Comparative efficiency of macroalgal extracts and booster biocides as antifouling agents to control growth of three diatom species

Marine Pollution Bulletin

Volumn 64, Issue 10, 2012, Pages 2039-2046

  Silkina, Alla ^a   Bazes, Alexandra ^a   Mouget, Jean Luc ^b   Bourgougnon, Nathalie ^a  

^a UNIVERSITÉ DE BRETAGNE SUD   (France)

^b UNIVERSITÉ DU MAINE   (France)

Author keywords

Antifouling; Booster biocides; Ceramium botryocarpum; Diatoms; EC50; Sargassum muticum

Indexed keywords

ALGAL GROWTH; ALTERNATIVE APPROACH; ANTIFOULANTS; ANTIFOULING; ANTIFOULING AGENTS; ANTIFOULING COMPOUNDS; CERAMIUM BOTRYOCARPUM; COMPARATIVE EFFICIENCIES; DIATOMS; ECO-FRIENDLY; ENVIRONMENTALLY FRIENDLY ALTERNATIVES; GROWTH EFFECTS; MARINE DIATOMS; MARINE ORGANISMS; RED ALGAE; SARGASSUM MUTICUM;

ALGAL EXTRACT; ANTIFOULING AGENT; BIOCIDE;

ALGA; ANTIFOULING AGENT; BIOFOULING; COMPARATIVE STUDY; DIATOM; ETHANOL; INHIBITION; MACROALGA; PESTICIDE; SEAWEED;

ALGAL GROWTH; ARTICLE; BIOMASS PRODUCTION; CERAMIUM BOTRYOCARPUM; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); DIATOM; ECOTOXICITY; ENVIRONMENTAL IMPACT ASSESSMENT; ENVIRONMENTAL MONITORING; FOULING CONTROL; GROWTH INHIBITION; NONHUMAN; SARGASSUM MUTICUM; SENSITIVITY ANALYSIS;

BIOFOULING; BIOLOGICAL AGENTS; CHLOROPHYLL; DIATOMS; DISINFECTANTS; PHAEOPHYTA; RHODOPHYTA; WATER POLLUTANTS, CHEMICAL;

ALGAE; BACILLARIOPHYTA; CERAMIUM BOTRYOCARPUM; NITZSCHIA ALBA; RHODOPHYTA; SARGASSUM MUTICUM;

EID: 84866764022     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2012.06.028     Document Type: Article

References (73)

1. Advisory Committee on Pesticides, 2000. In: Minutes of the 278th Meeting of the Advisory Committee on Pesticides (ACP), September 7, available online from http://www.pesticides.gov.uk/committees/ACP/ACP-278_mins.htm.
2. Araújo C.V.M., Blasco J., Moreno-Garrido I. Microphytobenthos in ecotoxicology: a review of the use of marine benthic diatoms in bioassays. Environ. Int. 2010, 36(6):637-664.
3. Arrhenius A., Gronvall F., Scholze M., Backhaus T., Blanck H. Predictability of the mixture toxicity of 12 similarly acting congeneric inhibitors of photosystem II in marine periphyton and epipsammon communities. Aquat. Toxicol. 2004, 66:351-367.
4. Bao V.W.W., Leung K.M.Y., Qiu J.-W., Lam M.H.W. Acute toxicities of five commonly used antifouling booster biocides to selected subtropical and cosmopolitan marine species. Mar. Pollut. Bull. 2011, 62:1147-1151.
5. Bayer CropScience, 2003. Bayer technical information. In: Confidor® (Ed.), Bayer, Germany.
6. Bazes A., Silkina A., Defer D., Bernède-Bauduin C., Quéméner E., Braud J.-P., Bourgougnon N. Active substances from Ceramium botryocarpum used as antifouling products in aquaculture. Aquaculture 2006, 258:664-674.
7. Bazes A., Silkina A., Douzenel P., Faÿ F., Kervarec N., Morin D., Berge J.-P., Bourgougnon N. Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J. Appl. Phycol. 2009, 10(1007):1573-1576.
8. Bellas J. Comparative toxicity of alternative antifouling biocides on embryos and larvae of marine invertebrates. Sci Total Environ. 2006, 367:573-585.
9. Bellas J. Toxicity of the booster biocide Sea-nine to the early developmental stages of the sea urchin Paracentrotus lividus. Aquat. Toxicol. 2007, 83:52-61.
10. Bellas J. Prediction and assessment of mixture toxicity of compounds in antifouling paints using the sea-urchin embryo-larval bioassay. Aquat. Toxicol. 2008, 88:308-315.
11. Bengtson Nash S.M., Quayle P.A., Schreiber U., Müller J.F. The selection of a model microalgal species as biomaterial for a novel aquatic phytotoxicity assay. Aquat. Toxicol. 2005, 72:315-326.
12. Boxall A.B.A., Comber S.D., Conrad A.U., Howcroft J., Zaman N. Inputs, monitoring and fate modelling of antifouling biocides in UK estuaries. Mar. Pollut. Bull. 2000, 40:898-905.
13. Buma A.G.J., Sjollema S.B., van de Poll W.H., Klamer H.J.C., Bakker J.F. Impact of the antifouling agent Irgarol 1051 on marine phytoplankton species. J. Sea Res. 2009, 61:133-139.
14. Chambers L.D., Stokes K.R., Walsh F.C., Wood R.J.K. Modern approaches to marine antifouling coatings. Surf. Coat. Technol. 2006, 201:3642-3652.
15. Chambers L.D., Hellio C., Stokes K.R., Dennington S.P., Goodes L.R., Wood R.J.K., Walsh F.C. Investigation of Chondrus crispus as a potential source of new antifouling agents. Int. Biodeterior. Biodegrad. 2011, 65:939-946.
16. Dafforn K.A., Lewis J.A., Johnston E.L. Antifouling strategies: history and regulation, ecological impacts and mitigation. Mar. Pollut. Bull. 2011, 62(3):453-465.
17. Daoud G.I., Veron B., Beach E., Kudyk J., Banaigs B., Patel A.V., Pope J., Hayes P.K., Hellio C. Biological activity and chemical fingerprint of microalgal extract for antifouling applications. Eur. J. Phycol. 2011, 46:60.
18. Dobretsov S., Xiong H., Xu Y., Levin L., Qian P.-Y. Novel antifoulants: inhibition of larval attachment by proteases. Mar. Biotechnol. 2007, 9:388-397.
19. Dubber D., Harder T. Extracts of Ceramium rubrum, Mastocarpus stellatus and Laminaria digitata inhibit growth of marine and fish pathogenic bacteria at ecologically realistic concentrations. Aquaculture 2008, 274:196-200.
20. Fai P.B., Grant A., Reid B.J. Compatibility of hydroxypropyl-b-cyclodextrin with algal toxicity bioassays. Environ. Pollut. 2009, 157:135-140.
21. Falciatore A., Bowler C. Revealing the molecular secrets of marine diatoms. Annu. Rev. Plant Biol. 2002, 53:109-130.
22. Faÿ F., Linossier I., Peron J.J., Langlois V., Vallee-Rehel K. Antifouling activity of marine paints: study of erosion. Prog. Org. Coat. 2007, 60:194-206.
23. Faÿ F., Linossier I., Carteau D., Dheilly A., Silkina A., Vallee-Rehel K. Booster biocides and microfouling. Biofouling 2010, 26:787-798.
24. Fernández-Alba A.R., Hernando M.D., Piedra L., Chisti Y. Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal. Chim. Acta 2002, 456:303-312.
25. Floerl O., Inglis G.J., Dey K., Smith A. The importance of transport hubs in stepping-stone invasions. J. Appl. Phycol. 2009, 46:37-45.
26. Fusetani N. Biofouling and antifouling. Nat. Prod. Rep. 2004, 21:94-104.
27. Fusetani N. Antifouling marine natural products. Nat. Prod. Rep. 2011, 28:400-410.
28. Ganti V., Kim K., Bhattarai H., Shin H. Isolation and s{cyrillic}haracterisation of some antifouling agents from the brown alga Sargassum confusum. J. Asian Nat. Prod. Res. 2006, 8:309-315.
29. Gatidou G., Thomaidis N.S. Evaluation of single and joint toxic effects of two antifouling biocides, their main metabolites and copper using phytoplankton bioassays. Aquat. Toxicol. 2007, 85:184-191.
30. Geoffroy L., Dewez D., Vernet G., Popovic R. Oxyfluorfen toxic effect on Scenedesmus obliquus evaluated by different photosynthetic and enzymatic biomarkers. Arch. Environ. Contam. Toxicol. 2003, 45:445-452.
31. Geoffroy L., Frankart C., Eullaffroy P. Comparison of different physiological parameter responses in Lemna minor and Scenedesmus obliquus exposed to herbicide flumioxazin. Environ. Pollut. 2004, 131:233-241.
32. Giacomazzi S., Cochet N. Environmental impact of diuron transformation: a review. Chemosphere 2004, 56:1021-1032.
33. Guillard R., Ryther J. Studies of marine planktonic diatoms, I: Cyclotella nana (Hustedt) and Detonula confervacea (Cleve). Can. J. Microbiol. 1972, 8:229-239.
34. Hellio C., Bremer G., Pons A.M., Le Gal Y., Bourgougnon N. Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Appl. Microbiol. Biotechnol. 2000, 54:543-549.
35. Hellio C., De La Broise D., Dufossé L., Le Gal Y., Bourgougnon N. Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar. Environ. Res. 2001, 52:231-247.
36. Hellio C., Maréchal J.-P., Da Gama B.A.P., Pereira R.C., Clare A.S. Natural marine products with antifouling activities. Advances in Marine Antifouling Coatings and Technologies 2009, 572-622. Woodhead Publishing Limited, Cambridge. C. Hellio, D. Yebra (Eds.).
37. ISO, 1995. Water quality - Marine algal growth inhibition test with Skeletonema costatum and Phaeodactylum tricornutum. International Organization for Standardization, Geneva I TC/174/SC5/ICS: 13.060.70.
38. Jones R.J. Testing the Photoinhibition model of coral bleaching using chemical inhibitors. Mar. Ecol. Prog. Ser. 2004, 284:133-145.
39. Natural Products from Seaweeds Plant-derived Natural Products 2009, Springer, New York, pp. 51-81. E. Ioannou, V. Roussis, A.E. Osbourn, V. Lanzotti (Eds.).
40. ICS and ISF, 2009. Overview of the international shipping industry. International Chamber of Shipping and International Shipping Federation, Web publication: (accessed 14.12.09). http://www.marisec.org/shippingfacts/keyfacts.
41. Koutsaftis A., Aoyama I. The interactive effects of binary mixtures of three antifouling biocides and three heavy metals against the marine algae Chaetoceros gracilis. Environ. Toxicol. 2006, 10.1002/tox.
42. Liao W.-R., Lin J.-Y., Shieh W.-Y., Jeng W.-L., Huang R. Antibiotic activity of lectins from marine algae against marine vibrios. J. Ind. Microbiol. Biotechnol. 2003, 30:433-439.
43. Ma J., Lin F., Wang S., Xu L. Acute toxicity assessment of 20 herbicides to the green alga Scenedesmus quadricauda (Turp) Breb. Bull. Environ. Contam. Toxicol. 2004, 72:1164-1171.
44. Ma J., Wang S., Wang P., Ma L., Chen X., Xu R. Toxicity assessment of 40 herbicides to the green alga Raphidocelis subcapitata. Ecotoxicol. Environ. Saf. 2006, 63:456-462.
45. Macedo R.S., Lombardi A.T., Omachi C.Y., Rörig L.R. Effects of the herbicide bentazon on growth and photosystem II maximum quantum yield of the marine diatom Skeletonema costatum. Toxicol. in Vitro 2008, 22:716-722.
46. Magnusson M., Heimann K., Negri A.P. Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar. Pollut. Bull. 2008, 56:1545-1552.
47. Maida M., Sammarco P.W., Coll J.C. A diffusion chamber for assessing efficiency of natural anti-fouling defenses in marine organisms. J. Exp. Mar. Biol. Ecol. 2006, 337:59-64.
48. Marechal J., Hellio C. Challenges for the development of new non-toxic antifouling solutions. Int. J. Mol. Sci. 2009, 10(11):4623-4637.
49. Molino P.J., Wetherbee R. The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 2008, 24:365-379.
50. Mukherjee A., Mohan Rao K.V., Ramesh U.S. Predicted concentrations of biocides from antifouling paints in Visakhapatnam Harbour. J. Environ. Manage. 2009, 90:51-59.
51. OECD, 1981. Guidelines for testing of chemicals In: 2, P.s. (Ed.), Organization of Economic Cooperation and Development, rue Andre-Pascal Paris Cedex 10 France.
52. OECD, 2006. Guidelines for testing of chemicals, Organization of Economic Cooperation and Development, Publication service 2, rue Andre-Pascal, 75775 Paris Cedex 10, France.
53. Okumura Y., Koyama J., Takaku H., Satoh H. Influence of organic solvents on the growth of marine microalgae. Arch. Environ. Contam. Toxicol. 2001, 41:123-128.
54. Omae I. General aspects of tin-free antifouling paints. Chem. Rev. 2003, 103:3431-3448.
55. Perschbacher P.W., Ludwig G.M. Effects of diuron and other aerially applied cotton herbicides and defoliants on the plankton communities of aquaculture ponds. Aquaculture 2004, 233:197-203.
56. Porsbring T., Blanck H., Tjellström H., Backhaus T. Toxicity of the pharmaceutical clotrimazole to marine microalgal communities. Aquat. Toxicol. 2009, 91:203-211.
57. Rao V.N.R. Adaptation of Algae to Heavy Metal Toxicity 1994, Rastogi Publications, Meerut, India.
58. Raveendran T.V., Limna Mol V.P., Parameswaran P.S. Natural product antifoulants - present scenario and future prospects. Proceedings of the International Conference on Biofouling and Ballast Water Management 2008, NIO, Goa, India, p. 37.
59. Reitsema, T., 2008. Antifouling Biocides in Perth Coastal Waters: A Snapshot at Select Areas of Vessel Activity. In: W.S.T.S.R.N. 1 (Ed.), Department of Water, Western Australia.
60. Renaud S.M., Thinh L.-V., Parry D.L. The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 1999, 170:147-159.
61. Rutherford A., Krieger-Liszkay A. Herbicide-induced oxidative stress in photosystem II. Trends Biochem. Sci. 2001, 26:648-653.
62. Sawant S.S., Sonak S., Garg A. Growth inhibition of fouling bacteria and diatoms by extract of terrestrial plant, Derris scandens (Dicotyledonae: Leguminocae). Indian J. Mar. Sci. 1995, 24:229-230.
63. Silkina A., Bazes A., Vouve F., Le Tilly V., Douzenel P., Mouget J.-L., Bourgougnon N. Antifouling activity of macroalgal extracts on Fragilaria pinnata (Bacillariophyceae): a comparison with Diuron. Aquat. Toxicol. 2009, 94:245-254.
64. Steinberg P.D., de Nys R. Chemical mediation of colonization of seaweed surfaces. J. Phycol. 2002, 38:621-629.
65. Stiger V., Deslandes E., Payri C.E. Phenolic contents of two brown algae, Turbinaria omata and Sargassum mangarevense on Tahiti (French Polynesia): interspecific, ontogenic and spatio-temporal variations. Bot. Mar. 2004, 47:402-409.
66. Thomas K.V., Brooks S. The environmental fate and effects of antifouling paint biocides. Biofouling 2010, 26:73-88.
67. Törneman N., Johansson M. Screening of Biocides and Organic Halogens SWECO Environment Screening Rapport 2008, Malmö 2009-01-28 2009, Sweden.
68. Underwood G.J.C., Paterson D.M. The importance of extracellular carbohydrate production by marine epipelic diatoms. Adv. Bot. Res. 2003, 40:184-240.
69. Urbani R., Magaletti E., Sist P., Cicero A.M. Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium, Thalassiosira pseudonana and Skeletonema costatum: effect of P-depletion and growth status. Sci. Total Environ. 2005, 353:300-306.
70. van Wezel A.P., van Vlaardingen P. Environmental risk limits for antifouling substances. Aquat. Toxicol. 2004, 66:427-444.
71. Voulvoulis N., Scrimshaw M.D., Lester J.N. Partitioning of selected antifouling biocides in the aquatic environment. Mar. Environ. Res. 2002, 53:1-16.
72. Yebra D.M., Kiil S., Dam-Johansen K. Antifouling technology-past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog. Org. Coat. 2004, 50:75-104.
73. Zhou X., Okamura H., Nagata S. Abiotic degradation of triphenylborane pyridine (TPBP) antifouling agent in water. Chemosphere 2007, 67:1904-1910.