Coral Reefs

, Volume 34, Issue 3, pp 863–870 | Cite as

Coralline algae disease reduces survival and settlement success of coral planulae in laboratory experiments

  • Gaëlle Quéré
  • Maggy M. Nugues


Disease outbreaks have been involved in the deterioration of coral reefs worldwide and have been particularly striking among crustose coralline algae (CCA). Although CCA represent important cues for coral settlement, the impact of CCA diseases on the survival and settlement of coral planulae is unknown. Exposing coral larvae to healthy, diseased, and recently dead crusts from three important CCA species, we show a negative effect of disease in the inductive CCA species Hydrolithon boergesenii on larval survivorship of Orbicella faveolata and settlement of O. faveolata and Diploria labyrinthiformis on the CCA surface. No effect was found with the less inductive CCA species Neogoniolithon mamillare and Paragoniolithon accretum. Additionally, a majority of planulae that settled on top of diseased H. boergesenii crusts were on healthy rather than diseased/dying tissue. Our experiments suggest that CCA diseases have the potential to reduce the survivorship and settlement of coral planulae on coral reefs.


Coral recruitment Settlement cue Disease Crustose coralline algae 



The research leading to these results has received funding from the European Union 7th Framework programme (P7/2007-2013) under Grant agreement No. 244161. MMN acknowledges support for the CNRS Chaire d’Excellence. We wish to thank the Carmabi foundation and staff for logistic support. We are grateful to M. Vermeij for providing the coral larvae and for useful discussions and to R. Longhitano and G. Fenwick for their help in the field. We additionally thank two anonymous reviewers for comments that greatly improved this manuscript.

Supplementary material

338_2015_1292_MOESM1_ESM.docx (41 kb)
Supplementary material 1 (DOCX 41 kb)


  1. Aeby GS, Work T, Fenner D, Didonato E (2008) Coral and crustose coralline algae disease on the reefs of American Samoa. In: proceedings of the 11th international coral reef symposium, 1:200–204Google Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson MJ (2004) PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  4. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  5. Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441–450CrossRefGoogle Scholar
  6. Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 201–218Google Scholar
  7. Doropoulos C, Ward S, Diaz-Pulido G, Hoegh-Guldberg O, Mumby PJ (2012) Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol Lett 15:338–346PubMedCrossRefGoogle Scholar
  8. Ghirardelli LA (2002) Endolithic microorganisms in live and dead thalli of coralline red algae (Corallinales, Rhodophyta) in the Northern Adriatic sea. Acta Geologia Hispanica 37:53–60Google Scholar
  9. Goreau T, 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, Quirolo C, Patterson K, Porter JW, Porter K (1998) Rapid spread of diseases in Caribbean coral reefs. Rev Biol Trop 46:157–171Google Scholar
  10. Harrington L, Fabricius K, De’Ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437CrossRefGoogle Scholar
  11. Hartmann AC, Kristen LM, Chamberland VF, Sandin SA, Vermeij MJA (2013) Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species. Ecology 94:1966–1976PubMedCrossRefGoogle Scholar
  12. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases–climate links and anthropogenic factors. Science 285:1505–1510PubMedCrossRefGoogle Scholar
  13. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279CrossRefGoogle Scholar
  14. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551PubMedCrossRefGoogle Scholar
  15. Johnson CR, Sutton DC, Olson RR, Giddins R (1991) Settlement of crown-of-thorns starfish: role of bacteria on surfaces of coralline algae and a hypothesis for deepwater. Mar Ecol Prog Ser 71:143–162CrossRefGoogle Scholar
  16. Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117CrossRefGoogle Scholar
  17. Littler MM, Littler DS (1995) Impact of CLOD pathogen on Pacific coral reefs. Science 267:1356–1360PubMedCrossRefGoogle Scholar
  18. Mason B, Beard M, Miller MW (2011) Coral larvae settle at a higher frequency on red surfaces. Coral Reefs 30:667–676CrossRefGoogle Scholar
  19. Miller MW (2014) Post-settlement survivorship in two Caribbean broadcasting corals. Coral Reefs 33:1041–1046CrossRefGoogle Scholar
  20. Miller MW, Valdivia A, Kramer KL, Mason B, Williams DE, Johnston L (2009) Alternate benthic assemblages on reef restoration structures and cascading effects on coral settlement. Mar Ecol Prog Ser 387:147–156CrossRefGoogle Scholar
  21. Miller IR, Logan M, Johns KA, Jonker MJ, Osborne K, Sweatman HPA (2013) Determining background levels and defining outbreaks of crustose coralline algae disease on the Great Barrier Reef. Mar Freshw Res 64:1022–1028CrossRefGoogle Scholar
  22. Morse DE, Morse ANC (1991) Enzymatic characterization of the morphogen recognized by Agaricia humilis (scleractinian coral) larvae. Biol Bull 181:104–122CrossRefGoogle Scholar
  23. Morse DE, Hooker N, Morse ANC, Jensen RJ (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217CrossRefGoogle Scholar
  24. Morse DE, Morse A, Raimondi PT, Hooker N (1994) Morphogen-based chemical flypaper for Agaricia humilis coral larvae. Biol Bull 186:172–181CrossRefGoogle Scholar
  25. Muller E, Vermeij MJA (2011) Day time spawning of a Caribbean coral. Coral Reefs 30:1147CrossRefGoogle Scholar
  26. Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131CrossRefGoogle Scholar
  27. Olsen K, Ritson-Williams R, Paul V, Ross C (2014) Combined effects of macroalgal presence and elevated temperature on the early life-history stages of a common Caribbean coral. Mar Ecol Prog Ser 509:181–191CrossRefGoogle Scholar
  28. Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ Microbiol 5:370–382PubMedCrossRefGoogle Scholar
  29. Paul V, Kuffner I, Walters L, Ritson-Williams R, Beach K, Becerro M (2011) Chemically mediated interactions between macroalgae Dictyota spp. and multiple life-history stages of the coral Porites astreoides. Mar Ecol Prog Ser 426:161–170CrossRefGoogle Scholar
  30. Quéré G, Steneck RS, Nugues MM (2015) Spatiotemporal and species-specific patterns of diseases affecting crustose coralline algae in Curaçao. Coral Reefs 34:259–273CrossRefGoogle Scholar
  31. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  32. Ritson-Williams R, Paul V, Arnold S, Steneck R (2010) Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29:71–81CrossRefGoogle Scholar
  33. Ritson-Williams R, Arnold SN, Paul VJ, Steneck RS (2014) Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae. Coral Reefs 33:59–66CrossRefGoogle Scholar
  34. Ritson-Williams R, Arnold S, Fogarty N, Steneck R, Vermeij M, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457CrossRefGoogle Scholar
  35. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3:512–521PubMedCrossRefGoogle Scholar
  36. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302CrossRefGoogle Scholar
  37. Suzuki Y, Takabayashi T, Kawaguchi T, Matsunaga K (1998) Isolation of an allelopathic substance from the crustose coralline algae, Lithophyllum spp., and its effect on the brown alga, Laminaria religiosa Miyabe (Phaeophyta). J Exp Mar Bio Ecol 225:69–77CrossRefGoogle Scholar
  38. Tribollet A, Payri C (2001) Bioerosion of the coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea, French Polynesia. Oceanol Acta 24:329–342CrossRefGoogle Scholar
  39. Tribollet A, Aeby G, Work T (2011) Survey and determination of coral and coralline algae diseases/lesions in the lagoon of New Caledonia. Scientific Report. COMPONENT 3D-Project 3D3 Studies of coral diseases in New Caledonia, CRISP, New CaledoniaGoogle Scholar
  40. Vargas-Ángel B (2010) Crustose coralline algal diseases in the US-Affiliated Pacific Islands. Coral Reefs 29:943–956CrossRefGoogle Scholar
  41. Vermeij MJA, Sandin SA (2008) Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89:1994–2004PubMedCrossRefGoogle Scholar
  42. Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128CrossRefGoogle Scholar
  43. Vermeij MJA, Smith JE, Smith CM, Vega Thurber R, Sandin SA (2009) Survival and settlement success of coral planulae: independent and synergistic effects of macroalgae and microbes. Oecologia 159:325–336PubMedCrossRefGoogle Scholar
  44. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R (2008) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol 10:3366–3376PubMedCrossRefGoogle Scholar
  45. Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, Blackall LL, Negri AP (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70:1213–1221PubMedCentralPubMedCrossRefGoogle Scholar
  46. Williams GJ, Price NN, Ushijima B, Aeby GS, Callahan S, Davy SK, Gove JM, Johnson MD, Knapp IS, Shore-Maggio A, Smith JE, Videau P, Work TM (2014) Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease. Proc R Soc B Biol Sci 281:20133069CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Leibniz Center for Tropical Marine Ecology (ZMT)BremenGermany
  2. 2.Laboratoire d’Excellence ‘CORAIL’ and USR 3278 CRIOBE EPHE-CNRS-UPVDPerpignan CedexFrance
  3. 3.Carmabi FoundationWillemstadCuraçao

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