Abstract
The dispersed pollution caused by microplastics (MPs) represents a current and global concern. While the fragmentation of plastic debris into smaller particles occurs in rivers, little MP research is done on freshwater species and is published compared to the marine environment. The Loire River is the longest river in France and is subject to moderate to high anthropic pressure while it represents major societal and economic issues. However, there are not many studies that have been put forward with regards to the effect of environmental MPs (EMPs) on aquatic organisms and no policies have been enacted to monitor the plastic pollution. In this study, freshwater bivalves, Corbicula fluminea, were exposed for 21 days to environmentally relevant concentrations of a mixture of <200 µm MPs generated from plastic litter collected directly along the banks of the Loire River. This mixture was composed of 40% polyethylene (PE), 40% polypropylene (PP), 10% polyethylene terephthalate (PET) and 10% polyvinylchloride (PVC) (mass percentage). Ecotoxicological effects were assessed from the individual to the molecular levels on several endpoints: condition index, filtration efficiency, enzyme activities, lipid peroxidation, energy reserves and gene expression. The ingestion of EMPs caused damages at the biochemical level. Indeed, we reported an increase in catalase activity in gills and digestive mass, a decrease in TBARs in gills, a decrease in acetylcholinesterase activity in the digestive mass, a decrease of glycogen and lipid contents in the whole organisms and a significant induction of the expression of gst, cat, mp, acp genes. The current results suggest therefore that long-term exposure to realistic doses of EMPs causes toxicity towards freshwater benthic biota. The analysis of biomarker activities and the analysis of gene expression are complementary to prevent the effects of a plastic contamination at higher biological levels in aquatic organisms.
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References
AFNOR (1985). Norme Française. Huitres creuses. Dénominations et Classification, NF V 45-056. Publication de l’association française de normalisation (AFNOR)
Ateia M, Zheng T, Calace S, Tharayil N, Pilla S, Karanfil T (2020) Sorption behavior of real microplastics (MPs): insights for organic micropollutants adsorption on a large set of well characterized MPs. Sci Total Environ 720:137634. https://doi.org/10.1016/j.scitotenv.2020.137634
Bayo J, Olmos S, López-Castellanos J (2020) Microplastics in an urban wastewater treatment plant: the influence of physicochemical parameters and environmental factors. Chemosphere 238:124593. https://doi.org/10.1016/j.chemosphere.2019.124593
Boening DW (1999) An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Environ Monitor Assess 55:459–470. https://doi.org/10.1023/A:1005995217901
Borković-Mitić S, Pavlović S, Perendija B, Despotović S, Gavrić J, Gačić Z, Saičić Z (2013) Influence of some metal concentrations on the activity of antioxidant enzymes and concentrations of vitamin E and SH-groups in the digestive gland and gills of the freshwater bivalve Unio tumidus from the Serbian part of Sava River. Ecol Indic 32:212–221. https://doi.org/10.1016/j.ecolind.2013.03.024
Bour A, Avio CG, Gorbi S, Regoli F, Hylland K (2018) Presence of microplastics in benthic and epibenthic organisms: influence of habitat, feeding mode and trophic level. Environ Pollut 243:1217–1225. https://doi.org/10.1016/j.envpol.2018.09.115
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bringer A, Cachot J, Prunier G, Dubillot E, Clerandeau C, Helene T (2020) Experimental ingestion of fluorescent microplastics by pacific oysters, Crassostrea gigas, and their effects on the behaviour and development at early stages. Chemosphere 254:126793. https://doi.org/10.1016/j.chemosphere.2020.126793
Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L). Environ Sci Technol 42(13):5026–5031. https://doi.org/10.1021/es800249a. Jul 1
Burns EE, Boxall ABA (2018) Microplastics in the aquatic environment: evidence for or against adverse impacts and major knowledge gaps. Environ Toxicol Chem 37:2776–2796. https://doi.org/10.1002/etc.4268
Capolupo M, Gunaalan K, Booth A, Sørensen L, Valbonesi P, Fabbri E (2021) The sub-lethal impact of plastic and tire rubber leachates on the Mediterranean mussel Mytilus galloprovincialis. Environ Pollut 283:ISSN 0269-7491. https://doi.org/10.1016/j.envpol.2021.117081
Carr RS, Neff JM (1984) Quantitative semi-automated enzymatic assay for tissue glycogen. Comp Biochem Physiol Part B: Comp Biochem 77B(3):447–449. https://doi.org/10.1016/0305-0491(84)90258-X
Chandurvelan R, Marsden ID, Gaw S, Glover CN (2013) Biochemical biomarker responses of green-lipped mussel, Perna canaliculus, to acute and subchronic waterborne cadmium toxicity. Aquat. Toxicol. 140–141:303–313. https://doi.org/10.1016/j.aquatox.2013.06.015
Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284
Duis K, Coors A (2016) Microplastics in the aquatic and terrestrial environment: sources (with a specific focus on personal care products), fate and effects. Environ Sci Eur 28:2. https://doi.org/10.1186/s12302-015-0069-y
Dusaucy J, Gateuille D, Perrette Y, Naffrechoux E (2021) Microplastic pollution of worldwide lakes. Environ. Pollut. 284:117075. https://doi.org/10.1016/j.envpol.2021.117075
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Ferreira I, Venâncio C, Lopes I, Oliveira M (2019) Nanoplastics and marine organisms: what has been studied? Environ. Toxicol. Pharmacol. 67:1–7. https://doi.org/10.1016/j.etap.2019.01.006
Frias JPGL, Lyashevska O, Joyce H, Pagter E, Nash R (2020) Floating microplastics in a coastal embayment: a multifaceted issue. Mar. Pollut. Bull. 158:111361. https://doi.org/10.1016/j.marpolbul.2020.111361
Frings CS, Dunn RT, Queen CA (1972) Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 18(7):673–674. https://doi.org/10.1093/clinchem/18.7.673
Fu L, Xi M, Nicholaus R, Wang Z, Wang X, Kong F, Yu Z (2022) Behaviors and biochemical responses of macroinvertebrate Corbicula fluminea to polystyrene microplastics. Sci Total Environ 813:152617. https://doi.org/10.1016/j.scitotenv.2021.152617
Galgani F, Bocquene G (1991) Semi-automated colorimetric and enzymatic assays for aquatic organisms using microplate readers. Water Res 25(2):147–150. https://doi.org/10.1016/0043-1354(91)90023-J
Gardon T, Reisser C, Soyez C, Quillien V, Le Moullac G (2018) Microplastics affect energy balance and gametogenesis in the pearl oyster Pinctada margaritifera. Environ Sci Technol 52:277–5286. https://doi.org/10.1021/acs.est.8b00168
Guilhermino L, Vieira LR, Ribeiro D, Tavares AS, Cardoso V, Alves A, Almeida JM (2018) Uptake and effects of the antimicrobial florfenicol, microplastics and their mixtures on freshwater exotic invasive bivalve Corbicula fluminea. Sci Total Environ 622–623:1131–1142. https://doi.org/10.1016/j.scitotenv.2017.12.020
Habib R, Thiemann T, Kendi R (2020) Microplastics and wastewater treatment plants—a review. J Water Resour Prot 12:1–35. https://doi.org/10.4236/jwarp.2020.121001
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139
Hahladakis JN, Velis CA, Weber R, Iacovidou E, Purnell P (2018) An overview of chemical additives present in plastics: migration, release, fate and environmental impact during their use, disposal and recycling. J Hazard Mater 344:179–199
Haider F, Sokolov EP, Sokolova IM (2018) Effects of mechanical disturbance and salinity stress on bioenergetics and burrowing behavior of the soft-shell clam Mya arenaria. J Exp Biol 221(Pt 4):jeb172643. https://doi.org/10.1242/jeb.172643
Hermabessiere L, Dehaut A, Paul-Pont I, Lacroix C, Jezequel R, Soudant P, Duflos G (2017) Occurrence and effects of plastic additives on marine environments and organisms: a review. Chemosphere 182:781–793. https://doi.org/10.1016/j.chemosphere.2017.05.096
Latchere O, Audroin T, Hétier J, Métais I, Châtel A (2021) The need to investigate continuums of plastic particle diversity, brackish environments and trophic transfer to assess the risk of micro and nanoplastics on aquatic organisms. Environ Pollut ume 273:116449. https://doi.org/10.1016/j.envpol.2021.116449. ISSN 0269-7491
Lee MC, Park JC, Lee JS (2018) Effects of environmental stressors on lipid metabolism in aquatic invertebrates. Aquat Toxicol 200:83–92. https://doi.org/10.1016/j.aquatox.2018.04.016
Li J, Liu H, Paul Chen J (2018) Microplastics in freshwater systems: a review on occurrence, environmental effects, and methods for microplastics detection. Water Res 137:362–374. https://doi.org/10.1016/j.watres.2017.12.056
Li L, Su L, Cai H, Rochman CM, Li Q, Kolandhasamy P, Peng J, Shi H (2019) The uptake of microfibers by freshwater Asian clams (Corbicula fluminea) varies based upon physicochemical properties. Chemosphere 221:107–114. https://doi.org/10.1016/j.chemosphere.2019.01.024
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408.2. https://doi.org/10.1006/meth.2001.1262
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Managing Rivers Wisely, WWF: https://wwfint.awsassets.panda.org/downloads/mrwloirecasestudy.pdf
Métais I, Latchere O, Roman C, Perrein-Ettajani H, Mouloud M, Georges D, Audroin T, Catrouillet C, Gigault J, Agnès-Feurtet-Mazel, Baudrimont M, Châtel A (2023) Continuum from microplastics to nanoplastics: effects of size and source on the estuarine bivalve Scrobicularia plana. Environ Sci Pollut Res Int 30(16):45725–45739. https://doi.org/10.1007/s11356-023-25588-3.
Mkuye R, Gong S, Zhao L, Masanja F, Ndandala C, Bubelwa E, Yang C, Deng Y (2022) Effects of microplastics on physiological performance of marine bivalves, potential impacts, and enlightening the future based on a comparative study. Sci Total Environ 838:155933. https://doi.org/10.1016/j.scitotenv.2022.155933
Modesto KA, Martinez CBR (2010) Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78(3):294–299. https://doi.org/10.1016/j.chemosphere.2009.10.047
Moreschi AC, Callil CT, Christo SW, Ferreira Junior AL, Nardes C, de Faria É, Girard P (2020) Filtration, assimilation and elimination of microplastics by freshwater bivalves. Case Stud Chem Environ Eng 2:100053. https://doi.org/10.1016/j.cscee.2020.100053
Naidu BC, Xavier KM, Shukla SP, Jaiswar AK, Nayak BB (2022) Comparative study on the microplastics abundance, characteristics, and possible sources in yellow clams of different demographic regions of the northwest coast of India. J Hazard Mater Lett 3:100051
Oliveira M, Almeida M, Miguel I (2019) A micro(nano)plastic boomerang tale: a never ending story? TrAC – Trends Anal Chem 112:196–200. https://doi.org/10.1016/j.trac.2019.01.005
Oliveira P De, Gomes AQ, Pacheco TR, Almeida VV De, Saldanha C (2012) Cell-specific regulation of acetylcholinesterase expression under inflammatory conditions 51, 129–137. https://doi.org/10.3233/CH-2011-1520
Oliveira P, Barboza LGA, Branco V, Figueiredo N, Carvalho C, Guilhermino L (2018) Effects of microplastics and mercury in the freshwater bivalve Corbicula fluminea (Müller, 1774): filtration rate, biochemical biomarkers and mercury bioconcentration. Ecotoxicol Environ Saf 164:155–163. https://doi.org/10.1016/j.ecoenv.2018.07.062
Pan G, Dutta HM (1998) The inhibition of brain acetylcholinesterase activity of juvenile largemouth bass micropterus salmoides by sublethal concentrations of diazinon. Environ Res 79(2):133–137. https://doi.org/10.1006/enrs.1998.3868
Parra S, Varandas S, Santos D, Fernandes L, Cabecinha E, Monteiro SM (2021) Multi-Biomarker Responses of Asian Clam Corbicula fluminea. Water.
Pedersen AF, Gopalakrishnan K, Boegehold AG, Peraino NJ, Westrick JA, Kashian DR (2020) Microplastic ingestion by quagga mussels, Dreissena bugensis, and its effects on physiological processes. Environ Pollut 260:113964. https://doi.org/10.1016/j.envpol.2020.113964
Phuong NN, Poirier L, Lagarde F, Kamari A, Zalouk-Vergnoux A (2018) Microplastic abundance and characteristics in French Atlantic coastal sediments using a new extraction method. Environ Pollut 243:228–237. https://doi.org/10.1016/j.envpol.2018.08.032
Pires A, Cuccaro A, Sole M, Freitas R (2022) Micro(nano)plastics and plastic additives effects in marine annelids: a literature review. Environ Res 214:113642. https://doi.org/10.1016/j.envres.2022.113642
Qu H, Ma R, Barrett H, Wang B, Han J, Wang F, Chen P, Wang W, Peng G, Yu G (2020) How microplastics affect chiral illicit drug methamphetamine in aquatic food chain? From green alga (Chlorella pyrenoidosa) to freshwater snail (Cipangopaludian cathayensis). Environ Int 136:105480. https://doi.org/10.1016/j.envint.2020.105480
Revel M, Lagarde F, Perrein-Ettajani H, Bruneau M, Akcha F, Sussarellu R, Rouxel J, Costil K, Decottignies P, Cognie B, Châtel A, Mouneyrac C (2019) Tissue-specific biomarker responses in the blue mussel Mytilus spp. exposed to a mixture of microplastics at environmentally relevant concentrations. Front Environ Sci 7:1–14. https://doi.org/10.3389/fenvs.2019.00033
Ribeiro F, Garcia AR, Pereira BP, Fonseca M, Mestre NC, Fonseca TG et al. (2017) Microplastics effects in Scrobicularia plana. Mar Pollut Bull 122:379–391. https://doi.org/10.1016/j.marpolbul.2017.06.078
Rochman CM, Parnis JM, Browne MA, Serrato S, Reiner EJ, Robson M, Young T, Diamond ML, Teh SJ (2017) Direct and indirect effects of different types of microplastics on freshwater prey (Corbicula fluminea) and their predator (Acipenser transmontanus). PLoS One 12(11):e0187664. https://doi.org/10.1371/journal.pone.0187664. Nov 6
Sendra M, Sparaventi E, Novoa B, Figueras A (2021) An overview of the internalization and effects of microplastics and nanoplastics as pollutants of emerging concern in bivalves. Sci Total Environ 753:142024. https://doi.org/10.1016/j.scitotenv.2020.142024
Shang Y, Wang X, Chang X, Sokolova IM, Wei S, Liu W, Wang Y (2021) The effect of microplastics on the bioenergetics of the mussel Mytilus coruscus assessed by cellular energy allocation approach. Front Mar Sci 8:754789
Statista Research Department, Jun 12, 2023. https://www.statista.com/statistics/282732/global-production-of-plastics-since-1950/
Su L, Cai H, Kolandhasamy P, Wu C, Rochman CM, Shi H (2018) Using the Asian clam as an indicator of microplastic pollution in freshwater ecosystems. Environ Pollut 234:347–355. https://doi.org/10.1016/j.envpol.2017.11.075
Su L, Xue Y, Li L, Yang D, Kolandhasamy P, Li D et al. (2016) Microplastics in Taihu Lake. China Environ Pollut 216:711–719. https://doi.org/10.1016/j.envpol.2017.11.075
Sunderman FW, Marzouk A, Hopfer SM, Zaharia O, Reid MC (1985) Increased lipid peroxidation in tissues of nickel chloride-treated rats Ann. Clin Lab Sci 15:229–236. pp.
Tan H, Yue T, Xu Y, Zhao J, Xing B (2020) Microplastics reduce lipid digestion in simulated human gastrointestinal system. Environ Sci Technol 54(19):12285–12294. https://doi.org/10.1021/acs.est.0c02608
Treilles R, Gasperi J, Gallard A, Saad M, Dris R, Partibane C, Tassin B (2021) Microplastics and microfibers in urban runoff from a suburban catchment of Greater Paris. Environ Pollut 287:117352. https://doi.org/10.1016/j.envpol.2021.117352
Uddin S, Fowler SW, Uddin MF, Behbehani M, Naji A (2021) A review of microplastic distribution in sediment profiles. Mar Pollut Bull 163:111973. https://doi.org/10.1016/j.marpolbul.2021.111973
Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen-Int. Ver. Für Limnol. 9:1–38
Vidal A, Phuong NN, Métais I, Gasperi J, Châtel A (2023) Assessment of microplastic contamination in the Loire River (France) throughout analysis of different biotic and abiotic freshwater matrices. Environ Pollut 122167:ISSN 0269-7491. https://doi.org/10.1016/j.envpol.2023.122167
Wang J, Liu X, Li Y, Powell T, Wang X, Wang G, Zhang P (2019) Microplastics as contaminants in the soil environment: a mini-review. Sci Total Environ 691:848–857. https://doi.org/10.1016/j.scitotenv.2019.07.209
Ward JE, Rosa M, Shumway SE (2019) Capture, ingestion, and egestion of microplastics by suspension-feeding bivalves: a 40-year history. Anthr Coasts 2(1):39–49. https://doi.org/10.1139/anc-2018-0027
Wirnkor VA, Ngozi VE, Ebere EC (2019) Microplastics, an emerging concern: a review of analytical techniques for detecting and quantifying microplatics. Anal Methods Environ Chem J 2:15–32. https://doi.org/10.24200/amecj.v2.i2.57
Wu H, Zhong M, Lu Z, Shan X, Li F, Ji C, Cong M (2018) Biological effects of tris (1-chloro-2-propyl) phosphate (TCPP) on immunity in mussel Mytilus galloprovincialis. Environ Toxicol Pharmacol 61:102–106. https://doi.org/10.1016/j.etap.2018.05.022
Wu Y, Yang J, Li Z, He H, Wang Y, Wu H, Xie L, Chen D, Wang L (2022) How does bivalve size influence microplastics accumulation? Environ Res 214(Part 1):113847. https://doi.org/10.1016/j.envres.2022.113847
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This work was supported by Angers Loire Metropole and the project plastinium funded by the Pays de Loire region and Nantes Metropole.
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AV, OL, IM and AC conceived and designed the experimental set up. AV performed the field campaign and the laboratory analyses, assisted by IM and AC. AV and JG realised the spectroscopy analyses. ALG did all the statistics on the results. AV collected all the data, interpreted it and wrote the first draft of the manuscript. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Vidal, A., Métais, I., Latchere, O. et al. Toxicity assessment of microplastics within the Loire River in the clam Corbicula fluminea exposed to environmentally relevant exposure conditions. Ecotoxicology 32, 1125–1140 (2023). https://doi.org/10.1007/s10646-023-02702-2
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DOI: https://doi.org/10.1007/s10646-023-02702-2