Understanding the harmful effects of polyethylene microplastics on Eisenia fetida: A toxicological evaluation
Article Main
Abstract
Microplastics, measuring less than 5 mm, are pervasive environmental pollutants raising concerns about their toxic effects on terrestrial ecosystems, especially earthworms.A comprehensive toxicological evaluation of polyethylene microplastics on earthworms will be beneficial for determining the detrimental impacts of these ubiquitous pollutants on soil ecosystem. Therefore, in the present study, the best representative soil organism, earthworms (Eisenia fetida), were opted for examining the toxicological effect of polyethylene microplastic. E. fetida were subjected to different concentrations of polyethylene microplastic (200, 400, 600, 800, and 1000 mg/kg) in soil and randomly picked out on days 7 to 56. Earthworms exposed to higher concentration of polyethylene (1000 mg/kg of artificial soil) showed a significant reduction in body weight and cocoon formation after 35th days of incubation. A consistent decrease in the concentration of carbohydrates, lipids, and protein was observed when the worms were exposed to the higher concentration of polyethylene. Further, antioxidant enzymes like superoxide dismutase, glutathione S-transferase, peroxidase, catalase, and malondialdehyde were determined for antioxidant stress.Exposure of 200 mg/kg to 1000 mg/kg of artificial soil caused a prominent amplification in the build-up of malonedialdehyde (a biological marker of oxidative stress) by 1.29-fold. It also considerably augmented the activity of the antioxidant enzymes viz., glutathione S-transferase (1.54-fold), superoxide dismutase (1.51-fold), peroxidase (1.25-fold), and catalase (1.87-fold). The present study's findings provide a new understanding of the toxic effect of microplastic on earthworm E. fetida, presenting a foundation for its risk evaluation on soil ecosystems and non-target biological toxicity.
Article Details
Article Details
Keywords
Antioxidant enzymes, Eisenia fetida, Polyethylene, Soil pollution, Toxicity
References
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Büks, F. & Kaupenjohann, M. (2020). Global concentrations of microplastics in soils–a review. Soil, 6(2), 649-662. https://doi.org/10.5194/soil-6-649-2020
Boots, B., Russell, C. W. & Green, D. S. (2019). Effects of Microplastics in Soil Ecosystems: Above and Below Ground. Environmental Science & Technology, 53(19), 11496–11506. https://doi.org/10.1021/acs.est.9b03304
Cao, D., Wang, X., Luo, X., Liu, G. & Zheng, H. (2017). Effects of polystyrene microplastics on the fitness of earthworms in an agricultural soil. IOP Conference Series: Earth and Environmental Science, 61(1), 012148. https://doi.org/10.1088/1755-1315/61/1/012148
Chen, K., Tang, R., Luo, Y., Chen, Y., EI-Naggar, A., Du, J., Bu, A., Yan, Y., Lu, X., Cai, Y. & Chang, S. X. (2022). Transcriptomic and metabolic responses of earthworms to contaminated soil with polypropylene and polyethylene microplastics at environmentally relevant concentrations. Journal of Hazardous Materials, 427, 128176. https://doi.org/10.1016/j.jhazmat.2021.128176
Chen, Y., Liu, X., Leng, Y.& Wang, J. (2020). Defense responses in earthworms (Eiseniafetida) exposed to low-density polyethylene microplastics in soils. Ecotoxicology and Environmental Safety, 187, 109788. https://doi.org/10.1016/j.ecoenv.2019.109788
Chiu, H.-W., Xia, T., Lee, Y.-H., Chen, C.-W., Tsai, J.-C.& Wang, Y.-J. (2015). Cationic polystyrene nanospheres induce autophagic cell death through the induction of endoplasmic reticulum stress. Nanoscale, 7(2), 736–746. https://doi.org/10.1039/c4nr05509h
Claiborne, A. L. (2018). Catalase activity. In CRC handbook of methods for oxygen radical research (pp. 283–284). CRC press.
De Coen, W. M.& Janssen, C. R. (1997). The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: A new methodology to assess the energy budget of toxicant-stressed Daphnia populations. Journal of Aquatic Ecosystem Stress and Recovery, 6(1), 43–55. https://doi.org/10.1023/A:1008228517955
Ding, W., Li, Z., Qi, R., Jones, D. L., Liu, Q., Liu, Q. & Yan, C. (2021). Effect thresholds for the earthworm Eisenia fetida: Toxicity comparison between conventional and biodegradable microplastics. Science of The Total Environment, 781, 146884. https://doi.org/10.1016/j.scitotenv.2021.146884
Dong, Y., Gao, M., Song, Z.& Qiu, W. (2020). Microplastic particles increase arsenic toxicity to rice seedlings. Environmental Pollution, 259, 113892. https://doi.org/10.1016/j.envpol.2019.113892
Gao, C., Xu, J., Li, J.& Liu, Z. (2016). Determination of Metallothionein, Malondialdehyde, and Antioxidant Enzymes in Earthworms (Eisenia fetida) Following Exposure to Chromium. Analytical Letters, 49(11), 1748–1757. https://doi.org/10.1080/00032719.2015.1120738
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Hans, R. K., Khan, M. A., Farooq, M. & Beg, M. U. (1993). Glutathione-S-transferase activity in an earthworm (Pheretimaposthuma) exposed to three insecticides. Soil Biology and Biochemistry, 25(4), 509–511. https://doi.org/10.1016/0038-0717(93)90076-N
He, F., Liu, Q., Jing, M., Wan, J., Huo, C., Zong, W., Tang, J. & Liu, R. (2021). Toxic mechanism on phenanthrene-induced cytotoxicity, oxidative stress and activity changes of superoxide dismutase and catalase in earthworm (Eisenia foetida): A combined molecular and cellular study. Journal of Hazardous Materials, 418, 126302. https://doi.org/10.1016/j.jhazmat.2021.126302
Huerta Lwanga, E., Gertsen, H., Gooren, H., Peters, P., Salánki, T., van der Ploeg, M., Besseling, E., Koelmans, A. A. &Geissen, V. (2016). Microplastics in the Terrestrial Ecosystem: Implications for Lumbricusterrestris (Oligochaeta, Lumbricidae). Environmental Science & Technology, 50(5), 2685–2691. https://doi.org/10.1021/acs.est.5b05478
Ju, H., Zhu, D. & Qiao, M. (2019). Effects of polyethylene microplastics on the gut microbial community, reproduction and avoidance behaviors of the soil springtail, Folsomiacandida. Environmental Pollution (Barking, Essex: 1987), 247, 890–897. https://doi.org/10.1016/j.envpol.2019.01.097
Judy, J. D., Williams, M., Gregg, A., Oliver, D., Kumar, A., Kookana, R.& Kirby, J. K. (2019). Microplastics in municipal mixed-waste organic outputs induce minimal short to long-term toxicity in key terrestrial biota. Environmental Pollution, 252, 522–531. https://doi.org/10.1016/j.envpol.2019.05.027
Kochba, J., Lavee, S. & Spiegel-Roy, P. (1977). Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’ orange ovular callus lines1. Plant and Cell Physiology, 18(2), 463–467. https://doi.org/10.1093/oxfordjournals.pcp.a075455
Lahive, E., Walton, A., Horton, A. A., Spurgeon, D. J. & Svendsen, C. (2019). Microplastic particles reduce reproduction in the terrestrial worm Enchytraeuscrypticus in a soil exposure. Environmental Pollution, 255, 113174. https://doi.org/10.1016/j.envpol.2019.113174
Lei, K., Qiao, F., Liu, Q., Wei, Z., Qi, H., Cui, S., Yue, X., Deng, Y.& An, L. (2017). Microplastics releasing from personal care and cosmetic products in China. Marine Pollution Bulletin, 123(1), 122–126. https://doi.org/10.1016/j.marpolbul.2017.09.016
Li, M., Jia, H., Gao, Q., Han, S., Yu, Y.& Sun, L. (2023). Influence of aged and pristine polyethylene microplastics on bioavailability of three heavy metals in soil: Toxic effects to earthworms (Eisenia fetida). Chemosphere, 311, 136833. https://doi.org/10.1016/j.chemosphere.2022.136833
Lowry, O. H., Rosebrough, N. J., Farr, A. L.& Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265–275.
Miller, G. L. (1959). Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Analytical Chemistry, 31(3), 426–428. https://doi.org/10.1021/ac60147a030
Muñoz Meneses, R. A., Cabrera-Papamija, G., Machuca-Martínez, F., Rodríguez, L. A., Diosa, J. E. & Mosquera-Vargas, E. (2022). Plastic recycling and their use as raw material for the synthesis of carbonaceous materials. Heliyon, 8(3), e09028. https://doi.org/10.1016/j.heliyon.2022.e09028
Nel, A., Xia, T., Mädler, L.& Li, N. (2006). Toxic potential of materials at the nanolevel. Science (New York, N.Y.), 311(5761), 622–627. https://doi.org/10.1126/science.1114397
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 Lumbricusterrestris. Environmental Pollution, 251, 453–459. https://doi.org/10.1016/j.envpol.2019.05.037
Rillig, M. C., Ziersch, L.& Hempel, S. (2017). Microplastic transport in soil by earthworms. Scientific Reports, 7(1), 1–6. https://doi.org/10.1038/s41598-017-01594-7
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 Bouché. Environmental Pollution, 220, 495–503. https://doi.org/10.1016/j.envpol.2016.09.092
Sajjad, M., Huang, Q., Khan, S., Khan, M. A., Liu, Y., Wang, J., Lian, F., Wang, Q.& Guo, G. (2022). Microplastics in the soil environment: A critical review. Environmental Technology & Innovation, 27, 102408. https://doi.org/10.1016/j.eti.2022.102408
Sobhani, Z., Panneerselvan, L., Fang, C., Naidu, R.&Megharaj, M. (2022). Chronic and transgenerational effects of polyethylene microplastics at environmentally relevant concentrations in earthworms. Environmental Technology & Innovation, 25, 102226. https://doi.org/10.1016/j.eti.2021.102226
Song, Y., Zhu, L. S., Wang, J., Wang, J. H., Liu, W. & Xie, H. (2009). DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biology and Biochemistry, 41(5), 905–909. https://doi.org/10.1016/j.soilbio.2008.09.009
Sun, W., Meng, Z., Li, R., Zhang, R., Jia, M., Yan, S., Tian, S., Zhou, Z.& Zhu, W. (2021). Joint effects of microplastic and dufulin on bioaccumulation, oxidative stress and metabolic profile of the earthworm (Eisenia fetida). Chemosphere, 263, 128171. https://doi.org/10.1016/j.chemosphere.2020.128171
Tang, R., Ying, M., Luo, Y., El-Naggar, A., Palansooriya, K. N., Sun, T., Cao, Y., Diao, Z., Zhang, Y., Lian, Y., Chen, K., Yan, Y., Lu, X., Cai, Y.& Chang, S. X. (2023). Microplastic pollution destabilized the osmoregulatory metabolism but did not affect intestinal microbial biodiversity of earthworms in soil. Environmental Pollution, 320, 121020. https://doi.org/10.1016/j.envpol.2023.121020
Thakur, S. S.& Yadav, S. (2018). Exploration of earthworms of India through online digital library. IntechOpen London, UK.
Valavanidis, A., Vlachogianni, T., Fiotakis, K.&Loridas, S. (2013). Pulmonary Oxidative Stress, Inflammation and Cancer: Respirable Particulate Matter, Fibrous Dusts and Ozone as Major Causes of Lung Carcinogenesis through Reactive Oxygen Species Mechanisms. International Journal of Environmental Research and Public Health, 10(9), 3886–3907. https://doi.org/10.3390/ijerph10093886
Wang, H.-T., Ding, J., Xiong, C., Zhu, D., Li, G., Jia, X.-Y., Zhu, Y.-G. & Xue, X.-M. (2019). Exposure to microplastics lowers arsenic accumulation and alters gut bacterial communities of earthworm Metaphire californica. Environmental Pollution, 251, 110–116. https://doi.org/10.1016/j.envpol.2019.04.054
Wang, X., Li, C., Liu, K., Zhu, L., Song, Z.& Li, D. (2020). Atmospheric microplastic over the South China Sea and East Indian Ocean: Abundance, distribution and source. Journal of Hazardous Materials, 389, 121846. https://doi.org/10.1016/j.jhazmat.2019.121846
Zhang, S., Ren, S., Pei, L., Sun, Y. & Wang, F. (2022). Ecotoxicological effects of polyethylene microplastics and ZnO nanoparticles on earthworm Eisenia fetida. Applied Soil Ecology, 176, 104469. https://doi.org/10.1016/j.apsoil.2022.104469
Zhou, Y., Liu, X. & Wang, J. (2020). Ecotoxicological effects of microplastics and cadmium on the earthworm Eisenia foetida. Journal of Hazardous Materials, 392, 122273. https://doi.org/10.1016/j.jhazmat.2020.122273
Zhu, D., Chen, Q.-L., An, X.-L., Yang, X.-R., Christie, P., Ke, X., Wu, L.-H.& Zhu, Y.-G. (2018). Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition. Soil Biology and Biochemistry, 116, 302–310. https://doi.org/10.1016/j.soilbio.2017.10.027
Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911–917.
Büks, F. & Kaupenjohann, M. (2020). Global concentrations of microplastics in soils–a review. Soil, 6(2), 649-662. https://doi.org/10.5194/soil-6-649-2020
Boots, B., Russell, C. W. & Green, D. S. (2019). Effects of Microplastics in Soil Ecosystems: Above and Below Ground. Environmental Science & Technology, 53(19), 11496–11506. https://doi.org/10.1021/acs.est.9b03304
Cao, D., Wang, X., Luo, X., Liu, G. & Zheng, H. (2017). Effects of polystyrene microplastics on the fitness of earthworms in an agricultural soil. IOP Conference Series: Earth and Environmental Science, 61(1), 012148. https://doi.org/10.1088/1755-1315/61/1/012148
Chen, K., Tang, R., Luo, Y., Chen, Y., EI-Naggar, A., Du, J., Bu, A., Yan, Y., Lu, X., Cai, Y. & Chang, S. X. (2022). Transcriptomic and metabolic responses of earthworms to contaminated soil with polypropylene and polyethylene microplastics at environmentally relevant concentrations. Journal of Hazardous Materials, 427, 128176. https://doi.org/10.1016/j.jhazmat.2021.128176
Chen, Y., Liu, X., Leng, Y.& Wang, J. (2020). Defense responses in earthworms (Eiseniafetida) exposed to low-density polyethylene microplastics in soils. Ecotoxicology and Environmental Safety, 187, 109788. https://doi.org/10.1016/j.ecoenv.2019.109788
Chiu, H.-W., Xia, T., Lee, Y.-H., Chen, C.-W., Tsai, J.-C.& Wang, Y.-J. (2015). Cationic polystyrene nanospheres induce autophagic cell death through the induction of endoplasmic reticulum stress. Nanoscale, 7(2), 736–746. https://doi.org/10.1039/c4nr05509h
Claiborne, A. L. (2018). Catalase activity. In CRC handbook of methods for oxygen radical research (pp. 283–284). CRC press.
De Coen, W. M.& Janssen, C. R. (1997). The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: A new methodology to assess the energy budget of toxicant-stressed Daphnia populations. Journal of Aquatic Ecosystem Stress and Recovery, 6(1), 43–55. https://doi.org/10.1023/A:1008228517955
Ding, W., Li, Z., Qi, R., Jones, D. L., Liu, Q., Liu, Q. & Yan, C. (2021). Effect thresholds for the earthworm Eisenia fetida: Toxicity comparison between conventional and biodegradable microplastics. Science of The Total Environment, 781, 146884. https://doi.org/10.1016/j.scitotenv.2021.146884
Dong, Y., Gao, M., Song, Z.& Qiu, W. (2020). Microplastic particles increase arsenic toxicity to rice seedlings. Environmental Pollution, 259, 113892. https://doi.org/10.1016/j.envpol.2019.113892
Gao, C., Xu, J., Li, J.& Liu, Z. (2016). Determination of Metallothionein, Malondialdehyde, and Antioxidant Enzymes in Earthworms (Eisenia fetida) Following Exposure to Chromium. Analytical Letters, 49(11), 1748–1757. https://doi.org/10.1080/00032719.2015.1120738
Griffith, C. M., Thai, A. C.& Larive, C. K. (2019). Metabolite biomarkers of chlorothalonil exposure in earthworms, coelomic fluid, and coelomocytes. Science of The Total Environment, 681, 435–443. https://doi.org/10.1016/j.scitotenv.2019.04.312
Hans, R. K., Khan, M. A., Farooq, M. & Beg, M. U. (1993). Glutathione-S-transferase activity in an earthworm (Pheretimaposthuma) exposed to three insecticides. Soil Biology and Biochemistry, 25(4), 509–511. https://doi.org/10.1016/0038-0717(93)90076-N
He, F., Liu, Q., Jing, M., Wan, J., Huo, C., Zong, W., Tang, J. & Liu, R. (2021). Toxic mechanism on phenanthrene-induced cytotoxicity, oxidative stress and activity changes of superoxide dismutase and catalase in earthworm (Eisenia foetida): A combined molecular and cellular study. Journal of Hazardous Materials, 418, 126302. https://doi.org/10.1016/j.jhazmat.2021.126302
Huerta Lwanga, E., Gertsen, H., Gooren, H., Peters, P., Salánki, T., van der Ploeg, M., Besseling, E., Koelmans, A. A. &Geissen, V. (2016). Microplastics in the Terrestrial Ecosystem: Implications for Lumbricusterrestris (Oligochaeta, Lumbricidae). Environmental Science & Technology, 50(5), 2685–2691. https://doi.org/10.1021/acs.est.5b05478
Ju, H., Zhu, D. & Qiao, M. (2019). Effects of polyethylene microplastics on the gut microbial community, reproduction and avoidance behaviors of the soil springtail, Folsomiacandida. Environmental Pollution (Barking, Essex: 1987), 247, 890–897. https://doi.org/10.1016/j.envpol.2019.01.097
Judy, J. D., Williams, M., Gregg, A., Oliver, D., Kumar, A., Kookana, R.& Kirby, J. K. (2019). Microplastics in municipal mixed-waste organic outputs induce minimal short to long-term toxicity in key terrestrial biota. Environmental Pollution, 252, 522–531. https://doi.org/10.1016/j.envpol.2019.05.027
Kochba, J., Lavee, S. & Spiegel-Roy, P. (1977). Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’ orange ovular callus lines1. Plant and Cell Physiology, 18(2), 463–467. https://doi.org/10.1093/oxfordjournals.pcp.a075455
Lahive, E., Walton, A., Horton, A. A., Spurgeon, D. J. & Svendsen, C. (2019). Microplastic particles reduce reproduction in the terrestrial worm Enchytraeuscrypticus in a soil exposure. Environmental Pollution, 255, 113174. https://doi.org/10.1016/j.envpol.2019.113174
Lei, K., Qiao, F., Liu, Q., Wei, Z., Qi, H., Cui, S., Yue, X., Deng, Y.& An, L. (2017). Microplastics releasing from personal care and cosmetic products in China. Marine Pollution Bulletin, 123(1), 122–126. https://doi.org/10.1016/j.marpolbul.2017.09.016
Li, M., Jia, H., Gao, Q., Han, S., Yu, Y.& Sun, L. (2023). Influence of aged and pristine polyethylene microplastics on bioavailability of three heavy metals in soil: Toxic effects to earthworms (Eisenia fetida). Chemosphere, 311, 136833. https://doi.org/10.1016/j.chemosphere.2022.136833
Lowry, O. H., Rosebrough, N. J., Farr, A. L.& Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265–275.
Miller, G. L. (1959). Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Analytical Chemistry, 31(3), 426–428. https://doi.org/10.1021/ac60147a030
Muñoz Meneses, R. A., Cabrera-Papamija, G., Machuca-Martínez, F., Rodríguez, L. A., Diosa, J. E. & Mosquera-Vargas, E. (2022). Plastic recycling and their use as raw material for the synthesis of carbonaceous materials. Heliyon, 8(3), e09028. https://doi.org/10.1016/j.heliyon.2022.e09028
Nel, A., Xia, T., Mädler, L.& Li, N. (2006). Toxic potential of materials at the nanolevel. Science (New York, N.Y.), 311(5761), 622–627. https://doi.org/10.1126/science.1114397
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 Lumbricusterrestris. Environmental Pollution, 251, 453–459. https://doi.org/10.1016/j.envpol.2019.05.037
Rillig, M. C., Ziersch, L.& Hempel, S. (2017). Microplastic transport in soil by earthworms. Scientific Reports, 7(1), 1–6. https://doi.org/10.1038/s41598-017-01594-7
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 Bouché. Environmental Pollution, 220, 495–503. https://doi.org/10.1016/j.envpol.2016.09.092
Sajjad, M., Huang, Q., Khan, S., Khan, M. A., Liu, Y., Wang, J., Lian, F., Wang, Q.& Guo, G. (2022). Microplastics in the soil environment: A critical review. Environmental Technology & Innovation, 27, 102408. https://doi.org/10.1016/j.eti.2022.102408
Sobhani, Z., Panneerselvan, L., Fang, C., Naidu, R.&Megharaj, M. (2022). Chronic and transgenerational effects of polyethylene microplastics at environmentally relevant concentrations in earthworms. Environmental Technology & Innovation, 25, 102226. https://doi.org/10.1016/j.eti.2021.102226
Song, Y., Zhu, L. S., Wang, J., Wang, J. H., Liu, W. & Xie, H. (2009). DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biology and Biochemistry, 41(5), 905–909. https://doi.org/10.1016/j.soilbio.2008.09.009
Sun, W., Meng, Z., Li, R., Zhang, R., Jia, M., Yan, S., Tian, S., Zhou, Z.& Zhu, W. (2021). Joint effects of microplastic and dufulin on bioaccumulation, oxidative stress and metabolic profile of the earthworm (Eisenia fetida). Chemosphere, 263, 128171. https://doi.org/10.1016/j.chemosphere.2020.128171
Tang, R., Ying, M., Luo, Y., El-Naggar, A., Palansooriya, K. N., Sun, T., Cao, Y., Diao, Z., Zhang, Y., Lian, Y., Chen, K., Yan, Y., Lu, X., Cai, Y.& Chang, S. X. (2023). Microplastic pollution destabilized the osmoregulatory metabolism but did not affect intestinal microbial biodiversity of earthworms in soil. Environmental Pollution, 320, 121020. https://doi.org/10.1016/j.envpol.2023.121020
Thakur, S. S.& Yadav, S. (2018). Exploration of earthworms of India through online digital library. IntechOpen London, UK.
Valavanidis, A., Vlachogianni, T., Fiotakis, K.&Loridas, S. (2013). Pulmonary Oxidative Stress, Inflammation and Cancer: Respirable Particulate Matter, Fibrous Dusts and Ozone as Major Causes of Lung Carcinogenesis through Reactive Oxygen Species Mechanisms. International Journal of Environmental Research and Public Health, 10(9), 3886–3907. https://doi.org/10.3390/ijerph10093886
Wang, H.-T., Ding, J., Xiong, C., Zhu, D., Li, G., Jia, X.-Y., Zhu, Y.-G. & Xue, X.-M. (2019). Exposure to microplastics lowers arsenic accumulation and alters gut bacterial communities of earthworm Metaphire californica. Environmental Pollution, 251, 110–116. https://doi.org/10.1016/j.envpol.2019.04.054
Wang, X., Li, C., Liu, K., Zhu, L., Song, Z.& Li, D. (2020). Atmospheric microplastic over the South China Sea and East Indian Ocean: Abundance, distribution and source. Journal of Hazardous Materials, 389, 121846. https://doi.org/10.1016/j.jhazmat.2019.121846
Zhang, S., Ren, S., Pei, L., Sun, Y. & Wang, F. (2022). Ecotoxicological effects of polyethylene microplastics and ZnO nanoparticles on earthworm Eisenia fetida. Applied Soil Ecology, 176, 104469. https://doi.org/10.1016/j.apsoil.2022.104469
Zhou, Y., Liu, X. & Wang, J. (2020). Ecotoxicological effects of microplastics and cadmium on the earthworm Eisenia foetida. Journal of Hazardous Materials, 392, 122273. https://doi.org/10.1016/j.jhazmat.2020.122273
Zhu, D., Chen, Q.-L., An, X.-L., Yang, X.-R., Christie, P., Ke, X., Wu, L.-H.& Zhu, Y.-G. (2018). Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition. Soil Biology and Biochemistry, 116, 302–310. https://doi.org/10.1016/j.soilbio.2017.10.027
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Understanding the harmful effects of polyethylene microplastics on Eisenia fetida: A toxicological evaluation. (2023). Journal of Applied and Natural Science, 15(4), 1520-1528. https://doi.org/10.31018/jans.v15i4.5056
