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Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae

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Abstract

Bacterial biofilms are increasingly seen as important for the successful settlement of marine invertebrate larvae. Here we tested the effects of biofilms on settlement of the sea urchin Heliocidaris erythrogramma. Larvae settled on many surfaces including various algal species, rocks, sand and shells. Settlement was reduced by autoclaving rocks and algae, and by treatment of algae with antibiotics. These results, and molecular and culture-based analyses, suggested that the bacterial community on plants was important for settlement. To test this, approximately 250 strains of bacteria were isolated from coralline algae, and larvae were exposed to single-strain biofilms. Many induced rates of settlement comparable to coralline algae. The genus Pseudoalteromonas dominated these highly inductive strains, with representatives from Vibrio, Shewanella, Photobacterium and Pseudomonas also responsible for a high settlement response. The settlement response to different bacteria was species specific, as low inducers were also dominated by species in the genera Pseudoalteromonas and Vibrio. We also, for the first time, assessed settlement of larvae in response to characterised, monospecific biofilms in the field. Larvae metamorphosed in higher numbers on an inducing biofilm, Pseudoalteromonas luteoviolacea, than on either a low-inducing biofilm, Pseudoalteromonas rubra, or an unfilmed control. We conclude that the bacterial community on the surface of coralline algae is important as a settlement cue for H. erythrogramma larvae. This study is also an example of the emerging integration of molecular microbiology and more traditional marine eukaryote ecology.

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References

  • Abelson A, Denny M (1997) Settlement of marine organisms in flow. Annu Rev Ecol Syst 28:317–339

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EE, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Anderson MJ, Underwood AJ (1997) Effects of gastropod grazers on recruitment and succession of an estuarine assemblage: a multivariate and univariate approach. Oecologia 109:442–453

    Article  Google Scholar 

  • Barbieri E et al (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo peali (Cephalopoda: Loliginidae). Environ Microbiol 3:151–167

    Article  PubMed  CAS  Google Scholar 

  • Boettcher AA, Targett NM (1998) Role of chemical inducers in larval metamorphosis of queen conch, Strombus gigas Linnaeus: relationship to other marine invertebrate systems. Biol Bull 194:132–142

    Article  CAS  Google Scholar 

  • Boxshall AJ (2000) The importance of flow and settlement cues to larvae of the abalone, Haliotis rufescens Swainson. J Exp Mar Biol Ecol 254:143–167

    Article  PubMed  CAS  Google Scholar 

  • Browne KA, Zimmer RK (2001) Controlled release of a waterborne chemical signal stimulates planktonic larvae to settle. Biol Bull 200:87–91

    Article  PubMed  CAS  Google Scholar 

  • Burke RD (1984) Pheromonal control of metamorphosis in the sand dollar, Dendraster excentricus. Science 225:442–443

    Article  PubMed  Google Scholar 

  • Burke RD (1986) Pheromones and the gregarious settlement of marine invertebrate larvae. Bull Mar Sci 39:584–593

    Google Scholar 

  • Butman CA (1987) Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processess. Oceanogr Mar Biol Annu Rev 25:113–165

    Google Scholar 

  • Caley MJ, Carr ME, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500

    Article  Google Scholar 

  • Callow ME et al (2002) Microtopographic cues for settlement of zoospores of the green fouling alga Enteromorpha. Biofouling 18:237–245

    Article  Google Scholar 

  • Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Dahllöf I, Baillie H, Kjelleberg S (2000) rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Appl Environ Microbiol 66:3376–3380

    Article  PubMed  Google Scholar 

  • Dahms H-U, Dobretsov S, Qian P-Y (2004) The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J Exp Mar Biol Ecol 313:191–209

    Article  Google Scholar 

  • Daume S, Brand-Gardner S, Woelkerling WJ (1999) Settlement of abalone larvae (Haliotis laevigata Donovan) in response to non-geniculate coralline red algae (Corallinales, Rhodophyta). J Exp Mar Biol Ecol 234:125–143

    Article  Google Scholar 

  • Daume S, Krsinich A, Farrell S, Gervis M (2000) Settlement, early growth and survival of Haliotis rubra in response to different algal species. J Appl Phycol 12:479–488

    Article  Google Scholar 

  • Fusetani N (1997) Marine natural products influencing larval settlement and metamorphosis of benthic invertebrates. Curr Org Chem 1:127–115

    CAS  Google Scholar 

  • Gallardo WG, Buen SA (2003) Evaluation of mucus, Navicula, and mixed diatoms as larval settlement inducers for the tropical abalone Haliotis asinina. Aquaculture 221:357–364

    Article  Google Scholar 

  • Gordon N, Shpigel M, Harpaz S, Lee JJ, Neori A (2004) The settlement of abalone (Haliotis discus hannai) larvae on culture layers of different diatoms. J Shellfish Res 23:561–568

    Google Scholar 

  • Gosselin P, Jangoux M (1996) Induction of metamorphosis in Paracentrotus lividus larvae (Echinodermata, Echinoidea). Oceanol Acta 19:293–296

    Google Scholar 

  • Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In: McClintock JB, Baker JB (eds) Marine chemical ecology. CRC, Boca Raton, Fla., pp 431–461

    Google Scholar 

  • Harder T, Lam C, Qian PY (2002) Induction of larval settlement in the polychaete Hydroides elegans by marine biofilms: an investigation of monospecific diatom films as settlement cues. Mar Ecol Prog Ser 229:105–112

    Article  Google Scholar 

  • Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35:305–312

    Article  PubMed  CAS  Google Scholar 

  • Hofmann DK, Brand U (1987) Induction of metamorphosis in the symbiotic Scyphozoan Cassiopea andromeda: role of marine bacteria and biochemicals. Symbiosis 4:99–116

    Google Scholar 

  • Holmström C, Kjelleberg S (1999) Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30:285–293

    PubMed  Google Scholar 

  • Holmström C, Kjelleberg S (2000) Bacterial interactions with marine fouling organisms. In: Evans LV (eds) Biofilms: recent advances in their study and control. Harwood Academic Publishers, Australia, pp 101–115

    Google Scholar 

  • Holmström C, Rittschof D, Kjelleberg S (1992) Inhibition of settlement by larvae of Balanus amphitrite and Ciona intestinalis by a surface-colonizing marine bacterium. Appl Environ Microbiol 58:2111–2115

    PubMed  Google Scholar 

  • Huang S, Hadfield MG (2003) Composition and density of bacterial biofilms determine larval settlement of the polycheate Hydroides elegans. Mar Ecol Prog Ser:161–172

  • Huggett MJ, de Nys R, Williamson JE, Heasman M, Steinberg PD (2005) Settlement of larval blacklip abalone, Haliotis rubra, in response to red and green macroalgae. Mar Biol 147:1155–1163

    Article  Google Scholar 

  • 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 120:305–310

    Article  Google Scholar 

  • Johnson CR, Muir DG, Reysenbach AL (1991a) Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar Ecol Prog Ser 74:281–294

    Article  Google Scholar 

  • Johnson CR, Sutton DC, Olson RR, Giddins R (1991b) Settlement of crown-of-thorns starfish: role of bacteria on surfaces of coralline algae and hypothesis of deep water recruitment. Mar Ecol Prog Ser 71:143–162

    Article  Google Scholar 

  • Keesing JK (2001) The ecology of Heliocidaris erythrogramma. In: Lawrence JM (eds) Edible sea urchins: biology and ecology. Elsevier, New York, pp 261–270

    Chapter  Google Scholar 

  • Keough MJ, Raimondi PT (1995) Responses of settling invertebrate larvae to bioorganic films: effects of different types of films. J Exp Mar Biol Ecol 185:235–253

    Article  Google Scholar 

  • Kobak J (2001) Light, gravity and conspecifics as cues to site selection and attachment behaviour of juvenile and adult Dreissena polymorpha Pallas, 1771. J Mollusc Stud 67:183–189

    Article  Google Scholar 

  • Krug PJ (2001) Bet-hedging dispersal strategy of a specialist marine herbivore: settlement dimorphism among sibling larvae of Alderia modesta. Mar Ecol Prog Ser 213:177–192

    Article  Google Scholar 

  • Krug PJ, Manzi AE (1999) Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine herbivore Alderia modesta. Biol Bull 197:94–103

    Article  CAS  Google Scholar 

  • Lamare MD, Barker MF (2001) Settlement and recruitment of the New Zealand sea urchin Evechinus chloroticus. Mar Ecol Prog Ser 218:153–166

    Article  Google Scholar 

  • Lau SK, Qian PY (2001) Larval settlment in the serpulid polycheate Hydroides elegans in response to bacterial films: an investigation of the nature of putitative larval settlement cue. Mar Biol 138:321–328

    Article  Google Scholar 

  • Lau SCK, Mak KKW, Chen F, Qian PY (2002) Bioactivity of bacterial strains isolated from marine biofilms in Hong Kong waters for the induction of larval settlement in the marine polychaete Hydroides elegans. Mar Ecol Prog Ser 226:301–310

    Article  Google Scholar 

  • Lau SCK, Harder T, Qian P (2003) Induction of larval settlement in the serpulid polycheate Hydroides elegans (Haswell): role of bacterial extracellular polymers. Biofouling 19:197–204

    Article  PubMed  CAS  Google Scholar 

  • Lau SCK, Thiyagarajan V, Cheung SCK, Qian P-Y (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat Microb Ecol 38:41–51

    Article  Google Scholar 

  • Leitz T (1997) Induction and metamorphosis of cnidarian larvae: signals and signal transduction. Invertebr Reprod Dev 31:109–122

    Google Scholar 

  • Morse AC (1992) Role of algae in the recruitment of marine invertebrate larvae. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos, vol 46. Clarendon Press, Oxford, pp 385–403

  • Morse ANC, Froyd CA, Morse DE (1984) Molecules from cyanobacteria and red algae that induce settlement and metamorphosis in the mollusc Haliotis rufescens. Mar Biol 81:293–298

    Article  CAS  Google Scholar 

  • Neal AL, Yule AB (1994) The interaction between Elminius modestus Darwin cyprids and biofilms of Deleya marina Ncmb1877. J Exp Mar Biol Ecol 176:127–139

    Article  Google Scholar 

  • 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 223:121–131

    Article  Google Scholar 

  • Patil JS, Anil AC (2005) Influence of diatom exoploymers and biofilms on metamorphosis in the barnacle Balanus amphitrite. Mar Ecol Prog Ser 301:231–245

    Article  CAS  Google Scholar 

  • Pawlik JR (1992) Chemical ecology of the settlement of marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273–335

    Google Scholar 

  • Pearce CM, Scheibling RE (1991) Effect of macroalgae, microbial films, and conspecifics on the induction of metamorphosis of the green sea urchin Strongylocentrotus droebachiensis (Muller). J Exp Mar Biol Ecol 147:147–162

    Article  Google Scholar 

  • Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297

    Article  Google Scholar 

  • Prescott LM, Harley JP, Klein DA (1995) Microbiology, 3rd edn. Brown, Dubuque

    Google Scholar 

  • Raimondi PT, Morse ANC (2000) The consequences of complex larval behaviour in a coral. Ecology 81(11):3193–3211

    Article  Google Scholar 

  • Roberts R (2001) A review of settlement cues for larval abalone (Haliotis spp.). J Shellfish Res 20:571–586

    Google Scholar 

  • Rodriguez SR, Ojeda FP, Inestrosa NC (1993) Settlement of benthic marine invertebrates. Mar Ecol Prog Ser 97:193–207

    Article  Google Scholar 

  • Rodriguez SR, Riquelme C, Campos EO, Chavez P, Brandan E, Inestrosa NC (1995) Behavioral responses of Concholepas concholepas (Bruguiere, 1789) larvae to natural and artificial settlement cues and microbial films. Biol Bull 189:272–279

    Article  Google Scholar 

  • Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629

    Article  CAS  Google Scholar 

  • Steinberg PD, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, Fla., pp 355–387

    Google Scholar 

  • Swanson RL, Williamson JE, de Nys R, Kumar N, Bucknall MP, Steinberg PD (2004) Induction of settlement of larvae of the sea urchin Holopneustes purpurascens by histamine from a host alga. Biol Bull 206:161–172

    Article  PubMed  CAS  Google Scholar 

  • Switzer-Dunlap M (1978) Larval biology and metamorphosis of Aplysiid gastropods. In: Chia F-S, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 197–206

    Google Scholar 

  • Switzer-Dunlap M, Hadfield M (1977) Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropa: Opisthobranchia) in laboratory culture. J Exp Mar Biol Ecol 29:245–261

    Article  Google Scholar 

  • Szewzyk U, Holstrom C, Wrangstadh M, Samuelsson M-O, Maki JS, Kjelleberg S (1991) Relevance of the exopolysaccharide of marine Pseudomonas sp. strain S9 for the attachment of Ciona intestinalis larvae. Mar Ecol Prog Ser 75:259–265

    Article  Google Scholar 

  • Thompson RC, Roberts MF, Norton TA, Hawkins SJ (2000) Feast or famine for intertidal grazing molluscs: a mis-match between seasonal variations in grazing intensity and the abundance of microbial resources. Hydrobiologia 440:357–367

    Article  Google Scholar 

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    Article  Google Scholar 

  • Towbridge CD (1992) Phenology and demography of a marine specialist herbivore: Placida dendritica (Gastropoda: Opisthobrancha) on the central coast of Oregon. Mar Biol 114:443–452

    Article  Google Scholar 

  • Unabia CRC, Hadfield MG (1999) Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol 133:55–64

    Article  Google Scholar 

  • Underwood AJ, Keough MJ (2000) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, Mass., pp 183–200

    Google Scholar 

  • Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, Blackall LL, Negri AJ (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70:1213–1221

    Article  PubMed  CAS  Google Scholar 

  • Weiner RM, Williams N, Birch G, Ramachandran C, Collwell RR (1989) Effect of biofilms of the marine bacterium Alteromonas colwelliana (LST) on set of oysters Crassostrea gigas Thunberg 1793 and Crassostrea virginica Gmelin 1791. J Shellfish Res 8:117–124

    Google Scholar 

  • Wieczorek SK, Todd CD (1998) Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12:81–118

    Article  Google Scholar 

  • Wilkinson L (1997) SYSTAT 7.0. SPSS, Chicago, Ill.

    Google Scholar 

  • Williams DHC, Anderson DT (1975) The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Aust J Zool 23:371–403

    Article  Google Scholar 

  • Williamson JE, de Nys R, Kumar N, Carson DG, Steinberg PD (2000) Induction of metamorphosis in the sea urchin Holopneustes purpurascens by a metabolite complex from the algal host Delisea pulchra. Biol Bull 198:332–345

    Article  PubMed  CAS  Google Scholar 

  • Xue-wu L, Gordon ME (1987) Tissue and cell culture of New Zealand Pterocladia and Porphyra species. Hydrobiologia 151/152:147–154

    Article  Google Scholar 

  • Zhao B, Qian PY (2002) Larval settlement and metamorphosis in the slipper limpet Crepidula onyx (Sowerby) in response to conspecific cues and the cues from biofilm. J Exp Mar Biol Ecol 269:39–51

    Article  Google Scholar 

  • Zobell CE, Allen EC (1935) The significance of marine bacteria in the fouling of submerged surfaces. J Bacteriol 29:230–251

    Google Scholar 

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Acknowledgements

This research was supported by an Australian Postgraduate Award to M. J. H., an ARC Large Grant to P. D. S. and R. d. N., and the Centre for Marine Biofouling and BioInnovation. We thank Sabine Daume and Sylvain Hutchette for Ulvella lens' cultures and Rebecca Swanson, Sharon Longford, Mike Taylor and Carola Holmström for assistance in the laboratory and field. Three anonymous reviewers provided helpful comments to improve the manuscript.

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Correspondence to Megan J. Huggett.

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Huggett, M.J., Williamson, J.E., de Nys, R. et al. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149, 604–619 (2006). https://doi.org/10.1007/s00442-006-0470-8

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