, 65:9 | Cite as

Carbonate dissolution by reef microbial borers: a biogeological process producing alkalinity under different pCO2 conditions

  • A. Tribollet
  • A. Chauvin
  • P. Cuet
Original Article
Part of the following topical collections:
  1. Bioerosion: An interdisciplinary approach


Rising atmospheric CO2 is acidifying the world’s oceans, affecting both calcification and dissolution processes in coral reefs. Among processes, carbonate dissolution by bioeroding microflora has been overlooked, and especially its impact on seawater alkalinity. To date, this biogeological process has only been studied using microscopy or buoyant weight techniques. To better understand its possible effect on seawater alkalinity, and thus on reef carbonate budget, an experiment was conducted under various seawater chemistry conditions (2 ≤ Ωarag ≤ 3.5 corresponding to 440 ≤ pCO2 (µatm) ≤ 940) at 25 °C under night and daylight (200 µmol photons m−2 s−1) with natural microboring communities colonizing dead coral blocks (New Caledonia). Both the alkalinity anomaly technique and microscopy methods were used to study the activity of those communities dominated by the chlorophyte Ostreobium sp. Results show that (1) the amount of alkalinity released in seawater by such communities is significant and varies between 12.8 ± 0.7 at ΩArag ~ 2 and 5.6 ± 0.4 mmol CaCO3 m−2 day−1 at ΩArag ~ 3–3.5 considering a 12:12 photoperiod; (2) although dissolution is higher at night (~ 80 vs. 20% during daylight), the process can occur under significant photosynthetic activity; and (3) the process is greatly stimulated when an acidity threshold is reached (pCO2 ≥ 920 µatm vs. current conditions at constant light intensity). We show that carbonate dissolution by microborers is a major biogeochemical process that could dissolve a large part of the carbonates deposited by calcifying organisms under ocean acidification.


Biogenic carbonate dissolution Microborers Euendoliths Coral reefs Ocean acidification Seawater alkalinity 



We would like to dedicate this paper to our colleague and friend Marlin Atkinson who passed away in 2013. A.T. and P.C. conceived the experimental design. A.T., P.C., and A.C. collected samples and analyzed data. A.T. and P.C. wrote the article and A.C. gave assistance on figure preparations and for formatting. We thank the Plateforme Alizes (IRD Bondy) for SEM access and S. Pyneeandy for her help with measurements of biogenic rates on coral blocks. We thank the Center IRD in Nouméa for its support in the field. Finally, this work was supported by the French Ministry of Ecology (program ‘MIDACOR’, 2011–2014) and the Institut de Recherche pour le Développement. The funding sponsors had no involvement in the present study development (design, collection, analysis, etc.).

Data availability

Datasets are available from the corresponding author ( upon reasonable request, while pending to be deposited on the SEANOE repository.


  1. Adey WH (1998) Review. Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406CrossRefGoogle Scholar
  2. Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann Rev Mar Sci 5:321–348CrossRefGoogle Scholar
  3. Andersson AJ, Mackenzie FT (2012) Revisiting four scientific debates in ocean acidification research. Biogeosciences 9:893–905CrossRefGoogle Scholar
  4. Andersson AJ, Bates NR, Mackenzie FT (2007) Dissolution of carbonate sediments under rising pCO2 and ocean acidification: observations from Devil’s Hole, Bermuda. Aquat Geochem 13:237–264CrossRefGoogle Scholar
  5. Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  6. Carreiro-Silva M, McClanahan TR, Kiene WE (2005) The role of inorganic nutrients and herbivory in controlling microbioerosion of carbonate substratum. Coral Reefs 24:214–221CrossRefGoogle Scholar
  7. Chan N, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290CrossRefGoogle Scholar
  8. Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30:911–923CrossRefGoogle Scholar
  9. Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M (1995) Bioerosion rates on coral reefs: interactions between macroborers, microborers and grazers (Moorea, French Polynesia). Palaeo3 113:189–198CrossRefGoogle Scholar
  10. Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M, Cuet P (2002) The effects of eutrophication-related alterations to coral reef communities on agents and rates of bioerosion (Reunion Island, Indian Ocean). Coral Reefs 21:375–390Google Scholar
  11. Comeau S, Carpenter RC, Lantz CA, Edmunds PJ (2015) Ocean acidification accelerates dissolution of experimental coral reef communities. Biogeosciences 12:365–372CrossRefGoogle Scholar
  12. Cyronak T, Schulz KG, Santos IR, Eyre BD (2014) Enhanced acidification of global coral reefs driven by regional biogeochemical feedbacks. Geophys Res Lett 41:5538–5546CrossRefGoogle Scholar
  13. Dickson AG (1990) Standard potential of the reaction: AgCl(s) + ½ H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127CrossRefGoogle Scholar
  14. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Pub 3:1–191Google Scholar
  15. Enochs IC, Manzello DP, Tribollet A et al (2016) Elevated colonization of microborers at a volcanically acidified coral reef. PLoS ONE 11:e0159818CrossRefGoogle Scholar
  16. Eyre BD, Andersson AJ, Cyronak T (2014) Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat Clim Change 4:969–976CrossRefGoogle 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. Falter JL, Lowe RJ, Atkinson MJ, Cuet P (2012) Seasonal coupling and de-coupling of net calcification rates from coral reef metabolism and carbonate chemistry at Ningaloo Reef. Western Australia. J Geophys Res 117:C05003CrossRefGoogle Scholar
  19. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366CrossRefGoogle Scholar
  20. Garcia-Pichel F, Ramírez-Reinat E, Gao Q (2010) Microbial excavation of solid carbonates powered by P-type ATPase-mediated transcellular Ca2+ transport. PNAS 107:21749–21754CrossRefGoogle Scholar
  21. 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 39:160–183CrossRefGoogle Scholar
  22. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Res 51:475–478Google Scholar
  23. Grange JS, Rybarczyk H, Tribollet A (2015) The three steps of the carbonate biogenic dissolution process by microborers in coral reefs (New Caledonia). Environ Sci Pollut Res 22:13625–13637CrossRefGoogle Scholar
  24. Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann N Y Acad Sci 1134:320–342CrossRefGoogle Scholar
  25. Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17:2488–2497CrossRefGoogle Scholar
  26. Hoskin CM, Reed JK, Mook DH (1986) Production and off-bank transport of carbonate sediment, Black Rock, southwest Little Bahama Bank. Mar Geol 73:125–144CrossRefGoogle Scholar
  27. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J Phycol 45:1236–1251CrossRefGoogle Scholar
  28. Johnson MD, Price NN, Smith JE (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411CrossRefGoogle Scholar
  29. Kinsey DW (1978) Productivity and calcification estimates using slack-water periods and field enclosures. In: Stoddart DR, Johannes RE (eds) Monographs on oceanographic methodology, Coral reefs: research methods. UNESCO, pp 439–468Google Scholar
  30. Kobluk DR, Risk MJ (1977) Calcification of exposed filaments of endolithic algae, micrite envelope formation and sediment production. J Sediment Res 47:517–528Google Scholar
  31. Krumins V, Gehlen M, Arndt S, Cappellen PV, Regnier P (2013) Dissolved inorganic carbon and alkalinity fluxes from coastal marine sediments: model estimates for different shelf environments and sensitivity to global change. Biogeosciences 10:371–398CrossRefGoogle Scholar
  32. Kuffner IB, Andersson AJ, Jokiel PL, Kuulei SR, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114CrossRefGoogle Scholar
  33. 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
  34. Le Campion-Alsumard T, Golubic S, Hutchings PA (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol Progress Ser 117:149–157CrossRefGoogle Scholar
  35. Milliman JD (1993) Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Glob Biogeochem Cycles 7:927–957CrossRefGoogle Scholar
  36. Morse JW (1983) The kinetics of calcium carbonate dissolution and precipitation. Rev Miner Geochem 11:227–264Google Scholar
  37. Noisette F, Duong G, Six C, Davoult D, Martin S (2013) Effects of elevated pCO2 on the metabolism of a temperate rhodolith Lithothamnion corallioides grown under different temperatures. J Phycol 49:746–757CrossRefGoogle Scholar
  38. Nothdurft LD, Webb GE (2009) Earliest diagenesis in scleractinian coral skeletons: implications for palaeoclimate-sensitive geochemical archives. Facies 55:161–201CrossRefGoogle Scholar
  39. Nothdurft LD, Webb GE, Bostrom T, Rintoul L (2007) Calcite-filled borings in the most recently deposited skeleton in live-collected Porites (Scleractinia): implications for trace element archives. Geochim Cosmochim Acta 71:5423–5438CrossRefGoogle Scholar
  40. Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686CrossRefGoogle Scholar
  41. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422CrossRefGoogle Scholar
  42. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105 Carbon Dioxide Information Analysis CenterGoogle Scholar
  43. Radtke G (1993) The distribution of microborings in molluscan shells from recent reef environments at Lee Stocking Island, Bahamas. Facies 29:81–92CrossRefGoogle Scholar
  44. Reyes-Nivia C, Diaz-Pulido G, Kline D, Guldberg OH, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Glob Change Biol 19:1919–1929CrossRefGoogle Scholar
  45. Reyes-Nivia C, Diaz-Pulido G, Dove S (2014) Relative roles of endolithic algae and carbonate chemistry variability in the skeletal dissolution of crustose coralline algae. Biogeosciences 11:4615–4626CrossRefGoogle Scholar
  46. Roy RN, Roy LN, Vogel KM et al (1993) The dissociation constants of carbonic acid in seawater at salinities 5–45 and temperatures 0–45 °C. Mar Chem 44:249–267CrossRefGoogle Scholar
  47. Sabine CL, Feely RA, Gruber N et al (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371CrossRefGoogle Scholar
  48. Schönberg CH, Fang JK, Carreiro-Silva M, Tribollet A, Wisshak M (2017) Bioerosion: the other ocean acidification problem. ICES J Mar Sci 74:895–925CrossRefGoogle Scholar
  49. Shamberger KEF, Feely RA, Sabine CL et al (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75CrossRefGoogle Scholar
  50. Shashar N, Stambler N (1992) Endolithic algae within corals-life in an extreme environment. JEMBE 163:277–286CrossRefGoogle Scholar
  51. Shaw EC, McNeil BI, Tilbrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res 117:C03038CrossRefGoogle Scholar
  52. Silverman J, Lazar B, Erez J (2007) Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82CrossRefGoogle Scholar
  53. Stocker TF, Qin D, Plattner GK et al (2013) Technical summary. In: Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge, UK and New York, NY, USA: Cambridge University Press, pp 33–115Google Scholar
  54. Stubler AD, Peterson BJ (2016) Ocean acidification accelerates net calcium carbonate loss in a coral rubble community. Coral Reefs 35:795–803CrossRefGoogle Scholar
  55. Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters. Wiley, New YorkGoogle Scholar
  56. Taylor AR, Chrachri A, Wheeler G, Goddard H, Brownlee C (2011) A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. PLoS Biol 9:e1001085CrossRefGoogle Scholar
  57. Tribollet A (2008a) Dissolution of dead corals by euendolithic microorganisms across the northern Great Barrier Reef (Australia). Microbial Ecol 55:569–580CrossRefGoogle Scholar
  58. Tribollet A (2008b) The boring microflora in modern coral reef ecosystems: a review of its roles. In: Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer, Berlin, pp 67–94CrossRefGoogle Scholar
  59. Tribollet A, Golubic S (2005) Cross-shelf differences in the pattern and pace of bioerosion of experimental carbonate substrates exposed for 3 years on the northern Great Barrier Reef, Australia. Coral Reefs 24:422–434CrossRefGoogle Scholar
  60. Tribollet A, Payri C (2001) Bioerosion of coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea French Polynesia. Oceanol Acta 24:329–342CrossRefGoogle Scholar
  61. Tribollet A, Langdon C, Golubic S, Atkinson M (2006) Endolithic microflora are major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292–303CrossRefGoogle Scholar
  62. Tribollet A, Godinot C, Atkinson M, Langdon C (2009) Effects of elevated pCO2 on dissolution of coral carbonates by microbial euendoliths. Glob Biogeochem Cycles 23(3):3008CrossRefGoogle Scholar
  63. Tribollet A, Golubic S, Radtke G, Reitner J (2011) On microbiocorrosion. In: Reitner J, Queric N-V, Arp G (eds) Advances in geobiology of stromatolite formation, vol 131. Lecture Notes in Earth Sciences. Springer, Heidelberg, pp 265–276CrossRefGoogle Scholar
  64. Trnovsky D, Stoltenberg L, Cyronak T, Eyre BD (2016) Antagonistic effects of ocean acidification and rising sea surface temperature on the dissolution of coral reef carbonate sediments. Front Mar Sci. CrossRefGoogle Scholar
  65. Tudhope AW, Risk MJ (1985) Rate of dissolution of carbonate sediments by microboring organisms, Davies Reef, Australia. J Sediment Res 55:440–447Google Scholar
  66. Vogel K, Gektidis M, Golubic S, Kiene WE, Radtke G (2000) Experimental studies on microbial bioerosion at Lee Stocking Island, Bahamas and One Tree Island, Great Barrier Reef, Australia: implications for paleoecological reconstructions. Lethaia 33:190–204CrossRefGoogle Scholar
  67. Vooren CM (1981) Photosynthetic rates of benthic algae from the deep coral reef of Curacao. Aquat Bot 10:143–159CrossRefGoogle Scholar
  68. Wisshak M, Tribollet A, Golubic S, Jakobsen J, Freiwald A (2011) Temperate bioerosion: ichnodiversity and biodiversity from intertidal to bathyal depths (Azores). Geobiology 9:492–520CrossRefGoogle Scholar
  69. Wisshak M, Schönberg CH, Form A, Freiwald A (2012) Ocean acidification accelerates reef bioerosion. PLoS ONE 7:e45124CrossRefGoogle Scholar
  70. Wu H, Dissard D, Douville E, Blamart D, Bordier L, Tribollet A, Le Cornec F, Pons-Branchu E, Dapoigny A, Lazareth CE (2018) Surface ocean pH variations since 1689 CE and recent ocean acidification in the tropical South Pacific. Nat Commun 9:2543. CrossRefGoogle Scholar
  71. Yates KK, Halley RB (2006) CO3 2− concentration and pCO2 thresholds for calcification and dissolution on the Molokai reef flat, Hawaii. Biogeosci Discuss 3:123–154CrossRefGoogle Scholar
  72. Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, phaeophyta) grown at low and high N supplies. J Phycol 47:87–97CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Centre IRD de Nouméa, UMR LOPBNouméa CedexNouvelle-Calédonie
  2. 2.UMR ENTROPIE (UMR450 IRD, CNRS, Université de La Réunion) UMR9220Saint-Denis de la RéunionFrance
  3. 3.Laboratoire d’Excellence CORAIL, Université de La RéunionSaint-Denis Cedex 9France
  4. 4.IRD-Sorbonne Universités (Univ. Paris, UPMC-CNRS-MNHN), Laboratoire IPSL-LOCEANParis CedexFrance

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