Skip to main content

The boring microflora in modern coral reef ecosystems: a review of its roles

  • Chapter
Current Developments in Bioerosion

Part of the book series: Erlangen Earth Conference Series ((ERLANGEN))

Abstract

Euendolithic microorganisms (boring microflora) – cyanobacteria, algae and fungi – colonize all carbonate substrates in modern coral reefs and are distributed worldwide. Recent studies showed that in dead carbonate, they are important primary producers and are fed upon by various excavating invertebrate and vertebrate grazers, contributing greatly to biodestruction processes (bioerosion) and sedimentation. Additionally, it has been shown that in some live calcifying organisms, they either inflict damages to live tissues or provide a benefit to the host, depending on the euendolithic community involved (parasitic or mutualistic relationships). Based on those recent studies, the following question is raised: Are euendoliths key organisms in the functioning and maintenance of coral reefs? Reviewed literature includes studies on (1) the mechanisms used by euendoliths to penetrate into carbonate substrates (production of acids or chelating fluids; use of the products of photosynthesis / respiration and / or calcium pumps), (2) their roles in reef bioerosion and sedimentation (major roles), (3) their metabolism (important rates of production), (4) their interactions with their live hosts (symbiosis, mutualism and / or parasitism) and (5) the effects of various environmental factors such as eutrophication, sedimentation and rising atmospheric pCO2 on euendolith activities. The review concentrates on modern coral reef ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adey WH (1998) Review. Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393-406

    Article  Google Scholar 

  • Agardh CA (1824) Systema algarum. Berling, Lund, 312 pp

    Google Scholar 

  • Alexandersson ET (1975) Marks of unknown carbonate-decomposing organelles in cyanophyte borings. Nature 254:237-238

    Article  Google Scholar 

  • Alker AP, Smith GW, Kiho K (2001) Characterization of Aspergillus sydowii(Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiol 460:105-111

    Article  Google Scholar 

  • Al-Thukair AA, Golubic S (1991) New endolithic cyanobacteria from the Arabian Gulf. I. Hyella immanissp. nov. J Phycol 27:766-780

    Article  Google Scholar 

  • Anagnostidis K, Pantazidou A (1988) Hyella kalligrammos sp. nov., Hyella maxima (Geitl.) comb. nov., and other freshwater morphotypes of the genus Hyella Born. et Flah. (Chroococcales, Cyanophyceae). Algol Stud 50/53:227-247

    Google Scholar 

  • Anderson AJ, Mackenzie FT, May Ver L (2003) Solution of shallow-water carbonates: An insignificant buffer against rising atmospheric CO2. Geol Soc Amer 31:513-516

    Google Scholar 

  • Ascaso C, Wierzchos J, Castello R (1998) Study of the biogenic weathering of calcareous litharenite stones caused by lichen and endolithic microorganisms. Int Biodeterior Biodegrad 42:29-38

    Article  Google Scholar 

  • Batters EAL (1902) A catalog of the Bristish marine algae. J Bot, Brit and Foreign 40 (Suppl):1-107

    Google Scholar 

  • Bellamy N, Risk MJ (1982) Coral gas: oxygen production in Millepora on the Great Barrier Reef. Science 215:1618-1619

    Article  Google Scholar 

  • Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254-260

    Article  Google Scholar 

  • Bornet E, Flahault C (1888) Note sur deux nouveaux genres d’algues perforantes. J Bot Morot 2:161-165

    Google Scholar 

  • Bornet E, Flahault C (1889) Sur quelques plantes vivant dans le test calcaire des mollusques. Bull Soc Bot France 36:147-177

    Google Scholar 

  • Borowitzka MA (1981) Photosynthesis and calcification in the articulated coralline algae Amphiroa anceps and A. foliaceaa. Mar Biol 62:17-23

    Article  Google Scholar 

  • Bruggemann JH, van Oppen MJH, Breeman AN (1994) Foraging by the spotlight parrotfish Sparisoma viride. I. Food selection in different, socially determined habitats. Mar Ecol Prog Ser 106:41-55

    Article  Google Scholar 

  • Campbell SE (1980) Palaeoconchocelis starmachii, a carbonate boring microfossil from the upper Silurian of Poland (425 millions years old): implications for the evolution of the Bangiaceae (Rhodophyta). Phycologia 19:25-36

    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 

  • Casareto B, Suzuki Y, Ishikawa Y, Kurosawa K (2004) Benthic primary production and N2 fixation in a fringing coral reef at Miyako Island, Okinawa, Japan. Proc 10th Int Coral Reef Symp, Okinawa, Japan, Abstr, p 192

    Google Scholar 

  • Chacón E, Berrendero E, Garcia-Pichel F (2006) Biological signatures of microboring cyanobacterial communities in marine carbonates from Cabo Rojo, Puerto Rico. Sediment Geol 185:215-228

    Article  Google Scholar 

  • Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M (1995) Bioerosion rates on coral reefs: interaction 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 

  • Dana JD (1846) Notice of some genera of Coclopacea. Amer J Sci Arts 1:225-230

    Google Scholar 

  • De Angelis d’Ossat G (1908) Altri Zoantari del Terziario della Patagonia. An Mus Nac Buenos Aires 3:93-102

    Google Scholar 

  • De Los Rios A, Wierzchos J, Sancho LG, Green TGA, Ascaso C (2005) Ecology of endolithic lichens colonizing granite in continental Antarctica. Lichenologist 37:383-395

    Article  Google Scholar 

  • Domart-Coulon IJ, Sinclair CS, Hill RT, Tambutté S, Purevel S, Ostrander GK (2004) A basidiomycete isolated from the skeleton of Pocillopora damicornis (Scleractinia) selectively stimulates short-term survival of coral skeletogenic cells. Mar Biol 144:583-592

    Article  Google Scholar 

  • Domart-Coulon IJ, Traylor-Knowles N, Peters E, Elbert D, Downs CA, Price K, Stubbs J, McLaughlin S, Cox E, Aeby G, Brown PR, Ostrander GK (2006) Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa. Coral Reefs 25:531-543

    Article  Google Scholar 

  • Eakin CM (1996) Where have all the carbonates gone? A model comparison of calcium carbonate budgets before and after the 1982-1983 El Niñio at Uva Island in the eastern Pacific. Coral Reefs 15:109-119

    Google Scholar 

  • Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices, and changes through time. Mar Poll Bull 36:617-630

    Article  Google Scholar 

  • Edinger EN, Limmon GV, Jompa J, Widjatmoko W, Heikoop J, Risk M (2000) Normal coral growth rates on dying reefs: Are coral growth rates good indicators of reef health? Mar Poll Bull 40:404-425

    Article  Google Scholar 

  • Edwards HGM, Russell NC, Wynn-Williams DD (1997) Fourier transform raman spectroscopic and scanning electron microscopic study of cryptoendolithic lichen from Antarctica. J Raman Spectrosc 28:685-690

    Article  Google Scholar 

  • Ehrenberg CG (1834) Beiträge zur physiologischen Kenntniss der Corallenthiere im allgemeinen, und besonders des Rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abh K Akad Wiss Berlin, Phys Math, 1832:225-380

    Google Scholar 

  • Ellis J, Solander D (1786) The natural history of many curious and uncommon zoophytes. White and Son, London, 208 pp

    Google Scholar 

  • Enriquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025-1032

    Google Scholar 

  • Ercogovic A (1927) Tri nova roda litofiskih cijanoiceja sa jadranske obale. Acta Bot 2:78-84

    Google Scholar 

  • Ercegovic A (1930) Sur quelques types peu connus de Cyanophycées lithophytes. Arch Protistenkd 71:361-373

    Google Scholar 

  • Ferrer LM, Szmant AM (1988) Nutrient regeneration by the endolithic communities in coral skeletons. Proc 6th Int Coral Reef Symp, Townsville, Australia, 3:1-4

    Google Scholar 

  • Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc Roy Soc London 269:1205-1210

    Article  Google Scholar 

  • Fine M, Zibrowius H, Loya Y (2001) Oculina patagonica, a non lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195-1203

    Article  Google Scholar 

  • Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Fresh Res 55:115-121

    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 Exper Biol 208:75-81

    Article  Google Scholar 

  • Fine M, Roff G, Ainsworth TD, Hoegh-Guldberg O (2006) Phototrophic microendoliths bloom during coral “white syndrome”. Coral Reefs 25:577-581

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Friedmann EI, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacterial communities of the Ross Desert, Antarctica. Polarforschung 58:215-259

    Google Scholar 

  • Garcia-Pichel F (2006) Plausible mechanisms for the boring on carbonates by microbial phototrophs. Sediment Geol 185:205-213

    Article  Google Scholar 

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

    Google Scholar 

  • Gektidis M, Golubic S (1996) A new endolithic cyanophyte / cyanobacterium: Hyella vacans sp. nov. from Lee Stocking Island, Bahamas. Nova Hedwigia, Beih 112:93-100

    Google Scholar 

  • Ghirardelli LA (2002) Endolithic microorganisms in live and dead thalli of coralline red algae (Corallinales, Rhodophyta) in the northern Adriatic Sea. Acta Geol Hisp 37:53-60

    Google Scholar 

  • Glaub I, Vogel K (2004) The stratigraphic record of microborings. Fossils Strata 51:126-135

    Google Scholar 

  • Golubic S, Schneider J (2003) Microbial endoliths as internal biofilms. In: Krumbein WE, Dornieden T, Volkmann M (eds) Fossil and Recent biofilms. Kluwer, Dordrecht, pp 249-263

    Google Scholar 

  • Golubic S, Perkins RD, Lukas KJ (1975) Boring microoganisms and microborings in carbonate substrates. In: Frey RW (ed) The study of trace fossils. Springer, New York, pp 229-259

    Google Scholar 

  • Golubic S, Knoll AH, Ran W (1980) Morphometry of late Ordovician microbial borings. Tech Summa Abstr AAPG Bull 64:713

    Google Scholar 

  • Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. Sediment Geol 51:475-478

    Google Scholar 

  • Golubic S, Campbell SE, Drobne K, Cameron B, Balsam WL, Cimerman F, Dubois L (1984) Microbial endoliths: a benthic overprint in the sedimentary record, and a paleobathymetric cross-reference with foraminifera. J Paleontol 58:351-361

    Google Scholar 

  • Golubic S, Hernandez-Marine M, Hoffmann L (1996) Developmental aspects of branching in filamentous Cyanophyta / Cyanobacteria. Algol Stud 83:303-329

    Google Scholar 

  • Golubic S, Radtke G, Le Campion-Alsumard T (2005) Endolithic fungi in marine ecosystems. Trends Microbiol 13:229-235

    Article  Google Scholar 

  • Gomont M (1892) Monographie des Oscillariees (Nostocacees homocystees) Ann Sci Nat Bot 15:263-368

    Google Scholar 

  • Goreau TJ, Cervino J, Goreau M, Hayes R, Hayes M, Richardson L, Smith G, DeMeyer K, Nagelkerken I, Garzon-Ferrera J, Gil D, Garrison G, Williams EH, Bunkley-Williams L, Quirrolo C, Patterson K, Porter JW, Porter K (1998) Rapid spread diseases in Caribbean coral reefs. Rev Biol Trop 46 (Suppl 5):157-171

    Google Scholar 

  • Halldal P (1968) Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol Bull 134: 411-424

    Article  Google Scholar 

  • Halley RB, Yates KK, Brock JC (2005) South Florida coral-reef sediment dissolution in response to elevated CO2. Proc 10th Int Coral Reef Symp, Okinawa, Japan, Abstr, p 178

    Google Scholar 

  • Hallock P (2005) Global change and modern coral reefs: New opportunities to understand shallow-water carbonate depositional processes. Sediment Geol 175:19-33

    Article  Google Scholar 

  • Harborne AR, Mumby PJ, Micheli F, Perry CT, Dahlgren CP, Holmes KE, Brumbaugh DR (2006) The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes. Adv Mar Biol 50:57-189

    Article  Google Scholar 

  • Harmelin-Vivien ML (1994) The effects of storms and cyclones on coral reefs: a review. J Coast Res Spec Issue 12:221-231

    Google Scholar 

  • Hauck F (1876) Verzeichnis der im Golf von Triest gesammelten Meeralgen (Fortsetzung). Österr Bot Z 26:24-26 and 54-57

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change coral bleaching and the future of the world‘s coral reefs. Greenpeace, 27 pp, http://cmbc.ucsd.edu/content/1/docs/hoegh-gulberg.pdf

    Google Scholar 

  • Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and elevated sea-level temperatures: bleaching of outer-reef slope communities in Moorea, French Polynesia. Mar Ecol Prog Ser 121:181-190

    Article  Google Scholar 

  • Hoffmann L (1999) Marine cyanobacteria in tropical regions: diversity and ecology. Europ J Phycol 34:371-379

    Google Scholar 

  • Houghton JT, Meira Filho LG, Callander BA, Harris N, Kattenberg A, Maskell K (1996) Climate change 1995. The science of climate change. Cambridge Univ Press, Cambridge, 306 pp

    Google Scholar 

  • Hubbard DK, Sadd JL, Miller AI, Gill IP, Dill RF (1981) The production, transportation and deposition of carbonate sediments on the insular shelf of St Croix, U.S. Virgin Island. West Indies Lab Rep Contrib N°76

    Google Scholar 

  • Hutchings PA (1986) Biological destruction of coral reefs. Coral Reefs 4:239-252

    Article  Google Scholar 

  • Jones B, Goodbody QH (1982) The geological significance of endolithic algae in glass. Canad J Earth Sci 19:671-678

    Google Scholar 

  • Kaehler S, McQuaid CD (1999) Lethal and sublethal effects of phototrophic endoliths attacking the shell of the intertidal mussel Perna perna. Mar Biol 13:497-503

    Article  Google Scholar 

  • Kanwisher JW, Wainwright SA (1967) Oxygen balance in some reef corals. Biol Bull 133:378-390

    Article  Google Scholar 

  • Kendrick B, Risk MJ, Michaelides J, Bergman K (1982) Amphibious microborers: bioeroding fungi isolated from live corals. Bull Mar Sci 32:862-867

    Google Scholar 

  • Kiene WE (1997) Enriched nutrients and their impact on bioerosion: results from ENCORE. Proc 8th Int Coral Reef Symp, Panama, 11:897-902

    Google Scholar 

  • Kiene WE, Radtke G, Gektidis M, Golubic S, Vogel K (1995) Factors controlling the distribution of microborers in Bahamian reef environments. Facies 32:145-188

    Article  Google Scholar 

  • Kinsey DW (1985) Metabolism, calcification and carbon production. I. Systems level studies. Proc 5th Int Coral Reef Congr, Tahiti, 4:505-526

    Google Scholar 

  • Klement KW, Toomey DF (1967) Role of bluegreen alga Girvanella in skeletal grain destruction and lime-mud formation in the lower Ordovician of west Texas. J Sediment Petrol 37:1045-1051

    Google Scholar 

  • Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118-120

    Article  Google Scholar 

  • Kleypas JA, Buddemeier RW, Gattuso JP (2001) The future of coral reefs in an age of global change. Int J Earth Sci 90:426-437

    Article  Google Scholar 

  • Knoll AH, Golubic S, Green J, Swett K (1986) Organically preserved microbial endoliths from the late Proterozoic of East Greenland. Nature 321:865-857

    Google Scholar 

  • Kobluk DR, Kahle CF (1977) Bibliography of the endolithic (boring) algae and fungi and related geologic processes. Bull Canad Petrol Geol 25:208-223

    Google Scholar 

  • Kobluk DR, Risk M (1977) Calcification of exposed filaments of endolithic algae, micrite envelope formation and sediment production. J Sediment Petrol 47:517-528

    Google Scholar 

  • Koehne B, Elli G, Jennings RC, Wilhelm C, Trissl HW (1999) Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim Biophys Acta 1412:94-107

    Article  Google Scholar 

  • Königshof P, Glaub I (2004) Traces of microboring organisms in Palaeozoic conodont elements. Geobios 37:416-424

    Article  Google Scholar 

  • Komárek J, Anagnostidis K (1999) Cyanoprokaryota 1. Chroococcales. In: Ettl H, Gärtner G, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa. Spektrum Akad Verl, Fischer, Jena, 19:1-548

    Google Scholar 

  • Komárek J, Anagnostidis K (2005) Cyanoprokaryota 2. Oscillatoriales. In: Büdel B, Gärtner G, Krienitz L, Schagerl M (eds) Süsswasserflora von Mitteleuropa. Elsevier, Spektrum Akad Verl, München, 19:1-759

    Google Scholar 

  • Kushmaro A, Rosenberg E, Fine M, Loya Y (1997) Bleaching of coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 147:159-165

    Article  Google Scholar 

  • Laborel J, Le Campion-Alsumard T (1979) Infestation massive du squelette de coraux vivants par des Rhodophycées de type Conchocelis. C R Acad Sci Paris 288:1575-1577

    Google Scholar 

  • Lagerheim G (1886) Notes sur le Mastigocoleus, nouveau genre des algues marines de l’ordre des Phycochromacées. Notarisia 1:65-69

    Google Scholar 

  • Lamouroux JVF (1812) Extrait d’un mémoire sur la classification des polypiers coralligènes non entièrement pierreux. Nouv Bull Sci Soc Philomat Paris 3:181-188

    Google Scholar 

  • Langdon C, Takahashi T, Marubini F, Atkinson MJ, Sweeney C, Aceves H, Barnet H, Chipman D, Goddard J (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639-654

    Article  Google Scholar 

  • Le Bris S, Le Campion-Alsumard T, Romano J-C (1998) Caractéristiques du feutrage algal des récifs coralliens de Polynésie française soumis à différentes intensités de bioérosion. Oceanolog Acta 21:695-708

    Article  Google Scholar 

  • Le Campion-Alsumard T (1975) Etude expérimentale de la colonisation d’éclats de calcite par les cyanophycées endolithes marines. Cah Biol Mar 16:177-185

    Google Scholar 

  • Le Campion-Alsumard T (1976) Etude préliminaire sur l’écologie et l’ultrastructure d’une cyanophycée Chrooccocale endolithe. J Microscop Biol Cell 26:53-60

    Google Scholar 

  • Le Campion-Alsumard T (1978) Les cyanophycées endolithes marines: systématique, ultrastructure, écologie et biodestruction. Thèse Univ Aix-Marseille II, 198 pp

    Google Scholar 

  • Le Campion-Alsumard T (1979) Les cyanophycées endolithes marines. Systématique, ultrastructure, écologie et biodestruction. Oceanolog Acta 2:143-156

    Google Scholar 

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

    Article  Google Scholar 

  • Le Campion-Alsumard T, Golubic S, Priess K (1995b) Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol Prog Ser 117:137-147

    Article  Google Scholar 

  • Lesser MP, Shick JM (1989) Photoadaptation and defenses against oxygen toxicity in zooxanthellae from natural populations of symbiotic cnidarians. J Exp Mar Biol Ecol 134:129-141

    Article  Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Laurentii Salvii, Holmiae, 824 pp

    Google Scholar 

  • Lukas KJ (1973) Taxonomy and ecology of the endolithic microflora of reef corals, with a review of the literature on endolithic microphytes. PhD Diss, Univ Rhode Island, 159 pp

    Google Scholar 

  • Lukas KJ (1974) Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J Phycol 10:331-335

    Google Scholar 

  • Lukas, KJ (1978) Depth distribution and form among common microboring algae from the Florida continental shelf. Geol Soc Amer, Abstr Programs 10:1-448

    Google Scholar 

  • Mallela J, Perry CT (2007) Calcium carbonate budgets for two coral reefs affected by different terrestrial runoff regimes, Rio Bueno, Jamaica. Coral Reefs 26:129-145

    Article  Google Scholar 

  • Mao Che L, Le Campion-Alsumard T, Boury-Esnault N, Payri C, Golubic S, Bézac C (1996) Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia. Mar Biol 126:509-519

    Article  Google Scholar 

  • Marubini F, Davis PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319-328

    Article  Google Scholar 

  • Meesters E, Bak R (1995) Age related deterioration of a physiological function in the branching coral Acropora palmata. Mar Ecol Prog Ser 121:203-209

    Article  Google Scholar 

  • Mumby PJ, Chisholm JRM, Edwards AJ, Clark CD, Roark EB, Andrefouet S, Jaubert J (2001) Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia. Mar Biol 139:183-189

    Article  Google Scholar 

  • Nothdurft LD, Webb GE, Buster NA, Holmes CW, Sorauf JE (2005) Brucite microbialites in living coral skeletons: indicators of extreme microenvironments in shallow-marine settings. Geol Soc Amer 33:169-172

    Google Scholar 

  • Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetak atoll. Ecol Monogr 25:291-320

    Article  Google Scholar 

  • Paerl HW, Pinckney JL (2005) A mini-review of microbial consortia: Their roles in aquatic production and biogeochemical cycling. Microbial Ecol 31:225-247

    Google Scholar 

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

    Article  Google Scholar 

  • Pari N, Peyrot-Clausade M, Hutchings PA (2002) Bioerosion of experimental substrates on high islands and atoll lagoons (French Polynesia) during 5 years of exposure. J Exp Mar Biol Ecol 276:109-127

    Article  Google Scholar 

  • Perry CT (1998) Grain susceptibility to the effects of microboring: implication for the preservation of skeletal carbonates. Sedimentology 45:39-51

    Article  Google Scholar 

  • Perry CT (2000) Factors controlling sediment preservation on a north Jamaican fringing reef: a process-based approach to microfacies analysis. J Sediment Res 70:633-648

    Article  Google Scholar 

  • Perry CT, MacDonald IA (2002) Impacts of light penetration on the bathymetry of reef microboring communities: implications for the development of microendolithic trace assemblages. Palaeogeogr Palaeoclimatol Palaeoecol 186:101-113

    Article  Google Scholar 

  • Porter D, Lingle WL (1992) Endolithic thraustrochytrid marine fungi from planted shell fragments. Mycologia 84:289-299

    Article  Google Scholar 

  • Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin BA (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Mar Biol 136:19-27

    Article  Google Scholar 

  • Radtke G (1993) The distribution of microborings in molluscan shells from recent reef environments at Lee Stocking Island, Bahamas. Facies 29:81-92

    Article  Google Scholar 

  • Radtke G, Golubic S (2005) Microborings in mollusc shells, Bay of Safaga, Egypt: morphometry and ichnology. Facies 51:118-134

    Article  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 

  • Radtke G, Le Campion-Alsumard T, Golubic S (1997a) Microbial assemblages involved in tropical coastal bioerosion: an Atlantic-Pacific comparison. Proc 8th Int Coral Reefs Symp, Panama, 2:1825-1830

    Google Scholar 

  • Radtke G, Hofmann K, Golubic S (1997b) A bibliographic overview of micro- and macroscopic bioerosion. In: Betzler C, Hüssner H (eds) Vogel-Festschrift. Courier Forschinst Senckenberg 201:307-340

    Google Scholar 

  • Raghukumar C, Sharma S, Lande V (1991) Distribution and biomass estimation of shell boring algae in the intertidal at Goa, India. Phycologia 30:303-309

    Google Scholar 

  • Rathbun R (1887) The crab, lobster, crayfish, rock lobster, shrimp, and prawn fisheries. In Goode GB (ed) The fisheries and fishery industries of the United States. Section V, History and Methods of the Fisheries II. U.S. Government Printing Office, Washington, pp 627-839

    Google Scholar 

  • Reaka-Kudla ML, Feingold JS, Glynn W (1996) Experimental studies of rapid bioerosion of coral reefs in the Galapagos Islands. Coral Reefs 15:101-107

    Google Scholar 

  • Risk MJ, Kramer JR (1981) Water chemistry inside coral heads: determination of pH, Ca and Mg. Proc 4th Int Coral Reef Symp, Manila, Abstr, p 54

    Google Scholar 

  • Risk MJ, Muller HR (1983) Porewater in coral heads: evidence for nutrient regeneration. Limnol Oceanogr 28:1004-1008

    Article  Google Scholar 

  • Risk MJ, Heikoop JM, Edinger EN, Erdmann MV (2001) The assessment ‘toolbox’: community-based reef evaluation methods coupled with geochemical techniques to identify sources of stress. Bull Mar Sci 69:443-458

    Google Scholar 

  • Rojtan RD, Lewis SM (2005) Selective predation by parrotfishes on the reef coral Porites astreoides. Mar Ecol Prog Ser 305:193-201

    Article  Google Scholar 

  • Russ G (1984) Distribution and abundance of herbivorous grazing fishes in the Central Great Barrier Reef. I. Levels of variability across the entire continental shelf. Mar Ecol Prog Ser 20:23-34

    Article  Google Scholar 

  • Russell NC, Edwards HGM, Wynn-Williams DD (1998) FT-Raman spectroscopic analysis of endolithic microbial communities from Beacon sandstone in Victoria Land, Antarctica. Antarct Sci 10:63-74

    Article  Google Scholar 

  • Shashar N, Stambler N (1992) Endolithic algae within corals – life in an extreme environment. J Exp Mar Biol Ecol 163:277-286

    Article  Google Scholar 

  • Sharshar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: Evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111:259-264

    Article  Google Scholar 

  • Sharshar N, Banaszak AT, Lesser MP, Amrami D (1997) Coral endolithic algae: Life in a protected environment. Pacif Sci 51:167-173

    Google Scholar 

  • Shibata K, Haxo FT (1969) Light transmission and spectral distribution through epi- and endozoic algal layers in the brain coral, Favia. Biol Bull 136:461-468

    Article  Google Scholar 

  • Schlichter D, Zscharnack B, Krisch H (1995) Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82:561-564

    Article  Google Scholar 

  • Schlichter D, Kampmann H, Conrady S (1997) Trophic potential and photoecology of endolithic algae living within coral skeletons. PSZN. Mar Ecol 18:299-317

    Article  Google Scholar 

  • Schneider J, Le Campion-Alsumard T (1999) Construction and destruction of carbonates by marine and freshwater cyanobacteria. Europ J Phycol 34:417-426

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schneider J, Schröder HG, Le Campion-Alsumard T (1983) Algal micro-reefs – Coated grains from freshwater environments. In: Peryt TM (ed) Coated grains. Springer, Berlin Heidelberg, pp 284-298

    Google Scholar 

  • Sheppard CRC, Spalding M, Bradshaw, Wilson S (2002) Erosion vs recovery of coral reefs after 1998 El Niño: Chagos reefs, Indian Ocean. Ambio 31:40-48

    Article  Google Scholar 

  • Szmant AM (2002) Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries 25:743-766

    Article  Google Scholar 

  • Tribollet A (2007) Dissolution of dead corals by euendolithic microorganisms across the northern Great Barrier Reef (Australia). Microbial Ecol DOI: 10.1007/s00248-007- 9302-6

    Google Scholar 

  • 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, Payri C (2001) Bioerosion of the crustose coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea, French Polynesia. Oceanolog Acta 24:329-342

    Article  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 (2006a) Endolithic microflora are major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292-303

    Article  Google Scholar 

  • Tribollet A, Atkinson M, Langdon C (2006b) Effects of elevated pCO2 on epilithic and endolithic metabolism of reef carbonates. Global Change Biol 12:2200-2208

    Article  Google Scholar 

  • Tudhope AW, Risk MJ (1985) Rate of dissolution of carbonate sediments by microboring organisms, Davies Reef, Australia. J Sediment Petrol 55:440-447

    Google Scholar 

  • 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 33:190-204

    Article  Google Scholar 

  • Vooren CM (1981) Photosynthetic rates of benthic algae from the deep coral reef of Curaçao. Aquat Bot 10:143-154

    Article  Google Scholar 

  • Voss JD, Richardson LL (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25:569-576

    Article  Google Scholar 

  • Wanders JBW (1977) The role of the benthic algae in the shallow reef of Curaçao (Netherlands Antilles). III. The significance of grazing. Aquat Bot 3:357-390

    Article  Google Scholar 

  • Weis VM, Smith GJ, Muscatine L (1989) A CO2 supply mechanism in zooxanthellate cnidarians: role of carbonic anhydraze. Mar Biol 100:195-202

    Article  Google Scholar 

  • Wilkinson C (2004) Status of coral reefs of the world: 2004. Austral Inst Mar Sci, Townsville, Australia, 557 pp

    Google Scholar 

  • Williams SL, Carpenter RC (1998) Effects of unidirectional and oscillatory flow on nitrogen fixation (acetylene reduction) in coral reef algal turfs, Kaneohe Bay, Hawaii. J Exp Mar Biol Ecol 226:293-316

    Article  Google Scholar 

  • Wisshak M, Gektidis M, Freiwald A, Lundälv T (2005) Bioerosion along a bathymetric gradient in cold-temperate setting (Kosterfjord, SW Sweden): an experimental study. Facies 51:93-117

    Article  Google Scholar 

  • Womersley HBS (1987) The marine benthic flora of southern Australia. Part II. South Austral Gov Print Div, Adelaide, pp 1-481

    Google Scholar 

  • Woolcott GW, Knoller K, King RJ (2000) Phylogeny of the Bryopsidaceae (Bryopsidales, Chlorophyta): cladistic analyses of morphological and molecular data. Phycologia 39:471-481

    Article  Google Scholar 

  • Zhang Y, Golubic S (1987) Endolithic microfossils (cyanophyta) from early Proterozoic stromatolites, Hebei, China. Acta Micropaleont Sin 4:1-12

    Google Scholar 

  • Zubia M, Peyrot-Clausade M (2001) Internal bioerosion of Acropora formosa in Réunion (Indian Ocean): microborer and macroborer activities. Oceanolog Acta 24:251-262

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Tribollet, A. (2008). The boring microflora in modern coral reef ecosystems: a review of its roles. In: Wisshak, M., Tapanila, L. (eds) Current Developments in Bioerosion. Erlangen Earth Conference Series. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-77598-0_4

Download citation

Publish with us

Policies and ethics