1. Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Prevention, Shantou University, Shantou 515063, China 2. State Key Laboratory of Marine Pollution, City University of Hong Kong, Hong Kong, China 3. Department of Forensic Medicine, Shantou University Medical College, Shantou 515041, China 4. Shaanxi Key Laboratory of Earth Surface System and Environmental Carrying Capacity, College of Urban and Environmental Sciences, Northwest University, Xi’an 710127, China
● 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.
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.
Okamura etal. (2006); Kobayashi and Okamura (2002)
Lytechinus variegatus
Embryos
3.5
–
0.53
Okamura etal. (2006)
Strongylocentrotus intermedius
Embryos
50
10.4
–
Wang etal. (2011)
Mussel
Mytilus galloprovincialis
–
96
2612.162
–
Marcheselli etal. (2010)
Diplostraca
Daphnia magna
–
48
22
–
Yamada (2007)
Tab.2
Taxa
Species
Stages
Duration (h)
EC50 or LC50 (μg/L)
NOEC (μg/L)
References
Pereiformes
Pagrus major
Juveniles
96
22
–
Mochida etal. (2006)
Pagrus major
Juveniles
96
7.67
–
Yamada (2007)
Rainbow trout
Oncorhynchus mykiss
Juveniles
168
7.6
––––
Okamura etal. (2002)
336
3.0
504
1.7
672
1.3
Chinook salmon
Oncorhynchus tshawytscha
Embryos
24
100
–
Okamura etal. (2002)
Beloniformes
Oryzias javanicus
Adults
96
16580
–
Mohamat-Yusuff etal. (2018)
Oryzias melastigma
Larvae
96
3.0 (13 °C)
––––––
Li etal. (2014)
3.1 (15 °C)
5.1 (20 °C)
5.7 (25 °C)
1.3 (28 °C)
0.3 (32 °C)
Oryzias melastigma
Larvae
96
8.2
–
Bao etal. (2011)
Diplostraca
Daphnia magna
–
48
22
–
Yamada (2007)
Mummichog
Fundulus heteroclitus
Larvae
96
2.9–8.4
0.24
Mochida etal. (2008)
Fundulus heteroclitus
Juveniles
96
5.0–17.8
–
Mochida etal. (2008)
Cypriniformes
Pimephakes promelas
–
96
8.2
–
Yamada (2007)
Tab.3
Fig.4
1
K M Almond, L D Trombetta. (2016). The effects of copper pyrithione, an antifouling agent, on developing zebrafish embryos. Ecotoxicology, 25(2): 389–398 https://doi.org/10.1007/s10646-015-1597-3
2
K M Almond, L D Trombetta. (2017). Copper pyrithione, a booster biocide, induces abnormal muscle and notochord architecture in zebrafish embryogenesis. Ecotoxicology, 26(7): 855–867 https://doi.org/10.1007/s10646-017-1816-1
3
C Alsterberg, K Sundbäck. (2013). Experimental warming and toxicant exposure can result in antagonistic effects in a shallow-water sediment system. Marine Ecology Progress Series, 488: 89–101 https://doi.org/10.3354/meps10357
4
C Alsterberg, K Sundbäck, F Larson. (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 https://doi.org/10.1016/j.jembe.2007.06.006
5
I Amara, W Miled, R B Slama, N Ladhari. (2018). Antifouling processes and toxicity effects of antifouling paints on marine environment: a review. Environmental Toxicology and Pharmacology, 57: 115–130 https://doi.org/10.1016/j.etap.2017.12.001
6
F Avelelas, R Martins, T Oliveira, F Maia, E Malheiro, A M V M Soares, S Loureiro, J Tedim. (2017). Efficacy and ecotoxicity of novel anti-fouling nanomaterials in target and non-target marine species. Marine Biotechnology, 19(2): 164–174 https://doi.org/10.1007/s10126-017-9740-1
7
V W Bao, A Koutsaftis, K M Leung. (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
V W Bao, K M Leung, J W Qiu, M H Lam. (2011). Acute toxicities of five commonly used antifouling booster biocides to selected subtropical and cosmopolitan marine species. Marine Pollution Bulletin, 62(5): 1147–1151 https://doi.org/10.1016/j.marpolbul.2011.02.041
9
V W Bao, G C Lui, K M Leung. (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 https://doi.org/10.1016/j.aquatox.2014.09.013
10
V W Bao, J W Yeung, K M Leung. (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 https://doi.org/10.1007/s13530-012-0135-4
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
N Bloecher, O Floerl. (2021). Towards cost-effective biofouling management in salmon aquaculture: a strategic outlook. Reviews in Aquaculture, 13(2): 783–795 https://doi.org/10.1111/raq.12498
13
D A Borg, L D Trombetta. (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 https://doi.org/10.1177/0748233710362381
14
C Bourdon, J Cachot, P Gonzalez, P Couture. (2024). Characterization of the bioaccumulation and toxicity of copper pyrithione, an antifouling compound, on juveniles of rainbow trout. Peer Community Journal, 4: e6 https://doi.org/10.24072/pcjournal.358
15
C Bourdon, P Couture, P Y Gourves, C Clérandeau, P Gonzalez, J Cachot. (2023). Comparison of the accumulation and effects of copper pyrithione and copper sulphate on rainbow trout larvae. Environmental Toxicology and Pharmacology, 104: 104308 https://doi.org/10.1016/j.etap.2023.104308
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
T Chen, S Li, Z Liang, L Li, H Guo. (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 https://doi.org/10.1016/j.cbpc.2022.109323
18
K Chiem, B A Fuentes, D L Lin, T Tran, A Jackson, M S Ramirez, M E Tolmasky. (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 https://doi.org/10.1128/AAC.01106-15
19
D Daehne, C Fürle, A Thomsen, B Watermann, M Feibicke. (2017). Antifouling biocides in German marinas: exposure assessment and calculation of national consumption and emission. Integrated Environmental Assessment and Management, 13(5): 892–905 https://doi.org/10.1002/ieam.1896
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
A J Dinning, I S I AL-Adham, P Austin, M Charlton, P J Collier. (1998). Pyrithione biocide interactions with bacterial phospholipid head groups. Journal of Applied Microbiology, 85(1): 132–140 https://doi.org/10.1046/j.1365-2672.1998.00477.x
22
C A Doose, J Ranke, F Stock, U Bottin-Weber, B Jastorff. (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 https://doi.org/10.1039/B314753C
23
V Dupraz, S Stachowski-Haberkorn, D Ménard, G Limon, F Akcha, H Budzinski, N Cedergreen. (2018). Combined effects of antifouling biocides on the growth of three marine microalgal species. Chemosphere, 209: 801–814 https://doi.org/10.1016/j.chemosphere.2018.06.139
S Eguchi, H Harino, Y Yamamoto. (2010). Assessment of antifouling biocides contaminations in Maizuru Bay, Japan. Archives of Environmental Contamination and Toxicology, 58(3): 684–693 https://doi.org/10.1007/s00244-009-9394-8
26
M Faimali, K Sepčić, T Turk, S Geraci. (2003). Non-toxic antifouling activity of polymeric 3-alkylpyridinium salts from the Mediterranean sponge Reniera sarai (Pulitzer-Finali). Biofouling, 19(1): 47–56 https://doi.org/10.1080/0892701021000036966
27
S Faßbender, A K Döring, B Meermann. (2019). Development of complementary CE-MS methods for speciation analysis of pyrithione-based antifouling agents. Analytical and Bioanalytical Chemistry, 411(27): 7261–7272 https://doi.org/10.1007/s00216-019-02094-5
28
R J Fenn, M T Alexander. (1988). Determination of zinc pyrithione in hair care products by normal phase liquid chromatography. Journal of Liquid Chromatography, 11(16): 3403–3413 https://doi.org/10.1080/01483918808082263
29
K S Grunnet, I Dahllof. (2005). Environmental fate of the antifouling compound zinc pyrithione in seawater. Environmental Toxicology and Chemistry, 24(12): 3001–3006 https://doi.org/10.1897/04-627R.1
30
F A Guardiola, A Cuesta, J Meseguer, M A Esteban. (2012). Risks of using antifouling biocides in aquaculture. International Journal of Molecular Sciences, 13(2): 1541–1560 https://doi.org/10.3390/ijms13021541
31
A Ç Günal, P Arslan, N İpiçürük, R Tural, A S Dinçel. (2022). Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio). Energy, Ecology and Environment, 7(5): 523–531 https://doi.org/10.1007/s40974-022-00245-6
32
E Gutner-Hoch, R Martins, F Maia, T Oliveira, M Shpigel, M Weis, J Tedim, Y Benayahu. (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 https://doi.org/10.1016/j.envpol.2019.05.031
33
E Gutner-Hoch, R Martins, T Oliveira, F Maia, A Soares, S Loureiro, C Piller, I Preiss, M Weis, S Larroze. et al.. (2018). Antimacrofouling efficacy of innovative inorganic nanomaterials loaded with booster biocides. Journal of Marine Science and Engineering, 6(1): 6 https://doi.org/10.3390/jmse6010006
34
H Harino. (2004). Occurrence and degradation of representative TBT free-antifouling biocides in aquatic environment. Coastal Marine Science, 29(1): 28–39
35
H Harino, S Eguchi, M Ohji. (2012). Occurrence of antifouling biocides in Japan and Southeast Asia: the survey for 10 years. Coastal Marine Science, 35: 246–254
36
H Harino, M Kitano, Y Mori, K Mochida, A Kakuno, S Arima. (2005). Degradation of antifouling booster biocides in water. Journal of the Marine Biological Association of the United Kingdom, 85(1): 33–38 https://doi.org/10.1017/S0025315405010799h
37
H Harino, Y Yamamoto, S Eguchi, S C Kawai, Y Kurokawa, T Arai, M Ohji, H Okamura, N Miyazaki. (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 https://doi.org/10.1007/s00244-006-0087-2
38
L Holmes, A Turner. (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 https://doi.org/10.1016/j.envpol.2009.06.018
39
F Horiguchi, T Eriguchi, T Ichikaw, K Nakata. (2009). Ecological risk assessment of copper pyrithione (CuPT) in Tokyo Bay. Journal of Advanced Marine Science and Technology Society, 15(1): 1–13
40
S M Jung, J S Bae, S G Kang, J S Son, J H Jeon, H J Lee, J Y Jeon, M Sidharthan, S H Ryu, H W Shin. (2017). Acute toxicity of organic antifouling biocides to phytoplankton Nitzschia pungens and zooplankton Artemia larvae. Marine Pollution Bulletin, 124(2): 811–818 https://doi.org/10.1016/j.marpolbul.2016.11.047
41
N S Kim, S H Hong, J G An, K H Shin, W J Shim. (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 https://doi.org/10.1016/j.marpolbul.2015.03.010
42
N S Kim, W J Shim, U H Yim, S H Hong, S Y Ha, G M Han, K H Shin. (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 https://doi.org/10.1016/j.marpolbul.2013.10.043
43
N Kobayashi, H Okamura. (2002). Effects of new antifouling compounds on the development of sea urchin. Marine Pollution Bulletin, 44(8): 748–751 https://doi.org/10.1016/S0025-326X(02)00052-8
44
A Koutsaftis, I Aoyama. (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 https://doi.org/10.1016/j.scitotenv.2007.07.023
45
A Koutsaftis, I Aoyama. (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 https://doi.org/10.1080/10934520802329794
46
J B Kristensen, R L Meyer, B S Laursen, S Shipovskov, F Besenbacher, C H Poulsen. (2008). Antifouling enzymes and the biochemistry of marine settlement. Biotechnology Advances, 26(5): 471–481 https://doi.org/10.1016/j.biotechadv.2008.05.005
47
N Kumari, M Jassal, A K Agrawal. (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 https://doi.org/10.1016/j.mtcomm.2022.105174
48
F Larson, D G Petersen, I Dahllöf, K Sundbäck. (2007). Combined effects of an antifouling biocide and nutrient status on a shallow-water microbenthic community. Aquatic Microbial Ecology, 48(3): 277–294 https://doi.org/10.3354/ame048277
49
V Lavtizar, D Kimura, S Asaoka, H Okamura. (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 https://doi.org/10.1016/j.ecoenv.2017.08.039
50
S Lee, M N Haque, D H Lee, J S Rhee. (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 https://doi.org/10.1016/j.cbpc.2023.109694
51
A J Li, P T Leung, V W Bao, A X Yi, K M Leung. (2014). Temperature-dependent toxicities of four common chemical pollutants to the marine medaka fish, copepod and rotifer. Ecotoxicology, 23(8): 1564–1573 https://doi.org/10.1007/s10646-014-1297-4
52
X Li, S Ru, H Tian, S Zhang, Z Lin, M Gao, J Wang. (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 https://doi.org/10.1016/j.scitotenv.2021.149131
53
X Li, J Wang, W Ba, S Zhang, Z Lin, M Gao, H Tian, S Ru. (2022). Mechanistic revealing of reproductive behavior impairment in male guppy (Poecilia reticulata) induced by environmentally realistic 2,2'-dithiobis-pyridine exposure. Chemosphere, 286: 131839 https://doi.org/10.1016/j.chemosphere.2021.131839
54
S LiangQ (2023) Zhong. Reducing environmental impacts through socioeconomic transitions: critical review and prospects. Frontiers of Environmental Science & Engineering, 17(2), 24
55
N Liu, C Liu, X Li, S Liao, W Song, C Yang, C Zhao, H Huang, L Guan, P Zhang. et al.. (2014). A novel proteasome inhibitor suppresses tumor growth via targeting both 19S proteasome deubiquitinases and 20S proteolytic peptidases. Scientific Reports, 4(1): 5240 https://doi.org/10.1038/srep05240
56
K Maraldo, I Dahllöf. (2004a). Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Marine Pollution Bulletin, 48(9–10): 894–901 https://doi.org/10.1016/j.marpolbul.2003.11.013
57
K Maraldo, I Dahllöf. (2004b). Seasonal variations in the effect of zinc pyrithione and copper pyrithione on pelagic phytoplankton communities. Aquatic Toxicology, 69(2): 189–198 https://doi.org/10.1016/j.aquatox.2004.05.006
58
M Marcheselli, C Rustichelli, M Mauri. (2010). Novel antifouling agent zinc pyrithione: determination, acute toxicity, and bioaccumulation in marine mussels (Mytilus galloprovincialis). Environmental Toxicology and Chemistry, 29(11): 2583–2592 https://doi.org/10.1002/etc.316
59
S E Martins, G Fillmann, A Lillicrap, K V Thomas. (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 https://doi.org/10.1080/08927014.2017.1404036
60
K McNally, N Warren, W Fransman, R K Entink, J Schinkel, M Van Tongeren, E Tielemans. (2014). Advanced REACH Tool: a Bayesian model for occupational exposure assessment. Annals of Occupational Hygiene, 58(5): 551–565
61
A Mishra, K Y Djoko, Y H Lee, R M Lord, G Kaul, A Akhir, D Saxena, S Chopra, J W Walton. (2023). Water-soluble copper pyrithione complexes with cytotoxic and antibacterial activity. Organic and Biomolecular Chemistry, 21(12): 2539–2544 https://doi.org/10.1039/D2OB01224C
62
K MochidaH AmanoK ItoM ItoT Onduka H IchihashiA KakunoH HarinoK (2012) Fujii. 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
K Mochida, H Amano, T Onduka, A Kakuno, K Fujii. (2011). Toxicity and metabolism of copper pyrithione and its degradation product, 2,2'-dipyridyldisulfide in a marine polychaete. Chemosphere, 82(3): 390–397 https://doi.org/10.1016/j.chemosphere.2010.09.074
64
K Mochida, K Ito, H Harino, A Kakuno, K Fujii. (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 https://doi.org/10.1897/05-688R.1
65
K Mochida, K Ito, H Harino, T Onduka, A Kakuno, K Fujii. (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 https://doi.org/10.1897/07-176R1.1
66
K Mochida, K Ito, H Harino, H Tanaka, T Onduka, A Kakuno, K Fujii. (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 https://doi.org/10.1016/j.cbpc.2009.01.003
67
F Mohamat-Yusuff, A G Sarah-Nabila, S Z Zulkifli, M N A Azmai, W N W Ibrahim, S Yusof, A Ismail. (2018). Acute toxicity test of copper pyrithione on Javanese medaka and the behavioural stress symptoms. Marine Pollution Bulletin, 127: 150–153 https://doi.org/10.1016/j.marpolbul.2017.11.046
68
H O’Brien, T Davoodian, M D Johnson. (2023). The promise of copper ionophores as antimicrobials. Current Opinion in Microbiology, 75: 102355 https://doi.org/10.1016/j.mib.2023.102355
69
H N Oh, W K Kim. (2023). Copper pyrithione and zinc pyrithione induce cytotoxicity and neurotoxicity in neuronal/astrocytic co-cultured cells via oxidative stress. Scientific Reports, 13(1): 23060 https://doi.org/10.1038/s41598-023-49740-8
70
M Ohji, H Harino. (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 https://doi.org/10.1007/s00244-017-0367-z
71
M Ohji, H Harino, W J Langston. (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 https://doi.org/10.1017/S0025315418001169
72
H Okamura, N Kobayashi, M Miyanaga, Y Nogami. (2006). Toxicity reduction of metal pyrithiones by near ultraviolet irradiation. Environmental Toxicology, 21(4): 305–309 https://doi.org/10.1002/tox.20183
73
H Okamura, T Nishida, Y Ono, W J Shim. (2003). Phytotoxic effects of antifouling compounds on nontarget plant species. Bulletin of Environmental Contamination and Toxicology, 71(5): 881–886 https://doi.org/10.1007/s00128-003-8803-3
74
H Okamura, L Togosmaa, T Sawamoto, K Fukushi, T Nishida, T Beppu. (2012a). Effects of metal pyrithione antifoulants on freshwater macrophyte Lemna gibba G3 determined by image analysis. Ecotoxicology, 21(4): 1102–1111 https://doi.org/10.1007/s10646-012-0865-8
75
H Okamura, T Watanabe, I Aoyama, M Hasobe. (2002). Toxicity evaluation of new antifouling compounds using suspension-cultured fish cells. Chemosphere, 46(7): 945–951 https://doi.org/10.1016/S0045-6535(01)00204-1
76
H Okamura, M Yagi, M Kawachi, T Hanyuda, H Kawai, I Walker. (2012b). Application of rotating cylinder method for ecotoxicological evaluation of antifouling paints. Toxicological and Environmental Chemistry, 94(3): 545–556 https://doi.org/10.1080/02772248.2012.662811
77
T Onduka, K Mochida, H Harino, K Ito, A Kakuno, K Fujii. (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 https://doi.org/10.1007/s00244-009-9430-8
78
E Paçal, B A Gümüş, A Ç Günal, B Erkmen, P Arslan, Z Yıldırım, F Erkoç. (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 https://doi.org/10.2298/PIF2202063P
79
C A Paz-Villarraga, Í B Castro, G Fillmann. (2022). Biocides in antifouling paint formulations currently registered for use. Environmental Science and Pollution Research, 29(20): 30090–30101 https://doi.org/10.1007/s11356-021-17662-5
80
D G Petersen, I Dahllof, L P Nielsen. (2004). Effects of zinc pyrithione and copper pyrithione on microbial community function and structure in sediments. Environmental Toxicology and Chemistry, 23(4): 921–928 https://doi.org/10.1897/03-196
81
V Piazza, I Dragić, K Sepčić, M Faimali, F Garaventa, T Turk, S Berne. (2014). Antifouling activity of synthetic alkylpyridinium polymers using the barnacle model. Marine Drugs, 12(4): 1959–1976 https://doi.org/10.3390/md12041959
82
J A Romano, D Rittschof, P D McClellan-Green, E R Holm. (2010). Variation in toxicity of copper pyrithione among populations and families of the barnacle, Balanus amphitrite. Biofouling, 26(3): 341–347 https://doi.org/10.1080/08927010903511618
83
E Sanjuan, J Barriga-Cuartero, O Andreu-Sánchez, A González, B Fouz. (2023). Study of sustainable HDPE-based materials for aquaculture applications: effects on fouling. Frontiers in Marine Science, 10: 1268695 https://doi.org/10.3389/fmars.2023.1268695
84
D Shin, Y Choi, Z Y Soon, M Kim, D J Kim, J H Jung. (2022). Comparative toxicity study of waterborne two booster biocides (CuPT and ZnPT) on embryonic flounder (Paralichthys olivaceus). Ecotoxicology and Environmental Safety, 233: 113337 https://doi.org/10.1016/j.ecoenv.2022.113337
85
S Sonak, P Pangam, A Giriyan, K Hawaldar. (2009). Implications of the ban on organotins for protection of global coastal and marine ecology. Journal of Environmental Management, 90: S96–S108 https://doi.org/10.1016/j.jenvman.2008.08.017
86
K Sundbäck, Petersen D Groth, I Dahllöf, F. (Ref. "Sundbäck Larson. (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 https://doi.org/10.3354/meps330013
87
K (2009) Takahashi. 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
G Tan, J Yang, T Li, J Zhao, S Sun, X Li, C Lin, J Li, H Zhou, J Lyu. et al.. (2017). Anaerobic copper toxicity and iron-sulfur cluster biogenesis in Escherichia coli. Applied and Environmental Microbiology, 83(16): e00867–17 https://doi.org/10.1128/AEM.00867-17
89
E Taşcı, S Hayretdağ. (2022). Investigation of spermiotoxic, embryotoxic and cytotoxic effects of copper pyrithione on Paracentrotus lividus (Lamarck, 1816). Pesticides and Phytomedicine, 37(1): 29–39 https://doi.org/10.2298/PIF2201029T
N Třešňáková, Günal A Çağlan, Kankılıç G Başaran, E Paçal, Tavşanoğlu Ü Nihan, R Uyar, F Erkoç. (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 https://doi.org/10.1080/02757540.2020.1735377
92
P A Turley, R J Fenn, J C Ritter. (2000). Pyrithiones as antifoulants: environmental chemistry and preliminary risk assessment. Biofouling, 15(1−3): 175–182 https://doi.org/10.1080/08927010009386308
93
P A Turley, R J Fenn, J C Ritter, M E Callow. (2005). Pyrithiones as antifoulants: environmental fate and loss of toxicity. Biofouling, 21(1): 31–40 https://doi.org/10.1080/08927010500044351
94
H Wang, Y Li, H Huang, X Xu, Y Wang. (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 https://doi.org/10.1002/etc.440
95
A Whelan, F Regan. (2006). Antifouling strategies for marine and riverine sensors. Journal of Environmental Monitoring, 8(9): 880–886 https://doi.org/10.1039/b603289c
96
H Yamada. (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
D M Yebra, S Kiil, K Dam-Johansen. (2004). Antifouling technology–past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progress in Organic Coatings, 50(2): 75–104 https://doi.org/10.1016/j.porgcoat.2003.06.001
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
