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Feeding, excretion, survival, and histological alterations in zebrafish Danio rerio from single and combined exposure to microplastics and copper

  • Hyeon Jin Kim (Department of Aqualife Medicine, Chonnam National University) ;
  • So Ryung Shin (Department of Aqualife Medicine, Chonnam National University) ;
  • Jung Jun Park (Aquaculture Industry Research Division, East Sea Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Jung Sick Lee (Department of Aqualife Medicine, Chonnam National University)
  • 투고 : 2023.11.29
  • 심사 : 2024.02.08
  • 발행 : 2024.03.31

초록

This study evaluated the risk of single and combined exposure to microplastics in zebrafish (Danio rerio) through biomarkers, such as survival rate, excretion rate, and histological alterations of organ systems. The experimental groups were the control(Cont.), single microplastics exposure group(MPs, 1.83%/fish total weight(g)), the copper group(Cu, 21.6 ㎍ L-1), and a group with combined exposure to MPs and copper (MPs*Cu). The experiment was conducted with individual exposure (7 days) for MP excretion rate analysis and group exposure (14 days) for biomarker analysis. The daily excretion rate of MPs tended to decrease in a time-dependent manner. The copper concentration in the body was not significantly different between single and combined copper exposure. The degeneration of mucous cells in the skin, capillary dilation of the gill lamella, increased intestinal mucous, hepatocyte hypertrophy, and the degeneration of glomeruli and renal tubules were observed in all exposure groups. These histological alterations showed the highest tendency in the MPs*Cu group. In this study, the changes in biomarkers were attributed to the single effect of copper or the combined effect of copper and MPs rather than being solely influenced by MPs.

키워드

과제정보

This work was supported by a grant from the National Institute of Fisheries Science (R2024046) of South Korea.

참고문헌

  1. Al-Bairuty GA, BJ Shaw, RD Handy and TB Henry. 2013. Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 126:104-115. https://doi.org/10.1016/j.aquatox.2012.10.005
  2. Avio CG, S Gorbi and F Regoli. 2017. Plastics and microplastics in the oceans: from emerging pollutants to emerged threat. Mar. Environ. Res. 128:2-11. https://doi.org/10.1016/j.marenvres.2016.05.012
  3. Bakir A, SJ Rowland and RC Thompson. 2012. Competitive sorption of persistent organic pollutants onto microplastics in the marine environment. Mar. Pollut. Bull. 64:2782-2789. https://doi.org/10.1016/j.marpolbul.2012.09.010
  4. Benedetti I, AG Albano and L Mola. 1989. Histomorphological changes in some organs of the brown bullhead, Ictalurus nebulosus LeSueur, following short- and long-term exposure to copper. J. Fish Biol. 34:273-280. https://doi.org/10.1111/j.1095-8649.1989.tb03308.x
  5. Boerger CM, GL Lattin, SL Moore and CJ Moore. 2010. Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Mar. Pollut. Bull. 60:2275-2278. https://doi.org/10.1016/j.marpolbul.2010.08.007
  6. Chen Q, M Gundlach, S Yang, J Jiang, M Velki, D Yin and H Hollert. 2017. Quantitative investigation of the mechanisms of microplastics and nanoplastics toward zebrafish larvae locomotor activity. Sci. Total Environ. 584:1022-1031. https://doi.org/10.1016/j.scitotenv.2017.01.156
  7. Chen X, J Wang, Y Xie, Y Ma, J Zhang, H Wei and AIE Abdou. 2022. Physiological response and oxidative stress of grass carp (Ctenopharyngodon idellus) under single and combined toxicity of polystyrene microplastics and cadmium. Ecotox. Environ. Safe. 245:114080. https://doi.org/10.1016/j.ecoenv.2022.114080
  8. Chen YC, M Priyadarshini and P Panula. 2009. Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem. Cell Biol. 132:375-381. https://doi.org/10.1007/s00418-009-0619-8
  9. Choi JS, YJ Jung, NH Hong, SH Hong and JW Park. 2018. Toxicological effects of irregularly shaped and spherical microplastics in a marine teleost, the sheepshead minnow (Cyprinodon variegatus). Mar. Pollut. Bull. 129:231-240. https://doi.org/10.1016/j.marpolbul.2018.02.039
  10. Ciji PP and SB Nandan. 2014. Toxicity of copper and zinc to Puntius parrah (Day, 1865). Mar. Environ. Res. 93:38-46. https://doi.org/10.1016/j.marenvres.2013.11.006
  11. de Sa LC, LG Luis and L Guilhermino. 2015. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environ. Pollut. 196:359-362. https://doi.org/10.1016/j.envpol.2014.10.026
  12. Digka N, C Tsangaris, H Kaberi, A Adamopoulou and C Zeri. 2018. Microplastic abundance and polymer types in a Mediterranean environment. pp. 17-24. In: Proceedings of the International Conference on Microplastic Pollution in the Mediterranean Sea (Cocca M, ED Pace, ME Errico, G Gentile, A Montarsolo and R Mossotti, eds.). Springer Water. Springer. Cham, Switzerland. https://doi.org/10.1007/978-3-319-71279-6_3
  13. Espinosa C, MA Esteban and A Cuesta. 2019. Dietary administration of PVC and PE microplastics produces histological damage, oxidative stress and immunoregulation in European sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol. 95:574-583. https://doi.org/10.1016/j.fsi.2019.10.072
  14. Fernandes C, A Fontainhas-Fernandes, E Rocha and MA Salgado. 2008. Monitoring pollution in Esmoriz-Paramos lagoon, Portugal: liver histological and biochemical effects in Liza saliens. Environ. Monit. Assess. 145:315-322. https://doi.org/10.1007/s10661-007-0041-4
  15. Fujii R. 1969. Chromatophores and pigments. pp. 307-344. In: Fish Physiology (Hoar WS and DJ Randall, eds.). Vol. 3. Academic Press. New York and London, United Kingdom. https://doi.org/10.1016/S1546-5098(08)60116-8
  16. Gao X, I Hassan, Y Peng, S Huo and L Ling. 2021. Behaviors and influencing factors of the heavy metals adsorption onto microplastics: A review. J. Clean. Prod. 319:128777. https://doi.org/10.1016/j.jclepro.2021.128777
  17. Geyer R, JR Jambeck and KL Law. 2017. Production, use, and fate of all plastics ever made. Sci Adv. 3:e1700782. https://doi.org/10.1126/sciadv.1700782
  18. Granby K, S Rainieri, RR Rasmussen, MJJ Kotterman, JJ Sloth, TL Cederberg, A Barranco, A Marques and BK Larsen. 2018. The influence of microplastics and halogenated contaminants in feed on toxicokinetics and gene expression in European seabass (Dicentrarchus labrax). Environ. Res. 164:430-443. https://doi.org/10.1016/j.envres.2018.02.035
  19. Hinton DE, PC Baumann, GR Gardner, WE Hawkins, JD Hendricks, RA Murchelano and MS Okihiro. 1992. Histopathologic biomarkers. pp. 155-196. In: Biomarkers (Huggett RJ, RA Kimerli, PM Mehrle Jr. and HL Bergman, eds.). CRC Press. Boca Raton, Florida.
  20. Hirai H, H Takada, Y Ogata, R Yamashita, K Mizukawa, M Saha, C Kwan, C Moore, H Gray, D Laursen, ER Zettler, JW Farrington, CM Reddy, EE Peacock and MW Ward. 2011. Organic micropollutants in marine plastics debris from the open ocean and remote and urban beaches. Mar. Pollut. Bull. 62:1683-1692. https://doi.org/10.1016/j.marpolbul.2011.06.004
  21. Hu L, M Chernick, AM Lewis, PL Ferguson and DE Hinton. 2020. Chronic microfiber exposure in adult Japanese medaka (Oryzias latipes). PLoS One 15:e0229962. https://doi.org/10.1371/journal.pone.0229962
  22. Iqbal R, MT Khan, H Bilal, MM Aslam, IA Khan, S Raja, M Arslan and PM Nguyen. 2022. Microplastics as vectors of environmental contaminants: Interactions in the natural ecosystems. Hum. Ecol. Risk Assess. 28:1022-1042. https://doi.org/10.1080/10807039.2022.2120846
  23. Jabeen K, B Li, Q Chen, L Su, C Wu, H Hollert and H Shi. 2018. Effects of virgin microplastics on goldfish (Carassius auratus). Chemosphere 213:323-332. https://doi.org/10.1016/j.chemosphere.2018.09.031
  24. Jezierska B and M Witeska. 2006. The metal uptake and accumulation in fish living in polluted waters. pp. 107-114. In: Soil and Water Pollution Monitoring, Protection and Remediation (Twardowska I, S Stefaniak, HE Allen and MM Haggblom, eds.). Springer. Dordrecht, Netherlands.
  25. Jin Y, J Xia, Z Pan, J Yang, W Wang and Z Fu. 2018. Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ. Pollut. 235:322-329. https://doi.org/10.1016/j.envpol.2017.12.088
  26. Karbalaei S, P Hanachi, G Rafiee and P Seifori. 2021. Toxicity of polystyrene microplastics on juvenile Oncorhynchus mykiss (rainbow trout) after individual and combined exposure with chlorpyrifos. J. Hazard. Mater. 403:123980. https://doi.org/10.1016/j.jhazmat.2020.123980
  27. Khan FR, K Syberg, Y Shashoua and NR Bury. 2015. Influence of polyethylene microplastic beads on the uptake and localization of silver in zebrafish (Danio rerio). Environ. Pollut. 206:73-79. https://doi.org/10.1016/j.envpol.2015.06.009
  28. Kim HJ, SR Shin, H Kim, JJ Park, YK Shin and JS Lee. 2021. Induction of sex ratio change and intersex in Tegillarca granosa (Bivalvia: Arcidae) by waterborne zinc exposure. Aquacult. Rep. 21:100794. https://doi.org/10.1016/j.aqrep.2021.100794
  29. Kim NS, JD Yoon, SE Lee, YJ Park and SH Woo. 2019. A study on the residual microplastics in freshwater and fishes in the Geum River watershed. Korean J. Ecol. Environ. 52:28-39. https://doi.org/10.11614/KSL.2019.52.1.028
  30. Lee H, WJ Shim and JH Kwon. 2014. Sorption capacity of plastic debris for hydrophobic organic chemicals. Sci. Total Environ. 470:1545-1552. https://doi.org/10.1016/j.scitotenv.2013.08.023
  31. Lee JS, JC Kang, YK Shin, KH Ma and P Chin. 2001. Histological responses of the flounder, Paralichthys olivaceus exposed to copper. J. Fish Pathol. 14:81-90.
  32. Lei L, S Wu, S Lu, M Liu, Y Song, Z Fu, H Shi, KM Raley-Susman and D He. 2018. Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci. Total Environ. 619:1-8. https://doi.org/10.1016/j.scitotenv.2017.11.103
  33. Limonta G, A Mancia, A Benkhalqui, C Bertolucci, L Abelli, MC Fossi and C Panti. 2019. Microplastics induce transcriptional changes, immune response and behavioral alterations in adult zebrafish. Sci. Rep. 9:15775. https://doi.org/10.1038/s41598-019-52292-5
  34. Liu S, J Shi, J Wang, Y Dai, H Li, J Li, X Liu, X Chen, Z Wang and P Zhang. 2021. Interactions between microplastics and heavy metals in aquatic environments: A review. Front. Microbiol. 12:652520. https://doi.org/10.3389/fmicb.2021.652520
  35. Liu XJ, Z Luo, BX Xiong, X Liu, YH Zhao, GF Hu and GJ Lv. 2010. Effect of waterborne copper exposure on growth, hepatic enzymatic activities and histology in Synechogobius hasta. Ecotox. Environ. Safe. 73:1286-1291. https://doi.org/10.1016/j.ecoenv.2010.06.019
  36. Lu K, R Qiao, H An and Y Zhang. 2018. Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish (Danio rerio). Chemosphere 202:514-520. https://doi.org/10.1016/j.chemosphere.2018.03.145
  37. Lu Y, Y Zhang, Y Deng, W Jiang, Y Zhao, J Geng, L Ding and H Ren. 2016. Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ. Sci. Technol. 50:4054-4060. https://doi.org/10.1021/acs.est.6b00183
  38. Mallatt J. 1985. Fish gill structural changes induced by toxicants and other irritants: A statistical review. Can. J. Fish. Aquat. Sci. 42:630-648. https://doi.org/10.1139/f85-083
  39. McCarter JA and M Roch. 1983. Hepatic metallothionein and resistance to copper in juvenile coho salmon. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 74:133-137. https://doi.org/10.1016/0742-8413(83)90164-0
  40. OECD. 1992. Guideline for Testing of Chemicals, 203. Fish, Acute Toxicity Test. Organisation for Economic Co-operation and Development. Paris.
  41. Okamoto K, M Nomura, Y Horie and H Okamura. 2022. Color preferences and gastrointestinal-tract retention times of microplastics by freshwater and marine fishes. Environ. Pollut. 304:119253. https://doi.org/10.1016/j.envpol.2022.119253
  42. Oliveira M, A Ribeiro, K Hylland and L Guilhermino. 2013. Single and combined effects of microplastics and pyrene on juveniles (0+ group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol. Indic. 34:641-647. https://doi.org/10.1016/j.ecolind.2013.06.019
  43. Olsvik PA, KK Lie, O Saele and M Sanden. 2007. Spatial transcription of CYP1A in fish liver. BMC physiol. 7:12. https://doi.org/10.1186/1472-6793-7-12
  44. Olurin KB, EAA Olojo, GO Mbaka and AT Akindele. 2006. Histopathological responses of the gill and liver tissues of Clarias gariepinus fingerlings to herbicide, glyphosate. Afr. J. Biotechnol. 5:2480-2487.
  45. Peda C, L Caccamo, MC Fossi, F Gai, F Andaloro, L Genovese, A Perdichizzi, T Romeo and G Maricchiolo. 2016. Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: preliminary results. Environ. Pollut. 212:251-256. https://doi.org/10.1016/j.envpol.2016.01.083
  46. Plastic Europe. 2022. Plastics - the Facts 2022. Plastics Europe. https://plasticseurope.org/knowledge-hub/plastics-the-facts-2022/. Accessed February 6, 2024.
  47. Rainieri S, N Conlledo, BK Larsen, K Granby and A Barranco. 2018. Combined effects of microplastics and chemical contaminants on the organ toxicity of zebrafish (Danio rerio). Environ. Res. 162:135-143. https://doi.org/10.1016/j.envres.2017.12.019
  48. Rochman CM, E Hoh, T Kurobe and SJ Teh. 2013. Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci. Rep. 3:3263. https://doi.org/10.1038/srep03263
  49. Romano N, N Renukdas, H Fischer, J Shrivastava, K Baruah, N Egnew and AK Sinha. 2020. Differential modulation of oxidative stress, antioxidant defense, histomorphology, ion -regulation and growth marker gene expression in goldfish (Carassius auratus) following exposure to different dose of virgin microplastics. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 238:108862. https://doi.org/10.1016/j.cbpc.2020.108862
  50. Santos D, A Luzio, C Matos, J Bellas, SM Monteiro and L Felix. 2021. Microplastics alone or co-exposed with copper induce neurotoxicity and behavioral alterations on zebrafish larvae after a subchronic exposure. Aquat. Toxicol. 235:105814. https://doi.org/10.1016/j.aquatox.2021.105814
  51. Santos D, A Luzio, L Felix, J Bellas and SM Monteiro. 2022. Oxidative stress, apoptosis and serotonergic system changes in zebrafish (Danio rerio) gills after long-term exposure to microplastics and copper. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 258:109363. https://doi.org/10.1016/j.cbpc.2022.109363
  52. Santos D, L Felix, A Luzio, S Parra, E Cabecinha, J Bellas and SM Monteiro. 2020. Toxicological effects induced on early life stages of zebrafish (Danio rerio) after an acute exposure to microplastics alone or co-exposed with copper. Chemosphere 261:127748. https://doi.org/10.1016/j.chemosphere.2020.127748
  53. Sayed AEDH, MN Hana, M Hamed, HM Abdel-Latif, JS Lee and HA Soliman. 2023. Protective efficacy of dietary natural antioxidants on microplastic particles-induced histopathological lesions in African catfish (Clarias gariepinus). Environ. Sci. Pollut. Res. 30:24424-24440. https://doi.org/10.1007/s11356-022-23789-w
  54. Sharma R, R Jindal and C Faggio. 2021. Impact of cypermethrin in nephrocytes of freshwater fish Catla catla. Environ. Toxicol. Pharmacol. 88:103739. https://doi.org/10.1016/j.etap.2021.103739
  55. Silva AG and CB Martinez. 2007. Morphological changes in the kidney of a fish living in an urban stream. Environ. Toxicol. Pharmacol. 23:185-192. https://doi.org/10.1016/j.etap.2006.08.009
  56. Sinha AK, P Dasgupta, S Chakrabarty, G Bhattacharyya and S Bhattacharjee. 2002. Bio-accumulation of heavy metals in different organs of some of the common edible fishes of Kharkai River, Jamshedpur. Indian J. Environ. Health 44:102-107.
  57. Soliman HA, M Hamed and AEDH Sayed. 2021. Investigating the effects of copper sulfate and copper oxide nanoparticles in Nile tilapia (Oreochromis niloticus) using multiple biomarkers: the prophylactic role of Spirulina. Environ. Sci. Pollut. Res. 28:30046-30057. https://doi.org/10.1007/s11356-021-12859-0
  58. Sun X, Q Li, Y Shi, Y Zhao, S Zheng, J Liang, T Liu and Z Tian. 2019. Characteristics and retention of microplastics in the digestive tracts of fish from the Yellow Sea. Environ. Pollut. 249:878-885. https://doi.org/10.1016/j.envpol.2019.01.110
  59. Sures B. 2003. Accumulation of heavy metals by intestinal helminths in fish: An overview and perspective. Parasitology 126:53-60. https://doi.org/10.1017/S003118200300372X
  60. Totaro EA, FA Pisanti, P Glees and A Continillo. 1986. The effect of copper pollution on mitochondrial degeneration. Mar. Environ. Res. 18:245-253. https://doi.org/10.1016/0141-1136(86)90024-3
  61. Wen B, SR Jin, ZZ Chen, JZ Gao, YN Liu, JH Liu and XS Feng. 2018. Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defence and innate immunity of the discus fish (Symphysodon aequifasciatus). Environ. Pollut. 243:462-471. https://doi.org/10.1016/j.envpol.2018.09.029
  62. Yin L, B Chen, B Xia, X Shi and K Qu. 2018. Polystyrene microplastics alter the behavior, energy reserve and nutritional composition of marine jacopever (Sebastes schlegelii). J. Hazard. Mater. 360:97-105. https://doi.org/10.1016/j.jhazmat.2018.07.110
  63. Zhang F, D Li, Y Yang, H Zhang, J Zhu, J Liu, X Bu, E Li, J Qin, N Yu, L Chen and X Wang. 2022. Combined effects of polystyrene microplastics and copper on antioxidant capacity, immune response and intestinal microbiota of Nile tilapia (Oreochromis niloticus). Sci. Total Environ. 808:152099. https://doi.org/10.1016/j.scitotenv.2021.152099
  64. Zhao Y, C Ma, W Wei, Y Wang, H Cao, N Cui, Y Liu and H Liang. 2024. Effects of single and combined exposure of virgin or aged polyethylene microplastics and penthiopyrad on zebrafish (Danio rerio). Sci. Total Environ. 921:171160. https://doi.org/10.1016/j.scitotenv.2024.171160
  65. Zhu L, H Bai, B Chen, X Sun, K Qu and B Xia. 2018. Microplastic pollution in North Yellow Sea, China: Observations on occurrence, distribution and identification. Sci. Total Environ. 636:20-29. https://doi.org/10.1016/j.scitotenv.2018.04.182
  66. Zuo Z, Q Wang, C Zhang and J Zou. 2022. Single and combined effects of microplastics and cadmium on juvenile grass carp (Ctenopharyngodon idellus). Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 261:109424. https://doi.org/10.1016/j.cbpc.2022.109424