Abstract
The effects of microplastic exposure in aquatic organisms have been widely reported. Nonetheless, there is limited evidence of the effects of exposure in soil systems. Thus, the objective of this study was to evaluate the effects of microplastic exposure using as a bioindicator the species Lumbricus terrestris, exposed to different concentrations of microplastic (2.5%; 5%, and 7% w/w). Avoidance bioassays were carried out for 48 h in soil with and without microplastic; the gastrointestinal tract—crop/gizzard, foregut, and midgut—was dissected and acetylcholinesterase (AChE) was used as a biomarker of neurotoxicity stress. In parallel, bioassays of microplastic ingestion were carried out, and after 48 h of initiating the ingestion assay, using a stereo and fluorescence microscope, the microplastic distribution was observed in the different earthworm segments. The results obtained in the avoidance assay indicated a lack of preference for either soil type; however, upon moving, the earthworms lost surface mucus, resulting in burns and lesions on their bodies, which were reflected in the increase in AChE enzyme levels, which was not directly related to microplastic ingestion, but rather likely acts as an external physical stress agent. The results of the ingestion bioassay showed that microplastic was present in all the earthworm segments, with a higher number of particles in the hindgut. The Lumbricus terrestris did not distinguish microplastics from soil particles, and given the high exposure concentrations, microplastics produced physical lesions on the mucus membranes of earthworms. Lumbricus terrestris showed to be a suitable bioindicator for testing the exposure to microplastic contamination in soil.
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References
Andrady, A. L. (2011). Microplastics in the marine environment. Marine Pollution Bulletin, 62(8), 1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030.
Araneda, A., Undurraga, P., López, D., Sáez, K., & Barra, R. (2016). Use of earthworms as a pesticide exposure indicator in soils under conventional and organic management. Chilean Journal of Agricultural Research, 76(3), 356–362. https://doi.org/10.4067/S0718-58392016000300014.
Arthur, C., Baker, J., Bamford, H. (2009). Proceedings of the international research workshop on the occurence, effects, and fate of microplastic marine debris. Department of Commerce, National Oceanic and Atmospheric Administration (Technical Memorandum NOSOR& R-30).
Biginagwa, F. J., Mayoma, B. S., Shashoua, Y., Syberg, K., & Khan, F. R. (2016). First evidence of microplastics in the African Great Lakes: recovery from Lake Victoria Nile perch and Nile tilapia. Journal of Great Lakes Research, 42(1), 146–149. https://doi.org/10.1016/j.jglr.2015.10.012.
Boyle, J. F. (2002). Inorganic geochemical methods in palaeolimnology. In W. M. Last & J. P. Smol (Eds.), Tracking environmental change using lake sediments. Developments in Paleoenvironmental Research (Vol. 2). Dordrecht: Springer. https://doi.org/10.1007/0-306-47670-3_5.
Calisi, A., Lionetto, M. G., & Schettino, T. (2011). Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Science of the Total Environment, 409(20), 4456–4464. https://doi.org/10.1016/j.scitotenv.2011.06.058.
Capowiez, Y., Dittbrenner, N., Rault, M., Triebskorn, R., Hedde, M., & Mazzia, C. (2010). Earthworm cast production as a new behavioural biomarker for toxicity testing. Environmental Pollution, 158, 388–393.
Cole, M., Lindeque, P., Halsband, C., & Galloway, T. S. (2011). Microplastics as contaminants in the marine environment: a review. Marine Pollution Bulletin, 62(12), 2588–2597. https://doi.org/10.1016/j.marpolbul.2011.09.025.
Cózar, A., Echevarría, F., González-Gordillo, J. I., Irigoien, X., Úbeda, B., Hernández-León, S., Palma, Á. T., Navarro, S., García-de-Lomas, J., Ruiz, A., Fernández-de-Puelles, M. L., & Duarte, C. M. (2014). Plastic debris in the open ocean. Proceedings of the National Academy of Sciences of the United States of America, 111(28), 10239–10244. https://doi.org/10.1073/pnas.1314705111.
Cuevas, M. C., Ferrera, R., Roldán, A., & Rodríquez, R. (2008). Chapter 3: Ensayo de toxicidad aguda con la lombriz de tierra Eisenia andrei. In P. Ramírez & A. Mendoza (Eds.), Ensayos toxicológicos para la evaluación de sustancias químicas en agua y suelo: La experiencia en México (pp. 211–223). Instituto Nacional de Ecología.
De Silva, P. M. C. S., & Van Gestel, C. A. M. (2009). Comparative sensitivity of Eisenia andrei and Perionyx excavatus in earthworm avoidance tests using two soil types in the tropics. Chemosphere., 77(11), 1609–1613. https://doi.org/10.1016/j.chemosphere.2009.09.034.
Desforges, J. P., Galbraith, M., & Ross, P. S. (2015). Ingestion of microplastics by zooplankton in the Northeast Pacific Ocean. Archives of Environmental Contamination and Toxicology, 69(3), 320–330. https://doi.org/10.1007/s00244-015-0172-5.
Ellman, G. L., Courtney, K. D., Andres, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88–95. https://doi.org/10.1016/0006-2952(61)90145-9.
Endo, S., Takizawa, R., Okuda, K., Takada, H., Chiba, K., Kanehiro, H., Ogi, H., Yamashita, R., & Date, T. (2005). Concentration of polychlorinated biphenyls (PCBs) in beached resin pellets: variability among individual particles and regional differences. Marine Pollution Bulletin, 50(10), 1103–1114. https://doi.org/10.1016/j.marpolbul.2005.04.030.
Fendall, L. S., & Sewell, M. A. (2009). Contributing to marine pollution by washing your face: microplastics in facial cleansers. Marine Pollution Bulletin, 58(8), 1225–1228. https://doi.org/10.1016/j.marpolbul.2009.04.025.
Galgani, F., Leaute, J. P., Moguedet, P., Souplet, A., Verin, Y., Carpentier, A., Goraguer, H., Latrouite, D., Andral, B., Cadiou, Y., Mahe, J. C., Poulard, J. C., & Nerisson, P. (2000). Litter on the sea floor along European coasts. Marine Pollution Bulletin, 40(6), 516–527. https://doi.org/10.1016/S0025-326X(99)00234-9.
Gornall, A. G., Bardawill, C. J., & David, M. M. (1949). Determination of serum proteins by means of the Biuret reaction. The Journal of Biological Chemistry, 177, 751–766.
Hallam, J., & Hodson, M. E. (2020). Impact of different earthworm ecotypes on water stable aggregates and soil water holding capacity. Biology and Fertility of Soils. https://doi.org/10.1007/s00374-020-01432-5.
Hodson, M. E., Duffus-Hodson, C. A., Clark, A., Prendergast-Miller, M. T., & Thorpe, K. L. (2017). Plastic bag derived-microplastics as a vector for metal exposure in terrestrial invertebrates. Environmental Science & Technology, 51(8), 4714–4721. https://doi.org/10.1021/acs.est.7b00635.
Huerta Lwanga, E., Gertsen, H., Gooren, H., Peters, P., Salánki, T., Van, d. P. M., Besseling, E., Koelmans, A. A., & Geissen, V. (2016). Microplastics in the terrestrial ecosystem: Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environmental Science & Technology, 50(5), 2685–2691. https://doi.org/10.1021/acs.est.5b05478.
Huerta Lwanga, E., Gertsen, H., Gooren, H., Peters, P., Salánki, T., Ploeg, M. V. D., Besseling, E., Koelmans, A. A., & Geissen, V. (2017). Incorporation of microplastics from litter into burrows of Lumbricus terrestris. Environmental Pollution, 220(PartA), 523–531. https://doi.org/10.1016/j.envpol.2016.09.096.
International Organization for Standardization (1993). Soil quality -effects of pollutants on earthworms (Eisenia fetida). Part 1: Determination of acute toxicity using artificial soil substrate. No.11268–1. Geneva.
International Organization for Standardization (1998). Soil quality -effects of pollutants on earthworms (Eisenia fetida). Part 2: Determination of effects on reproduction. No. 11268–2. Geneva.
International Organization for Standardization (2008). Soil quality— avoidance tests for determining the quality of soils and effects of chemicals on behaviour — part 1: test with earthworms (Eisenia fetida and Eisenia andrei). N°17512-1. Geneva, Switzerland.
Jambeck, J. R., Geyer, R., Wilcox, C., Siegler, T. R., Perryman, M., Andrady, A., Narayan, R., & Law, K. L. (2015). Plastic waste inputs from land into the ocean. Science., 347(6223), 768–771. https://doi.org/10.1126/science.1260352.
Kedzierski, M., Le Tilly, V., Bourseau, P., Bellegou, H., César, G., Sire, O., & Bruzaud, S. (2016). Microplastics elutriation from sandy sediments: a granulometric approach. Marine Pollution Bulletin, 107(1), 315–323. https://doi.org/10.1016/j.marpolbul.2016.03.041.
Kokalj, A. J., Horvat, P., Skalar, T., & Kržan, A. (2018). Plastic bag and facial cleanser derived microplastic do not affect feeding behaviour and energy reserves of terrestrial isopods. Sci. Total Environ., 615, 761–766. https://doi.org/10.1016/j.scitotenv.2017.10.020.
Law, K. L., & Thompson, R. C. (2014). Microplastics in the seas. Science., 345(6193), 144–145. https://doi.org/10.1126/science.1254065.
Lee, J., Hong, S., Song, Y. K., Hong, S. H., Jang, Y. C., Jang, M., Heo, N. W., Han, G. M., Lee, M. J., Kang, D., & Shim, W. J. (2013). Relationships among the abundances of plastic debris in different size classes on beaches in South Korea. Marine Pollution Bulletin, 77(1–2), 349–354. https://doi.org/10.1016/j.marpolbul.2013.08.013.
NCh 1515 Of. (1979). Mecánica de suelos – Determinación de la humedad. Santiago: Instituto Nacional de Normalización.
Perreault, J. M., & Whalen, J. K. (2006). Earthworm burrowing in laboratory microcosms as influenced by soil temperature and moisture. Pedobiologia, 50, 397–403.
Prendergast-Miller, M. T., Katsiamides, A., Abbass, M., Sturzenbaum, S. R., Thorpe, K. L., & Hodson, M. E. (2019). Polyester-derived microfibre impacts on the soil-dwelling earthworm Lumbricus terrestris. Environmental Pollution, 251, 453–459. https://doi.org/10.1016/j.envpol.2019.05.037.
Qiang, L. Y., & Cheng, J. P. (2019). Exposure to microplastics decreases swimming competence in larval zebrafish (Danio rerio). Ecotoxicology and Environmental Safety, 176, 226–233. https://doi.org/10.1016/j.ecoenv.2019.03.088.
Qiu, Q. X., Peng, J. P., Yu, X. B., Chen, F. C. Z., Wang, J. D., & Dong, F. Q. (2015). Occurrence of microplastics in the coastal marine environment: first observation on sediment of China. Marine Pollution Bulletin, 98(1–2), 274–280. https://doi.org/10.1016/j.marpolbul.2015.07.028.
Rault, M., Mazzia, C., & Capowiez, Y. (2007). Tissue distribution and characterization of cholinesterase activity in six earthworm species. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 147(2), 340–346. https://doi.org/10.1016/j.cbpb.2007.01.022.
Rodriguez-Seijo, A., Lourenço, J., Rocha-Santos, T. A. P., da Costa, J., Duarte, A. C., Vala, H., & Pereira, R. (2017). Histopathological and molecular effects of microplastics in Eisenia andrei Bouche. Environmental Pollution, 220(PartA), 495–503. https://doi.org/10.1016/j.envpol.2016.09.092.
Song, Y., Cao, C. J., Qiu, R., Hu, J. N., Liu, M. T., Lu, S. B., Shi, H. H., Raley-Susman, K. M., Kathleen, M., & He, D. F. (2019). Uptake and adverse effects of polyethylene terephthalate microplastics fibers on terrestrial snails (Achatina fulica) after soil exposure. Environmental Pollution, 250, 447–455. https://doi.org/10.1016/j.envpol.2019.04.066.
Teuten, E. L., Rowland, S. J., & Galloway, T. S. (2007). Potential for plastics to transport hydrophobic contaminants. Environmental Science & Technology, 41(22), 7759–7764. https://doi.org/10.1021/es071737s.
Teuten, E. L., Saquing, J. M., Knappe, D. R. U., Barlaz, M. A., Jonsson, S., Bjorn, A., Rowland, S. J., Thompson, R. C., Galloway, T. S., Yamashita, R., Ochi, D., Watanuki, Y., Moore, C., Viet, P. H., Tana, T. S., Prudente, M., Boonyatumanond, R., Zakaria, M. P., Akkhavong, K., Ogata, Y., Hirai, H., Iwasa, S., Mizukawa, K., Hagino, Y., Imamura, A., Saha, M., & Takada, H. (2009). Transport and release of chemicals from plastics to the environment and to wildlife. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 364(1526), 2027–2045. https://doi.org/10.1098/rstb.2008.0284.
Van Cauwenberghe, L., Devriese, L., Galgani, F., Robbens, J., & Janssen, C. R. (2015). Microplastics in sediments: a review of techniques, occurrence and effects. Marine Environmental Research, 111, 5–17. https://doi.org/10.1016/j.marenvres.2015.06.007.
Wesch, C., Barthel, A. K., Braun, U., Klein, R., & Paulus, M. (2016). No microplastics in benthic eelpout (Zoarces viviparus): an urgent need for spectroscopic analyses in microplastic detection. Environmental Research, 148, 36–38. https://doi.org/10.1016/j.envres.2016.03.017.
Wheelock, C. E., Eder, K. J., Werner, I., Huang, H., Jones, P. D., Brammell, B. F., Elskus, A. A., & Hammock, B. D. (2005). Individual variability in esterase activity and CYP1A levels in Chinook salmon (Oncorhynchus tshawytscha) exposed to esfenvalerate and chlorpyrifos. Aquatic Toxicology, 74(2), 172–192. https://doi.org/10.1016/j.aquatox.2005.05.009.
Wurl, O., & Obbard, J. P. (2004). A review of pollutants in the sea-surface microlayer (SML): a unique habitat for marine organisms. Marine Pollution Bulletin, 48(11–12), 1016–1030. https://doi.org/10.1016/j.marpolbul.2004.03.016.
Young, A. M., & Elliott, J. A. (2016). Characterization of microplastic and mesoplastic debris in sediments from Kamilo Beach and Kahuku Beach, Hawai’i. Marine Pollution Bulletin, 113(1–2), 477–482. https://doi.org/10.1016/j.marpolbul.2016.11.009.
Zhao, S. Y., Zhu, L. X., Wang, T., & Li, D. J. (2014). Suspended microplastics in the surface water of the Yangtze Estuary System, China: first observations on occurrence, distribution. Marine Pollution Bulletin, 86(1–2), 562–568. https://doi.org/10.1016/j.marpolbul.2014.06.032.
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This research was supported by CRHIAM/ANID/FONDAP 15130015 and by FONDECYT 1180063 granted to Ricardo Barra.
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Baeza, C., Cifuentes, C., González, P. et al. Experimental Exposure of Lumbricus terrestris to Microplastics. Water Air Soil Pollut 231, 308 (2020). https://doi.org/10.1007/s11270-020-04673-0
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DOI: https://doi.org/10.1007/s11270-020-04673-0