Skip to main content
SpringerLink
Log in

Cypris Habitat Selection Facilitated by Microbial Films Influences the Vertical Distribution of Subtidal Barnacle Balanus trigonus

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The potential driving force(s) of the vertical distribution of subtidal barnacle Balanus trigonus Darwin were investigated using both field and laboratory experiments. Early juveniles (∼24 h old) placed in intertidal [∼0.5 m above mean low water level (MLWL)] and subtidal (∼3 m below MLWL) habitats survived equally well, indicating that the intertidal absence of B. trigonus in Hong Kong waters was not determined by differential mortality. However, enhanced attachment of cyprids in subtidal habitats indicated the importance of differential larval choice in determining their vertical distribution. In the laboratory, cyprids preferred to attach in response to subtidal microbial films, which may implicate microbial films as a primary cue in driving the adult vertical distribution. Microbial films developed in these two habitats differed in their biomass (=total organic carbon), abundance of bacteria and diatoms (determined by fluorescence microscopy), and bacterial diversity (determined by DNA fingerprinting analysis). For example, 6-day films in subtidal habitat had a significantly higher biomass than in films from intertidal habitat (P<0.05). There was no difference in the biomass of films from these two habitats in 9-day films (P>0.05); however, bacterial abundance was greater in subtidal films than in intertidal films, irrespective of the age of the film, although there was no difference in diatom abundance in films from these two habitats. Neither the abundance of bacteria and diatoms nor the biomass correlated with the attachment preferences of cyprids. This study has not provided any data to prove the existence of inductive and inhibitive (to cyprid attachment) bacterial species in subtidal and intertidal films, respectively; however, results indicate that bacterial community provided qualitative information that might explain the preferential attachment of B. trigonus cyprids in subtidal habitat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Baird, AH, Babcock, RC, Mundy, CP (2003) Habitat selection by larvae influences the depth distribution of six common coral species. Mar Ecol Prog Ser 252: 289–293

    Article  Google Scholar 

  2. Bertness, MD, Gaines, SD, Stephens, EG, Yund, PO (1992) Components of recruitment in populations of the acorn barnacle Semibalanus balanoides (Linnaeus). J Exp Mar Biol Ecol 156: 199–215

    Article  Google Scholar 

  3. Bingham, BL (1992) Life histories in an epifaunal community: coupling of adult and larval process. Ecology 73: 2244–2259

    Article  Google Scholar 

  4. Clare, AS, Freet, RK, McClary, MJ (1994) On the antennular secretion of the cyprid of Balanus amphitrite amphitrite, and its role as a settlement pheromone. J Mar Biol Assoc UK 74: 243–250

    Article  Google Scholar 

  5. Connell, JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42: 710–723

    Article  Google Scholar 

  6. Delany, J, Myers, AA, McGrath, D, O'Riordan, RM, Power, AM (2003) Roles of post-settlement mortality and “supply-side” ecology in settling patterns of intertidal distribution in the chthamalid barnacles Chthamalus montagui and C. stellatus. Mar Ecol Prog Ser 249: 207–214

    Article  Google Scholar 

  7. Denley, EJ, Underwood, AJ (1979) Experiments on factors influencing settlement, survival, and growth of two species of barnacles in New South Wales. J Exp Mar Biol Ecol 36: 269–293

    Article  Google Scholar 

  8. Dollhopf, SL, Hashsham, SA, Tiedje, JM (2001) Interpreting 16S rDNA T-RFLP data: application of self-organizing maps and principal components analysis to describe community dynamics and convergence. Microb Ecol 42: 495–505

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  10. Findlay, RH, Watling, L (1998) Seasonal variation in the structure of a marine benthic microbial community. Microb Ecol 36: 23–30

    Article  PubMed  Google Scholar 

  11. Finelli, CM, Wethey, DS (2003) Behavior of oyster (Crassostrea virginica) larvae in flume boundary layer flows. Mar Biol 143: 703–711

    Article  Google Scholar 

  12. Fletcher, M (1977) The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Can J Microbiol 23: 1–6

    Article  Google Scholar 

  13. Foster, BA (1971) Desiccation as a factor in the intertidal zonation of barnacles. Mar Biol 8: 12–29

    Article  Google Scholar 

  14. Freiberger, A, Cologer, CP (1966) Rearing acorn barnacle cyprids in the laboratory for marine fouling studies. J Am Soc Nav Eng 78: 881–890

    Google Scholar 

  15. Gaines, S, Roughgarden, J (1985) Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone. Proc Natl Acad Sci 82: 3707–3711

    Article  PubMed  Google Scholar 

  16. Grassle, JP, Butman, CA, Mills, SW (1992) Active habitat selection by Capitella spp. I and II. Multiple-choice experiments in still water and flume flows. J Mar Res 50: 717–743

    Article  Google Scholar 

  17. Grosberg, RK (1982) Intertidal zonation of barnacles: the influence of planktonic zonation of larvae on vertical distribution of adults. Ecology 63: 894–899

    Article  Google Scholar 

  18. Harder, T, Thiyagarajan, V, Qian, PY (2001) Effect of cyprid age on the settlement of Balanus amphitrite Darwin in response to natural biofilms. Biofouling 17: 211–219

    Google Scholar 

  19. Heuer, H, Wieland, G, Schoenfeld, J, Schoenwaelder, A, Gomes, NCM, Smalla, K (2001) Bacterial community profiling using DGGE or TGGE analysis. In: Rochelle, PA (Ed.) Environmental Molecular Microbiology: Protocols and Applications. Horizon Scientific Press, UK, pp 177–190

    Google Scholar 

  20. Holmstrom, C, Kjelleberg, S (2000) Bacterial interactions with marine fouling organisms. In: Evans, LV (Ed.) Biofilms: Recent Advances in their Study and Control. Harwood Academic Publisher, Amsterdam, pp 101–115

    Google Scholar 

  21. Jarrett, JN, Pechenik, JA (1997) Temporal variation in cyprid quality and juvenile growth capacity for an intertidal barnacle. Ecology 78: 1262–1265

    Article  Google Scholar 

  22. Jeffery, CJ (2002) New settlers and recruits do not enhance settlement of a gregarious intertidal barnacle in New South Wales. J Exp Mar Biol Ecol 275: 131–146

    Article  Google Scholar 

  23. Kirchman, D, Mitchell, R (1979) Adaptation of bacteria to rapidly changing environmental conditions. Biol Bull 157: 375–376

    Google Scholar 

  24. Lau, SCK, Thiyagarajan, V, Qian, PY (2003) The bioactivity of bacterial isolates in Hong Kong waters for the inhibition of barnacle (Balanus amphitrite Darwin) settlement. J Exp Mar Biol Ecol 282: 43–60

    Article  Google Scholar 

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

    Article  Google Scholar 

  26. Maki, JS, Rittschof, D, Mitchell, R (1992) Inhibition of larval barnacle attachment to bacterial films: an investigation of physical properties. Microb Ecol 23: 97–106

    Article  Google Scholar 

  27. Minchinton, TE, Scheibling, RE (1993) Free space availability and larval substratum selection on determinants of barnacle population structure in a developing rocky intertidal community. Mar Ecol Prog Ser 95: 233–244

    Article  Google Scholar 

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

    Article  Google Scholar 

  29. Mitchell, R, Maki, JS (1988) Microbial surface films and their influence on larval settlement and metamorphosis in the marine environment. In: Thompson, M, Sarojini, R, Nagabhushanam, R (Eds.) Marine Biodeterioration: Advanced Techniques Applicable to the Indian Ocean, Oxford and IBH Publishing, New Delhi, India, pp 489–497

    Google Scholar 

  30. Muyzer G, Brinkoff, T, Nuebel, U, Santegoeds, C, Schaefer, H, Wawer, C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. Mol Microbial Ecol Man 3: 1–27

    Google Scholar 

  31. Nubel, U, Engelen, B, Felske, A, Snaidr, J, Wieshuber, A, Amann, RI, Ludwig, W, Backhaus, H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178: 5636–5643

    PubMed  CAS  Google Scholar 

  32. 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 

  33. Pineda, J, Riebensahm, D, Medeiros-Bergen, D (2002) Semibalanus balanoides in winter and spring: larval concentration, settlement, and substrate occupancy. Mar Biol 140: 789–800

    Article  Google Scholar 

  34. 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 

  35. Raimondi, PT (1988) Settlement cues and determination of the vertical limit of an intertidal barnacle. Ecology 69: 400–407

    Article  Google Scholar 

  36. Roberts, D, Rittschof, D, Holm, E, Schmidt, AR (1991) Factors influencing initial larval settlement: temporal, spatial and surface molecular components. J Exp Mar Biol Ecol 150: 203–211

    Article  Google Scholar 

  37. Satumanatpan, S, Keough, MJ (2001) Roles of larval supply and behavior in determining settlement of barnacles in a temperate mangrove forest. J Exp Mar Biol Ecol 260: 133–153

    Article  PubMed  Google Scholar 

  38. Snelgrove, PVR, Grant, J, Pilditch, CA (1999) Habitat selection and adult–larvae interactions in settling larvae of soft-shell clam Mya arenaria. Mar Ecol Prog Ser 182: 149–159

    Article  Google Scholar 

  39. Steinberg, PD, Nys, RD, Kjelleberg, S (2001) Chemical mediation of surface colonization. In: McClintock, JB, Baker, JB (Eds.) Marine Chemical Ecology. CRC Press, Boca Raton, FL, pp 355–387

    Google Scholar 

  40. 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  Google Scholar 

  41. Svane, IB, Young, CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27: 45–90

    Google Scholar 

  42. Thiyagarajan, V, Harder, T, Qian, PY (2003) Combined effects of temperature and salinity on larval development and attachment of the subtidal barnacle Balanus trigonus Darwin. J Exp Mar Biol Ecol 287: 223–236

    Article  Google Scholar 

  43. Thiyagarajan, V, Harder, T, Qiu, JW, Qian, PY (2003) Energy content at metamorphosis and growth rate of the early juvenile barnacle Balanus amphitrite. Mar Biol 143: 543–554

    Article  Google Scholar 

  44. Thomason, 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 

  45. Todd, CD (2003) Assessment of a trap for measuring larval supply of intertidal barnacles on wave-swept, semi-exposed shores. J Exp Mar Biol Ecol 290: 247–269

    Article  Google Scholar 

  46. Tsurumi, K, Fusetani, N (1998) Effects of early fouling communities formed in the field on settlement and metamorphosis of cyprids of the barnacle, Balanus amphitrite Darwin. Biofouling 12: 119–131

    Google Scholar 

  47. Walters, LJ, Miron, G, Bourget, E (1999) Endoscopic observations of invertebrate larval substratum exploration and settlement. Mar Ecol Prog Ser 182: 95–108

    Article  Google Scholar 

  48. Werner, WE (1967) The distribution and ecology of the barnacle Balanus trigonus. Bull Mar Sci 17: 64–84

    Google Scholar 

  49. Wieczorek, SK, Todd, CD (1998) Biofilm cues and larval settlement. Biofouling 12: 81–118

    Article  Google Scholar 

  50. Wintzingerode, FV, Goebel, UB, Stackebrandt, E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21: 213–229

    Article  Google Scholar 

  51. Zar, JH (1999) Biostatistical Analysis, 4th edn. Prentice-Hall, Englewood Cliffs, NJ 07632

    Google Scholar 

  52. Zhou, J, Bruns, MA, Tiedje, JM (1996) DNA recovery from soil of diverse composition. App Environ Microbiol 62: 316–322

    CAS  Google Scholar 

Download references

Acknowledgments

Special thanks are extended to Dr. T. Harder (University of Oldenburg, Germany) for productive discussions, M.M.Y. Tsoi for assistance in DGGE analysis, L. Soo and Y. K. Tam for assistance in algal cultures and TOC analysis, and Dr. V. Unkefer (technical writer, HKUST) for English correction. We also wish to thank three anonymous referees, whose comments made a significant contribution to the final version of this article. This work was supported by RGC grants (CA00/01.SC01, HKUST6119/01M, HKUST6100/02M, HKUST 6281/03M) to P.Y. Qian.

Author information

Authors and Affiliations

  1. Department of Biology, The Hong Kong University of Science and Technology, Hong Kong SAR, China

    Vengatesen Thiyagarajan, Stanley C. K. Lau, Sam C. K. Cheung & Pei-Yuan Qian

Authors
  1. Vengatesen Thiyagarajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stanley C. K. Lau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sam C. K. Cheung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pei-Yuan Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pei-Yuan Qian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thiyagarajan, V., Lau, S.C.K., Cheung, S.C.K. et al. Cypris Habitat Selection Facilitated by Microbial Films Influences the Vertical Distribution of Subtidal Barnacle Balanus trigonus . Microb Ecol 51, 431–440 (2006). https://doi.org/10.1007/s00248-006-9041-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9041-0

Keywords

Search

Navigation