Environmental sources, fate, toxicological effects, and health risks of copper pyrithione: an overview

Highlights

● Toxicological effects of copper pyrithione on aquatic organisms were reviewed.

● Copper pyrithione causes copper-induced oxidative stress and cell death.

● Copper pyrithione induces severe deformities in fish.

● Long-term effects and associated risks of copper pyrithione remain unknown.

Abstract

Copper pyrithione (CuPT) is an alternative to tributyltin that is widely used as an antifoulant and biocide in paint for ship hulls, fishing nets, and other marine environmental facilities. It gradually leaches from antifouling coatings into the aquatic environment, posing health risks to aquatic organisms. In recent years, there have been increasing concerns regarding the impacts of CuPT and its degradation products on organisms, as well as the associated health risks. Although the ecotoxicity of CuPT and its degradation products in various species has been studied, there are no comprehensive reviews in the literature that have collated and interpreted these data. This review provides a comprehensive summary of the ecotoxicological effects of CuPT and its degradation products on microorganisms, plants, invertebrates, fish, and mammals. CuPT and its degradation products can affect the light utilization of plants, thereby altering primary production in ecosystems. It can disrupt cell membranes, antioxidant capacity, and cellular pH gradients in animals, leading to developmental toxicity, deformities, morphological damages, endocrine disruption, reproductive toxicity, hepatotoxicity, and neurotoxicity. Mitochondria are believed to be the primary target of CuPT-induced toxicity in aquatic animals; however, further investigations are warranted to reveal the long-term (e.g., multigenerational and transgenerational) impacts and associated molecular mechanisms of CuPT and its degradation products—particularly at environmentally realistic levels. This will facilitate a more comprehensive understanding of the health effects (both in terms of toxicity and hormesis) and environmental risks of CuPT and its degradation products, facilitating more effective regulation and mitigation.

Graphical abstract

Keywords

Copper pyrithione / Ecotoxicity / Environmental fate / Ecological risk assessment / Review

References

[1] Almond K M, Trombetta L D. (2016). The effects of copper pyrithione, an antifouling agent, on developing zebrafish embryos. Ecotoxicology, 25(2): 389–398

[2] Almond K M, Trombetta L D. (2017). Copper pyrithione, a booster biocide, induces abnormal muscle and notochord architecture in zebrafish embryogenesis. Ecotoxicology, 26(7): 855–867

[3] Alsterberg C, Sundbäck K. (2013). Experimental warming and toxicant exposure can result in antagonistic effects in a shallow-water sediment system. Marine Ecology Progress Series, 488: 89–101

[4] Alsterberg C, Sundbäck K, Larson F. (2007). Direct and indirect effects of an antifouling biocide on benthic microalgae and meiofauna. Journal of Experimental Marine Biology and Ecology, 351(1−2): 56–72

[5] Amara I, Miled W, Slama R B, Ladhari N. (2018). Antifouling processes and toxicity effects of antifouling paints on marine environment: a review. Environmental Toxicology and Pharmacology, 57: 115–130

[6] Avelelas F, Martins R, Oliveira T, Maia F, Malheiro E, Soares A M V M, Loureiro S, Tedim J. (2017). Efficacy and ecotoxicity of novel anti-fouling nanomaterials in target and non-target marine species. Marine Biotechnology, 19(2): 164–174

[7] Bao V W, Koutsaftis A, Leung K M. (2008). Temperature-dependent toxicities of chlorothalonil and copper pyrithione to the marine copepod ‘Tigriopus japonicus’ and dinoflagellate ‘Pyrocystis lunula’. Australian Journal of Ecotoxicology, 14(2/3): 45–54

[8] Bao V W, Leung K M, Qiu J W, Lam M H. (2011). Acute toxicities of five commonly used antifouling booster biocides to selected subtropical and cosmopolitan marine species. Marine Pollution Bulletin, 62(5): 1147–1151

[9] Bao V W, Lui G C, Leung K M. (2014). Acute and chronic toxicities of zinc pyrithione alone and in combination with copper to the marine copepod Tigriopus japonicus. Aquatic Toxicology, 157: 81–93

[10] Bao V W, Yeung J W, Leung K M. (2012). Acute and sub-lethal toxicities of two common pyrithione antifouling biocides to the marine amphipod Elasmopus rapax. Toxicology and Environmental Health Sciences, 4(3): 194–202

[11] Bloecher N, Floerl O (2020). Efficacy testing of novel antifouling coatings for pen nets in aquaculture: how good are alternatives to traditional copper coatings? Aquaculture, 519: 734936

[12] Bloecher N, Floerl O. (2021). Towards cost-effective biofouling management in salmon aquaculture: a strategic outlook. Reviews in Aquaculture, 13(2): 783–795

[13] Borg D A, Trombetta L D. (2010). Toxicity and bioaccumulation of the booster biocide copper pyrithione, copper 2-pyridinethiol-1-oxide, in gill tissues of Salvelinus fontinalis (brook trout). Toxicology and Industrial Health, 26(3): 139–150

[14] Bourdon C, Cachot J, Gonzalez P, Couture P. (2024). Characterization of the bioaccumulation and toxicity of copper pyrithione, an antifouling compound, on juveniles of rainbow trout. Peer Community Journal, 4: e6

[15] Bourdon C, Couture P, Gourves P Y, Clérandeau C, Gonzalez P, Cachot J. (2023). Comparison of the accumulation and effects of copper pyrithione and copper sulphate on rainbow trout larvae. Environmental Toxicology and Pharmacology, 104: 104308

[16] Bressy C, Briand J F, Lafond S, Davy R, Mazeas F, Tanguy B, Martin C, Horatius L, Anton C, Quiniou F, Compère C (2022). What governs marine fouling assemblages on chemically-active antifouling coatings? Progress in Organic Coatings, 164: 106701

[17] Chen T, Li S, Liang Z, Li L, Guo H. (2022). Effects of copper pyrithione (CuPT) on apoptosis, ROS production, and gene expression in hemocytes of white shrimp Litopenaeus vannamei. Comparative Biochemistry and Physiology. Toxicology & Pharmacology, 256: 109323

[18] Chiem K, Fuentes B A, Lin D L, Tran T, Jackson A, Ramirez M S, Tolmasky M E. (2015). Inhibition of aminoglycoside 6’-N-acetyltransferase type Ib-mediated amikacin resistance in Klebsiella pneumoniae by zinc and copper pyrithione. Antimicrobial Agents and Chemotherapy, 59(9): 5851–5853

[19] Daehne D, Fürle C, Thomsen A, Watermann B, Feibicke M. (2017). Antifouling biocides in German marinas: exposure assessment and calculation of national consumption and emission. Integrated Environmental Assessment and Management, 13(5): 892–905

[20] de Campos B G, Figueiredo J, Perina F, Abessa D M D S, Loureiro S, Martins R (2022). Occurrence, effects and environmental risk of antifouling biocides (EU PT21): Are marine ecosystems threatened? Critical Reviews in Environmental Science and Technology, 52(18): 3179–3210

[21] Dinning A J, AL-Adham I S I, Austin P, Charlton M, Collier P J. (1998). Pyrithione biocide interactions with bacterial phospholipid head groups. Journal of Applied Microbiology, 85(1): 132–140

[22] Doose C A, Ranke J, Stock F, Bottin-Weber U, Jastorff B. (2004). Structure–activity relationships of pyrithiones–IPC-81 toxicity tests with the antifouling biocide zinc pyrithione and structural analogs. Green Chemistry, 6(5): 259–266

[23] Dupraz V, Stachowski-Haberkorn S, Ménard D, Limon G, Akcha F, Budzinski H, Cedergreen N. (2018). Combined effects of antifouling biocides on the growth of three marine microalgal species. Chemosphere, 209: 801–814

[24] ECHA(2019). Copper Pyrithione (PT 21) Sweden. Helsinki: European Chemicals Agency

[25] Eguchi S, Harino H, Yamamoto Y. (2010). Assessment of antifouling biocides contaminations in Maizuru Bay, Japan. Archives of Environmental Contamination and Toxicology, 58(3): 684–693

[26] 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): 47–56

[27] Faßbender S, Döring A K, Meermann B. (2019). Development of complementary CE-MS methods for speciation analysis of pyrithione-based antifouling agents. Analytical and Bioanalytical Chemistry, 411(27): 7261–7272

[28] Fenn R J, Alexander M T. (1988). Determination of zinc pyrithione in hair care products by normal phase liquid chromatography. Journal of Liquid Chromatography, 11(16): 3403–3413

[29] Grunnet K S, Dahllof I. (2005). Environmental fate of the antifouling compound zinc pyrithione in seawater. Environmental Toxicology and Chemistry, 24(12): 3001–3006

[30] Guardiola F A, Cuesta A, Meseguer J, Esteban M A. (2012). Risks of using antifouling biocides in aquaculture. International Journal of Molecular Sciences, 13(2): 1541–1560

[31] Günal A Ç, Arslan P, İpiçürük N, Tural R, Dinçel A S. (2022). Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio). Energy, Ecology and Environment, 7(5): 523–531

[32] Gutner-Hoch E, Martins R, Maia F, Oliveira T, Shpigel M, Weis M, Tedim J, Benayahu Y. (2019). Toxicity of engineered micro-and nanomaterials with antifouling properties to the brine shrimp Artemia salina and embryonic stages of the sea urchin Paracentrotus lividus. Environmental Pollution, 251: 530–537

[33] Gutner-Hoch E, Martins R, Oliveira T, Maia F, Soares A, Loureiro S, Piller C, Preiss I, Weis M, Larroze S. . (2018). Antimacrofouling efficacy of innovative inorganic nanomaterials loaded with booster biocides. Journal of Marine Science and Engineering, 6(1): 6

[34] Harino H. (2004). Occurrence and degradation of representative TBT free-antifouling biocides in aquatic environment. Coastal Marine Science, 29(1): 28–39

[35] Harino H, Eguchi S, Ohji M. (2012). Occurrence of antifouling biocides in Japan and Southeast Asia: the survey for 10 years. Coastal Marine Science, 35: 246–254

[36] Harino H, Kitano M, Mori Y, Mochida K, Kakuno A, Arima S. (2005). Degradation of antifouling booster biocides in water. Journal of the Marine Biological Association of the United Kingdom, 85(1): 33–38

[37] Harino H, Yamamoto Y, Eguchi S, Kawai S C, Kurokawa Y, Arai T, Ohji M, Okamura H, Miyazaki N. (2007). Concentrations of antifouling biocides in sediment and mussel samples collected from Otsuchi Bay, Japan. Archives of Environmental Contamination and Toxicology, 52(2): 179–188

[38] Holmes L, Turner A. (2009). Leaching of hydrophobic Cu and Zn from discarded marine antifouling paint residues: evidence for transchelation of metal pyrithiones. Environmental Pollution, 157(12): 3440–3444

[39] Horiguchi F, Eriguchi T, Ichikaw T, Nakata K. (2009). Ecological risk assessment of copper pyrithione (CuPT) in Tokyo Bay. Journal of Advanced Marine Science and Technology Society, 15(1): 1–13

[40] Jung S M, Bae J S, Kang S G, Son J S, Jeon J H, Lee H J, Jeon J Y, Sidharthan M, Ryu S H, Shin H W. (2017). Acute toxicity of organic antifouling biocides to phytoplankton Nitzschia pungens and zooplankton Artemia larvae. Marine Pollution Bulletin, 124(2): 811–818

[41] Kim N S, Hong S H, An J G, Shin K H, Shim W J. (2015). Distribution of butyltins and alternative antifouling biocides in sediments from shipping and shipbuilding areas in South Korea. Marine Pollution Bulletin, 95(1): 484–490

[42] Kim N S, Shim W J, Yim U H, Hong S H, Ha S Y, Han G M, Shin K H. (2014). Assessment of TBT and organic booster biocide contamination in seawater from coastal areas of South Korea. Marine Pollution Bulletin, 78(1−2): 201–208

[43] Kobayashi N, Okamura H. (2002). Effects of new antifouling compounds on the development of sea urchin. Marine Pollution Bulletin, 44(8): 748–751

[44] Koutsaftis A, Aoyama I. (2007). Toxicity of four antifouling biocides and their mixtures on the brine shrimp Artemia salina. Science of the Total Environment, 387(1−3): 166–174

[45] Koutsaftis A, Aoyama I. (2008). Toxicity of Diuron and copper pyrithione on the brine shrimp, Artemia franciscana: the effects of temperature and salinity. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 43(14): 1581–1585

[46] Kristensen J B, Meyer R L, Laursen B S, Shipovskov S, Besenbacher F, Poulsen C H. (2008). Antifouling enzymes and the biochemistry of marine settlement. Biotechnology Advances, 26(5): 471–481

[47] Kumari N, Jassal M, Agrawal A K. (2023). Effect of metal ion on UV protective and antimicrobial properties of in-situ synthesized pyrithione complexes on cellulosic textiles. Materials Today. Communications, 34: 105174

[48] Larson F, Petersen D G, Dahllöf I, Sundbäck K. (2007). Combined effects of an antifouling biocide and nutrient status on a shallow-water microbenthic community. Aquatic Microbial Ecology, 48(3): 277–294

[49] Lavtizar V, Kimura D, Asaoka S, Okamura H. (2018). The influence of seawater properties on toxicity of copper pyrithione and its degradation product to brine shrimp Artemia salina. Ecotoxicology and Environmental Safety, 147: 132–138

[50] Lee S, Haque M N, Lee D H, Rhee J S. (2023). Comparison of the effects of sublethal concentrations of biofoulants, copper pyrithione and zinc pyrithione on a marine mysid: a multigenerational study. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 271: 109694

[51] Li A J, Leung P T, Bao V W, Yi A X, Leung K M. (2014). Temperature-dependent toxicities of four common chemical pollutants to the marine medaka fish, copepod and rotifer. Ecotoxicology, 23(8): 1564–1573

[52] Li X, Ru S, Tian H, Zhang S, Lin Z, Gao M, Wang J. (2021). Combined exposure to environmentally relevant copper and 2,2'-dithiobis-pyridine induces significant reproductive toxicity in male guppy (Poecilia reticulata). Science of the Total Environment, 797: 149131

[53] Li X, Wang J, Ba W, Zhang S, Lin Z, Gao M, Tian H, Ru S. (2022). Mechanistic revealing of reproductive behavior impairment in male guppy (Poecilia reticulata) induced by environmentally realistic 2,2'-dithiobis-pyridine exposure. Chemosphere, 286: 131839

[54] LiangSZhong Q (2023). Reducing environmental impacts through socioeconomic transitions: critical review and prospects. Frontiers of Environmental Science & Engineering, 17(2), 24

[55] Liu N, Liu C, Li X, Liao S, Song W, Yang C, Zhao C, Huang H, Guan L, Zhang P. . (2014). A novel proteasome inhibitor suppresses tumor growth via targeting both 19S proteasome deubiquitinases and 20S proteolytic peptidases. Scientific Reports, 4(1): 5240

[56] Maraldo K, Dahllöf I. (2004a). Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Marine Pollution Bulletin, 48(9–10): 894–901

[57] Maraldo K, Dahllöf I. (2004b). Seasonal variations in the effect of zinc pyrithione and copper pyrithione on pelagic phytoplankton communities. Aquatic Toxicology, 69(2): 189–198

[58] Marcheselli M, Rustichelli C, Mauri M. (2010). Novel antifouling agent zinc pyrithione: determination, acute toxicity, and bioaccumulation in marine mussels (Mytilus galloprovincialis). Environmental Toxicology and Chemistry, 29(11): 2583–2592

[59] Martins S E, Fillmann G, Lillicrap A, Thomas K V. (2018). Ecotoxicity of organic and organo-metallic antifouling co-biocides and implications for environmental hazard and risk assessments in aquatic ecosystems. Biofouling, 34(1): 34–52

[60] McNally K, Warren N, Fransman W, Entink R K, Schinkel J, Van Tongeren M, Tielemans E. (2014). Advanced REACH Tool: a Bayesian model for occupational exposure assessment. Annals of Occupational Hygiene, 58(5): 551–565

[61] Mishra A, Djoko K Y, Lee Y H, Lord R M, Kaul G, Akhir A, Saxena D, Chopra S, Walton J W. (2023). Water-soluble copper pyrithione complexes with cytotoxic and antibacterial activity. Organic and Biomolecular Chemistry, 21(12): 2539–2544

[62] MochidaKAmano HItoKItoMOndukaT IchihashiHKakuno AHarinoHFujiiK (2012). Species sensitivity distribution approach to primary risk analysis of the metal pyrithione photodegradation product, 2,2'-dipyridyldisulfide in the Inland Sea and induction of notochord undulation in fish embryos. Aquatic Toxicology, 118–119: 152–163

[63] Mochida K, Amano H, Onduka T, Kakuno A, Fujii K. (2011). Toxicity and metabolism of copper pyrithione and its degradation product, 2,2'-dipyridyldisulfide in a marine polychaete. Chemosphere, 82(3): 390–397

[64] Mochida K, Ito K, Harino H, Kakuno A, Fujii K. (2006). Acute toxicity of pyrithione antifouling biocides and joint toxicity with copper to red sea bream (Pagrus major) and toy shrimp (Heptacarpus futilirostris). Environmental Toxicology and Chemistry, 25(11): 3058–3064

[65] Mochida K, Ito K, Harino H, Onduka T, Kakuno A, Fujii K. (2008). Early life-stage toxicity test for copper pyrithione and induction of skeletal anomaly in a teleost, the mummichog (Fundulus heteroclitus). Environmental Toxicology and Chemistry, 27(2): 367–374

[66] Mochida K, Ito K, Harino H, Tanaka H, Onduka T, Kakuno A, Fujii K. (2009). Inhibition of acetylcholinesterase by metabolites of copper pyrithione (CuPT) and its possible involvement in vertebral deformity of a CuPT-exposed marine teleostean fish. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 149(4): 624–630

[67] Mohamat-Yusuff F, Sarah-Nabila A G, Zulkifli S Z, Azmai M N A, Ibrahim W N W, Yusof S, Ismail A. (2018). Acute toxicity test of copper pyrithione on Javanese medaka and the behavioural stress symptoms. Marine Pollution Bulletin, 127: 150–153

[68] O’Brien H, Davoodian T, Johnson M D. (2023). The promise of copper ionophores as antimicrobials. Current Opinion in Microbiology, 75: 102355

[69] Oh H N, Kim W K. (2023). Copper pyrithione and zinc pyrithione induce cytotoxicity and neurotoxicity in neuronal/astrocytic co-cultured cells via oxidative stress. Scientific Reports, 13(1): 23060

[70] Ohji M, Harino H. (2017). Comparison of toxicities of metal pyrithiones including their degradation compounds and organotin antifouling biocides to the Japanese killifish Oryzias latipes. Archives of Environmental Contamination and Toxicology, 73(2): 285–293

[71] Ohji M, Harino H, Langston W J. (2019). Differences in susceptibility of marine bacterial communities to metal pyrithiones, their degradation compounds and organotin antifouling biocides. Journal of the Marine Biological Association of the United Kingdom, 99(5): 1033–1039

[72] Okamura H, Kobayashi N, Miyanaga M, Nogami Y. (2006). Toxicity reduction of metal pyrithiones by near ultraviolet irradiation. Environmental Toxicology, 21(4): 305–309

[73] Okamura H, Nishida T, Ono Y, Shim W J. (2003). Phytotoxic effects of antifouling compounds on nontarget plant species. Bulletin of Environmental Contamination and Toxicology, 71(5): 881–886

[74] Okamura H, Togosmaa L, Sawamoto T, Fukushi K, Nishida T, Beppu T. (2012a). Effects of metal pyrithione antifoulants on freshwater macrophyte Lemna gibba G3 determined by image analysis. Ecotoxicology, 21(4): 1102–1111

[75] Okamura H, Watanabe T, Aoyama I, Hasobe M. (2002). Toxicity evaluation of new antifouling compounds using suspension-cultured fish cells. Chemosphere, 46(7): 945–951

[76] Okamura H, Yagi M, Kawachi M, Hanyuda T, Kawai H, Walker I. (2012b). Application of rotating cylinder method for ecotoxicological evaluation of antifouling paints. Toxicological and Environmental Chemistry, 94(3): 545–556

[77] 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. Archives of Environmental Contamination and Toxicology, 58(4): 991–997

[78] Paçal E, Gümüş B A, Günal A Ç, Erkmen B, Arslan P, Yıldırım Z, Erkoç F. (2022). Oxidative stress response as biomarker of exposure of a freshwater invertebrate model organism (Unio mancus Lamarck, 1819) to antifouling copper pyrithione. Pesticides and Phytomedicine, 37(2): 63–76

[79] Paz-Villarraga C A, Castro Í B, Fillmann G. (2022). Biocides in antifouling paint formulations currently registered for use. Environmental Science and Pollution Research, 29(20): 30090–30101

[80] Petersen D G, Dahllof I, Nielsen L P. (2004). Effects of zinc pyrithione and copper pyrithione on microbial community function and structure in sediments. Environmental Toxicology and Chemistry, 23(4): 921–928

[81] Piazza V, Dragić I, Sepčić K, Faimali M, Garaventa F, Turk T, Berne S. (2014). Antifouling activity of synthetic alkylpyridinium polymers using the barnacle model. Marine Drugs, 12(4): 1959–1976

[82] Romano J A, Rittschof D, McClellan-Green P D, Holm E R. (2010). Variation in toxicity of copper pyrithione among populations and families of the barnacle, Balanus amphitrite. Biofouling, 26(3): 341–347

[83] Sanjuan E, Barriga-Cuartero J, Andreu-Sánchez O, González A, Fouz B. (2023). Study of sustainable HDPE-based materials for aquaculture applications: effects on fouling. Frontiers in Marine Science, 10: 1268695

[84] Shin D, Choi Y, Soon Z Y, Kim M, Kim D J, Jung J H. (2022). Comparative toxicity study of waterborne two booster biocides (CuPT and ZnPT) on embryonic flounder (Paralichthys olivaceus). Ecotoxicology and Environmental Safety, 233: 113337

[85] Sonak S, Pangam P, Giriyan A, Hawaldar K. (2009). Implications of the ban on organotins for protection of global coastal and marine ecology. Journal of Environmental Management, 90: S96–S108

[86] Sundbäck K, Groth Petersen D, Dahllöf I, Larson F. (Ref. "Sundbäck. (2007). Combined nutrient–toxicant effects on a shallow-water marine sediment system: sensitivity and resilience of ecosystem functions. Marine Ecology Progress Series, 330: 13–30

[87] TakahashiK (2009). Release rate of biocides from antifouling paints. In: Arai T, Harino H, Ohji M, Langston W J, eds. Ecotoxicology of Antifouling Biocides. Tokyo: Springer

[88] Tan G, Yang J, Li T, Zhao J, Sun S, Li X, Lin C, Li J, Zhou H, Lyu J. . (2017). Anaerobic copper toxicity and iron-sulfur cluster biogenesis in Escherichia coli. Applied and Environmental Microbiology, 83(16): e00867–17

[89] Taşcı E, Hayretdağ S. (2022). Investigation of spermiotoxic, embryotoxic and cytotoxic effects of copper pyrithione on Paracentrotus lividus (Lamarck, 1816). Pesticides and Phytomedicine, 37(1): 29–39

[90] Thomas K V, Brooks S. (2010). The environmental fate and effects of antifouling paint biocides. Biofouling, 26(1): 73–88

[91] Třešňáková N, Çağlan Günal A, Başaran Kankılıç G, Paçal E, Nihan Tavşanoğlu Ü, Uyar R, Erkoç F. (2020). Sub-lethal toxicities of zinc pyrithione, copper pyrithione alone and in combination to the indicator mussel species Unio crassus Philipsson, 1788 (Bivalvia, Unionidae). Chemistry and Ecology, 36(4): 292–308

[92] Turley P A, Fenn R J, Ritter J C. (2000). Pyrithiones as antifoulants: environmental chemistry and preliminary risk assessment. Biofouling, 15(1−3): 175–182

[93] Turley P A, Fenn R J, Ritter J C, Callow M E. (2005). Pyrithiones as antifoulants: environmental fate and loss of toxicity. Biofouling, 21(1): 31–40

[94] Wang H, Li Y, Huang H, Xu X, Wang Y. (2011). Toxicity evaluation of single and mixed antifouling biocides using the Strongylocentrotus intermedius sea urchin embryo test. Environmental Toxicology and Chemistry, 30(3): 692–703

[95] Whelan A, Regan F. (2006). Antifouling strategies for marine and riverine sensors. Journal of Environmental Monitoring, 8(9): 880–886

[96] Yamada H. (2007). Behaviour, occurrence, and aquatic toxicity of new antifouling biocides and preliminary assessment of risk to aquatic ecosystems. Bulletin of Fisheries Research Agency, 21: 31–45

[97] Yebra D M, Kiil S, Dam-Johansen K. (2004). Antifouling technology–past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progress in Organic Coatings, 50(2): 75–104

[98] Zhang S, Yin Q, Wang S, Yu X, Feng M (2023). Integrated risk assessment framework for transformation products of emerging contaminants: what we know and what we should know. Frontiers of Environmental Science & Engineering, 17(7): 91

Acknowledgements

This work was supported by Shantou University STU Scientific Research Initiation Grant (NTF23010), the Program for University Innovation Team of Guangdong Province (2022KCXTD008), and the Science and Technology Planning Project of Guangdong Province (2021B1212050025).

Conflict of Interests

The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

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