Coral Reefs

, Volume 36, Issue 2, pp 453–462 | Cite as

Crustose coralline algae and associated microbial biofilms deter seaweed settlement on coral reefs

Report

Abstract

Crustose coralline algae (CCA), a group of calcifying red algae found commonly in benthic marine ecosystems worldwide, perform essential ecological functions on coral reefs, including creating benthic substrate, stabilizing the reef structure and inducing coral settlement. An important feature of CCA is the ability to keep their surfaces free of epiphytic algae, thereby reducing algal overgrowth and allowing them access to light. However, the mechanisms by which CCA prevent settlement of opportunistic seaweeds (fleshy macroalgae) are not fully understood, nor is whether these mechanisms vary among CCA species. In our study based on the Great Barrier Reef, we demonstrate that three common CCA species (Titanoderma pustulatum, Porolithon onkodes and Neogoniolithon sp.) have a remarkable ability to deter settlement of seaweed spores. We provide experimental evidence that the CCA use allelopathy and microbial inhibition against the settlement of spores of the brown seaweed Padina boergesenii. Methanol extracts of allelopathic compounds from T. pustulatum, Po. onkodes and Neogoniolithon sp. significantly reduced the settlement of Pa. boergesenii spores by 4.3 times, 3.0 and 3.8 times, respectively. Further, we found that microbial biofilms, while having a lower inhibitory effect than allelopathic compounds, also reduced seaweed settlement of Pa. boergesenii. Our study demonstrates that allelopathy and microbial inhibition, in addition to epithallial tissue sloughing, are mechanisms employed by CCA to prevent the settlement of epiphytic algae. Understanding the mechanisms by which CCA avoid seaweed overgrowth contributes to our understanding of the dynamics of seaweed proliferations on reefs and to the ecological knowledge of this important group of reef-building organisms.

Keywords

Crustose coralline algae Antifouling mechanisms Bacteria Allelopathy Macroalgal spores Great Barrier Reef 

References

  1. Armstrong E, Yan LM, Boyd KG, Wright PC, Burgess JG (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461:37–40CrossRefGoogle Scholar
  2. Berland BR, Bonin DJ, Maestrin SY (1972) Are some bacteria toxic for marine algae? Mar Biol 12:189–193CrossRefGoogle Scholar
  3. Bowman JP (2007) Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs 5:220–241CrossRefPubMedPubMedCentralGoogle Scholar
  4. Braten T (1971) The ultrastructure of fertilization and zygote formation in the green alga Ulva mutabilis Foyn. J Cell Sci 9:621–635PubMedGoogle Scholar
  5. Bucolo P, Amsler CD, McClintock JB, Baker BJ (2012) Effects of macroalgal chemical extracts on spore behavior of the antarctic epiphyte Elachista antarctica Phaeophyceae. J Phycol 48:1403–1410CrossRefPubMedGoogle Scholar
  6. Dean AJ, Steneck RS, Tager D, Pandolfi JM (2015) Distribution, abundance and diversity of crustose coralline algae on the Great Barrier Reef. Coral Reefs 34:581–594CrossRefGoogle Scholar
  7. Denboh T, Suzuki M, Mizuno Y, Ichimura T (1997) Suppression of Laminaria sporelings by allelochemicals from coralline red algae. Bot Mar 40:249–256CrossRefGoogle Scholar
  8. Diaz-Pulido G, Villamil L, Almanza V (2007) Herbivory effects on the morphology of the brown alga Padina boergesenii (Phaeophyta). Phycologia 46:131–136CrossRefGoogle Scholar
  9. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS ONE 4:e5239CrossRefPubMedPubMedCentralGoogle Scholar
  10. Diaz-Pulido G, Harii S, McCook LJ, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203–208CrossRefGoogle Scholar
  11. 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 15:338–346CrossRefPubMedGoogle Scholar
  12. Dunnett CW (1964) New tables for multiple comparisons with a control. Biometrics 20:482–491CrossRefGoogle Scholar
  13. Egan S, Holmstrom C, Kjelleberg S (2001a) Pseudoalteromonas ulvae sp. nov., a bacterium with antifouling activities isolated from the surface of a marine alga. Int J Syst Evol Microbiol 51:1499–1504CrossRefPubMedGoogle Scholar
  14. Egan S, James S, Holmstrom C, Kjelleberg S (2001b) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. Fems Microbiol Ecol 35:67–73CrossRefPubMedGoogle Scholar
  15. Egan S, James S, Holmstrom C, Kjelleberg S (2002) Correlation between pigmentation and antifouling compounds produced by Pseudoalteromonas tunicata. Environ Microbiol 4:433–442CrossRefPubMedGoogle Scholar
  16. Ganesan M, Rao PV (1999) Culture of marine brown alga Padina boergesenii (Dictyotales, Phaeophyta) at Mandapam coast, southeast coast of India. Indian J Mar Sci 28:461–463Google Scholar
  17. Ganesan M, Mairh OP, Rao PV (2000) Seasonal variations in growth and spore production of marine brown algae Padina boergesenii and P. tetrastromatica (Dictyotales/Phaeophyta) in the Mandapam region, southeast coast of India. Indian J Mar Sci 29:253–257Google Scholar
  18. Gordon GD, Masaki T, Akioka H (1976) Floristic and distributional account of the common crustose coralline algae on Guam. Micronesica 12:247–277Google Scholar
  19. Harder T, Dobretsov S, Qian PY (2004) Waterborne polar macromolecules act as algal antifoulants in the seaweed Ulva reticulata. Mar Ecol Prog Ser 274:133–141CrossRefGoogle Scholar
  20. 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
  21. 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 318:1737–1742CrossRefPubMedGoogle Scholar
  22. Holmstrom C, James S, Egan S, Kjelleberg S (1996) Inhibition of common fouling organisms by marine bacterial isolates with special reference to the role of pigmented bacteria. Biofouling 10:251–259CrossRefPubMedGoogle Scholar
  23. Hughes TP (1994) Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  24. Itoh N, Hasan AKMQ, Izumi Y, Yamada H (1987) Immunological properties of bromoperoxidases in coralline algae. Biochem Int 15:27–33Google Scholar
  25. Jackson J, Donovan M, Cramer K, Lam V (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef monitoring network. IUCN, GlandGoogle Scholar
  26. Johnson CR, Mann KH (1986) The crustose coralline alga, Phymatolithon foslie, inhibits the overgrowth of seaweeds without relying on herbivores. J Exp Mar Biol Ecol 96:127–146CrossRefGoogle Scholar
  27. Johnson CR, Sutton DC (1994) Bacteria on the surface of crustose coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Mar Biol 120:305–310CrossRefGoogle Scholar
  28. Kakisawa H, Asari F, Kusumi T, Toma T, Sakurai T, Oohusa T, Hara Y, Chihara M (1988) An allelopathic fatty acid from the brown alga Cladosiphon okamuranus. Phytochemistry 27:731–735CrossRefGoogle Scholar
  29. Keats DW, Groener A, Chamberlain YM (1993) Cell sloughing in the littoral zone coralline alga, Spongites yendoi (Foslie) Chamberlain (Corallinales, Rhodophyta). Phycologia 32:140–150CrossRefGoogle Scholar
  30. Keats DW, Wilton P, Maneveldt G (1994) Ecological significance of deep-layer sloughing in the eulittoral zone coralline alga, Spongites yendoi (Foslie) Chamberlain (Corallinaceae, Rhodophyta) in South Africa. J Exp Mar Biol Ecol 175:145–154CrossRefGoogle Scholar
  31. Keats DW, Knight MA, Pueschel CM (1997) Antifouling effects of epithallial shedding in three crustose coralline algae (Rhodophyta, Coralinales) on a coral reef. J Exp Mar Biol Ecol 213:281–293CrossRefGoogle Scholar
  32. Kim J, Choi JS, Kang SE, Cho JY, Jin HJ, Chun BS, Hong YK (2004) Multiple allelopathic activity of the crustose coralline alga Lithophyllum yessoense against settlement and germination of seaweed spores. J Appl Phycol 16:175–179CrossRefGoogle Scholar
  33. Littler MM (1971) Standing stock measurements of crustose coralline algae (Rhodophyta) and other saxicolous organisms. J Exp Mar Biol Ecol 6:91–99CrossRefGoogle Scholar
  34. Littler MM, Littler DS (1997) Disease-induced mass mortality of crustose coralline algae on coral reefs provides rationale for the conservation of herbivorous fish stocks. In: Proceedings of the 8th international Coral Reef symposium, vol 1. pp 719–724Google Scholar
  35. Littler MM, Littler DS (1999) Epithallus sloughing: a self-cleaning mechanism for coralline algae. Coral Reefs 18:204–204CrossRefGoogle Scholar
  36. Littler MM, Littler DS, Taylor PR (1995) Selective herbivore increases biomass of its prey—a chiton–coralline reef-building association. Ecology 76:1666–1681CrossRefGoogle Scholar
  37. Lovejoy C, Bowman JP, Hallegraeff GM (1998) Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, Gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl Environ Microbiol 64:2806–2813PubMedPubMedCentralGoogle Scholar
  38. Ma YX, Liu PL, Yu S, Li DT, Cao SM (2009) Inhibition of common fouling organisms in mariculture by epiphytic bacteria from the surfaces of seaweeds and invertebrates. Acta Ecol Sin 29:222–226CrossRefGoogle Scholar
  39. Masaki TF, Fujita D, Hagen NT (1984) The surface ultrastructure and epithallium shedding of crustose coralline algae in an ‘Isoyake’ area of southwestern Hokkaido, Japan. Hydrobiologia 116(117):218–223CrossRefGoogle Scholar
  40. Matsuda S (1989) Succession and growth rates of encrusting crustose coralline algae (Rhodophyta, Cryptonemiales) in the upper fore-reef environment off Ishigaki Island, Ryukyu Islands. Coral Reefs 7:185–195CrossRefGoogle Scholar
  41. McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417CrossRefGoogle Scholar
  42. Mieszkin S, Callow ME, Callow JA (2013) Interactions between microbial biofilms and marine fouling algae: a mini review. Biofouling 29:1097–1113CrossRefPubMedGoogle Scholar
  43. Okamoto DK, Stekoll MS, Eckert GL (2013) Coexistence despite recruitment inhibition of kelps by subtidal algal crusts. Mar Ecol Prog Ser 493:103–112CrossRefGoogle Scholar
  44. Patel P, Callow ME, Joint I, Callow JA (2003) Specificity in the settlement-modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha. Environ Microbiol 5:338–349CrossRefPubMedGoogle Scholar
  45. Price N (2010) Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 163:747–758CrossRefPubMedPubMedCentralGoogle Scholar
  46. Quoc-Hai L, Ji-Young C, Jae-Suk C, Ji-Young K, Nam GP, Yong-Ki H (2009) Isolation of algal spore lytic C17 fatty acid from the crustose coralline seaweed Lithophyllum yessoense. J Appl Phycol 21:423–427CrossRefGoogle Scholar
  47. Reyes-Nivia C (2013) Effect of future climate scenarios on reef bioerosion processes, Ph.D. thesis, University of Queensland, Brisbane, Australia, p 102Google Scholar
  48. Siboni N, Abrego D, Seneca F, Motti CA, Andreakis N, Tebben J, Blackall LL, Harder T (2012) Using bacterial extract along with differential gene expression in Acropora millepora larvae to decouple the processes of attachment and metamorphosis. PLoS ONE 7:e37774CrossRefPubMedPubMedCentralGoogle Scholar
  49. Silva-Aciares F, Riquelme C (2008) Inhibition of attachment of some fouling diatoms and settlement of Ulva lactuca zoospores by film-forming bacterium and their extracellular products isolated from biofouled substrata in Northern Chile. Electron J Biotechnol 11:60–70CrossRefGoogle Scholar
  50. Steneck RS (1983) Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9:44–61CrossRefGoogle Scholar
  51. Steneck RS (1986) The ecology of coralline algal crusts—convergent patterns and adaptive strategies. Annu Rev Ecol Syst 17:273–303CrossRefGoogle Scholar
  52. 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 Biol Ecol 225:69–77CrossRefGoogle Scholar
  53. Tebben J, Motti C, Tapiolas D, Thomas-Hall P, Harder T (2014) A coralline algal-associated bacterium, Pseudoalteromonas strain J010, yields five new korormicins and a bromopyrrole. Mar Drugs 12:2802–2815CrossRefPubMedPubMedCentralGoogle Scholar
  54. Vermeij MJA, Dailer ML, Smith CM (2011) Crustose coralline algae can suppress macroalgal growth and recruitment on Hawaiian coral reefs. Mar Ecol Prog Ser 422:1–7CrossRefGoogle Scholar
  55. Villas-Bôas AB, Figueiredo MA (2004) Are anti-fouling effects in coralline algae species specific? Braz J Oceanogr 52:11–18CrossRefGoogle Scholar
  56. 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 70:1213–1221CrossRefPubMedPubMedCentralGoogle Scholar
  57. Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 6:86PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Griffith School of Environment, Australian Rivers Institute – Coast and EstuariesGriffith UniversityBrisbaneAustralia
  2. 2.Australian Research Council Centre of Excellence for Coral Reef StudiesTownsvilleAustralia

Personalised recommendations