Skip to main content

Advertisement

SpringerLink
Log in

Potential Invasion of Microorganisms and Pathogens via ‘Interior Hull Fouling’: Biofilms Inside Ballast Water Tanks

  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Surfaces submerged in an aquatic milieu are covered to some degree with biofilms – organic matrices that can contain bacteria, microalgae, and protozoans, sometimes including disease-causing forms. One unquantified risk of aquatic biological invasions is the potential for biofilms within ships’ ballast water tanks to harbor pathogens, and, in turn, seed other waters. To begin to evaluate this vector, we collected biofilm samples from tanks’ surfaces and deployed controlled-surface sampling units within tanks. We then measured a variety of microbial metrics within the biofilms to test the hypotheses that pathogens are present in biofilms and that biofilms have higher microbial densities compared to ballast water. Field experiments and sampling of coastwise and oceangoing ships arriving at ports in Chesapeake Bay and the North American Great Lakes showed the presence of abundant microorganisms, including pathogens, in biofilms. These results suggest that ballast-tank biofilms represent an additional risk of microbial invasion, provided they release cells into the water or they are sloughed off during normal ballasting operations.

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

Similar content being viewed by others

References

  • A Ali MH Rasid DKR Karaolis (2002) ArticleTitleHigh-frequency rugose exopolysaccharide production by Vibrio cholerae Applied and Environmental Microbiology 68 5773–5778 Occurrence Handle12406780

    PubMed  Google Scholar 

  • RI Amann W Ludwig KH Schleifer (1995) ArticleTitlePhylogenetic identification and in situ detection of individual microbial cells without cultivation Microbiological Review 59 143–169

    Google Scholar 

  • DM Anderson Y Fukuyo K Matsuoka (1995) Cyst methodologies GM Hallegraeff DM Anderson AD Cembella (Eds) Manual on Harmful Marine Microalgae UNESCO Paris 229–250

    Google Scholar 

  • Australian Quarantine and Inspection Service (2001) AQIS Approved Ballast Water Management Option for Ships Entering Australia from 1 July 2001. Agriculture Fisheries and Forestry–Australia.

  • RE Baier (1984) Initial events in microbial film formation JD Costlow RC Tipper (Eds) Marine Biodeterioration: An Interdisciplinary Study Naval Institute Press Annapolis, MD 57–62

    Google Scholar 

  • SI Blackburn GM Hallegraeff CJ Bolch (1989) ArticleTitleVegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatumTasmania Australian Journal of Phycology 25 577–590

    Google Scholar 

  • CJB Bolch (1997) ArticleTitleThe use of sodium polytungstate for the separation and concentration of living dinoflagellate cysts from marine sediments Phycologia 36 472–478

    Google Scholar 

  • HA Bowers T Tengs HB Glasgow SuffixJr JM Burkholder PA Rublee DW Oldach (2000) ArticleTitleDevelopment of real-time PCR assays for rapid detections of Pfiesteria piscicida and related dinoflagellates Applied and Environmental Microbiology 66 4641–4648

    Google Scholar 

  • JT Carlton (1985) ArticleTitleTransoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water Oceanography and Marine Biology Annual Review 23 313–371

    Google Scholar 

  • KR Carman FC Dobbs (1997) ArticleTitleEpibiotic microorganisms on copepods and other aquatic crustaceans Microscopy Research and Technique 37 116–135 Occurrence Handle10.1002/(SICI)1097-0029(19970415)37:2<116::AID-JEMT2>3.0.CO;2-M Occurrence Handle9145394

    Article  PubMed  Google Scholar 

  • N Choopun L Valérie A Huq RR Colwell (2002) ArticleTitleSimple procedure for rapid identification of Vibrio choleraefrom the aquatic environment Applied Environmental Microbiology 68 95–998 Occurrence Handle10.1128/AEM.68.2.995-998.2002

    Article  Google Scholar 

  • WJ Conover RL Inman (1981) ArticleTitleRank transformation as a bridge between parametric and non-parametric statistics The American Statistician 35 124–129

    Google Scholar 

  • JW Costerton PS Stewart EP Greenberg (1999) ArticleTitleBacterial biofilms: a common cause of persistent infections Science 284 1318–1322 Occurrence Handle10.1126/science.284.5418.1318 Occurrence Handle10334980

    Article  PubMed  Google Scholar 

  • AW Decho (1990) ArticleTitleMicrobial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes Oceanography and Marine Biology Annual Review 28 73–153

    Google Scholar 

  • AW Decho (2000) ArticleTitleMicrobial biofilms in intertidal systems: an overview Continental Shelf Research 20 1257–1273 Occurrence Handle10.1016/S0278-4343(00)00022-4

    Article  Google Scholar 

  • Doblin MA, Dobbs FC, Drake LA, Bednarski M, Coyne K, Heinemann S, DiTullio J, Kampschmidt L, Mullady T, Murphy K and Ruiz G (2003) Effects of open-oceanexchange on microbial communities in ships’ ballast tanks. Poster presented at the Third International Conference on Marine Bioinvasions. La Jolla, California

  • Doblin MA, Drake LA, Coyne KJ, Rublee PA and Dobbs FC (in press) Pfiesteriaspecies identified in ships’ ballast water and residuals: a possible vector for introductions to coastal areas. In: Proceedings from the Xth International Conference on Harmful Algae, St. Pete’s Beach, Florida.

  • LA Drake K-H Choi GM Ruiz FC Dobbs (2001) ArticleTitleGlobal redistribution of bacterioplankton and virioplankton communities Biological Invasions 3 193–199 Occurrence Handle10.1023/A:1014561102724

    Article  Google Scholar 

  • LA Drake GM Ruiz BS Galil TL Mullady DO Friedmann FC Dobbs (2002) ArticleTitleMicrobial ecology of ballast water during a trans-oceanic voyage Marine Ecology Progress Series 233 13–20

    Google Scholar 

  • Federal Register (1991) International Maritime Organization Ballast Water Control Guidelines, Notice, 56 FR 64831-64836 (12 December 1991)

  • Forsberg RL (2003) Surface characterization of naturally formed ballast biofilms and distributions of “benchmark” species. Masters thesis, Biomaterials Graduate Program, State University of New York at Buffalo, 120 pp

  • Forsberg R, Friedmann D, Drake L, Galil B, Hülsmann N, Meyer A, Dobbs F and Baier B (2002) Material surface control of ballast biofilm complexes introduced to Great Lakes. In: Proceedings 45th Conference on Great Lakes Research, pp 41–42

  • RRL Guillard (1975) Culture of phytoplankton for feeding marine invertebrates WI Smith MH Chanley (Eds) Culture of Marine Invertebrate Animals Plenum Press New York 29–60

    Google Scholar 

  • GM Hallegraeff (1998) ArticleTitleTransport of toxic dinoflagellates via ships’ ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies Marine Ecology Progress Series 168 297–309

    Google Scholar 

  • GM Hallegraeff CJ Bolch (1991) ArticleTitleTransport of toxic dinoflagellate cysts via ships’ ballast water Marine Pollution Bulletin 22 27–30 Occurrence Handle10.1016/0025-326X(91)90441-T

    Article  Google Scholar 

  • GM Hallegraeff CJ Bolch (1992) ArticleTitleTransport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture Journal of Plankton Research 14 1067–1084

    Google Scholar 

  • Hülsmann N, Galil B and Baier R (2000) Spatio-temporal distribution of viable heterotrophic protists in ballast water and sediments during a transatlantic voyage. Paper presented at the Aquatic Sciences Meeting hosted by the American Society of Limnology and Oceanography. Copenhagen, Denmark.

  • WP Johnson P Zhang MF Fuller TD Scheibe BJ Mailloux TC Onstott MF DeFlaun SS Hubbard J Radtke WP Kovacik W Holben (2000) ArticleTitleFerrographic tracking of bacterial transport in the field at the Narrow Channel Focus Area, Oyster, VA Environmental Science and Technology 35 182–191 Occurrence Handle10.1021/es001170e

    Article  Google Scholar 

  • WP Johnson P Zhang PM Gardner ME Fuller MF Flaun ParticleDe (2001) ArticleTitleEvidence for detachment of indigenous bacteria from aquifer sediment in response to arrival of injected bacteria Applied and Environmental Microbiology 67 4908–4913 Occurrence Handle10.1128/AEM.67.10.4908-4913.2001 Occurrence Handle11571201

    Article  PubMed  Google Scholar 

  • JM Kelly (1993) ArticleTitleBallast water and sediments as mechanisms for unwanted species introductions into Washington state Journal of Shellfish Research 12 405–410

    Google Scholar 

  • I Knight CS Wells B Wiggins H Russell KA Reynolds A Huq (1999) Detection and enumeration of fecal indicators and pathogens in the ballast water of transoceanic vessels entering the Great Lakes. In: General Meeting of the American Society for Microbiology American Society for Microbiology Washington, DC Chicago IL 594

    Google Scholar 

  • DM Lavoie LD Smith GM Ruiz (1999) ArticleTitleThe potential for intracoastal transfer of non-indigenous species in the ballast water of ships Estuarine, Coastal and Shelf Science 48 551–564

    Google Scholar 

  • K Matsuoka Y Fukuyo (1995) Taxonomy of cysts GM Hallegraeff DM Anderson AD Cembella (Eds) Manual on Harmful Marine Microalgae UNESCO Paris 381–401

    Google Scholar 

  • TA McCollin JP Hamer IAN Lucas (2000) Transport of phytoplankton via ships’s ballast into ports around England and Wales J. Pederson (Eds) Marine Bioinvasions: Proceedings of the First National Conference Massachusetts Institute of Technology, MIT Sea Grant College Program Cambridge, MA 282–288

    Google Scholar 

  • Meyer AE, Baier R, Hülsmann N, Galil B, Friedmann D and Forsberg R (2000) Risk assessment, prediction, and limitation of transport of bioinvaders in biofilms. Abstracts book, American Society of Limnology and Oceanography, Aquatic Sciences Meeting, June 5–9, 2000, Copenhagen, Denmark, abstract #SS08-p22

  • Meyer AE, Fornalik MS, Baier RE, King RW, Zambon JJ, Huber PS, Wattle BJ and Gucinski H (1984) Microfouling survey of Atlantic Ocean waters. In: Proceedings, 6thInternational Congress on Marine Corrosion and Fouling, pp 605–621.

  • RT Noble JA Fuhrman (1998) ArticleTitleUse of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria Aquatic Microbial Ecology 14 113–118

    Google Scholar 

  • JA Novitsky DM Karl (1986) ArticleTitleCharacterization of microbial activity in the surface layers of a coastal sub-tropical sediment Marine Ecology Progress Series 28 49–55

    Google Scholar 

  • TR Parsons Y Maita CM Lalli (1992) A Manual of Chemical and Biological Methods for Seawater Analysis Pergamon Press Elmsford 173

    Google Scholar 

  • GM Ruiz TK Rawlings FC Dobbs LA Drake T Mullady A Huq RR Colwell (2000) ArticleTitleGlobal spread of microorganisms by ships Nature 408 49–50 Occurrence Handle10.1038/35040695 Occurrence Handle11081499

    Article  PubMed  Google Scholar 

  • Schaefer EF (1997) A DNA assay to detect the toxic dinoflagellate Pfiesteria piscicida, and the application of a PCR based probe. MS thesis, Department of Biological Sciences, University of North Carolina-Greensboro, 86 pp

  • DL Smith MJ Wonham LD McCann GM Ruiz AH Hines JT Carlton (1999) ArticleTitleInvasion pressure to a ballast-flooded estuary and an assessment of inoculant survival Biological Invasions 1 67–89 Occurrence Handle10.1023/A:1010091918466

    Article  Google Scholar 

  • FJR Taylor U Pollingher (1987) Ecology of dinoflagellates FJR Taylor (Eds) The Biology of Dinoflagellates Blackwell Scientific Publications Oxford 399–529

    Google Scholar 

  • MJW Veldhuis TL Cucci ME Sieracki (1997) ArticleTitleCellular DNA content of marine phytoplankton using two new fluorochromes: taxonomic and ecological implications Journal of Phycology 33 527–541 Occurrence Handle10.1111/j.0022-3646.1997.00527.x

    Article  Google Scholar 

  • JJ Zambon PS Huber AE Meyer J Slots MS Fornalik RE Baier (1984) ArticleTitleIn situ identification of bacterial species in marine microfouling films by using an immunofluorescence technique Applied and Environmental Microbiology 48 1214–1220 Occurrence Handle6393875

    PubMed  Google Scholar 

  • P Zhang WP Johnson R Rowland (1999a) ArticleTitleBacterial tracking using ferrographic separation Environmental Science and Technology 33 2456–2460 Occurrence Handle10.1021/es990059+

    Article  Google Scholar 

  • P Zhang WP Johnson V Westcott W Seifert (1999b) ArticleTitleRapid selective ferrographic enumeration of bacteria Journal of Magnetism and Magnetic Materials 194 267–274 Occurrence Handle10.1016/S0304-8853(98)00582-4

    Article  Google Scholar 

  • Y Zo C Grimm M Matte G Matte I Knight A Huq RR Colwell (1999) Detection and enumeration of pathogenic bacteria in ballast water of transoceanic vessels entering the Great Lakes and resistance to common antibiotics. In: General Meeting of the American Society for Microbiology American Society for Microbiology Chicago IL, Washington, DC 594

    Google Scholar 

  • CE ZoBell DQ Anderson (1936) ArticleTitleObservations on the multiplication of bacteria in different volumes of stored sea water and the influence of oxygen tension and solid surfaces Biological Bulletin 71 324–342

    Google Scholar 

Download references

Author information

Author notes

  1. Lisa A. Drake

    Present address: Department of Science, Marine Science Section, US Coast Guard Academy, 27 Mohegan Avenue, New London, CT, 06320, USA

Authors and Affiliations

  1. Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, 4600 Elkhorn Avenue, Norfolk, VA, 23529, USA

    Lisa A. Drake, Martina A. Doblin, Stefan Heinemann & Fred C. Dobbs

  2. Industry/University Center for Biosurfaces, University at Buffalo, 110 Parker Hall, Buffalo, NY, 14214, USA

    Anne E. Meyer, Robert L. Forsberg & Robert E. Baier

  3. Department of Geology and Geophysics, University of Utah, 135 South 1460 East, Salt Lake City, UT, 84112, USA

    William P. Johnson & Michael Koch

  4. Department of Biology, University of North Carolina Greensboro, 312 Eberhart Building, Greensboro, NC, 27402, USA

    Parke A. Rublee

Authors
  1. Lisa A. Drake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne E. Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert L. Forsberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert E. Baier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martina A. Doblin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stefan Heinemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. William P. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michael Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Parke A. Rublee
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fred C. Dobbs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa A. Drake.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Drake, L.A., Meyer, A.E., Forsberg, R.L. et al. Potential Invasion of Microorganisms and Pathogens via ‘Interior Hull Fouling’: Biofilms Inside Ballast Water Tanks. Biol Invasions 7, 969–982 (2005). https://doi.org/10.1007/s10530-004-3001-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-004-3001-8

Keywords

Search

Navigation