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Meteorological and climatic variability influences anthropogenic microparticle content in the stomach of the European anchovy Engraulis encrasicolus

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Abstract

Meteorological and climatic phenomena affect oceanographic characteristics and, consequently, anthropogenic microparticle aggregation. The same phenomena influence the ecology of pelagic fish, but whether there is a connection between meteorological and climatic characteristics and microparticle ingestion remains unknown. In the NW Mediterranean during the springs of 2011–2014, the incidence of contaminated European anchovies (35 ± 17%) and microparticle abundance in the stomach content (0.46 ± 0.25 microparticles ind−1) may have owed to higher concentrations of microparticles due to hydrodynamism. Year 2011 showed a higher fragment contribution (60 ± 17%). The statistical analysis indicated a link between fragment abundance and climatic characteristics, with low North Atlantic Oscillation index values for the previous cold season indicating the transport of water from the polluted Tyrrhenian Sea. Low-density microplastic (polyethylene and polypropylene) was found, a selection due to the pelagic behaviour of anchovy. Fibre abundance remained quite constant throughout the 4-year period, pointing to diffused input not dependent on meteorological forcing. In 2012, anchovies were subjected to bottom-up limitation, due to adverse meteorological forcing (high early spring temperatures, low rainfall). The anchovies mainly ingested fibres through less energy-expensive filter-feeding. Therefore, meteorological and climatic forcing regulates microparticle intake by fish and should be considered for pollution mitigation.

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References

  • Alomar, C. & S. Deudero, 2017. Evidence of microplastic ingestion in the shark Galeus melastomus Rafinesque, 1810 in the continental shelf off the western Mediterranean Sea. Environmental Pollution 223: 223–229.

    CAS  PubMed  Google Scholar 

  • Arthur, C., J. Baker & H. Bamford, 2009. Effects and fate of microplastic marine debris, in: Proceedings of the International Research Workshop on the Occurrence. Tacoma, WA: NOAA Technical Memorandum, NOS-OR&R: 30 pp.

  • Astraldi, M., S. Balopoulos, J. Candela, J. Font, M. Gacic, G. P. Gasparini, B. Manca, A. Theocharis & J. Tintoré, 1999. The role of straits and channels in understanding the characteristics of Mediterranean circulation. Progress in Oceanography 44: 65–108.

    Google Scholar 

  • Baini, M., M. C. Fossi, M. Galli, I. Caliani, T. Campani, M. G. Finoia & C. Panti, 2018. Abundance and characterization of microplastics in the coastal waters of Tuscany (Italy): the application of the MSFD monitoring protocol in the Mediterranean Sea. Marine Pollution Bulletin 133: 543–552.

    CAS  PubMed  Google Scholar 

  • Barrows, A. P. W., S. E. Cathey & C. W. Petersen, 2018. Marine environment microfiber contamination: global patterns and the diversity of microparticle origins. Environmental Pollution 237: 275–284.

    CAS  PubMed  Google Scholar 

  • Bellas, J., J. Martínez-Armental, A. Martínez-Cámara, V. Besada & C. Martínez-Gómez, 2016. Ingestion of microplastics by demersal fish from the Spanish Atlantic and Mediterranean coasts. Marine Pollution Bulletin 109: 55–60.

    CAS  PubMed  Google Scholar 

  • Belzagui, F., C. Gutierrez-Bouzán, A. Alvarez-Sánchez & M. Vilaseca, 2020. Textile microfibers reaching aquatic environments: a new estimation approach. Environmental Pollution 265: 114889.

    CAS  PubMed  Google Scholar 

  • Boerger, C. M., G. L. Lattin, S. L. Moore & C. J. Moore, 2010. Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin 60: 2275–2278.

    CAS  PubMed  Google Scholar 

  • Bolle, H.-J. (ed), 2002. Mediterranean Climate: Variability and Trend. Springer, Berlin, 450.

    Google Scholar 

  • Bonanno, A., M. Barra, G. Basilone, S. Genovese, P. Rumolo, S. Goncharov, S. Popov, B. B. Nardelli, G. Procaccini, S. Aronica, B. Patti, G. Giacalone, R. Ferreri, I. Fontana, G. Tranchida, S. Mangano, M. Pulizzi, A. Gargano, A. di Maria & S. Mazzola, 2016. Environmental processes driving anchovy and sardine distribution in a highly variable environment: the role of the coastal structure and riverine input. Fisheries Oceanography 25: 471–490.

    Google Scholar 

  • Bonanno, A., M. Giannoulaki, M. Barra, G. Basilone, A. Machias, S. Genovese, S. Goncharov, S. Popov, P. Rumolo, M. Di Bitetto, S. Aronica, B. Patti, I. Fontana, G. Giacalone, R. Ferreri, G. Buscaino, S. Somarakis, M.-M. Pyrounaki, S. Tsoukali & S. Mazzola, 2014. Habitat selection response of small pelagic fish in different environments. Two examples from the oligotrophic Mediterranean Sea. PLoS ONE 9(7): e101498.

    PubMed  PubMed Central  Google Scholar 

  • Browne, M. A., P. Crump, S. J. Niven, E. Teuten, A. Tonkin, T. Galloway & R. Thompson, 2011. Accumulation of microplastic on shorelines worldwide: sources and sinks. Environmental Science & Technology 45: 9175–9179.

    CAS  Google Scholar 

  • Capone, A., M. Petrillo & C. Misic, 2020. Ingestion and elimination of anthropogenic fibers and microplastic fragments by the European anchovy (Engraulis encrasicolus) of the NW Mediterranean Sea. Marine Biology 167: 166.

    CAS  Google Scholar 

  • Cedervall, T., L. A. Hansson, M. Lard, B. Frohm & S. Linse, 2012. Food chain transport of nanoparticles affects behaviour and fat metabolism in fish. PLoS ONE 7: e32254.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Claessens, M., S. D. Meester, L. V. Landuyt, K. D. Clerck & C. R. Janssen, 2011. Occurrence and distribution of microplastics inmarine sediments along the Belgian coast. Marine Pollution Bulletin 62: 2199–2204.

    CAS  PubMed  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 2001. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edn. PRIMER-E, Plymouth

  • Collignon, A., J.-H. Hecq, F. Galgani, P. Voisin, F. Collard & A. Goffart, 2012. Neustonic microplastic and zooplankton in the North Western Mediterranean Sea. Marine Pollution Bulletin 64: 861–864.

    CAS  PubMed  Google Scholar 

  • Compa, M., A. Ventero, M. Iglesias & S. Deudero, 2018. Ingestion of microplastics and natural fibres in Sardina pilchardus (Walbaum, 1972) and Engraulis encrasicolus (Linnaeus, 1758) along the Spanish Meiterranean coast. Marine Pollution Bulletin 128: 89–96.

    CAS  PubMed  Google Scholar 

  • Davison, P. & R. G. Asch, 2011. Plastic ingestion by mesopelagic fishes in the North Pacific Subtropical Gyre. Marine Ecology – Progress Series 432: 173–180.

    Google Scholar 

  • de Sá, L. C., L. G. Lús & L. Guilhermino, 2015. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environmental Pollution 196: 359–362.

    Google Scholar 

  • Deudero, S. & C. Alomar, 2015. Mediterranean marine biodiversity under threat: Reviewing influence of marine litter on species. Marine Pollution Bulletin 98: 58–68.

    CAS  PubMed  Google Scholar 

  • Drinkwater, K. F., A. Belgrano, A., Borja, A. Conversi, M. Edwards, C. H. Greene, G. Ottersen, A. J. Pershing & H. Walker, 2003. The response of marine ecosystems to climate variability associated with the North Atlantic Oscillation. In Hurrell, J. W., Y. Kushnir, G. Ottersen & M. Visbeck (eds), The North Atlantic Oscillation. Climatic Significance and Environmental Impact. Geophysical Monograph. American Geophysical Union, Washington DC, 134 pp.

  • Enders, K., R. Lenz, C. A. Stedmon & T. G. Nielsen, 2015. Abundance, size and polymer composition of marine microplastics ≥10 μm in the Atlantic Ocean and their modelled vertical distribution. Marine Pollution Bulletin 100(1): 70–81.

    CAS  PubMed  Google Scholar 

  • Enfrin, M., J. Lee, Y. Gibert, F. Basheer, L. Kong & L. F. Dumée, 2020. Release of hazardous nanoplastic contaminants due to microplastics fragmentation under shear stress forces. Journal of Hazardous Materials 384: 121393.

    CAS  PubMed  Google Scholar 

  • Eriksen, M., L. C. M. Lebreton, H. S. Carson, M. Thiel, C. J. Moore, J. C. Borerro, F. Galgani, P. G. Ryan & J. Reisser, 2014. Plastic Pollution in the World’s Oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS ONE. https://doi.org/10.1371/journal.pone.0111913.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández de Puelles, M. L., F. Alemany & J. Jansá, 2007. Zooplankton time-series in the Balearic Sea (Western Mediterranean): variability during the decade 1994–2003. Progress in Oceanography 74: 329–354.

    Google Scholar 

  • Fernández de Puelles, M. L. & J. C. Molinero, 2007. North Atlantic climate control on plankton variability in the Balearic Sea, western Mediterranean. Geophysical Research Letters 34: L04608. https://doi.org/10.1029/2006GL028354.

    Article  Google Scholar 

  • Ferreira, G. V. B., M. Barletta, A. R. A. Lima, S. A. Morley & M. F. Costa, 2019. Dynamics of marine debris ingestion by profitable fishes along the estuarine ecocline. Scientific Reports 9: 13514.

    PubMed  PubMed Central  Google Scholar 

  • Fossi, M. C., C. Panti, C. Guerranti, D. Coppola, M. Giannetti, L. Marsili & R. Minutoli, 2012. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Marine Pollution Bulletin 64: 2374–2379.

    CAS  PubMed  Google Scholar 

  • Froese, B. R., 2006. Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology 22: 241–253.

    Google Scholar 

  • Gago, J., O. Carretero, A. V. Filgueiras & L. Viñas, 2018. Synthetic microfibers in the marine environment: a review on their occurrence in seawater and sediments. Marine Pollution Bulletin 127: 365–376.

    CAS  PubMed  Google Scholar 

  • Hartline, N. L., N. J. Bruce, S. N. Karba, E. O. Ruff, S. U. Sonar & P. A. Holden, 2016. Microfiber masses recovered from conventional machine washing of new or aged garments. Environmental Science & Technology 50: 11532–11538.

    CAS  Google Scholar 

  • James, A. G., T. Probyn & J. Seiderer, 1989. The relationship between respiration rate, swimming speed and feeding behaviour in the cape anchovy Engraulis capensis Gilchris. Journal of Experimental Marine Biology and Ecology 131: 81–100.

    Google Scholar 

  • Jiang, Y., F. Yang, Y. Zhao & J. Wang, 2020. Greenland Sea Gyre increases microplastic pollution in the surface waters of the Nordic Seas. Science of the Total Environment 712: 136484.

    CAS  Google Scholar 

  • Jovanović, B., 2017. Potential consequences of fish ingestion of microplastic. Integrated Environmental Assessment and Management 13: 510–515.

    PubMed  Google Scholar 

  • Kanhai, L. D. K., K. Gårdfeldt, O. Lyashevska, M. Hassellov, R. C. Thompson & I. O’Connor, 2018. Microplastics in sub-surface waters of the Arctic Central Basin. Marine Pollution Bulletin 130: 8–18.

    CAS  PubMed  Google Scholar 

  • Lacroix, G. J., N. P. Nezlin & S. Djenidi, 2001. Ecosystem response to the atmospheric forcing in the Southern Ligurian Sea in 1997–1999. Rapp. Comm. Int. Mer Medit. 36: 72.

    Google Scholar 

  • Ladewig, S. M., S. Bao & A. T. Chow, 2015. Natural fibers: a missing link to chemical pollution dispersion in aquatic environments. Environmental Science & Technology 49: 12609–12610.

    CAS  Google Scholar 

  • Lebreton, L. C. M., J. van der Zwet, J.-W. Damsteeg, B. Slat, A. L. Andrady & J. Reisser, 2017. River plastic emissions to the world’s oceans. Nature Communications 8: 15611.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lima, A. R. A., M. F. Costa & M. Barletta, 2014. Distribution patterns of microplastics within the plankton of a tropical estuary. Environmental Research 132: 146–155.

    CAS  PubMed  Google Scholar 

  • Lima, A. R. A., M. D. Silva, F. E. Possatto, G. V. B. Ferreira & A. P. Krelling, 2020. Plastic contamination in Brazilian Freshwater and coastal environments: a source-to-Sea transboundary approach. In Handbook of Environmental Chemistry: 1–12. Springer, Cham. https://doi.org/10.1007/698_2020_514.

  • Lima, A. R. A., G. V. B. Ferreira, A. P. W. Barrows, K. S. Christiansen, G. Treinish & M. C. Toshack, 2021. Global patterns for the spatial distribution of floating microfibers: Arctic Ocean as a potential accumulation zone. Journal of Hazardous Materials 403: 123796.

    CAS  PubMed  Google Scholar 

  • Lleonart, J. & F. Maynou, 2003. Fish stock assessments in the Mediterranean: state of the art. Scientia Marina 67(Suppl. 1): 37–49.

    Google Scholar 

  • Lusher, A. L., M. McHugh & R. C. Thompson, 2013. Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Marine Pollution Bulletin 67: 94–99.

    CAS  PubMed  Google Scholar 

  • Lusher, A. L., V. Tirelli, I. O’Connor & R. Officer, 2015. Microplastics in Arctic polar waters: the first reported values of particles in surface and sub-surface samples. Scientific Reports 5: 1–9.

    Google Scholar 

  • Marshall, J., Y. Kushnir, D. S. Battisti, P. Chang, J. Hurrell, M. McCartney, R. Saravanan & M. Visbeck, 2002. North Atlantic climate variability: phenomena, impacts and mechanisms. International Journal of Climatology 15: 1863–1898.

    Google Scholar 

  • Misic, C., M. Castellano & A. Covazzi Harriague, 2011. Organic matter features, degradation and remineralisation at two coastal sites in the Ligurian Sea (NW Mediterranean) differently influenced by anthropogenic forcing. Marine Environmental Research 72: 6–74.

    Google Scholar 

  • Nadal, M. A., C. Alomar & S. Deudero, 2016. High levels of microplastic ingestion by the semipelagic fish bogue Boops boops (L.) around the Balearic Islands. Environmental Pollution 214: 517–523.

    CAS  PubMed  Google Scholar 

  • Neves, D., P. Sobral, J. L. Ferreira & T. Pereira, 2015. Ingestion of microplastics by commercial fish off the Portuguese coast. Marine Pollution Bulletin 101: 119–126.

    CAS  PubMed  Google Scholar 

  • Pedá, C., L. Caccamo, M. C. Fossi, F. Gai Andaloro, L. Genovese, A. Perdichizzi, T. Romeo & G. Maricchiolo, 2016. Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus 1758) exposed to microplastics: preliminary results. Environmental Pollution 212: 251–256.

    PubMed  Google Scholar 

  • Pesce, M., A. Critto, S. Torresan, E. Giubilato, M. Santini, A. Zirino, W. Ouyang & A. Marcomini, 2018. Modelling climate change impacts on nutrients and primary production in coastal waters. Science of the Total Environment 628–629: 919–937.

    Google Scholar 

  • Politikos, D. V., G. Triantafyllou, G. Petihakis, K. Tsiaras, S. Somarakis, S.-I. Ito & B. A. Megrey, 2011. Application of a bioenergetics growth model for European anchovy (Engraulis encrasicolus) linked with a lower trophic level ecosystem model. Hydrobiologia 670: 141–163.

    Google Scholar 

  • Remy, F., F. Collard, B. Gilbert, P. Compère, G. Eppe & G. Lepoint, 2015. When microplastic is not plastic: the ingestion of artificial cellulose fibers by macrofauna living in seagrass macrophytodetritus. Environmental Science & Technology 49: 11158–11166.

    CAS  Google Scholar 

  • Rios-Fuster, B., C. Alomar, M. Compa, B. Guijarro & S. Deudero, 2019. Anthropogenic particles ingestion in fish species from two areas of the western Mediterranean Sea. Marine Pollution Bulletin 144: 325–333.

    CAS  PubMed  Google Scholar 

  • Rumolo, P., A. Bonanno, M. Barra, E. Fanelli, M. Calabrò, S. Genovese, R. Ferreri, S. Mazzola & G. Basilone, 2016. Spatial variations in feeding habits and trophic levels of two small pelagic fish species in the central Mediterranean Sea. Marine Environmental Research 115: 65–77.

    CAS  PubMed  Google Scholar 

  • Setälä, O., M., Lehtiniemi, R., Coppock, M. Cole, 2018. Microplastics in marine food webs. Microplastic Contam. Aquat. Environ. 339–363. https://doi.org/10.1016/B978-0-12-813747-5.00011-4

  • Van Sebille, E., C. Wilcox, L. Lebreton, N. Maximenko, B. D. Hardesty, J. A. van Franeker, M. Eriksen, D. Siegel, F. Galgani & K. L. Law, 2015. A global inventory of small floating plastic debris. Environmental Research Letters 10: 124006.

    Google Scholar 

  • Sillanpää, M. & P. Sainio, 2017. Release of polyester and cotton fibers from textiles in machine washings. Environmental Science and Pollution Research International 24: 19313–19321.

    PubMed  Google Scholar 

  • Suaria, G., C. G. Avio, A. Mineo, G. L. Lattin, M. G. Magaldi, G. Belmonte, C. J. Moore, F. Regoli & S. Aliani, 2016. The Mediterranean Plastic Soup: synthetic polymers in Mediterranean surface waters. Scientific Reports 6(1): 37551.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka, K. & H. Takada, 2016. Microplastic fragments and microbeads in digestive tracts of planktivorous fish from urban coastal waters. Scientific Reports 6: 34351.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turner, A., 2019. Trace elements in laundry dryer lint: A proxy for household contamination and discharges to waste water. Science of the Total Environment 665: 568–573.

    CAS  Google Scholar 

  • Vignudelli, S., G. P. Gasparini, M. Astraldi & M. E. Schiano, 1999. A possible influence of the North Atlantic Oscillation on the circulation of the Western Mediterranean Sea. Geophysical Research Letters 26: 623–626.

    Google Scholar 

  • Yu, F., C. Yang, Z. Zhu, X. Bai & J. Ma, 2019. Adsorption behavior of organic pollutants and metals on micro/nanoplastics in the aquatic environment. Science of the Total Environment 694: 133643.

    CAS  Google Scholar 

  • Zhu, L., H. Bai, B. Chen, X. Sun, K. Qu & B. Xia, 2018. Microplastic pollution in North Yellow Sea, China: observations on occurrence, distribution and identification. Science of the Total Environment 636: 20–29.

    CAS  Google Scholar 

  • Zuur, A. F., E. N. Ieno & G. M. Smith, 2007. Analysing Ecological Data, Springer, New York:

    Google Scholar 

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Acknowledgements

We thank L. Viviani for kindly providing the anchovy samples and C. Bottinelli and W. Sgroi for the FT-IR analyses. This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

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  1. Department of Earth, Environment and Life Sciences, University of Genova, Corso Europa 26, 16132, Genoa, Italy

    Cristina Misic, Alessandro Capone & Mario Petrillo

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  1. Cristina Misic
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Alessandro Capone and Mario Petrillo. The first draft of the manuscript was written by Cristina Misic and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Misic, C., Capone, A. & Petrillo, M. Meteorological and climatic variability influences anthropogenic microparticle content in the stomach of the European anchovy Engraulis encrasicolus. Hydrobiologia 849, 589–602 (2022). https://doi.org/10.1007/s10750-021-04727-2

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