Article Cite This: Environ. Sci. Technol. 2019, 53, 8036−8046
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Microplastics in the Coral Reef Systems from Xisha Islands of South China Sea Jinfeng Ding,† Fenghua Jiang,† Jingxi Li,† Zongxing Wang,† Chengjun Sun,*,†,‡ Zhangyi Wang,§ Liang Fu,∥ Neal Xiangyu Ding,⊥ and Changfei He†
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Key Laboratory of Marine Bioactive Substances, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China ‡ Laboratory of Marine Drugs and Bioproducts, Pilot National Laboratory for Marine Science and Technology, Qingdao 266071, China § State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan 570228, China ∥ Sansha Trackline Institute of Coral Reef Environment Protection, Sansha 573199, China ⊥ Menaul School, Qingdao 266071, China S Supporting Information *
ABSTRACT: The impacts of microplastics on coral reefs are gaining attention due to findings that microplastics affect coral health. This work investigated the distribution and characteristics of microplastics in the seawater, fish, and corals in 3 atolls from the Xisha Islands of South China Sea. In the seawater samples, microplastics were detected in the outer reef slopes, reef flats, and lagoons with abundances ranging from 0.2 to 11.2, 1.0 to 12.2, and 1.0 to 45.2 items L−1, respectively. Microplastic abundance was 0−12.0 items individual−1 (0−4.7 items g−1) in fish and 1.0−44.0 items individual−1(0.02−1.3 items g−1) in coral. The predominant shape and polymer of microplastics in seawater, fish, and coral were fibrous rayon and polyethylene terephthalate (PET). Microplastic sizes primarily ranged from 20−330 μm in both the seawater and fish, while there were relatively more 1−5 mm microplastics in the corals. The shape, size, color, and polymer type distribution patterns of microplastics in seawater more closely resembled those in fish gills than those in fish gastrointestinal tracts or coral samples. This study shows that microplastics are abundant in these coral reef systems and they are captured by fish or “trapped” by corals.
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INTRODUCTION Over the past decade, the widespread occurrence of microplastics (defined as particles 40 islands and reefs. Currently, the coral reefs are suffering from a variety of natural and human-related activities, including coral bleaching, coral diseases, ocean acidification, overfishing, tropic storms, pollution, tourism, and land reclamation, which result in a significant degeneration of complex coral reef ecosystems.27 The microplastic contamination in the coral reef ecosystems in Xisha islands has not been investigated. The aim of this study is to investigate the abundance and characteristics of microplastic pollution in the seawater, fish, and corals of the coral ecosystems in Xisha islands and examine the relationship between biota and their surrounding environment.
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MATERIALS AND METHODS Study Area. The South China Sea is the largest marginal sea in the southeast region of the South China continental shelf, which exists in a semienclosed environment. It joins the East China Sea by the Taiwan Strait and connects to the western Pacific Ocean through the Luzon Strait. Xisha Islands is the biggest archipelago in the South China Sea, with a total 8037
DOI: 10.1021/acs.est.9b01452 Environ. Sci. Technol. 2019, 53, 8036−8046
Article
Environmental Science & Technology
was rinsed with Milli-Q water before being removed. The rinse-off was pooled with the HCl treated solution and filtered. The membrane was treated the same way as mentioned above. A schematic diagram of the microplastics attached on the surface and inside of a coral skeleton is shown in Figure S2. Observation and Identification of Microplastic. All samples on the membrane were observed under a stereo microscope (Nikon SMZ1270, Japan), and images (20−80× magnification) were obtained with a Nikon Ds-Ri2 digital camera. Microplastics and suspected microplastic particles were selected and identified using a PerkinElmer Spectrum Spotlight 400 micro-Fourier transform infrared spectroscope (μ-FT-IR; PerkinElmer Inc., U.S.A.), equipped with a liquid nitrogen-cooled mercury cadmium telluride (MCT) array detector, and attenuated total reflection (ATR) consisting of a germanium (Ge) crystal. The spectrum range was from 4000 to 750 cm−1 with a spectral resolution of 8 cm−1 and a spatial resolution of 6.25 μm (highest spatial resolution is 1.56 μm). Sixteen coscans were performed in each measurement. The scanning area ranged from 100 μm × 100 μm to 1000 μm × 1000 μm. The ATR imaging attachment was in direct contact with the microplastics on the filter membrane during data acquisition. Therefore, the diameter of microplastics down to 6.25 μm could be identified in our study. Polymer type analysis and the characterization of the functional groups were conducted by comparison of the acquired data against the database. All of the spectra were compared with the Sadltler Library, and the characteristic peaks of the functional groups were combined to verify the polymer type. When interpreting FTIR output, only readings with confidence levels of 70% or greater were considered reliable and accepted (after visual inspection). All confirmed polymer types were included in our results. The surface structures of plastics were examined using a scanning electron microscope (SEM; Hitachi S-4800, Japan). Quality Control of Experiments. All the containers (conical flask, glass beaker, plexiglass water sampler, Niskin water sampler) were rinsed at least three times with Milli-Q water before being used. The reagents (ethanol, sodium chloride solution, and 10% KOH solution) used in this study were filtered through Whatman GF/F filters prior to use. When using ATR-μ-FTIR, the surface of the Ge crystal was thoroughly cleaned with 100% filtered ethanol after every specimen to avoid cross-contamination. To minimize environmental contamination, solution preparation and biological dissection were always conducted in a semiclosed space. In addition, all of the containers were always covered with aluminum foil to avoid contamination. Gloves (nitrile) and cotton lab coats were always worn throughout the experiment. In the laboratory, blank experiments without seawater, coral, and fish tissue were carried out simultaneously to correct and evaluate background contamination. Data Analysis. The abundance of microplastics in seawater was expressed as particles per liter in this study. Microplastic abundances regarding fish and coral samples were presented as both the number of microplastic particles per gram of wet weight (unit: items g−1) and the number of microplastics per fish or coral individual (unit: items individual−1). Since coral is a colony animal, we used units of items individual−1 in coral merely to reflect the microplastics number in the corals we analyzed. Additionally, the microplastics concentrations in the fish gills and fish GITs were shown separately, and the microplastics abundances both on the surface and inside of coral skeleton were also separated.
section. Weather conditions (wind direction, wind power, and wind speed) were recorded by the mobile weather station at the vessel. Fish and coral samples were obtained by scuba diving and snorkeling. Fish were sampled from outer reef slopes at the North Reef and the Yongle Atoll within 3 m (Table S2). Coral samples were collected from outer reef slopes at the Yongle Atoll and Passu Keah, within a depth of 17 m (Table S3). All fish were euthanized before further handling. Altogether, 31 fish and 27 coral samples were collected. Euthanized samples were individually wrapped in aluminum foil and stored at −60 °C before being transferred to the laboratory for microplastics analysis. Isolation of Microplastics. In the laboratory, fish specimens were photographed and identified. For each individual, both the body wet weight (g) and fork length (cm) were recorded before dissection. As previous experiments showed, 5 and 20 μm diameter microplastics could accumulate in the gills of zebrafish (Danio rerio);29 we also analyzed microplastics in the gills besides the whole gastrointestinal tract (GIT) in the present study. In order to test and find the differences in microplastic abundance between tissues, gills and GITs of fish were dissected out, weighted, and treated separately. The abundance of microplastics in the gills and GITs were calculated based on the weight of these tissues. A new procedure for microplastics isolation modified from two of the previous studies was used in the present study.30,31 Briefly, the procedures were run as following: (1) Gills from each fish were respectively added into saturated sodium chloride solution (NaCl, 1.2 g cm−3, filtered through Whatman GF/F membranes) and sonicated (200 W, room temperature) for 30 min using a high-power digital ultrasonic instrument. After settling overnight, each supernatant was filtered through a 0.7 μm pore size, 47 mm diameter glass fiber membrane (Whatman GF/F, UK) using a glass filtration device under a vacuum. After filtration, the filters were carefully transferred to Petri dishes and dried at 50 °C for further analysis. (2) The GIT from each fish was respectively placed in a 250 mL conical flask with 100 mL of 10% KOH solution. Then, the flask was covered with aluminum foil and sonicated for 5 min before being placed on an oscillation incubator shaking at 90 rpm for 24 to 48 h at 60 °C to remove the organic matter. After digestion, the solution was filtered through a glass fiber membrane without cooling. The membranes were placed in clean Petri dishes and dried for further analysis as listed above. The isolation of microplastics from corals was based on previous study.25 Coral individuals were photographed and identified in the laboratory. Coral skeleton’s total wet weight was recorded. In order to obtain the microplastics from both the surface and inside of the coral skeleton, we implemented the following procedures: Step (1) To obtain microplastics attached to the surface of the coral skeleton, the whole coral skeleton was soaked in saturated sodium chloride solution in a glass beaker covered with alumnium foil. The skeleton was sonicated (200 W, room temperature) for 5 min to strip off microplastics attached to the surface. The glass beaker was then placed at room temperature to settle for 24 h. After 24 h, all the solution was carefully decanted and filtered through a 0.7 μm pore size, 47 mm diameter glass fiber membrane. Step (2) To collect microplastics from inside the coral skeleton (main component: CaCO3), about 20 g of coral skeleton from step 1 was dissolved in 37% HCl for 30 min. The HCl solution then was diluted using Milli-Q water and filtered through the glass fiber membrane. When there was undissolved skeleton, it 8038
DOI: 10.1021/acs.est.9b01452 Environ. Sci. Technol. 2019, 53, 8036−8046
Article
Environmental Science & Technology
seawater depth at the three outer reef slopes, and the seawater column at the depth of 10 m had the highest microplastics accumulation. For instance, the outer reef slope at the Passu Keah contained 11.2 items L−1 at the depth of 10 m, showing the highest microplastics contamination level, while Yongle Atoll only had 0.2 items microplastics L−1 at the depth of 40 m, showing the lowest microplastics abundance. Spatial heterogeneity in microplastic abundance was apparent at three reef flats. At the depth of 1 m, microplastic abundance ranged from 1.0 to 12.2 items L−1 and averaged 6.1 items L−1 at the three reef flats. The highest abundance of microplastics among the reef flats was found at the North Reef, and the lowest abundance was found at Yongle Atoll. Additionally, the changing tendency in microplastic abundance associated with seawater depth among the three lagoons resembles that of the outer reef slope. Relatively higher microplastic abundance was observed in the lagoon at a depth of 5 m at the North Reef, while at the Yongle Atoll, the lowest microplastic abundance was found at a depth of 15 m. The highest microplastic abundance in the reef flats and lagoons were all detected at the North Reef while the lowest microplastics abundance were all detected at the Yongle Atoll. The average abundance of microplastics in seawater samples from the North Reef reached 10.5 items L−1, showing the greatest microplastic contamination in comparison with microplastic abundance in the Passu Keah (4.8 items L−1) and Yongle Atoll (3.4 items L−1) (Figure 3). Multiple microplastic shapes, including fibers, fragments, granules, and films, were detected in the seawater samples. Fibers were the predominant shape of microplastics identified in seawater (79.7%), followed by fragments and granules, at 13.2% and 5.2%, respectively (Figure S3A). Red, black, and blue were the three dominant colors of microplastics, making up 76.9% of all color classes in seawater (Figure S3B). The average size of microplastics was 388.4 μm, ranging from 7 to 4856 μm. In order to compare with other research data, five size categories were divided in our study. A total of 2.4% of the microplastics were smaller than 20 μm, while the 20−330 μm size fraction accounted for 64.8% of all the microplastics in the seawater samples. The 20−330 μm size fraction was the most abundant of all the size classes in the seawater samples (Figure 4A). In the seawater samples, a total of 87.9% of granules were in the size range of 20−330 μm, while the percentage of films (8.3%) was highest compared with other shape types in the
