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Marine Biology

, Volume 149, Issue 1, pp 7–16 | Cite as

A new photodegradable molecule as a low impact ballast water biocide: efficacy screening on marine organisms from different trophic levels

  • M. Faimali
  • F. Garaventa
  • E. Chelossi
  • V. Piazza
  • O.D. Saracino
  • F. Rubino
  • G.L. Mariottini
  • L. Pane
Research Article

Abstract

Marine species carried by the ships’ ballast waters are a potentially serious environmental problem. Many strategies are being adopted to minimize the transfer of invasive or pathogenic marine species between different aquatic ecosystems. This problem is often addressed by using biocides for ballast water treatment; however, the biocide could be dangerous to native organisms once the ballast water is discharged. Chemical treatments such as chlorination and addition of glutaraldehyde could cause problems related to toxicity and application costs. The search for new effective molecules with a low environmental impact is pressing. This paper presents data from a preliminary efficacy screening of a promising molecule derived from alkylated naphtoquinones on a battery of ballast water model organisms. Results show that this new molecule is very effective in the absence of light and is extremely photodegradable (half-life <6 h). It can thus be easily degraded when released in the environment.

Keywords

Minimum Inhibitory Concentration Dinoflagellate Biocide Ballast Water Minimum Bactericidal Concentration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Vanetta S.p.A. Milano for the financial support.

References

  1. Bailey SA, Duggan IC, van Overdijk CDA (2003) Viability of invertebrate diapausing eggs collected from residual ballast sediment. Limnol Oceanogr 48(4):1701–1710CrossRefGoogle Scholar
  2. Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27(4):313–323CrossRefGoogle Scholar
  3. Benson HJ (1990) Microbiological applications: a laboratory manual in general microbiology. Wm. C. Brown Publishers, DubuqueGoogle Scholar
  4. Carli A, Fiori A (1977) Morphological analysis of the two Tigriopus species found along the European coast (Copepoda Harpacticoida). Natura 68:101–110Google Scholar
  5. Carli A, Mariottini GL, Pane L (1989) Reproduction of the rook pools harpacticoid copepod Tigriopus fulvus (Fischer 1860), suitable for aquaculture. Deuxième Congrès International d’Aquariologie, 1988, Monaco. Bull Inst Ocèanogr Monaco Spécial 5:295–300Google Scholar
  6. Carli A, Pane L, Casareto L, Bertone S, Pruzzo C (1993) Occurrence of Vibrio alginolyticus in Ligurian coast rock pools (Tyrrhenian Sea, Italy) and its association with the copepod Tigriopus fulvus (Fischer 1860). Appl Environ Microbiol 59:1960–1962PubMedPubMedCentralGoogle Scholar
  7. Carlton JT (1987) Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bull Mar Sci 41:452–465Google Scholar
  8. Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273CrossRefGoogle Scholar
  9. Carlton JT (1996) Marine bioinvasions: the alteration of marine ecosystems by non-indigenous species. Oceanography 9:36–43CrossRefGoogle Scholar
  10. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  11. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–557CrossRefGoogle Scholar
  12. Colwell RR, Seidler RJ, Kaper J, Joseph SW, Garges S, Lockman H, Maneval D, Bradford H, Roberts N, Remmers E, Huq I, Huq A (1981) Occurrence of Vibrio cholerae serotype 01 in Maryland and Louisiana estuaries. Appl Environ Microbiol 41:555–558PubMedPubMedCentralGoogle Scholar
  13. Colwell RR (1996) Global climate and infectious disease: the cholera pardigm. Science 274:2025–2031CrossRefGoogle Scholar
  14. Colwell RR (2000) Bacterial death revisited. In: Colwell RR, Grimes DJ (eds) Nonculturable microorganisms in the environment. American Society for Microbiology, Washington, DC, pp 325–342CrossRefGoogle Scholar
  15. Cutler HG, Belson NA, Dawson R, Wright DA (2000) Method for treating aquatic pest. US Patent 6,164,244, pp 164–244Google Scholar
  16. Cutler HG, Cutler SJ, Dawson R, Wright DA (2002) Method of controlling zoological and aquatic plant growth. US Patent 3,602,194, pp340–468Google Scholar
  17. Drake LA, Ruiz GM, Galil BS, Mullady TL, Friedmann DO, Dobbs FC (2002) Microbial ecology of ballast water during a transoceanic voyage and the effects of open-sea exchange. Mar Ecol Prog Ser 233:13–20CrossRefGoogle Scholar
  18. Faimali M, Sepčić K, Turk T, Geraci S (2003) Non-toxic antifouling activity of polymeric 3-alkylpyridinium salts from the Mediterranean sponge Reniera sarai (Pulitzer Finali). Biofouling 19(1):47–56CrossRefGoogle Scholar
  19. Fernández-Alba AR, Hernando MD, Piedra L, Chisti Y (2002) Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal Chim Acta 456:303–312CrossRefGoogle Scholar
  20. Finney DJ (1978) Statistical method in biological assay, 3rd (edn). Charles Griffin & Co. Ltd., London, 508 ppGoogle Scholar
  21. Forget J, Pavillon JF, Menasria MR, Bocquene G (1998) Mortality and LC50 values for several stages of the marine copepod Tigriopus brevicornis (Muller) exposed to the metals arsenic and cadmium. Ecotoxicol Environ Saf 40(3):239–244CrossRefGoogle Scholar
  22. Fuchs R, Steiner RN, de Wild I, Voigt M (2001) Paraclean ocean-a potential ballast water treatment option. Abstract 1st. In: Proceedings of the international ballast water treatment R & D symposium IMO, London, EnglandGoogle Scholar
  23. Gaggi C, Sbrilli G, Elnaby A, Bucci M, Duccini M, Bacci E (1995) Toxicity and hazard ranking of s-triazine herbicides using microtox®, two green algal species and a marine crustacean. Environ Toxicol Chem 14(6):1065–1069Google Scholar
  24. Galil BS (2000) A sea under siege–alien species in the Mediterranean. Biol Invasions 2:177–186CrossRefGoogle Scholar
  25. Galil BS, Hülsmann N (1997) Protist transport via ballast water, biological classification of ballast tanks by food web interactions. Eur J Protistol 33:244–253CrossRefGoogle Scholar
  26. Hai Y, Gang P (2002) Toxicity and bioaccumulation of copper in three green microalgal species. Chemosphere 49:471–476CrossRefGoogle Scholar
  27. Hallegraeff GM, Bolch CJ (1991) Transport of toxic dinoflagellate cysts via ships’ ballast water. Mar Poll Bull 22:27–30CrossRefGoogle Scholar
  28. Hallegraeff GM, Bolch CJ (1992) Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. J Plankton Res 14:1067–1084CrossRefGoogle Scholar
  29. Hamer JP, McCollin TA, Lucas IAN (1998) Viability of decapod larvae in ships’ ballast water. Mar Poll Bull 36(8):646–647CrossRefGoogle Scholar
  30. Hellio C, De La Broise D, Dufosse L, Le Gal Y, Bourgougnon N (2001) Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar Environ Res 52(3):231–247CrossRefGoogle Scholar
  31. Hon-Wing L (2001) Ecotoxicology of glutaraldehyde: review of environmental fate and effects studies. Ecotoxicol Environ Saf 49:26–39CrossRefGoogle Scholar
  32. Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR (1983) Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45:275–283PubMedPubMedCentralGoogle Scholar
  33. Huq A, West PA, Small EB, Huq MI, Colwell RR (1984) Influence of water temperature, salinity and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms. Appl Environ Microbiol 48:420–424PubMedPubMedCentralGoogle Scholar
  34. IMO (1997) Guidelines for the control and management of ship’s ballast water to minimize the transfer of harmful aquatic organisms and pathogens—Resolution A. 868(20)Google Scholar
  35. Jacobson AH, Willingham GL (2000) Sea-nine antifoulant: an environmentally acceptable alternative to organotin antifoulants. Sci Total Environ 258:103–110CrossRefGoogle Scholar
  36. Jianyi M, Rongquan Z, Ligen X, Shufeng W (2002) Differential sensitivity of two green algae, Scenedesmus obliquus and Chlorella pyrenoidosa, to12 pesticides. Ecotoxicol Environ Saf 52:57–61CrossRefGoogle Scholar
  37. Jui-Hung Y, Kuo-Hsiung L, Yei-Shung W (2002) Acute lethal toxicity of environmental pollutants to aquatic organisms. Ecotoxicol Environ Saf 52:113–116CrossRefGoogle Scholar
  38. Kalhmeter G (1999) The swedish reference group for antibiotics (SRGA) and its subcommittee on methodology (SRGA-M) [On-line, version 3, SRGA homepage] www.SRGA.org (2 april 2001 date last accessed)Google Scholar
  39. Kissa E, Moraitou-Apostolopoulou M, Kiortsis V (1984) Effects of four heavy metals on survival and hatching rate of Artemia salina (L.). Arch Hydrobiol 102(2):255–264Google Scholar
  40. Lavoie DM, Smith LD, Ruiz GM (1999) The potential for intracoastal transfer of non-indigenous species in the ballast water of ships. Estuar Coast Shelf Sci 48:551–564CrossRefGoogle Scholar
  41. Levy K (2004) Neglected consequences: role of introduced aquatic species in the spread of infectious diseases. Econ Health 1:296–305Google Scholar
  42. Macdonald EM, Davidson RD (1997) Ballast water project—final report. Fisheries research services report number 3/97, FRS Marine Laboratory Aberdeen, 83 ppGoogle Scholar
  43. McCarthy S, Khambaty FM (1994) International dissemination of epidemic Vibrio cholerae by cargo ship ballast water and other non potable waters. Environ Microbiol 60:2597–2601Google Scholar
  44. Menasria R, Pavillon JF (1994) Toxic effects of two trace metals, copper and silver, on a crustacean harpacticoid copepod Tigriopus brevicornis (Muller). J Rech Oceanogr 19(3–4):157–165Google Scholar
  45. Mills EL, Strayer DL, Scheurell MD, Carlton JT (1996) Exotic species in the Hudson river basin: a history of invasions and introductions. Estuaries 19:14–823CrossRefGoogle Scholar
  46. Min-Jin S, Mal-Nam K (2003) Antimicrobial action of p-hydroxyphenyl acrylate. Int Biodeterior Biodegradation 52:107–113CrossRefGoogle Scholar
  47. Montanari MP, Pruzzo C, Pane L, Colwell RR (1999) Vibrios associated with plankton in a coastal zone of the Adriatic Sea (Italy). FEMS Microbiol Ecol 29:241–247CrossRefGoogle Scholar
  48. NCCLS (National Committee for Clinical Laboratory Standards) (1997) Performance standards for antimicrobial disk susceptibility test, 6th edn. Approved Standard. M2-A6, Wayne, PAGoogle Scholar
  49. National Committee for Clinical Laboratory Standards (1998). Development of in vitro susceptibility testing criteria and quality control parameters: Approved standard M23-T3, vol 18, No. 5. NCCLS, Villanova, PAGoogle Scholar
  50. NCCLS (National Committee for Clinical Laboratory Standards) (2002) Performance standards for antimicrobial susceptibility testing, 8th informational supplement. M100 S12. National Committee for Clinical Laboratory Standards, Villanova, PAGoogle Scholar
  51. National Research Council (1996) Stemming the tide: controlling introductions of nonindigenous species by ships’ ballast water. National Academy Press, Washington, DC, pp11–21Google Scholar
  52. Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Poll Bull 46(5):542–551CrossRefGoogle Scholar
  53. OECD 301A: Ready Biodegradability DOC die-Away Test. Section 3: Degradation and Accumulation, July 1992Google Scholar
  54. Okamoto OK, Shao L, Hastings JW, Colepicolo P (1999) Acute and chronic effects of toxic metals on viability, encystment and bioluminescence in the dinoflagellate Gonyaulax polyedra. Comp Biochem Physiol C 123(1):75–83PubMedGoogle Scholar
  55. Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL (2000) Fate and ecotoxicity of the new antifouling compound Irgarol 1051 in the aquatic environment. Water Res 34:3523–3530CrossRefGoogle Scholar
  56. Pane L, Feletti M, Carli A (1996) Fattori ambientali e fluttuazioni della popolazione del copepode Tigriopus fulvus delle pozze di scogliera di Genova Nervi. S.It.E. Atti. 17:317–320Google Scholar
  57. Pati AC, Belmonte G (2003) Disinfection efficacy on cyst viability of Artemia franciscana (Crustacea), Hexarthra fennica (Rotifera) and Fabrea salina (Ciliophora). Mar Biol 142:895–904CrossRefGoogle Scholar
  58. Pavicic J, Skreblin M, Kregar I, Tusek-Znidaric M, Stegnar P (1994) Embryo-larval tolerance of Mytilus galloprovincialis, exposed to the elevated sea water metal concentrations I. Toxic effects of Cd, Zn and Hg. Comp Biochem Physiol C 107(2):249–257Google Scholar
  59. Pierce R, Carlton JT, Carlton D, Geller JB (1997) Ballast water as a vector for tintinnid transport. Mar Ecol Prog Ser 149:295–297CrossRefGoogle Scholar
  60. Pruzzo C, Crippa A, Bertone S, Pane L, Carli A (1996) Attachment of Vibrio alginolyticus to chitin mediated by chitin–binding proteins. Microbiology 142:2181–2186CrossRefGoogle Scholar
  61. Pruzzo C, Tarsi R, Lleò MM, Signoretto C, Zampini M, Pane L, Colwell RR, Canepari P (2003) Persistence of adhesive properties in Vibrio cholerae after long-term exposure to sea water. Environ Microbiol 5:850–858CrossRefGoogle Scholar
  62. Ricciardi A, MacIsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends Ecol Evol 15(2):62–65CrossRefGoogle Scholar
  63. Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379PubMedPubMedCentralGoogle Scholar
  64. Rubino F, Belmonte G, Miglietta A, Geraci S, Boero F (2000) Resting stages of plankton in recent North Adriatic sediments. PSZN Mar Ecol 21(3–4):263–286CrossRefGoogle Scholar
  65. Ruiz GM, Fofonoff PE, Carlton JJ, Wonham MJ, Hines AH (2000a) Invasions of coastal marine communities in North America: apparent patterns, process, and biases. Annu Rev Ecol Syst 31:481–531CrossRefGoogle Scholar
  66. Ruiz GM, Rawlings TK, Dobbs FG, Drake LA, Mullady T, Hug A, Colwell RR (2000b) Global spread of microorganisms by ships: ballast water discharged from vessels harbours a cocktail of potential pathogens. Nature 408:49–50CrossRefGoogle Scholar
  67. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632CrossRefGoogle Scholar
  68. Sano LL, Mapili MA, Krueger A, Garcia E, Gossiaux D, Phillips K, Landrum PF (2004) Comparative efficacy of potential chemical disinfectants for treating unballasted vessels. J Great Lakes Res 30(1):201–216CrossRefGoogle Scholar
  69. Signoretto C, Burlacchini G, Leò MdM, Pruzzo C, Zampini M, Pane L, Franzini G, Canepari P (2004) Adhesion of Enterococcus faecalis in the monoculturale state to plankton is the main mechanism responsible for persistence of this bacterium in both lake and seawater. Appl Environ Microbiol 70(11):6892–6896CrossRefGoogle Scholar
  70. Simpson G (2001) Ballast water disinfection with ClO2. Proceedings of the second international conference on marine bioinvasions. New Orleans, LA, 131ppGoogle Scholar
  71. Slabbert JL, Venter EA (1999) Biological assays for aquatic toxicity testing. Water Sci Tech 39(10–11):367–373CrossRefGoogle Scholar
  72. Snell TW, Persoone G (1989) Acute toxicity bioassays using rotifers: II. A freshwater test with Branchionuys rubens. Aquat Toxicol 14:81–92Google Scholar
  73. Swedish Reference Group for Antibiotics (1997) Antimicrobial susceptibility testing in Sweden. Scand J Infect Dis 105:5–31Google Scholar
  74. Talman S, Bite JS, Campbell SJ, Holloway M, McArthur M, Ross DJ, Storey M (1999) Impacts of some introduced marine species found in Port Phillip Bay. In: Hewitt CL, Campbell ML, Thresher RE, Martin RB (eds) Marine biological invasions of Port Phillip Bay, Victoria. Centre for research on introduced marine pests. CSIRO marine research, Hobart, Tasmania, pp 193–121Google Scholar
  75. Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup 01 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56:1977–1980PubMedPubMedCentralGoogle Scholar
  76. Tarsi R, Pane L, Carli A, Pruzzo C (2000) Vibrio attachment to chitin containing surfaces: a survival strategy in the aquatic environment. Recent Res Devel Microbiol 4:599–605Google Scholar
  77. Williamson M (1996) Biological invasions. Chapman and Hall, London, pp 244Google Scholar
  78. Williams RJ, Griyths FB, Van der Wal EJ, Kelly J (1988) Cargo vessel ballast water as a vector for the transport of nonindigenous marine species. Estuar Coast Shelf Sci 26:409–420CrossRefGoogle Scholar
  79. Wonham MJ, Carlton JT, Ruiz GM, Smith LD (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Mar Biol 136:1111–1121CrossRefGoogle Scholar
  80. Wright DA (2002) A natural product biocide for ballast water treatment. In: Proceedings of the 11th international conference on aquatic invasive species, Alexandria, VA (Abstract)Google Scholar
  81. Wright DA, Dawson R (2001) Seakleen®, a potential natural biocide for ballast water treatment (Abstract 1st). In: International ballast water treatment R & D symposium IMO, London, EnglandGoogle Scholar
  82. Zhang F, Dickman M (1999) Mid-ocean exchange of container vessel ballast water 1: Seasonal factors affecting the transport of harmful dinoflagellates and diatoms. Mar Ecol Prog Ser 176:243–251CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • M. Faimali
    • 1
  • F. Garaventa
    • 1
  • E. Chelossi
    • 1
  • V. Piazza
    • 1
  • O.D. Saracino
    • 2
  • F. Rubino
    • 2
  • G.L. Mariottini
    • 3
  • L. Pane
    • 3
  1. 1.Sezione Tecnologie Marine, CNRIstituto di Scienze MarineGenovaItaly
  2. 2.Sez. Talassografico A. Cerruti, CNRIstituto per l’Ambiente Marino CostieroTarantoItaly
  3. 3.Dipartimento di Biologia, Viale Benedetto XVUniversità di GenovaGenovaItaly

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