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The three steps of the carbonate biogenic dissolution process by microborers in coral reefs (New Caledonia)

  • Microbial Ecology of the Continental and Coastal Environments
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Abstract

Biogenic dissolution of carbonates by microborers is one of the main destructive forces in coral reefs and is predicted to be enhanced by eutrophication and ocean acidification by 2100. The chlorophyte Ostreobium sp., the main agent of this process, has been reported to be one of the most responsive of all microboring species to those environmental factors. However, very little is known about its recruitment, how it develops over successions of microboring communities, and how that influences rates of biogenic dissolution. Thus, an experiment with dead coral blocks exposed to colonization by microborers was carried out on a reef in New Caledonia over a year period. Each month, a few blocks were collected to study microboring communities and the associated rates of biogenic dissolution. Our results showed a drastic shift in community species composition between the 4th and 5th months of exposure, i.e., pioneer communities dominated by large chlorophytes such as Phaeophila sp. were replaced by mature communities dominated by Ostreobium sp. Prior the 4th month of exposure, large chlorophytes were responsible for low rates of biogenic dissolution while during the community shift, rates increased exponentially (×10). After 6 months of exposure, rates slowed down and reached a “plateau” with a mean of 0.93 kg of CaCO3 dissolved per m2 of reef after 12 months of exposure. Here, we show that (a) Ostreobium sp. settled down in new dead substrates as soon as the 3rd month of exposure but dominated communities only after 5 months of exposure and (b) microbioerosion dynamics comprise three distinct steps which fully depend on community development stage and grazing pressure.

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References

  • Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann Rev Mar Sci 5:321–348

    Article  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446

    Article  CAS  Google Scholar 

  • Bornet E, Flahault C (1889) Sur quelques plantes vivant dans le test calcaire des mollusques. Bull de la Société Botanique de France 36:CXLVII–CLXXVI

    Article  Google Scholar 

  • Bruggemann JH, Vanoppen MJH, Breeman AM (1994) Foraging by the stoplight Parrotfish Sparisoma viride. 1. Food selection in different, socially determined habitats. Mar Ecol Prog Ser 106:41–55

    Article  Google Scholar 

  • Bucher DJ, Harriott VJ, Roberts LG (1998) Skeletal micro-density, porosity and bulk density of acroporid corals. J Exp Mar Biol Ecol 228:117–136

    Article  Google Scholar 

  • Carreiro-Silva M, McClanahan TR, Kiene WE (2005) The role of inorganic nutrients and herbivory in controlling microbioerosion of carbonate substratum. Coral Reefs 24:214–221

    Article  Google Scholar 

  • Carreiro-Silva M, Kiene WE, Golubic S, McClanahan TR (2012) Phosphorus and nitrogen effects on microbial euendolithic communities and their bioerosion rates. Mar Pollut Bull 64:602–613

    Article  CAS  Google Scholar 

  • Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30:911–923

    Article  Google Scholar 

  • Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M (1995) Bioerosion rates on coral reefs: interactions between macroborers, microborers and grazers (Moorea, French Polynesia). Palaeogeogr Palaeoclimatol Palaeoecol 113:189–198

    Article  Google Scholar 

  • 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 21:375–390

    Google Scholar 

  • Edinger EN, Limmon GV, Jompa J, Widjatmoko W, Heikoop JM, Risk MJ (2000) Normal coral growth rates on dying reefs: are coral growth rates good indicators of reef health? Mar Pollut Bull 40:404–425

    Article  CAS  Google Scholar 

  • Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68

    Article  Google Scholar 

  • Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208:75–81

    Article  Google Scholar 

  • Fork DC, Larkum AWD (1989) Light harvesting in green-alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar Biol 103:381–385

    Article  Google Scholar 

  • Garcia-Pichel F, Ramirez-Reinat E, Gao QJ (2010) Microbial excavation of solid carbonates powered by P-type ATPase-mediated transcellular Ca2+ transport. Proc Natl Acad Sci U S A 107:21749–21754

    Article  CAS  Google Scholar 

  • Gektidis M (1999) Development of microbial euendolithic communities: the influence of light and time. Bull Geol Soc Den 45:147–150

    Google Scholar 

  • Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland C (ed) Life and Death Of Coral Reefs. Chapman and Hall, USA, pp 68–98

    Chapter  Google Scholar 

  • Golubic S, Brent G, Le Campion-Alsumard T (1970) Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting-embedding technique. Lethaia 3:203–209

    Article  Google Scholar 

  • Grothendieck G (2013): nls2: non-linear regression with brute force

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  Google Scholar 

  • Hollander M, Douglas AV, Chicken E (2014) Nonparametric statistical methods. Hoboken, New Jersey

    Google Scholar 

  • Huand D (2012) Threatened reef corals of the world. Plos One 7

  • Jessen C, Voolstra CR, Wild C (2014) In situ effects of simulated overfishing and eutrophication on settlement of benthic coral reef invertebrates in the Central Red Sea. Peer J 2:e339

    Article  Google Scholar 

  • Kiene WE, Hutchings PA (1994) Bioerosion experiments at Lizard-Island, Great Barrier Reef. Coral Reefs 13:91–98

    Article  Google Scholar 

  • Kiene W, Radtke G, Gektidis M, Golubic S, Vogel K (1995): Factors controlling the distribution of microborers in Bahamian Reef environments. In: Schuhmacher H, Kiene W, Dullo WC (Editors), Factors controlling Holocene reef growth: an interdisciplinary approach. Facies, pp. 174–188

  • Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral reef biodiversity. In: McIntyre A (ed) Life in the world’s oceans: diversity, distribution, and abundance. Wiley-Blackwell, Oxford, pp 65–77

    Chapter  Google Scholar 

  • Lazar B, Loya Y (1991) Bioerosion of coral reefs—a chemical approach. Limnol Oceanogr 36:377–383

    Article  CAS  Google Scholar 

  • Le Campion-Alsumard T (1975) Experimental study of the colonization of calcite fragments by marine endolithic Cyanophyceae. Cah Biol Mar 16:177–185

    Google Scholar 

  • Le Campion-Alsumard T, Golubic S, Hutchings P (1995) Microbial endoliths in skeletons of live and dead corals—Porites lobata (Moorea, French Polynesia). Mar Ecol Prog Ser 117:149–157

  • Lukas KJ (1978) Depth distribution and form among common microboring algae from the Florida continental shelf. Geol Soc Am Abstr Prog 10:1–448

    Google Scholar 

  • Murtagh F, Legendre P (2014) Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? J Classif 31:274–295

    Article  Google Scholar 

  • Neumann AC (1966) Observations on coastal erosion in Bermuda and measurements of boring rate of sponge Cliona lampa. Limnol Oceanogr 11:92–108

    Article  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  Google Scholar 

  • Pari N, Peyrot-Clausade M, Le Campion-Alsumard T, Hutchings P, Chazottes V, Golubic S, Le Campion J, Fontaine MF (1998) Bioerosion of experimental substrates on high islands and on atoll lagoons (French Polynesia) after two years of exposure. Mar Ecol Prog Ser 166:119–130

    Article  Google Scholar 

  • Peyrot-Clausade M, Le Campion-Alsumard T, Hutchings P, Le Campion J, Payri C, Fontaine MC (1995) Initial bioerosion and bioaccretion on experimental substrates in high island and atoll lagoons (French Polynesia). Oceanol Acta 18:531–541

    CAS  Google Scholar 

  • R. Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Radtke G, le Campion-Alsumard T, Golubic S (1996) Microbial assemblages of the bioerosional “notch” along tropical limestone coasts. Algol Stud 83:469–482

    Google Scholar 

  • Reyes-Nivia C, Diaz-Pulido G, Kline D, Guldberg O-H, Dove S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Glob Chang Biol 19:1919–1929

    Article  Google Scholar 

  • Schneider J, Torunski H (1983) Biokarst on limestone coasts, morphogenesis and sediments production. Mar Ecol 4:45–63

    Article  Google Scholar 

  • Schonberg CHL (2001) Small-scale distribution of great barrier reef bioeroding sponges in shallow water. Ophelia 55:39–54

    Article  Google Scholar 

  • Scoffin P, Alexandersson E, Bowes G, Clokie J, Farrow G, Milliman J (1980) Recent, temperate, sub-photic, carbonate sedimentation: Rockall bank, Northeast Atlantic. J Sediment Res 50:331–355

    Google Scholar 

  • Tribollet A (2008a) Dissolution of dead corals by euendolithic microorganisms across the northern Great Barrier Reef (Australia). Microb Ecol 55:569–580

    Article  Google Scholar 

  • Tribollet A (2008b) The boring microflora in modern coral reef ecosystems: a review of its roles. Current Developments in Bioerosion, 67–94

  • 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 24:422–434

    Article  Google Scholar 

  • Tribollet A, Golubic S (2011) Reef bioerosion: agents and processes. In: Dubisnky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Berlin Heidelberg, pp 435–450

    Chapter  Google Scholar 

  • Tribollet A, Decherf G, Hutchings PA, Peyrot-Clausade M (2002) Large-scale spatial variability in bioerosion of experimental coral substrates on the Great Barrier Reef (Australia): importance of microborers. Coral Reefs 21:424–432

    Google Scholar 

  • 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 42:292–303

    Article  CAS  Google Scholar 

  • 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

  • Tribollet A, Atkinson M, Cuet P, Chauvin A (2014) Production of seawater alkalinity by bioeroding microflora increases with ocean acidification, Ocean Sciences Meeting, Honolulu, Hawaii, USA

  • Vogel K, Gektidis M, Golubic S, Kiene W, 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 33:190–204

    Article  Google Scholar 

  • Wilkinson C (2008): Status of coral reefs of the world: 2008, Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, Australia

  • Wisshak M, Tribollet A, Golubic S, Jakobsen J, Freiwald A (2011) Temperate bioerosion: ichnodiversity and biodiversity from intertidal to bathyal depths (Azores). Geobiology 9:492–520

    Article  CAS  Google Scholar 

  • Wisshak M, Schoenberg CHL, Form A, Freiwald A (2014) Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgol Mar Res 68:253–262

    Article  Google Scholar 

  • Zundelevich A, Lazar B, Ilan M (2007) Chemical versus mechanical bioerosion of coral reefs by boring sponges—lessons from Pione cf. vastifica. J Exp Biol 210:91–96

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to deeply thank John Butscher and the diving team of IRD located in New Caledonia (Center of IRD, Nouméa), especially Armelle Renaud and Bertrand Bourgeois, for helping us on the field. We thank Cécile Dupouy for in situ CTD measurements. We thank Sandrine Caquineau for helping us on how to use the scanning electronic microscope on the ALIZES facility (IRD-UPMC), which was funded by the Région Ile-de-France. We also thank Stjepko Golubic for discussions and help with euendolith identification. Finally, we thank the Institut National des Sciences de l’Univers (INSU)—EC2CO (Microbien and PNEC programs), the Institut de Recherche pour le Développement, and the Grand Observatoire de l’Environnement et de la Diversité Terrestre et Marine du Pacifique Sud (GOPS) for funding this project.

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  1. IRD-Sorbonne Universités (Univ. Paris 6) UPMC-CNRS-MNHN, Laboratoire IPSL-LOCEAN, 32 Avenue Henri Varagnat, 93143, Bondy, France

    J. S. Grange & A. Tribollet

  2. MNHN-Sorbonne Universités (Univ. Paris 6) UPMC-CNRS-IRD, Laboratoire BOREA, 61 rue Buffon, 75005, Paris, France

    H. Rybarczyk

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  1. J. S. Grange
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Correspondence to J. S. Grange.

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Grange, J.S., Rybarczyk, H. & Tribollet, A. The three steps of the carbonate biogenic dissolution process by microborers in coral reefs (New Caledonia). Environ Sci Pollut Res 22, 13625–13637 (2015). https://doi.org/10.1007/s11356-014-4069-z

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