893–1905

    Article  Google Scholar 

  29. Guo WF (2019) Seawater temperature and buffering capacity modulate coral calcifying pH. Sci Rep 9:1–3

    Article  CAS  Google Scholar 

  30. Hall-Spencer JM, Harvey BP (2019) Ocean acidification impacts on coastal ecosystem services due to habitat degradation. Emerg Top Life Sci 3:197–206

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  31. Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:158

    Article  Google Scholar 

  32. Holcomb M, Cohen AL, Gabitov RI, Hutter JL (2009) Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim Cosmochim Acta 73:4166–4179

    CAS  Article  Google Scholar 

  33. Holcomb M, Venn AA, Tambutte E, Tambutte S, Allemand D, Trotter J, McCulloch M (2014) Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep 4:5207

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101

    CAS  Article  Google Scholar 

  35. Inoue M, Nakamura T, Tanaka Y, Suzuki A, Yokoyama Y, Kawahata H, Sakai K, Gussone N (2018) A simple role of coral-algal symbiosis in coral calcification based on multiple geochemical tracers. Geochim Cosmochim Acta 235:76–88

    CAS  Article  Google Scholar 

  36. IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. In: Core Writing Team RKPaLAM (ed) IPCC, Geneva, Switzerland, p 151

  37. 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): bicarbonate concentrations best predict calcification rates. Glob Change Biol 16:1632–1644

    Article  Google Scholar 

  38. Kuhl M, Cohen Y, Dalsgaard T, Jorgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Article  Google Scholar 

  39. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    CAS  Article  Google Scholar 

  40. Langdon C, Albright R, Baker AC, Jones P (2018) Two threatened Caribbean coral species have contrasting responses to combined temperature and acidification stress. Limnol Oceanogr 63:2450–2464

    CAS  Article  Google Scholar 

  41. Leder JJ, Swart PK, Szmant AM, Dodge RE (1996) The origin of variations in the isotopic record of scleractinian corals.1. Oxygen. Geochimica Cosmochimica Acta 60:2857–2870

    CAS  Article  Google Scholar 

  42. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Climate Change 2:623–633

    CAS  Article  Google Scholar 

  43. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    CAS  Article  Google Scholar 

  44. Okazaki RR, Towle EK, van Hooidonk R, Mor C, Winter RN, Piggot AM, Cunning R, Baker AC, Klaus JS, Swart PK, Langdon C (2017) Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs. Glob Change Biol 23:1023–1035

    Article  Google Scholar 

  45. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    CAS  PubMed  Article  Google Scholar 

  46. Pearse VB (1970) Incorporation of metabolic CO2 into coral skeleton. Nature 228:383

    CAS  PubMed  Article  Google Scholar 

  47. Pearse VB, Muscatin L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull 141:350–363

    CAS  Article  Google Scholar 

  48. Polinski JM, Voss JD (2018) Evidence of photoacclimatization at mesophotic depths in the coral-symbiodinium symbiosis at flower garden banks national marine sanctuary and mcgrail bank. Coral Reefs 37:779–789

    Article  Google Scholar 

  49. Porter JW (1974) Zooplankton feeding by the Caribbean reef-building coral Montastrea cavernosa. Proc Second Int Symp Coral Reefs 1:111–112

    Google Scholar 

  50. R Core Development Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  51. Raz-Bahat M, Douek J, Moiseeva E, Peters EC, Rinkevich B (2017) The digestive system of the stony coral Stylophora pistillata. Cell Tissue Res 368:311–323

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  54. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    CAS  Article  Google Scholar 

  55. Rinkevich B, Loya Y (1984) Does light enhance calcification in hermatypic corals. Mar Biol 80:1–6

    CAS  Article  Google Scholar 

  56. Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology: a functional evolutionary approach. Brooks/Cole, Belmont

    Google Scholar 

  57. Scheufen T, Kramer WE, Iglesias-Prieto R, Enriquez S (2017) Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Sci Rep 7:1–15

    CAS  Article  Google Scholar 

  58. Schoepf V, Jury CP, Toonen RJ, McCulloch MT (2017) Coral calcification mechanisms facilitate adaptive responses to ocean acidification. Proc R Soc B Biol Sci 284:20172117

    Article  CAS  Google Scholar 

  59. Schoepf V, Grottoli AG, Warner ME, Cai WJ, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS ONE 8:e75049

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Scott PJB (1990) Chronic pollution recorded in coral skeletons in Hong-Kong. J Exp Mar Biol Ecol 139:51–64

    Article  Google Scholar 

  61. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary-layers surrounding stony corals. Biol Bull 185:455–461

    CAS  PubMed  Article  Google Scholar 

  62. Suggett DJ, Goyen S, Evenhuis C, Szabo M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381

    PubMed  Article  Google Scholar 

  63. Swart PK (1983) Carbon and oxygen isotope fractionation in scleractinian corals - A review. Earth Sci Rev 19:51–80

    CAS  Article  Google Scholar 

  64. Szmant-Froelich A, Pilson MEQ (1984) Effects of feeding frequency and symbiosis with zooxanthellae on nitrogen-metabolism and respiration of the coral Astrangia-danae. Mar Biol 81:153–162

    CAS  Article  Google Scholar 

  65. Tagliafico A, Rudd D, Rangel MS, Kelaher BP, Christidis L, Cowden K, Scheffers SR, Benkendorff K (2017) Lipid-enriched diets reduce the impacts of thermal stress in corals. Mar Ecol Prog Ser 573:129–141

    CAS  Article  Google Scholar 

  66. Tans P, Keeling R (2017) Recent monthly average Mauna loa CO2. NOAA/ESRL and Scripps institution of oceanography, San Diego, California, USA

  67. Tresguerres M, Barott K, Barron M, Deheyn D, Kline D, Linsmayer L (2017) Cell biology of reef-building corals: ion transport, acid/base regulation, and energy metabolism. In: Weihrauch D, O’Donnell M (eds) Acid-base balance and nitrogen excretion in invertebrates. Springer, Cham, pp 193–218

    Chapter  Google Scholar 

  68. Venn A, Tambutte E, Holcomb M, Allemand D, Tambutte S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6:e20013

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. Venn AA, Tambutte E, Holcomb M, Laurent J, Allemand D, Tambutte S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Natl Acad Sci USA 110:1634–1639

    CAS  PubMed  Article  Google Scholar 

  70. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  71. Von Euw S, Zhang QH, Manichev V, Murali N, Gross J, Feldman LC, Gustafsson T, Flach C, Mendelsohn R, Falkowski PG (2017) Biological control of aragonite formation in stony corals. Science 356:933–938

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was partially funded by the National Oceanographic and Atmospheric Administration Office of Exploration and Research Grant NA09OAR4320073 to Florida Atlantic University and University of North Carolina Wilmington under the Cooperative Institute for Ocean Exploration, Research and Technology (CIOERT) Program.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alina M. Szmant.

Ethics declarations

Conflict of interest

Authors declare that research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 40 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bove, C.B., Whitehead, R.F. & Szmant, A.M. Responses of coral gastrovascular cavity pH during light and dark incubations to reduced seawater pH suggest species-specific responses to the effects of ocean acidification on calcification. Coral Reefs 39, 1675–1691 (2020). https://doi.org/10.1007/s00338-020-01995-7

Download citation

Keywords

  • Ocean acidification
  • Gastrovascular cavity
  • Gastrovascular chemistry
  • Photosynthesis
  • Coral calcification
  • Seawater pH
  • Coral metabolism