Impact of polyethylene microplastics on the clam Ruditapes decussatus (Mollusca: Bivalvia): examination of filtration rate, growth, and immunomodulation.
Biomarkers
Clam
Development
Filtering activity
Immune response
Plastic pollution
Journal
Ecotoxicology (London, England)
ISSN: 1573-3017
Titre abrégé: Ecotoxicology
Pays: United States
ID NLM: 9885956
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
accepted:
05
07
2023
medline:
25
8
2023
pubmed:
18
7
2023
entrez:
17
7
2023
Statut:
ppublish
Résumé
The present study was conducted to assess, for the first time, the effects of a 14 days experimental exposure to polyethylene (PE) based MPs (40-48 µm) on the clam Ruditapes decussatus. Clams were exposed to three different concentrations of MPs in controlled laboratory conditions: 10 µg/L (low), 100 µg/L (medium), and 1000 µg/L (high). The effects of MPs were assessed using a multi-marker approach, including the filtration rate, growth, and the integrity of immune cells (such as haemocyte numbers, viability, and lysosomal membrane destabilization). The results revealed that as the concentration of PE-MPs increased, the filtration rate decreased, indicating that PE-MPs hindered the clams' ability to filter water. Furthermore, there was a noticeable decrease in the overall weight of the clams, particularly in the group exposed to 1000 µg/L. This decrease could be attributed to the impairment of their nutrient filtration function. In terms of immune system biomarkers, exposure to PE-MPs led to immune system disruption, characterized by a significant increase in the number of haemocytic cells, especially in the group exposed to the high concentration. Additionally, there was a notable reduction in the viability of haemocytes, resulting in the destabilization of their lysosomal membranes, particularly in the groups exposed to medium and high PE-MPs concentrations. The findings of this study indicate that the sensitivity of hemolymph parameter changes and filtration rate in R. decussatus exposed to PE-MPs (100 and 1000 µg/L), surpasses that of growth performance and can serve as reliable indicators to assess habitat conditions and contaminant levels.
Identifiants
pubmed: 37460906
doi: 10.1007/s10646-023-02683-2
pii: 10.1007/s10646-023-02683-2
doi:
Substances chimiques
Microplastics
0
Plastics
0
Polyethylene
9002-88-4
Water Pollutants, Chemical
0
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
746-755Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Abidli S, Akkari N, Lahbib Y, Trigui El Menif N (2021a) First evaluation of microplastics in two commercial fish species from the lagoons of Bizerte and Ghar El Melh (Northern Tunisia). Reg Stud Mar Sci 41:101581
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
Abidli S, Pinheiro M, Lahbib Y, Neuparth T, Santos MM, Trigui El Menif N (2021b) Effects of environmnetally relevant levels of polyethylene microplastic on Mytilus galloprovincialis (Mollusca: Bivalvia): Filtration rate and oxidative stress. Environ Sci Pollut Res 28:26643–26652
doi: 10.1007/s11356-021-12506-8
Al Marshoudi M, Al Reasi HA, Al-Habsi A, Barry MJ (2023) Additive effects of microplastics on accumulation and toxicity of cadmium in male zebrafish. Chemosphere 334:138969
doi: 10.1016/j.chemosphere.2023.138969
Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62:1596–1605
doi: 10.1016/j.marpolbul.2011.05.030
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
doi: 10.1016/j.envpol.2014.12.021
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
Bringer A, Thomas H, Prunier G, Dubillot E, Bossut N, Churlaud C, Clérandeau C, Le Bihanic F, Cachot J (2020) High density polyethylene (HDPE) microplastics impair development and swimming activity of Pacific oyster D-larvae, Crassostrea gigas, depending on particle size. Environ Pollut 260:113978
doi: 10.1016/j.envpol.2020.113978
Brousseau P, Pillet S, Frouin H, Auffret M, Gagné F, Fournier M (2012) Linking immunotoxicity and Ecotoxicological Effects at Higher Biological Levels. Ecological Biomarkers: Indicators of Ecotoxicological Effects, Amiard-Triquet C, Amiard JC & Rainbow PS (Édit.) CRC Press, Boca Raton. p 132–146.
Canesi L, Ciacci C, Bergami E, Monopoli MP, Dawson KA, Papa S, Canonico B, Corsi I (2015) Evidence for immunomodulation and apoptotic processes induced by cationic polystyrene nanoparticles in the hemocytes of the marine bivalve Mytilus. Mar Environ Res 111:34–40
doi: 10.1016/j.marenvres.2015.06.008
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
Coughlan J (1969) Estimation of filtering rate from clearance of suspensions. Mar Biol 2:356–358
doi: 10.1007/BF00355716
Détrée C, Gallardo-Escárate C (2018) Single and repetitive microplastics exposures induce immune system modulation and homeostasis alteration in the edible mussel Mytilus galloprovincialis. Fish Shellfish Immunol 83:52–60
doi: 10.1016/j.fsi.2018.09.018
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
Donaghy L, Lambert C, Choi KS, Soudant P (2009) Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): current knowledge and future prospects. Aquaculture 297:10–24
doi: 10.1016/j.aquaculture.2009.09.003
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
Faggio C, Tsarpali V, Dailianis S (2018) Mussel digestive gland as a model tissue for assessing xenobiotics: an overview. Sci Total Environ 636:220–229
doi: 10.1016/j.scitotenv.2018.04.264
Fournier M, Blakley B, Boermans H, Brousseau P (2005) Toxicologicical considerations making the connection between toxicologic and immunotoxicologic studies as these relate to human and ecosystem health. Investigative Immunotoxicology, Tryphonas H, Fournier M, Blakley BR, Smits JEG & Brousseau P (Édit) CRC Press, Boca Raton. p 385–406.
Gagné F, Douville M, Fortier M, Fournier M (2015) Effects of a municipal effluent on freshwater mussel Elliptio complanata following challenge with Vibrio anguillarum. J Environ Sci 37:91–99
doi: 10.1016/j.jes.2015.03.029
Guan X, Tang Y, Zha S, Han Y, Shi W, Ren P, Yan M, Pan Q, Hu Y, Fang J (2019) Exogenous Ca2+ mitigates the toxic effects of TiO2 nanoparticles on phagocytosis, cell viability, and apoptosis in haemocytes of a marine bivalve mollusk, Tegillarca granosa. Environ Pollut 252:1764–1771
doi: 10.1016/j.envpol.2019.06.053
Gueguen Y, Cadoret JP, Flament D, Barreau-Roumiguière C, Girardot AL, Garnier J, Hoareau A, Bachère E, Escoubas JM (2003) Immune gene discovery by expresses sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 303:139–145
doi: 10.1016/S0378-1119(02)01149-6
He W, Liu S, Zhang W, Yi K, Zhang C, Pang H, Huang D, Huang J, Li X (2023) Recent advances on microplastic aging: identification, mechanism, influence factors, and additives release. Sci Total Environ 889:164035
doi: 10.1016/j.scitotenv.2023.164035
Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryma M, Andrady A, Narayan R (2015) Plastic waste inputs from land into the ocean and Kara Lavender Law. Science 347:768–771
doi: 10.1126/science.1260352
Jiang W, Fang J, Du M, Gao Y, Fang J, Jiang Z (2022) Microplastics influence physiological processes, growth and reproduction in the Manila clam, Ruditapes philippinarum. Environ Pollut 293:118502
doi: 10.1016/j.envpol.2021.118502
Kolandhasamy P, Su L, Li J, Qu X, Jabeen K, Shi H (2018) Adherence of microplastics to soft tissue of mussels: a novel way to uptake microplastics beyond ingestion. Sci Total Environ 610:635–640
doi: 10.1016/j.scitotenv.2017.08.053
Leslie HA, van Velzen MJM, Brandsma SH, Vethaak AD, Garcia-Vallejo JJ, Lamoree MH (2022) Discovery and quantification of plastic particle pollution in human blood. Environ Int 163:107199
doi: 10.1016/j.envint.2022.107199
Liu S, Shi W, Guo C, Zhao X, Han Y, Peng C, Chai X, Liu G (2016) Ocean acidification weakens the immune response of blood clam through hampering the NF-kappa beta and toll-like receptor pathways. Fish Shellfish Immunol 54:322–327
doi: 10.1016/j.fsi.2016.04.030
Martínez-Gómez C, Benedicto J, Campillo JA, Moore M (2008) Application and evaluation of the neutral red retention (NRR) assay for lysosomal stability in mussel populations along the Iberian Mediterranean coast. J Environ Monit 10:490–499
doi: 10.1039/b800441m
Moore MN, Allen JI, McVeigh A (2006) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304
doi: 10.1016/j.marenvres.2005.10.005
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
Oliveira P, Gabriel L, Barboza A, Branco V, Figueired N, Carvalho C, Guilhermino L (2018) Effets des microplastiques et du mercure chez le bivalve d'eau douce Corbicula fluminea (Müller, 1774): Taux de filtration, biomarqueurs biochimiques et bioconcentration du mercure. Ecotoxicol Environ Saf 30:155–163
doi: 10.1016/j.ecoenv.2018.07.062
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
Pipe RK, Coles JA (1995) Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol 5:581–595
doi: 10.1016/S1050-4648(95)80043-3
PlasticsEurope (2022) Plastics – the Facts 2022, an analysis of European plastics production, demand, conversion and waste management. 81p
Qu X, Su L, Li H, Liang M, Shi H (2018) Assessing the relationship between the abundance and properties of microplastics in water and in mussels. Sci Total Environ 621:679–686
doi: 10.1016/j.scitotenv.2017.11.284
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
Revel M, Châtel A, Mouneyrac C (2018) Micro(nano)plastics: a threat to human health? Curr Opin Environ Sci Health 1:17–23
doi: 10.1016/j.coesh.2017.10.003
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 7:33
doi: 10.3389/fenvs.2019.00033
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
Rodrigues FG, Vieira H, Campos D, Pires SFS, Rodrigues A, Silva AL, Soares A, Oliveira JMM, Bordalo M (2022) Co-Exposure with an Invasive Seaweed Exudate Increases Toxicity of Polyamide Microplastics in the Marine Mussel Mytilus galloprovincialis. Toxics. 10:43
doi: 10.3390/toxics10020043
Salo H, Dautremepuits C, Smits J, Brousseau P, Fournier M (2005) Immune markers in ecotoxicology: a comparison across species. Investigative Immunotoxicology, Tryphonas H, Fournier M, Blakley BR, Smits JEG & Brousseau P (Édit) CRC Press, Boca Raton. p 147–162.
Saud S, Yang A, Jiang Z, Ning D, Fahad S (2023) New insights in to the environmental behavior and ecological toxicity of microplastics. J Hazardous Mater Adv 10:100298
doi: 10.1016/j.hazadv.2023.100298
Shi W, Han Y, Guan X, Rong J, Su W, Zha S, Tang Y, Du X, Liu G (2019) Fluoxetine suppresses the immune responses of blood clams by reducing haemocyte viability, disturbing signal transduction and imposing physiological stress. Sci Total Environ 683:681–689
doi: 10.1016/j.scitotenv.2019.05.308
Shi W, Han Y, Sun S, Tang Y, Zhou W, Du X, Liu G (2020) Immunotoxicities of microplastics and sertraline, alone and in combination, to a bivalve species: size-dependent interaction and potential toxication mechanism. J Hazard Mater 396:122603
doi: 10.1016/j.jhazmat.2020.122603
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
Stankovic S, Kalaba P, Stankovic AR (2014) Biota as toxic metal indicators. Environ Chem Lett 12:63–84
doi: 10.1007/s10311-013-0430-6
Sussarellu R, Suquet M, Thomas Y, Lambert C, Fabioux C, Pernet MEJ, Le Goïc N, Quillien V, Mingant C, Epelboin Y, Corporeau C, Guyomarch J, Robbens J, Paul-Pont I, Soudant P, Huvet A (2016) Oyster reproduction is affected by exposure to polystyrene microplastics. PNAS 113:2430–2435
doi: 10.1073/pnas.1519019113
Talvitie J, Heinonen M, Pääkkönen JP, Vahtera E, Mikola A, Setälä O, Vahala R (2015) Do wastewater treatment plants act as a potential point source of microplastics? Preliminary study in the coastal Gulf of Finland, Baltic Sea. Water Sci Technol 72:1495–1504
doi: 10.2166/wst.2015.360
Tang Y, Han Y, Zhang W, Yu Y, Huang L, Zhou W, Shi W, Tian D, Liu G (2022) Bisphenol A and microplastics weaken the antimicrobial ability of blood clams by disrupting humoral immune responses and suppressing hemocyte chemotactic activity. Environ Pollut 307:119497
doi: 10.1016/j.envpol.2022.119497
Tang Y, Zhou W, Sun S, Du X, Han Y, Shi W, Liu G (2020) Immunotoxicity and neurotoxicity of bisphenol A and microplastics alone or in combination to a bivalve species, Tegillarca granosa. Environ Pollut 265:115115
doi: 10.1016/j.envpol.2020.115115
Tanguy M, McKenna P, Gauthier-Clerc S, Pellerin J, Danger JM, Siah M (2013) Sequence analysis of a normalized cDNA library of Mytilus edulis hemocytes exposed to Vibrio splendidus LGP32 strain. Results Immunol 3:40–50
doi: 10.1016/j.rinim.2013.04.001
Tiwari M, Rathod TD, Ajmal PY, Bhangare RC, Sahu SK (2019) Distribution and characterization of microplastics in beach sand from three different indian coastal environments. Mar Pollut Bull 140:262–273
doi: 10.1016/j.marpolbul.2019.01.055
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
Trestrail C, Walpitagama M, Miranda A, Nugegoda D, Shimeta J (2021) Microplastics alter digestive enzyme activities in the marine bivalve, Mytilus galloprovincialis. Sci Total Environ 779:146418
doi: 10.1016/j.scitotenv.2021.146418
Van Cauwenberghe L, Claessens M, Vandegehuchte MB, Janssen CR (2015) Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina) living in natural habitats. Environ Pollut 199:10–17
doi: 10.1016/j.envpol.2015.01.008
Von Moos N, Burkhardt-Holm P, Köhler A (2012) Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environ Sci Technol 46:11327–11335
doi: 10.1021/es302332w
Worm B, Lotze HK, Jubinville I, Wilcox C, Jambeck J (2017) Plastic as a persistent marine pollutant. Annu Rev Environ Resour 42:1–26
doi: 10.1146/annurev-environ-102016-060700
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