Marine Biology

, Volume 158, Issue 11, pp 2495–2504 | Cite as

Microalgae from the mucus layer of two massive corals: more than sunken plankton

  • F. Cavada
  • R. Ayala
  • L. Troccoli
  • J. J. Cruz-MottaEmail author
Original Paper


The mucus of scleractinian corals harbors a variety of prokaryotic and eukaryotic microorganisms, but little is known about the eukaryotic fraction of this microbiota. In this study, a quantitative and qualitative description of microalgae assemblages associated with the mucus of two species of massive corals is presented. During the first half of 2004, in “Los Frailes” Archipelago (Southern Caribbean), samples of mucus were randomly taken from healthy colonies of Diploria sp. and Colpophyllia sp. Also, samples of water surrounding each colony were taken monthly for six months. Multivariate analysis showed that microalgae assemblages from the mucus were significantly different from those found in the water column, and that variation of microalgae assemblage composition in time was dependent on the coral species. The results indicate that most of the microalgae assemblage associated with the mucus did not originate from a passive trapping of species commonly found in the phytoplankton. Nevertheless, temporal variations of both assemblages (i.e., phytoplankton and mucus) were very dynamic but closely associated.


Microalgae Coral Species Scleractinian Coral Mucus Layer Massive Coral 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Sampling assistance was kindly provided by Mayne Cacique and Zhandra Marcano. We thank Aquanauts Diving Center for providing the diving equipment and boat transportation. We are especially grateful to Dr. Carolina Bastidas (Universidad Simón Bolívar) and three anonymous reviewers, who helped considerably to improve this manuscript.

Supplementary material

227_2011_1750_MOESM1_ESM.pdf (48 kb)
Supplementary material 1 (PDF 48 kb)


  1. Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46Google Scholar
  2. Anthony K, Fabricius K (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253CrossRefGoogle Scholar
  3. Avedaño-Herrera R, Riquelme C (2007) Production of a diatom-bacteria biofilm in a photobioreactor for aquaculture applications. Aquac Eng 36(2):97–104CrossRefGoogle Scholar
  4. Baker A (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 177–194CrossRefGoogle Scholar
  5. Banin E, Ben-Haim Y, Israely T, Loya Y, Rosenberg E (2000a) Effect of the environment on the bacterial bleaching of corals. Water Air Soil Poll 123:337–352CrossRefGoogle Scholar
  6. Banin E, Israely T, Kushmaro A, Loya Y, Orr E, Rosenberg E (2000b) Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. Appl Environ Biol Ecol 66(7):3031–3036CrossRefGoogle Scholar
  7. Banin E, Israely T, Fine M, Loya Y, Rosenberg E (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199:33–37CrossRefGoogle Scholar
  8. Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55CrossRefGoogle Scholar
  9. Ben-Haim Y, Banin E, Kushmaro A, Loya Y, Rosenberg E (1999) Inhibition of photosynthesis and bleaching of zooxanthellae by the coral pathogen Vibrio shiloi. Environ Microbiol 1:223–229CrossRefGoogle Scholar
  10. Ben-Haim Y, Zicherman M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69(7):4236–4242CrossRefGoogle Scholar
  11. Bianchi F, Acri F, Bernardi Aubry F, Berton A, Boldrin A, Camatti E, Cassin D, Comaschi A (2003) Can plankton communities be considered as bio-indicators of water quality in the Lagoon of Venice? Mar Poll Bull 46:964–971CrossRefGoogle Scholar
  12. Bode A, Gonzalez N, Rodriguez C, Varela M, Varela M (2005) Seasonal variability of plankton blooms in the Ria de Ferrol (NW Spain): I. Nutrient concentrations and nitrogen uptake rates. Est Coast and Shelf Sci 63:269–284CrossRefGoogle Scholar
  13. Bourne D, Munn C (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7(8):1162–1174CrossRefGoogle Scholar
  14. Brouwer J, Stahl L (2001) Short term dynamics on microphytobenthos distribution and associated extracellular carbohydrates in surface sediments of an intertidal mudflat. Mar Ecol Progr Ser 218:33–44CrossRefGoogle Scholar
  15. Castellanos P, Varela R, Muller-Kager F (2002) Descripción de las áreas de surgencia al sur del mar Caribe examinadas con el sensor infrarrojo AVHRR. Mem FLASA Ciens Nat 154:55–76Google Scholar
  16. Clark K, Warwick R (2001) Changes in marine Community: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd., PlymouthGoogle Scholar
  17. Clavier J, Chauvaud L, Fichez R, Chifflet S (2005) Benthic response to ammonium pulses in a tropical lagoon: implications for coastal environmental processes. J Exp Mar Biol Ecol 316:231–241CrossRefGoogle Scholar
  18. Danger M, Lefleive J, Oumarou C, Ten-hage L, Lacroix G (2007) Control of phytoplankton bacteria interaction by stoichiometric constrains. Oikos 116(7):1079–1086Google Scholar
  19. Descy J, Coste M (1990) Utilisation des diatome′ es benthiques pour l’ evaluation de la qualite′ des aux courantes, Contrat CEE B-71-23, Rapport final, CemagrefGoogle Scholar
  20. Dodds W, Biggs B, Lowe R (1999) Photosynthesis-irradiance patterns in benthic microalgae: variations as a function of assemblages thickness and community structure. J Phycol 35:42–53CrossRefGoogle Scholar
  21. Facca C, Sfrisso A (2007) Epipelic diatom spatial and temporal distribution and relationship with the main environmental parameters in coastal water. Est Coast and Shelf Sci 75:35–49CrossRefGoogle Scholar
  22. Facca C, Sfrisso A, Soca G (2002) Changes in abundance and composition of phytoplankton and microphytobenthos due to increased sediment fluxes in the Venice Lagoon, Italy. Est Coast Shelf Sci 54:773–792CrossRefGoogle Scholar
  23. Falkowski P, Raven J (2007) Aquatic photosynthesis. Princeton, New JerseyGoogle Scholar
  24. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc Lond 269:1205–1210CrossRefGoogle Scholar
  25. Frías-López J, Zerkle A, Bonheyo G, Fouke B (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68(5):2214–2228CrossRefGoogle Scholar
  26. García A, Cróquer A, Malaver N (2004) Algunas características funcionales de las comunidades bacterianas del mucus asociado a tejidos sanos y con síndrome de banda amarilla en Montastraea annularis. Interciencia 29(1):39–45Google Scholar
  27. Gil S, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488CrossRefGoogle Scholar
  28. Hasle G (1978) The inverted microscope method. In: Sournia L (ed) Phytoplankton manual. SCOR-UNESCO, Paris, pp 250–337Google Scholar
  29. Huang B, Hong H, Wang H (1999) Size-fractionated primary productivity and the phytoplankton-bacteria relationship in the Taiwan Strait. Mar Ecol Progr Ser 183:29–38CrossRefGoogle Scholar
  30. Kellogg C (2004) Tropical archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88CrossRefGoogle Scholar
  31. Klaus J, Janse I, Heikoop J, Sanfors R, Fouke B (2007) Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol 9(5):1291–1305CrossRefGoogle Scholar
  32. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as an habitat. Am Nat 162(Scs Mod):50–62Google Scholar
  33. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72(8):5254–5259CrossRefGoogle Scholar
  34. Larkum A, Koch E, Kuhl M (2003) Diffusive boundary layers and photosynthesis of the epilithic algal community of coral reefs. Mar Biol 142:1073–1082CrossRefGoogle Scholar
  35. Lesser M, Mazel C, Gorbunov M, Falkowski P (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000CrossRefGoogle Scholar
  36. Licursi M, Gomez N (2009) Effects of dredging on benthic diatom assemblages in lowland stream. J Environ Manag 90:973–982CrossRefGoogle Scholar
  37. Marshall J, Ross T, Pyecroft S, Hallegraeff G (2005) Superoxide production by marine microalgae II. Towards understanding ecological consequences and possible functions. Mar Biol 147:541–549CrossRefGoogle Scholar
  38. Mindl B, Sonntag B, Pernthaler J, Vrba J, Psenner R, Posch T (2005) Effects of phosphorus loading on interactions of algae and bacteria: reinvestigation of the ‘phytoplankton–bacteria paradox’ in a continuous cultivation system. Aquat Microb Ecol 38:203–213CrossRefGoogle Scholar
  39. Miyajima T, Umezawa M, Koike I (2001) Microbiological nitrogen transformation in carbonate sediments of coral-reef lagoon and associated seagrass beds. Mar Ecol Progr Ser 271:273–286CrossRefGoogle Scholar
  40. Nagai H, Masayuki S, Yasumoto T (1990) Antimicrobial activities of polyether compounds of dinoflagellate origins. J Appl Phycol 2:305–308CrossRefGoogle Scholar
  41. Naumann R, Richter C, el-Zibdah M, Wild C (2009) Coral mucus as an efficient trap for picoplanktonic cyanobacteria: implications for pelagic-benthic coupling in the reef ecosystem. Mar Ecol Progr Ser 385:65–76CrossRefGoogle Scholar
  42. Paul J, DeFlaunn M, Jeffrey W (1986) Elevated levels of microbial activities in the coral surface microlayer. Mar Ecol Prog Ser 33:29–40CrossRefGoogle Scholar
  43. Piontek J, Handel N, Langer G, Wohlers J, Riebesell U, Engel A (2009) Effects of rising temperature on the formation and microbial degradation of marine diatom aggregates. Aquat Microbiol Ecol 54:305–318CrossRefGoogle Scholar
  44. Pismam T, Galayda Y, Loginova N (2005) Population dynamics of an algal–bacterial cenosis in closed ecological system. Adv Space Res 35(9):1579–1583CrossRefGoogle Scholar
  45. Ralph P, Larkum A, Kuhl A (2007) Photobiology of endolithic microorganisms in living coral skeletons: 1. Pigmentation, spectral reflectance and variable chlorophyll fluorescence analysis of endoliths in the massive corals Cyphastrea serailia, Porites lutea and Goniastrea australensis. Mar Biol 152:395–404CrossRefGoogle Scholar
  46. Reis A, Araújo S, Moura R, Francini-Filho R, Pappas G, Coelho A, Krüger R, Thompson F (2009) Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis. J Appl Microbiol 106:1378–1387CrossRefGoogle Scholar
  47. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8(12):2068–2073CrossRefGoogle Scholar
  48. Richardson L (1997) Occurrence of the black band disease cyanobacterium on healthy corals of the Florida keys. Bull Mar Sci 61(2):485–490Google Scholar
  49. Richardson L, Kuta K (2003) Ecological physiology of the black band disease cyanobacterium Phormidium corallyticum. FEMS Microbiol Ecol 43:287–298CrossRefGoogle Scholar
  50. Richardson L, Smith G, Ritchie K, Carlton R (2001) Integrating microbiological, microsensor, and physiologic techniques in the study of coral disease pathogenesis. Hydrobiologia 460:71–89CrossRefGoogle Scholar
  51. Ritchie K (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Progr Ser 322:3–14CrossRefGoogle Scholar
  52. Ritchie K, Smith G (1995) Carbon-source utilization patterns of coral-associated marine heterotrophs. J Mar Biotechnol 3:105–107Google Scholar
  53. Ritchie K, Smith G (2004) Microbial communities of coral surface polysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 259–263CrossRefGoogle Scholar
  54. Rohwer F, Breitbar M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  55. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Progr Ser 243:1–10CrossRefGoogle Scholar
  56. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nature Rev Microbiol 5:335–362Google Scholar
  57. Santavy D, Peters E, Kozlowski J, Wilkinson S (1995) Characterization of the bacterium suspected in the incidence of white band disease. Abstr Gen Meet Am Soc Microbiol 95(N-1):332Google Scholar
  58. Sommer U (1994) Are marine diatoms favoured by high Si:N ratios? Mar Ecol Progr Ser 115:309–315CrossRefGoogle Scholar
  59. Strickland J, Parsons T (1972) Manual of seawater analysis. Bull Fish Res Bd Canadá 125:310Google Scholar
  60. Toller R, Rowan R, Knowlton N (2002) Genetic evidence for a protozoan (phylum Apicomplexa) associated with the corals of the Montastraea annularis species complex. Coral Reefs 21:143–146Google Scholar
  61. Trench R (1987) Dinoflagellates in non-parasitic symbiosis. In: Taylor F (ed) Biology of dinoflagellates. Blackwell, Oxford, pp 530–570Google Scholar
  62. Tuchman N, Schollett M, Rier S, Geddes P (2006) Differential heterotrophic utilization of organic compounds by diatoms and bacteria under light and dark conditions. Hydrobiologia 561:167–177CrossRefGoogle Scholar
  63. Ukeles R, Rose W (1976) Observations on organic carbon utilization by photosynthetic marine microalgae. Mar Biol 37:11–28CrossRefGoogle Scholar
  64. Urban-Malinga B, Wiktor J (2003) Microphytobenthic primary production along a non-tidal sandy beach gradient: an annual study from the Baltic Sea. Oceanologia 45(4):705–720Google Scholar
  65. Valdor R, Aboal M (2007) Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon 49(6):769–779CrossRefGoogle Scholar
  66. Van Oppen M, Palstra F, Piquet A, Miller D (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond 268:1759–1767CrossRefGoogle Scholar
  67. Vardi A, Schatz D, Beeri K, Motro U, Sukenik A, Levne A, Kaplan A (2002) Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr Biol 12:1767–1772CrossRefGoogle Scholar
  68. Warner M, Chilcoat G, McFarland F, Fitt W (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef building coral Montastraea. Mar Biol 141:31–38CrossRefGoogle Scholar
  69. Warner M, LaJeunesse T, Robison J, Thur R (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897CrossRefGoogle Scholar
  70. Wassmund N, Voss M, Lochte K (2001) Evidence of nitrogen fixation by non-heterocystous cyanobacteria in the Baltic Sea and re-calculation of a budget of nitrogen fixation. Mar Ecol Progr Ser 214:1–14CrossRefGoogle Scholar
  71. Watermann F, Gerdes G, Krumbein W, Sommer U (1999) Competition between benthic cyanobacteria and diatoms as influenced by different grain sizes and temperatures. Mar Ecol Progr Ser 187:77–87CrossRefGoogle Scholar
  72. Wild C, Huettel M, Klueter A, Kremb S, Rasheed M, Jergensen B (2004) Coral mucus as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • F. Cavada
    • 1
  • R. Ayala
    • 1
  • L. Troccoli
    • 2
  • J. J. Cruz-Motta
    • 1
    • 3
    Email author
  1. 1.Laboratorio de Ecología ExperimentalUniversidad Simón BolívarCaracasVenezuela
  2. 2.Laboratorio de Productividad PrimariaUniversidad de Oriente, Núcleo Nueva EspartaMargaritaVenezuela
  3. 3.Departamento de Estudios AmbientalesUniversidad Simón BolívarCaracasVenezuela

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