Occurrence and partitioning of antifouling booster biocides in sediments and porewaters from Brazilian Northeast

Environmental Pollution 255 (2019) 112988

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Occurrence and partitioning of antifouling booster biocides in sediments and porewaters from Brazilian Northeast*
Lucas Martins Viana a, Sara Raiane Viana dos Santos a, Jose
rcio Aure
lio Pinheiro Almeida b Teresa Cristina Rodrigues dos Santos Franco a, *, Ma a b

~o, Av. Dos Portugueses, 1966, Sa ~o Luís, Maranha ~o, Brazil
rio de Química Analítica e Ecotoxicologia (LAEC), Universidade Federal do Maranha Laborato ~o, Av. Dos Portugueses, 1966, Sa ~o Luís, Maranha ~o, Brazil Curso de Ci^ encia e Tecnologia, Universidade Federal do Maranha

a r t i c l e i n f o

a b s t r a c t

Article history: Received 27 May 2019 Received in revised form 30 July 2019 Accepted 30 July 2019 Available online 5 August 2019

Fouling organisms attach and grow on submerged surfaces causing several economic losses. Thus, biocides have been introduced in antifouling paints in order to avoid this phenomenon, but their widespread use became a global problem, mainly in ports, leisure and fishing boat harbors, since these substances can be highly toxic to non-target organisms. The occurrence and environmental behavior of antifouling biocides are especially unknown in some peculiar regions, such as Amazon areas. Thus, the aim of this work was to evaluate, for the first time, levels and the partitioning behavior of the antifouling organic biocides irgarol, diuron and also stable degradation products of dichlofluanid and diuron (DMSA and DCPMU, respectively) in sediments and porewaters from a high boat traffic area located in the Northeast of Brazil, a pre-Amazon region. Our results showed high concentrations of irgarol (<1.0 e89.7 mg kg
1) and diuron (<5.0e55.2 mg kg
1) in sediments. In porewater, DCPMU (<0.03e0.67 mg L
1) and DMSA (<0.008e0.263 mg L
1) were the mainly substances detected. High Kd and Koc obtained for both irgarol and diuron showed a partitioning preference in the solid phase. This work represents one of the few registers of contamination by antifouling substances in Amazonian areas, despite their environmental relevance. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Antifouling Porewater Sediment Partitioning Brazilian Northeast

1. Introduction Marine biofouling is the undesirable accumulation of microorganisms, plants, and animals on artificial surfaces immersed in sea water. It is ubiquitous in the marine environment and causes serious problems for the shipping industry (Dafforn et al., 2011; Yebra et al., 2004). Its effects on ship hulls include frictional resistance, loss of maneuverability, increase in the frequency of drydocking operations and corrosion processes, which lead to an increased fuel consumption (Yebra et al., 2004). In order to prevent and minimize impacts from biofouling, antifouling paints are applied to boat hulls and other submerged structures (Turner, 2010) to maximize their effects against biofouling organisms. For a long time organotins, such as tributyltin (TBT), were the most used antifouling agents, however, due their extreme toxicity, they were banned from new formulations by International Maritime

* This paper has been recommended for acceptance by Eddy Y. Zeng. * Corresponding author. E-mail address: [email protected] (T.C.R. dos Santos Franco).

https://doi.org/10.1016/j.envpol.2019.112988 0269-7491/© 2019 Elsevier Ltd. All rights reserved.

Organization (IMO) (Almeida et al., 2007; Amara et al., 2018; Castro et al., 2011; Tornero and Hanke, 2016). Some substitutes of TBT-based paints widely used in recent years include non-metallic organic compounds such as irgarol (2methythio-4-tert-butylamino-6-cyclopropylamino-s-triazine), diuron (3-(3,4-dichlorophenyl)-1,1-dimethylurea) and dichlofluanid (1,1-dichloro-N-[(dimethylamino)sulfonyl]-1-fluoro-Nphenylmethane-sulfonamide), which are used along with copper to improve its performance against certain more resistant algal fouling (Tornero and Hanke, 2016). Irgarol is a herbicide used as an antifouling biocide, being one of the world's most detected antifouling biocides (Castro et al., 2011). It acts inhibiting the photosystem-II by interfering with the photosynthetic electron capture in chloroplasts (Yebra et al., 2004). Diuron is a substituted phenylurea herbicide frequently employed for the control of a range of crops but also as antifouling biocide. Diuron acts inhibiting photosynthesis by preventing oxygen production and blocking electron transfer at the level of photosystem-II of photosynthetic organisms (Giacomazzi and Cochet, 2004), and degrades by Ndemethylation under aerobic conditions to metabolites, including

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DCPMU (1-(3,4-dichlorophenyl)-3-methylurea) (Gatidou and Thomaidis, 2007). Dichlofluanid is a fungicide that acts as inhibitor of thiol-containing enzymes (Ansanelli et al., 2017) and it is characterized by a high hydrolytic transformation rate, resulting in a few hours half-life in seawater at different temperatures. Despite this, its major degradation product, N0 -dimethyl-N-phenyl-sulphamide (DMSA), is stable and remains for long periods without further hydrolysis (Hamwijk et al., 2005; Schouten et al., 2005). Both diuron and irgarol are classified as priority substances according to the European Union Directive 2013/39/EU (Sousa et al., 2018) and their use is prohibited in antifouling formulations in European countries (Decision (EU), No 2016/107, Commission Decision 2007/565/EC, respectively). On the other hand, Brazil does not regulate the use of these substances. The toxicity of such substances was investigated on a wide range of organisms (Akcha et al., 2012; Ali et al., 2015; Barranger et al., 2014; Cardoso et al., 2013; Katsumata and Takeuchi, 2017; Mai et al., 2013; Moreira et al., 2018; Pereira et al., 2015; Zhang et al., 2019). However, limited information is available on the presence of those compounds in sediments and porewaters, and a study focusing on the occurrence and behavior of antifouling biocides in both matrices simultaneously, as far as we know, is inexistent in South America. Porewater is one important mean by which the toxicity of a contaminant may affect aquatic organisms, since the fraction of contaminants associated with the sediment particles is unlikely to be bioavailable (Mozeto, 2006). So, sediment-porewater partitioning is a fundamental process controlling the transport, fate and ecotoxicological risk of the microlevels of lipophilic contaminants in the aquatic environment (Xu et al., 2014; Yu et al., 2009). Even after years being used in antifouling formulations, knowledge on the occurrence, fate and behavior of this type of contamination is still poorly studied in tropical areas, such as the Brazilian coast (Diniz et al., 2014; Dominguez et al., 2014), despite being an area of recognized environmental relevance. In South America, studies about antifouling biocides mainly have focused on TBT (Artifon et al., 2016; Batista et al., 2016; Castro et al., 2018). On the other hand, the presence and fate of antifouling booster biocides have been widely evaluated in European (Ansanelli et al., 2017; Gonzalez-Rey et al., 2015), Asian (Lam et al., 2017; Lee and Lee, 2016) and North American areas (Gardinali et al., 2002; Sapozhnikova et al., 2013). ~o Luís island is located at the Northeast of Brazil, just where Sa the Amazonian region begins. Due to its proximity to North ~o Luís has one of the biggest American and European markets, Sa commercial ports in Brazil (Itaqui Port). Additionally, there are several small fishing harbors, ports for passenger transport and vessel maintenance that surround the entire island, being potential sources of contamination by antifouling substances. Thus, this work aimed to provide first insights on the current contamination status and spatial distribution of commonly used antifouling biocides (irgarol, diuron, DCPMU and DMSA) in sediments and porewaters ~o Luís. Moreover, the partitioning behavior from boating areas of Sa between these two environmental compartments and possible risks posed to biota were further investigated.

Analytical standards of diuron, DCPMU and the internal isotopically labeled standards atrazine-d5 and diuron-d6 were purchased from Sigma-Aldrich (St. Louis, MO, USA). DMSA and irgarol were acquired from Dr. Ehrenstorfer (Augsburg, Germany). Octadecylsilane (C18) was obtained from solid-phase extraction cartridges Strata® C18-E (55 mm, 70 Å) (Phenomenex®, Torrance, CA, USA). Individual standard stock solutions (10 mg mL
1) for each one of the analytes were prepared in methanol, and then stored in the dark at 4  C. A mixture of all analytes at 0.5 mg mL
1 was used as spiking solution, except the isotopically labeled internal standards, which were prepared separately at 1 mg mL
1. 2.2. Instrumentation Chromatographic analyses were carried out by a binary HPLC pump 1525m (Waters®) using a Kinetex® C18 (100  3.0 mm I.D.) (5 mm; 10 Å) analytical column (Phenomenex®, Torrance, CA, USA). Ultrapure acidified water (0.1% formic acid) (A) and acetonitrile (B) were used as mobile phases and the elution was performed in gradient mode as follows: 0e2 min, 90% (A)/10% (B); 2e4.5 min, 10% (A)/90% (B); 4.5e6 min, 90% (A)/10% (B). The flow rate was 0.3 mL min
1, the oven temperature was 30  C and the injection volume was 5 mL. The detection of the analytes was performed by a mass spectrometer SQ Detector 2 (Waters®), equipped with electrospray ionization (ESI) source. All analytes were analyzed in the positive mode (ESþ) and at least two different mass charge ratios (m/z) were monitored for each analyte in SIR (single ion recording) mode. More information on the MS method can be found in Supplementary Information (Text S1; Table S1). 2.3. Sampling area ~o Luís Island, located in the northeast of Brazil, is the capital of Sa ~o State, and is part of the Brazilian Amazon region. It is in Maranha one of the biggest mangrove zones in the world (Souza Filho, 2005), providing a unique ecological environment for diverse fauna and flora. Due to its strategic geographical location, a large port complex ~o Luís, with Itaqui Port accounting for more than 22 is based in Sa million tons of cargo in 2018, according to data from Itaqui Port Authority (EMAP) (http://www.portodoitaqui.ma.gov.br/). Moreover, several fishing harbors, ports for passenger transport and small shipyards surround the entire island, being potential inputs of contamination by antifouling substances into the aquatic environment. In order to provide information on the occurrence of antifouling substances in sediments and porewaters from this region, ~o Luís Island coast ten sampling points were selected along Sa (Fig. 1; Table S3). The sites were chosen to be representative of the most common boating activities taking place in the Island. According to this criterion, sampling points were divided as follows: (1) fishing sites, covering small fishermen villages and commercial fishing harbors, (2) waterway transport/leisure boating, covering two terminals frequented by ferry boats and a marina frequented by leisure crafts and (3) commercial port, located in a very busy pier in Itaqui Port. Additional information can be seen in Table S3.

2. Materials and methods 2.4. Samples collection and treatment 2.1. Chemicals HPLC grade methanol, acetonitrile and formic acid were acquired from Merck (Darmstadt, Germany). Trichloromethane was purchased from Honeywell International Inc. (Muskegon, MI, USA), and ultrapure water (18.2 MU cm; 25  C) was obtained by a DirectQ®3 UV ultra-purification system (Millipore, Milford, MA, USA).

About 2 kg of sub-superficial sediment was collected per site in April 2018 by a Van Veen grab sampler, in duplicate. The samples were put into stainless steel trays and transported to the laboratory. Each sediment sample was divided into two parts: the first one was frozen, and then freeze-dried (72 h) and the second one was used for obtaining porewaters. In order to determine total organic

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~o Luís Island. Fig. 1. Sampling sites in Sa

carbon (TOC), freeze-dried sediments were previously homogenized, and 1.0 g of a composite sample from each sampling site was put into a desiccator under concentrated HCl vapor for 48 h for removing inorganic carbon. Afterwards, the samples were oven dried (60  C) until constant weight and 0.05 g were analyzed by a TOC-L total organic carbon analyzer coupled to a combustion unit to solid samples SSM-500A (Shimadzu). Particle-size analysis was performed using calibrated metal sieves for determination the grain size from 2 mm to 63 mm in mesh diameter, and this characteristic was presented as % of fine fraction (<63 mm). Porewater was removed from sediments by a vacuum extractor consisting in a 20 cm vacuum ceramic filter. No further treatment was needed before chemical extractions of the biocides from this matrix.

2.6. Extraction of antifouling biocides from porewater samples The analytes were extracted from porewaters according to a vortex assisted liquid-liquid microextraction (VA-DLLME) methodology fully validated by our research group: 7.5 mL of porewater (pH 4.0) was transferred to 15 mL conical glass tubes, followed by a rapid injection of 1.5 mL of a 1:10 mixture of trichloromethane and acetonitrile. The samples were vortexed for 30 s and then centrifuged for 2 min. The organic drop deposited at the bottom of the conical flask was collected by a micro syringe to a Syncore® Analyst (BÜCHI) glass flask where solvent was dried. The reconstitution was done with 25 mL of a solution of the internal standards atrazine-d5 and diuron-d6 at 10 mg L
1, in methanol. VA-DLLME extractions were carried out in duplicate and analyzed twice.

2.7. Analytical parameters 2.5. Extraction of antifouling biocides from sediment samples The analytes were extracted from sediment samples by vortex assisted matrix solid phase dispersion (VA-MSPD), according to Batista-Andrade et al. (2018) with minor modifications. Briefly, 2 g of freeze-dried sediments and 0.25 g of octadecylsilane were homogenized with a pestle into a porcelain mortar for 5 min. The solid mixture was transferred to a glass tube (15 mL of capacity) and 5 mL of methanol was added, then the mixture was agitated by vortex for 1 min and centrifuged for 10 min (3600 rpm). The extract was collected (1 mL) and 10 mL of a mix solution of the internal standards atrazine-d5 and diuron-d6 at 1 mg mL
1 was added. All VAMSPD extractions were carried out in duplicate and analyzed twice. All concentrations in sediments were reported as mg kg
1 (dry weight).

Linearity was assessed by calculating the coefficients of determination (r2) of matrix matched analytical curves prepared by spiking blank samples at five different concentrations in triplicate. Method detection (LODs) and quantification limits (LOQs) were based on measures of the standard deviations in blank samples and their relation to the slope of the matrix matched analytical curves (Kruve et al., 2015). Matrix effects (ME) were minimized by spiking all extracts with isotopic labeled internal standards atrazine-d5 and diuron-d6 at 10 mg L
1. The extent of ME was assessed by comparing the slopes of analytical curves prepared in solvent with slopes of analytical curves prepared in post-extraction spiking assays, according to Economou et al. (2009). Recoveries (%) were obtained by spiking different known concentrations (5 levels) of the analytes and comparing the obtained signal after the analytical process with

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the initial spiking levels. 2.8. Statistical analysis Statistical analysis was carried out with the software PAST (Paleontological Statistics) version 3.21 (Hammer et al., 2001) and Microsoft Excel. Normality of data and homogeneity of variances were tested by the ShapiroeWilk test and Levene test, respectively. Comparison of biocides levels in sediments and porewaters were done by one-way analysis of variance (ANOVA) or ManneWhitney test. TukeyeKramer test was conducted for pairwise comparisons of parametric data. Kruskal-Wallis test followed by the Dunn's posthoc test was used for pairwise comparisons of non-parametric data sets, and correlations between variables were tested by Spearman test. All data were tested using a significance level of 0.05. 3. Results and discussion 3.1. Analytical parameters Both extraction methodologies based on VA-MSPD and VADLLME showed suitable sensitivity and linearity (r2 > 0.99). The linear ranges for all analytes were from LOQ to 100 mg kg
1 in sediment samples. In porewaters, the linear range was from 0.005 to 0.15 mg L
1 for irgarol, from 0.01 to 0.50 mg L
1 for DMSA and from 0.05 to 0.50 mg L
1 for diuron and DCPMU. All analytical parameters evaluated are shown in Table S2. 3.2. Sediment characterization Total organic carbon content (%TOC) from sediment samples varied between 0.2%, found in sediments collected at SP5, and 2.0%, found in sediments from SP6. Samples collected at SP4 showed the lowest fine fraction (31.5%), and the highest % of fines was found at SP10 (87.2%), as can be seen in Table S3. Overall, samples with high %TOC showed high fine fraction. In fact, Spearman correlation test confirmed that % TOC and % of fines were significantly and positively correlated (r ¼ 0.74; p ¼ 0.015). 3.3. Occurrence of antifouling biocides in sediment 3.3.1. DMSA DMSA was not detected in any of the sediment samples analyzed. This was related to the low affinity of DMSA to the sedimented phase, indicated by its low octanol-water partitioning coefficient of 1.59 (Hamwijk et al., 2005). Thus, the organic matter content of the sediment samples may have not been high enough to promote an effective binding with the substance. Additionally, DMSA has a high solubility in water (1,300 mg L
1), which allows desorption from the sediments to the overlying water. Usually, DMSA and its parent compound are less studied in sediments than other common biocides (Hamwijk et al., 2005; Schouten et al., 2005), and for the best of our knowledge, this is the first study about the presence of DMSA in sediments collected from boating areas of the Brazilian coast. 3.3.2. Diuron and DCPMU Diuron was the most detected compound in sediment samples, with a detection frequency of 76% and levels ranging from <5.0 to 55.2 mg kg
1 (Fig. 2.). Kruskal-Wallis test followed by Dunn's posthoc showed that mean levels of diuron were significantly higher (p > 0.05) in sites where fishing activities take place, which may indicate incorrect/excessive application of antifouling agents by fishermen, as well as it may be result of the semi-enclosed configuration observed in most of the fishing sites or even the

Fig. 2. Mean levels (mg kg
1 dw), with indication of one standard deviation (1s; N ¼ 4, except for SP3, which N ¼ 2), of antifouling biocides found in sediments. Brown bars: irgarol; black bars: Diuron; grey bars: DCPMU. SP4 is not represented, as none of the analytes were detected in this site.

high residence times of boats in those places. On the other hand, mean level of this biocide in waterway transport/leisure boat areas and commercial port were statistically equal (p < 0.05). The low concentrations observed in Itaqui Port may be related to the strong ~o Marcos Bay has a tidal contribution of hydrodynamics, since Sa range that can reach more than 8 m and shows macro-tidal (>4 m)
lez-Gorben ~ a et al., 2015), causing disturbs in the conditions (Gonza sediments and dilution of the substances eventually present. A high variation of diuron levels among replicates was observed in SP2 (<5.0e55.2 mg kg
1), and it was attributed to the possible presence of antifouling paint particles (APPs) in this site. APPs are generated from cleaning or scrapping of boat hulls, being discarded in the environment and subsequently transported to the aquatic compartment (Muller-Karanassos et al., 2019; Parks et al., 2010; Soroldoni et al., 2017; Tolhurst et al., 2007; Turner, 2010). Moreover, APPs are known by their slow leaching of biocides into the environment, being potential sources of local contamination by antifouling substances (Thomas et al., 2002). It was observed that repairing, scrapping and painting of artisanal boats take place at SP2. Additionally, SP2 was the only site where DCPMU was found, with a mean concentration of 2.8 mg kg
1. Diuron was also found in sediments collected in SP6, SP7, SP8 and SP9. These sampling points are located in a busy artisanal fishing harbor with a semi-enclosed configuration and limited sea water exchange. Such characteristics probably resulted in high concentrations of antifouling substances (Ansanelli et al., 2017; Gardinali et al., 2004; Lamoree et al., 2002). At SP6 and SP7, located in the busiest part of the harbor, the concentrations of diuron were significantly higher (p < 0.05) than concentrations detected at SP8 and SP9, where a small number of boats was observed during the sampling period. A similar finding was related by Martínez and
(2001) in sediment samples from a marina in Catalonia. Barcelo Overall, sediments from fishing sites showed relatively high total organic carbon content (0.8e2.0%), which may promote adsorption of hydrophobic contaminants. However, mean levels of diuron in sediments were not statistically correlated to both % TOC (r ¼ 0.58; p ¼ 0.076) and % of fines (r ¼ 0.48; p ¼ 0.16). In areas with direct influence of tidal and with high water exchange rate, as SP3, SP5 and SP10, the levels of diuron were up to 6.4 mg kg
1. The levels of diuron found in this work were similar to the reported by Saleh et al. (2016) in sediments from Persic Gulf (13.6e29.1 mg kg
1), however, the authors related a low detection frequency. The same was shown by Gatidou et al. (2007) in Shoreham Harbor, where concentrations between 59.7 and 66.4 mg kg
1 were detected. Lam et al. (2017) reported a wide distribution of diuron, with the highest levels found in small shipyards

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from Korea. The predominance of diuron in fishing harbors was shown by S
anchez-Rodríguez et al. (2011) in sediment samples from Gran Canaria Island. Low levels (0.4e6.2 mg kg
1), but widely distributed were found by Thomas et al. (2002) in samples collected in the UK. Besides diuron, DCPMU was also determined in that study, however, it was only found in water samples from high contaminated areas. 3.3.3. Irgarol The highest mean concentration of irgarol was found in samples from SP5 (45.6 mg kg
1), however, we also attribute this fact to the possible presence of APPs, since the range for replicate samples was from 2.4 to 89.7 mg kg
1. Moreover, the sediment was poor in both organic carbon content (0.2%) and fine fraction (35.5%), being unlikely to promote binding of nonpolar substances. The mean levels of irgarol in sediments from SP6, SP7 and SP8 ranged between <1.0 and 14.1 mg kg
1, and it was not found in samples from both SP10 (Itaqui Port), SP3 and SP9. The results showed that the commercial port did not represent the main source of antifouling biocides in sediments. However, it is important to emphasize that Itaqui Port suffers high tidal influence and its open configuration favors the resuspension of the sediments and the consequent dilution of the substances present in this matrix. The only report about biocide contamination in this port was presented by Diniz et al. (2014) for water samples, where extremely high levels of irgarol were detected. Due to both high density and residence time of leisure boats and relative enclosed configuration, high levels of antifouling biocides were expected in sediments from SP4. However, it was the only site where none of the substances analyzed were found. Spearman correlation test has shown that the mean concentrations of irgarol were not significantly related to both % TOC (r ¼ 0.041; p ¼ 0.91) and % of fines (r ¼ 0.081; p ¼ 0.82) of the sediment samples. The correlation between the concentrations of irgarol and diuron were also evaluated, but no statistically significant correlation was observed (r ¼ 0.15; p ¼ 0.68). Irgarol did not show a clear distribution pattern in the evaluated areas, since there was no significant difference between its mean levels in fishing and waterway transport areas (Mann-Whitney, U ¼ 96; p ¼ 0.10). The concentrations of irgarol found in this work are higher than the levels related by Thomas et al. (2002) in sediments from the UK (0.4e3.5 mg kg
1) and by Tsang et al. (2009) in Kwun Tong (21.3 mg kg
1). As seen in this work, other authors related low levels of irgarol even in high busy shipping zones, as the findings of Batista-Andrade et al. (2018) in the Panama Canal, where the levels of irgarol ranged between < 0.08 and 2.8 mg kg
1. 3.4. Occurrence of antifouling biocides in porewaters As shown in Fig. 3, the pattern of contamination in porewaters, indicated by relative distribution, was very different to the observed for sediment samples. In the left side of Fig. 3, the predominance of diuron is very clear, whereas DCPMU and DMSA are in evidence in the right side. These changes were attributed to different properties of both sediments and analytes and are discussed in the following sections. 3.4.1. DMSA Despite not being detected in any of the sediment samples, DMSA was found in most of the analyzed porewaters (Fig. 4.), with a detection frequency of 66%. Its highest concentrations were found in the samples from SP6 and SP8 (0.24 and 0.14 mg L
1, respectively), where fishing activities take place. In samples from SP1, SP2 and SP4 mean levels were similar, ranging between 0.040 and

Fig. 3. Relative distribution of irgarol, diuron, DCPMU and DMSA in sediments (left) ~o Luís Island, Brazil. Brown bars: irgarol; black bars: and porewaters (right) taken in Sa Diuron; Grey bars: DCPMU; striped bars: DMSA.

0.058 mg L
1. At SP10, DMSA was detected in only one of the replicates, with a concentration of 0.011 mg L
1. Kruskal-Wallis test followed by to Dunn's post-hoc have shown that concentrations of DMSA in fishing areas were statistically higher (p ¼ 0.017) than other sites studied in this work. This finding means that occurrence ~o Luís may be mainly of dichlofluanid in the coastal areas of Sa associated with its use on small boat hulls. In areas where passenger transport activities and at Itaqui Port, mean concentrations were considered statistically equal (p ¼ 0.197). The presence of DMSA in porewaters and its absence in sediment samples is an indication of its preference to the aqueous phase instead the sedimented phase, as aforementioned, due both its low log Kow and high water solubility (Hamwijk et al., 2005). 3.4.2. Diuron and DCPMU The detection frequency of diuron in porewaters was 26%. Its absence in most of the porewaters from highly contaminated sediments may be related to non-recent inputs of this contaminant into the aquatic environment, since the tendency of sorbed organic pollutants to become more strongly bound with increasing of the interaction time is demonstrated for selected pesticides (Chefetz et al., 2004). The octanol/water partitioning coefficient (logKow) of diuron is 2.6 (Giacomazzi and Cochet, 2004), being an indicative of its low availability to porewaters, since diuron is likely to be bonded to the organic matter present in the sediments, which is an essential factor controlling the fate, availability and distribution of organic contaminants into the aquatic environment (Artifon et al., 2019). Moreover, according to Chefetz et al. (2004) it is common that hydrophobic organic compounds, including pesticides, show desorption strongly impaired or even impeded when comparing to their sorption rate in sediments. The levels of diuron detected in porewaters ranged from <0.047 mg L
1 to 0.47 mg L
1, with the highest level (p < 0.05) observed at SP2. The high levels of diuron at SP2 in both matrices strongly support the assumption of the presence of APPs in this sample, as explained before. In this case, APPs may represent a potential source of contamination also to the interstitial environment, since the fraction of contaminants present in this matrix is bioavailable to the biota (Persson et al., 2005; Xu et al., 2014). The mean concentrations of diuron at SP5 (0.075 mg L
1) and SP9 (0.064 mg L
1) were statistically the same (p ¼ 0.949) despite very

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Fig. 4. Mean levels (mg L
1), with indication of one standard deviation (1s; N ¼ 4, except for SP7, which N ¼ 2), of antifouling biocides found in porewaters collected in S~ao Luís Island, Brazil. Brown bars: irgarol; black bars: Diuron; grey bars: DCPMU.

different properties between sediments of these sampling sites. The presence of diuron in porewaters from SP5 may have been favored by its weak binding to the sedimented phase, since low organic matter content was present. In contrast, sediments collected at SP9 showed high % TOC (1.4%) and also % of fines (silt þ clay) (66.2%), allowing more effective binding to the sedimented phase, which justified the low concentrations in porewaters, since the levels of diuron available in the sediments were high. The presence of diuron is not usually studied in porewaters. So, there is little information about its availability in this matrix. Among the rare works within this theme, we highlight that developed by Magnusson et al. (2013) who have analyzed a series of herbicides in porewaters of Australian rivers. The authors reported diuron concentrations in the range from 0.0045 to 0.068 mg L
1, and as observed in this work, higher detection frequency was found in sediment samples than porewaters. DCPMU was the most detected substance in porewater samples, with a detection frequency of 71%, and levels ranging from 0.065 to 0.670 mg L
1. Although its only detection in sediments from SP2, DCPMU was not found in porewaters collected at this sampling site. The highest mean concentration of DCPMU was detected in porewaters from SP9 (0.64 mg L
1), which is 10-fold the concentration of its parental compound in this same site. In porewaters from SP5, the predominance of DCPMU in relation to its parental compound was also observed. Its mean levels were similar to each other in porewaters from SP1, SP3 and SP10 (0.28, 0.35 and 0.23 mg L
1, respectively), and at SP6, SP7 and SP8, the concentrations of DCPMU were the lowest observed (0.16, 0.090 and 0.12 mg L
1, respectively). The concentrations of DCPMU in the porewaters analyzed were always higher than those of its parent compound and, in most of the sampling sites, diuron was not even detected. These findings may lead to two hypotheses: 1) degradation of diuron to DCPMU is more likely to occur in porewaters than in sediments; 2) the persistence of DCPMU is higher in porewater than in sediments, favoring its high concentrations in the liquid phase. Quite similar results were showed by Panshin et al. (2000) for degradation products of atrazine, which were found to be more persistent in porewater than their parent compound. There are no reports in the literature about the occurrence of DCPMU in porewater samples, so comparisons and more precise deductions about the persistence of this substance in this matrix cannot be made. Therefore, the importance of this study as one of the initial points for clarification on the degradation and transport processes of diuron in the interstitial environment and its implications for the other aquatic compartments is emphasized.

3.4.3. Irgarol Irgarol was detected in 50% of the porewater samples analyzed, with concentrations ranging between <0.0030 and 0.083 mg L
1. The highest mean concentration of irgarol was observed at SP7 (0.051 mg L
1), where the lowest mean concentration in sediment was detected. At SP3, SP4 and SP10, irgarol was only detected in porewater, but not in sediments. In the samples SP2, SP6 and SP8 irgarol was only detected in sediments, which was related to the % TOC of these samples (<1%). Thus, irgarol may have been strongly bonded to the organic matter of the sediments and less available to porewaters. Indeed, irgarol has a log Kow of 3.78, making it difficult to be transported to the aqueous phase. In samples from SP1, SP5 and SP7 irgarol was found in both matrices. Meanwhile, relative levels observed in porewaters were much lower than those detected in sediments, as shown in Fig. 3. Although irgarol reports in porewaters were not found during the literature review for this work, other triazines have already been detected in this matrix, such as atrazine and simazine, which were quantified by Magnusson et al. (2013) in porewaters from sediments collected in Australian rivers. The maximum concentration was 0.0502 mg L
1 and 0.0056 mg L
1, respectively. Much higher levels of atrazine (2.61e8.44 mg L
1) were reported by Panshin et al. (2000) in porewaters collected in Indiana (USA). 3.5. Partitioning of antifouling biocides into the aquatic environment The partitioning behavior of the biocides into the aquatic environment was assessed in terms of distribution coefficient (Kd) and organic carbon/water partition (Koc). The Kd is the ratio of solute concentration in the solid phase and in the aqueous phase in equilibrium, and was normalized to the organic carbon fraction of the matrix (foc) to obtain Koc (Artifon et al., 2019). Determining irgarol Kd values was only possible for samples collected at SP1, SP5 Table 1 Distribution coefficient (Kd), organic carbon/water partition (log Koc) and its mean values (one standard deviation) calculated for irgarol and diuron. Sampling site

SP1 SP2 SP5 SP7 SP9 Mean value

Irgarol

Diuron

Kd (L kg
1)

logKoc

Kd (L kg
1)

LogKoc

6,473.3 e 2,680.0 15.3 e 3,053.0 (3,245.4)

5.6 e 6.1 3.1 e 4.9 (1.6)

e 67.9 45.7 e 163.4 92.3 (62.3)

e 3.7 4.3 e 4.3 4.1 (0.3)

J.L.M. Viana et al. / Environmental Pollution 255 (2019) 112988

and SP7, where this biocide was detected in both matrices (Table 1). The Kd values for diuron were obtained for samples from SP2, SP5 and SP9. A high Kd value and the highest log Koc for irgarol was determined in SP5, however, it may be considered the possible presence of APPs in this sample, which is a source of bias. Overall, it was observed that the interstitial environment accounted for a very limited part of the concentration of irgarol when comparing to sediment. There is no data on the presence or distribution of irgarol in porewaters, so more accurate comparisons of the contaminant in this matrix are not feasible. In general, both Kd and log Koc for diuron were lower than the determined for irgarol, which may be due its affinity to the aqueous phase indicated by its lower log Kow value. It was not possible to calculate the distribution coefficients for DCPMU and DMSA, as those substances were not detected simultaneously in both matrices in any of the sampling points.

3.6. Risks posed by environmental concentrations of antifouling biocides In Brazil, there is no legislation regarding the use of the studied biocides in antifouling formulations. Thus, the concentrations of the detected antifouling substances in sediments and porewaters ~o Luís were compared with international guidelines sampled in Sa in order to get an estimation of the actual risk of contamination to aquatic species. Parameters such as international environmental quality guidelines (EQGs), environmental risk limits (ERLs) and concentration levels for which toxic effects have been reported in previous studies were selected. The mean levels of irgarol found in porewater samples from SP3, SP5, SP7 and SP10 were higher than the minimum concentration (0.01 mg L
1) in which genotoxic effect was observed for embryos of Crassostrea gigas (Mai et al., 2012). The root growth of Apium nodifloru and PSII quantum efficiency of Chara vulgaris (EC50 0.013 mg L
1 and 0.017 mg L
1, respectively) are also likely to be affected by environmental levels found in those sites (Lambert et al., 2006). Additionally, the maximum irgarol concentration detected in porewaters (0.083 mg L
1) was near to the EC50 calculated for growth rate and quantum yield of Tetraselmis sp. (0.116 mg L
1) and Fibrocapsa japonica (0.110 mg L
1), respectively (Buma et al., 2009). The mean concentrations (normalized to 1% TOC) of irgarol in sediments from SP1, SP5 and SP8 may be classified as “very bad”, whereas SP2, SP6 and SP7 may be classified as “bad”, according to the Norwegian classification system for metals and organic contaminants in seawater and sediments (Bakke et al., 2010). Levels of irgarol (normalized to 10% organic matter) above Dutch Environmental Risk Limit (ERL) (1.4 mg kg
1) (Van Wezel and Van Vlaardingen, 2004) were observed in all samples in which this substance was detected. All porewater samples contaminated by diuron showed levels higher than the EC50 (0.00026 mg L
1) calculated by Lambert et al. (2006) for the root growth of Apium nodifloru. Moreover, mean concentrations of diuron were higher than the lowest concentration that significantly affected embryo-larval development of oysters (0.050 mg L
1) (Akcha et al., 2012). All sediment samples in which diuron was detected were classified as “bad” or “very bad”, except SP8 and SP10, which were considered “moderate”, according to Norwegian classification system for metals and organic contaminants in sediments(normalized to 1% TOC) (Bakke et al., 2010). The levels of DCPMU detected in this work are similar and even higher than the concentrations in which decrease testicular steroidogenesis and quantity of spermatids and spermatozoa in

7

Oreochromis niloticus (0.20 mg L
1), when associated with other diuron degradation products (Pereira et al., 2015). The mean levels detected in all sampling sites, except SP7, are higher than the concentration found to induce hormonal imbalance and to promote behavioral changes in O. niloticus, when associated to other degradation products of diuron (0.10 mg L
1) (Boscolo et al., 2018). Although, levels of DCPMU and diuron found in porewaters from ~o Luís are lower than the reported by Gatidou and Thomaidis Sa (2007) for 96 h EC50 (345 mg L
1 and 5.9 mg L
1, respectively) on Dunaliella tertiolecta. The degradation product showed higher toxicity than its parental against Daphnia magna. However, the 48 h-EC50 is about 60-fold greater than the maximum DCPMU con~o Luís (Ferna
ndez-Alba centration found in porewaters from Sa et al., 2002). The higher toxicity of DCPMU in relation to diuron was also related by Tixier et al. (2000), who used Vibrio fischeri as a test organism. Studies about the toxicity of DMSA are extremely scarce. However, some authors relate that its parental compound, dichlofluanid, has a lower toxicity in comparison to other common antifouling agents. Despite this, DMSA has been found to be moderately toxic to invertebrates (Amara et al., 2018). Considering the toxicity of dichlofluanid, the results found in porewaters are much lower than the toxic levels frequently reported. For example, 96 h-EC50 for the growth of Nitzschia pungens calculated by Jung et al. (2017) was 377 mg L
1 and the LC50 for Artemia larvae was 154,944 mg L
1. 4. Conclusion Antifouling booster biocides were widely distributed along ~o Luís. Diuron and irgarol were manly found in coastal areas from Sa sediment samples, whereas DCPMU and DMSA showed more affinity to the aqueous phase. The highest levels of both irgarol and diuron in sediments were likely to be result of discarded antifouling paint particles generated by scrapping of boat hulls, and contamination patterns observed indicated that contamination by diuron in sediments is intrinsically related to fishing activities, whereas irgarol showed more homogeneous distribution along the sampled sites. The levels of diuron, irgarol and DCPMU detected in this work were as high as the levels commonly found to induce deleterious effects on non-target organisms and are higher to some international environmental quality guidelines. This work represents the first study about the occurrence of antifouling biocides in both sediments and porewater samples in S~ ao Luís Island and is one of the few works dealing with organic contaminants into the interstitial environment. Thus, more studies are needed in order to better understand the mobility of antifouling biocides, and the different patterns of degradation of these substances in porewaters. We emphasize the importance of this study as one of the initial data sources on this type of contamination in Amazonian and preAmazonian regions, since concern about this topic is very recent in those areas, and legislation regarding this theme is not available in Brazil. Authors contributions and order
Lucas Martins Viana e Investigation, Formal First author: Jose analysis, Validation, Writing-original draft; Second author: Sara Raiane Viana dos Santos e Investigation, Validation and Formal analysis; Third author: Teresa Cristina Rodrigues dos Santos Franco e Conceptualization, Project administration, Supervision, Validation, Writing-review and editing;
lio Pinheiro Almeida e Supervision, Fourth author: M
arcio Aure

8

J.L.M. Viana et al. / Environmental Pollution 255 (2019) 112988

Writing-review and editing. Declarations of interest None. Acknowledgements ~o de AperfeiThis work was supported by CAPES (Coordenaça çoamento de Pessoal de Nível Superior) (Process 23038004307/
Lucas Martins Viana and Sara Raiane Viana dos 2014-61). Jose ~o de Santos received financial support from FAPEMA (Fundaça
gico Amparo  a Pesquisa e ao Desenvolvimento Científico e Tecnolo ~o) (BM-02411/17 and BIC-05954/18, respectively). The do Maranha
rio de Microcontaminantes authors also thank the Laborato
tica (CONECO e FURG) for the Org^ anicos e Ecotoxicologia Aqua granulometric and total organic carbon analyzes, and EMAP (Itaqui Port Authority) for the support given during sampling in Itaqui Port and Ponta da Espera Terminal. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.envpol.2019.112988. References Akcha, F., Spagnol, C., Rouxel, J., 2012. Genotoxicity of diuron and glyphosate in oyster spermatozoa and embryos. Aquat. Toxicol. 106e107, 104e113. https://doi. org/10.1016/j.aquatox.2011.10.018. Ali, H.R., Ariffin, M.M., Sheikh, M.A., Mohamed Shazili, N.A., Bachok, Z., 2015. Toxicological studies of Irgarol-1051 and its effects on fatty acid composition of Asian sea-bass. Lates calcarifer. Reg. Stud. Mar. Sci. 2, 171e176. https://doi.org/ 10.1016/j.rsma.2015.09.008. Almeida, E., Diamantino, T.C., Sousa, O. de, 2007. Marine paints: the particular case of antifouling paints. Prog. Org. Coat. 59, 2e20. https://doi.org/10.1016/j. porgcoat.2007.01.017. Amara, I., Miled, W., Slama, R. Ben, Ladhari, N., 2018. Antifouling processes and toxicity effects of antifouling paints on marine environment. A review. Environ. Toxicol. Pharmacol. 57, 115e130. https://doi.org/10.1016/j.etap.2017.12.001. Ansanelli, G., Manzo, S., Parrella, L., Massanisso, P., Chiavarini, S., Di Landa, G., Ubaldi, C., Cannarsa, S., Cremisini, C., 2017. Antifouling biocides (Irgarol, Diuron and dichlofluanid) along the Italian Tyrrhenian coast: temporal, seasonal and spatial threats. Reg. Stud. Mar. Sci. 16, 254e266. https://doi.org/10.1016/j.rsma. 2017.09.011. Artifon, V., Castro,
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