Abstract
To clarify whether microplastics contribute to elevated bioaccumulation of methylmercury (MeHg) in aquatic organisms, we studied the sorption pattern of MeHg on polystyrene beads (PBs) and evaluated MeHg accumulation, via uptake of MeHg-adsorbed PB, in the oyster Crassostrea gigas. MeHg-cysteine conjugates were added to seawater at 10, 100, and 1000 µg/L as Hg. Polystyrene beads (φ = 0.02, 0.2, and 2 µm) were immersed in the seawater for 24 h. The concentrations of total mercury (T-Hg) adsorbed onto the PBs were then measured using the reduction vaporization method. T-Hg concentrations for the PBs with diameters of 0.02, 0.2, and 2 µm were 10.6 ± 0.4, 1.8 ± 0.1, and 1.3 ± 0.1 ng/mg-PBs, respectively, when immersed in 2 mL of MeHg-added seawater (100 µg/L as Hg). Thus, the adsorption efficiency of MeHg onto PBs was higher in the presence of smaller diameter PBs. Next, 1 mg of PBs immersed in 2 mL of seawater containing 100 µg/L of MeHg for 24 h was added to an oyster tank containing 1 L of seawater. The T-Hg concentration of the oysters was measured after 6 h of exposure. No significant difference was found in the T-Hg concentration of oysters in the presence of PBs (0.30 ± 0.01 to 0.37 ± 0.05 ng/mg as dry weight) with MeHg and in the absence of PBs (0.36 ± 0.03 ng/mg as dry weight). Our results suggest that the presence of PBs in seawater has little effect on MeHg uptake by oysters.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of Data and Materials
All data generated or analyzed during this study are included in this published article.
References
Andrady AL (2015) Persistence of plastic litter in the oceans. In: Bergmann M, Gutow L, Klages M (eds) Marine anthropogenic litter. Springer, Cham, pp 57–72. https://doi.org/10.1007/978-3-319-16510-3_3
Barboza LGA, Vieira LR, Guilhermino L (2018) Single and combined effects of microplastics and mercury on juveniles of the European seabass (Dicentrarchus labrax): changes in behavioural responses and reduction of swimming velocity and resistance time. Environ Pollut 236:1014–1019. https://doi.org/10.1016/j.envpol.2017.12.082
Cincinelli A, Scopetani C, Chelazzi D et al (2017) Microplastic in the surface waters of the Ross Sea (Antarctica): occurrence, distribution and characterization by FTIR. Chemosphere 175:391–400. https://doi.org/10.1016/j.chemosphere.2017.02.024
Cunningham PA (1976) Inhibition of shell growth in the presence of mercury and subsequent recovery of juvenile oysters. Proc Natl Shellfish Assoc 66:1–5
Ehrich MK, Harris LA (2015) A review of existing eastern oyster filtration rate models. Ecol Modell 297:201–212. https://doi.org/10.1016/j.ecolmodel.2014.11.023
Eshak MB, Omar WMW (2017) Isochrysis maritima billard and gayral isolated from penang national park coastal waters as a potential microalgae for aquaculture. Trop Life Sci Res 28:163–177. https://doi.org/10.21315/tlsr2017.28.2.12
Faganeli J, Horvat M, Covelli S, Fajon V, Lipej L, Cermelj B (2003) Mercury and methylmercury in the Gulf of Trieste (northern Adriatic Sea). Sci Total Environ 304(1–3):315–326. https://doi.org/10.1016/S0048-9697(02)00578-8
Fitzgerald WF, Lamborg CH, Hammerschmidt CR (2007) Marine biogeochemical cycling of mercury. Chem Rev 107:641–662. https://doi.org/10.1021/cr050353m
Food and Drug Administration, USA (2017) Mercury levels in commercial fish and shellfish (1990–2012). https://www.fda.gov/food/metals-and-your-food/mercury-levels-commercial-fish-and-shellfish-1990-2012. Accessed 26 Jan 2021
Galimany E, Rose JM, Dixon MS, Alix R, Li Y, Wikfors GH (2018) Design and use of an apparatus for quantifying bivalve suspension feeding at sea. J Vis Exp. https://doi.org/10.3791/58213
Galloway TS, Cole M, Lewis C (2017) Interactions of microplastic debris throughout the marine ecosystem. Nat Ecol Evol 1:0116. https://doi.org/10.1038/s41559-017-0116
Gosling E (2003) How bivalves feed. In: Gosling E (ed) Bivalve molluscs: biology, ecology and culture. Blackwell, London, pp 87–130. https://doi.org/10.1002/9780470995532.ch4
Isobe A, Uchida K, Tokai T, Iwasaki S (2015) East asian seas: a hot spot of pelagic microplastics. Mar Pollut Bull 101:618–623. https://doi.org/10.1016/j.marpolbul.2015.10.042
Isobe A, Iwasaki S, Uchida K, Tokai T (2019) Abundance of non-conservative microplastics in the upper ocean from 1957 to 2066. Nat Commun 10(1):417. https://doi.org/10.1038/s41467-019-08316-9
Joint FAO/WHO Expert Committee on Food Additives (2003) Evaluation of certain food additives and contaminants: sixty-first report of the Joint FAO/WHO Expert Committee on Food Additives. WHO technical report series, 922. ISBN: 9241209224. https://apps.who.int/iris/handle/10665/42849
Kerin EJ, Gilmour CC, Roden E, Suzuki MT, Coates JD, Mason RP (2006) Mercury methylation by dissimilatory iron-reducing bacteria. Appl Environ Microbiol 72:7919–7921. https://doi.org/10.1128/aem.01602-06
Laist DW (1997) Impacts of marine debris: Entanglement of marine life in marine debris including a comprehensive list of species with entanglement and ingestion records. In: Coe JM, Rogers DB (eds) Marine debris: sources, impacts, and solutions. Springer, New York, pp 99–139. https://doi.org/10.1007/978-1-4613-8486-1_10
Lee C-S, Fisher NS (2017) Bioaccumulation of methylmercury in a marine diatom and the influence of dissolved organic matter. Mar Chem 197:70–79. https://doi.org/10.1016/j.marchem.2017.09.005
Lusher AL, Burke A, O’Connor I, Officer R (2014) Microplastic pollution in the Northeast Atlantic Ocean: validated and opportunistic sampling. Mar Pollut Bull 88:325–333. https://doi.org/10.1016/j.marpolbul.2014.08.023
Matsuyama A, Eguchi T, Sonoda I, Tada A, Yano S, Tai A, Marumoto K, Tomiyasu T, Akagi H (2011) Mercury speciation in the water of Minamata Bay, Japan. Water Air Soil Pollut 218:399–412. https://doi.org/10.1007/s11270-010-0654-z
Michels J, Stippkugel A, Lenz M, Wirtz K, Engel A (2018) Rapid aggregation of biofilm-covered microplastics with marine biogenic particles. Proc Biol Sci. https://doi.org/10.1098/rspb.2018.1203
Ministry of the Environment, Japan (2004) Mercury analysis manual. http://nimd.env.go.jp/kenkyu/docs/march_mercury_analysis_manual(e).pdf
Olenina I, Hajdu S, Edler L et al (2006) Biovolumes and size-classes of phytoplankton in the Baltic Sea. HELCOM Balt Sea Environ Proc 106:1–144
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Ravichandran M (2004) Interactions between mercury and dissolved organic matter––a review. Chemosphere 55:319–331. https://doi.org/10.1016/j.chemosphere.2003.11.011
Richard H, Carpenter EJ, Komada T, Palmer PT, Rochman CM (2019) Biofilm facilitates metal accumulation onto microplastics in estuarine waters. Sci Total Environ 683:600–608. https://doi.org/10.1016/j.scitotenv.2019.04.331
Rivera-Hernandez JR, Fernandez B, Santos-Echeandia J, Garrido S, Morante M, Santos P, Albentosa M (2019) Biodynamics of mercury in mussel tissues as a function of exposure pathway: natural vs. microplastic routes. Sci Total Environ 674:412–423. https://doi.org/10.1016/j.scitotenv.2019.04.175
Rummel CD, Jahnke A, Gorokhova E, Kühnel D, Schmitt-Jansen M (2017) Impacts of biofilm formation on the fate and potential effects of microplastic in the aquatic environment. Environ Sci Technol Lett 4:258–267. https://doi.org/10.1021/acs.estlett.7b00164
Sakamoto H, Tomiyasu T, Yonehara N (1995) The contents and chemical forms of mercury in sediments from Kagoshima Bay, in comparison with Minamata Bay and Yatsushiro Sea, southwestern Japan. Geochem J 29:97–105. https://doi.org/10.2343/geochemj.29.97
Schmidt D (1992) Mercury in Baltic and North Sea waters. Water Air Soil Pollut 62:43–55. https://doi.org/10.1007/BF00478452
Selin NE (2009) Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63. https://doi.org/10.1146/annurev.environ.051308.084314
Serranti S, Fiore L, Bonifazi G, Takeshima A, Takeuchi H, Kashiwada S (2019) Microplastics characterization by hyperspectral imaging in the SWIR range. SPIE Fut Sens Technol. https://doi.org/10.1117/12.2542793
Sikdokur E, Belivermiş M, Sezer N, Pekmez M, Bulan ÖK, Kılıç Ö (2020) Effects of microplastics and mercury on manila clam Ruditapes philippinarum: feeding rate, immunomodulation, histopathology and oxidative stress. Environ Pollut 262:114247. https://doi.org/10.1016/j.envpol.2020.114247
Stelfox M, Hudgins J, Sweet M (2016) A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs. Mar Pollut Bull 111:6–17. https://doi.org/10.1016/j.marpolbul.2016.06.034
Swarr GJ, Kading T, Lamborg CH, Hammerschmidt CR, Bowman KL (2016) Dissolved low-molecular weight thiol concentrations from the US GEOTRACES North Atlantic Ocean zonal transect. Deep Sea Res Part I Oceanogr Res Pap 116:77–87. https://doi.org/10.1016/j.dsr.2016.06.003
UNEP (2016) Marine plastic debris and microplastics—global lessons and research to inspire action and guide policy change. United Nations Environment Programme, Nairobi. http://hdl.handle.net/20.500.11822/7720. Accessed 26 Mar 2021
Van Cauwenberghe L, Claessens M, Vandegehuchte MB, Janssen CR (2015) Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina) living in natural habitats. Environ Pollut 199:10–17. https://doi.org/10.1016/j.envpol.2015.01.008
Waite HR, Donnelly MJ, Walters LJ (2018) Quantity and types of microplastics in the organic tissues of the eastern oyster Crassostrea virginica and Atlantic mud crab Panopeus herbstii from a Florida estuary. Mar Pollut Bull 129:179–185. https://doi.org/10.1016/j.marpolbul.2018.02.026
Ward JE, Zhao S, Holohan BA, Mladinich KM, Griffin TW, Wozniak J, Shumway SE (2019) Selective ingestion and egestion of plastic particles by the blue mussel (Mytilus edulis) and eastern oyster (Crassostrea virginica): Implications for using bivalves as bioindicators of microplastic pollution. Environ Sci Technol 53:8776–8784. https://doi.org/10.1021/acs.est.9b02073
Woods MN, Stack ME, Fields DM, Shaw SD, Matrai PA (2018) Microplastic fiber uptake, ingestion, and egestion rates in the blue mussel (Mytilus edulis). Mar Pollut Bull 137:638–645. https://doi.org/10.1016/j.marpolbul.2018.10.061
Yamamoto M (1996) Stimulation of elemental mercury oxidation in the presence of chloride ion in aquatic environments. Chemosphere 32:1217–1224. https://doi.org/10.1016/0045-6535(96)00008-2
Acknowledgements
We are grateful to Ms. Mayumi Onoue of the National Institute for Minamata Disease for her technical support. This project was supported by a Grant-in-Aid for a Japan Society for the Promotion of Science Research Fellow (17J04482 to CK) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and the Kurita Water and Environment Foundation (19B058 and 20K012 to CK). We also thank Natalie Kim, PhD, from Edanz Group (https://en-author-services.edanz.com/ac) for editing a draft of this manuscript.
Funding
This project was supported by a Grant-in-Aid for a Japan Society for the Promotion of Science Research Fellow (17J04482 to CK) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and the Kurita Water and Environment Foundation (19B058 and 20K012 to CK).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Rights and permissions
About this article
Cite this article
Kataoka, C., Yoshino, K., Kashiwada, S. et al. Do Polystyrene Beads Contribute to Accumulation of Methylmercury in Oysters?. Arch Environ Contam Toxicol 81, 36–45 (2021). https://doi.org/10.1007/s00244-021-00848-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-021-00848-w