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Efficacy and Ecotoxicity of Novel Anti-Fouling Nanomaterials in Target and Non-Target Marine Species

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Abstract

Biofouling is a global problem that affects virtually all the immersed structures. Currently, several novel environmentally friendly approaches are being tested worldwide to decrease the toxicity of biocides in non-fouling species, such as the encapsulation/immobilization of commercially available biocides, in order to achieve control over the leaching rate. The present study addresses the toxicity of two widely used booster biocides, zinc pyrithione (ZnPT) and copper pyrithione (CuPT), in its free and incorporated forms in order to assess their toxicity and anti-fouling efficacy in target and non-target species. To achieve this goal, the following marine organisms were tested; the green microalgae Tetraselmis chuii (non-target species) and both target species, the diatom Phaeodactylum tricornutum and the mussel Mytilus edulis. Organisms were exposed to both biocides, two unloaded nanostructured materials and nanomaterials loaded with biocides, from 10 μg/L to 100 mg/L total weight, following standard protocols. The most eco-friendly and simultaneously efficient anti-fouling solution against the two photosynthetic species (nanoclays loaded with ZnPT) was then tested on mussels to assess its lethal efficacy (LC50 = 123 μg/L) and compared with free biocide (LC50 = 211 μg/L) and unloaded material (LC50 > 1000 μg/L). A second exposure test with sub-lethal concentrations (lower than 100 μg/L), using mussels, was carried out to assess biochemical changes caused by the tested compounds. Oxidative stress, detoxification and neurotransmission markers were not responsive; however, different antioxidant patterns were found with free ZnPT and loaded nanoclay exposures. Thus, the immobilization of the biocide ZnPT into nanoclays proved to be a promising efficient and eco-friendly anti-fouling strategy.

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References

  • Adams L, Lyon DY, Alvarez PJJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40:3527–3532

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Harino H, Ohji M, Langston WJ (2009) Ecotoxicology of antifouling biocides. Springer, Japan

    Book  Google Scholar 

  • ASTM (2002) Standard guide for conducting acute toxicity tests on test materials with fishes, macroinvertebrates, and amphibians. ASTM E729–96 (Reapproved 2002). American Society for Testing and Materials, West Conshohocken, 22 pp

  • Bellas J, Granmo A, Beiras R (2005) Embryotoxicity of the antifouling biocide zinc pyrithione to sea urchin (Paracentrotus lividus) and mussel (Mytilus edulis). Mar Pollut Bull 50:1382–1385

    Article  CAS  PubMed  Google Scholar 

  • Bi X, Zhang H, Dou L (2014) Layered double hydroxide-based nanocarriers for drug delivery. Pharmaceutics 6:298–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Methods Enzymol 105:299–305

    Article  CAS  PubMed  Google Scholar 

  • Borg DA, Trombetta LD (2010) Toxicity and bioaccumulation of the booster biocide copper pyrithione, copper 2-pyridinethiol-1-oxide, in gill tissues of Salvelinus fontinalis (brook trout). Toxicol Ind Health 26:139–150

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buffet P-E, Tankoua OF, Pan J-F, Berhanu D, Herrenknecht C, Poirier L, Amiard-Triquet C, Amiard J-C, Berard J-B, Risso C, Guibbolini M, Romeo M, Reip P, Valsami-Jones E, Mouneyrac C (2011) Behavioural and biochemical responses of two marine invertebrates Scrobicularia plana and Hediste diversicolor to copper oxide nanoparticles. Chemosphere 84:166–174

    Article  CAS  PubMed  Google Scholar 

  • Canesi L, Fabbri R, Gallo G, Vallotto D, Marcomini A, Pojana G (2010) Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). Aquat Toxicol 100:168–177

    Article  CAS  PubMed  Google Scholar 

  • Canesi L, Frenzilli G, Balbi T, Bernardeschi M, Ciacci C, Corsolini S, Torre CD, Fabbri R, Faleri C, Focardi S, Guidi P, Kocan A, Marcomini A, Mariottini M, Nigro M, Pozo-Gallardo K, Rocco L, Scarcelli V, Smerilli A, Corsi I (2014) Interactive effects of n-TiO2 and 2,3,7,8-TCDD on the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 153:53–65

    Article  CAS  PubMed  Google Scholar 

  • Ciriminna R, Bright FV, Pagliaro M (2015) Ecofriendly antifouling marine coatings. ACS Sustain Chem Eng 3:559–565

    Article  CAS  Google Scholar 

  • Clairborne A (1985) Catalase activity. In: Greenwald R (ed) Handbook methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284

  • Dinning AJ, Al-Adam ISI, Austin P, Charlton M, Collier PJ (1998) Pyrithione biocide interactions with bacterial phospholipid head groups. J Appl Microbiol 85:132–140

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  PubMed  Google Scholar 

  • Emolayeva E, Sanders D (1995) Mechanism of pyrithione-induced membrane depolarization in Neurospora crassa. Appl Environ Microbiol 61:3385–3390

    Google Scholar 

  • Frasco MF, Guilhermino L (2002) Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiol Biochem 26:149–156

    Article  CAS  Google Scholar 

  • Galvão T, Neves CS, Caetano APF, Maia F, Mata D, Malheiro E, Ferreira MJ, Bastos AC, Salak AN, Gomes JRB, Tedim J, Ferreira MGS (2016) Control of crystallite and particle size in the synthesis of layered double hydroxides: macromolecular insights and a complementary modelling tool. J Colloid Interface Sci 468:86–94

    Article  PubMed  Google Scholar 

  • Geiger T, Delavy P, Hany R, Schleuniger J, Zinn M (2004) Encapsulated zosteric acid embedded in poly[3-hydroxyalkanoate] coatings-protection against biofouling. Polym Bull 52(1):65–72

    Article  CAS  Google Scholar 

  • Gittens JE, Smith TJ, Suleiman R, Akid R (2013) Current and emerging environmentally-friendly systems for fouling control in the marine environment. Biotechnol Adv 31(8):1738–1753

    Article  CAS  PubMed  Google Scholar 

  • Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM (1996) Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32:727–738

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Harino H, Langston WJ (2009) Degradation of alternative biocides in the aquatic environment. In: Arai T et al. (eds) Ecotoxicology of antifouling biocides. Springer, Japan, pp 397–412

  • Hart RL, Virgallito DR, Work DE (2010) Microencapsulation of biocides and antifouling agents. European patent EP1791424B1, 19/05/2010

  • IMO (International Maritime Organisation) (2001) International convention on the control of harmful antifouling systems on ships. Anti-fouling systems convention, AFS/CONF/26. International Maritime Organization, London. http://www.imo.org

    Google Scholar 

  • ISO (2007) Water quality—determination of selected elements by inductively coupled plasma optical emission spectrometry (ICP-OES). ISO 11885:2007. International Organization for Standardization, Geneva, Switzerland

    Google Scholar 

  • Karlsson J, Eklund B (2004) New biocide-free anti-fouling paints are toxic. Mar Pollut Bull 49:456–464

    Article  CAS  PubMed  Google Scholar 

  • Knopp D, Tang D, Niessner R (2009) Review: bioanalytical applications of biomolecule-functionalized nanometer-sized doped silica particles. Anal Chim Acta 647:14–30

    Article  CAS  PubMed  Google Scholar 

  • Koutsaftis A, Aoyama I (2006) The interactive effects of binary mixtures of three antifouling biocides and three heavy metals against the marine algae Chaetoceros gracilis. Environ Toxicol 21:432–439

    Article  CAS  PubMed  Google Scholar 

  • Kura A, Hussein M, Fakurazi S, Arulselvan P (2014) Layered double hydroxide nanocomposite for drug delivery systems; bio-distribution, toxicity and drug activity enhancement. Chem Cent J 8:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Maia F, Tedim J, Lisenkov AL, Salak AN, Zheludkevich ML (2012) Silica nanocontainers for active corrosion protection. Nanoscale 4:1287–1298

    Article  CAS  PubMed  Google Scholar 

  • Maia F, Silva AP, Fernandes S, Cunha A, Almeida A, Tedim T, Zheludkevich ML, Ferreira MGS (2015) Incorporation of biocides in nanocapsules for protective coatings used in maritime applications. Chem Eng J 270:150–157

    Article  CAS  Google Scholar 

  • Maraldo K, Dahllöf I (2004) Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Mar Pollut Bull 48:894–901

    Article  CAS  PubMed  Google Scholar 

  • Marcheselli M, Conzo F, Mauri M, Simonini R (2010a) Novel antifouling agent-zinc pyrithione: short- and long-term effects on survival and reproduction of the marine polychaete Dinophilus gyrociliatus. Aquat Toxicol 98:204–210

    Article  CAS  PubMed  Google Scholar 

  • Marcheselli M, Rustichelli C, Mauri M (2010b) Novel antifouling agent zinc pyrithione: determination, acute toxicity, and bioaccumulation in marine mussels (Mytilus galloprovincialis). Environ Toxicol Chem 29(11):2583–2592

    Article  CAS  PubMed  Google Scholar 

  • Mochida K, Ito K, Harino H, Kakuno A, Fuji K (2006) Acute toxicity of pyrithione antifouling biocides and joint toxicity with copper to red sea bream (Pagrus major) and toy shrimp (Heptacarpus futilirostris). Environ Toxicol Chem 25(11):3058–3064

    Article  PubMed  Google Scholar 

  • Nunes B, Braga MR, Campos JC, Gomes R, Ramos AS, Antunes SC, Correia AT (2015) Ecotoxicological effect of zinc pyrithione in the freshwater fish Gambusia holbrooki. Ecotoxicology 24(9):1896–1905

    Article  CAS  PubMed  Google Scholar 

  • OECD (2006) Test no. 201: freshwater alga and cyanobacteria, growth inhibition test. OECD guidelines for the testing of chemicals. Organization for Economic Co-Operation and Development, Paris, Adopted in 23 March 2006, 25 pp

    Book  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  • Onduka T, Mochida K, Harino H, Ito K, Kakuno A, Fujii K (2010) Toxicity of metal pyrithione photodegradation products to marine organisms with indirect evidence for their presence in seawater. Arch Environ Contam Toxicol 58(4):991–997

    Article  CAS  PubMed  Google Scholar 

  • Poznyak SK, Tedim J, Rodrigues LM, Salak AN, Zheludkevich ML, Dick LFP, Ferreira MGS (2009) Novel inorganic host layered double hydroxides intercalated with guest organic inhibitors for anticorrosion applications. Appl Mater Interfaces 1:2353–2362

    Article  CAS  Google Scholar 

  • Price ARG, Readman JW (2013) Booster biocide antifoulants: is history repeating itself? In: Gee D et al. (eds) Emerging lessons from ecosystems. Late lessons from early warnings: science, precaution, innovation. European Environment Agency, Publications Office of the European Union, Luxembourg, pp 265–278

  • Rousseeuw PJ, Croux C (1993) Alternatives to the median absolute deviation. J Am Stat Assoc 88:1273–1283

    Article  Google Scholar 

  • Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98

    Article  CAS  PubMed  Google Scholar 

  • Shchukin DG, Grigoriev DO, Möhwald H (2013) Corrosion inhibiting pigments and methods for preparing the same. European patent EP2604661A1, 19/06/2013

  • Szabó T, Molnár-Nagy L, Bognár J, Nyikos L, Telegdi J (2011) Self-healing microcapsules and slow release microspheres in paints. Prog Org Coat 72:52–57

    Article  Google Scholar 

  • Takahashi K (2009) Release rate of biocides from antifouling paints. In: Arai T et al. (eds) Ecotoxicology of antifouling biocides. Springer, Japan, pp 3–22

  • Tedim J, Poznyak SK, Kuznetsova A, Raps D, Hack T, Zheludkevich ML, Ferreira MGS (2010) Enhancement of active corrosion protection via combination of inhibitor-loaded nanocontainers. ACS Appl Mater Interfaces 2(5):1528–1535

    Article  CAS  PubMed  Google Scholar 

  • Thomas KV (2001) The environmental fate and behaviour of antifouling paint booster biocides: a review. Biofouling 17:73–86

    Article  CAS  Google Scholar 

  • Trevisan R, Flesch S, Mattos JJ, Milani MR, Bainy ACD, Dafre AL (2014) Zinc causes acute impairment of glutathione metabolism followed by coordinated antioxidant defenses amplification in gills of brown mussels Perna perna. Comp Biochem Physiol C 159:22–30

    CAS  Google Scholar 

  • Turley PA, Fenn RJ, Ritter JC, Callow ME (2005) Pyrithiones as antifoulants: environmental fate and loss of toxicity. Biofouling 21:31–40

    Article  CAS  PubMed  Google Scholar 

  • USEPA (1996) Ecological effects test guidelines OPPTS 850.1055 bivalve acute toxicity test. EPA 712–C–96–160. U.S. Environmental Protection Agency, Washington, 7 pp

    Google Scholar 

  • Wages PA, Silbajoris R, Speen A, Brighton L, Henriquez A, Tong H, Bromberg PA, Simmons SO, Samet JM (2014) Role of H2O2 in the oxidative effects of zinc exposure in human airway epithelial cells. Redox Biol 3:47–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189

    Article  Google Scholar 

  • Ward JE, Kach DJ (2009) Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar Environ Res 68:137–142

    Article  CAS  PubMed  Google Scholar 

  • Wegner A, Besseling E, Foekema EM, Kamermans P, Koelmans AA (2012) Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environ Toxicol Chem 31:2490–2497

    Article  CAS  PubMed  Google Scholar 

  • Yamada H (2007) Behaviour, occurrence, and aquatic toxicity of new antifouling biocides and preliminary assessment of risk to aquatic ecosystems. Bull Fish Res Agen 21:31–45

  • Yebra DM, Kill S, Dam-Johansen K (2004) Antifouling technology: past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104

    Article  CAS  Google Scholar 

  • Zhang C, Cui F, Zeng G-M, Jiang M, Yang Z-Z, Yu Z-G, Zhu M-Y, Shen L-Q (2015) Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Sci Total Environ 518–519:352–362

    Article  PubMed  Google Scholar 

  • Zheludkevich ML, Poznyak SK, Rodrigues LM, Raps D, Hack T, Dick LF, Nunes T, Ferreira MGS (2010) Active protection coatings with layered double hydroxide nanocontainers of corrosion inhibitor. Corros Sci 52(2):602–611

    Article  CAS  Google Scholar 

  • Zheludkevich ML, Tedim J, Ferreira MGS (2012) “Smart” coatings for active corrosion protection based on multi-functional micro and nanocontainers. Electrochim Acta 82:314–323

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the BYEFOULING project, funded by European Union through the Seventh Framework Programme for research, technological development and demonstration (Grant agreement no. 612717). We acknowledge for the financial support to CESAM (UID/AMB/50017), CICECO - Aveiro Institute of Materials (POCI-01-0145-FEDER-007679; UID/CTM/50011/2013) and FCT/MEC through national funds and co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. Roberto Martins and João Tedim benefitted from a Post-Doctoral grant (SFRH/BPD/93225/2013) and a Researcher grant (IF/00347/2013), respectively, awarded by the Portuguese Science Foundation (FCT), funded by the Human Potential Operational Programme (POPH) through QREN and European Social Fund (ESF) and by national funds through the Portuguese Ministry of Education and Science. Susana Loureiro has a fellowship from the program “Science Without Borders” from CAPES (Project #106/2013).

We kindly acknowledge the R&D company Lonza, particularly Dr. Peter Vanaken and Dr. Juergen Riegler, by providing both active species (CuPT and ZnPT) to be incorporated in the nanostructured material. Smallmatek also acknowledge the Polytechnic Institute of Leiria (ESTM, Peniche) by kindly providing the algal strains.

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Avelelas, F., Martins, R., Oliveira, T. et al. Efficacy and Ecotoxicity of Novel Anti-Fouling Nanomaterials in Target and Non-Target Marine Species. Mar Biotechnol 19, 164–174 (2017). https://doi.org/10.1007/s10126-017-9740-1

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