Biocide’s occurrence in the antifouling paint formulations registered for use
Different profiles of biocides register and/or use may be associated to different nationwide or international restrictions. Chlorothalonil and Irgarol, for instance, were banned in the EU (ECHA 2019), while TBT and TPT were banned worldwide in 2008 by IMO (IMO 2008). This pattern can be seen in the present study, where cuprous oxide was the only biocide present in all databases, while DCOIT and zinc pyrithione were in all but OTSAF. BRAF and JPMA dataset showed, respectively, 15 and 14 out of 25 different active ingredients registered for use, whilst the remaining presented 8 to 10 biocides (Fig. 1). Although 25 biocides were identified in the current dataset (Fig. 1), the number reached 30 active ingredients registered and/or used in paint or coating formulations already listed in antifouling systems for vessels and other submerged surfaces (Omae 2003; Thomas and Brooks 2010; Castro et al. 2011) (Table 1). Even listed as antifouling biocides in these previous reviews, capsaicin, copper naphthenate, maneb, N-(2,4,6-Trichlorophenyl) maleimide and TCMTB (Busan) were not found in any antifouling paint formulations registered for use in the dataset used in the current study. It does not necessarily mean they are no longer used as biocides and may be a limitation of the current dataset. On contrary, even not previously listed in the reviews, copper, cupric oxide, cupric acetate, N-ethyl-2-methylbenzenesulfonamide and terbutrin have been identified in antifouling paint formulations registered for use.
The biocides most frequently registered for use were the metal-based (e.g., copper or zinc). Cuprous oxide, copper pyrithione, zinc pyrithione, zineb and cuprous thiocyanate were present in 76.1, 28.8, 16.7, 11.5 and 8.8 % of the examined antifouling paint formulations, respectively (Fig. 2). Indeed, cuprous oxide has already been identified as a biocide frequently used in antifouling paints (Omae 2003; van Wezel and van Vlaardingen 2004; Thomas and Brooks 2010; Castro et al. 2011). In addition, zinc oxide and copper were present in 3.7 and 1.6 % of the reviewed formulations. However, the non-metallic biocides DCOIT, Irgarol, PTPB, diuron, tralopyril and dichlofluanid were also listed in 9.3, 4.5, 4.1, 3.9, 2.7 and 1.9 %, respectively, of paint formulations registered for use. Thiram, tolyfluanid, chlorothalonil, tributyltin methacrylate, Ziram, tebutrin, medetomidine, tributyltin oxide, TCMS, cupric oxide, cupric acetate and N-ethyl-2-methylbenzenesulfonamide were listed in less than 1% of examined paints. Thus, there may have been a decrease in the frequency of use of some compounds described in the literature as “commonly used”, such as dichlofluanid and chlorothalonil (Omae 2003; van Wezel and van Vlaardingen 2004; Harino 2017), since they were listed in less than 2% of paints formulations currently registered for use. Such decrease is also seen by comparing a previous study in Japan, that reported chlorothalonil and dichlofluanid in 5.2 and 6 %, respectively, of paint formulations (Okamura and Mieno 2006), and the present JPMA dataset, where only chlorothalonil (1.1 %) was reported. Although still among the top 10 most frequently used biocides within the revised paint formulations, the same applies for diuron and Irgarol that have decreased from 16.6 % and 8.4 % (Okamura and Mieno 2006) to 8.2 % and 5.8 % (present JPMA dataset), respectively, their frequency in formulations registered for use. Postulated as antifouling candidates a decade ago (Pérez et al. 2009; Thomas and Brooks 2010), pyridine-triphenylborane (PTPB) (4.1%), tralopyril (2.7%) and medetomidine (0.2%) still presented a relatively low frequency of use in the registered formulations. DCOIT (9.3 %) is the fifth most frequently registered biocide for use, being increased its frequency of use in comparison to what was previously seen in Japan (10.2 % from Okamura and Mieno (2006) to 15.1 % for the present JPMA dataset). Considering the representativeness of the current dataset, these can be considered global trends.
Table 1
Biocides as active ingredients of antifouling paint formulations identified in the databases and literature.
Common name | IUPAC name | CAS number | Identified in present work | Previously cited reference |
Capsaicin | (E)-N-[(4-hydroxy-3-methoxyphenyl)methyl]-8-methylnon-6-enamide | 404-86-4 | No | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Chlorothalonil | 2,4,5,6-tetrachloroisophthalonitrile | 1897-45-6 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Copper | Copper | 7440-50-8 | Yes | |
Copper naphthenate | copper,naphthalene-2-carboxylate | 1338-02-09 | No | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Copper pyrithione | copper, bis(1,hydroxy-2(1H)-pyridinethionato O,S)- | 14915-37-8 | Yes | Thomas and Brooks 2010; Castro et al. 2011 |
Cupric acetate/copper (II) acetate | copper; diacetate | 142-71-2 | Yes | |
Cupric oxide/copper (II) oxide | Oxocopper | 1317-38-0 | Yes | |
Cuprous oxide/copper (I) oxide | copper; hydrate | 1317-39-1 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Cuprous thiocyanate | copper (1+) thiocyanate | 1111-67-7 | Yes | Omae 2003; Castro et al. 2011 |
DCOIT | 4,5-dichloro-2-n-octyl-4-isothiazolin-3-one | 64359-81-5 | Yes | Omae 2003; Castro et al. 2011 |
Dichlofluanid | N-[dichloro(fluoro)methyl]sulfanyl-N-(dimethylsulfamoyl)aniline | 1085-98-9 | Yes | Omae 2003; Castro et al. 2011 |
Diuron | 3-(3,4-dichlorophenyl)-1,1-dimethylurea | 330-54-1 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Irgarol | 2-methylthio-4-tert-butylamino-6-cyclopropylamino-s-triazine | 28159-98-0 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Maneb | manganese(2+);N -[2-(sulfidocarbothioylamino)ethyl]carbamodithioate | 12427-38-2 | No | Thomas and Brooks 2010; Castro et al. 2011 |
Medetomidine | 5-[1-(2,3-dimethylphenyl)ethyl]-1H-imidazole | 86347-14-0 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
N-(2,4,6-Trichlorophenyl) maleimide | 1-(2,4,6-trichlorophenyl)pyrrole-2,5-dione | 13167-25-4 | No | Omae 2003; Thomas and Brooks 2010 |
N-ethyl-2-methylbenzenesulfonamide | N-ethyl-2-methylbenzenesulfonamide | 1077-56-1 | Yes | |
Pyridine-triphenylborane PTPB | pyridine;triphenylborane | 971-66-4 | Yes | Omae 2003; Castro et al. 2011 |
TCMS Pyridine / Densil | 2,3,5,6-tetrachloro-4-(methylsulphonyl)pyridine | 13108-52-6 | Yes | Omae 2003; Castro et al. 2011 |
TCMTB / Busan | 2-(thiocyanomethylthio)benzothiazole | 21564-17-0 | No | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Terbutrin | 2-N-tert-butyl-4-N-ethyl-6-methylsulfanyl-1,3,5-triazine-2,4-diamine | 886-50-0 | Yes | |
Thiram | dimethylcarbamothioylsulfanyl N,N-dimethylcarbamodithioate | 137-26-8 | Yes | Thomas and Brooks 2010; Castro et al. 2011 |
Tolylfluanid | methanesulfenamide, 1,1-dichloro-N-((dimethylamino) sulfonyl)-1-fluoro-N-(4-methylphenyl) | 731-27-1 | Yes | Thomas and Brooks 2010; Castro et al. 2011 |
Tralopyril | 4-bromo-2-(4-chlorophenyl)-5-(trifluoromethyl)-1H-pyrrole-3-carbonitrile | 122454-29-9 | Yes | Thomas and Brooks 2010; Castro et al. 2011 |
Tributyltin methacrylate | tributylstannyl 2-methylprop-2-enoate | 2155-70-6 | Yes | Omae 2003 |
Tributyltin oxide | tributyl(tributylstannyloxy)stannane | 56-35-9 | Yes | Omae 2003 |
Zinc oxide/zinc (II) oxide | oxozinc | 1314-13-2 | Yes | Castro et al. 2011 |
Zinc pyrithione | zinc-2-pyridinethiol-1-oxide | 13463-41-7 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Zineb | zinc ethylenebis (dithiocarbamate) | 12122-67-7 | Yes | Thomas and Brooks 2010 |
Ziram | zinc dimethyl dithiocarbamate | 137-30-4 | Yes | Omae 2003; Thomas and Brooks 2010; Castro et al. 2011 |
Simultaneous use of biocides in the paint formulations registered for use
The current dataset confirmed that manufactures are still using combinations of different biocides in antifouling paint formulations. Although a simultaneous use of up to four biocides has been previously reported (Okamura and Mieno 2006), the formulations examined in the present study proved that up to six biocides can be used simultaneously. The combination of two (51.6 %), one (33.3 %) and three (10.9 %) biocides were the most frequent, while 4 or more biocides were listed in only 1.8 % of paint formulations registered for use (Fig. 3). Biocide-free products were listed in 2.4 % of antifouling paint formulations. However, this number might be biased since only one database included biocide-free paints. In formulations using only one active ingredient, cuprous oxide, cuprous thiocyanate, zinc pyrithione, copper pyrithione, copper and pyridine-triphenylborane were present in 77.7, 6.2, 5.3, 3.2, 3.0 and 1.5 %, respectively, of examined antifouling paints registrations. DCOIT, Irgarol, cupric oxide, diuron, tralopyril, tributyltin methacrylate and tributyltin oxide were uniquely listed in less than 0.6 % of the assessed paints.
Formulations with more than one active ingredient were assessed and the main pairs of biocide combinations is shown in Fig. 4. Molecules containing copper (half of the circle plot are represented by these compounds), especially cuprous oxide and copper pyrithione, are the most frequent biocides used in the paint formulations registered for use. Although copper pyrithione represents almost 50% of the combinations, other biocides are also commonly associated to cuprous oxide, such as zineb, DCOIT, diuron, Irgarol, zinc oxide and zinc pyrithione. Other associations can also be found at much lower frequency (e.g., thiram and dichlofluanid), while some biocides do not appear in combination with cuprous oxide but with zinc pyrithione, such as cuprous thiocyanate, tralopyril and pyridine-triphenylborane (PTPB), or with DCOIT and with zinc oxide, such as N-ethyl-2-methylbenzenesulfonamide. Tralopyril is used in formulations sold as copper-free antifouling paints (Janssen 2019). In addition to zinc pyrithione, it can be eventually found in combination with zinc oxide or DCOIT. These biocides employed in formulations along with copper- and zinc-based compounds are so-known as booster biocides (Bowman et al. 2003; Takahashi 2009). These so-called co-biocides play an important role by improving the toxicity over the fouling organisms and, thus, the efficiency of antifouling paints (Myers et al. 2006; Silkina et al. 2012; Ohlauson and Blanck 2014).
Nominal concentration of biocides in the paint formulations registered for use
The biocides reports with the highest nominal concentrations (average ± standard deviation) in the paint formulations registered for use were cuprous oxide (35.9 ± 12.8 % w/w), tributyltin methacrylate (26.9 ± 18.8 % w/w), copper (powder) (19.3 ± 21.0 % w/w) and cuprous thiocyanate (18.1 ± 8.02 % w/w) (Fig. 5). Although the average copper (powder) concentration was 19.3%, this active ingredient was recorded in formulation with concentrations that can reach up to 66% w/w (Fig. 5), which will be mixed to create a product that will ultimately be used as antifouling paint. Those concentrations are probably responsible for the high environmental levels of copper in areas under the influence of maritime activities around the world (Eklund and Eklund 2014; Costa et al. 2016; Bighiu et al. 2016). Formulations using organometallic biocides, such as zineb, zinc pyrithione and copper pyrithione, were listed with average concentrations of 5.4 ± 2.0, 4.0 ± 5.3, 2.9 ± 1.6 % w/w, respectively, while the metal-free biocides, such as tralopyril, diuron, thiram, DCOIT, Irgarol, dichlofluanid and terbutrin, were listed with average levels of 5.2 ± 1.8, 3.9 ± 1.5, 2.4 ± 0.1, 1.9 ± 1.9, 1.7 ± 0.6, 1.6 ± 0.8 and 0.05 ± 0 % w/w, respectively. Concentrations for Ziram (5 % w/w), cupric acetate (3 % w/w) and N-ethyl-2-methylbenzenesulfonamide (3 % w/w) were reported for single paint products (Fig. 5). No information was available regarding concentrations used in the assessed antifouling paint formulations containing chlorothalonil, medetomidine, pyridine-triphenylborane (PTPB), TCMS pyridine/Densil and tolylfluanid.
In general, biocides used at lower concentrations are more toxic (e.g., Irgarol, DCOIT, dichlofluanid) than those used at higher concentration (Brooks and Waldock 2009; Silkina et al. 2012; Harino 2017), which may explain the observed concentration pattern. Some of these biocides have been found in environmental samples nearby areas of intense maritime traffic, which make antifouling paints one of their most likely source, even for formulations using relatively low concentrations (Harino 2017).
Environmental levels of biocides present in the antifouling paint formulations registered for use
Environmental levels of some biocides used in the antifouling paint formulations reviewed are summarized in Table S3 (Online Resource 1). The high concentrations of copper reported in sediments of Brazil (up to 768 µg g− 1 dw; (Costa et al. 2016))and biofouling and boat hull in Sweden (4,686 ± 5,506 and 7,122 ± 12,207 µg g− 1 dw, respectively; (Bighiu et al. 2016))nearby ports and shipyards areas (Table S3, Online Resource 1) could be related, in some cases, to the high frequency of use of highly concentrated copper-based antifouling paints. The present study has pointed out that cuprous oxide and another cooper compounds are the most used active ingredients in paint formulations registered for use. Thus, copper associated to antifouling paints continues to be an important subject of monitoring, especially the most toxic labile fraction for the biota (Brooks and Waldock 2009) and in areas with restrict water circulation and high boat and ship traffic.
Zinc has also been found in high concentrations in the environment (e.g., up to 578 µg g− 1 dw in sediments of Brazil (Costa et al. 2016); 21,650 ± 41,092 and 29,568 ± 31,024 µg g− 1 dw, respectively, in biofouling and boat hulls in Sweden (Bighiu et al. 2016)) (Table S3, Online Resource 1), which may be also associate to its wider use as antifouling paint biocide (Soroldoni et al. 2018). Zinc-based biocides made up to 32 % of frequency of use in the assessed antifouling paint formulations (present study), where zinc oxide is used in a high average concentration, while the other zinc-based biocides are used in concentration up to 5 % w/w. Although zinc oxide is considered one of the main contributors to the environment contamination (Costa et al. 2016), less than 4% of the antifouling paint formulations reviewed are using zinc oxide as an active ingredient. However, this frequency of use can be underestimated and should be carefully considered since not all data sources listed this compound as an active biocide in the antifouling paint formulations. In the current dataset, only APVMA and BRAF reported zinc oxide. Although it has antifouling properties and has been used as antifouling biocide since the mid-twentieth century (Castro et al. 2011), in some cases, in legal terms (e.g., European Union, UE), zinc oxide is not considered an active biocide in antifouling paints (DIRECTIVE 98/8/EC OF THE EUROPEAN PARLIAMENT AND OF THE COUNCIL 1998).
Despite the relative relevance of copper and zinc pyrithione, and copper thiocyanate as active ingredients in antifouling paint formulations, little information is available about their environmental levels. Although Cu-pyrithione had being detected (22 ng g− 1 dw) in a study performed in Japan (Harino et al. 2007), most of the few studies carried out in both water and sediments found levels of Cu- and Zn-pyrithiones below detection limits (< LODs) (Harino et al. 2005; Eguchi et al. 2010; Kim et al. 2014, 2015) (Table S3, Online Resource 1). The rapid degradation and transquelation make the detection of these compounds difficult (Soon et al. 2019). Thiocyanate (SCN−) had been detected in coastal waters of Japan (Rong et al. 2005) and Portugal (Silva et al. 2011), but the association with its use as antifouling biocide was not assessed. Similar situation can occur with other biocides. Although tralopyril and medetomidine may be present in the environment, since they are offered by the paint industry as a copper-free option (Janssen 2019; I-Tech AB 2020), they have not yet been sufficiently evaluated or reported in monitoring studies. Therefore, the knowledge about the presence and sources of these compounds must be improved to enable a better appraisal towards the risks associated to their use as antifouling paint biocides.
Diuron, Irgarol, DCOIT, dichlofluanid, chlorothalonil, TCMTB and TBT, identified as active ingredients in the present study, have also been detected in the aquatic environment (Table S3, Online Resource 1). Interestingly, the non-metallic biocides detected in environmental samples were present in less than 10% of paint formulations registered for use at average concentrations lower than 5% w/w. In the case of DCOIT, despite its low environmental half-life (Jacobson and Willingham 2000), it has been frequently detected in water and sediments under the influence of maritime activities (e.g., ports and marinas) (Chen and Lam 2017; Abreu et al. 2020), which is a clear indication of the high frequency of use of antifouling paints with this biocide as active ingredient.
Despite pointing out, especially in conjunction with previously reported environmental levels, which biocides may be more relevant to future environment studies, the present study (based on their frequency of occurrence in antifouling paint formulations registered for use in their respective regions) only partially reflects the current general situation. It was not an exhaustive compilation of all paints worldwide registered for use and some relevant information was not available to be considered. To perform a more accurate study, it would have been crucial to consider the relative frequency of use of these antifouling paints (and consequently their active ingredients) by countries or region. As the amount of each antifouling paint used in each region/country is unknown, even a biocide that occurs less frequently in the formulations reviewed can end up having a significant environmental level. In addition, it is also important to consider that some of these biocides, such as diuron, chlorothalonil and dichlofluanid (Jennings and Li 2017; ANVISA 2017; HSE 2021), are also active ingredients of pesticides used in agriculture or as wood preservatives. Thus, these alternative sources can contribute to the contamination levels detected in aquatic environments, mainly when used nearby water bodies. For these reason, marketing studies and databases of antifouling products and frequencies of application in boats and ships must be generated or become publicly available data. This action may potentially improve the understanding of input rates and, consequently, the environment levels, which end up providing a better starting point for environmental and ecotoxicological studies.