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Influence of bacteria and diatoms in biofilms on metamorphosis of the marine slipper limpet Crepidula onyx

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Abstract

Larvae of the slipper limpet Crepidula onyx metamorphose in response to marine biofilms. In this study, we investigated how the percentage of larval metamorphosis in this species was affected by biofilms that differed in certain attributes. To manipulate bacterial and diatom cell densities and community composition, we developed biofilms in the laboratory (1) at different temperatures (16, 23 and 30°C) and salinities (20, 27 and 34‰), (2) with or without addition of antibiotics, and (3) in the light or in the dark. We also allowed biofilms to develop at three field sites with different prevailing environmental conditions so as to generate biofilms with different, but natural, attributes. Bacterial and diatom community composition in biofilms were determined using a DNA fingerprinting technique and microscopic examination, respectively. The effects of biofilms on metamorphosis were investigated in laboratory assays. The percentage of larval metamorphosis correlated with bacterial and diatom cell densities in only one of the three experiments conducted, but was substantially affected by differences in bacterial and diatom community composition in all three experiments. It also appears that metamorphosis of C. onyx depends on the simultaneous presence of both bacterial and diatom communities in biofilms.

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References

  • Anderson MJ (1995) Variations in biofilms colonizing artificial surfaces: seasonal effects and effects of grazers. Mar Biol 75:705–714

    Google Scholar 

  • Avelin SRM, Vitalina SRM, Rittschof D, Nagabhushanam R (1993) Bacterial–barnacle interaction: potential of using juncellins and antibiotics to alter structure of bacterial communities. J Chem Ecol 19:2155–2167

    Article  Google Scholar 

  • Bonar DB, Weiner RM, Colwell RR (1986) Microbial-invertebrate interactions and potential for biotechnology. Microb Ecol 12:101–110

    Article  CAS  Google Scholar 

  • Brandini FP, Da Silva ET, Pellizzari FM, Fonseca ALO, Fernandes LF (2001) Production and biomass accumulation of periphytic diatoms growing on glass slides during a 1-year cycle in a subtropical estuarine environment (Bay of Paranagua, southern Brazil). Mar Biol 138:163–171

    Article  CAS  Google Scholar 

  • Bryan PJ, Qian PY (1998) Induction of larval attachment and metamorphosis in the abalone Haliotis diversicolor (Reeve). J Exp Mar Biol Ecol 223:39–51

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Natural Environmental Research Council, Plymouth

    Google Scholar 

  • Coe WR (1935) Sexual phases in prosobranch mollusks of the genus Crepidula. Science 81:570–572

    Article  CAS  Google Scholar 

  • Daume S, Brand-Gardner S, Woelkerling W (1999) Preferential settlement of abalone larvae: diatom films vs. non-geniculate coralline red algae. Aquaculture 174:243–254

    Article  Google Scholar 

  • Ebert E, Houk J (1984) Elements and innovations in the cultivation of red abalone Haliotis diversicolor (Reeve). Aquaculture 39:375–392

    Article  Google Scholar 

  • Eilers H, Pernthaler J, Glockner FO, Amann R (2000) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66:3044–3051

    Article  CAS  Google Scholar 

  • Eyster LS, Pechenik JA (1988) Comparison of growth, respiration, and feeding of juvenile Crepidula fornicata (L.) following natural or KCl-triggered metamorphosis. J Exp Mar Biol Ecol 118:269–279

    Article  Google Scholar 

  • Griffith P, Shiah FK, Gloersen K, Ducklow HW, Fletcher M (1994) Activity and distribution of attached bacteria in Chesapeake Bay. Mar Ecol Prog Ser 108:1–10

    Article  Google Scholar 

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

    Chapter  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 

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

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang ZG, Morton B, Yip YW (1984) The distribution and ecological and biological features of Crepidula onyx in Hong Kong. Acta Oceanol Sin 5:827–839

    Google Scholar 

  • Ito S, Kitamura H (1997) Induction of larval metamorphosis in the sea cucumber Stichopus japonicus by periphitic diatoms. Hydrobiologia 358:281–284

    Article  Google Scholar 

  • Kawamura T, Kikuchi S (1992) Effects of benthic diatoms on settlement and metamorphosis of abalone larvae. Suisanzoshoku 40:403–409

    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 158:235–253

    Article  Google Scholar 

  • Keough MJ, Raimondi PT (1996) Responses of settling invertebrate larvae to bioorganic films: effects of large-scale variation in films. J Exp Mar Biol Ecol 207:59–78

    Article  Google Scholar 

  • Lam C, Harder T, Qian PY (2003) Induction of larval settlement in the polychaete Hydroides elegans by surface-associated settlement cues of marine benthic diatoms. Mar Ecol Prog Ser 263:83–92

    Article  Google Scholar 

  • Lau SCK, Thiyagarajan V, Cheung SCK, Qian PY (2005) A laboratory investigation of the role of bacterial community in biofilm as an indicator of local environmental conditions for the settling larvae of marine invertebrates. Aquat Microbial Ecol 38:41–51

    Article  Google Scholar 

  • Le Tourneux F, Bourget E (1988) Importance of physical and biological settlement cues used at different scales by the larvae of Semibalanus balanoides. Mar Biol 97:57–66

    Article  Google Scholar 

  • Lima GM, Pechenik JA (1985) The influence of temperature on growth rate and length of larval life of the gastropod Crepidula plana (Say). J Exp Mar Biol Ecol 90:55–71

    Article  Google Scholar 

  • Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maki JS, Rittschof D, Costlow JD, Mitchell R (1988) Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface film. Mar Biol 97:199–206

    Article  Google Scholar 

  • Maki JS, Ding L, Stokes J, Kavouras JH, Rittschof D (2000) Substratum/bacterial interactions and larval attachment: Films and exopolysaccharides of Halomonas marina (ATCC 25374) and their effect on barnacle cyprid larvae, Balanus amphitrite Darwin. Biofouling 16:159–170

    Article  CAS  Google Scholar 

  • McGee BL, Targett NM (1989) Larval habitat selection in Crepidula (L.) and its effect on adult distribution patterns. J Exp Mar Biol Ecol 131:195–214

    Article  Google Scholar 

  • Miron G, Boudreau B, Bourget E (1999) Intertidal barnacle distribution: a case study using a multiple working hypothesis. Mar Ecol Prog Ser 189:205–219

    Article  Google Scholar 

  • Montiel YA, Chaparro OR, Segura CJ (2005) Changes in feeding mechanisms during early ontogeny in juveniles of Crepidula fecunda (Gastropoda: Calyptraeidae). Mar Biol 147:1333–1342

    Article  Google Scholar 

  • Navarro JM, Chaparro OR (2002) Grazing-filtration as feeding mechanisms in motile specimens of Crepidula fecunda (Gastropoda: Calyptraeidae). J Exp Mar Biol Ecol 270:111–122

    Article  Google Scholar 

  • Olivier F, Tremblay R, Bourget E, Rittschof D (2000) Barnacle settlement: field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus amphitrite cyprids. Mar Ecol Prog Ser 199:185–204

    Article  Google Scholar 

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

    Google Scholar 

  • Pearce CM, Scheibling RE (1991) Effects of macroalgae, microbial films and conspecifics on the induction of metamorphosis of the green sea urchin Strongylocentrotus droebrachiensis (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 

  • Pechenik JA, Gee CC (1993) Onset of metamorphic competence in larvae of the gastropod Crepidula fornicata (L.), judged by a natural and an artificial cue. J Exp Mar Biol Ecol 167:59–72

    Article  Google Scholar 

  • Pechenik JA, Heyman WD (1987) Using KCl to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol 112:27–38

    Article  Google Scholar 

  • Pechenik JA, Li W, Cochrane DE (2002) Timing is everything: the effects of putative dopamine antagonists on metamorphosis vary with larval age and experimental duration in the prosobranch gastropod Crepidula fornicata. Biol Bull 202:137–147

    Article  CAS  Google Scholar 

  • Qian PY, Thiyagarajan V, Lau SCK, Cheung SCK (2003) Relationship between bacterial community profile in biofilm and attachment of the acorn barnacle Balanus amphitrite. Aquat Microb Ecol 33:225–237

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. University Press, Cambridge, pp 199–201

    Book  Google Scholar 

  • Rittschof D, Branscomb ES, Costlow JD (1984) Settlement and behavior in relation to flow and surface in larval barnacles, Balanus amphitrite Darwin. J Exp Mar Biol Ecol 82:131–146

    Article  Google Scholar 

  • Slattery M (1992) Larval settlement and juvenile survival in the red abalone (Haliotis rufescens): an examination of inductive cues and substrate selection. Aquaculture 102:143–153

    Article  Google Scholar 

  • Sonak S, Bhosle NB (1995) Observations on biofilm bacteria isolated from aluminum panels immersed in estuarine waters. Biofouling 8:243–254

    Article  Google Scholar 

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

    Google Scholar 

  • Strathmann RR, Branscomb ES, Vedder K (1981) Fatal errors in set as a cost of dispersal and the influence of intertidal flora on set of barnacles. Oecologia 48:13–18

    Article  CAS  Google Scholar 

  • Tani Y, Ito Y (1979) Effects of benthic diatoms on settlement and metamorphosis of the sea urchin, Pseudocentrotus depressus. Suisanzoshoku 27:148–150

    Google Scholar 

  • Thompson RC, Norton TA, Hawkins SJ (1998) The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids—a comparison between laboratory and field experiments. Hydrobiologia 375:203–216

    Article  Google Scholar 

  • Thornton DCO, Dong LF, Underwood GJC, Nedwell DB (2002) Factors affecting microphytobenthic biomass, species composition and production in the Colne Estuary (UK). Aquat Microb Ecol 27:285–300

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Todd CD, Keough MJ (1994) Larval settlement in hard substratum epifaunal assemblages: a manipulative field study of the effects of substratum filming and the presence of incumbents. J Exp Mar Biol Ecol 181:159–187

    Article  Google Scholar 

  • Tomas CR (ed) (1996) Identifying marine diatoms and dinoflagellates. Academic, San Diego

  • 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 

  • Wieczorek SK, Murray AWA, Todd CD (1996) Seasonal variation in the effects of hard substratum biofilming on settlement of marine invertebrate larvae. Biofouling 10:309–330

    Article  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Englewood Cliffs

    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 

  • Zhao B, Qiu JW, Qian PY (2003) Effects of food availability on larval development in the slipper limpet Crepidula onyx (Sowerby). J Exp Mar Biol Ecol 294:219–233

    Article  Google Scholar 

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Acknowledgments

This manuscript was greatly benefited by the comments and suggestions by two anonymous reviewers, especially those on the statistical analysis and interpretation. We also wish to thank Stanley Lau (National University of Singapore) for his advice on drafting this manuscript. We are grateful to Mandy Tsoi and Ki Tam for kindly assisting in the terminal-restriction fragment length polymorphism analysis and technical supports. This study was supported by the Area of excellence scheme of UGC (project#AoE/P–04/2004) and RGC grants (HKUST 6402/05M) to PY Qian.

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Authors and Affiliations

  1. Department of Biology/Coastal Marine Laboratory, The Hong Kong University of Science and Technology, Clearwater Bay, Kowloon, Hong Kong SAR, China

    Jill Man-Ying Chiu, Vengatesen Thiyagarajan, Oi-Shing Hung & Pei-Yuan Qian

  2. Biology Department, Tufts University, Medford, MA, 02155, USA

    Jan A. Pechenik

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  1. Jill Man-Ying Chiu
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  2. Vengatesen Thiyagarajan
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  3. Jan A. Pechenik
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  4. Oi-Shing Hung
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  5. Pei-Yuan Qian
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Correspondence to Pei-Yuan Qian.

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Communicated by S. Nishida, Tokyo.

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Chiu, J.MY., Thiyagarajan, V., Pechenik, J.A. et al. Influence of bacteria and diatoms in biofilms on metamorphosis of the marine slipper limpet Crepidula onyx . Mar Biol 151, 1417–1431 (2007). https://doi.org/10.1007/s00227-006-0580-1

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  • DOI: https://doi.org/10.1007/s00227-006-0580-1

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