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Spatial variability in the concentrations of metals in beached microplastics
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Spatial variability in the concentrations of metals in beached microplastics M.C. Vedolina,⁎, C.Y.S. Teophiloa, A. Turrab, R.C.L. Figueiraa a b
Laboratório de Química Inorgânica Marinha, Departamento de Oceanografia Química, Instituto Oceanográfico, USP, São Paulo, SP, Brazil Laboratório de Manejo, Ecologia e Conservação Marinha, Departamento de Oceanografia Biológica, Instituto Oceanográfico, USP, São Paulo, SP, Brazil
A R T I C L E I N F O
A B S T R A C T
Keywords: Pellets Microplastics Metals Inorganic pollutants Pollution São Paulo coast
Heavy metals and microplastics have been considered as threats to the marine environment and the interactions between these two pollutants are poorly understood. This study investigates the interactions between metals adsorbed in pellets collected randomly from 19 beaches along the coast of São Paulo State in southeastern Brazil, comparing these levels with those in virgin pellets. The samples were analyzed for Al, Cr, Cu, Fe, Mn, Sn, Ti and Zn by inductively coupled plasma optical emission spectroscopy (ICP-OES). The polymers were solubilized via acid digestion. The highest levels occurred with Fe (227.78 mg kg− 1 - Itaguaré) and Al (45.27 mg kg− 1 Guaraú) in the same areas, which are closer to the Port of Santos. The metal adsorption on pellets collected is greater than that on virgin pellets. In this context, pellets can be considered to be a carrier for the transport of metals in the environment, even in small quantities.
1. Introduction Since the development of the first synthetic polymer, “Bakelite”, in 1909, a number of low cost techniques have been developed to produce a plastic product that is durable, inert and resistant (Plastics Europe, 2011). However, the properties that make plastics so useful (e.g., low density, durability) have created a problem related to the management of waste due to improper discarding (Barnes et al., 2009; Hopewell et al., 2009), especially in the oceans. Microplastics are commonly defined as any plastic particles measuring < 5 mm in diameter, but they can also be classified as “primary microplastics”, which include production pellets and microbeads, or “secondary microplastics”, which come from larger plastic items that have degraded and consequently fragmented (Andrady, 2011; GESAMP, 2016). Plastic pellets are composed of polymers, usually polyethylene, polystyrene or polypropylene; these pellets are from 2 to 5 mm in diameter and are used as raw materials in the production of plastic items (Ogata et al., 2009). They can be found in a range of aquatic environments, which suggests that they can be lost during loading and transportation, both on land and at sea, and during their handling at plastic transformation factories and harbors (Carpenter et al., 1972; Gregory, 1977, 1978; Ryan, 1988; EPA, 1992; Mato et al., 2001; Moore et al., 2001a; Reddy et al., 2006; Costa et al., 2009; Ogata et al., 2009). In addition to their visual impacts, microplastics in the marine environment are a threat to animals by accumulation, entrapment,
entanglement, suffocation and fouling (Thompson et al., 2004; Colabuono et al., 2009; Gregory, 2009; Majer et al., 2012; GESAMP, 2016). In the marine environment, these particles are able to sequester contaminants from sea water, contaminants such as polychlorinated biphenyl (PCB), dichlorodiphenyltrichloroethane (DDT), polycyclic aromatic hydrocarbons (PAHs) and metals (Mato et al., 2001; Endo et al., 2005; Ogata et al., 2009; Ashton et al., 2010; Holmes et al., 2012, 2014; Brennecke et al., 2016). Thus, they can act as a source of these contaminants to organisms via ingestion, since they may be mistaken for food items (Teuten et al., 2009) or accidentally ingested by filterfeeders (Santana et al., 2016a). Most of these pollutants are toxic and bioaccumulative, and if leached from pellets and assimilated by an organism, can be introduced into the food chain (Browne et al., 2013). Until recently, interactions between metals and plastic pellets had not been considered, because polymers are considered to be relatively inert toward aqueous metal ions (Plastics Europe, 2011). However, recent studies recorded the presence of adsorbed metals in plastics due to surface alterations in the marine environment (Ashton et al., 2010; Holmes et al., 2012, 2014). Fotopoulou and Karapanagioti (2012) described the surface of beached pellets as rough and with pronounced cavities compared to virgin pellets. These alterations increase the surface area and generate anionic active sites such as carbonyls for the adsorption of metals from seawater (Holmes et al., 2012, 2014), which might explain why there are lower concentrations of trace metals in newly released (virgin) pellets than in beached pellets. The sources of metals to the oceans are diverse, though many arise
⁎ Corresponding author at: Departamento de Oceanografia Química, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, Cidade Universitária, São Paulo, SP 05508-120, Brazil. E-mail address: [email protected] (M.C. Vedolin).
http://dx.doi.org/10.1016/j.marpolbul.2017.10.019 Received 11 April 2017; Received in revised form 5 October 2017; Accepted 7 October 2017 0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Vedolin, M.C., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2017.10.019
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along the São Paulo coast during 2012 (Fig. 1). Approximately 300 pellets were collected by hand from each site and stored in polyethylene bags. Each sample was washed with sea-water and dried under ambient conditions. In the laboratory, pellets from each site were pooled in 3 replicates with 100 pellets for subsequent analyses.
from the irresponsible dumping of sewage, of industrial and household waste and many other sources, such as release from surfaces covered by antifouling coatings, or urban drainage, atmospheric deposition, disposal of mining residues, among others. Some metals found on plastic debris derive from the manufacturing process (additives), but several metals have been found to occur on plastic debris as a result of environmental sorption (Holmes et al., 2012, 2014; Rochman et al., 2014). Nobre et al. (2015) showed that beached pellets have lower toxicity than virgin pellets, although their toxicity may vary as a function of the different additives, like organic compounds, used in their production. The environmental risks posed by microplastics are defined as a combination of their presence (number; e.g., Turra et al., 2014) and potential effects on the environment (e.g., concentration of contaminants such as PCBs and PAHs) (GESAMP, 2016). Recent studies have shown the spatial variability of the contamination in beached pellets by organic pollutants on various spatial scales ranging from meters to global (Ogata et al., 2009; Karapanagioti and Klontza, 2008; Karapanagioti et al., 2010; Frias et al., 2010; Hirai et al., 2011; Heskett et al., 2012; Fisner et al., 2013a, 2013b; Taniguchi et al., 2016), but no information is available about the concentrations of metals specific to the Brazil area. The main objective was to determine the concentrations of metals in pellets from 19 beaches along the coast of the São Paulo state, assess their variability and also compare them to those levels found in virgin pellets.
2.2. Sample digestion The samples of beached pellets were subjected to partial acid digestion following the method US EPA 3050B (USEPA, 1996). The three 100 pools of pellets (~ 2 g each) were taken in a 50 mL beaker and then 10 mL of HNO3 (1:1), 5 mL of pure HNO3, 3.0 mL of H2O2 (30% V/V), and 10 mL of HCl were added at 90 °C. Subsequently, these digests were filtered and diluted to 40 mL with Millipore Milli-Q water. The samples were analyzed for Al, Cr, Cu, Fe, Mn, Sn, Ti and Zn by inductively coupled plasma optical emission spectroscopy (ICP-OES; Varian, model 710ES). Pellets were analyzed as sediment samples, i.e., we assumed that they have some capacity to adsorb and desorb (leach) metals and other chemical compounds on/from their surfaces; thus, they were considered as a potential source of contamination for the marine environment. In this way, one certified reference material for sediment (SS-1) from EnvironMAT™ SPC Science were subjected to the same analytical procedure in order to evaluate the precision and accuracy of the method. Additionally, four types (polypropylene, high density polyethylene and two grades/colors of polyethylene, black and blue) of virgin resin pellets were obtained from a local plastic processing facility (Braskem SA, São Paulo) and analyzed accordingly for comparison with the data collected from the beached pellets.
2. Materials and methods 2.1. Sampling This investigation was developed on the coast of São Paulo State in southeastern Brazil (23°21′54.20″S/44°44′21.94″O and 25°18′30.81″S/ 48° 5′37.25″O). São Paulo has a coastline of approximately 620 km, which is highly urbanized, especially in the central coast region known as “Baixada Santista”. This region is heavily impacted by the Port of Santos (the largest port in Latin American) and the Industrial Complex of Cubatão (Harari and Gordon, 2001; Silva et al., 2011). As a result of the anthropogenic activities in this area, many pollutants, such as PCBs and PAHs, have been found in sediment samples (Bícego et al., 2006). The transport of plastic pellets through Santos Harbor is responsible for 50,000 tons of granules/month (Fisner et al., 2013a, 2013b), and a large quantity of pellets has been reported on nearby beaches (Turra et al., 2014; Moreira et al., 2016). Pellets were collected randomly from nineteen coastal beaches
2.3. Data analysis Differences in the levels of metals between each site were evaluated using a non- parametric Kruskal-Wallis test followed by the post hoc Dunn's test. The elements Cr and Sn, which usually exhibited values below the detection limit of the method were excluded from analyses. Differences between virgin pellets samples were also evaluated using ANOVA (one-way) followed by the post hoc Tukey test. To visualize the similarities among and between samples (beached and virgins), a non-Metric Multidimensional Scaling (nMDS) was applied to the similarity matrix (Bray Curtis similarity) and permutational multivariate analyses of variance (PERMANOVA). The trace statistic for the null hypothesis of no group differences was calculated with 999 permutations. Fig. 1. Beaches (municipalities) where pellets were sampled along the São Paulo state coast in 2012. Note: 1Cardoso Island (Cananeia); 2- Boqueirão do Sul (Ilha Comprida); 3- Arpoador (Peruíbe); 4- Guaraú (Peruíbe); 5Ruínas (Peruíbe); 6- Sonho (Itanhaém); 7- Vila São Paulo (SP) (Mongaguá); 8- Guilhermina (Praia Grande); 9Gonzaga (Santos); 10- Enseada (Guarujá); 11- Itaguaré (Bertioga); 12- Boraceia (São Sebastião); 13- Santiago (São Sebastião); 14- Massaguaçu (Caraguatatuba); 15- Tabatinga (Caraguatatuba); 16- Sete Fontes (Ubatuba); 17- Anchieta Island (Ubatuba); 18- Grande (Ubatuba); and 19- Fazenda (Ubatuba).
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Table 1 Metals levels (mg kg− 1; mean ± standard deviation; n = 3; MQL: method quantitation limit) in samples (2 g; ~ 100 particles) of different resin types (PE: polyethylene; HDPE: high density polyethylene; PP: polypropylene) available after acid digestion. Values followed by the same letter in the column do not differ by Tukey test, p < 0.05. Resins
Elements (mg kg− 1) Al
1. 2. 3. 4.
PE - Black PE - Blue HDPE PP
Cr a
4.7 ± 0.1 7.4 ± 0.3b 16.0 ± 1.8c 5.7 ± 0.4a
0.370 0.430 0.330 0.490
Cu ± ± ± ±
a
0.010 0.008b 0.004d 0.020a
Fe
< MQL < MQL < MQL < MQL
2.30 3.30 4.10 7.60
Mn ± ± ± ±
a
0.03 0.40a 1.50a 1.20b
Sn
< MQL < MQL < MQL < MQL
Ti
Zn
< MQL < MQL < MQL < MQL
1.35 ± 0.07a 2.40 ± 0.30b < MQL < MQL
a
3.6 ± 0.1 4.6 ± 0.7b < MQL < MQL
Note: MQL values for Al 0.65 mg kg− 1, Cr 0.20 mg kg− 1, Cu 0.14 mg kg− 1, Fe 0.48 mg kg− 1, Mn 2.72 mg kg− 1, Sn 1.12 mg kg− 1, Ti 1.53 mg kg− 1, Zn 0.87 mg kg− 1.
and plasticizers, which may contain metallic elements such as Cd, Mn, Pb, Sn and Zn (Michaeli, 1995; Rodriguez, 1996). From this list, only Zn was detected in this study, and in low concentration; moreover, might be originated from the production process and there is not a strong evidence indicating the toxicity about virgin pellets.
The Statistica 12.0 and Primer 7 software packages were employed for data treatment and analysis. Data were transformed prior to all analysis log(x + 1), when necessary.
3. Results and discussion 3.1. Virgin pellets analysis
3.2. Metals levels in beached pellets
Digestion analysis in polymers is applied mainly for the determination of the metal levels in plastics that will be used in the food industry (Nomura et al., 2001; Zenebon et al., 2004; Takahashi et al., 2008a, 2008b). In addition, there are other studies that describe a similar method for plastic pellets (Ashton et al., 2010; Holmes et al., 2012, 2014). Table 1 summarizes the concentration of pre-existing trace metals on virgin pellets and the Tukey's test result. The levels of metals do not exhibit obvious variations in this sample but the differences between types of pellets were confirmed in the ANOVA results (p < 0.05) significant differences were observed between the types of pellets for Al Cr, Fe, Sn and Zn. According Rochman et al. (2014), in general, all types of plastic tended to accumulate similar concentrations of metals; however the results on virgins samples in this study show that this can vary. For certain metals, such as Al and Fe, the concentrations in the plastic pellets can be explained by contamination during manufacturing via abrasion caused by friction in the equipment (Hoffman et al., 1991). Since plastics have become widely used, plastic production has grown and created a demand for different kinds of plastics with various combinations of properties (EPA, 1990). The additives provide some features that give such properties to plastics. The most important additives are antioxidants, polymer stabilizers, flame retardants, pigments
Metals levels that were detectable in partial acid digests of the beached pellets showed variability among the three replicates and reflected the heterogeneity of the accumulation process(es) (Table 2). These values are similar to the result described by Ashton et al. (2010) and Holmes et al. (2012) who also measured the metal accumulation in plastic pellets. The order of metal accumulation (Fe > Al > Mn > Cu = Zn) is similar in these studies too, and the mean concentrations are within an order of magnitude of the corresponding concentrations in pellets sampled from different places. There were differences in metals levels between some locations for the majority of the elements (Kruskall Wallis p < 0.05). However, there was no significant difference between beaches for elements Al and Zn (Kruskall Wallis - ANOVA p > 0.05). Fig. 2 shows the median levels of metals (n = 3) for each sampling site and compared these results with other studies. For all metals, concentration accumulated on pellets varied significantly between locations, which is similar to what is observed for organic pollutants (Fisner et al., 2013a, 2013b; Taniguchi et al., 2016), see Fig. 2. Statistical differences between places were shown (Dunn's teste p < 0.05) for Cu, Fe, Mn and Ti in Appendix A. Table 2 shows that some beaches at North and South exhibited pellets with high concentrations of some elements - Al (45 mg kg− 1 Guaraú) and Zn (8 mg kg− 1 Massaguaçu), for example. Besides some elements more related with the earth's crust and presence in marine
Table 2 Metals levels (mg kg− 1; mean ± standard deviation; n = 3) in pellet sampled from 19 beaches along São Paulo coast in 2012. Beaches
Al
Cu
Fe
Mn
Ti
Cardoso Island Boqueirão do Sul Arpoador Guaraú Ruínas Sonho Vila SP Guilhermina Gonzaga Enseada Itaguaré Boraceia Santiago Massaguaçu Tabatinga Sete Fontes Anchieta Island Grande Fazenda
7 ± 9 18 ± 17 14 ± 0.3 45 ± 9 23 ± 10 22 ± 5 24 ± 3 25 ± 3 30 ± 27 28 ± 5 33 ± 10 23 ± 6 27 ± 11 13 ± 14 41 ± 19 30 ± 21 26 ± 23 29 ± 14 44 ± 3
1 ± 1 0.3 ± 0.1 0.3 ± 0.1 0.5 ± 1 0.4 ± 0.4 0.5 ± 0.5 1 ± 1 0.2 ± 0 1 ± 1 1 ± 0 0.5 ± 0 1 ± 1 0.1 ± 0.1 1 ± 0 0.2 ± 0.2 1 ± 1 0.3 ± 0.2 0.2 ± 0.2 0.2 ± 0.2
58 ± 17 55 ± 24 90 ± 22 150 ± 15 95 ± 19 55 ± 49 114 ± 63 119 ± 27 99 ± 86 86 ± 22 228 ± 142 65 ± 13 67 ± 11 122 ± 55 56 ± 7 58 ± 13 36 ± 35 56 ± 18 114 ± 8
9 ± 5 2 ± 1 2 ± 0.3 3 ± 1 2 ± 1 2 ± 0.3 3 ± 1 3 ± 0.3 3 ± 3 9 ± 6 4 ± 2 2 ± 1 0.5 ± 1 1 ± 01 0.3 ± 0.3 0.5 ± 0.3 < 0.01 ± 0 3 ± 1 3 ± 1
2 2 2 3 2 2 2 2 2 2 2 1 1 1 2 1 1 2 2
3
Zn ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0 1 1 0.4 1 1 1 0 2 0.3 0.3 0.2 0 0.3 0.3 0.5 1 2 0.5
1 ± 1 1 ± 1 1 ± 1 1 ± 1 0.3 ± 0.3 0.4 ± 0.3 1 ± 1 0.4 ± 0.4 1 ± 0 1 ± 1 3 ± 1 1 ± 1 3 ± 0.3 8 ± 9 3 ± 2 2 ± 2 2 ± 2 1 ± 0 5 ± 5
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Fig. 2. Metals levels (mg kg − 1; median; n = 3) in pellet sampled from 19 beaches along São Paulo coast in 2012 and 4 different resin types (PE: polyethylene; HDPE: high density polyethylene; PP: polypropylene) available after acid digestion. Significant difference among elements (p < 0.05) is indicated by *. Comparison of level metal in pellets sample with other studies using mean results (Ashton et al., 2010 and Holmes et al., 2012).
Paulo Southeastern Coast) can reach 15.877 mg kg− 1 for Al and 18.893 for Fe mg kg− 1 (Kim et al., 2015), the highest levels observed in this study - versus the concentrations of adsorbed heavy metals in the plastic pellets, the role of these particles cannot be considered alarming vectors for marine organisms. This study do not corroborates those of Claessens et al. (2011) and Holmes et al. (2012), who have obtained results in that the concentration of metals increases with proximity to anthropogenic sources, especially in port regions. Moreover, in contrast to what is observed for organic pollutants, PAHs (Fisner et al., 2013a, 2013b) and PCBs (Taniguchi et al., 2016) in the same area, the lowest levels were found
sediment (Al and Fe) were highly variable and may be indicating the proximity with estuaries. Holmes et al. (2014) were the first to examine the interactions of metals with plastics in estuaries and suggested that changes in some conditions like salinity and pH may affect adsorption of metals in pellets superficies. Although estuaries have long been recognized as filters and accumulators of sediment and contaminants, recent studies show that they represent a potential receptor for plastic waste (Browne et al., 2010; Holmes et al., 2014) which increases the interaction between plastic pellets and these contaminants. However, considering the heavy metal concentrations found in the sediment which a high concentration at the Santos São Vicente Estuary (São 4
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Fig. 3. Multidimensional scaling (MDS) applied to similarity matrix (Bray Curtis). Each number represents a sample (n = 3); 1- Cardoso Island, 2- Boqueirão do Sul, 3Arpoador, 4- Guaraú, 5- Ruínas, 6- Sonho, 7- Vila SP, 8Guilhermina, 9- Gonzaga, 10- Enseada, 11- Itaguaré, 12Boraceia, 13- Santiago, 14- Massaguaçu, 15-Tabatinga, 16Sete Fontes, 17- Anchieta Island, 18- Grande, 19- Fazenda, 20- Black Polyethylene, 21- Blue Polyethylene, 22Polypropylene, 23- High Density Polyethylene. Vectors directions indicated sample associated with elements.
contaminants (Moore et al., 2002). Ashton et al. (2010) and Turner and Holmes (2011) conducted a suspension experiment with pellets and showed a tendency to accumulate metals directly from the water column or from the surface layer. There are possible metal uptake mechanisms that include adsorption of cations or complexes with neutral charge sites or regions of the plastic surface and co-precipitation or adsorption of Fe and Mn hydroxides (Giusti et al., 1994; Cobelo-Garcia et al., 2007; Fischer et al., 2007). Thus pellets, acting as chemical carriers, could function similarly to organic matter (such as fulvic and humic acid molecules, which may carry metals and organics). The beach environment acts as an energy receiver and can create a constant remobilization of sediment, causing recurrent burial and unearthing of plastic pellets (Turra et al., 2014). This dynamic changes the surface area of the pellets by increasing the number of cracks which may increase the adsorption capacity for pollutants (Endo et al., 2005; Ogata et al., 2009). The aging process of pellets, while suspended in water or when beached, alters the pellet characteristics and confers a more heterogeneous and reactive surface (Andrady, 2011). These alterations are engendered through both the erosion of the plastic itself, including the formation of various surface functional groups, and the attrition and adsorption–precipitation of various charged minerals and organic matter (Fotopoulou and Karapanagioti, 2012). While these interactions may be well-studied, the bioavailability and ecological risks of metal contaminants on pellets remain unknown and deserving of future examination. To characterize the behaviors of metals on beached and virgin samples, a multidimensional scaling (MDS) was performed and is shown in Fig. 3. There were differences in metals levels between some locations' samples and the virgins sample (PERMANOVA < 0.05) (Fig. 3). Here, patterns among polymers generally varied based on the specific metal and location. This analysis grouped all metals, except Zn which can indicated that these element comes from another source such mining (Mahiques et al., 2013). These differences are expected based upon their local sources to the bay (e.g., storm water runoff, shipyard activity, recreational boating) and prior research showing that concentrations of sorbed pollutants on plastic reflect regional differences (Ashton et al., 2010; Holmes et al., 2012; Fisner et al., 2013a, 2013b and Taniguchi et al., 2016). The results show a correlation between elements and some samples, mainly with the virgin samples (20, 21, 22 and 23). This behavior was expected for this group due the similarity between these samples (Table 1), which reveals a pattern on virgin
at northern areas, probably due the presence of currents and local dynamic. Considering beach morphodynamics, pellet distribution and that contaminant sources may vary on different scales, it is expected that the variability (see Table 2) would be reflected in the concentrations of metals. This variability probably makes the plastic pellets not ideal as indicators for metals contamination, but regardless, as a geochemical carrier the pellets represent a threat to the environment because of their persistence and buoyancy and because they can adsorb these contaminants onto their surface during environmental transport from the original source (Fotopoulou and Karapanagioti, 2012). Thus, the variability of the contaminants in seawater may be the main factor responsible for this variability in the concentrations on plastic pellets (Teuten et al., 2009). A comparison was made between the present and two other studies, Ashton et al. (2010) and Holmes et al. (2012), which were conducted in England (Fig. 2), to understand the contribution of pellets as a contamination vector for metals. Comparisons were made for some elements: Al, Cu, Fe, Mn and Zn, which were selected because they are the only ones in common. These studies found similar values for all elements and Al and Fe presented the highest values, being 45.27 mg kg− 1 (Guaraú) and 227.78 mg kg− 1 (Itaguaré), respectively, in the present study. Levels of Cu, Mn and Zn were low and similar to those found in other studies with exception of “Holmes et al., 2012_1” (Holmes et al., 2012) sample, in which the highest value of Mn was 20.50 mg kg− 1, about two times greater than the maximum level found in the present study (8.68 mg kg− 1 at Enseada sample). Such studies also reported that the importance of pellets as reservoirs for metals is relatively low on beaches, even for those containing the higher density plastics. However, Gouin et al. (2011) maintain the hypothesis that increasing the amount of plastics will result in increased levels of certain metals and other pollutants into the environment, due the hypothesis that pellets which would have already leached their additives. Clearly, further investigations are required regarding the mechanisms and kinetics of plastic-metal interactions and the effects of different environmental factors on these processes. In this study we found that metal concentrations are considerably increased on beached pellets - some of them can reach levels twice or greater than the virgin ones. Although the importance of pellets as reservoirs for metals is relatively low compared with that for organic contaminants, it is still necessary to consider it, given the persistence of pellets in the marine environment, their size and buoyancy, and the fact that pellets afford a means of ready transport of metals and other 5
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Kim, B.S.M., Salaroli, A.B., Ferreira, P.A.L., Sartoretto, J.R., Mahiques, M.M., Figueira, R.C.L., 2015. Spatial distribution and enrichment assessment of heavy metals in surface sediments from Baixada Santista, Southeastern Brazil. Mar. Pollut. Bull. 103, 333–338. Mahiques, M.M., Figueira, R.C.L., Salaroli, A.B., Alves, D.P.V., Gonçalves, C., 2013. 150 years of anthropogenic metal input in a Biosphere Reserve: the case study of the Cananéia–Iguape coastal system, Southeastern Brazil. Environ. Earth Sci. 68, 1073–1087. Majer, A.P., Vedolin, M.C., Turra, A., 2012. Plastic pellets as oviposition site and means of dispersal for the ocean-skater insect Halobates. Mar. Pollut. Bull. 64, 1143–1147. Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Otake, C., Kaminuma, T., 2001. Plastic resin pellets as a transport medium for toxic chemicals in the marine environment. Environ. Sci. Technol. 35 (2), 318–324. Michaeli, W., 1995. Tecnologia dos Plásticos. Edgard Blucher Ltda, São Paulo. Moore, S.L., Gregorio, D., Carreon, M., Weisberg, S.B., Leecaster, M.K., 2001. Composition and distribution of beach debris in Orange County, California. Mar. Pollut. Bull. 4 (2), 241–245. Moore, C.J., Moore, S.L., Leecaster, M.K., Lattin, G., Zellers, A., 2002. A comparison of neustonic plastic and zooplankton abundance in southern California's coastal waters. Mar. Pollut. Bull. 44, 1035–1038. Moreira, F.T., Balthazar-Silva, D., Barbosa, L., Turra, A., 2016. Revealing accumulation
samples. For the beached group, it would be desirable to monitor the levels in order to avoid a possible increase of heavy metal contents as a consequence of human activities. This can also be associated with content that can create a better condition of accumulation of these elements. The groups observed in MDS analysis can illustrate the location of those groups in the data space and allow for an interpretation of how the individual metals levels are important to this study. Based on the knowledge of field conditions, these groups correspond notably well to the samples, mainly with the virgin pellets. However, our results are only preliminary and there are other issues that need further discussion, such as whether or not the pellets accurately reflect the magnitude of contaminant inputs (Zhang et al., 2015). 4. Conclusions The primary purpose of this study was to show that plastic pellets act as a metal carrier in the marine environment, both virgin and those that are distributed throughout the state of São Paulo. These results provide the first record for this area, furthering the understanding of the occurrence of metals in microplastics. The analysis has shown that metal concentrations can have substantial variability, both within a beach (among samples) and among beaches. The study also reveals that there are local factors such as the presence of anthropogenic activities, which may affect certain regions. Nevertheless, pellet presence is of concern as solid waste in the environment; therefore, environmental monitoring of microplastics must be conducted continually in order to check the impacts of this material and to further our understanding of the problem as a whole. Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2017.10.019. Acknowledgments Financial support for this study was mainly provided by CNPq (157967/2011-5) and technical support from Oceanographic Institute of University of São Paulo (IOUSP). References Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Ashton, K., Holmes, L., Turner, A., 2010. Association of metals with plastic production pellets in the marine environment. Mar. Pollut. Bull. 60, 2050–2055. Barnes, D.K.A., Galagani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and fragmentation of plastic debris in global environments. Philos. Trans. R. Soc. B 364, 1985–1998. Bícego, M.C., Taniguchi, S., Yogui, G.T., Montone, R.C., da Silva, D.A.M., Lourenço, R.A., Martins, C.C., Sasaki, S.T., Pellizari, V.H., Weber, R.R., 2006. Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Mar. Pollut. Bull. 52, 1784–1832. Brennecke, D., Duarte, B., Paiva, F., Caçador, I., Canning- Clode, J., 2016. Microplastics as vector for heavy metal contamination from the marine environment. Estuar. Coast. Shelf Sci. 178, 189–195. Browne, M.A., Galloway, T.S., Thompson, R.C., 2010. Spatial patterns of plastic debris along estuarine shorelines. Environ. Sci. Technol. 44, 3404–3409. Browne, M.A., Niven, S.J., Galloway, T.S., Rowland, S.J., Thompson, R.C., 2013. Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr. Biol. 23, 2388–2392. Carpenter, E.J., Anderson, S.J., Harvey, G.R., Miklas, H.P., Peck, B.B., 1972. Polystyrene spherules in coastal waters. Science 178, 749–750. Claessens, M., De Meester, S., Van Landuyt, L., De Clerk, K., Janssen, C.R., 2011. Occurrence and distribution of microplastic in marine sediment along the Belgian coast. Mar. Pollut. Bull. 62 (10), 2199–2220. Cobelo-Garcia, A., Turner, A., Millward, G.E., 2007. Behaviour of palladium(II), platinum (IV) and rhodium(III) in artificial and natural waters: influence of reactor surface and geochemistry on metal recovery. Anal. Chim. Acta 585, 202–210. Colabuono, F.I., Barquete, V., Domingues, B.S., Montone, R.C., 2009. Plastic ingestion by Procellariiformes in Southern Brazil. Mar. Pollut. Bull. 58, 93–96. Costa, M.F., Ivar do Sul, J.A., Silva- Cavalcanti, J.S., Araújo, M.C.B., Spengler, A., Tourinho, P.S., 2009. On the importance of size of plastic fragments and pellets on the strandline: a snapshot of a Brazilian beach. Environ. Monit. Assess. 168 (1–4),
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Butylin residues in livers of humans and wild terrestrial mammals and in plastic products. Environ. Pollut. 106, 203–218. Takahashi, Y., Samuna, K., Itai, T., Zheng, G., Sato, M., 2008b. Speciation of antimony in PET bottles produced in Japan and China by X-ray absorption fine structure spectroscopy. Environ. Sci. Technol. 42, 9045–9050. Taniguchi, S., Colabuono, F.I., Dias, P.S., Oliveira, R., Fisner, M., Turra, A., Izar, G.M., Abessa, D.M.S., Saha, M., Hosoda, J., Yamashita, R., Takada, H., Lourenço, R.A., Magalhães, C.A., Bícego, M.C., Montone, R.C., 2016. Spatial variability in persistent organic pollutants and polycyclic aromatic hydrocarbons found in beach-stranded pellets along the coast of the state of São Paulo, southeastern Brazil. Mar. Pollut. Bull. 106, 87–94. Teuten, E.L., Saquing, J.M., Knappe, D.R.U., Barlaz, M.A., Jonsson, S., Björn, A., Rowland, S.J., Thompson, R.C., Galloway, T.S., Yamashita, R., Ochi, D., Watanuki, Y., Moore, C., Viet, P.H., Tana, T.S., Prudente, M., Boonyatumanond, R., Zakaria, P.M., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K., Hagino, Y., Imamura, A., Saha, M., Takada, H., 2009. Transport and release of chemicals from plastics to the environment and to wildlife. Philos. Trans. R. Soc. B 364, 2027–2045. Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G., McGonigle, D., Russel, A.E., 2004. Lost at sea: where does all the plastic go? Science 304, 838. Turner, A., Holmes, L., 2011. Occurrence, distribution and characteristics of beached plastic production pellets on the island of Malta (central Mediterranean). Mar. Pollut. Bull. 62, 377–381. Turra, A., Manzano, A.B., Dias, R.J.S., Mahiques, M.M., Barbosa, L., Balthazar-Silva, D., Moreira, F.T., 2014. Three-dimensional distribution of plastic pellets in a sandy beach: shifting paradigms. Sci. Rep. 4, 4435. http://www.nature.com/srep/2014/ 140327/srep04435/full/srep04435.html. USEPA (United States Environmental Protection Agency), 1996. Method 3050B. Acid Digestion of Sediments, Sludges and Soil. Revision 2. (December). Zenebon, O., Muarata, L.T.F., Pascuet, N., Alcântara, M.R.S., Nunes, M.C.D., Ribeiro, E.R., Tiglea, P., 2004. Determinação de metais presentes em corantes e pigmentos utilizados em embalagens para alimentos. Rev. Inst. Adolfo Lutz 63 (1), 56–62. Zhang, W., Ma, X., Zhang, Z., Wang, Y., Wang, J., Ma, D., 2015. Persistent organic pollutants carried on plastic resin pellets from two beaches in China. Mar. Pollut. Bull. 99, 28–34.
zones of plastic pellets in sandy beaches. Environ. Pollut. 218, 313–321. Nobre, C.R., Santana, M.F.M., Maluf, A., Cortez, F.S., Cesar, A., Pereira, C.D.S., Turra, A., 2015. Assessment of microplastic toxicity to embryonic development of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Mar. Pollut. Bull. 92, 99–104. Nomura, D.H., Mateus, S.F., Saiki, M., Bode, P., 2001. Characterization of inorganic components in plastic materials. J. Radioanal. Nucl. Chem. 244 (1), 61–65. Ogata, Y.A., Takada, H.A., Mizukawa, K.A., Hirai, H.A., Iwasa, S.A., Endo, S.A., Mato, Y.A., Saha, M.A., Okuda, K.A., Nakashima, A.A., Murakami, M.B., Zurcher, N.C., Booyatumanondo, R.D., Zakaria, M.P.E., Dung, L.Q.F., Gordon, M.G., Miguez, C.H., Suzuki, S.I., Moore, C.J., Karapanagioti, H.K.K., Weerts, S.L., McClurg, T.L., Burresm, E., Smith, W.N., Van Velkenburg, M.O., Lang, J.S.P., Lang, R.C.P., Laursen, D.Q., Danner, B.R., Stewardson, N.S., Thompson, R.C.T., 2009. International Pellet Watch: global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Mar. Pollut. Bull. 58, 1437–1446. Plastics Europe, 2011. Plastics – The Facts 2011: An Analysis of European Plastic Production, Demand and Recovery for 2010. European Association of Plastics Manufacturers, Brussels. Reddy, M.S., Basha, S., Adimrthy, S., Ramachandraiah, G., 2006. Description of the small plastics fragments in marine sediments along the Alang-Sosiya shipbreaking yard, India. Estuar. Coast. Shelf Sci. 68 (3–4), 656–660. Rochman, C.M., Kurobe, T., Flores, I., Teh, S.J., 2014. Early warning signs of endocrine disruption in adult fish from the ingestion of polyethylene with and without sorbed chemical pollutants from the marine environment. Sci. Total Environ. 493, 656–661. Rodriguez, F., 1996. Principles of Polymer Systems. Taylor & Francis, Washington. Ryan, P.G., 1988. The characteristics and distribution of plastic particles at the sea-surface off the southwestern Cape Province, South Africa. Mar. Environ. Res. 15, 249–273. Santana, F.M.F., Moreira, F., Turra, A., 2016. Trophic transference, assimilation and retention of microplastics in marine organisms: are there evidences for bioaccumulation and biomagnification? Mar. Pollut. Bull. 106, 183–189. Silva, P.S.C., Damatto, S.R., Maldonado, C., Fávaro, D.I.T., Mazzilli, B.P., 2011. Metal distribution in sediment core from São Paulo State Coast, Brazil. Mar. Pollut. Bull. 62, 1130–1139. Takahashi, Y., Mukai, H., Tanabe, S., Sakaiama, K., Miyazaki, T., Masuno, H., 2008a.
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Spatial variability in the concentrations of metals in beached microplastics M.C. Vedolina,⁎, C.Y.S. Teophiloa, A. Turrab, R.C.L. Figueiraa a b
Laboratório de Química Inorgânica Marinha, Departamento de Oceanografia Química, Instituto Oceanográfico, USP, São Paulo, SP, Brazil Laboratório de Manejo, Ecologia e Conservação Marinha, Departamento de Oceanografia Biológica, Instituto Oceanográfico, USP, São Paulo, SP, Brazil
A R T I C L E I N F O
A B S T R A C T
Keywords: Pellets Microplastics Metals Inorganic pollutants Pollution São Paulo coast
Heavy metals and microplastics have been considered as threats to the marine environment and the interactions between these two pollutants are poorly understood. This study investigates the interactions between metals adsorbed in pellets collected randomly from 19 beaches along the coast of São Paulo State in southeastern Brazil, comparing these levels with those in virgin pellets. The samples were analyzed for Al, Cr, Cu, Fe, Mn, Sn, Ti and Zn by inductively coupled plasma optical emission spectroscopy (ICP-OES). The polymers were solubilized via acid digestion. The highest levels occurred with Fe (227.78 mg kg− 1 - Itaguaré) and Al (45.27 mg kg− 1 Guaraú) in the same areas, which are closer to the Port of Santos. The metal adsorption on pellets collected is greater than that on virgin pellets. In this context, pellets can be considered to be a carrier for the transport of metals in the environment, even in small quantities.
1. Introduction Since the development of the first synthetic polymer, “Bakelite”, in 1909, a number of low cost techniques have been developed to produce a plastic product that is durable, inert and resistant (Plastics Europe, 2011). However, the properties that make plastics so useful (e.g., low density, durability) have created a problem related to the management of waste due to improper discarding (Barnes et al., 2009; Hopewell et al., 2009), especially in the oceans. Microplastics are commonly defined as any plastic particles measuring < 5 mm in diameter, but they can also be classified as “primary microplastics”, which include production pellets and microbeads, or “secondary microplastics”, which come from larger plastic items that have degraded and consequently fragmented (Andrady, 2011; GESAMP, 2016). Plastic pellets are composed of polymers, usually polyethylene, polystyrene or polypropylene; these pellets are from 2 to 5 mm in diameter and are used as raw materials in the production of plastic items (Ogata et al., 2009). They can be found in a range of aquatic environments, which suggests that they can be lost during loading and transportation, both on land and at sea, and during their handling at plastic transformation factories and harbors (Carpenter et al., 1972; Gregory, 1977, 1978; Ryan, 1988; EPA, 1992; Mato et al., 2001; Moore et al., 2001a; Reddy et al., 2006; Costa et al., 2009; Ogata et al., 2009). In addition to their visual impacts, microplastics in the marine environment are a threat to animals by accumulation, entrapment,
entanglement, suffocation and fouling (Thompson et al., 2004; Colabuono et al., 2009; Gregory, 2009; Majer et al., 2012; GESAMP, 2016). In the marine environment, these particles are able to sequester contaminants from sea water, contaminants such as polychlorinated biphenyl (PCB), dichlorodiphenyltrichloroethane (DDT), polycyclic aromatic hydrocarbons (PAHs) and metals (Mato et al., 2001; Endo et al., 2005; Ogata et al., 2009; Ashton et al., 2010; Holmes et al., 2012, 2014; Brennecke et al., 2016). Thus, they can act as a source of these contaminants to organisms via ingestion, since they may be mistaken for food items (Teuten et al., 2009) or accidentally ingested by filterfeeders (Santana et al., 2016a). Most of these pollutants are toxic and bioaccumulative, and if leached from pellets and assimilated by an organism, can be introduced into the food chain (Browne et al., 2013). Until recently, interactions between metals and plastic pellets had not been considered, because polymers are considered to be relatively inert toward aqueous metal ions (Plastics Europe, 2011). However, recent studies recorded the presence of adsorbed metals in plastics due to surface alterations in the marine environment (Ashton et al., 2010; Holmes et al., 2012, 2014). Fotopoulou and Karapanagioti (2012) described the surface of beached pellets as rough and with pronounced cavities compared to virgin pellets. These alterations increase the surface area and generate anionic active sites such as carbonyls for the adsorption of metals from seawater (Holmes et al., 2012, 2014), which might explain why there are lower concentrations of trace metals in newly released (virgin) pellets than in beached pellets. The sources of metals to the oceans are diverse, though many arise
⁎ Corresponding author at: Departamento de Oceanografia Química, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, Cidade Universitária, São Paulo, SP 05508-120, Brazil. E-mail address: [email protected] (M.C. Vedolin).
http://dx.doi.org/10.1016/j.marpolbul.2017.10.019 Received 11 April 2017; Received in revised form 5 October 2017; Accepted 7 October 2017 0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Vedolin, M.C., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2017.10.019
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along the São Paulo coast during 2012 (Fig. 1). Approximately 300 pellets were collected by hand from each site and stored in polyethylene bags. Each sample was washed with sea-water and dried under ambient conditions. In the laboratory, pellets from each site were pooled in 3 replicates with 100 pellets for subsequent analyses.
from the irresponsible dumping of sewage, of industrial and household waste and many other sources, such as release from surfaces covered by antifouling coatings, or urban drainage, atmospheric deposition, disposal of mining residues, among others. Some metals found on plastic debris derive from the manufacturing process (additives), but several metals have been found to occur on plastic debris as a result of environmental sorption (Holmes et al., 2012, 2014; Rochman et al., 2014). Nobre et al. (2015) showed that beached pellets have lower toxicity than virgin pellets, although their toxicity may vary as a function of the different additives, like organic compounds, used in their production. The environmental risks posed by microplastics are defined as a combination of their presence (number; e.g., Turra et al., 2014) and potential effects on the environment (e.g., concentration of contaminants such as PCBs and PAHs) (GESAMP, 2016). Recent studies have shown the spatial variability of the contamination in beached pellets by organic pollutants on various spatial scales ranging from meters to global (Ogata et al., 2009; Karapanagioti and Klontza, 2008; Karapanagioti et al., 2010; Frias et al., 2010; Hirai et al., 2011; Heskett et al., 2012; Fisner et al., 2013a, 2013b; Taniguchi et al., 2016), but no information is available about the concentrations of metals specific to the Brazil area. The main objective was to determine the concentrations of metals in pellets from 19 beaches along the coast of the São Paulo state, assess their variability and also compare them to those levels found in virgin pellets.
2.2. Sample digestion The samples of beached pellets were subjected to partial acid digestion following the method US EPA 3050B (USEPA, 1996). The three 100 pools of pellets (~ 2 g each) were taken in a 50 mL beaker and then 10 mL of HNO3 (1:1), 5 mL of pure HNO3, 3.0 mL of H2O2 (30% V/V), and 10 mL of HCl were added at 90 °C. Subsequently, these digests were filtered and diluted to 40 mL with Millipore Milli-Q water. The samples were analyzed for Al, Cr, Cu, Fe, Mn, Sn, Ti and Zn by inductively coupled plasma optical emission spectroscopy (ICP-OES; Varian, model 710ES). Pellets were analyzed as sediment samples, i.e., we assumed that they have some capacity to adsorb and desorb (leach) metals and other chemical compounds on/from their surfaces; thus, they were considered as a potential source of contamination for the marine environment. In this way, one certified reference material for sediment (SS-1) from EnvironMAT™ SPC Science were subjected to the same analytical procedure in order to evaluate the precision and accuracy of the method. Additionally, four types (polypropylene, high density polyethylene and two grades/colors of polyethylene, black and blue) of virgin resin pellets were obtained from a local plastic processing facility (Braskem SA, São Paulo) and analyzed accordingly for comparison with the data collected from the beached pellets.
2. Materials and methods 2.1. Sampling This investigation was developed on the coast of São Paulo State in southeastern Brazil (23°21′54.20″S/44°44′21.94″O and 25°18′30.81″S/ 48° 5′37.25″O). São Paulo has a coastline of approximately 620 km, which is highly urbanized, especially in the central coast region known as “Baixada Santista”. This region is heavily impacted by the Port of Santos (the largest port in Latin American) and the Industrial Complex of Cubatão (Harari and Gordon, 2001; Silva et al., 2011). As a result of the anthropogenic activities in this area, many pollutants, such as PCBs and PAHs, have been found in sediment samples (Bícego et al., 2006). The transport of plastic pellets through Santos Harbor is responsible for 50,000 tons of granules/month (Fisner et al., 2013a, 2013b), and a large quantity of pellets has been reported on nearby beaches (Turra et al., 2014; Moreira et al., 2016). Pellets were collected randomly from nineteen coastal beaches
2.3. Data analysis Differences in the levels of metals between each site were evaluated using a non- parametric Kruskal-Wallis test followed by the post hoc Dunn's test. The elements Cr and Sn, which usually exhibited values below the detection limit of the method were excluded from analyses. Differences between virgin pellets samples were also evaluated using ANOVA (one-way) followed by the post hoc Tukey test. To visualize the similarities among and between samples (beached and virgins), a non-Metric Multidimensional Scaling (nMDS) was applied to the similarity matrix (Bray Curtis similarity) and permutational multivariate analyses of variance (PERMANOVA). The trace statistic for the null hypothesis of no group differences was calculated with 999 permutations. Fig. 1. Beaches (municipalities) where pellets were sampled along the São Paulo state coast in 2012. Note: 1Cardoso Island (Cananeia); 2- Boqueirão do Sul (Ilha Comprida); 3- Arpoador (Peruíbe); 4- Guaraú (Peruíbe); 5Ruínas (Peruíbe); 6- Sonho (Itanhaém); 7- Vila São Paulo (SP) (Mongaguá); 8- Guilhermina (Praia Grande); 9Gonzaga (Santos); 10- Enseada (Guarujá); 11- Itaguaré (Bertioga); 12- Boraceia (São Sebastião); 13- Santiago (São Sebastião); 14- Massaguaçu (Caraguatatuba); 15- Tabatinga (Caraguatatuba); 16- Sete Fontes (Ubatuba); 17- Anchieta Island (Ubatuba); 18- Grande (Ubatuba); and 19- Fazenda (Ubatuba).
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Table 1 Metals levels (mg kg− 1; mean ± standard deviation; n = 3; MQL: method quantitation limit) in samples (2 g; ~ 100 particles) of different resin types (PE: polyethylene; HDPE: high density polyethylene; PP: polypropylene) available after acid digestion. Values followed by the same letter in the column do not differ by Tukey test, p < 0.05. Resins
Elements (mg kg− 1) Al
1. 2. 3. 4.
PE - Black PE - Blue HDPE PP
Cr a
4.7 ± 0.1 7.4 ± 0.3b 16.0 ± 1.8c 5.7 ± 0.4a
0.370 0.430 0.330 0.490
Cu ± ± ± ±
a
0.010 0.008b 0.004d 0.020a
Fe
< MQL < MQL < MQL < MQL
2.30 3.30 4.10 7.60
Mn ± ± ± ±
a
0.03 0.40a 1.50a 1.20b
Sn
< MQL < MQL < MQL < MQL
Ti
Zn
< MQL < MQL < MQL < MQL
1.35 ± 0.07a 2.40 ± 0.30b < MQL < MQL
a
3.6 ± 0.1 4.6 ± 0.7b < MQL < MQL
Note: MQL values for Al 0.65 mg kg− 1, Cr 0.20 mg kg− 1, Cu 0.14 mg kg− 1, Fe 0.48 mg kg− 1, Mn 2.72 mg kg− 1, Sn 1.12 mg kg− 1, Ti 1.53 mg kg− 1, Zn 0.87 mg kg− 1.
and plasticizers, which may contain metallic elements such as Cd, Mn, Pb, Sn and Zn (Michaeli, 1995; Rodriguez, 1996). From this list, only Zn was detected in this study, and in low concentration; moreover, might be originated from the production process and there is not a strong evidence indicating the toxicity about virgin pellets.
The Statistica 12.0 and Primer 7 software packages were employed for data treatment and analysis. Data were transformed prior to all analysis log(x + 1), when necessary.
3. Results and discussion 3.1. Virgin pellets analysis
3.2. Metals levels in beached pellets
Digestion analysis in polymers is applied mainly for the determination of the metal levels in plastics that will be used in the food industry (Nomura et al., 2001; Zenebon et al., 2004; Takahashi et al., 2008a, 2008b). In addition, there are other studies that describe a similar method for plastic pellets (Ashton et al., 2010; Holmes et al., 2012, 2014). Table 1 summarizes the concentration of pre-existing trace metals on virgin pellets and the Tukey's test result. The levels of metals do not exhibit obvious variations in this sample but the differences between types of pellets were confirmed in the ANOVA results (p < 0.05) significant differences were observed between the types of pellets for Al Cr, Fe, Sn and Zn. According Rochman et al. (2014), in general, all types of plastic tended to accumulate similar concentrations of metals; however the results on virgins samples in this study show that this can vary. For certain metals, such as Al and Fe, the concentrations in the plastic pellets can be explained by contamination during manufacturing via abrasion caused by friction in the equipment (Hoffman et al., 1991). Since plastics have become widely used, plastic production has grown and created a demand for different kinds of plastics with various combinations of properties (EPA, 1990). The additives provide some features that give such properties to plastics. The most important additives are antioxidants, polymer stabilizers, flame retardants, pigments
Metals levels that were detectable in partial acid digests of the beached pellets showed variability among the three replicates and reflected the heterogeneity of the accumulation process(es) (Table 2). These values are similar to the result described by Ashton et al. (2010) and Holmes et al. (2012) who also measured the metal accumulation in plastic pellets. The order of metal accumulation (Fe > Al > Mn > Cu = Zn) is similar in these studies too, and the mean concentrations are within an order of magnitude of the corresponding concentrations in pellets sampled from different places. There were differences in metals levels between some locations for the majority of the elements (Kruskall Wallis p < 0.05). However, there was no significant difference between beaches for elements Al and Zn (Kruskall Wallis - ANOVA p > 0.05). Fig. 2 shows the median levels of metals (n = 3) for each sampling site and compared these results with other studies. For all metals, concentration accumulated on pellets varied significantly between locations, which is similar to what is observed for organic pollutants (Fisner et al., 2013a, 2013b; Taniguchi et al., 2016), see Fig. 2. Statistical differences between places were shown (Dunn's teste p < 0.05) for Cu, Fe, Mn and Ti in Appendix A. Table 2 shows that some beaches at North and South exhibited pellets with high concentrations of some elements - Al (45 mg kg− 1 Guaraú) and Zn (8 mg kg− 1 Massaguaçu), for example. Besides some elements more related with the earth's crust and presence in marine
Table 2 Metals levels (mg kg− 1; mean ± standard deviation; n = 3) in pellet sampled from 19 beaches along São Paulo coast in 2012. Beaches
Al
Cu
Fe
Mn
Ti
Cardoso Island Boqueirão do Sul Arpoador Guaraú Ruínas Sonho Vila SP Guilhermina Gonzaga Enseada Itaguaré Boraceia Santiago Massaguaçu Tabatinga Sete Fontes Anchieta Island Grande Fazenda
7 ± 9 18 ± 17 14 ± 0.3 45 ± 9 23 ± 10 22 ± 5 24 ± 3 25 ± 3 30 ± 27 28 ± 5 33 ± 10 23 ± 6 27 ± 11 13 ± 14 41 ± 19 30 ± 21 26 ± 23 29 ± 14 44 ± 3
1 ± 1 0.3 ± 0.1 0.3 ± 0.1 0.5 ± 1 0.4 ± 0.4 0.5 ± 0.5 1 ± 1 0.2 ± 0 1 ± 1 1 ± 0 0.5 ± 0 1 ± 1 0.1 ± 0.1 1 ± 0 0.2 ± 0.2 1 ± 1 0.3 ± 0.2 0.2 ± 0.2 0.2 ± 0.2
58 ± 17 55 ± 24 90 ± 22 150 ± 15 95 ± 19 55 ± 49 114 ± 63 119 ± 27 99 ± 86 86 ± 22 228 ± 142 65 ± 13 67 ± 11 122 ± 55 56 ± 7 58 ± 13 36 ± 35 56 ± 18 114 ± 8
9 ± 5 2 ± 1 2 ± 0.3 3 ± 1 2 ± 1 2 ± 0.3 3 ± 1 3 ± 0.3 3 ± 3 9 ± 6 4 ± 2 2 ± 1 0.5 ± 1 1 ± 01 0.3 ± 0.3 0.5 ± 0.3 < 0.01 ± 0 3 ± 1 3 ± 1
2 2 2 3 2 2 2 2 2 2 2 1 1 1 2 1 1 2 2
3
Zn ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0 1 1 0.4 1 1 1 0 2 0.3 0.3 0.2 0 0.3 0.3 0.5 1 2 0.5
1 ± 1 1 ± 1 1 ± 1 1 ± 1 0.3 ± 0.3 0.4 ± 0.3 1 ± 1 0.4 ± 0.4 1 ± 0 1 ± 1 3 ± 1 1 ± 1 3 ± 0.3 8 ± 9 3 ± 2 2 ± 2 2 ± 2 1 ± 0 5 ± 5
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Fig. 2. Metals levels (mg kg − 1; median; n = 3) in pellet sampled from 19 beaches along São Paulo coast in 2012 and 4 different resin types (PE: polyethylene; HDPE: high density polyethylene; PP: polypropylene) available after acid digestion. Significant difference among elements (p < 0.05) is indicated by *. Comparison of level metal in pellets sample with other studies using mean results (Ashton et al., 2010 and Holmes et al., 2012).
Paulo Southeastern Coast) can reach 15.877 mg kg− 1 for Al and 18.893 for Fe mg kg− 1 (Kim et al., 2015), the highest levels observed in this study - versus the concentrations of adsorbed heavy metals in the plastic pellets, the role of these particles cannot be considered alarming vectors for marine organisms. This study do not corroborates those of Claessens et al. (2011) and Holmes et al. (2012), who have obtained results in that the concentration of metals increases with proximity to anthropogenic sources, especially in port regions. Moreover, in contrast to what is observed for organic pollutants, PAHs (Fisner et al., 2013a, 2013b) and PCBs (Taniguchi et al., 2016) in the same area, the lowest levels were found
sediment (Al and Fe) were highly variable and may be indicating the proximity with estuaries. Holmes et al. (2014) were the first to examine the interactions of metals with plastics in estuaries and suggested that changes in some conditions like salinity and pH may affect adsorption of metals in pellets superficies. Although estuaries have long been recognized as filters and accumulators of sediment and contaminants, recent studies show that they represent a potential receptor for plastic waste (Browne et al., 2010; Holmes et al., 2014) which increases the interaction between plastic pellets and these contaminants. However, considering the heavy metal concentrations found in the sediment which a high concentration at the Santos São Vicente Estuary (São 4
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Fig. 3. Multidimensional scaling (MDS) applied to similarity matrix (Bray Curtis). Each number represents a sample (n = 3); 1- Cardoso Island, 2- Boqueirão do Sul, 3Arpoador, 4- Guaraú, 5- Ruínas, 6- Sonho, 7- Vila SP, 8Guilhermina, 9- Gonzaga, 10- Enseada, 11- Itaguaré, 12Boraceia, 13- Santiago, 14- Massaguaçu, 15-Tabatinga, 16Sete Fontes, 17- Anchieta Island, 18- Grande, 19- Fazenda, 20- Black Polyethylene, 21- Blue Polyethylene, 22Polypropylene, 23- High Density Polyethylene. Vectors directions indicated sample associated with elements.
contaminants (Moore et al., 2002). Ashton et al. (2010) and Turner and Holmes (2011) conducted a suspension experiment with pellets and showed a tendency to accumulate metals directly from the water column or from the surface layer. There are possible metal uptake mechanisms that include adsorption of cations or complexes with neutral charge sites or regions of the plastic surface and co-precipitation or adsorption of Fe and Mn hydroxides (Giusti et al., 1994; Cobelo-Garcia et al., 2007; Fischer et al., 2007). Thus pellets, acting as chemical carriers, could function similarly to organic matter (such as fulvic and humic acid molecules, which may carry metals and organics). The beach environment acts as an energy receiver and can create a constant remobilization of sediment, causing recurrent burial and unearthing of plastic pellets (Turra et al., 2014). This dynamic changes the surface area of the pellets by increasing the number of cracks which may increase the adsorption capacity for pollutants (Endo et al., 2005; Ogata et al., 2009). The aging process of pellets, while suspended in water or when beached, alters the pellet characteristics and confers a more heterogeneous and reactive surface (Andrady, 2011). These alterations are engendered through both the erosion of the plastic itself, including the formation of various surface functional groups, and the attrition and adsorption–precipitation of various charged minerals and organic matter (Fotopoulou and Karapanagioti, 2012). While these interactions may be well-studied, the bioavailability and ecological risks of metal contaminants on pellets remain unknown and deserving of future examination. To characterize the behaviors of metals on beached and virgin samples, a multidimensional scaling (MDS) was performed and is shown in Fig. 3. There were differences in metals levels between some locations' samples and the virgins sample (PERMANOVA < 0.05) (Fig. 3). Here, patterns among polymers generally varied based on the specific metal and location. This analysis grouped all metals, except Zn which can indicated that these element comes from another source such mining (Mahiques et al., 2013). These differences are expected based upon their local sources to the bay (e.g., storm water runoff, shipyard activity, recreational boating) and prior research showing that concentrations of sorbed pollutants on plastic reflect regional differences (Ashton et al., 2010; Holmes et al., 2012; Fisner et al., 2013a, 2013b and Taniguchi et al., 2016). The results show a correlation between elements and some samples, mainly with the virgin samples (20, 21, 22 and 23). This behavior was expected for this group due the similarity between these samples (Table 1), which reveals a pattern on virgin
at northern areas, probably due the presence of currents and local dynamic. Considering beach morphodynamics, pellet distribution and that contaminant sources may vary on different scales, it is expected that the variability (see Table 2) would be reflected in the concentrations of metals. This variability probably makes the plastic pellets not ideal as indicators for metals contamination, but regardless, as a geochemical carrier the pellets represent a threat to the environment because of their persistence and buoyancy and because they can adsorb these contaminants onto their surface during environmental transport from the original source (Fotopoulou and Karapanagioti, 2012). Thus, the variability of the contaminants in seawater may be the main factor responsible for this variability in the concentrations on plastic pellets (Teuten et al., 2009). A comparison was made between the present and two other studies, Ashton et al. (2010) and Holmes et al. (2012), which were conducted in England (Fig. 2), to understand the contribution of pellets as a contamination vector for metals. Comparisons were made for some elements: Al, Cu, Fe, Mn and Zn, which were selected because they are the only ones in common. These studies found similar values for all elements and Al and Fe presented the highest values, being 45.27 mg kg− 1 (Guaraú) and 227.78 mg kg− 1 (Itaguaré), respectively, in the present study. Levels of Cu, Mn and Zn were low and similar to those found in other studies with exception of “Holmes et al., 2012_1” (Holmes et al., 2012) sample, in which the highest value of Mn was 20.50 mg kg− 1, about two times greater than the maximum level found in the present study (8.68 mg kg− 1 at Enseada sample). Such studies also reported that the importance of pellets as reservoirs for metals is relatively low on beaches, even for those containing the higher density plastics. However, Gouin et al. (2011) maintain the hypothesis that increasing the amount of plastics will result in increased levels of certain metals and other pollutants into the environment, due the hypothesis that pellets which would have already leached their additives. Clearly, further investigations are required regarding the mechanisms and kinetics of plastic-metal interactions and the effects of different environmental factors on these processes. In this study we found that metal concentrations are considerably increased on beached pellets - some of them can reach levels twice or greater than the virgin ones. Although the importance of pellets as reservoirs for metals is relatively low compared with that for organic contaminants, it is still necessary to consider it, given the persistence of pellets in the marine environment, their size and buoyancy, and the fact that pellets afford a means of ready transport of metals and other 5
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299–304. Endo, S., Takizawa, R., Okuda, K., Takada, H., Chiba, K., Kanehiro, H., Ogi, H., Yamashita, R., Date, T., 2005. Concentration of polychlorinated biphenyls (PCBs) in beached resin pellets: variability among individual particles and regional differences. Mar. Pollut. Bull. 50 (10), 1103–1114. EPA, 1990. Methods to manage and control plastic wastes. In: Report to the Congress. Washington: EPA/530-SW-89-051. Environ Prot. Age. EPA, 1992. Plastics pellets in the aquatic environment: sources and recommendations. In: Washington: EPA/842-B-92-010. Final Report. Environ. Prot. Age. Fischer, A.C., Kroon, J.J., Verburg, T.G., Teunissen, T., Wolterbeek, H.T., 2007. On the relevance of iron adsorption to container materials in small-volume experiments on iron marine chemistry: 55Fe-aided assessment of capacity, affinity and kinetics. Mar. Chem. 107, 533–546. Fisner, M., Taniguchi, S., Majer, A.P., Bícego, M.C., Turra, A., 2013a. P concentration and composition of polycyclic aromatic hydrocarbons (PAHs) in plastic pellets: implications for small-scale diagnostic and environmental monitoring. Mar. Pollut. Bull. 76, 349–354. Fisner, M., Taniguchi, S., Moreira, F., Bícego, M.C., Turra, A., 2013b. Polycyclic aromatic hydrocarbons (PAHs) in plastic pellets: variability in the concentration and composition at different sediment depths in a Sandy beach. Mar. Pollut. Bull. 70, 219–226. Fotopoulou, K., Karapanagioti, H.K., 2012. Surface properties of beached plastic pellets. Mar. Environ. Pollut. 81, 70–77. Frias, J.P.G.L., Sobral, P., Ferreira, A.M., 2010. Organic pollutants in microplastics from two beaches of the Portuguese coast. Mar. Pollut. Bull. 60, 1988–1992. GESAMP, 2016. Sources, fate and effects of microplastics in the marine environment: part 2 a global assessment. In: Kershaw, P.J. (Ed.), (IMO/FAO/UNESCO-IOC/UNIDO/ WMO/IAEA/UN/UNEP/UNDP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection). Rep. Stud. GESAMP No. 93, (220 pp.). Giusti, L., Hamilton-Taylor, J., Davison, W., Newitt, C.N., 1994. Artefacts in sorption experiments with trace metals. Sci. Total Environ. 152, 227–238. Gouin, T., Roche, N., Lohmann, R., Hodges, G.A., 2011. Thermodynamic approach for assessing the environmental exposure of chemicals absorbed to microplastic. Environ. Sci. Technol. 45, 1466–1472. Gregory, M.R., 1977. Plastic pellets on New Zealand beaches. Mar. Pollut. Bull. 8, 82–84. Gregory, M.R., 1978. Accumulation and distribution of virgin plastic granules on New Zealand beaches. N. Z. J. Mar. Freshw. Res. 12 (4), 399–414. Gregory, M.R., 2009. Environmental implications of plastic debris in marine settings—entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos. Trans. R. Soc. B 364, 2013–2025. Harari, J., Gordon, M., 2001. Simulações numéricas da dispersão de substâncias no Porto e Baía de Santos, sob ação das marés. Rev. Bras. Recur. Hidr. 6 (4), 115–131. Heskett, M., Takada, H., Yamashita, R., Yuyama, M., Ito, M., Geok, Y.B., Ogata, Y., Kwan, C., Heckhausen, A., Taylor, H., Powell, T., Morishige, C., Young, D., Patterson, H., Robertson, B., Bailey, E., Mermoz, J., 2012. Measurement of persistent organic pollutants (POPs) in plastic resin pellets from remote islands: toward establishment of background concentrations for International Pellet Watch. Mar. Pollut. Bull. 64, 445–448. Hirai, H., Takada, H., Ogata, Y., Yamashita, R., Mizukawa, K., Saha, M., Kwan, C., Moore, C., Gray, H., Laursen, D., Zettler, E.R., Farrington, J.W., Reddy, C.M., Peacock, E.E., Ward, M.W., 2011. Organic micropollutants in marine plastics from the open ocean and remote and urban beaches. Mar. Pollut. Bull. 62, 1683–1692. Hoffman, P., Paller, G., Thybusch, Stingl, U., 1991. Determination of stainless steel constituents in plastics. Fresenius J. Anal. Chem. 339, 230–234. Holmes, L., Turner, A., Thompson, R.C., 2012. Adsorption of trace metals to plastics resin pellets in the marine environment. Environ. Pollut. 160, 42–48. Holmes, L., Turner, A., Thompson, R.C., 2014. Interactions between trace metals and plastic production pellets under estuarine conditions. Mar. Chem. 167, 25–32. Hopewell, J., Dvorak, R., Kosior, E., 2009. Plastics recycling: challenges and opportunities. Philos. Trans. R. Soc. B 364, 2115–2126. Karapanagioti, H.K., Klontza, I., 2008. Testing phenanthrene distribution properties of virgin plastic pellets and plastic eroded pellets found on Lesvos island beaches (Greece). Mar. Environ. Res. 65, 283–290. Karapanagioti, H.K., Endo, S., Ogata, Y., Takada, H., 2010. Diffuse pollution by persistent organic pollutants as measured in plastic pellets sampled from various beaches in Greece. Mar. Pollut. Bull. 62 (2), 312–317. Kim, B.S.M., Salaroli, A.B., Ferreira, P.A.L., Sartoretto, J.R., Mahiques, M.M., Figueira, R.C.L., 2015. Spatial distribution and enrichment assessment of heavy metals in surface sediments from Baixada Santista, Southeastern Brazil. Mar. Pollut. Bull. 103, 333–338. Mahiques, M.M., Figueira, R.C.L., Salaroli, A.B., Alves, D.P.V., Gonçalves, C., 2013. 150 years of anthropogenic metal input in a Biosphere Reserve: the case study of the Cananéia–Iguape coastal system, Southeastern Brazil. Environ. Earth Sci. 68, 1073–1087. Majer, A.P., Vedolin, M.C., Turra, A., 2012. Plastic pellets as oviposition site and means of dispersal for the ocean-skater insect Halobates. Mar. Pollut. Bull. 64, 1143–1147. Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Otake, C., Kaminuma, T., 2001. Plastic resin pellets as a transport medium for toxic chemicals in the marine environment. Environ. Sci. Technol. 35 (2), 318–324. Michaeli, W., 1995. Tecnologia dos Plásticos. Edgard Blucher Ltda, São Paulo. Moore, S.L., Gregorio, D., Carreon, M., Weisberg, S.B., Leecaster, M.K., 2001. Composition and distribution of beach debris in Orange County, California. Mar. Pollut. Bull. 4 (2), 241–245. Moore, C.J., Moore, S.L., Leecaster, M.K., Lattin, G., Zellers, A., 2002. A comparison of neustonic plastic and zooplankton abundance in southern California's coastal waters. Mar. Pollut. Bull. 44, 1035–1038. Moreira, F.T., Balthazar-Silva, D., Barbosa, L., Turra, A., 2016. Revealing accumulation
samples. For the beached group, it would be desirable to monitor the levels in order to avoid a possible increase of heavy metal contents as a consequence of human activities. This can also be associated with content that can create a better condition of accumulation of these elements. The groups observed in MDS analysis can illustrate the location of those groups in the data space and allow for an interpretation of how the individual metals levels are important to this study. Based on the knowledge of field conditions, these groups correspond notably well to the samples, mainly with the virgin pellets. However, our results are only preliminary and there are other issues that need further discussion, such as whether or not the pellets accurately reflect the magnitude of contaminant inputs (Zhang et al., 2015). 4. Conclusions The primary purpose of this study was to show that plastic pellets act as a metal carrier in the marine environment, both virgin and those that are distributed throughout the state of São Paulo. These results provide the first record for this area, furthering the understanding of the occurrence of metals in microplastics. The analysis has shown that metal concentrations can have substantial variability, both within a beach (among samples) and among beaches. The study also reveals that there are local factors such as the presence of anthropogenic activities, which may affect certain regions. Nevertheless, pellet presence is of concern as solid waste in the environment; therefore, environmental monitoring of microplastics must be conducted continually in order to check the impacts of this material and to further our understanding of the problem as a whole. Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2017.10.019. Acknowledgments Financial support for this study was mainly provided by CNPq (157967/2011-5) and technical support from Oceanographic Institute of University of São Paulo (IOUSP). References Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Ashton, K., Holmes, L., Turner, A., 2010. Association of metals with plastic production pellets in the marine environment. Mar. Pollut. Bull. 60, 2050–2055. Barnes, D.K.A., Galagani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and fragmentation of plastic debris in global environments. Philos. Trans. R. Soc. B 364, 1985–1998. Bícego, M.C., Taniguchi, S., Yogui, G.T., Montone, R.C., da Silva, D.A.M., Lourenço, R.A., Martins, C.C., Sasaki, S.T., Pellizari, V.H., Weber, R.R., 2006. Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Mar. Pollut. Bull. 52, 1784–1832. Brennecke, D., Duarte, B., Paiva, F., Caçador, I., Canning- Clode, J., 2016. Microplastics as vector for heavy metal contamination from the marine environment. Estuar. Coast. Shelf Sci. 178, 189–195. Browne, M.A., Galloway, T.S., Thompson, R.C., 2010. Spatial patterns of plastic debris along estuarine shorelines. Environ. Sci. Technol. 44, 3404–3409. Browne, M.A., Niven, S.J., Galloway, T.S., Rowland, S.J., Thompson, R.C., 2013. Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr. Biol. 23, 2388–2392. Carpenter, E.J., Anderson, S.J., Harvey, G.R., Miklas, H.P., Peck, B.B., 1972. Polystyrene spherules in coastal waters. Science 178, 749–750. Claessens, M., De Meester, S., Van Landuyt, L., De Clerk, K., Janssen, C.R., 2011. Occurrence and distribution of microplastic in marine sediment along the Belgian coast. Mar. Pollut. Bull. 62 (10), 2199–2220. Cobelo-Garcia, A., Turner, A., Millward, G.E., 2007. Behaviour of palladium(II), platinum (IV) and rhodium(III) in artificial and natural waters: influence of reactor surface and geochemistry on metal recovery. Anal. Chim. Acta 585, 202–210. Colabuono, F.I., Barquete, V., Domingues, B.S., Montone, R.C., 2009. Plastic ingestion by Procellariiformes in Southern Brazil. Mar. Pollut. Bull. 58, 93–96. Costa, M.F., Ivar do Sul, J.A., Silva- Cavalcanti, J.S., Araújo, M.C.B., Spengler, A., Tourinho, P.S., 2009. On the importance of size of plastic fragments and pellets on the strandline: a snapshot of a Brazilian beach. Environ. Monit. Assess. 168 (1–4),
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