Abstract
Microplastic (MP) is a major contaminant in the aquatic environment. In addition to the physical threats posed by microplastic ingestion, their potential as a vector for the transport of hydrophobic pollutants is required to be adequately addressed. This study examined the effects of polystyrene microplastics individually or combined with chlorpyrifos insecticide on nutritional parameters in muscle of rainbow trout (Onchorhynchus mykiss). Fish were exposed to individual polystyrene microplastic concentrations (30 or 300 μg/L), or individual chlorpyrifos concentrations (2 or 6 μg/L), and their combination at similar concentrations of chlorpyrifos and microplastics. Results showed individual polystyrene microplastics had minimal effects on amino acid and fatty acid composition and no effect on protein contents of fish muscle. However, significant alterations in amino acid and fatty acid composition, and protein contents, were observed in combined polystyrene microplastics and chlorpyrifos groups. These findings suggested that polystyrene microplastics cause toxicity and increase the adverse effects of chlorpyrifos on the muscle of fish. This investigation provided evidence toward low nutritional value of farmed or wild fish muscle that grows in areas with high concentrations of microplastics and pesticides.
Similar content being viewed by others
References
Abbasi S, Soltani N, Keshavarzi B et al (2018) Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 205:80–87. https://doi.org/10.1016/j.chemosphere.2018.04.076
Akhbarizadeh R, Moore F, Keshavarzi B, Moeinpour A (2017) Microplastics and potentially toxic elements in coastal sediments of Iran’s main oil terminal (Khark Island). Environ Pollut 220:720–731. https://doi.org/10.1016/j.envpol.2016.10.038
AOAC (2005) Official methods of analysis. 18th ed.. Gaithersburg, MD: Association of Official Analytical Chemists.
Ariño A, Beltrán JA, Herrera A, Roncalés P (2013) Fish and seafood: nutritional value. In: Caballero B (ed) Encyclopedia of human nutrition (third edition). Academic Press, Waltham, pp 254–261. doi:https://doi.org/10.1016/B978-0-12-375083-9.00110-0
Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d'Errico G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222. https://doi.org/10.1016/j.envpol.2014.12.021
Barboza LGA, Vethaak AD, Lavorante BR et al (2018a) Marine microplastic debris: an emerging issue for food security, food safety and human health. Mar Pollut Bull 133:336–348. https://doi.org/10.1016/j.marpolbul.2018.05.047
Barboza LGA, Vieira LR, Guilhermino L (2018b) 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
Bellas J, Gil I (2020) Polyethylene microplastics increase the toxicity of chlorpyrifos to the marine copepod Acartia tonsa. Environ Pollut 114059:114059. https://doi.org/10.1016/j.envpol.2020.114059
Bergmann M, Gutow L, Klages M (2015) Marine anthropogenic litter. Springer Nature
Çakir Ş, Sarikaya R (2005) Genotoxicity testing of some organophosphate insecticides in the Drosophila wing spot test. Food Chem Toxicol 43:443–450. https://doi.org/10.1016/j.fct.2004.11.010
Carbery M, O’Connor W, Palanisami T (2018) Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environ Int 115:400–409. https://doi.org/10.1016/j.envint.2018.03.007/j.envint.2018.03.007
Crawford CB, Quinn B (2017) 6 - The interactions of microplastics and chemical pollutants. In: Quinn B (ed) Crawford CB. Elsevier, Microplastic pollutants, pp 131–157. https://doi.org/10.1016/B978-0-12-809406-8.00006-2
Eerkes-Medrano D, Thomicroplastics on RC, Aldridge DC (2015) Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res 75:63–82. https://doi.org/10.1016/j.watres.2015.02.012
Eriksen M, Lebreton LCM, Carson HS, Thiel M, Moore CJ, Borerro JC, Galgani F, Ryan PG, Reisser J (2014) Plastic pollution in the world’s oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS One 9:e111913. https://doi.org/10.1371/journal.pone.0111913
Fokina NN, Ruokolainen TR, Nemova NN, Bakhmet IN (2013) Changes of blue mussels Mytilus edulis L. lipid composition under cadmium and copper toxic effect. Biol Trace Elem Res 154:217–225. https://doi.org/10.1007/s12011-013-9727-3
Folch J, Lees M, Stanley GS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509
Garrido S, Linares M, Campillo JA, Albentosa M (2019) Effect of microplastics on the toxicity of chlorpyrifos to the microalgae Isochrysis galbana, clone t-ISO. Ecotoxicol Environ Saf 173:103–109. https://doi.org/10.1016/j.ecoenv.2019.02.020
Gonçalves AMM, Mesquita AF, Verdelhos T, Coutinho JAP, Marques JC, Gonçalves F (2016) Fatty acids’ profiles as indicators of stress induced by of a common herbicide on two marine bivalves species: Cerastoderma edule (Linnaeus, 1758) and Scrobicularia plana (da Costa, 1778). Ecol Indic 63:209–218. https://doi.org/10.1016/j.ecolind.2015.12.006
González-Soto N, Hatfield J, Katsumiti A, Duroudier N, Lacave JM, Bilbao E, Orbea A, Navarro E, Cajaraville MP (2019) Impacts of dietary exposure to different sized polystyrene microplastics alone and with sorbed benzo[a] pyrene on biomarkers and whole organism responses in mussels Mytilus galloprovincialis. Sci Total Environ 684:548–566. https://doi.org/10.1016/j.scitotenv.2019.05.161
Hanachi P, Karbalaei S, Walker TR, Cole M, Hosseini SV (2019) Abundance and properties of microplastics found in commercial fish meal and cultured common carp (Cyprinus carpio). Environ Sci Pollut Res 26:23777–23787. https://doi.org/10.1007/s11356-019-05637-6
Ismail M, Ali R, Shahid M, Khan MA, Zubair M, Ali T, Mahmood Khan Q (2018) Genotoxic and hematological effects of chlorpyrifos exposure on freshwater fish Labeo rohita. Drug Chem Toxicol 41:22–26. https://doi.org/10.1080/01480545.2017.1280047
Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryman M, Andrady A, Narayan R, Law KL (2015) Plastic waste inputs from land into the ocean. Science 347:768–771. https://doi.org/10.1126/science.1260352
Karami A, Karbalaei S, Bagher FZ et al (2016a) Alterations in juvenile diploid and triploid African catfish skin gelatin yield and amino acid composition: effects of chlorpyrifos and butachlor exposures. Environ Pollut 215:170–177. https://doi.org/10.1016/j.envpol.2016.05.014
Karami A, Romano N, Galloway T, Hamzah H (2016b) Virgin microplastics cause toxicity and modulate the impacts of phenanthrene on biomarker responses in African catfish (Clarias gariepinus). Environ Res 151:58–70. https://doi.org/10.1016/j.envres.2016.07.024
Karami A, Golieskardi A, Choo CK et al (2017a) The presence of microplastics in commercial salts from different countries. Sci Rep 7:46173
Karami A, Groman DB, Wilson SP et al (2017b) Biomarker responses in zebrafish (Danio rerio) larvae exposed to pristine low-density polyethylene fragments. Environ Pollut 223:466–475. https://doi.org/10.1016/j.envpol.2017.01.047/j.envpol.2017.01.047
Karami A, Golieskardi A, Choo CK, Larat V, Karbalaei S, Salamatinia B (2018a) Microplastic and mesoplastic contamination in canned sardines and sprats. Sci Total Environ 612:1380–1386. https://doi.org/10.1016/j.scitotenv.2017.09.005
Karami A, Karbalaei S, Ebrahimi M, Ismail A, Jahromi MF, Simpson SL, Eghtesadi Araghi P, Lim RP, Liang JB (2018b) Changes in nutritional values induced by butachlor in juvenile diploid and triploid Clarias gariepinus. Int J Environ Sci Technol 15:2117–2128. https://doi.org/10.1007/s13762-017-1582-x
Karbalaei S, Karami A, Ebrahimi M, Jahromi MF, Ismail A, Liang JB, Simpson SL, Ismail SNS, Goh YM (2017) Changes in nutritional parameters in diploid and triploid African catfish Clarias gariepinus following chlorpyrifos exposure. Aquat Biol 26:101–111. https://doi.org/10.3354/ab00678
Karbalaei S, Hanachi P, Walker TR, Cole M (2018) Occurrence, sources, human health impacts and mitigation of microplastic pollution. Environ Sci Pollut Res 25:36046–36063. https://doi.org/10.1007/s11356-018-3508-7
Karbalaei S, Hanachi P, Walker TR (2019a) Microplastic accumulation in rainbow trout (Oncorhynchus Mykiss). Turkish-German University, Turkey, pp 18–26
Karbalaei S, Golieskardi A, Hamzah HB, Abdulwahid S, Hanachi P, Walker TR, Karami A (2019b) Abundance and characteristics of microplastics in commercial marine fish from Malaysia. Mar Pollut Bull 148:5–15. https://doi.org/10.1016/j.marpolbul.2019.07.072
Karbalaei S, Golieskardi A, Watt DU, Boiret M, Hanachi P, Walker TR, Karami A (2019c) Analysis and inorganic composition of microplastics in commercial Malaysian fish meals. Mar Pollut Bull 110687:110687. https://doi.org/10.1016/j.marpolbul.2019.110687
Karbalaei S, Hanachi P, Rafiee G, Seifori P (2021) Toxicity of polystyrene microplastics on juvenile Oncorhynchus mykiss (rainbow trout) after individual and combined exposure with chlorpyrifos. J Hazard Mater 123980:123980. https://doi.org/10.1016/j.jhazmat.2020.123980
Karlsson F, Tremaroli V, Nielsen J, Bäckhed F (2013) Assessing the human gut microbiota in metabolic diseases. Diabetes 62:3341–3349. https://doi.org/10.2337/db13-0844
Kenari AA, Regenstein JM, Hosseini SV, Rezaei M, Tahergorabi R, Nazari RM, Mogaddasi M, Kaboli SA (2009) Amino acid and fatty acid composition of cultured Beluga (Huso huso) of different ages. J Aquat Food Prod Technol 18:245–265. https://doi.org/10.1080/10498850902758586
Koelmans AA (2015) Modeling the role of microplastics in bioaccumulation of organic chemicals to marine aquatic organisms. A critical review in: Marine anthropogenic litter. Springer, Cham, pp. 309–324. https://doi.org/10.1007/978-3-319-16510-3
León VM, García I, González E, Samper R, Fernández-González V, Muniategui-Lorenzo S (2018) Potential transfer of organic pollutants from littoral plastics debris to the marine environment. Environ Pollut 236:442–453. https://doi.org/10.1016/j.envpol.2018.01.114
Li WC, Tse HF, Fok L (2016) Plastic waste in the marine environment: a review of sources, occurrence and effects. Sci Total Environ 566:333–349. https://doi.org/10.1016/j.scitotenv.2016.05.084
Lu L, Wan Z, Luo T, Fu Z, Jin Y (2018) Polystyrene microplastics induce gut microbiota dysbiosis and hepatic lipid metabolism disorder in mice. Sci Total Environ 631:449–458. https://doi.org/10.1016/j.scitotenv.2018.03.051
Ma H, Pu S, Liu S et al (2020) Microplastics in aquatic environments: Toxicity to trigger ecological consequences. Environ Pollut 261:114089. https://doi.org/10.1016/j.envpol.2020.114089
Mehdinia A, Dehbandi R, Hamzehpour A, Rahnama R (2020) Identification of microplastics in the sediments of southern coasts of the Caspian Sea, north of Iran. Environ Pollut 258:113738. https://doi.org/10.1016/j.envpol.2019.113738
Moreno-González R, Campillo JA, León VM (2013) Influence of an intensive agricultural drainage basin on the seasonal distribution of organic pollutants in seawater from a Mediterranean coastal lagoon (Mar Menor, SE Spain). Mar Pollut Bull 77:400–411. https://doi.org/10.1016/j.marpolbul.2013.09.040
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267. https://doi.org/10.1126/science.1223813
OECD (1992) Test no. 203: fish, acute toxicity test. OECD guidelines for the testing of chemicals, section 2. OECD Publishing.
OECD (2011) Test no. 234: fish sexual development test, OECD guidelines for the testing of chemicals, section 2. Paris. OECD, 1992. Guideline for the Testing of Chemicals no.203. Fish, Acute Toxicity Test. Organ.Econ.CO-Oper.Dev.Paris.
Olivares-Rubio HF, Vega-López A (2016) Fatty acid metabolism in fish species as a biomarker for environmental monitoring. Environ Pollut 218:297–312. https://doi.org/10.1016/j.envpol.2016.07.005
Oliveira M, Ribeiro A, Hylland K, Guilhermino L (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
Pinto MI, Vale C, Sontag G, Noronha JP (2016) Pathways of priority pesticides in sediments of coastal lagoons: the case study of Óbidos Lagoon. Portugal Mar Pollut Bull 106:335–340. https://doi.org/10.1016/j.marpolbul.2016.03.028
Pirsaheb M, Fattahi N, Rahimi R, Sharafi K, Ghaffari HR (2017) Evaluation of abamectin, diazinon and chlorpyrifos pesticide residues in apple product of Mahabad region gardens: Iran in 2014. Food Chem 231:148–155. https://doi.org/10.1016/j.foodchem.2017.03.120
Qiao R, Sheng C, Lu Y, Zhang Y, Ren H, Lemos B (2019) Microplastics induce intestinal inflammation, oxidative stress, and disorders of metabolome and microbiome in zebrafish. Sci Total Environ 662:246–253. https://doi.org/10.1016/j.scitotenv.2019.01.245
Rainieri S, Conlledo N, Larsen BK, Granby K, Barranco A (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
Rani VJS, Janaiah C (1991) Ammonia metabolism in freshwater teleost, Clarias batrachus (Linn.) on exposure to trichlorfon. Bull Environ Contam Toxicol 46:731–737. https://doi.org/10.1007/BF01689960
Rial D, León VM, Bellas J (2017) Integrative assessment of coastal marine pollution in the Bay of Santander and the Upper Galician Rias. J Sea Res 130:239–247. https://doi.org/10.1016/j.seares.2017.03.006
Rivera-Hernández JR, Fernández 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
Rocchetta I, Mazzuca M, Conforti V, Ruiz L, Balzaretti V, de Molina MCR (2006) Effect of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ Pollut 141:353–358. https://doi.org/10.1016/j.envpol.2005.08.035
Rochman CM, Browne MA, Halpern BS, Hentschel BT, Hoh E, Karapanagioti HK, Rios-Mendoza LM, Takada H, Teh S, Thompson RC (2013a) Classify plastic waste as hazardous. Nature 494:169–171. https://doi.org/10.1038/494169a
Rochman CM, Hoh E, Kurobe T, Teh SJ (2013b) Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci Rep 3:3263. https://doi.org/10.1038/srep03263
Rochman CM, Cook A-M, Koelmans AA (2016) Plastic debris and policy: Using current scientific understanding to invoke positive change. Environ Toxicol Chem 35:1617–1626
Salin KR, Arun VV, Nair CM, Tidwell JH (2018) Sustainable aquafeed. In: Sustainable aquaculture. Springer, pp 123–151. https://doi.org/10.1007/978-3-319-73257-2_4
Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199. https://doi.org/10.1016/S0044-8486(99)00083-6
Sargent JR, Tocher DR, Bell JG (2003) The lipids. In: Fish nutrition. Elsevier, pp 181–257. https://doi.org/10.1016/B978-012319652-1/50005-7
Shang-gui D, Zhi-ying P, Fang C, Ping Y, Tie W (2004) Amino acid composition and anti-anaemia action of hydrolyzed offal protein from Harengula Zunasi Bleeker. Food Chem 87:97–102. https://doi.org/10.1016/j.foodchem.2003.10.024
Sıkdokur 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
Silva CO, Simões T, Novais SC, Pimparel I, Granada L, Soares AMVM, Barata C, Lemos MFL (2017) Fatty acid profile of the sea snail Gibbula umbilicalis as a biomarker for coastal metal pollution. Sci Total Environ 586:542–550. https://doi.org/10.1016/j.scitotenv.2017.02.015
Strungaru S-A, Jijie R, Nicoara M, Plavan G, Faggio C (2019) Micro- (nano) plastics in freshwater ecosystems: abundance, toxicological impact and quantification methodology. TrAC Trends Anal Chem 110:116–128. https://doi.org/10.1016/j.trac.2018.10.025
Telahigue K, Rabeh I, Hajji T, Trabelsi W, Bejaoui S, Chouba L, el Cafsi M’, Soudani N (2019) Effects of acute mercury exposure on fatty acid composition and oxidative stress biomarkers in Holothuria forskali body wall. Ecotoxicol Environ Saf 169:516–522. https://doi.org/10.1016/j.ecoenv.2018.11.051
U. S. Environmental Protection Agency (1996) Ecological effects test guidelines: OPPTS 850.1075 fish acute toxicity test, freshwater and marine. U. S. Environmental Protection Agency, Washington, D.C. US (EPA 712-C-96-118)
Uniyal S, Sharma RK (2018) Technological advancement in electrochemical biosensor based detection of organophosphate pesticide chlorpyrifos in the environment: a review of status and prospects. Biosens Bioelectron 116:37–50. https://doi.org/10.1016/j.bios.2018.05.039
Waller CL, Griffiths HJ, Waluda CM, Thorpe SE, Loaiza I, Moreno B, Pacherres CO, Hughes KA (2017) Microplastics in the Antarctic marine system: an emerging area of research. Sci Total Environ 598:220–227. https://doi.org/10.1016/j.scitotenv.2017.03.283
Xing H, Chen J, Peng M, Wang Z, Liu F, Li S, Teng X (2019) Identification of signal pathways for immunotoxicity in the spleen of common carp exposed to chlorpyrifos. Ecotoxicol Environ Saf 182:109464. https://doi.org/10.1016/j.ecoenv.2019.109464
Yin L, Chen B, Xia B, Shi X, Qu K (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
Yonar ME (2018) Chlorpyrifos-induced biochemical changes in Cyprinus carpio: ameliorative effect of curcumin. Ecotoxicol Environ Saf 151:49–54. https://doi.org/10.1016/j.ecoenv.2017.12.065
Yousif E, Haddad R (2013) Photodegradation and photostabilization of polymers, especially polystyrene. SpringerPlus 2:398. https://doi.org/10.1186/2193-1801-2-398
Zhang J, Liu L, Ren L, Feng W, Lv P, Wu W, Yan Y (2017) The single and joint toxicity effects of chlorpyrifos and beta-cypermethrin in zebrafish (Danio rerio) early life stages. J Hazard Mater 334:121–131. https://doi.org/10.1016/j.jhazmat.2017.03.055
Zhao J, Chen B (2016) Species sensitivity distribution for chlorpyrifos to aquatic organisms: model choice and sample size. Ecotoxicol Environ Saf 125:161–169. https://doi.org/10.1016/j.ecoenv.2015.11.039
Zhao S, Zhu L, Wang T, Li D (2014) Suspended microplastics in the surface water of the Yangtze Estuary System, China: first observations on occurrence, distribution. Mar Pollut Bull 86:562–568. https://doi.org/10.1016/j.marpolbul.2014.06.032
Acknowledgements
This study was supported by the Center for International Scientific Studies and Collaboration (CISSC), Ministry of Science, Research and Technology, Iran (391890).
Availability of data and materials
All data analyzed during this study are included in this published article and its supplementary information files.
Funding
This work was financially supported by the Center for International Scientific Studies and Collaboration (CISSC), Ministry of Science, Research and Technology, Iran (391890).
Author information
Authors and Affiliations
Contributions
Parichehr Hanachi: funding acquisition, methodology, review and editing. Samaneh Karbalaei: project administration, conceptualization, writing original draft, visualization, formal analysis, investigation. Sujuan Yu: analysis, review and editing.
Corresponding author
Ethics declarations
Ethics approval
The experimental fish used in the present study were cultured following the terms of use of animals approved by the Iranian academic center for education, culture and research (approval ID: IR.ACECR.IBCRC.REC.1398.008/2019).
Consent to participate
No human data was used in this study.
Consent for publication
All of the authors have given the consent to publish this data.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Bruno Nunes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 142 kb)
Rights and permissions
About this article
Cite this article
Hanachi, ., Karbalaei, S. & Yu, S. Combined polystyrene microplastics and chlorpyrifos decrease levels of nutritional parameters in muscle of rainbow trout (Oncorhynchus mykiss). Environ Sci Pollut Res 28, 64908–64920 (2021). https://doi.org/10.1007/s11356-021-15536-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-15536-4