- Email: [email protected]
Adsorption of Cd and Cu to different types of microplastics in estuarine salt marsh medium
Marine Pollution Bulletin xxx (xxxx) xxxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Adsorption of Cd and Cu to different types of microplastics in estuarine salt marsh medium ⁎
C. Marisa R. Almeidaa, , Edite Manjatea,b, Sandra Ramosa a CIMAR/CIIMAR – Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal b Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 687, 4169-007 Porto, Portugal
A R T I C LE I N FO
A B S T R A C T
Keywords: Metals Polyethylene microspheres Fishing line fibers Film plastic bags MPs Bottle cap particles
This study aimed to investigate if microplastics (MPs) type (polyethylene microspheres (mPE), fishing line fibers, film plastic bags MPs and bottle cap particles) and aging affect MPs capacity to sorb Cd or Cu in estuarine salt marsh medium. Tests were carried out in elutriate solution, a simple medium obtained by mixing rhizosediment (sediment in contact with plants roots) with the respective estuarine water, that can be used to simulate watersediment exchanges in estuarine salt marsh environments. After 7 days of exposure, metals adsorption was only detected for film MPs. No differences were observed between virgin and aged MPs. Salinity also did not influence metal adsorption to mPE. Present results indicate that in estuarine salt marsh areas some types of MPs might adsorb metals, which could affect metals availability.
1. Introduction Microplastics, debris with a diameter smaller than 5 mm, normally of plastic, can be produced intentionally, as resin pellets or ingredients for cosmetics, or can be a product of the degradation of larger plastic debris (EU Commission, 2011; Wagner et al., 2014). Their reduced size coupled with the lower density of some types of MPs (e.g. polyethylene and foamed polystyrene), facilitates their widespread transport along the ocean (Avio et al., 2016). MPs have been found in salty waters as well as in beaches (EU Commission, 2011), including those of the Portuguese coast (Antunes et al., 2018). But MPs have been found also in brackish and freshwaters ecosystems such as lakes, rivers and estuaries (Eerkes-Medrano et al., 2015; Wagner et al., 2014; Browne et al., 2010; Rezania et al., 2018; Li et al., 2018; Rodrigues et al., 2019). Several reports indicated that MPs have capacity to adsorb different types of contaminants, such as persistent organic pollutants, xenoestrogens and metals (e.g. Frias et al., 2010; Bakir et al., 2014; Holmes et al., 2014; Koelmans et al., 2016; Brennecke et al., 2016; Wang et al., 2018; Wang et al., 2019), but the adsorption potential can change with MP type. In addition, pollutants adsorption can increase when MPs surface is alter due to environmental dynamic, the so called aging of MPs (Brennecke et al., 2016; Koelmans et al., 2016; Holmes et al., 2014; Kedzierski et al., 2018). Metal adsorption by metals can reduce metal availability and interfere for instance with some ecosystem services provided by estuarine salt marsh environments. For instance, MPs ⁎
adsorption of metals can interfere with salt marsh plant phytoremediation potential as metal might not be available for plant uptake. The main aim of this work was to investigate if MPs physical properties, type and aging, affect MPs interaction with metals in estuarine salt marsh environments. For that, elutriate solutions were used to test MPs potential adsorption of two metals, Cd and Cu. Elutriate solution is a simple medium obtained by mixing sediment with the respective natural water, that can be used to simulate estuarine salt marsh environment, namely exchanges between water and sediment (Almeida et al., 2008). Salt marshes occur on low-energy shorelines, in sheltered environments such as estuaries, and consist of mud or sand flats that retain sediments from inflowing rivers and streams. Both metals and MPs can be retained in these areas. MPs can float in estuarine waters but with water fluctuations they can sink and be trapped within these sediments and interaction between metals and MPs can occur, namely in interstitial water present in these sediments, a medium that can be simulated by elutriate solutions. 2. Materials and methods 2.1. Sampling Sampling was carried out in October 2015, for tests with Cu, and May 2016, for test with Cd, in the estuary of the Lima River, near the city of Viana do Castelo in the NW of Portugal (41° 46′N; 8° 34′W). Both
Corresponding author. E-mail address: [email protected] (C.M.R. Almeida).
https://doi.org/10.1016/j.marpolbul.2019.110797 Received 23 August 2019; Received in revised form 28 November 2019; Accepted 2 December 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: C. Marisa R. Almeida, Edite Manjate and Sandra Ramos, Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110797
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
dried in a lab oven at 30 °C, for 5 days.
estuarine water and sediment were collected. Lima river estuary is subject to some anthropogenic pressures, due to the presence of a cargo port (located at Viana do Castelo), a high population density and several industrial and urban activities, which can lead to the inputs of several contaminants, e.g. metals, hydrocarbons and eventually MPs, that can be retained in the salt marsh areas. No contaminants analysis was carried out at this area at the time of sampling, although this area is considered to have a low pollution level (Gouveia et al., 2018; Rocha et al., 2019).
2.2.1. Impact of salinity on adsorption of metals by mPE To test if salinity could influence the adsorption of Cu or Cd, mPE were suspended in deionized water, doped with Cu or Cd, and containing different concentrations of NaCl (0, 5, 10, 15, 20, 25, 30 and 35 g/l). This is a simple medium where there are no interferences of other compounds. 2.3. Metal levels determinations
2.2. Elutriate preparation and experimental conditions To prevent contamination, all sampling and lab ware materials were soaked in a 20% (v/v) HNO3 solution for at least 24 h, rinsed several times with bi-deionized water (conductivity < 0.1 μS cm−1) and dried in an oven at 30 °C. Suprapure concentrated HNO3, from Merck, was used without further purification. All remaining reagents were pro analysis grade or equivalent. The levels of Cu or Cd in elutriate solutions were determined by atomic absorption spectrophotometry with flame atomization (PU 9200X, Philips), following procedures validated before in the laboratory (Almeida et al., 2004). External calibration with aqueous metal standard solutions was used for quantification. Recovery percentages of solutions doped with known amount of the respective metal varied between 80 and 120%.
Elutriate solutions were prepared accordingly to USEPA protocol (1991), by mixing sediment with estuarine water in a proportion 1:4 and shaking during 30 min in a mechanical shaker (P Selecta-Unitronic OR). Prior to mixing, all detritus were removed from sediments, which were thoroughly homogenized. Solution was left to rest for 12 h and then filtered through cellulose nitrate membranes (0.45 μm, Millipore). Filtration removed suspended particulate matter (except colloids) and decreased the concentration of microorganisms present in solution. In all experiments, elutriate solutions were doped ca. 10 mg/l of Cu or ca. 1 mg/l of Cd. No metal concentration were detected in elutriate solutions before doping. These metal concentrations have been used in previous studies to evaluate salt marsh phytoremediation potential (e.g. Almeida et al., 2008) and in a parallel study to evaluate in the short run the possible effect of the presence of microplastics on metal phytoremediation processes by salt marsh plants (unpublished study). This addition of the metal to the medium simulates also a contamination event in an estuarine area that can occur due to a contaminated river discharge. A concentration of 1500 mg/l MPs was selected based on studies of MPs interactions (e.g. Bakir et al., 2014; Brennecke et al., 2016; Holmes et al., 2014). MPs were added to the elutriate solution doped with Cu or with Cd and all treatments in all experiments were done in triplicate. In all experiments, solution was sampled at days 1, 3 and 7 to determine the dissolved metal levels in the medium along time. The time period of 7 days was chosen aiming to investigate what happens in the immediate when there is an input of contaminated water, contaminated both with microplastics and metals, into an estuarine salt marsh area. Elutriate solution sampled was acidified with 1% concentrated HNO3 and refrigerated at 4 °C until metal analysis. Four types of MPs were used, corresponding to those that are commonly found in the environment, namely: PE microspheres (mPE), MPs fishing line fibers (fibers), MPs of film plastic bags (film) and MPs of bottle caps particles (particles) (Eerkes-Medrano et al., 2015; Wagner et al., 2014). With the exception of PE microspheres, all other MPs were obtained by manually breaking large items of plastics, representing secondary MPs: film plastic bags (Low-density Polyethylene (PE-LD); specific gravity 0.93 g/cm3), bottle caps particles (High-density Polyethylene (PE-HD); 1.37 g/cm3) and fishing line fibers (polyamide (PA); 1.13 g/cm3). The large plastic items were new and have never been exposed to any environmental conditions. The pink PE Microspheres (Low-density Polyethylene microspheres, 1.00 g/cm3 (diameter 850–1000 μm)), representing primary MPs, were used as purchase (from Cospheric Innovations in Microtechnology). For the aging process each type of MP was placed in a beaker with 400 ml of estuarine water and agitated in a mechanical shaker for 2 weeks at a constant velocity of 50 units per minute, to simulate the river water waving in an estuary. In estuarine areas interactions with water suspended particles might cause changes in MPs surface, making them more irregular, which could increase adsorption surface area (Alimi et al., 2018). After the 2 weeks, MPs were washed with deionized water, immersed in 20% (v/v) HNO3 solution for 1 h, washed again with deionized water, and left in deionized water for one day to remove possible adsorbed metals from the estuarine water. Then, MPs were
2.4. Statistical analysis Cu and Cd mean values and respective standard deviation were calculated for each treatment (n = 3). One-way Analysis of Variance (ANOVA) and Tukey pair wise comparisons test was applied (Dell Statistica 13 software) to determine the significance of differences among treatments. 3. Results 3.1. Adsorption of Cu by MPs 3.1.1. Adsorption of Cu by different types of MPs The Cu levels in elutriate solutions showed a decreasing trend along time (Fig. 1A). However, only fibers and film MPs showed significantly higher Cu concentration at day 1 comparing to other days of the experiment (ANOVA fibers: F = 19.404 p = 0.002401; ANOVA film: F = 20.1126 p = 0.0002187). Cu concentration in solution decreased 20% and 35% in the presence of fibers and film MPs, respectively, relatively to control (ANOVA day 1: F = 16.740 p = 0.000198). For day 3 and day 7, only film MPs showed a significantly lower Cu concentration (ca. 55% and 45% reduction, respectively) in solution than control (day 3 ANOVA: F = 3.1114 p = 0.049218; day 7 ANOVA: F = 8.1561 p = 0.003431). 3.1.2. Adsorption of Cu by different types of “aged” MPs Once again Cu concentrations in elutriate solutions decreased along time (Fig. 1B). However, significant decreases were only observed in a few cases: afibers MPs between day 1 and days 3 and 7 (ANOVA afibers: F = 16.369 p = 0.003716); amPE MPs between day 1 and day 7 (ANOVA aPE: F = 32.603 p = 0.000598); afilm MPs among all days (ANOVA afilm: F = 123.310 p = 0.000013). At day 1, Cu concentration in elutriate with afilm MPs was the only one significantly lower than control treatment (ca. 30% reduction) (ANOVA day 1: F = 0.8455 p = 0.527477) (Fig. 3, Fig. 1B). At day 3, afibers, aparticles and afilm solutions showed significantly lower Cu concentrations than control (ANOVA day 3: F = 33.534 p = 0.000009). But at day 7, only afilm MPs showed significantly lower Cu levels (ca. 53%) than control (ANOVA day 7: F = 4.7197 p = 0.021252). The reduction of Cu concentrations in solution were, in general, similar to those observed for MPs not exposed to simulated 2
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
time (Fig. 2B), the only exception being the solution with 20 g/l of NaCl (ANOVA 0 g/l: F = 18 p < 0.05; ANOVA 5 g/l: F = 60 p < 0.05; ANOVA 10 g/l: 13 p < 0.05; ANOVA 15 g/l: F = 41 p < 0.05; ANOVA 25 g/l: F = 81 p < 0.05; ANOVA 30 g/l: F = 20 p < 0.05; ANOVA 35: F = 186 p < 0.05). Small changes occurred among the different NaCl concentrations at each day, with only a few significant increases relatively to control (Fig. 2B) (ANOVA day 3 10 g/l NaCl: F = 14 p < 0.05; ANOVA day 7 10, 15 and 20 NaCl g/l: F = 14 p < 0.05). 4. Discussion 4.1. MPs interaction with Cu Different types of MPs can be found in the environment (EerkesMedrano et al., 2015; Wagner et al., 2014; EU Commission, 2011; Frias et al., 2010), all having distinct characteristics and properties that can condition metal adsorption by MPs. In fact, the affinity would be dependent on polymer and surface properties of the plastics. Some plastics can be originally in MP form, like PE microspheres. But, MPs can result from the breaking of larger plastics items, such as film and particle MPs, which can have very irregular surfaces. So, different types of MPs were tested: fishing line fibers (fibers), film MPs (obtained from thin plastic bags), particle MPs (obtained from bottle caps) and mPE. Tests were carried out with elutriate solution, a matrix more complex and with more compounds than that of river or sea water. Elutriates have, for instance, considerable amounts of colloidal species, such as humic and fulvic acids, which can affect metal interactions. Experiments were designed to evaluate short term effects. Authors intend to investigate what happens in the immediate when there is an input of contaminated water, contaminated both with microplastics and metals, into an estuarine area. As such, microbial interference/influence on metals-MPs interactions was not considered, as elutriate solutions were filtered, reducing significantly the amount of microorganisms present in solution. Therefore, possible microbial degradation of contaminants was not considered. Results showed that only film MPs adsorbed detectable levels of Cu. For the remaining MPs, Cu concentrations in solution were identical to those observed in the control group (without MPs). So, MPs type can lead to different interactions with metals. For instance, Brennecke et al. (2016) observed higher Cu adsorption on polyvinyl chloride fragments than on polystyrene beads. Film MPs have a higher surface of contact than the other types of MPs, which probably favored Cu adsorption. Although adsorption of metals by MPs has been previously reported (Ashton et al., 2010; Holmes et al., 2012, 2014), to our knowledge, the comparison of metal adsorption by different types of MPs had not yet been researched. However, Frias et al. (2010) showed that MPs with different colors adsorbed distinct levels of organic contaminants and Wang et al. (2018) observed higher adsorption of phenantrene by PE fibers than nylon fibers. Plastic aging is another factor that can affect MPs capacity to adsorb metals (Kedzierski et al., 2018). In dynamic and natural conditions MPs are subjected to modifications, namely, erosion, formation of functional groups in MPs surface, adsorption and precipitation of different charged mineral and organic matter, which may result in MPs surface heterogeneity and reactivity (Ashton et al., 2010; Holmes et al., 2012, 2014). Regarding the capability to adsorb Cu, results showed no differences between MPs not exposed and exposed to simulated estuarine conditions. In this study, water fluctuation in estuarine areas, caused by river flow and tide regime, was simulated to “age” the MPs. One should be aware that UV light can also be an aging agent (Cai et al., 2018). In estuarine areas, waters might contain significant amount of suspended particles which can make MPs sink and be less exposed to UV light and therefore, this aging agent was not considered in the present study. These results are contrary to those of Holmes et al. (2014) that observed a higher adsorption of metals, including Cu, in aged MP pellets (which were suspended in harbor water for 8 weeks). The exposition period
Fig. 1. Concentrations of Cu (mean and standard deviation, n = 3) in elutriate solutions doped with Cu (10 mg/l) without (control) and with different types of MPs (A) or of “aged” MPs (B) (MPs at 1500 mg/l) at days 1, 3 and 7 of experiment. For each day, different letters indicate significant differences between control and one MP (p < 0.05).
environmental conditions. 3.1.3. Impact of salinity on adsorption of Cu by mPE The Cu levels in deionized water amended with Cu, mPE and different amounts of NaCl showed, in general, no significant temporal variations and no significant differences among different NaCl concentrations (Fig. 2A). 3.2. Adsorption of Cd by MPs 3.2.1. Adsorption of Cd by different types of MPs The Cd levels in elutriate solutions showed, in general, an increasing trend along time (Fig. 3A). For each day, only a few significant differences were observed, Cd only decreasing significantly in solution with film MPs (ca. 8% reduction) (ANOVA day 1 PE: F = 5.48 p = 0.013354; ANOVA day 3 film: F = 10.15 p = 0.002165; ANOVA day 7 film: F = 15.11 p = 0.000500). 3.2.2. Adsorption of Cd by different types of “aged” MPs The concentrations of Cd in elutriate solution without (control group) MPs and with “aged” MPs (aPE, aparticles, afibers and afilm) (Fig. 3B), in general, did not varied significantly among treatment groups, nor along the experimental time when compared with control group. Results were in general, similar to those observed for MPs not exposed to simulated environmental conditions. 3.2.3. Impact of salinity on adsorption of Cd by mPE In general, Cd concentration within each group decreased along 3
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
Fig. 2. Concentrations of Cu (A) or Cd (B) (mean and standard deviation, n = 3) in deionized water amended with different concentrations of NaCl (0 to 35 g/l) and mPE (1500 mg/l), at days 1, 3 and 7 of experiment. For each day, “a” indicates a value significantly different than the one in solution without NaCl (p < 0.05).
different particle sizes. So, medium and MPs type can influence Cd adsorption.
used in this study was probably not enough to induce pronounced changes on MPs surfaces and more studies are needed with longer aging periods. According to Holmes et al. (2014), salinity can also affect the adsorption of metals by MPs, as beach pellets adsorbed greater amount of trace metals in river water than in sea water. Our results indicate that salinity (simulated by using aqueous solutions with different amounts of NaCl) did not affect significantly Cu adsorption by MPs. In fact, despite some changes over time, probably due to an initial adaptation of Cu to reach equilibrium in the solution (Brennecke et al., 2016; Holmes et al., 2014), no relevant differences in soluble Cu concentration in solution were observed at the end of the experiment. Bakir et al. (2014) also demonstrated that salinity had no influence in the sorption rate of POPs by MPs. However, Bakir et al. (2014) also concluded that sorption of POPs into sediments differed according to the levels of salinity present in the environment, and that an increase of salinity might reduce POPs solubility, making them available to interact with sediments and buried plastics materials. Therefore, salinity may not have a direct impact on metal adsorption but it can influence indirectly MPs capacity to adsorb other contaminants.
5. Conclusions In general, adsorption of metals by MPs was not detected. Significant differences on metal concentrations were only observed in elutriate solutions with film MPs. This might be due to the higher surface area film MPs have relatively to the other types of MPs, which probably allowed a higher adsorption of Cu and Cd. Present results clearly indicate that medium and MP type can affect metal adsorption and more tests should be carried out with other types of MPs. Acknowledgements To Filipa Santos, Bruno Gonçalves e Leonor Ferreira for their help in preparation of elutriate solution for Cd experiments. This research was partially supported by the Strategic Funding UID/Multi/04423/2013 and UID/Multi/04423/2019 through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of PT2020.
4.2. MPs interaction with Cd Authors contribution statement All the experiments carried out with Cu were repeated for Cd. With the exception of film MPs, no adsorption of Cd by MPs was detected, either for virgin or “aged” MPs. These results are in agreement with the observations made by Ashton et al. (2010), with Cd not being detected on the surface of PE pellets suspended in harbor sea water for 8 weeks. On the other hand, as in experiments with Cu, significant differences between Cd concentrations in elutriate solution with or without film MPs were observed. Cd capacity to bound to organic ligands, such as plastic polymers and MPs, has been already documented by some studies (Holmes et al., 2012; EU Commission, 2011) and, for instance, Wang et al. (2019) observed Cd adsorption on high-density PE of
C. Marisa R. Almeida: Conceptualization, Methodology, Validation, Resources, Writing - Review & Editing, Supervision, Funding acquisition; Edite Manjate: Methodology, Formal analysis, Investigation, Writing - Original Draft; Sandra Ramos: Conceptualization, Methodology, Validation, Resources, Writing Review & Editing, Funding acquisition. Declaration of competing interest The authors declare that they have no known competing financial 4
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
Antunes, J., Frias, J., Sobral, P., 2018. Microplastics on the Portuguese coast. Mar. Pollut. Bull. 131, 294–302. Ashton, K., Holmes, L., Turner, A., 2010. Association of metals with plastic production pellets in the marine environment. Mar. Pollut. Bull. 60, 2050–2055. Avio, C.G., Gorbi, S., Regoli, F., 2016. Plastics and microplastics in the oceans: from emerging pollutants to emerged threat. Mar. Environ. Res. 128, 2–11. Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Transport of persistent organic pollutants by microplastics in estuarine conditions. Estuarine Coast. Shelf Sci. 140, 14–21. Brennecke, D., Duarte, B., Paiva, F., Caçador, I., Canning-Clode, J., 2016. Microplastics as vector for heavy metal contamination from the marine environment. Estuarine 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. Cai, L., Wang, J., Peng, J., Wu, Z., Tan, X., 2018. Observation of the degradation of three types of plastic pellets exposed to UV irradiation in three different environments. Sci. Total Environ. 628–629, 740–747. Eerkes-Medrano, D., Thompson, R.C., Aldridge, D.C., 2015. Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res. 75, 63–82. European Commission, 2011. Plastic Waste: Ecological and Human Health Impacts. Science for Environment Policy, Bristol, England. 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. Gouveia, V., Almeida, C.M.R., Almeida, T., Teixeira, C., Mucha, A.P., 2018. Indigenous microbial communities along the NW Portuguese coast: potential for hydrocarbons degradation and relation with sediment contamination. Mar. Pollut. Bull. 131, 620–632. Holmes, L.A., Turner, A., Thompson, R.C., 2012. Adsorption of trace metals to plastic resin pellets in the marine environment. Environ. Pollut. 160, 42–48. Holmes, L.A., Turner, A., Thompson, R.C., 2014. Interactions between trace metals and plastic production pellets under estuarine conditions. Mar. Chem. 167, 25–32. Kedzierski, M., D'Almeida, M., Magueresse, A., Le Grand, A., Duval, H., César, G., Sire, O., Bruzaud, S., Le Tilly, V., 2018. Threat of plastic ageing in marine environment. Adsorption/desorption of micropollutants. Mar. Pollut. Bull. 127, 684–694. Koelmans, A.A., Bakir, A., Burton, G.A., Janssen, C.R., 2016. Microplastic as a vector for chemicals in the aquatic environment: critical review and model-supported reinterpretation of empirical studies. Environ. Sci. Technol. 50, 3315–3326. Li, J., Liu, H., Chen, J., 2018. Microplastics in freshwater systems: a review on occurrence, environmental effects, and methods for microplastics detection. Water Res. 137, 362–374. Rezania, S., Park, J., Din, M.F.M., Taib, S.M., Talaiekhozani, A., Yadav, K.K., Kamyab, H., 2018. Microplastics pollution in different aquatic environments and biota: a review of recent studies. Mar. Pollut. Bull. 133, 191–208. Rocha, F., Rocha, A.C., Baião, L.F., Gadelha, J., Camacho, C., Carvalho, M.L., Arenas, F., Oliveira, A., Maia, M.R.G., Cabrita, A.R., Pintado, M., Nunes, M.L., Almeida, C.M.R., Valente, L.M.P., 2019. Seasonal effect in nutritional quality and safety of the wild sea urchin Paracentrotus lividus harvested in the European Atlantic shores. Food Chem. 282, 84–94. Rodrigues, S.M., Almeida, C.M.R., Silva, D., Cunha, J., Antunes, C., Freitas, V., Ramos, S., 2019. Microplastics contamination in an urban estuary: abundance and distribution of microplastics and fish larvae in the Douro estuary. Sci. Total Environ. 659, 1071–1081. US EPA, 1991. Evaluation of dredged material proposed for ocean disposal. Evaluation 228, 220–228. Wagner, M., Scherer, C., Alvarez-Muñoz, D., Brennholt, N., Bourrain, X., Buchinger, S., Fries, E., Grosbois, C., Klasmeier, J., Marti, T., Rodrigues-Mozaz, S., Urbatzka, R., Vethaak, A.D., Winther-Nielsen, M., Reifferscheid, G., 2014. Microplastics in freshwater ecosystems: what we know and what we need to know. Environ. Sci. Europe 26, 12. Wang, Z., Chen, M., Zhang, L., Wang, K., Yu, X., Zheng, Z., Zheng, R., 2018. Sorption behaviors of phenanthrene on the microplastics identified in a mariculture farm in Xiangshan Bay, southeastern China. Sci. Total Environ. 628–629, 1617–1626. Wang, F., Yang, W., Cheng, P., Zhang, S., Zhang, S., Jiao, W., Sun, Y., 2019. Adsorption characteristics of cadmium onto microplastics from aqueous solutions. Chemosphere 235, 1073–1080.
Fig. 3. Concentrations of Cd (mean and standard deviation, n = 3) in elutriate solutions doped with Cd (10 mg/l) without (control) and with different types of MPs (A) or “aged” MPs (B) (MPs at 1500 mg/l) at days 1, 3 and 7 of experiment. For each day, “a” indicates significant differences between control and one MP (p < 0.05).
interests or personal relationships that could have appeared to influence the work reported in this paper. References Alimi, O.S., Farner Budarz, J., Hernandez, L.M., Tufenkji, N., 2018. Microplastics and nanoplastics in aquatic environments: aggregation, deposition, and enhanced contaminant transport. Environ. Sci. Technol. 52, 1704–1724. Almeida, C.M.R., Mucha, A.P., Vasconcelos, M.T.S., 2004. Influence of the sea rush Juncus maritimus on metal concentration and speciation in estuarine sediment colonized by the plant. Environ. Sci. Technol. 38, 3112–3118. Almeida, C.M.R., Mucha, A.P., Bordalo, A.A., Vasconcelos, M.T.S., 2008. Influence of a salt marsh plant (Halimione portulacoides) on the concentrations and potential mobility of metals in sediments. Sci. Total Environ. 403, 188–195.
5
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Adsorption of Cd and Cu to different types of microplastics in estuarine salt marsh medium ⁎
C. Marisa R. Almeidaa, , Edite Manjatea,b, Sandra Ramosa a CIMAR/CIIMAR – Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal b Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 687, 4169-007 Porto, Portugal
A R T I C LE I N FO
A B S T R A C T
Keywords: Metals Polyethylene microspheres Fishing line fibers Film plastic bags MPs Bottle cap particles
This study aimed to investigate if microplastics (MPs) type (polyethylene microspheres (mPE), fishing line fibers, film plastic bags MPs and bottle cap particles) and aging affect MPs capacity to sorb Cd or Cu in estuarine salt marsh medium. Tests were carried out in elutriate solution, a simple medium obtained by mixing rhizosediment (sediment in contact with plants roots) with the respective estuarine water, that can be used to simulate watersediment exchanges in estuarine salt marsh environments. After 7 days of exposure, metals adsorption was only detected for film MPs. No differences were observed between virgin and aged MPs. Salinity also did not influence metal adsorption to mPE. Present results indicate that in estuarine salt marsh areas some types of MPs might adsorb metals, which could affect metals availability.
1. Introduction Microplastics, debris with a diameter smaller than 5 mm, normally of plastic, can be produced intentionally, as resin pellets or ingredients for cosmetics, or can be a product of the degradation of larger plastic debris (EU Commission, 2011; Wagner et al., 2014). Their reduced size coupled with the lower density of some types of MPs (e.g. polyethylene and foamed polystyrene), facilitates their widespread transport along the ocean (Avio et al., 2016). MPs have been found in salty waters as well as in beaches (EU Commission, 2011), including those of the Portuguese coast (Antunes et al., 2018). But MPs have been found also in brackish and freshwaters ecosystems such as lakes, rivers and estuaries (Eerkes-Medrano et al., 2015; Wagner et al., 2014; Browne et al., 2010; Rezania et al., 2018; Li et al., 2018; Rodrigues et al., 2019). Several reports indicated that MPs have capacity to adsorb different types of contaminants, such as persistent organic pollutants, xenoestrogens and metals (e.g. Frias et al., 2010; Bakir et al., 2014; Holmes et al., 2014; Koelmans et al., 2016; Brennecke et al., 2016; Wang et al., 2018; Wang et al., 2019), but the adsorption potential can change with MP type. In addition, pollutants adsorption can increase when MPs surface is alter due to environmental dynamic, the so called aging of MPs (Brennecke et al., 2016; Koelmans et al., 2016; Holmes et al., 2014; Kedzierski et al., 2018). Metal adsorption by metals can reduce metal availability and interfere for instance with some ecosystem services provided by estuarine salt marsh environments. For instance, MPs ⁎
adsorption of metals can interfere with salt marsh plant phytoremediation potential as metal might not be available for plant uptake. The main aim of this work was to investigate if MPs physical properties, type and aging, affect MPs interaction with metals in estuarine salt marsh environments. For that, elutriate solutions were used to test MPs potential adsorption of two metals, Cd and Cu. Elutriate solution is a simple medium obtained by mixing sediment with the respective natural water, that can be used to simulate estuarine salt marsh environment, namely exchanges between water and sediment (Almeida et al., 2008). Salt marshes occur on low-energy shorelines, in sheltered environments such as estuaries, and consist of mud or sand flats that retain sediments from inflowing rivers and streams. Both metals and MPs can be retained in these areas. MPs can float in estuarine waters but with water fluctuations they can sink and be trapped within these sediments and interaction between metals and MPs can occur, namely in interstitial water present in these sediments, a medium that can be simulated by elutriate solutions. 2. Materials and methods 2.1. Sampling Sampling was carried out in October 2015, for tests with Cu, and May 2016, for test with Cd, in the estuary of the Lima River, near the city of Viana do Castelo in the NW of Portugal (41° 46′N; 8° 34′W). Both
Corresponding author. E-mail address: [email protected] (C.M.R. Almeida).
https://doi.org/10.1016/j.marpolbul.2019.110797 Received 23 August 2019; Received in revised form 28 November 2019; Accepted 2 December 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: C. Marisa R. Almeida, Edite Manjate and Sandra Ramos, Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110797
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
dried in a lab oven at 30 °C, for 5 days.
estuarine water and sediment were collected. Lima river estuary is subject to some anthropogenic pressures, due to the presence of a cargo port (located at Viana do Castelo), a high population density and several industrial and urban activities, which can lead to the inputs of several contaminants, e.g. metals, hydrocarbons and eventually MPs, that can be retained in the salt marsh areas. No contaminants analysis was carried out at this area at the time of sampling, although this area is considered to have a low pollution level (Gouveia et al., 2018; Rocha et al., 2019).
2.2.1. Impact of salinity on adsorption of metals by mPE To test if salinity could influence the adsorption of Cu or Cd, mPE were suspended in deionized water, doped with Cu or Cd, and containing different concentrations of NaCl (0, 5, 10, 15, 20, 25, 30 and 35 g/l). This is a simple medium where there are no interferences of other compounds. 2.3. Metal levels determinations
2.2. Elutriate preparation and experimental conditions To prevent contamination, all sampling and lab ware materials were soaked in a 20% (v/v) HNO3 solution for at least 24 h, rinsed several times with bi-deionized water (conductivity < 0.1 μS cm−1) and dried in an oven at 30 °C. Suprapure concentrated HNO3, from Merck, was used without further purification. All remaining reagents were pro analysis grade or equivalent. The levels of Cu or Cd in elutriate solutions were determined by atomic absorption spectrophotometry with flame atomization (PU 9200X, Philips), following procedures validated before in the laboratory (Almeida et al., 2004). External calibration with aqueous metal standard solutions was used for quantification. Recovery percentages of solutions doped with known amount of the respective metal varied between 80 and 120%.
Elutriate solutions were prepared accordingly to USEPA protocol (1991), by mixing sediment with estuarine water in a proportion 1:4 and shaking during 30 min in a mechanical shaker (P Selecta-Unitronic OR). Prior to mixing, all detritus were removed from sediments, which were thoroughly homogenized. Solution was left to rest for 12 h and then filtered through cellulose nitrate membranes (0.45 μm, Millipore). Filtration removed suspended particulate matter (except colloids) and decreased the concentration of microorganisms present in solution. In all experiments, elutriate solutions were doped ca. 10 mg/l of Cu or ca. 1 mg/l of Cd. No metal concentration were detected in elutriate solutions before doping. These metal concentrations have been used in previous studies to evaluate salt marsh phytoremediation potential (e.g. Almeida et al., 2008) and in a parallel study to evaluate in the short run the possible effect of the presence of microplastics on metal phytoremediation processes by salt marsh plants (unpublished study). This addition of the metal to the medium simulates also a contamination event in an estuarine area that can occur due to a contaminated river discharge. A concentration of 1500 mg/l MPs was selected based on studies of MPs interactions (e.g. Bakir et al., 2014; Brennecke et al., 2016; Holmes et al., 2014). MPs were added to the elutriate solution doped with Cu or with Cd and all treatments in all experiments were done in triplicate. In all experiments, solution was sampled at days 1, 3 and 7 to determine the dissolved metal levels in the medium along time. The time period of 7 days was chosen aiming to investigate what happens in the immediate when there is an input of contaminated water, contaminated both with microplastics and metals, into an estuarine salt marsh area. Elutriate solution sampled was acidified with 1% concentrated HNO3 and refrigerated at 4 °C until metal analysis. Four types of MPs were used, corresponding to those that are commonly found in the environment, namely: PE microspheres (mPE), MPs fishing line fibers (fibers), MPs of film plastic bags (film) and MPs of bottle caps particles (particles) (Eerkes-Medrano et al., 2015; Wagner et al., 2014). With the exception of PE microspheres, all other MPs were obtained by manually breaking large items of plastics, representing secondary MPs: film plastic bags (Low-density Polyethylene (PE-LD); specific gravity 0.93 g/cm3), bottle caps particles (High-density Polyethylene (PE-HD); 1.37 g/cm3) and fishing line fibers (polyamide (PA); 1.13 g/cm3). The large plastic items were new and have never been exposed to any environmental conditions. The pink PE Microspheres (Low-density Polyethylene microspheres, 1.00 g/cm3 (diameter 850–1000 μm)), representing primary MPs, were used as purchase (from Cospheric Innovations in Microtechnology). For the aging process each type of MP was placed in a beaker with 400 ml of estuarine water and agitated in a mechanical shaker for 2 weeks at a constant velocity of 50 units per minute, to simulate the river water waving in an estuary. In estuarine areas interactions with water suspended particles might cause changes in MPs surface, making them more irregular, which could increase adsorption surface area (Alimi et al., 2018). After the 2 weeks, MPs were washed with deionized water, immersed in 20% (v/v) HNO3 solution for 1 h, washed again with deionized water, and left in deionized water for one day to remove possible adsorbed metals from the estuarine water. Then, MPs were
2.4. Statistical analysis Cu and Cd mean values and respective standard deviation were calculated for each treatment (n = 3). One-way Analysis of Variance (ANOVA) and Tukey pair wise comparisons test was applied (Dell Statistica 13 software) to determine the significance of differences among treatments. 3. Results 3.1. Adsorption of Cu by MPs 3.1.1. Adsorption of Cu by different types of MPs The Cu levels in elutriate solutions showed a decreasing trend along time (Fig. 1A). However, only fibers and film MPs showed significantly higher Cu concentration at day 1 comparing to other days of the experiment (ANOVA fibers: F = 19.404 p = 0.002401; ANOVA film: F = 20.1126 p = 0.0002187). Cu concentration in solution decreased 20% and 35% in the presence of fibers and film MPs, respectively, relatively to control (ANOVA day 1: F = 16.740 p = 0.000198). For day 3 and day 7, only film MPs showed a significantly lower Cu concentration (ca. 55% and 45% reduction, respectively) in solution than control (day 3 ANOVA: F = 3.1114 p = 0.049218; day 7 ANOVA: F = 8.1561 p = 0.003431). 3.1.2. Adsorption of Cu by different types of “aged” MPs Once again Cu concentrations in elutriate solutions decreased along time (Fig. 1B). However, significant decreases were only observed in a few cases: afibers MPs between day 1 and days 3 and 7 (ANOVA afibers: F = 16.369 p = 0.003716); amPE MPs between day 1 and day 7 (ANOVA aPE: F = 32.603 p = 0.000598); afilm MPs among all days (ANOVA afilm: F = 123.310 p = 0.000013). At day 1, Cu concentration in elutriate with afilm MPs was the only one significantly lower than control treatment (ca. 30% reduction) (ANOVA day 1: F = 0.8455 p = 0.527477) (Fig. 3, Fig. 1B). At day 3, afibers, aparticles and afilm solutions showed significantly lower Cu concentrations than control (ANOVA day 3: F = 33.534 p = 0.000009). But at day 7, only afilm MPs showed significantly lower Cu levels (ca. 53%) than control (ANOVA day 7: F = 4.7197 p = 0.021252). The reduction of Cu concentrations in solution were, in general, similar to those observed for MPs not exposed to simulated 2
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
time (Fig. 2B), the only exception being the solution with 20 g/l of NaCl (ANOVA 0 g/l: F = 18 p < 0.05; ANOVA 5 g/l: F = 60 p < 0.05; ANOVA 10 g/l: 13 p < 0.05; ANOVA 15 g/l: F = 41 p < 0.05; ANOVA 25 g/l: F = 81 p < 0.05; ANOVA 30 g/l: F = 20 p < 0.05; ANOVA 35: F = 186 p < 0.05). Small changes occurred among the different NaCl concentrations at each day, with only a few significant increases relatively to control (Fig. 2B) (ANOVA day 3 10 g/l NaCl: F = 14 p < 0.05; ANOVA day 7 10, 15 and 20 NaCl g/l: F = 14 p < 0.05). 4. Discussion 4.1. MPs interaction with Cu Different types of MPs can be found in the environment (EerkesMedrano et al., 2015; Wagner et al., 2014; EU Commission, 2011; Frias et al., 2010), all having distinct characteristics and properties that can condition metal adsorption by MPs. In fact, the affinity would be dependent on polymer and surface properties of the plastics. Some plastics can be originally in MP form, like PE microspheres. But, MPs can result from the breaking of larger plastics items, such as film and particle MPs, which can have very irregular surfaces. So, different types of MPs were tested: fishing line fibers (fibers), film MPs (obtained from thin plastic bags), particle MPs (obtained from bottle caps) and mPE. Tests were carried out with elutriate solution, a matrix more complex and with more compounds than that of river or sea water. Elutriates have, for instance, considerable amounts of colloidal species, such as humic and fulvic acids, which can affect metal interactions. Experiments were designed to evaluate short term effects. Authors intend to investigate what happens in the immediate when there is an input of contaminated water, contaminated both with microplastics and metals, into an estuarine area. As such, microbial interference/influence on metals-MPs interactions was not considered, as elutriate solutions were filtered, reducing significantly the amount of microorganisms present in solution. Therefore, possible microbial degradation of contaminants was not considered. Results showed that only film MPs adsorbed detectable levels of Cu. For the remaining MPs, Cu concentrations in solution were identical to those observed in the control group (without MPs). So, MPs type can lead to different interactions with metals. For instance, Brennecke et al. (2016) observed higher Cu adsorption on polyvinyl chloride fragments than on polystyrene beads. Film MPs have a higher surface of contact than the other types of MPs, which probably favored Cu adsorption. Although adsorption of metals by MPs has been previously reported (Ashton et al., 2010; Holmes et al., 2012, 2014), to our knowledge, the comparison of metal adsorption by different types of MPs had not yet been researched. However, Frias et al. (2010) showed that MPs with different colors adsorbed distinct levels of organic contaminants and Wang et al. (2018) observed higher adsorption of phenantrene by PE fibers than nylon fibers. Plastic aging is another factor that can affect MPs capacity to adsorb metals (Kedzierski et al., 2018). In dynamic and natural conditions MPs are subjected to modifications, namely, erosion, formation of functional groups in MPs surface, adsorption and precipitation of different charged mineral and organic matter, which may result in MPs surface heterogeneity and reactivity (Ashton et al., 2010; Holmes et al., 2012, 2014). Regarding the capability to adsorb Cu, results showed no differences between MPs not exposed and exposed to simulated estuarine conditions. In this study, water fluctuation in estuarine areas, caused by river flow and tide regime, was simulated to “age” the MPs. One should be aware that UV light can also be an aging agent (Cai et al., 2018). In estuarine areas, waters might contain significant amount of suspended particles which can make MPs sink and be less exposed to UV light and therefore, this aging agent was not considered in the present study. These results are contrary to those of Holmes et al. (2014) that observed a higher adsorption of metals, including Cu, in aged MP pellets (which were suspended in harbor water for 8 weeks). The exposition period
Fig. 1. Concentrations of Cu (mean and standard deviation, n = 3) in elutriate solutions doped with Cu (10 mg/l) without (control) and with different types of MPs (A) or of “aged” MPs (B) (MPs at 1500 mg/l) at days 1, 3 and 7 of experiment. For each day, different letters indicate significant differences between control and one MP (p < 0.05).
environmental conditions. 3.1.3. Impact of salinity on adsorption of Cu by mPE The Cu levels in deionized water amended with Cu, mPE and different amounts of NaCl showed, in general, no significant temporal variations and no significant differences among different NaCl concentrations (Fig. 2A). 3.2. Adsorption of Cd by MPs 3.2.1. Adsorption of Cd by different types of MPs The Cd levels in elutriate solutions showed, in general, an increasing trend along time (Fig. 3A). For each day, only a few significant differences were observed, Cd only decreasing significantly in solution with film MPs (ca. 8% reduction) (ANOVA day 1 PE: F = 5.48 p = 0.013354; ANOVA day 3 film: F = 10.15 p = 0.002165; ANOVA day 7 film: F = 15.11 p = 0.000500). 3.2.2. Adsorption of Cd by different types of “aged” MPs The concentrations of Cd in elutriate solution without (control group) MPs and with “aged” MPs (aPE, aparticles, afibers and afilm) (Fig. 3B), in general, did not varied significantly among treatment groups, nor along the experimental time when compared with control group. Results were in general, similar to those observed for MPs not exposed to simulated environmental conditions. 3.2.3. Impact of salinity on adsorption of Cd by mPE In general, Cd concentration within each group decreased along 3
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
Fig. 2. Concentrations of Cu (A) or Cd (B) (mean and standard deviation, n = 3) in deionized water amended with different concentrations of NaCl (0 to 35 g/l) and mPE (1500 mg/l), at days 1, 3 and 7 of experiment. For each day, “a” indicates a value significantly different than the one in solution without NaCl (p < 0.05).
different particle sizes. So, medium and MPs type can influence Cd adsorption.
used in this study was probably not enough to induce pronounced changes on MPs surfaces and more studies are needed with longer aging periods. According to Holmes et al. (2014), salinity can also affect the adsorption of metals by MPs, as beach pellets adsorbed greater amount of trace metals in river water than in sea water. Our results indicate that salinity (simulated by using aqueous solutions with different amounts of NaCl) did not affect significantly Cu adsorption by MPs. In fact, despite some changes over time, probably due to an initial adaptation of Cu to reach equilibrium in the solution (Brennecke et al., 2016; Holmes et al., 2014), no relevant differences in soluble Cu concentration in solution were observed at the end of the experiment. Bakir et al. (2014) also demonstrated that salinity had no influence in the sorption rate of POPs by MPs. However, Bakir et al. (2014) also concluded that sorption of POPs into sediments differed according to the levels of salinity present in the environment, and that an increase of salinity might reduce POPs solubility, making them available to interact with sediments and buried plastics materials. Therefore, salinity may not have a direct impact on metal adsorption but it can influence indirectly MPs capacity to adsorb other contaminants.
5. Conclusions In general, adsorption of metals by MPs was not detected. Significant differences on metal concentrations were only observed in elutriate solutions with film MPs. This might be due to the higher surface area film MPs have relatively to the other types of MPs, which probably allowed a higher adsorption of Cu and Cd. Present results clearly indicate that medium and MP type can affect metal adsorption and more tests should be carried out with other types of MPs. Acknowledgements To Filipa Santos, Bruno Gonçalves e Leonor Ferreira for their help in preparation of elutriate solution for Cd experiments. This research was partially supported by the Strategic Funding UID/Multi/04423/2013 and UID/Multi/04423/2019 through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of PT2020.
4.2. MPs interaction with Cd Authors contribution statement All the experiments carried out with Cu were repeated for Cd. With the exception of film MPs, no adsorption of Cd by MPs was detected, either for virgin or “aged” MPs. These results are in agreement with the observations made by Ashton et al. (2010), with Cd not being detected on the surface of PE pellets suspended in harbor sea water for 8 weeks. On the other hand, as in experiments with Cu, significant differences between Cd concentrations in elutriate solution with or without film MPs were observed. Cd capacity to bound to organic ligands, such as plastic polymers and MPs, has been already documented by some studies (Holmes et al., 2012; EU Commission, 2011) and, for instance, Wang et al. (2019) observed Cd adsorption on high-density PE of
C. Marisa R. Almeida: Conceptualization, Methodology, Validation, Resources, Writing - Review & Editing, Supervision, Funding acquisition; Edite Manjate: Methodology, Formal analysis, Investigation, Writing - Original Draft; Sandra Ramos: Conceptualization, Methodology, Validation, Resources, Writing Review & Editing, Funding acquisition. Declaration of competing interest The authors declare that they have no known competing financial 4
Marine Pollution Bulletin xxx (xxxx) xxxx
C.M.R. Almeida, et al.
Antunes, J., Frias, J., Sobral, P., 2018. Microplastics on the Portuguese coast. Mar. Pollut. Bull. 131, 294–302. Ashton, K., Holmes, L., Turner, A., 2010. Association of metals with plastic production pellets in the marine environment. Mar. Pollut. Bull. 60, 2050–2055. Avio, C.G., Gorbi, S., Regoli, F., 2016. Plastics and microplastics in the oceans: from emerging pollutants to emerged threat. Mar. Environ. Res. 128, 2–11. Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Transport of persistent organic pollutants by microplastics in estuarine conditions. Estuarine Coast. Shelf Sci. 140, 14–21. Brennecke, D., Duarte, B., Paiva, F., Caçador, I., Canning-Clode, J., 2016. Microplastics as vector for heavy metal contamination from the marine environment. Estuarine 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. Cai, L., Wang, J., Peng, J., Wu, Z., Tan, X., 2018. Observation of the degradation of three types of plastic pellets exposed to UV irradiation in three different environments. Sci. Total Environ. 628–629, 740–747. Eerkes-Medrano, D., Thompson, R.C., Aldridge, D.C., 2015. Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res. 75, 63–82. European Commission, 2011. Plastic Waste: Ecological and Human Health Impacts. Science for Environment Policy, Bristol, England. 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. Gouveia, V., Almeida, C.M.R., Almeida, T., Teixeira, C., Mucha, A.P., 2018. Indigenous microbial communities along the NW Portuguese coast: potential for hydrocarbons degradation and relation with sediment contamination. Mar. Pollut. Bull. 131, 620–632. Holmes, L.A., Turner, A., Thompson, R.C., 2012. Adsorption of trace metals to plastic resin pellets in the marine environment. Environ. Pollut. 160, 42–48. Holmes, L.A., Turner, A., Thompson, R.C., 2014. Interactions between trace metals and plastic production pellets under estuarine conditions. Mar. Chem. 167, 25–32. Kedzierski, M., D'Almeida, M., Magueresse, A., Le Grand, A., Duval, H., César, G., Sire, O., Bruzaud, S., Le Tilly, V., 2018. Threat of plastic ageing in marine environment. Adsorption/desorption of micropollutants. Mar. Pollut. Bull. 127, 684–694. Koelmans, A.A., Bakir, A., Burton, G.A., Janssen, C.R., 2016. Microplastic as a vector for chemicals in the aquatic environment: critical review and model-supported reinterpretation of empirical studies. Environ. Sci. Technol. 50, 3315–3326. Li, J., Liu, H., Chen, J., 2018. Microplastics in freshwater systems: a review on occurrence, environmental effects, and methods for microplastics detection. Water Res. 137, 362–374. Rezania, S., Park, J., Din, M.F.M., Taib, S.M., Talaiekhozani, A., Yadav, K.K., Kamyab, H., 2018. Microplastics pollution in different aquatic environments and biota: a review of recent studies. Mar. Pollut. Bull. 133, 191–208. Rocha, F., Rocha, A.C., Baião, L.F., Gadelha, J., Camacho, C., Carvalho, M.L., Arenas, F., Oliveira, A., Maia, M.R.G., Cabrita, A.R., Pintado, M., Nunes, M.L., Almeida, C.M.R., Valente, L.M.P., 2019. Seasonal effect in nutritional quality and safety of the wild sea urchin Paracentrotus lividus harvested in the European Atlantic shores. Food Chem. 282, 84–94. Rodrigues, S.M., Almeida, C.M.R., Silva, D., Cunha, J., Antunes, C., Freitas, V., Ramos, S., 2019. Microplastics contamination in an urban estuary: abundance and distribution of microplastics and fish larvae in the Douro estuary. Sci. Total Environ. 659, 1071–1081. US EPA, 1991. Evaluation of dredged material proposed for ocean disposal. Evaluation 228, 220–228. Wagner, M., Scherer, C., Alvarez-Muñoz, D., Brennholt, N., Bourrain, X., Buchinger, S., Fries, E., Grosbois, C., Klasmeier, J., Marti, T., Rodrigues-Mozaz, S., Urbatzka, R., Vethaak, A.D., Winther-Nielsen, M., Reifferscheid, G., 2014. Microplastics in freshwater ecosystems: what we know and what we need to know. Environ. Sci. Europe 26, 12. Wang, Z., Chen, M., Zhang, L., Wang, K., Yu, X., Zheng, Z., Zheng, R., 2018. Sorption behaviors of phenanthrene on the microplastics identified in a mariculture farm in Xiangshan Bay, southeastern China. Sci. Total Environ. 628–629, 1617–1626. Wang, F., Yang, W., Cheng, P., Zhang, S., Zhang, S., Jiao, W., Sun, Y., 2019. Adsorption characteristics of cadmium onto microplastics from aqueous solutions. Chemosphere 235, 1073–1080.
Fig. 3. Concentrations of Cd (mean and standard deviation, n = 3) in elutriate solutions doped with Cd (10 mg/l) without (control) and with different types of MPs (A) or “aged” MPs (B) (MPs at 1500 mg/l) at days 1, 3 and 7 of experiment. For each day, “a” indicates significant differences between control and one MP (p < 0.05).
interests or personal relationships that could have appeared to influence the work reported in this paper. References Alimi, O.S., Farner Budarz, J., Hernandez, L.M., Tufenkji, N., 2018. Microplastics and nanoplastics in aquatic environments: aggregation, deposition, and enhanced contaminant transport. Environ. Sci. Technol. 52, 1704–1724. Almeida, C.M.R., Mucha, A.P., Vasconcelos, M.T.S., 2004. Influence of the sea rush Juncus maritimus on metal concentration and speciation in estuarine sediment colonized by the plant. Environ. Sci. Technol. 38, 3112–3118. Almeida, C.M.R., Mucha, A.P., Bordalo, A.A., Vasconcelos, M.T.S., 2008. Influence of a salt marsh plant (Halimione portulacoides) on the concentrations and potential mobility of metals in sediments. Sci. Total Environ. 403, 188–195.
5