Abstract
Bioplastics such as polylactic acid are actually promoted as eco-friendly alternatives to fossil fuel-derived plastics, yet bioplastic toxicity remains poorly known. Here we studied the acute and multigenerational effects of polylactic acid microplastics on the copepod Eurytemora affinis, a bioindicator species of zooplankton. Results on acute toxicity revealed that lethal concentration values are higher for adult males, of 134.6 mg microplastic/L, than for adult females, of 106.9 mg/L. In multigeneration exposure, 400 µg/L polylactic acid microplastics induced higher mortality, production of smaller-sized eggs, elongation of the naupliar phase, and offspring with lower fitness. This led to reduction in female body size, including prosome length, width, and volume. Noteworthy, we also observed a recovery in copepod survival and reproductive parameters in the fifth filial generation.
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References
Ali W, Ali H, Gillani S, Zinck P, Souissi S (2023a) Polylactic acid synthesis, biodegradability, conversion to microplastics and toxicity: a review. Environ Chem Lett 21:1761–1786. https://doi.org/10.1007/s10311-023-01564-8
Ali W, Ali H, Souissi S, Zinck P (2023b) Are bioplastics an ecofriendly alternative to fossil fuel plastics? Environ Chem Lett 21:1991–2002. https://doi.org/10.1007/s10311-023-01601-6
Ali W, Jeong H, Lee JS, Zinck P, Souissi S (2024) Biodegradable microplastics interaction with pollutants and their potential toxicity for aquatic biota: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-024-01703-9
An G, Na J, Song J, Jung J (2024) Chronic toxicity of biodegradable microplastic (Polylactic acid) to Daphnia magna: a comparison with polyethylene terephthalate. Aquat Toxicol 266:106790. https://doi.org/10.1016/j.aquatox.2023.106790
Beiras R, Bellas J, Cachot J et al (2018) Ingestion and contact with polyethylene microplastics does not cause acute toxicity on marine zooplankton. J Hazard Mater 360:452–460. https://doi.org/10.1016/j.jhazmat.2018.07.101
Botterell ZL, Beaumont N, Dorrington T et al (2019) Bioavailability and effects of microplastics on marine zooplankton: a review. Environ Pollut 245:98–110. https://doi.org/10.1016/j.envpol.2018.10.065
Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger J, Galloway TS (2013) Microplastic ingestion by zooplankton. Environ Sci Technol 47:6646–6655
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. https://doi.org/10.1021/es504525u
Corona S, Hirst A, Atkinson D, Atkinson A (2021) Density-dependent modulation of copepod body size and temperature–size responses in a shelf sea. Limnol Oceanogr 66:3916. https://doi.org/10.1002/lno.11930
Cózar A, Echevarría F, González-Gordillo JI et al (2014) Plastic debris in the open ocean. Proc Natl Acad Sci 111:28. https://doi.org/10.1073/pnas.1314705111
Das S, Souissi A, Ouddane B, Hwang JS, Souissi S (2023) Trace metals exposure in three different coastal compartments show specific morphological and reproductive traits across generations in a sentinel copepod. Sci Tot Environ 859:160378. https://doi.org/10.1016/j.scitotenv.2022.160378
Di Giannantonio M, Gambardella C, Miroglio R et al (2022) Ecotoxicity of polyvinylidene difluoride (PVDF) and polylactic acid (PLA) microplastics in marine zooplankton. Toxics 10:479. https://doi.org/10.3390/toxics10080479
Eltemsah YS, Bøhn T (2019) Acute and chronic effects of polystyrene microplastics on juvenile and adult Daphnia magna. Environ Pollut 254:112919. https://doi.org/10.1016/j.envpol.2019.07.087
EuropeanBioplastics (2023) Bioplastics market development update 2023. https://docs.european-bioplastics.org/publications/market_data/2023/EUBP_Market_Data_Report_2023.pdf (Accessed Dec 2023)
Eze CG, Nwankwo CE, Dey S, Sundaramurthy S, Okeke ES (2024) Food chain microplastics contamination and impact on human health: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-024-01734-2
Ferreira PS, Ribeiro SM, Pontes R, Nunes J (2024) Production methods and applications of bioactive polylactic acid: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-024-01729-z
Gréve HV, Almeda R, Lindegren M, Kiorboe T (2017) Gender-specific feeding rates in planktonic copepods with different feeding behavior. J Plankton Res 39:631–644. https://doi.org/10.1093/plankt/fbx033
Hämäläinen A, McAdam AG et al (2017) Fitness consequences of peak reproductive effort in a resource pulse system. Sci Rep 7:9335. https://doi.org/10.1038/s41598-017-09724-x
Jamieson CD, Santer B (2003) Maternal aging in the univoltine freshwater copepod Cyclops kolensis: variation in egg sizes, egg development times, and naupliar development times. Hydrobiologia 510:75. https://doi.org/10.1023/B:HYDR.0000008533.64765.87
Jemec A, Horvat P, Kunej U, Bele M, Kržan A (2016) Uptake and effects of microplastic textile fibers on freshwater crustacean Daphnia magna. Environ Pollut 219:201. https://doi.org/10.1016/j.envpol.2016.10.037
John J, Nandhini AR, Velayudhaperumal Chellam P, Sillanpää M (2022) Microplastics in mangroves and coral reef ecosystems: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-021-01326-4
Kadiene EU, Bialais C et al (2017) Differences in lethal response between male and female calanoid copepods and life cycle traits to cadmium toxicity. Ecotoxicology 26:1227–1239. https://doi.org/10.1007/s10646-017-1848-6
Kadiene EU, Meng PJ, Hwang JS, Souissi S (2019) Acute and chronic toxicity of cadmium on the copepod Pseudodiaptomus annandalei: A life history traits approach. Chemosphere 233:396–404. https://doi.org/10.1016/j.chemosphere.2019.05.220
Kazour M, Jemaa S et al (2019) Microplastics pollution along the Lebanese coast (Eastern Mediterranean Basin): occurrence in surface water, sediments and biota samples. Sci Tot Environ 696:133933. https://doi.org/10.1016/j.scitotenv.2019.133933
Le Gall M, Niu Z, Curto M et al (2022) Behaviour of a self-reinforced polylactic acid (SRPLA) in seawater. Polym Testing 111:107619. https://doi.org/10.1016/j.polymertesting.2022.107619
Lee KW, Shim WJ, Kwon OY, Kang JH (2013) Size-dependent effects of micropolystyrene particles in the marine copepod Tigriopus japonicus. Environ Sci Technol 47:11278–11283. https://doi.org/10.1021/es401932b
Liu Z, Yu P, Cai M et al (2019) Polystyrene nanoplastic exposure induces immobilization, reproduction, and stress defense in the freshwater cladoceran Daphnia pulex. Chemosphere 215:74. https://doi.org/10.1016/j.chemosphere.2018.09.176
Lo HKA, Chan KYK (2018) Negative effects of microplastic exposure on growth and development of Crepidula onyx. Environ Pollut 233:588–595. https://doi.org/10.1016/j.envpol.2017.10.095
Martins A, Guilhermino L (2018) Transgenerational effects and recovery of microplastics exposure in model populations of the freshwater cladoceran Daphnia magna Straus. Sci Tot Environ 631:421. https://doi.org/10.1016/j.scitotenv.2018.03.054
Na J, Song J, Jung J (2023) Elevated temperature enhanced lethal and sublethal acute toxicity of polyethylene microplastic fragments in Daphnia magna. Environ Toxicol Pharmacol 102:104212. https://doi.org/10.1016/j.etap.2023.104212
Osman AI, Hosny M, Eltaweil AS, Omar S, Elgarahy AM, Farghali M, Yap PS, Wu YS, Nagandran S, Batumalaie K, Gopinath SC (2023) Microplastic sources, formation, toxicity and remediation: a review. Environ Chem Lett 2:2129–2169. https://doi.org/10.1007/s10311-023-01593-3
Savva K, Farré M, Barata C (2023) Sublethal effects of bio-plastic microparticles and their components on the behaviour of Daphnia magna. Environ Res 236:116775. https://doi.org/10.1016/j.envres.2023.116775
Schür C, Zipp S, Thalau T, Wagner M (2020) Microplastics but not natural particles induce multigenerational effects in Daphnia magna. Environ Pollut 260:113904. https://doi.org/10.1016/j.envpol.2019.113904
Shore EA, DeMayo JA, Pespeni MH (2021) Microplastics reduce net population growth and fecal pellet sinking rates for the marine copepod. Acartia Tonsa Environ Pollut 284:117379. https://doi.org/10.1016/j.envpol.2021.117379
Souissi S, Souissi A (2021) Promotion of the development of sentinel species in the water column: example using body size and fecundity of the egg-bearing calanoid copepod Eurytemora affinis. Water 13:1442. https://doi.org/10.3390/w13111442
Souissi A, Souissi S, Hansen BW (2016a) Physiological improvement in the copepod Eurytemora affinis through thermal and multi-generational selection. Aquacult Res 47:2227–2242. https://doi.org/10.1111/are.12675
Souissi A, Souissi S, Hwang JS (2016b) Evaluation of the copepod Eurytemora affinis life history response to temperature and salinity increases. Zool Stud 55:e4. https://doi.org/10.6620/ZS.2016.55-04
Souissi A, Hwang JS, Souissi S (2021) Reproductive trade-offs of the estuarine copepod Eurytemora affinis under different thermal and haline regimes. Sci Rep 11:20139. https://doi.org/10.1038/s41598-021-99703-0
Sroda S, Cossu-Leguille C (2011) Effects of sublethal copper exposure on two gammarid species: which is the best competitor? Ecotoxicology 20:264. https://doi.org/10.1007/s10646-010-0578-9
Thery J, Li LL, Das S et al (2023) Multigenerational exposure of microplastics on the microbiota of E. affinis (copepod): a comparative study between biodegradable and non-biodegradable microplastics. Front Ecol Evol 11:1231346. https://doi.org/10.3389/fevo.2023.1231346
Wang J, Li Y, Lu L et al (2019) Polystyrene microplastics cause tissue damages, sex-specific reproductive disruption and transgenerational effects in marine medaka (Oryzias melastigma). Environ Pollut 254:113024. https://doi.org/10.1016/j.envpol.2019.113024
Yu J, Tian JY, Xu R et al (2020) Effects of microplastics exposure on ingestion, fecundity, development, and dimethylsulfide production in Tigriopus japonicus (Harpacticoida, copepod). Environ Pollut 267:115429. https://doi.org/10.1016/j.envpol.2020.115429
Zhao J, Lan R, Wang Z et al (2023) Microplastic fragmentation by rotifers in aquatic ecosystems contributes to global nanoplastic pollution. Nat Nanotechnol. https://doi.org/10.1038/s41565-023-01534-9
Zimmermann L, Göttlich S et al (2020) What are the drivers of microplastic toxicity? Comparing the toxicity of plastic chemicals and particles to Daphnia magna. Environ Pollut 267:115392. https://doi.org/10.1016/j.envpol.2020.115392
Acknowledgements
0We are thankful to Samira Benali and Jean-Marie Raquez of the University of Mons, Belgium, for their efforts in producing and characterizing microplastics. We also thank Anissa Souissi for assistance in Figure 1.
Funding
We acknowledge Program for Early-Stage Researchers in Lille (PEARL), coordinated by Foundation I-SITE ULNE, for funding through the project ‘Assessing the toxicity of plastic fragments on zooplankton ecology via video tracking and behavioral analysis’ (TOPAZ). We also acknowledge PRIORITY COST ACTION CA20101 and the French government through the Program ‘Investissements d’avenir’ (I-SITE ULNE/ANR-16-IDEX-0004 ULNE) managed by the National Research Agency. This paper is part of the contribution to the CPER IDEAL 2021-2027 project funded by the Hauts-de-France region, the French government, Europe (FEDER), and IFREMER.
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WA contributed to the experiments, data collection, analysis, and writing of the original draft. SD and JT contributed to the experimental design and editing. HJ contributed to the experiment, data analysis, and revision. J-.SL was involved in supervising and editing. PZ and SS contributed to supervising, editing, and funding acquisition.
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Ali, W., Das, S., Thery, J. et al. Acute and multigenerational toxicity of polylactic acid microplastics on a copepod bioindicator. Environ Chem Lett (2024). https://doi.org/10.1007/s10311-024-01747-x
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DOI: https://doi.org/10.1007/s10311-024-01747-x