[en] Anthropogenic particles (APs), including microplastics, are ingested by a wide variety of marine organisms. Exposure of Clupeiformes (e.g. herrings, anchovies, sardines) is poorly studied despite their economic and ecological importance. This study aims to describe the morphology of the filtration apparatus of three wild-caught Clupeiformes (Sardina pilchardus, Clupea harengus and Engraulis encrasicolus) and to relate the results to ingested APs. Consequently, the species with the more efficient filtration apparatus will be more likely to ingest APs. We hypothesized that sardines were the most exposed species. The filtration area and particle retention threshold were determined in the three species, with sardines displaying the highest filtration area and the closest gill rakers. Sardines ingested more fibers and smaller fragments, confirming that it is the most efficient filtering species. These two results lead to the conclusion that, among the three studied, the sardine is the species most exposed to APs.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Alexandrino, P., Faria, R., Linhares, D., Castro, F., Le Corre, M., Sabatié, R., Baglinière, J.L., Weiss, S., Interspecific differentiation and intraspecific substructure in two closely related clupeids with extensive hybridization, Alosa alosa and Alosa fallax. J. Fish Biol. 69 (2006), 242–259, 10.1111/j.1095-8649.2006.01289.x.
Alsafy, M.A.M., Gill morphology in two Mediterranean Sea fishes of similar feeding preferences: sea bream (Sparus aurata L.) and sea bass (Dicentrarchus labrax). Vet. Res. Commun. 37 (2013), 163–170.
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. Environ. Pollut. 198C (2015), 211–222, 10.1016/j.envpol.2014.12.021.
Batty, R.S., Blaxter, J.H.S., Libby, D.A., Herring (Clupea harengus) filter-feeding in the dark. Mar. Biol. 91 (1986), 371–375.
Batty, R.S., Blaxter, J.H.S., Richard, J.M., Light intensity and the feeding behaviour of herring, Clupea harengus. Mar. Biol. 107 (1990), 383–388, 10.1007/BF01313419.
Besseling, E., Wegner, A., Foekema, E.M., Van Den Heuvel-Greve, M.J., Koelmans, A.A., Effects of microplastic on fitness and PCB bioaccumulation by the lugworm Arenicola marina (L.). Environ. Sci. Technol. 47 (2013), 593–600.
Bjorndal, K.A., Bolten, A.B., Lagueux, C.J., Ingestion of marine debris by juvenile sea turtles in coastal Florida habitats. Mar. Pollut. Bull. 28 (1994), 154–158.
Boren, L.J., Morrissey, M., Muller, C.G., Gemmell, N.J., Entanglement of New Zealand fur seals in man-made debris at Kaikoura, New Zealand. Mar. Pollut. Bull. 52 (2006), 442–446, 10.1016/j.marpolbul.2005.12.003.
Brandão, M.L., Braga, K.M., Luque, J.L., Marine debris ingestion by Magellanic penguins, Spheniscus magellanicus (Aves: Sphenisciformes), from the Brazilian coastal zone. Mar. Pollut. Bull. 62 (2011), 2246–2249, 10.1016/j.marpolbul.2011.07.016.
Browne, M.A., Niven, S.J., Galloway, T.S., Rowland, S.J., Thompson, R.C., Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr. Biol. 23 (2013), 2388–2392, 10.1016/j.cub.2013.10.012.
Bugoni, L., Krause, L., Virgı́nia Petry, M., Marine debris and human impacts on sea turtles in southern Brazil. Mar. Pollut. Bull. 42 (2001), 1330–1334, 10.1016/S0025-326X(01)00147-3.
Bulgakova, Y.V., Feeding in the black Sea anchovy: diet composition, feeding behaviour, feeding periodicity and daily rations (abstract). Sci. Mar. 60 (1996), 283–284.
Cedervall, T., Hansson, L.-A., Lard, M., Frohm, B., Linse, S., Food chain transport of nanoparticles affects behaviour and fat metabolism in fish. PLoS One, 7, 2012, e32254, 10.1371/journal.pone.0032254.
Cole, M., Lindeque, P., Halsband, C., Galloway, T.S., Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. 62 (2011), 2588–2597.
Cole, M., Lindeque, P., Fileman, E., Halsband, C., Goodhead, R., Moger, J., Galloway, T.S., Microplastic ingestion by zooplankton. Environ. Sci. Technol. 47 (2013), 6646–6655.
Collard, F., Gilbert, B., Eppe, G., Parmentier, E., Das, K., Detection of anthropogenic particles in fish stomachs: an isolation method adapted to identification by Raman spectroscopy. Arch. Environ. Contam. Toxicol. 69 (2015), 331–339, 10.1007/s00244-015-0221-0.
Costalago, D., Palomera, I., Feeding of European pilchard (Sardina pilchardus) in the northwestern Mediterranean: from late larvae to adults. Sci. Mar. 78 (2014), 41–54, 10.3989/scimar.03898.06D.
Costalago, D., Garrido, S., Palomera, I., Comparison of the feeding apparatus and diet of European sardines Sardina pilchardus of Atlantic and Mediterranean waters: ecological implications. J. Fish Biol. 86 (2015), 1348–1362, 10.1111/jfb.12645.
Cózar, A., Sanz-Martín, M., Martí, E., González-Gordillo, J.I., Ubeda, B.A., Gálvez, J., Irigoien, X., Duarte, C.M., Plastic accumulation in the mediterranean sea 10. PLoS ONE, 2015, 10.1371/journal.pone.0121762.
da Silva Mendes, S., de Carvalho, R.H., de Faria, A.F., de Sousa, B.M., Marine debris ingestion by Chelonia mydas (Testudines: Cheloniidae) on the Brazilian coast. Mar. Pollut. Bull. 92 (2015), 8–10, 10.1016/j.marpolbul.2015.01.010.
Dibattista, J.D., Randall, J.E., Bowen, B.W., Review of the Round Herrings of the Genus Etrumeus (Clupeidae: Dussumieriinae) of Africa, with Descriptions of Two New Species. 2012 (Cybium).
Elsheikh, E.H., Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes. J. Basic Appl. Zool. 66 (2013), 121–130, 10.1016/j.jobaz.2013.07.005.
FAO, The State of World Fisheries and Aquaculture 2014. 2014 (Rome).
Farrell, P., Nelson, K., Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environ. Pollut. 177 (2013), 1–3, 10.1016/j.envpol.2013.01.046.
Fife, D.T., Robertson, G.J., Shutler, D., Braune, B.M., Mallory, M.L., Trace elements and ingested plastic debris in wintering dovekies (Alle alle). Mar. Pollut. Bull. 91 (2015), 368–371, 10.1016/j.marpolbul.2014.11.029.
Foekema, E.M., De Gruijter, C., Mergia, M.T., van Franeker, J.A., Murk, A.J., Koelmans, A.A., Plastic in north sea fish. Environ. Sci. Technol. 47 (2013), 8818–8824, 10.1021/es400931b.
Garrido, S., Van der Lingen, C.D., Feeding Biology and Ecology. Ganias, K., (eds.) Biology and Ecology of Sardines and Anchovies, 2014, CRC Press, Taylor & Francis Group, 394.
Garrido, S., Marçalo, A., Zwolinski, J., van der Lingen, C., Laboratory investigations on the effect of prey size and concentration on the feeding behaviour of Sardina pilchardus. Mar. Ecol. Prog. Ser. 330 (2007), 189–199, 10.3354/meps330189.
Gerking, S.D., Feeding ecology of fish. Feeding Ecology of Fish, 1994, Elsevier, 10.1016/B978-0-12-280780-0.50013-X.
Gibson, R.N., Development, morphometry and particle retention capability of the gill rakers in the herring, Clupea harengus L. J. Fish Biol. 32 (1988), 949–962, 10.1111/j.1095-8649.1988.tb05438.x.
Gregory, M.R., Environmental implications of plastic debris in marine settings–entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 364 (2009), 2013–2025, 10.1098/rstb.2008.0265.
Gregory, P., Stead, C.V., The Degradation of Water-soluble Azo Compounds by Dilute Sodium Hypochlorite Solution. J. Soc. Dye. Colour. 94 (1978), 402–407, 10.1111/j.1478-4408.1978.tb03426.x.
Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., Microplastics in the marine environment: a review of the methods used for identification and quantification. Environ. Sci. Technol. 46 (2012), 3060–3075.
Iwata, K., Morphological and physiological studies on the phytoplankton feeders in cyprinid fishes, 1: developmental changes of feeding organs and ingestion rates in Kawachibuna (Carassius auratus cuvieri), silver carp (Hypophthalmichthys molitrix) and Nigorobuna C. Japanese J. Limnol. 37 (1976), 135–147.
Jacobsen, J.K., Massey, L., Gulland, F., Fatal ingestion of floating net debris by two sperm whales (Physeter macrocephalus). Mar. Pollut. Bull. 60 (2010), 765–767, 10.1016/j.marpolbul.2010.03.008.
Jakubowski, M., Gill structure and morphometry of its respiratory components in the Baikalian golomyankas (Comephoridae; Cottoidei; Pisces). J. Morphol. 228 (1996), 19–26.
Jambeck, J.R., Geyer, R., Wilcox, C., Siegler, T.R., Perryman, M., Andrady, A., Narayan, R., Law, K.L., Plastic waste inputs from land into the ocean. Science 80:347 (2015), 768–771, 10.1126/science.1260352.
Jiménez, S., Domingo, A., Brazeiro, A., Defeo, O., Phillips, R.A., Marine debris ingestion by albatrosses in the Southwest Atlantic Ocean. Mar. Pollut. Bull. 96 (2015), 149–154, 10.1016/j.marpolbul.2015.05.034.
Kashiwada, S., Distribution of nanoparticles in the see-through Medaka (Oryzias latipes). Environ. Health Perspect. 114 (2006), 1697–1702, 10.1289/ehp.9209.
Klaine, S.J., Koelmans, A.A., Horne, N., Carley, S., Handy, R.D., Kapustka, L., Nowack, B., von der Kammer, F., Paradigms to assess the environmental impact of manufactured nanomaterials. Environ. Toxicol. Chem. 31 (2012), 3–14, 10.1002/etc.733.
Koelmans, A.A., Besseling, E., Shim, W.J., Nanoplastics in the aquatic environment. Critical review. Marine Anthropogenic Litter, 2015, 325–340, 10.1007/978-3-319-16510-3_12.
Lagler, K.F., Bardach, J.E., Miller, R.R., Ichthyology. 1962, John Wiley & Sons, Inc., New York.
Laist, D.W., Impacts of marine debris: entanglement of marine life in marine debris including a comprehensive list of species with entanglement and ingestion records. Coe, J.M., Rogers, D.B., (eds.) Marine Debris: Sources, Impacts, and Solutions, 1997, Springer-Verlag, New York, 99–140.
Lazzaro, X., A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia 146 (1987), 97–167, 10.1007/BF00008764.
Lu, Y., Zhang, Y., Deng, Y., Jiang, W., Zhao, Y., Geng, J., Ding, L., Ren, H., Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ. Sci. Technol. 50 (2016), 4054–4060, 10.1021/acs.est.6b00183.
Lusher, A.L., McHugh, M., Thompson, R.C., Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar. Pollut. Bull. 67 (2013), 94–99.
Magnuson, J.J., Heitz, J.G., Gill raker apparatus and food selectivity among mackerels, tunas, and dolphins. Fish. Bull. 69 (1971), 361–370.
Mattsson, K., Ekvall, M.T., Hansson, L.-A., Linse, S., Malmendal, A., Cedervall, T., Altered behavior, physiology, and metabolism in fish exposed to polystyrene nanoparticles. Environ. Sci. Technol. 49 (2015), 553–561, 10.1021/es5053655.
Misty Paig-Tran, E.W., Summers, A.P., Comparison of the structure and composition of the branchial filters in suspension feeding elasmobranchs. Anat. Rec. (Hoboken) 297 (2014), 701–715, 10.1002/ar.22850.
Neves, D., Sobral, P., Ferreira, J.L., Pereira, T., Ingestion of microplastics by commercial fish off the Portuguese coast. Mar. Pollut. Bull. 101 (2015), 119–126, 10.1016/j.marpolbul.2015.11.008.
Nikolioudakis, N., Isari, S., Pitta, P., Somarakis, S., Diet of sardine Sardina pilchardus: an “end-to-end” field study. Mar. Ecol. Prog. Ser. 453 (2012), 173–188, 10.3354/meps09656.
Northcott, M.E., Beveridge, M.C.M., The development and structure of pharyngeal apparatus associated with filter feeding in tilapias (Oreochromis niloticus). J. Zool. (Lond.) 215 (1988), 133–149.
Oliveira, M., Ribeiro, A., Hylland, K., Guilhermino, L., Single and combined effects of microplastics and pyrene on juveniles (0 + group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol. Indic. 34 (2013), 641–647, 10.1016/j.ecolind.2013.06.019.
Pedà, C., Caccamo, L., Fossi, M.C., Gai, F., Andaloro, F., Genovese, L., Perdichizzi, A., Romeo, T., Maricchiolo, G., Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: preliminary results. Environ. Pollut. 212 (2016), 251–256, 10.1016/j.envpol.2016.01.083.
Remy, F., Collard, F., Gilbert, B., Compère, P., Eppe, G., Lepoint, G., When microplastic is not plastic: the ingestion of artificial cellulose fibers by macrofauna living in seagrass macrophytodetritus. Environ. Sci. Technol. 49 (2015), 11158–11166, 10.1021/acs.est.5b02005.
Robinson, T., McMullan, G., Marchant, R., Nigam, P., Remediation of dyes in textile effluent: a critical review on current treatment technologies with a proposed alternative. Bioresour. Technol. 77 (2001), 247–255, 10.1016/S0960-8524(00)00080-8.
Rochman, C.M., Hoh, E., Kurobe, T., Teh, S.J., Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci. Rep., 3, 2013, 10.1038/srep03263http://www.nature.com/srep/2013/131121/srep03263/abs/srep03263.html#supplementary-information.
Rochman, C.M., Kurobe, T., Flores, I., Teh, S.J., Early warning signs of endocrine disruption in adult fish from the ingestion of polyethylene with and without sorbed chemical pollutants from the marine environment. Sci. Total Environ. 493 (2014), 656–661, 10.1016/j.scitotenv.2014.06.051.
Romeo, T., Pietro, B., Pedà, C., Consoli, P., Andaloro, F., Fossi, M.C., First evidence of presence of plastic debris in stomach of large pelagic fish in the Mediterranean Sea. Mar. Pollut. Bull. 95 (2015), 358–361, 10.1016/j.marpolbul.2015.04.048.
Rykaczewski, R.R., Influence of Oceanographic Variability on the Planktonic Prey and Growth of Sardine and Anchovy in the California Current Ecosystem. 2009, University of California, San Diego.
Sanderson, S.L., Chesnutt, C.R., Lobel, P.S., Evidence for ram suspension feeding by the piscivore, Seriola dumerili (Carangidae). Environ. Biol. Fish 46 (1996), 365–373.
Secchi, E.R., Zarzur, S., Plastic debris ingested by a Blainville's beaked whale, Mesoplodon densirostris, washed ashore in Brazil. Aquat. Mamm. 25 (1999), 21–24.
Setälä, O., Fleming-Lehtinen, V., Lehtiniemi, M., Ingestion and transfer of microplastics in the planktonic food web. Environ. Pollut. 185 (2014), 77–83, 10.1016/j.envpol.2013.10.013.
Smith, J.C., Sanderson, S.L., Mucus function and crossflow filtration in a fish with gill rakers removed versus intact. J. Exp. Biol. 210 (2007), 2706–2713, 10.1242/jeb.000703.
Tanaka, H., Aoki, I., Ohshimo, S., Feeding habits and gill raker morphology of three planktivorous pelagic fish species off the coast of northern and western Kyushu in summer. J. Fish Biol. 68 (2006), 1041–1061.
Urano, H., Fukuzaki, S., The mode of action of sodium hypochlorite in the decolorization of azo dye orange II in aqueous solution. Biocontrol Sci. 16 (2011), 123–126, 10.4265/bio.16.123.
Van Cauwenberghe, L., Janssen, C.R., Microplastics in bivalves cultured for human consumption. Environ. Pollut. 193 (2014), 65–70, 10.1016/j.envpol.2014.06.010.
Walker, W.A., Coe, J.M., Survey of marine debris ingestion by odontocete cetaceans. Shomura, R.S., Godfrey, M.L., (eds.) Proceedings of the 2nd International Conference on Marine Debris, 1989, United States Department of Commerce, Honolulu, Hawaii, 747–774.
Wright, S.L., Thompson, R.C., Galloway, T.S., The physical impacts of microplastics on marine organisms: a review. Environ. Pollut. 178 (2013), 483–492.
