Microplastic size matters for absorption and excretion by Artemia salina and Acipenser ruthenus larvae in models of water pollution and food chain transfer
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Supplementary Files

Supplementary material 1

Keywords

Microplastics
polystyrene
Acipenser ruthenus,
Artemia salina
absorption
excretion
particle transfer
food chain

How to Cite

Frank, Y. A., Interesova, E. A., Filinova, S. A., Noskov, Y. A., & Vorobiev, D. S. (2024). Microplastic size matters for absorption and excretion by Artemia salina and Acipenser ruthenus larvae in models of water pollution and food chain transfer. Acta Biologica Sibirica, 10, 745–765. https://doi.org/10.5281/zenodo.13254570

Abstract

Microplastics pervade the hydrosphere and inevitably come into contact with aquatic organisms. The study reports quantitative data on absorption and excretion of polystyrene microspheres 2 and 10 µm in diameter by zooplankton and fish larvae on the example of Artemia salina L. and Acipenser rithenus L. At the initial concentration of 500 µg/L, A. salina accumulated 2 and 10 µm particles in amounts up to 0.103 and 0.151 ng/individual, respectively, at a similar rate. The mass content of large-sized particles in A. salina was significantly higher (p < 0.01) compared to small-sized particles throughout the experiment. Artemia salina and A. rithenus larvae did not accumulate microplastics in the gastrointestinal tract over a period of 96 and 72 h, respectively. Consumption of microplastics by A. ruthenus larvae with A. salina through the food chain was slower and less pronounced in mass than their direct absorption from water. The rates of absorption of 2 and 10 μm particles by fish attained 0.9 and 8.22 ng/individual/h from water, and 0.06 and 0.23 ng/individual/h with food, respectively. In the models of water pollution and food chain transfer, A. ruthenus larvae consumed more 10 µm particles in mass compared to 2 µm particles (p < 0.05) and at a higher rate. For 2 µm particles, the excretion time for 50% of particles from the gastrointestinal tract of fish (T50) was 32–33 h, whereas for 10 µm particles, the excretion of particles consumed with food was slower (T50=45 h) compared to that of particles absorbed directly from water (T50=25 h). The data obtained can be used to simulate transport and circulation of microplastics of different sizes in the environment.

https://doi.org/10.5281/zenodo.13254570
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References

Albano M, Panarello G, Di Paola D, Capparucci F, Crupi R, Gugliandolo E, Spanò N, Capillo G, Savoca S (2021) The influence of polystyrene microspheres abundance on development and feeding behavior of Artemia salina (Linnaeus, 1758). Applied Sciences 11(8): b3352. https://doi.org/10.3390/app11083352b

Athey SN, Albotra SD, Gordon CA, Monteleone B, Seaton P, Andrady AL, Taylor AR, Brander SM (2020) Trophic transfer of microplastics in an estuarine food chain and the effects of a sorbed legacy pollutant. Limnology and Oceanography Letters 5: 154–162. https://doi.org/10.1002/lol2.10130

Atici AA (2022) The first evidence of microplastic uptake in natural freshwater mussel, Unio stevenianus from Karasu River, Turkey. Biomarkers 27(2): 118–126. https://doi.org/10.1080/1354750X.2021.2020335

Au SY, Lee CM, Weinstein JE, van den Hurk P, Klaine SJ (2017) Trophic transfer of microplastics in aquatic ecosystems: Identifying critical research needs. Integrated Environmental Assessment and Management 13(3): 505–509. https://doi.org/10.1002/ieam.1907

Browne RA, MacDonald GH (1982) Biogeography of the Brine shrimp, Artemia: Distribution of parthenogenetic and sexual populations. Journal of Biogeography 9: 331. https://doi.org/10.2307/2844719

Bulannga RB, Schmidt S (2022) Uptake and accumulation of microplastic particles by two freshwater ciliates isolated from a local river in South Africa. Environmental Research 204(Pt B): 112123. https://doi.org/10.1016/j.envres.2021.112123

Burns CW (1968) The relationship between body size of filter‐feeding Cladocera and the maximum size of particle ingested. Limnology and Oceanography 13: 675–678. https://doi.org/10.4319/lo.1968.13.4.0675

Capone A, Petrillo M, Misic C (2022) Ingestion and elimination of anthropogenic fibres and microplastic fragments by the European anchovy (Engraulis encrasicolus) of the NW Mediterranean Sea. Marine Biology 167: 166. https://doi.org/10.1007/s00227-020-03779-7

Chae Y, Kim D, Kim SW, An YJ (2018) Trophic transfer and individual impact of nano-sized polystyrene in a four-species freshwater food chain. Scientific Reports 8(1): 284. https://doi.org/10.1038/s41598-017-18849-y

Chae Y, Kim D, An YJ (2019) Effects of micro-sized polyethylene spheres on the marine microalga Dunaliella salina: focusing on the algal cell to plastic particle size ratio. Aquatic Toxicology 216: 105296. https://doi.org/10.1016/j.aquatox.2019.105296

Claus C, Benijts F, Vandeputte G, Gardner W (1979) The biochemical composition of the larvae of two strains of Artemia salina (L.) reared on two different algal foods. Journal of Experimental Marine Biology and Ecology 36(2): 171–183. https://doi.org/10.1016/0022-0981(79)90107-2

Cole M, Coppock R, Lindeque PK, Altin D, Reed S, Pond DW, Sørensen L, Galloway TS, Booth AM (2019) Effects of nylon microplastic on feeding, lipid accumulation, and moulting in a coldwater copepod. Environmental Science and Technology 53(12): 7075–7082. https://doi.org/10.1021/acs.est.9b01853

Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger J, Galloway TS (2013) Microplastic ingestion by zooplankton. Environmental Science and Technology 47(12): 6646–6655. https://doi.org/10.1021/es400663f

Cole M, Lindeque P, Fileman E, Halsband C, Galloway T (2015) The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environmental Science and Technology 49(2): 1130−1137. https://doi.org/10.1021/es504525u

Cui X, Yang T, Li Z, Nowack B (2024) Meta-analysis of the hazards of microplastics in freshwaters using species sensitivity distributions. Journal of Hazardous Materials 463: 132919. https://doi.org/10.1016/j.jhazmat.2023.132919

da Silva JVF, Lansac-Tôha FM, Segovia BT, Amadeo FE, Braghin LSM, Velho LFM, Sarmento H, Bonecker CC (2022) Experimental evaluation of microplastic consumption by using a size-fractionation approach in the planktonic communities. Science of the Total Environment 821: 153045. https://doi.org/10.1016/j.scitotenv.2022.153045

Desforges JP, Galbraith M, Ross PS (2015) Ingestion of microplastics by zooplankton in the Northeast Pacific Ocean. Archives of Environmental Contamination and Toxicology 69(3): 320–30. https://doi.org/10.1007/s00244-015-0172-5

Dyomin V, Morgalev Y, Morgalev S, Morgaleva T, Davydova A, Polovtsev I, Kirillov N, Olshukov A, Kondratova O (2023) Features of phototropic response of zooplankton to paired photostimulation under adverse environmental conditions. Environmental Monitoring and Assessment 195(4): 503. https://doi.org/10.1007/s10661-023-11102-2

Foley CJ, Feiner ZS, Malinich TD, Höök TO (2018) A meta-analysis of the efects of exposure to microplastics on fsh and aquatic invertebrates. Science of The Total Environment 631–632: 550–559. https://doi.org/10.1016/j.scitotenv.2018.03.046

Frank Y, Ershova A, Batasheva S, Vorobiev E, Rakhmatullina S, Vorobiev D, Fakhrullin R (2022) Microplastics in freshwater: A focus on the Russian inland waters. Water 14(23): 3909. https://doi.org/10.3390/w14233909

Frank YA, Interesova EA, Solovyev MM, Xu J, Vorobiev DS (2023b) Effect of microplastics on the activity of digestive and oxidative-stress-related enzymes in Peled Whitefish (Coregonus peled Gmelin) larvae. International Journal of Molecular Science 24: 10998. https://doi.org/10.3390/ijms241310998

Frank YA, Vorobiev DS, Kayler OA, Vorobiev ED, Kulinicheva KS, Trifonov AA, Soliman Hunter T (2021a) Evidence for microplastics contamination of the remote tributary of the Yenisei River, Siberia. The pilot study results. Water 13: 3248. https://doi.org/10.3390/w13223248

Frank YA, Vorobiev ED, Vorobiev DS, Trifonov AA, Antsiferov DV, Soliman Hunter T, Wilson SP, Strezov V (2021b) Preliminary screening for microplastic concentrations in the surface water of rivers Ob and Tom in Siberia, Russia. Sustainability 13(1): 80. https://doi.org/10.3390/su13010080

Grigorakis S, Mason SA, Drouillard KG (2017) Determination of the gut retention of plastic microbeads and microfibers in goldfish (Carassius auratus). Chemosphere 169: 233– 238. https://doi.org/10.1016/j.chemosphere.2016.11.055

Hanslik L, Sommer C, Huppertsberg S, Dittmar S, Knepper TP, Braunbeck T (2020) Microplastic-associated trophic transfer of benzo(k)fluoranthene in a limnic food web: Effects in two freshwater invertebrates (Daphnia magna, Chironomus riparius) and zebrafish (Danio rerio). Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 237: 108849. https://doi.org/10.1016/j.cbpc.2020.108849

Hitchcock JN (2022) Microplastics can alter phytoplankton community composition. Science of The Total Environment 819: 153074. https://doi.org/10.1016/j.scitotenv.2022.153074

Hoellein T, Rovegno C, Uhrin AV, Johnson E, Herring C (2021) Microplastics in invasive freshwater mussels (Dreissena sp.): Spatiotemporal variation and occurrence with chemical contaminants. Frontiers in Marine Science 8: 690401. https://doi.org/10.3389/fmars.2021.690401

Hou L, MaNeish R, Hoellein TJ (2023) Egestion rates of microplastic fibres in fish scaled to in situ concentration and fish density. Freshwater Biology 68(1): 33–45. https://doi.org/10.1111/fwb.14007

Huang W, Song B, Liang J, Niu Q, Zeng G, Shen M, Deng J, Luo Y, Wen X, Zhang Y (2021) Microplastics and associated contaminants in the aquatic environment: A review on their ecotoxicological effects, trophic transfer, and potential impacts to human health. Journal of Hazardous Materials 405: 124187. https://doi.org/10.1016/j.jhazmat.2020.124187

Il’ina OV, Kolobov MY, Il’inskii VV (2021) Plastic pollution of the coastal surface water in the Middle and Southern Baikal. Water Resources 48: 56–64. https://doi.org/10.1134/S0097807821010188

Interesova EA, Babkina IB, Suslyaev VV, Blokhin AN, Reshetnikova SN, Babkin AM, Kolesov AN (2018) Sterlet Acipenser ruthenus L. in the middle Ob basin (within the Tomsk region). Distribution, fishing dynamics, age and growth. Vestnik Rybokhozyaistvennoi Nauki 5(2): 60–71. [In Russian]

Jeyavani J, Sibiya A, Bhavaniramya S, Mahboob S, Al-Ghanim KA, Nisa ZU, Riaz MN, Nicoletti M, Govindarajan M, Vaseeharan B (2022) Toxicity evaluation of polypropylene microplastic on marine microcrustacean Artemia salina: An analysis of implications and vulnerability. Chemosphere 296: 133990. https://doi.org/10.1016/j.chemosphere.2022.133990

Jovanović B (2017) Ingestion of microplastics by fish and its potential consequences from a physical perspective. Integrated Environmental Assessment and Management 13(3): 510–515. https://doi.org/10.1002/ieam.1913

Kim JH, Yu YB, Choi JH (2021) Toxic effects on bioaccumulation, hematological parameters, oxidative stress, immune responses and neurotoxicity in fish exposed to microplastics: A review. Journal of Hazardous Materials 413: 125423. https://doi.org/10.1016/j.jhazmat.2021.125423

Krokhalevsky VR, Babkina IB, Vizer AM, Dorogin MA, Zhirkov FN, Zaitsev VF, Interesova EA, Karpova LN, Peterfeld VA, Yankova NV (2018) The state of sturgeon fish stocks in Siberian water bodies. Voprosy Rybolovstva 19(3): 269–284. [In Russian]

Li C, Busquets R, Campos LC (2020) Assessment of microplastics in freshwater systems: a review. Science of The Total Environment 707: 135578. https://doi.org/10.1016/j.scitotenv.2019.135578

Lu Y, Zhang Y, Deng Y, Jiang W, Zhao Y, Geng J, Ding L, Ren H (2016) Uptake and accumulation of polystyrene microplastics in Zebrafish (Danio rerio) and toxic effects in liver. Environmental Science & Technology 50: 4054–4060. https://doi.org/10.1021/acs.est.6b00183

Malygina N, Mitrofanova E, Kuryatnikova N, Biryukov R, Zolotov D, Pershin D, Chernykh D (2021) Microplastic pollution in the surface waters from plain and mountainous lakes in Siberia, Russia. Water 13(16): 2287. https://doi.org/10.3390/w13162287

McGoran AR, Clark PF, Morritt D (2017) Presence of microplastic in the digestive tracts of European flounder, Platichthys flesus, and European smelt, Osmerus eperlanus, from the River Thames. Environmental Pollution 220: 744–751. https://doi.org/10.1016/j.envpol.2016.09.078

Morgalev Y, Dyomin V, Morgalev S, Davydova A, Morgaleva T, Kondratova O, Polovtsev I, Kirillov N, Olshukov A (2022) Environmental contamination with micro- and nanoplastics changes the phototaxis of euryhaline zooplankton to paired photostimulation. Water 14(23): 3918. https://doi.org/10.3390/w14233918

Moyo S (2022) An enigma: A meta-analysis reveals the effect of ubiquitous microplastics on different taxa in aquatic systems. Frontiers in Environmental Science 10: 999349. https://doi.org/10.3389/fenvs.2022.999349

O'Connor JD, Lally HT, Koelmans AA, Mahon AM, O'Connor I, Nash R, O'Sullivan JJ, Bruen M, Heerey L, Murphy S (2022) Modelling the transfer and accumulation of microplastics in a riverine freshwater food web. Environmental Advances 8: 100192. https://doi.org/10.1016/j.envadv.2022.100192

Orlov AM, Interesova EA, Dyldin YuV, Romanov VI (2022) The endangered Eurasian freshwater Sturgeons. In: DellaSala DA, Goldstein MI (Eds) Imperiled: The Encyclopedia of Conservation. Elsevier, Amsterdam, 541–553. https://doi.org/10.1016/B978-0-12-821139-7.00135-5

Pan Ch-G, Mintenig SM, Redondo-Hasselerharm PE, Neijenhuis PHMW, Yu, Ke-F, Wang Y-H, Koelmans AA (2021) Automated μFTIR imaging demonstrates taxon-specific and selective uptake of microplastic by freshwater invertebrates. Environmental Science and Technology 55(14): 9916–9925. https://doi.org/10.1021/acs.est.1c03119

Piper J (2018) Artemia: A model specimen for educational microscopy projects in biological and ecological fields. Microscopy Today 26(4): 12–19. https://doi.org/10.1017/S1551929518000652

Popov PA (2007) Fishes of Siberia: distribution, ecology, catch. Publishing house of Novosibirsk State University, Novosibirsk, 526 pp. [In Russian]

Provencher JF, Ammendolia J, Rochman CM, Mallory ML (2019) Assessing plastic debris in aquatic food webs: what we know and don’t know about uptake and trophic transfer. Environmental reviews 27(3): 304–317. https://doi.org/10.1139/er-2018-0079

Richon C, Gorgues T, Paul-Pont I, Maes C (2022) Zooplankton exposure to microplastics at global scale: Influence of vertical distribution and seasonality. Frontiers in Marine Science 9: 947309. https://doi.org/10.3389/fmars.2022.947309

Roch S, Friedrich C, Brinker A (2020) Uptake routes of microplastics in fishes: practical and theoretical approaches to test existing theories. Scientific Reports 10: 3896. https://doi.org/10.1038/s41598-020-60630-1

Roch S, Ros AFH, Friedrich C, Brinker A (2021) Microplastic evacuation in fish is particle size-dependent. Freshwater Biology 66: 926–935. https://doi.org/10.1111/fwb.13687

Roch S, Walter T, Ittner LD, Friedrich C, Brinker A (2019) A systematic study of the microplastic burden in freshwater fishes of south-western Germany – Are we searching at the right scale? Science of the Total Environment 689: 1001–1011. https://doi.org/10.1016/j.scitotenv.2019.06.404

Rochman CM, Hoh E, Kurobe T, Teh SJ (2013) Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Scientific Reports 3: 3263. https://doi.org/10.1038/srep03263

Schell T, Rico A, Vighi M (2020) Occurrence, fate and fluxes of plastics and microplastics in terrestrial and freshwater ecosystems. Reviews of Environmental Contamination and Toxicology 250: 1–43. https://doi.org/10.1007/398_2019_40

Scherer C, Brennholt N, Reifferscheid G, Wagner M (2017) Feeding type and development drive the ingestion of microplastics by freshwater invertebrates. Scientific Reports 7(1): 17006. https://doi.org/10.1038/s41598-017-17191-7

Serrão C, Marques-Santos LF (2023) The genus Artemia, the nanoplastics, the microplastics, and their toxic effects: a review. Environmental Science and Pollution Research 30(35): 83025–83050. https://doi.org/10.1007/s11356-023-27868-4

Setälä O, Fleming-Lehtinen V, Lehtiniemi M (2014) Ingestion and transfer of microplastics in the planktonic food web. Environmental Pollution 185: 77–83. https://doi.org/10.1016/j.envpol.2013.10.013

Talbot R, Chang H (2022) Microplastics in freshwater: A global review of factors affecting spatial and temporal variations. Environmental Pollution 292(Pt B): 118393. https://doi.org/10.1016/j.envpol.2021.118393

Triebskorn R, Braunbeck T, Grummt T, Hanslik L, Huppertsberg S, Jekel M, Knepper TP, Krais S, Müller Y, Pittroff M, Ruhl AS, Schmieg H, Schür C, Stobel C, Wagner M, Zumbülte N, Köhler H (2019) Relevance of nano- and microplastics for freshwater ecosystems: a critical review. Trends in Analytical Chemistry 110: 375–392. https://doi.org/10.1016/j.trac.2018.11.023

van Emmerik T, Mellink Y, Hauk R, Waldschläger K, Schreyers L (2022) Rivers as plastic reservoirs. Frontiers in Water 3: 786936. https://doi.org/10.3389/frwa.2021.786936

Vorobiev DS, Frank YA, Rakhmatullina SN, Vorobiev ED, Poskrebysheva YR, Oladele O, Trifonov AA (2024) Microplastic ingestion by fish with different feeding habits in the Ob and Yenisei Rivers. Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya [Tomsk State University Journal of Biology] 66: 252–266. https://doi.org/10.17223/19988591/66/13

Wang W, Gao H, Jin S, Li R, Na G (2019) The ecotoxicological effects of microplastics on aquatic food web, from primary producer to human: A review. Ecotoxicology and environmental safety 173: 110–117. https://doi.org/10.1016/j.ecoenv.2019.01.113

Wang J, Bucci K, Helm PA, Hoellein T, Hoffman MJ, Rooney R, Rochman CM (2022) Runoff and discharge pathways of microplastics into freshwater ecosystems: A systematic review and meta-analysis. FACETS 7: 1473–1492. https://doi.org/10.1139/facets-2022-0140

Wang S, Zhang C, Pan Z, Sun D, Zhou A, Xie S, Wang J, Zou J (2020) Microplastics in wild freshwater fish of different feeding habits from Beijiang and Pearl River Delta regions, south China. Chemosphere 258: 127345. https://doi.org/10.1016/j.chemosphere.2020.127345

Wang Y, Zhang D, Zhang M, Mu J, Ding G, Mao Z, Cao Y, Jin F, Cong Y, Wang L, Zhang W, Wang J (2019) Effects of ingested polystyrene microplastics on brine shrimp, Artemia parthenogenetica. Environmental Pollution 244: 715–722. https://doi.org/10.1016/j.envpol.2018.10.024

Wong JKH, Lee KK, Tang KHD, Yap PS (2020) Microplastics in the freshwater and terrestrial environments: Prevalence, fates, impacts and sustainable solutions. Science of the Total Environment 719: 137512. https://doi.org/10.1016/j.scitotenv.2020.137512

Yıldız D, Yalçın G, Jovanović B, Boukal DS, Vebrová L, Riha D, Stanković J, Savić-Zdraković D, Metin M, Akyürek YN, Balkanlı D, Filiz N, Milošević D, Feuchtmayr H, Richardson JA, Beklioğlu M (2022) Effects of a microplastic mixture differ across trophic levels and taxa in a freshwater food web: In situ mesocosm experiment. Science of the Total Environment 836: 155407. https://doi.org/10.1016/j.scitotenv.2022.155407

Zeytin S, Wagner G, Mackay-Roberts N, Gerdts G, Schuirmann E, Klockmann S, Slater M (2020) Quantifying microplastic translocation from feed to the fillet in European sea bass Dicentrarchus labrax. Marine Pollution Bulletin 156: 111210. https://doi.org/10.1016/j.marpolbul.2020.111210

Zhang C, Chen X, Wang J, Tan L (2017) Toxic effects of microplastic on marine microalgae Skeletonema costatum: Interactions between microplastic and algae. Environmental pollution 220: 1282–1288. https://doi.org/10.1016/j.envpol.2016.11.005

Zhang T, Jiang B, Xing Y, Ya H, Lv M, Wang X (2022) Current status of microplastics pollution in the aquatic environment, interaction with other pollutants, and effects on aquatic organisms. Environmental Science and Pollution Research 29(12): 16830–16859. https://doi.org/10.1007/s11356-022-18504-8

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