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Heavy metals contamination of sedimentary microplastics in Hong Kong
Marine Pollution Bulletin 153 (2020) 110977
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Heavy metals contamination of sedimentary microplastics in Hong Kong a,1
a,1
a
b
a
Wenjie Li , Hoi-Shing Lo , Ho-Man Wong , Man Zhou , Chun-Yuen Wong , ⁎ Nora Fung-Yee Tama, Siu-Gin Cheunga,c, a b c
T
Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region Research Institute for Environmental Innovation (Suzhou), Tsinghua, RIET, Jinfeng Road, Suzhou, China State Key Laboratory of Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region
ARTICLE INFO
ABSTRACT
Keywords: Heavy metals Microplastic Marine debris
This is the first study of heavy metals (As, Zn, Cd, Ni, Fe, Mn, Cu) contamination of microplastics on sandy beaches in Hong Kong. Three study sites are located in the eastern waters (Pak Lap Wan, Stanley Bay, Tung Lung Chau) and the other three in the western waters (Tai Pai Tsui, Ha Pak Nai, Shui Hau Wan). The three most abundant types of microplastics were polyethylene (42.2%), polypropylene (23.3%) and polystyrene (19.5%). The median concentration of Fe (302 mg kg−1) was the highest and followed by Zn (19.6 mg kg−1) and Mn (18.6 mg kg−1). Very low concentrations of Cu (0.89 mg kg−1), Ni (0.15 mg kg−1), As (< LOD) and Cd (< LOD) were measured. The western sites have significantly higher concentrations of Ni, Fe, Mn and Cu than the eastern sites, indicating that Pearl River was likely to be a major source of heavy metals on microplastics. In view of a continual increase in the abundance of microplastics in the marine environment and its potential impacts on marine organisms, immediate actions should be taken in establishing long term monitoring programs for heavy metals associated with microplastics. In-depth research on the mechanisms of adsorption and desorption processes between metals and microplastics will help assess the associated risks to both human health and the environment.
1. Introduction Microplastics are smaller pieces of plastic with a diameter < 5 mm. Primary microplastics are produced to serve specific purposes such as fibers for clothing and nurdles for manufacturing of plastic products whereas secondary microplastics are produced from natural breakdown of larger plastic products. Because of their small size and light weight, they are carried by water or air to almost everywhere on earth (Thompson et al., 2004; Allen et al., 2019). By 2018, microplastics have been found in > 114 aquatic species (https://www.britannica.com/ technology/microplastic). Studies have shown that different kinds of organisms, such as zooplankton, benthic invertebrates, bivalves, fish and large marine mammals, can ingest microplastics as food (Cole et al., 2013; Van Cauwenberghe and Janssen, 2014; Li et al., 2016; Güven et al., 2017; McGoran et al., 2017; Steer et al., 2017). Ingestion of microplastics by marine animals blocks food passages, resulting in false satiety, hence reduces the energy and nutrient intake and causes death (Andrady, 2011). The harmful effects of microplastics on marine animals can also be due to contaminants adsorbed on the surface of microplastics. Due to
their large specific surface area and hydrophobic characteristics, microplastics can accumulate high concentrations of POPs and heavy metals in the marine environment, such as polychlorinated biphenyls (PCBs) (Mato et al., 2001), dichlorodiphenyltrichloroethane (DDT) (Frias et al., 2010), hydrocarbons (HCs) (Hirai et al., 2011; Van et al., 2012; Lo et al., 2019) and heavy metals (Ashton et al., 2010; Holmes et al., 2012). Microplastics may be inadvertently ingested by marine organisms (Mrosovsky et al., 2009; Sleight et al., 2017) and seabirds (Auman et al., 1997), and the heavy metal contaminants carried by these microplastics may be released in the acidic digestive tract of animals (Ashton et al., 2010; Holmes et al., 2014; Sleight et al., 2017). Since the accumulation of heavy metals in plastic particles can have potential negative effects on marine organisms, there is an urgency to develop monitoring programs for heavy metals in microplastics in the marine environment. The main anthropogenic sources of heavy metals in the marine environment are industrial and municipal wastewater, sewage discharges, agricultural runoff, and antifouling coatings in ports, docks and ships (Yeats, 2010). The adsorption of heavy metals on microplastics occurs through complex mechanisms (Brennecke et al., 2016).
Corresponding author at: Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region. E-mail address: [email protected] (S.-G. Cheung). 1 These authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.marpolbul.2020.110977 Received 19 August 2019; Received in revised form 10 February 2020; Accepted 10 February 2020 Available online 14 February 2020 0025-326X/ © 2020 Elsevier Ltd. All rights reserved.
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Major heavy metal elements that pollute the ocean include mercury, cadmium, lead, zinc, chromium, and copper. They enter the aquatic system, and are transferred and accumulated through physical, chemical and biological migrations. Inorganic minerals and organic compounds precipitate on the surface of plastic particles, leading to the change of their surface properties and the formation of various active binding sites of metal ions (Ashton et al., 2010; Holmes et al., 2014; Rochman et al., 2014). Holmes et al. (2012) reported that plastic pellets could be an important vehicle for the transport of metals in the marine environment because microplastics could be transported for considerable distances while buoyant. The adsorption of heavy metals to plastic pellets is metal specific with Cd, Co, Ni and Pb increasing whereas Cr(V(I) decreasing adsorption with increasing pH and decreasing salinity. Weathering of plastics further facilitates the metal adsorption (Holmes et al., 2012). A field experiment has demonstrated strong correlations between adsorbability of PP and PVC towards Pb and Mn, and the concentration of these metals in seawater (Gao et al., 2019). Routine water quality monitoring in Hong Kong is conducted by the Environmental Protection Department (EPD) with > 60 physical, chemical and biological parameters measured for sediment samples taken from various sites in ten water control zones around Hong Kong. Since the implementation of the marine monitoring programme in 1986, heavy metals such as copper and silver have been detected in Victoria Harbour and Tsuen Wan, probably due to industrial pollution emissions during the 1960s and 1980s before the introduction of pollution control. The feasibility of using barnacles and mussels as biomonitors of heavy metals contamination in Hong Kong was reported upon by Phillips and Rainbow
(1988). Blackmore (2001) determined the cumulative concentrations of cadmium, copper and zinc in the bodies of 19 species of intertidal invertebrates from two coasts of a relatively uncontaminated area in Hong Kong, the Cape d'Aguilar marine reserve. In general, the concentrations of metals in the body could be explained by the accumulation strategies and physiological requirements of the analyzed organisms. The first study of microplastic pollution in Hong Kong was published by Fok and Cheung (2015) which has demonstrated regional differences in the pollution level with higher concentrations of microplastics being collected on sandy beaches in the western waters than eastern waters, probably due to the input of Pearl River, the third longest river in China, of which the estuary is located in the western side of Hong Kong. In this study, we had collected microplastics from six shores in Hong Kong with three of them located in the western waters and the others in the eastern waters. Chemical compositions of the microplastics and concentrations of seven metals (As, Zn, Cd, Ni, Fe, Mn, Cu) on the microplastics were determined to understand the spatial variations of heavy metals contamination of microplastics in Hong Kong waters. 2. Materials and methods 2.1. Sampling of microplastics The sampling was conducted in the dry season between November and December 2018 at six sites, namely Pak Lap Wan (PL), Stanley Bay (SB) and Tung Lung Chau (TLC) in the eastern waters, and Shui Hau (SH), Tai Pai Tsui (TPT) and Ha Pak Nai (HPN) in the western waters (Fig. 1). Sediment for microplastic characterization was collected from
Fig. 1. Geographic location of Hong Kong and sampling sites in this study. Three study sites are located in the eastern waters: Pak Lap Wan (PL), Stanley Bay (SB), and Tung Lung Chau (TLC), and the remaining sites in the western waters: Tai Pai Tsui (TPT), Ha Pak Nai (HPN) and Shui Hau (SH). 2
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a quadrat (0.25 m × 0.25 m) using a stainless steel shovel to a depth of 2–3 cm along the strandline during low tide and five replicates were collected at 3–5 m intervals (depending on the shore length). Microplastics were extracted in-situ by transferring the sediment to a bucket filled with ambient seawater. Particles floating on the water surface were collected and passed through a sieve with a pore size of 0.5 mm. Particles retained on the sieves were rinsed and stored in plastic tubes. Particles larger than 5 mm were removed and the remaining particles were within a size range of 0.5–5 mm. These microplastics were characterized by FTIR later. For heavy metals quantification, microplastics of the size of approximately 5 mm were identified by naked eyes and hand-picked. This was to prevent metal contamination of the microplastics by the stainless steel shovel and sieves. Further precautions included wearing laboratory latex gloves and cotton clothing during sampling. Over 100 pieces of microplastics of different sizes, colours, shapes and other physical properties were collected for each replicate, and there were 5 replicates for each site. The samples were put in sealed plastic bags and transported to the laboratory immediately and stored in a freezer at −20 °C for further analysis.
Table 1 Detection limits of the ICP-OES for different metals and the recovery rate of metals from oyster tissue as standard reference material. Metal
Detection limit of ICP-OES (ml L−1)
Recovery rate (%)
As Cd Cu Fe Mn Ni Zn
0.00828 0.00063 0.00153 0.00174 0.00315 0.00201 0.00168
139 108 120 85 111 126 89
Plasma Atomic Emission Spectrometer (PE optima 6000)). The recovery rate and limit of detection are listed in Table 1. The glassware were washed with tap water, rinsed with deionized water, dipped in detergent for 24 h and rewashed with deionized water. They were then put in an acid bath with 25% HNO3 for 24 h, and rinsed with deionized water followed by Milli-Q. 2.4. Statistical analysis
2.2. Chemical composition of microplastics
Statistical analyses were performed using R and SPSS 22. Prior to analysis, data were tested for normality and homogeneity of variance using Shapiro-Wilk test and Levene's test, respectively. As the above tests for statistical assumptions failed even after data transformation, the nonparametric Kruskal-Wallis test was used in combination with Mann-Whitney U test (statistical significance level: 0.05) for comparing the concentrations of individual heavy metals among study sites and between geographical regions. The relationships between polymer compositions and metal concentrations were analyzed using Pearson correlation coefficient.
The samples were freeze-dried for 48 h. After removal of impurities, selected microplastics were examined under a microscope with a magnification of 7.3× − 120× (M165C, Leica Microsystems). According to the criteria established by Free et al. (2014) and McCormick et al. (2014), microplastics were identified by their shape, colour and surface texture, and were categorized into five classes, namely “pellet”, “fragment”, “fiber”, “foam” and “film”. Thirty pieces of microplastics were selected randomly from the samples at each study site, or 180 pieces of microplastics from all the sites, and examined using Fourier Transform Infrared (FTIR) spectroscopic analysis (Nicolet iS50 equipped with a built-in iS50 ATR module, Thermo Scientific, WI, USA). The obtained spectra were compared with the reference spectra in the Hummel polymer library, and only a matching of > 70% was accepted. The microplastics were identified successfully as polyethylene (PE), polypropylene (PP), polystyrene (PS), polyvinyl chloride (PVC), polyester (PET), polyamide (PA) or others including acrylonitrile butadiene styrene (ABS), polyether urethane (PEUT), cellulose acetate (CA) and unknown particles that were not found in the Hummel Polymer Library.
3. Results 3.1. Heavy metals contamination of microplastics Median concentrations of heavy metals in microplastics are shown in Table 2. The concentration of Fe was much higher than that of all the other metals (Mann–Whitney U test, p < 0.05). Concentrations of Mn and Zn were not significantly different from each other but they were all significantly higher than that of Cu, Ni, As and Cd (Mann–Whitney U test, p < 0.05). There was no significant regional difference between western shores and eastern shores for As, Zn, and Cd, but the western shores had significantly higher concentrations of Fe, Ni, Mn and Cu (Mann-Whitney U test, p < 0.05) (Table 3). The greatest regional difference was found in Cu with that in the western shores being 8 times that in the eastern shores. Differences in Fe, Mn and Ni between the two regions varied between 3 times and 5 times.
2.3. Heavy metal analysis The microplastic samples were dried in a desiccator for 48 h to prevent the loss of metals. Each replicate was weighted to the nearest 0.001 g in a glass container, and subsequently suspended in 20 mL of 20% aqua regia (1:3 HNO3:HCl). The suspension was shaken at 150 rpm overnight at room temperature to desorb heavy metals. The resulting liquid was filtered through a 0.45 μm acid washed membrane filter (MiliPore) to remove fine particles. The filtrate was then made up to 25 mL using MiliQ water for metal analysis. This metal extraction method could prevent clogging of polymers in the ICP-OES during injection. Blank tests were prepared following the same procedure but without the microplastic samples to determine the background contamination. Five replicates and two blank solutions were prepared for each study site. The recovery efficiency of the digestion process was checked using oyster tissue (0.0902 g) as a standard reference material because there was no commercially available standard reference microplastics for heavy metals determination. Considering that the microplastics has been freeze-dried and treated by sonication, oyster tissue was selected as a standard reference material because the processing procedures were similar. Concentrations of heavy metals in the solution were determined using a quadrupole ICP-OES (Inductively Coupled
Table 2 Median concentrations of heavy metals in microplastics collected from six study sites in Hong Kong. Values are expressed as medians ± median absolute deviation.
As Cd Cu Fe Mn Ni Zn
Concentration (mg kg−1)
Groupinga
0.00 ± 0.00 (< LOD) 0.00 ± 0.00 (< LOD) 0.89 ± 0.89 302 ± 224 18.6 ± 12.7 0.15 ± 0.13 19.6 ± 11.4
A AB C E D B D
a Different letters indicate significant differences among the sampling sites at the level of p < 0.05 according to Kruskal–Wallis test and Mann–Whitney U test. < LOD indicates below detection limits.
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detected in the river water, riverbed sediment and estuarine sediment in Pearl River Estuary and its tributaries (Fan et al., 2019). Since Pearl River is one of the major sources of microplastics in the western waters of Hong Kong (Fok and Cheung, 2015; Cheung et al., 2016), this helps explain why microplastics collected at HPN contained high concentrations of heavy metals especially for Cu, Fe, Ni, and Mn because the concentrations of these metals were also significantly higher in the sediments in this region (EPD, 2017). On the other hand, there were no significant regional differences for As, Cd and Zn. A recent study has reported that Cd and Zn have been used as heat stabilizers and slip agents for plastic materials and could comprise up to 3% of the polymer composition (Hahladakis et al., 2018). Therefore, Cd and Zn are not pollutants but rather additives of microplastics, hence no regional differences in their concentrations were observed. The concentration of As in microplastics was < LOD at all the study sites. An earlier study in Hong Kong (Cheung and Wong, 1992) also showed that As content in sediment was very low when compared with Cu, Cd and Cr, and there was no specific pollution source of As in Hong Kong because As is usually derived from natural sources. Similar findings were reported upon by Turner (2016) for beached litter collected in SW England where the concentration of As was always the lowest when compared with other metals. Pearl River as a major source of heavy metals in microplastics was further supported by significantly lower concentrations of Ni, Fe, Mn and Cu at the sites in the eastern waters, i.e., SB, TLC and PL, because most of the areas in the eastern waters are inside country parks with very low levels of human activity and disturbance, and the eastern shores are facing South China Sea with low levels of pollution. All the six study sites had lower concentrations of heavy metals in microplastics compared to those on sediments as monitored by the Environmental Protection Department (EPD, 2017). Such differences may be due to different sampling techniques, time of exposure, and geological backgrounds. But more importantly, a recent study has demonstrated that the concentrations of heavy metals between sediments and microplastics are not significantly correlated (Mohsen et al., 2019), which means that the sorption behaviour of heavy metals towards microplastics and sediments was different. Such behaviour is dependent on the grain size, chemical compositions, and organic matter content of the carriers (Yu et al., 2019), which are fundamentally different between microplastics and sediments, not to mention that the chemical composition of microplastics is very diverse. The most abundant type of polymer found in this study was PE. Similar results were found in our previous study in which PE, PP and PET were most abundant in beach sediments (Lo et al., 2018). Rochman et al. (2014) demonstrated that low density PE absorbs much less Cd, Ni, Pb and Zn in seawater than other polymers such as PET and PP. Although sorption kinetics of plastic towards metals may alter their concentrations, there was no significant relationship between %PE in the samples and individual metal concentrations in this study (p > 0.05). This indicated that other factors may superimpose the effect of sorption kinetics. For example, the site-specific level of metal contamination could be more critical in determining the metal concentration especially it is known that Pearl River is a major source of metal pollution in Hong Kong waters. Moreover, Rochman et al. (2014) found that some kinds of polymer require up to 12 months to reach equilibrium towards heavy metals, yet the exposure time of microplastics in the ocean is unknown. Among all the metals included in this study, Cd is of the greatest concern due to its risks to human health and the environment. Cd could be used as a heat and UV stabilizer incorporated into products made from PVC. Although the use of Cd in plastics has been restricted or banned in some countries, it was still detected in field-collected plastic samples (Ashton et al., 2010; Turner, 2016; Massos and Turner,
Table 3 Differences in the median concentrations of heavy metals (As, Cd, Cu, Fe, Mn, Ni, Zn) between eastern and western sites. Concentration (mg kg−1)
As Cd Cu Fe Mn Ni Zn
Eastern sites
Western sites
0.00 ± 0.00 (< LOD) 0.04 ± 0.04 0.43 ± 0.43 164 ± 98.4 7.50 ± 3.07 0.06 ± 0.06 12.8 ± 9.89
0.00 ± 0.00 (< LOD) 0.00 ± 0.00 (< LOD) 3.47 ± 2.83 799 ± 507 25.3 ± 14.6 0.18 ± 0.14 24.2 ± 9.29
Statistical comparisonsa NS NS ** ** * * NS
a Asterisks (*, **) indicate significant differences between the two regions at the level of p < 0.05 and p < 0.01; NS indicates no significant difference, according to Mann–Whitney U test. < LOD indicates below detection limits.
Results of inter-site comparisons of the median concentration of individual heavy metals are shown in Fig. 2 (a–g). As, Zn and Cd showed no significant differences among all the study sites (Fig. 2a–c). For Ni, the concentration at HPN (0.88 mg kg−1) was significantly higher than at SB (0.06 mg kg−1) and PL (< LOD) (Fig. 2d). Similarly, the concentration of Fe was significantly higher at HPN (1114 mg kg−1) than at SB (99.4 mg kg−1) and PL (164 mg kg−1) (Fig. 2e). HPN also has the highest concentration of Mn (112 mg kg−1) which was significantly higher than that at SB (7.44 mg kg−1), PL (4.42 mg kg−1) and TPT (18.6 mg kg−1), but it is worth mentioning that one of the samples in TLC had the highest concentration of Mn (567 mg kg−1) which was more than ten times higher compared to other replicates at this site. The concentration of Cu at HPN was also the highest (8.53 mg kg−1) and significantly higher than at TLC (0.43 mg kg−1) and PL (0.24 mg kg−1). 3.2. Chemical composition of microplastics Forms of microplastics collected included fragments, fiber, foam, film and pellet (Fig. 3). For chemical composition of microplastics, polyethylene (42.2%) was the most abundant (Fig. 4) and followed by polypropylene (23.3%), polystyrene (19.5%), polyester (6.1%), polyvinyl chloride (3.3%) and polyamide (1.1%). The remaining items were either minor types of microplastics or unidentified particles (4.5%). The composition of microplastics was more diverse at SB, TLC, HPN and TPT than at PL and SH. PE was the most abundant polymer among all the sites, ranging from 33.3% at HPL to 50% at PL and TLC. No PA was found in samples from SB, PL, SH and TPT. 4. Discussion The most polluted site was HPN located in Deep Bay which is a large shallow bay on the eastern side of the Pearl River Estuary with an average depth of about 3 m. Strong riverine inputs from within and outside the bay are the major sources of pollution, resulting in the highest level of total inorganic nitrogen (0.5–0.7 mg l−1) among the ten water quality control zones in Hong Kong (EPD, 2017). Pearl River is the third longest river in China with a population of 65 million living along the estuary. The river has been polluted by heavy metals since 1970s, in which surface sediment, agricultural soil, plants, water and animals (edible bivalves and gastropods) were found to contain considerable amount of heavy metals (Fang et al., 2001; Wong et al., 2002; Ye et al., 2012; Zhao et al., 2017; Jiao et al., 2018; Gu and Gao, 2019). Surface water of Pearl River was contaminated by metal processing and electroplating industries, and by the discharge of industrial wastewater and domestic sewage (Jiao et al., 2018). Microplastics were widely
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Fig. 2. Inter-site differences in heavy metal contamination. (a) As, (b) Zn, (c) Cd, (d) Ni, (e) Fe, (f) Mn and (g) Cu. Bars with different letters indicate significant differences among sampling sites at the level of p < 0.05 according to Mann–Whitney U test. “ns” indicates the differences were statistically indistinguishable. * and ** represents significant difference at p < 0.05 and p < 0.01, respectively according to Kruskal–Wallis test. < LOD indicates below detection limits.
2017). Ongoing illegal use of Cd in plastics is suspected to be a major source of recent inputs. Under the strongly acidic condition, Cd could be leached from plastics (Turner, 2019) and eventually pollutes the environment and causes harmful effects on living organisms.
Therefore, immediately actions should be taken in the monitoring of Cd in microplastics in the environment and a detail understanding of the sorption-desorption process between Cd and microplastics is needed. 5
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Fig. 3. Photographs of different types of microplastics collected: (a) fragment, (b) fiber, (c) foam, (d) film, and (e) pellet.
processes between metals and microplastics will help assess the associated risks to both human health and the environment. CRediT authorship contribution statement Wenjie Li:Investigation, Writing - original draft.Hoi-Shing Lo:Supervision, Investigation, Writing - original draft.Ho-Man Wong:Investigation.Man Zhou:Investigation.Chun-Yuen Wong: Project administration, Funding acquisition.Nora Fung-Yee Tam:Project administration, Funding acquisition.Siu-Gin Cheung: Supervision, Writing - review & editing, Project administration, Funding acquisition. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Fig. 4. Relative abundance of microplastics of different chemical compositions: PE (polyethylene), PP (polypropylene), PS (polystyrene), PET (polyethylene terephthalate), PA (polyamide), PVC (polyvinyl chloride) and other polymers (polyester, acrylate polymer).
Acknowledgments The work described was supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. CityU 11302815).
5. Conclusion Microplastics collected in this study were contaminated with heavy metals and higher concentrations of Ni, Fe, Mn and Cu were obtained from sites in the western waters probably due to the input of Pearl River. The three most common types of microplastics found were polyethylene, polypropylene and polystyrene. No significant correlation was found between polymer composition and individual metal concentrations, indicating that other factors such as geological settings and exposure time should be taken into considerations. The risks associated with the metals adsorbed to microplastics are dependent on the bioavailability and mobility of both the polymer and metals. In view of a continual increase in the global production of plastics, the microplastic abundance in the environment is expected to increase. Immediate actions should be taken in the establishment of long term monitoring programs for heavy metals associated with microplastics and in-depth research on the mechanisms of adsorption and desorption
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Heavy metals contamination of sedimentary microplastics in Hong Kong a,1
a,1
a
b
a
Wenjie Li , Hoi-Shing Lo , Ho-Man Wong , Man Zhou , Chun-Yuen Wong , ⁎ Nora Fung-Yee Tama, Siu-Gin Cheunga,c, a b c
T
Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region Research Institute for Environmental Innovation (Suzhou), Tsinghua, RIET, Jinfeng Road, Suzhou, China State Key Laboratory of Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region
ARTICLE INFO
ABSTRACT
Keywords: Heavy metals Microplastic Marine debris
This is the first study of heavy metals (As, Zn, Cd, Ni, Fe, Mn, Cu) contamination of microplastics on sandy beaches in Hong Kong. Three study sites are located in the eastern waters (Pak Lap Wan, Stanley Bay, Tung Lung Chau) and the other three in the western waters (Tai Pai Tsui, Ha Pak Nai, Shui Hau Wan). The three most abundant types of microplastics were polyethylene (42.2%), polypropylene (23.3%) and polystyrene (19.5%). The median concentration of Fe (302 mg kg−1) was the highest and followed by Zn (19.6 mg kg−1) and Mn (18.6 mg kg−1). Very low concentrations of Cu (0.89 mg kg−1), Ni (0.15 mg kg−1), As (< LOD) and Cd (< LOD) were measured. The western sites have significantly higher concentrations of Ni, Fe, Mn and Cu than the eastern sites, indicating that Pearl River was likely to be a major source of heavy metals on microplastics. In view of a continual increase in the abundance of microplastics in the marine environment and its potential impacts on marine organisms, immediate actions should be taken in establishing long term monitoring programs for heavy metals associated with microplastics. In-depth research on the mechanisms of adsorption and desorption processes between metals and microplastics will help assess the associated risks to both human health and the environment.
1. Introduction Microplastics are smaller pieces of plastic with a diameter < 5 mm. Primary microplastics are produced to serve specific purposes such as fibers for clothing and nurdles for manufacturing of plastic products whereas secondary microplastics are produced from natural breakdown of larger plastic products. Because of their small size and light weight, they are carried by water or air to almost everywhere on earth (Thompson et al., 2004; Allen et al., 2019). By 2018, microplastics have been found in > 114 aquatic species (https://www.britannica.com/ technology/microplastic). Studies have shown that different kinds of organisms, such as zooplankton, benthic invertebrates, bivalves, fish and large marine mammals, can ingest microplastics as food (Cole et al., 2013; Van Cauwenberghe and Janssen, 2014; Li et al., 2016; Güven et al., 2017; McGoran et al., 2017; Steer et al., 2017). Ingestion of microplastics by marine animals blocks food passages, resulting in false satiety, hence reduces the energy and nutrient intake and causes death (Andrady, 2011). The harmful effects of microplastics on marine animals can also be due to contaminants adsorbed on the surface of microplastics. Due to
their large specific surface area and hydrophobic characteristics, microplastics can accumulate high concentrations of POPs and heavy metals in the marine environment, such as polychlorinated biphenyls (PCBs) (Mato et al., 2001), dichlorodiphenyltrichloroethane (DDT) (Frias et al., 2010), hydrocarbons (HCs) (Hirai et al., 2011; Van et al., 2012; Lo et al., 2019) and heavy metals (Ashton et al., 2010; Holmes et al., 2012). Microplastics may be inadvertently ingested by marine organisms (Mrosovsky et al., 2009; Sleight et al., 2017) and seabirds (Auman et al., 1997), and the heavy metal contaminants carried by these microplastics may be released in the acidic digestive tract of animals (Ashton et al., 2010; Holmes et al., 2014; Sleight et al., 2017). Since the accumulation of heavy metals in plastic particles can have potential negative effects on marine organisms, there is an urgency to develop monitoring programs for heavy metals in microplastics in the marine environment. The main anthropogenic sources of heavy metals in the marine environment are industrial and municipal wastewater, sewage discharges, agricultural runoff, and antifouling coatings in ports, docks and ships (Yeats, 2010). The adsorption of heavy metals on microplastics occurs through complex mechanisms (Brennecke et al., 2016).
Corresponding author at: Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Hong Kong Special Administrative Region. E-mail address: [email protected] (S.-G. Cheung). 1 These authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.marpolbul.2020.110977 Received 19 August 2019; Received in revised form 10 February 2020; Accepted 10 February 2020 Available online 14 February 2020 0025-326X/ © 2020 Elsevier Ltd. All rights reserved.
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Major heavy metal elements that pollute the ocean include mercury, cadmium, lead, zinc, chromium, and copper. They enter the aquatic system, and are transferred and accumulated through physical, chemical and biological migrations. Inorganic minerals and organic compounds precipitate on the surface of plastic particles, leading to the change of their surface properties and the formation of various active binding sites of metal ions (Ashton et al., 2010; Holmes et al., 2014; Rochman et al., 2014). Holmes et al. (2012) reported that plastic pellets could be an important vehicle for the transport of metals in the marine environment because microplastics could be transported for considerable distances while buoyant. The adsorption of heavy metals to plastic pellets is metal specific with Cd, Co, Ni and Pb increasing whereas Cr(V(I) decreasing adsorption with increasing pH and decreasing salinity. Weathering of plastics further facilitates the metal adsorption (Holmes et al., 2012). A field experiment has demonstrated strong correlations between adsorbability of PP and PVC towards Pb and Mn, and the concentration of these metals in seawater (Gao et al., 2019). Routine water quality monitoring in Hong Kong is conducted by the Environmental Protection Department (EPD) with > 60 physical, chemical and biological parameters measured for sediment samples taken from various sites in ten water control zones around Hong Kong. Since the implementation of the marine monitoring programme in 1986, heavy metals such as copper and silver have been detected in Victoria Harbour and Tsuen Wan, probably due to industrial pollution emissions during the 1960s and 1980s before the introduction of pollution control. The feasibility of using barnacles and mussels as biomonitors of heavy metals contamination in Hong Kong was reported upon by Phillips and Rainbow
(1988). Blackmore (2001) determined the cumulative concentrations of cadmium, copper and zinc in the bodies of 19 species of intertidal invertebrates from two coasts of a relatively uncontaminated area in Hong Kong, the Cape d'Aguilar marine reserve. In general, the concentrations of metals in the body could be explained by the accumulation strategies and physiological requirements of the analyzed organisms. The first study of microplastic pollution in Hong Kong was published by Fok and Cheung (2015) which has demonstrated regional differences in the pollution level with higher concentrations of microplastics being collected on sandy beaches in the western waters than eastern waters, probably due to the input of Pearl River, the third longest river in China, of which the estuary is located in the western side of Hong Kong. In this study, we had collected microplastics from six shores in Hong Kong with three of them located in the western waters and the others in the eastern waters. Chemical compositions of the microplastics and concentrations of seven metals (As, Zn, Cd, Ni, Fe, Mn, Cu) on the microplastics were determined to understand the spatial variations of heavy metals contamination of microplastics in Hong Kong waters. 2. Materials and methods 2.1. Sampling of microplastics The sampling was conducted in the dry season between November and December 2018 at six sites, namely Pak Lap Wan (PL), Stanley Bay (SB) and Tung Lung Chau (TLC) in the eastern waters, and Shui Hau (SH), Tai Pai Tsui (TPT) and Ha Pak Nai (HPN) in the western waters (Fig. 1). Sediment for microplastic characterization was collected from
Fig. 1. Geographic location of Hong Kong and sampling sites in this study. Three study sites are located in the eastern waters: Pak Lap Wan (PL), Stanley Bay (SB), and Tung Lung Chau (TLC), and the remaining sites in the western waters: Tai Pai Tsui (TPT), Ha Pak Nai (HPN) and Shui Hau (SH). 2
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a quadrat (0.25 m × 0.25 m) using a stainless steel shovel to a depth of 2–3 cm along the strandline during low tide and five replicates were collected at 3–5 m intervals (depending on the shore length). Microplastics were extracted in-situ by transferring the sediment to a bucket filled with ambient seawater. Particles floating on the water surface were collected and passed through a sieve with a pore size of 0.5 mm. Particles retained on the sieves were rinsed and stored in plastic tubes. Particles larger than 5 mm were removed and the remaining particles were within a size range of 0.5–5 mm. These microplastics were characterized by FTIR later. For heavy metals quantification, microplastics of the size of approximately 5 mm were identified by naked eyes and hand-picked. This was to prevent metal contamination of the microplastics by the stainless steel shovel and sieves. Further precautions included wearing laboratory latex gloves and cotton clothing during sampling. Over 100 pieces of microplastics of different sizes, colours, shapes and other physical properties were collected for each replicate, and there were 5 replicates for each site. The samples were put in sealed plastic bags and transported to the laboratory immediately and stored in a freezer at −20 °C for further analysis.
Table 1 Detection limits of the ICP-OES for different metals and the recovery rate of metals from oyster tissue as standard reference material. Metal
Detection limit of ICP-OES (ml L−1)
Recovery rate (%)
As Cd Cu Fe Mn Ni Zn
0.00828 0.00063 0.00153 0.00174 0.00315 0.00201 0.00168
139 108 120 85 111 126 89
Plasma Atomic Emission Spectrometer (PE optima 6000)). The recovery rate and limit of detection are listed in Table 1. The glassware were washed with tap water, rinsed with deionized water, dipped in detergent for 24 h and rewashed with deionized water. They were then put in an acid bath with 25% HNO3 for 24 h, and rinsed with deionized water followed by Milli-Q. 2.4. Statistical analysis
2.2. Chemical composition of microplastics
Statistical analyses were performed using R and SPSS 22. Prior to analysis, data were tested for normality and homogeneity of variance using Shapiro-Wilk test and Levene's test, respectively. As the above tests for statistical assumptions failed even after data transformation, the nonparametric Kruskal-Wallis test was used in combination with Mann-Whitney U test (statistical significance level: 0.05) for comparing the concentrations of individual heavy metals among study sites and between geographical regions. The relationships between polymer compositions and metal concentrations were analyzed using Pearson correlation coefficient.
The samples were freeze-dried for 48 h. After removal of impurities, selected microplastics were examined under a microscope with a magnification of 7.3× − 120× (M165C, Leica Microsystems). According to the criteria established by Free et al. (2014) and McCormick et al. (2014), microplastics were identified by their shape, colour and surface texture, and were categorized into five classes, namely “pellet”, “fragment”, “fiber”, “foam” and “film”. Thirty pieces of microplastics were selected randomly from the samples at each study site, or 180 pieces of microplastics from all the sites, and examined using Fourier Transform Infrared (FTIR) spectroscopic analysis (Nicolet iS50 equipped with a built-in iS50 ATR module, Thermo Scientific, WI, USA). The obtained spectra were compared with the reference spectra in the Hummel polymer library, and only a matching of > 70% was accepted. The microplastics were identified successfully as polyethylene (PE), polypropylene (PP), polystyrene (PS), polyvinyl chloride (PVC), polyester (PET), polyamide (PA) or others including acrylonitrile butadiene styrene (ABS), polyether urethane (PEUT), cellulose acetate (CA) and unknown particles that were not found in the Hummel Polymer Library.
3. Results 3.1. Heavy metals contamination of microplastics Median concentrations of heavy metals in microplastics are shown in Table 2. The concentration of Fe was much higher than that of all the other metals (Mann–Whitney U test, p < 0.05). Concentrations of Mn and Zn were not significantly different from each other but they were all significantly higher than that of Cu, Ni, As and Cd (Mann–Whitney U test, p < 0.05). There was no significant regional difference between western shores and eastern shores for As, Zn, and Cd, but the western shores had significantly higher concentrations of Fe, Ni, Mn and Cu (Mann-Whitney U test, p < 0.05) (Table 3). The greatest regional difference was found in Cu with that in the western shores being 8 times that in the eastern shores. Differences in Fe, Mn and Ni between the two regions varied between 3 times and 5 times.
2.3. Heavy metal analysis The microplastic samples were dried in a desiccator for 48 h to prevent the loss of metals. Each replicate was weighted to the nearest 0.001 g in a glass container, and subsequently suspended in 20 mL of 20% aqua regia (1:3 HNO3:HCl). The suspension was shaken at 150 rpm overnight at room temperature to desorb heavy metals. The resulting liquid was filtered through a 0.45 μm acid washed membrane filter (MiliPore) to remove fine particles. The filtrate was then made up to 25 mL using MiliQ water for metal analysis. This metal extraction method could prevent clogging of polymers in the ICP-OES during injection. Blank tests were prepared following the same procedure but without the microplastic samples to determine the background contamination. Five replicates and two blank solutions were prepared for each study site. The recovery efficiency of the digestion process was checked using oyster tissue (0.0902 g) as a standard reference material because there was no commercially available standard reference microplastics for heavy metals determination. Considering that the microplastics has been freeze-dried and treated by sonication, oyster tissue was selected as a standard reference material because the processing procedures were similar. Concentrations of heavy metals in the solution were determined using a quadrupole ICP-OES (Inductively Coupled
Table 2 Median concentrations of heavy metals in microplastics collected from six study sites in Hong Kong. Values are expressed as medians ± median absolute deviation.
As Cd Cu Fe Mn Ni Zn
Concentration (mg kg−1)
Groupinga
0.00 ± 0.00 (< LOD) 0.00 ± 0.00 (< LOD) 0.89 ± 0.89 302 ± 224 18.6 ± 12.7 0.15 ± 0.13 19.6 ± 11.4
A AB C E D B D
a Different letters indicate significant differences among the sampling sites at the level of p < 0.05 according to Kruskal–Wallis test and Mann–Whitney U test. < LOD indicates below detection limits.
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detected in the river water, riverbed sediment and estuarine sediment in Pearl River Estuary and its tributaries (Fan et al., 2019). Since Pearl River is one of the major sources of microplastics in the western waters of Hong Kong (Fok and Cheung, 2015; Cheung et al., 2016), this helps explain why microplastics collected at HPN contained high concentrations of heavy metals especially for Cu, Fe, Ni, and Mn because the concentrations of these metals were also significantly higher in the sediments in this region (EPD, 2017). On the other hand, there were no significant regional differences for As, Cd and Zn. A recent study has reported that Cd and Zn have been used as heat stabilizers and slip agents for plastic materials and could comprise up to 3% of the polymer composition (Hahladakis et al., 2018). Therefore, Cd and Zn are not pollutants but rather additives of microplastics, hence no regional differences in their concentrations were observed. The concentration of As in microplastics was < LOD at all the study sites. An earlier study in Hong Kong (Cheung and Wong, 1992) also showed that As content in sediment was very low when compared with Cu, Cd and Cr, and there was no specific pollution source of As in Hong Kong because As is usually derived from natural sources. Similar findings were reported upon by Turner (2016) for beached litter collected in SW England where the concentration of As was always the lowest when compared with other metals. Pearl River as a major source of heavy metals in microplastics was further supported by significantly lower concentrations of Ni, Fe, Mn and Cu at the sites in the eastern waters, i.e., SB, TLC and PL, because most of the areas in the eastern waters are inside country parks with very low levels of human activity and disturbance, and the eastern shores are facing South China Sea with low levels of pollution. All the six study sites had lower concentrations of heavy metals in microplastics compared to those on sediments as monitored by the Environmental Protection Department (EPD, 2017). Such differences may be due to different sampling techniques, time of exposure, and geological backgrounds. But more importantly, a recent study has demonstrated that the concentrations of heavy metals between sediments and microplastics are not significantly correlated (Mohsen et al., 2019), which means that the sorption behaviour of heavy metals towards microplastics and sediments was different. Such behaviour is dependent on the grain size, chemical compositions, and organic matter content of the carriers (Yu et al., 2019), which are fundamentally different between microplastics and sediments, not to mention that the chemical composition of microplastics is very diverse. The most abundant type of polymer found in this study was PE. Similar results were found in our previous study in which PE, PP and PET were most abundant in beach sediments (Lo et al., 2018). Rochman et al. (2014) demonstrated that low density PE absorbs much less Cd, Ni, Pb and Zn in seawater than other polymers such as PET and PP. Although sorption kinetics of plastic towards metals may alter their concentrations, there was no significant relationship between %PE in the samples and individual metal concentrations in this study (p > 0.05). This indicated that other factors may superimpose the effect of sorption kinetics. For example, the site-specific level of metal contamination could be more critical in determining the metal concentration especially it is known that Pearl River is a major source of metal pollution in Hong Kong waters. Moreover, Rochman et al. (2014) found that some kinds of polymer require up to 12 months to reach equilibrium towards heavy metals, yet the exposure time of microplastics in the ocean is unknown. Among all the metals included in this study, Cd is of the greatest concern due to its risks to human health and the environment. Cd could be used as a heat and UV stabilizer incorporated into products made from PVC. Although the use of Cd in plastics has been restricted or banned in some countries, it was still detected in field-collected plastic samples (Ashton et al., 2010; Turner, 2016; Massos and Turner,
Table 3 Differences in the median concentrations of heavy metals (As, Cd, Cu, Fe, Mn, Ni, Zn) between eastern and western sites. Concentration (mg kg−1)
As Cd Cu Fe Mn Ni Zn
Eastern sites
Western sites
0.00 ± 0.00 (< LOD) 0.04 ± 0.04 0.43 ± 0.43 164 ± 98.4 7.50 ± 3.07 0.06 ± 0.06 12.8 ± 9.89
0.00 ± 0.00 (< LOD) 0.00 ± 0.00 (< LOD) 3.47 ± 2.83 799 ± 507 25.3 ± 14.6 0.18 ± 0.14 24.2 ± 9.29
Statistical comparisonsa NS NS ** ** * * NS
a Asterisks (*, **) indicate significant differences between the two regions at the level of p < 0.05 and p < 0.01; NS indicates no significant difference, according to Mann–Whitney U test. < LOD indicates below detection limits.
Results of inter-site comparisons of the median concentration of individual heavy metals are shown in Fig. 2 (a–g). As, Zn and Cd showed no significant differences among all the study sites (Fig. 2a–c). For Ni, the concentration at HPN (0.88 mg kg−1) was significantly higher than at SB (0.06 mg kg−1) and PL (< LOD) (Fig. 2d). Similarly, the concentration of Fe was significantly higher at HPN (1114 mg kg−1) than at SB (99.4 mg kg−1) and PL (164 mg kg−1) (Fig. 2e). HPN also has the highest concentration of Mn (112 mg kg−1) which was significantly higher than that at SB (7.44 mg kg−1), PL (4.42 mg kg−1) and TPT (18.6 mg kg−1), but it is worth mentioning that one of the samples in TLC had the highest concentration of Mn (567 mg kg−1) which was more than ten times higher compared to other replicates at this site. The concentration of Cu at HPN was also the highest (8.53 mg kg−1) and significantly higher than at TLC (0.43 mg kg−1) and PL (0.24 mg kg−1). 3.2. Chemical composition of microplastics Forms of microplastics collected included fragments, fiber, foam, film and pellet (Fig. 3). For chemical composition of microplastics, polyethylene (42.2%) was the most abundant (Fig. 4) and followed by polypropylene (23.3%), polystyrene (19.5%), polyester (6.1%), polyvinyl chloride (3.3%) and polyamide (1.1%). The remaining items were either minor types of microplastics or unidentified particles (4.5%). The composition of microplastics was more diverse at SB, TLC, HPN and TPT than at PL and SH. PE was the most abundant polymer among all the sites, ranging from 33.3% at HPL to 50% at PL and TLC. No PA was found in samples from SB, PL, SH and TPT. 4. Discussion The most polluted site was HPN located in Deep Bay which is a large shallow bay on the eastern side of the Pearl River Estuary with an average depth of about 3 m. Strong riverine inputs from within and outside the bay are the major sources of pollution, resulting in the highest level of total inorganic nitrogen (0.5–0.7 mg l−1) among the ten water quality control zones in Hong Kong (EPD, 2017). Pearl River is the third longest river in China with a population of 65 million living along the estuary. The river has been polluted by heavy metals since 1970s, in which surface sediment, agricultural soil, plants, water and animals (edible bivalves and gastropods) were found to contain considerable amount of heavy metals (Fang et al., 2001; Wong et al., 2002; Ye et al., 2012; Zhao et al., 2017; Jiao et al., 2018; Gu and Gao, 2019). Surface water of Pearl River was contaminated by metal processing and electroplating industries, and by the discharge of industrial wastewater and domestic sewage (Jiao et al., 2018). Microplastics were widely
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Fig. 2. Inter-site differences in heavy metal contamination. (a) As, (b) Zn, (c) Cd, (d) Ni, (e) Fe, (f) Mn and (g) Cu. Bars with different letters indicate significant differences among sampling sites at the level of p < 0.05 according to Mann–Whitney U test. “ns” indicates the differences were statistically indistinguishable. * and ** represents significant difference at p < 0.05 and p < 0.01, respectively according to Kruskal–Wallis test. < LOD indicates below detection limits.
2017). Ongoing illegal use of Cd in plastics is suspected to be a major source of recent inputs. Under the strongly acidic condition, Cd could be leached from plastics (Turner, 2019) and eventually pollutes the environment and causes harmful effects on living organisms.
Therefore, immediately actions should be taken in the monitoring of Cd in microplastics in the environment and a detail understanding of the sorption-desorption process between Cd and microplastics is needed. 5
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Fig. 3. Photographs of different types of microplastics collected: (a) fragment, (b) fiber, (c) foam, (d) film, and (e) pellet.
processes between metals and microplastics will help assess the associated risks to both human health and the environment. CRediT authorship contribution statement Wenjie Li:Investigation, Writing - original draft.Hoi-Shing Lo:Supervision, Investigation, Writing - original draft.Ho-Man Wong:Investigation.Man Zhou:Investigation.Chun-Yuen Wong: Project administration, Funding acquisition.Nora Fung-Yee Tam:Project administration, Funding acquisition.Siu-Gin Cheung: Supervision, Writing - review & editing, Project administration, Funding acquisition. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Fig. 4. Relative abundance of microplastics of different chemical compositions: PE (polyethylene), PP (polypropylene), PS (polystyrene), PET (polyethylene terephthalate), PA (polyamide), PVC (polyvinyl chloride) and other polymers (polyester, acrylate polymer).
Acknowledgments The work described was supported by a grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. CityU 11302815).
5. Conclusion Microplastics collected in this study were contaminated with heavy metals and higher concentrations of Ni, Fe, Mn and Cu were obtained from sites in the western waters probably due to the input of Pearl River. The three most common types of microplastics found were polyethylene, polypropylene and polystyrene. No significant correlation was found between polymer composition and individual metal concentrations, indicating that other factors such as geological settings and exposure time should be taken into considerations. The risks associated with the metals adsorbed to microplastics are dependent on the bioavailability and mobility of both the polymer and metals. In view of a continual increase in the global production of plastics, the microplastic abundance in the environment is expected to increase. Immediate actions should be taken in the establishment of long term monitoring programs for heavy metals associated with microplastics and in-depth research on the mechanisms of adsorption and desorption
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