Ingestion of microplastics by the heterotrophic dinoflagellate Oxyrrhis marina
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Abstract
Incorporation of microplastics (MP) into the microbial food web and its further transport to higher trophic levels have been hitherto poorly studied. In this work, the patterns of MP ingestion by the unicellular heterotrophic dinoflagellate Oxyrrhis marina (OXY) were analyzed. The prymnesiophycean Isochrysis galbana (ISO), 5.6-µm polystyrene microspheres (MS), and their mixture (ISO-MS) were used as food objects for O. marina. Dynamics of the abundance of microorganisms and microspheres was investigated using a flow cytometer. As shown, the heterotroph O. marina ingested MP even in the presence of its natural prey (microalgae), and feeding on MP did not result in a decrease in the dinoflagellate abundance. The grazing rates of “preys” in the OXY-ISO-MS mixture were (0.21 ± 0.01) MS·cell−1·h−1 (± standard deviation) and (0.38 ± 0.01) ISO·cell−1·h−1. These rates were significantly lower than in the mono-diet experiments – with OXY-ISO [(1.93 ± 0.68) ISO·cell−1·h−1] and OXY-MS [(0.45 ± 0.04) MS·cell−1·h−1]. Thus, the expansion of the range of food objects led to a decrease in the grazing rate. In the mono-diet experiments, the clearance rates were (0.12 ± 0.04) and (0.19 ± 0.06) μL·cell−1·h−1 for OXY-ISO and OXY-MS, respectively; thereby, O. marina spent less time on capturing ISO cells than on capturing MS. The same pattern was observed in the experiments with the OXY-ISO-MS mixture: the clearance rate for microalgae [(0.17 ± 0.02) μL·cell−1·h−1] was slightly lower than that for MS [(0.19 ± 0.003) μL·cell−1·h−1]. Since O. marina re-consumed MS even in the presence of its natural food object (I. galbana), no trophic adaptation of the dinoflagellate to MS occurred. No selective grazing of O. marina for any “prey” was revealed, either ISO or MS. The obtained results indicate the possibility (and high probability) of the incorporation of MP into the microbial food web and the significant role of unicellular organisms in the transport of MP to higher trophic levels.
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References
Козловский Н. В., Блиновская Я. Ю. Микропластик – макропроблема Мирового океана // Международный журнал прикладных и фундаментальных исследований. 2015. № 10-1. С. 159–162. [Kozlovskii N. V., Blinovskaia J. Y. Microplastic is World Ocean macroproblem. Mezhdunarodnyi zhurnal prikladnykh i fundamental’nykh issledovanii, 2015, vol. 10-1, pp. 159–162. (in Russ.)]
Ханайченко А. Н., Битюкова Ю. Е. Избирательность питания личинок калкана и выбор стратегии их кормления // Экология моря. 1999. Вып. 48. С. 63–67. [Khanaichenko A. N., Bityukova Y. E. Black Sea turbot larvae feeding selectivity and choice of feeding strategy. Ekologiya morya, 1999, iss. 3, pp. 63–67. (in Russ.)]. URL: https://repository.marine-research.ru/handle/299011/4212
Ateia M., Zheng T., Calace S., Tharayil N., Pilla S., Karanfil T. Sorption behavior of real microplastics (MPs): Insights for organic micropollutants adsorption on a large set of well-characterized MPs. Science of The Total Environment, 2020, vol. 720, art. no. 137634 (7 p.). https://doi.org/10.1016/j.scitotenv.2020.137634
Auta H. S., Emenike C. U., Fauziah S. H. Distribution and importance of microplastics in the marine environment: A review of the sources, fate, effects, and potential solutions. Environment International, 2017, vol. 102, pp. 165–176. https://doi.org/10.1016/j.envint.2017.02.013
Avio C. G., Gorbi S., Milan M., Benedetti M., Fattorini D., d’Errico G., Pauletto M., Bargelloni L., Regoli F. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environmental Pollution, 2015, vol. 198, pp. 211–222. https://doi.org/10.1016/j.envpol.2014.12.021
Barnes D. K. A., Galgani F., Thompson R. C., Barlaz M. Accumulation and fragmentation of plastic debris in global environments. Philosophical Transactions of the Royal Society B, 2009, vol. 364, iss. 1526, pp. 1985–1998. https://doi.org/10.1098/rstb.2008.0205
Batel A., Linti F., Scherer M., Erdinger L., Braunbeck Th. Transfer of benzo[a]pyrene from microplastics to Artemia nauplii and further to zebrafish via a trophic food web experiment: CYP1A induction and visual tracking of persistent organic pollutants. Environmental Toxicology and Chemistry, 2016, vol. 35, iss. 7, pp. 1656–1666. https://doi.org/10.1002/etc.3361
Betts K. Why small plastic particles may pose a big problem in the oceans. Environmental Science and Technology, 2008, vol. 42, iss. 24, pp. 8995. https://doi.org/10.1021/es802970v
Christaki U., Dolan J. R., Pelegri S., Rassoulzadegan F. Consumption of picoplankton-size particles by marine ciliates: Effects of physiological state of the ciliate and particle quality. Limnology and Oceanography, 1998, vol. 43, iss. 3, pp. 458–464. https://doi.org/10.4319/lo.1998.43.3.0458
Cooper D. A., Corcoran P. L. Effects of mechanical and chemical processes on the degradation of plastic beach debris on the island of Kauai, Hawaii. Marine Pollution Bulletin, 2010, vol. 60, iss. 5, pp. 650–654. https://doi.org/10.1016/j.marpolbul.2009.12.026
Cordova M. R., Purwiyanto A. I. S., Suteja Y. Abundance and characteristics of microplastics in the northern coastal waters of Surabaya, Indonesia. Marine Pollution Bulletin, 2019, vol. 142, pp. 183–188. https://doi.org/10.1016/j.marpolbul.2019.03.040
Coutteau P. Micro-Algae. In: Manual on the Production and Use of Live Food for Aquaculture / P. Lavens, P. Sorgeloos (Eds). Rome : FAO, 1996, pp. 7–48. (FAO Fisheries Technical Paper ; no. 361).
Desforges J. W., Galbraith M., Ross P. S. Ingestion of microplastics by zooplankton in the northeast Pacific Ocean. Archives of Environmental Contamination and Toxicology, 2015, vol. 69, iss. 3, pp. 320–330. https://doi.org/10.1007/s00244-015-0172-5
Egbeocha C. O., Malek S., Emenike C. U., Milow P. Feasting on microplastics ingestion by and effects on marine organisms. Aquatic Biology, 2018, vol. 27, pp. 93–106. https://doi.org/10.3354/ab00701
Fendall L. S., Sewell M. A. Contributing to marine pollution by washing your face: Microplastics in facial cleansers. Marine Pollution Bulletin, 2009, vol. 58, iss. 8, pp. 1225–1228. https://doi.org/10.1016/j.marpolbul.2009.04.025
Flynn K. J., Davidson K., Cunningham A. Prey selection and rejection by a microflagellate; implications for the study and operation of microbial food webs. Journal of Experimental Marine Biology and Ecology, 1996, vol. 196, iss. 1–2, pp. 357–372. https://doi.org/10.1016/0022-0981(95)00140-9
Frost B. W. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography, 1972, vol. 17, iss. 6, pp. 805–815. https://doi.org/10.4319/lo.1972.17.6.0805
Hansen P. J. Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Marine Ecology Progress Series, 1991, vol. 73, no. 2/3, pp. 253–261. http://doi.org/10.3354/meps073253
Hansen F. C., Witte H. J., Passarge J. Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: Size selectivity and preference for calcified Emiliania huxleyi cells. Aquatic Microbial Ecology, 1996, vol. 10, iss. 3, pp. 307–313. https://doi.org/10.3354/ame010307
Hammer A., Grüttner C., Schumann R. The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (Dinoflagellate). Protist, 1999, vol. 150, iss. 4, pp. 375–382. https://doi.org/10.1016/s1434-4610(99)70039-8
Hartz A. J. Investigating the Ecological Role of Cell Signaling in Free-living Marine Heterotrophic Protists. PhD thesis / Oregon State University. Oregon, 2010, 182 p.
Ivlev V. S. Experimental Ecology of the Feeding of Fishes. New Haven : Yale University Press, 1961, 302 p.
Koelmans A. A. Modeling the role of microplastics in bioaccumulation of organic chemicals to marine aquatic organisms. A critical review. In: Marine Anthropogenic Litter / M. Bergmann, L. Gutow, M. Klages (Eds). Berlin : Springer, 2015, pp. 309–324. https://doi.org/10.1007/978-3-319-16510-3_11
Kwon B. G., Saido K., Koizumi K., Sato H., Ogawa N., Chung S. Y., Kusui T., Kodera Y., Kogure K. Regional distribution of styrene analogues generated from polystyrene degradation along the coastlines of the North-East Pacific Ocean and Hawaii. Environmental Pollution, 2014, vol. 188, pp. 45–49. https://doi.org/10.1016/j.envpol.2014.01.019
Lyakurwa D. J. Uptake and effects of microplastic particles in selected marine microalgae species; Oxyrrhis marina and Rhodomonas baltica. PhD thesis / Norwegian University of Science and Technology. Trondheim, 2017, 51 p.
Martel C. M. Conceptual bases for prey biorecognition and feeding selectivity in the microplanktonic marine phagotroph Oxyrrhis marina. Microbial Ecology, 2009, vol. 57, iss. 4, pp. 589–597. https://doi.org/10.1007/s00248-008-9421-8
McCormick A. R., Hoellein T. J., London M. G., Hittie J., Scott J. W., Kelly J. J. Microplastic in surface waters of urban rivers: Concentration, sources, and associated bacterial assemblages. Ecosphere, 2016, vol. 7, iss. 11, art. no. e01556 (22 p.). https://doi.org/10.1002/ecs2.1556
Moore C. J. Synthetic polymers in the marine environment: A rapidly increasing, long-term threat. Environmental Research, 2008, vol. 108, iss. 2, pp. 131–139. https://doi.org/10.1016/j.envres.2008.07.025
Ogata Y., Takada H., Mizukawa K., Hirai H., Iwasa S., Endo S., Mato Y., Saha M., Okuda K., Nakashima A., Murakami M., Zurcher N., Booyatumanondo R., Zakaria M. P., Dung L. Q., Gordon M., Miguez C., Suzuki S., Moore Ch., Karapanagioti H. K., Weerts S., McClurg T., Burres E., Smith W., Van Velkenburg M., Lang J. S., Lang R. C., Laursen D., Danner B., Stewardson N., Thompson R. C. International Pellet Watch: Global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Marine Pollution Bulletin, 2009, vol. 58, iss. 10, pp. 1437–1446. https://doi.org/10.1016/j.marpolbul.2009.06.014
Ogonowski M., Schür C., Jarsén A., Gorokhova E. The effects of natural and anthropogenic microparticles on individual fitness in Daphnia magna. PLoS One, 2016, vol. 11, iss. 5, art. no. e0155063 (20 p.). https://doi.org/10.1371/journal.pone.0155063
Procter J., Hopkins F. E., Fileman E. S., Lindeque P. K. Smells good enough to eat: Dimethyl sulfide (DMS) enhances copepod ingestion of microplastics. Marine Pollution Bulletin, 2019, vol. 138, pp. 1–6. https://doi.org/10.1016/j.marpolbul.2018.11.014
Rehse S., Kloas W., Zarfl C. Short-term exposure with high concentrations of pristine microplastic particles leads to immobilisation of Daphnia magna. Chemosphere, 2016, vol. 153, pp. 91–99. https://doi.org/10.1016/j.chemosphere.2016.02.133
Rillig M. C., Bonkowski M. Microplastic and soil protists: A call for research. Environmental Pollution, 2018, vol. 241, pp. 1128–1131. https://doi.org/10.1016/j.envpol.2018.04.147
Roberts E. C., Wootton E. C., Davidson K., Jeong H. J., Lowe C. D., Montagnes D. J. Feeding in the dinoflagellate Oxyrrhis marina: Linking behaviour with mechanisms. Journal of Plankton Research, 2010, vol. 33, iss. 4, pp. 603–614. https://doi.org/10.1093/plankt/fbq118
Støttrup J. G., Richardson K., Kirkegaard E., Pihl N. J. The cultivation of Acartia tonsa Dana for use as a live food source for marine fish larvae. Aquaculture, 1986, vol. 52, iss. 2, pp. 87–96. https://doi.org/10.1016/0044-8486(86)90028-1
Van Cauwenberghe L., Claessens M., Vandegehuchte M. B., Janssen C. R. Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola marina) living in natural habitats. Environmental Pollution, 2015, vol. 199, pp. 10–17. https://doi.org/10.1016/j.envpol.2015.01.008
Watts A. J. R., Lewis C., Goodhead R. M., Beckett S. J., Moger J., Tyler Ch. R., Galloway T. S. Uptake and retention of microplastics by the shore crab Carcinus maenas. Environmental Science and Technology, 2014, vol. 48, iss. 15, pp. 8823–8830. https://doi.org/10.1021/es501090e
Wolfe G. V., Steinke M., Kirst G. O. Grazing-activated chemical defence in a unicellular marine alga. Nature, 1997, vol. 387, pp. 894–897. https://doi.org/10.1038/43168
Wootton E., Zubkov M., Jones D., Jones R., Martel C., Thornton C., Roberts E. Biochemical prey recognition by planktonic protozoa. Environmental Microbiology, 2007, vol. 9, iss. 1, pp. 216–222. https://doi.org/10.1111/j.1462-2920.2006.01130.x
Wright S. L., Thompson R. C., Galloway T. S. The physical impacts of microplastics on marine organisms: A review. Environmental Pollution, 2013, vol. 178, pp. 483–492. https://doi.org/10.1016/j.envpol.2013.02.031
Wu F., Wang Y., Leung J. Y. S., Huang W., Zeng J., Tang Y., Chen J., Shi A., Yu X., Xu X., Zhang H., Cao L. Accumulation of microplastics in typical commercial aquatic species: A case study at a productive aquaculture site in China. Science of the Total Environment, 2020, vol. 708, art. no. 135432 (11 p.). https://doi.org/10.1016/j.scitotenv.2019.135432