Effects of environmentally relevant levels of polyethylene microplastic on Mytilus galloprovincialis (Mollusca: Bivalvia): filtration rate and oxidative stress.
Biomarkers
Filtration rate
Microplastics
Mytilus galloprovincialis
Polyethylene
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
Jun 2021
Jun 2021
Historique:
received:
25
09
2020
accepted:
12
01
2021
pubmed:
27
1
2021
medline:
1
6
2021
entrez:
26
1
2021
Statut:
ppublish
Résumé
The objective of the present study was to evaluate the potential toxic effects of polyethylene microplastics (PE-MPs) (40-48 μm) on the Mediterranean mussel Mytilus galloprovincialis in controlled laboratory conditions. The exposure was carried out for 14 days with three environmentally relevant PE-MPs concentrations of 1, 10, and 100 and a high concentration of 1000 μg/L. Effects of PE-MPs were assessed by evaluating the filtration rate (FR) after 7 and 14 days of exposure and by analyzing biochemical biomarkers of oxidative stress (catalase - CAT, glutathione S-transferase - GST, and the levels of lipid peroxidation - LPO) in the M. galloprovincialis digestive gland after 14 days of exposure. Results showed that M. galloprovincialis does not accumulate PE-MPs of 40-48 μm size in its whole tissues. The filtration rate was significantly reduced with the increase of PE-MPs concentrations. The biochemical biomarkers indicated that PE-MPs induced oxidative damage (LPO) at low concentrations (1 and 10 μg/L) with a significant reduction in females of 1000 μg/L treated group and inactivate antioxidative system (CAT and GST) in the digestive gland of both sexes at high concentrations (100 and 1000 μg/L). This study demonstrates that PE-MPs have biological effects on M. galloprovincialis at environmentally relevant concentrations thus brings new insights on the potential impacts of PE-MPs in marine bivalves.
Identifiants
pubmed: 33495949
doi: 10.1007/s11356-021-12506-8
pii: 10.1007/s11356-021-12506-8
doi:
Substances chimiques
Biomarkers
0
Microplastics
0
Plastics
0
Water Pollutants, Chemical
0
Polyethylene
9002-88-4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26643-26652Références
Abidli S, Toumi H, Lahbib Y, Trigui El Menif N (2017) The first evaluation of microplastics in sediments from the complex Lagoon-Channel of Bizerte (northern Tunisia). Water Air Soil Pollut 228:262
doi: 10.1007/s11270-017-3439-9
Abidli S, Antunes JC, Ferreira JL, Lahbib Y, Sobral P, Trigui El Menif N (2018) Microplastics in sediments from the littoral zone of the north Tunisian coast (Mediterranean Sea). Estuar Coast Shelf Sci 205:1–9
doi: 10.1016/j.ecss.2018.03.006
Abidli S, Lahbib Y, Trigui El Menif N (2019) Microplastics in commercial molluscs from the lagoon of Bizerte (Northern Tunisia). Mar Pollut Bull 142:243–252
doi: 10.1016/j.marpolbul.2019.03.048
Aebi H 1974 Catalase. In Bergmeyer HU (ed) Methods of enzymatic analysis (2nd edn). Academic Press, pp 673–684
Allen S, Allen D, Phoenix VR, Le Roux G, Jimenez PD, Simonneau A, Binet S, Galop D (2019) Atmospheric transport and deposition of microplastics in a remote mountain catchment. Nat Geosci 12:339–344
doi: 10.1038/s41561-019-0335-5
Allsopp M, Walters A, Santillo D, Johnsto P (2006) Plastic debris in the world’s oceans. Greenpeace International, Amsterdam
Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62:1596–1605
doi: 10.1016/j.marpolbul.2011.05.030
Andrady AL (2015) Plastics in the oceans. In: Plastics and Environmental Sustainability. John Wiley & Sons, Inc., pp 295–318
Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico G, Pauletto M, Bargelloni L, Regoli F (2015a) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222
doi: 10.1016/j.envpol.2014.12.021
Avio CG, Gorbi S, Regoli F (2015b) Experimental development of a new protocol for extraction and characterization of microplastics in fish tissues: first observations in commercial species from Adriatic Sea. Mar Environ Res 111:18–26
doi: 10.1016/j.marenvres.2015.06.014
Avio CG, Gorbi S, Regoli F (2017) Plastics and microplastics in the oceans: from emerging pollutants to emerged threat. Mar Environ Res 128:2–11
doi: 10.1016/j.marenvres.2016.05.012
Ayala A, Muñoz MF, Argüelles S (2014) Lipid Peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev 2014:360438
doi: 10.1155/2014/360438
Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C Toxicol Pharmacol 140:175–186
doi: 10.1016/j.cca.2005.01.013
Barnes DKA, Galgani F, Thompson RC, Barlaz M (2009) Accumulation and fragmentation of plastic debris in global environments. Philos Trans R Soc B Biol Sci 364:1985–1998
doi: 10.1098/rstb.2008.0205
Beyer J, Green NW, Brooks S, Allan IJ, Ruus A, Gomes T, Bråte ILN, Schøyen M (2017) Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: a review. Mar Environ Res 130:338–365
doi: 10.1016/j.marenvres.2017.07.024
Branch GM, Steffani NC (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215
doi: 10.1016/j.jembe.2003.12.007
Bråte ILN, Blazquez M, Brooks SJ, Thomas KV (2018) Weathering impacts the uptake of polyethylene microparticles from toothpaste in Mediterranean mussels (M. galloprovincialis). Sci Total Environ 626:1310–1318
doi: 10.1016/j.scitotenv.2018.01.141
Capela R, Raimundo J, Santos MM, Caetano M, Micaelo C, Vale C, Guimarães L, Reis-Henriques MA (2016) The use of biomarkers as integrative tools for transitional water bodies monitoring in the Water Framework Directive context — a holistic approach in Minho river transitional waters. Sci Total Environ 539:85–96
doi: 10.1016/j.scitotenv.2015.08.113
Castro M, Santos MM, Monteiro NM, Vieira N (2004) Measuring lysosomal stability as an effective tool for marine coastal environmental monitoring. Mar Environ Res 58:741–745
doi: 10.1016/j.marenvres.2004.03.088
Catsiki VA, Florou H (2006) Study on the behaviour of the heavy metals Cu, Cr, Ni, Zn, Fe, Mn and 137Cs in an estuarine ecosystem using Mytilus galloprovincialis as a bioindicator species: the case of Thermaikos gulf, Greece. J Environ Radioact 86:31–44
doi: 10.1016/j.jenvrad.2005.07.005
Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bull 62:2588–2597
doi: 10.1016/j.marpolbul.2011.09.025
Cole M, Lindeque P, Fileman E, Halsband C, Galloway TS (2015) The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ Sci Technol 49:1130–1137
doi: 10.1021/es504525u
Coughlan J (1969) Estimation of filtering rate from clearance of suspensions. Mar Biol 2:356–358
doi: 10.1007/BF00355716
Digka N, Tsangaris C, Torre M, Anastasopoulou A, Zeri C (2018) Microplastics in mussels and fish from the Northern Ionian Sea. Mar Pollut Bull 135:30–40
doi: 10.1016/j.marpolbul.2018.06.063
Duis K, Coors A (2016) Microplastics in the aquatic and terrestrial environment: sources (with a specific focus on personal care products), fate and effect. Environ Sci Eur 28:2
doi: 10.1186/s12302-015-0069-y
Eriksen M, Maximenko N, Thiel M, Cummins A, Lattin G, Wilson S, Hafner J, Zellers A, Rifman S (2013) Plastic pollution in the South Pacific subtropical gyre. Mar Pollut Bull 68:71–76
doi: 10.1016/j.marpolbul.2012.12.021
Erni-Cassola G, Zadjelovic V, Gibson MI, Christie-Oleza MJ (2019) Distribution of plastic polymer types in the marine environment; a meta-analysis. J Hazard Mater 369:691–698
doi: 10.1016/j.jhazmat.2019.02.067
Faggio C, Pagano M, Alampi R, Vazzana I, Felice MR (2016) Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of quaternium-15 in Mytilus galloprovincialis. Aquat Toxicol 180:258–265
doi: 10.1016/j.aquatox.2016.10.010
Ferreira M, Moradas-Ferreira P, Reis-Henriques MA (2007) The effect of long-term depuration on levels of oxidative stress biomarkers in mullets (Mugil cephalus) chronically exposed to contaminants. Mar Environ Res 64:181–190
doi: 10.1016/j.marenvres.2007.01.001
Ferreira M, Antunes P, Costa J, Amado J, Gil O, Pousao-Ferreira P, Vale C, Reis-Henriques MA (2008) Organochlorine bioaccumulation and biomarkers levels in culture and wild white seabream (Diplodus sargus). Chemosphere 73:1669–1674
doi: 10.1016/j.chemosphere.2008.07.070
Galgani F, Hanke G, Werner S, De Vrees L (2013) Marine litter within the European marine strategy framework directive. ICES J Mar Sci 70:1055–1064
doi: 10.1093/icesjms/fst122
Goldstein MC, Rosenberg M, Cheng L (2012) Increased oceanic microplastic debris enhances oviposition in an endemic pelagic insect. Biol Lett 8:817–820
doi: 10.1098/rsbl.2012.0298
Güven O, Gökdağ K, Jovanović B, Kıdeyş AE (2017) Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ Pollut 223:286–294
doi: 10.1016/j.envpol.2017.01.025
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
doi: 10.1016/S0021-9258(19)42083-8
Halliwell B, Gutteridge JM (2015) Free radicals in biology and medicine, 4th edn. Oxford University Press, USA
doi: 10.1093/acprof:oso/9780198717478.001.0001
Ivar do Sul JA, Costa MF (2014) The present and future of microplastic pollution in the marine environment. Environ Pollut 185:352–364
doi: 10.1016/j.envpol.2013.10.036
Ivar do Sul JA, Costa MF, Fillmann G (2014) Microplastics in the pelagic environment around oceanic islands of the Western Tropical Atlantic Ocean. Water Air Soil Pollut 225:2004
doi: 10.1007/s11270-014-2004-z
James K, Vasanta K, Padua S, Gopinatha V, Abilash KS, Jeyabaskaran R, Babua A, John S (2020) An assessment of microplastics in the ecosystem and selected commercially important fishes off Kochi, south eastern Arabian Sea, India. Mar Pollut Bull 154:111027
doi: 10.1016/j.marpolbul.2020.111027
Jeong CB, Won EJ, Kang HM, Lee MC, Hwang DS, Hwang UK, Zhou B, Souissi S, Lee JS (2016) Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ Sci Technol 50:8849–8857
doi: 10.1021/acs.est.6b01441
Jeong CB, Kang HM, Lee MC, Kim DH, Han J, Hwang DS, Souissi S, Lee SJ, Shin KH, Park HG, Lee JS (2017) Adverse effects of microplastics and oxidative stress-induced MAPK/Nrf2 pathway-mediated defense mechanisms in the marine copepod Paracyclopina nana. Sci Rep 7:41323
doi: 10.1038/srep41323
Lenz R, Enders K, Nielsen TG (2016) Microplastic exposure studies should be environmentally realistic. Proc Natl Acad Sci USA 113:E4121–E4122
doi: 10.1073/pnas.1606615113
Li HX, Ma LS, Lin L, Ni ZX, Xu XR, Shi HH, Yan Y, Zheng GM, Rittschof D (2018) Microplastics in oysters Saccostrea cucullata along the Pearl River Estuary, China. Environ Pollut 236:619–625
doi: 10.1016/j.envpol.2018.01.083
Li J, Lusher AL, Rotchell JM, Deudero S, Turra A, Bråte ILN, Sun C, Shahadat Hossain M, Li Q, Kolandhasamy P, Shi H (2019) Using mussel as a global bioindicator of coastal microplastic pollution. Environ Pollut 244:522–533
doi: 10.1016/j.envpol.2018.10.032
Livingstone DR, Lips F, Garcia Martinez P, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Biol 112:265–276
doi: 10.1007/BF00702471
Livingstone DR, Chipman JK, Lowe DM, Minier C, Mitchelmore CL, Moore MN, Peters LD, Pipe RK (2000) Development of biomarkers to detect the effects of organic pollution on aquatic invertebrates: recent molecular, genotoxic, cellular and immunological studies on the common mussel (Mytilus edulis L.) and other mytilids. Int J Environ Pollut 13:56–91
doi: 10.1504/IJEP.2000.002311
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
doi: 10.1016/S0021-9258(19)52451-6
Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C 153:175–190
Lusher AL, Welden NA, Sobral P, Cole M (2017) Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal Methods 9:1346–1360
doi: 10.1039/C6AY02415G
Moreschi AC, Callil CT, Christo SW, Ferreira Junior AL, Nardes C, de Faria E, Girard P (2020) Filtration, assimilation and elimination of microplastics by freshwater bivalves. Case Stud Chem Environ Eng 2:100053
doi: 10.1016/j.cscee.2020.100053
Nam TG (2011) Lipid peroxidation and its toxicological implications. Toxicol Res 27:1–6
doi: 10.5487/TR.2011.27.1.001
Nelms SE, Barnett J, Brownlow A, Davison NJ, Deaville R, Galloway TS, Lindeque PK, Santillo D, Godley BJ (2019) Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory? Sci Rep 9:1075
doi: 10.1038/s41598-018-37428-3
Ng EL, Huerta Lwanga E, Eldridge SM, Johnston P, Hu HW, Geissen V, Chen D (2018) An overview of microplastic and nanoplastic pollution in agroecosystems. Sci Total Environ 627:1377–1388
doi: 10.1016/j.scitotenv.2018.01.341
Oberbeckmann S, Löder MGJ, Labrenz M (2015) Marine microplastic-associated biofilms – a review. Environ Chem 12:551–562
doi: 10.1071/EN15069
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 30:155–163
doi: 10.1016/j.ecoenv.2018.07.062
Orescanin V, Lovrencic I, Mikelic L, Barisic D, Matasin Z, Lulic S, Pezelj D (2006) Biomonitoring of heavy metals and arsenic on the coast of the Middle Adriatic sea using Mytilus galloprovincialis. Nucl Inst Methods Phys Res B 245:495–500
doi: 10.1016/j.nimb.2005.11.050
OSPAR (2015) OSPAR request on development of a common monitoring protocol for plastic particles in fish stomachs and selected shellfish on the basis of existing fish disease surveys. In ICES Advice 2015, Book 1
Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2012) Biochemical response of anthracene and benzo [a] pyrene in milkfish Chanos chanos. Ecotoxicol Environ Saf 75:187–197
doi: 10.1016/j.ecoenv.2011.08.028
Paul-Pont I, Lacroix C, González Fernández C, Hégaret H, Lambert C, Le Goïc N, Frère L, Cassone AL, Sussarellu R, Fabioux C, Guyomarch J, Albentosa M, Huvet A, Soudant P (2016) Exposure of marine mussels Mytilus spp. to polystyrene microplastics: toxicity and influence on fluoranthene bioaccumulation. Environ Pollut 216:724–737
doi: 10.1016/j.envpol.2016.06.039
Penning WE, Pozzato L, Vijverberg J, Noordhuis R, Bij de Vaate A, Van Donk E, Dionisio Pires LM (2013) Effects of suspended sediments on food uptake for zebra mussels in Lake Markermeer, The Netherlands. Inland Waters 3:437–450
doi: 10.5268/IW-3.4.473
Pinheiro M, Caetano M, Neuparth T, Barros S, Soares J, Raimundo J, Vale C, Coimbra J, Castro LFC, Santos MM (2019) Ecotoxicology of deep-sea environments: functional and biochemical effects of suspended sediments in the model species Mytilus galloprovincialis under hyperbaric conditions. Sci Total Environ 670:218–225
doi: 10.1016/j.scitotenv.2019.03.196
PlasticsEurope (2019) Plastics – the Facts 2019 - an analysis of European plastics production, demand and waste data, p42
Prokić MD, Petrović TG, Gavrić JP, Despotović SG, Gavrilović BR, Radovanović TB, Faggio C, Saičić ZS (2018) Comparative assessment of the antioxidative defense system in subadult and adult anurans: a lesson from the Bufotes viridis toad. Zoology 130:30–37
doi: 10.1016/j.zool.2018.08.001
Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106–117
doi: 10.1016/j.marenvres.2013.07.006
Renzi M, Guerranti C, Blašković A (2018) Microplastic contents from maricultured and natural mussels. Mar Pollut Bull 131:248–251
doi: 10.1016/j.marpolbul.2018.04.035
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 Environ Toxicol 7:33
doi: 10.3389/fenvs.2019.00033
Revel M, Châtel A, Perrein-Ettajani H, Bruneau M, Akcha F, Sussarellu R, Rouxel J, Costil K, Decottignies P, Cognie B, Lagarde F, Mouneyrac C (2020) Realistic environmental exposure to microplastics does not induce biological effects in the Pacific oyster Crassostrea gigas. Mar Pollut Bull 150:110627
doi: 10.1016/j.marpolbul.2019.110627
Rist S, Steensgaard IM, Guven O, Nielsen TG, Jensen LH, Møller LF, Hartmann NB (2019) The fate of microplastics during uptake and depuration phases in a blue mussel exposure system. Environ Toxicol Chem 38:99–105
doi: 10.1002/etc.4285
Rochman CM, Tahir A, Williams SL, Baxa DV, Lam R, Miller JT, Teh FC, Werorilangi S, Teh SJ (2015) Anthropogenic debris in seafood: plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Sci Rep 5:14340
doi: 10.1038/srep14340
Rosa M, Ward JE, Shumway SE (2018) Selective capture and ingestion of particles by suspension-feeding bivalve molluscs: a review. J Shellfish Res 37:727–746
doi: 10.2983/035.037.0405
Sellami B, Khazri A, Louati H, Dellali M, Driss MR, Aïssa P, Mahmoudi E, Hamouda B, Coelho AV, Sheehan D (2015) Effects of anthracene on filtration rates, antioxidant defense system, and redox proteomics in the Mediterranean clam Ruditapes decussatus (Mollusca: Bivalvia). Environ Sci Pollut Res 22:10956–10968
doi: 10.1007/s11356-015-4328-7
Sıkdokur E, Belivermis M, Sezer N, Pekmez M, Bulan OK, Kılıç O (2020) Effects of microplastics and mercury on manila clam Ruditapes philippinarum: feeding rate, immunomodulation, histopathology andoxidative stress. Environ Pollut 262:114247
doi: 10.1016/j.envpol.2020.114247
Sussarellu R, Soudant P, Lambert C, Fabioux C, Corporeau C, Laot C, Le Goic N, Quillien V, Boudry P, Long M, Mingant C, Petton B, Maes T, Vethaak D, Robbens J, Huvet A (2016) Oyster reproduction is affected by exposure to polystyrene microplastics. Proc Natl Acad Sci 113:2430–2435
doi: 10.1073/pnas.1519019113
Tlili S, Jemai D, Brinis S, Regaya I (2020) Microplastics mixture exposure at environmentally relevantconditions induce oxidative stress and neurotoxicity in the wedge clam Donax trunculus. Chemosphere 258:127344
doi: 10.1016/j.chemosphere.2020.127344
Toumi H, Abidli S, Bejaoui M (2019) Microplastics in freshwater environment: the first evaluation in sediments from seven water streams surrounding the lagoon of Bizerte (Northern Tunisia). Environ Sci Pollut Res 26:14673–14682
doi: 10.1007/s11356-019-04695-0
Tran D, Fournier E, Durrieu G, Massabuau JC (2007) Inorganic mercury detection by valve closure response in the freshwater clam Corbicula fluminea: integration of time and water metal concentration changes. Environ Toxicol Chem 26:1545–1551
doi: 10.1897/06-390R1.1
Ward JE, Shumway SE (2004) Separating the grain from the chaff: Particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130
doi: 10.1016/j.jembe.2004.03.002
WEF (2016) The New Plastics Economy Rethinking the future of plastics, p 36
Wegner A, Besseling E, Foekema EM, Kamermans P, Koelmans AA (2012) Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environ Toxicol Chem 31:2490–2497
doi: 10.1002/etc.1984
Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161
doi: 10.1016/0166-445X(91)90033-6
Wright SL, Thompson RC, Galloway TS (2013) The physical impacts of microplastics on marine organisms: a review. Environ Pollut 178:483–492
doi: 10.1016/j.envpol.2013.02.031
Xu X-Y, Lee WT, Chan AKY, Lo HS, Shin PKS, Cheung SG (2017) Microplastic ingestion reduces energy intake in the clam Atactodea striata. Mar Pollut Bull 124:798–802
doi: 10.1016/j.marpolbul.2016.12.027
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
doi: 10.1016/j.jhazmat.2018.07.110