High intake rates of microplastics in a Western Atlantic predatory fish, and insights of a direct fishery effect

Environmental Pollution

Volumn 236, Issue , 2018, Pages 706-717

  Ferreira, Guilherme V B ^a   Barletta, Mário ^a   Lima, André R A ^a   Morley, Simon A ^b   Justino, Anne K S ^a   Costa, Monica F ^a  

^a FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^b BRITISH ANTARCTIC SURVEY   (United Kingdom)

Author keywords

Fishery resource; Marine debris; Microplastic filaments; Seafood contamination; Trophic transfer

Indexed keywords

COLOR; CONTAMINATION; ESTUARIES; FISH; FISHERIES; WEATHERING;

ECOLOGICAL INTERACTIONS; ENVIRONMENTAL GRADIENT; FISHERY RESOURCES; FISHING ACTIVITIES; HYDRODYNAMIC FORCES; MARINE DEBRIS; TROPHIC TRANSFER; WESTERN ATLANTIC;

MARINE POLLUTION;

BIOACCUMULATION; FISH; FISHERY PRODUCTION; MARINE POLLUTION; PLASTIC;

ADULT; ARTICLE; CONTAMINATION; ESTUARY; FEEDING; FISHERY; FISHING; GASTROINTESTINAL TRACT; HABITAT; HUMAN; HYDRODYNAMICS; INGESTION; JUVENILE; NONHUMAN; PREDATOR; SEA FOOD; SEASON; SUBADULT; TRANSFERENCE; WEATHERING; ZOOPLANKTON; ANALYSIS; ANIMAL; ATLANTIC OCEAN; EATING; ECOSYSTEM; ENVIRONMENTAL MONITORING; METABOLISM; PERCIFORMES; PROCEDURES; RIVER; STATISTICS AND NUMERICAL DATA; WATER POLLUTANT;

ATLANTIC OCEAN;

CYNOSCION ACOUPA;

PLASTIC; RAIN;

ANIMALS; ATLANTIC OCEAN; EATING; ECOSYSTEM; ENVIRONMENTAL MONITORING; ESTUARIES; FISHERIES; PERCIFORMES; PLASTICS; RAIN; RIVERS; SEASONS; WATER POLLUTANTS, CHEMICAL; ZOOPLANKTON;

EID: 85041931294     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2018.01.095     Document Type: Article

References (80)

1. Acha, E.M., Mianzan, H.W., Iribarne, O., Gagliardini, D.A., Lasta, C., Daleo, P., The role of the Río de la Plata bottom salinity front in accumulating debris. Mar. Pollut. Bull. 46 (2003), 197–202.
2. Arthur, C., Baker, J., Bamford, H., Proceedings of the International Research Workshop on the Occurrence, Effects, and Fate of Microplastic Marine Debris, 2009 Group 530.
3. Au, S.Y., Lee, C.M., Weinstein, J.E., van den Hurk, P., Klaine, S.J., Trophic transfer of microplastics in aquatic ecosystems: identifying critical research needs. Integrated Environ. Assess. Manag. 13 (2017), 505–509, 10.1002/ieam.1907.
4. Barletta, M., Amaral, C.S., Corrêa, M.F.M., Guebert, F., Dantas, D.V., Lorenzi, L., Saint-Paul, U., Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. J. Fish. Biol. 73 (2008), 1314–1336, 10.1111/j.1095-8649.2008.02005.x.
5. Barletta, M., Barletta-Bergan, A., Saint-Paul, U., Description of the fisheries structure in the mangrove-dominated region of Bragança (State of Para, north Brazil). Ecotropica 4 (1998), 41–53.
6. Barletta, M., Costa, M.F., Living and non-living resources exploitation in a tropical semi-arid estuary. J. Coast Res. 2009 (2009), 371–375.
7. Barletta, M., Cysneiros, F.J.A., Lima, A.R.A., Effects of dredging operations on the demersal fish fauna of a South American tropical–subtropical transition estuary. J. Fish. Biol. 89 (2016), 890–920, 10.1111/jfb.12999.
8. Barnes, D.K.A., Biodiversity Invasions by marine life on plastic debris. Nature 416 (2002), 808–809, 10.1038/416808a.
9. Barnes, D.K.A., Milner, P., Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean. Mar. Biol. 146 (2005), 815–825, 10.1007/s00227-004-1474-8.
10. Barnes, D.K. a, Galgani, F., Thompson, R.C., Barlaz, M., Accumulation and fragmentation of plastic debris in global environments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 1985–1998, 10.1098/rstb.2008.0205.
11. Blaber, S.J.M., Removals (wild harvesting) of the biological resources from systems. Wolanski, E., McLusky, D., (eds.) Treatise on Estuarine and Coastal Science, 2012, Elsevier Inc., 253–275, 10.1016/B978-0-12-374711-2.00813-5.
12. Blaber, S.J.M., Ching, C.V., Day, J.W., Elliott, M., Fonseca, M.S., Hoss, D.E., Orensanz, J., Potter, I.C., Silvert, W., Effects of fishing on the structure and functioning of estuarine and nearshore ecosystems. ICES J. Mar. Sci. 57 (2000), 590–602, 10.1006/jmsc.2000.0723.
13. Boerger, C.M., Lattin, G.L., Moore, S.L., Moore, C.J., Plastic ingestion by planktivorous fishes in the north Pacific Central Gyre. Mar. Pollut. Bull. 60 (2010), 2275–2278, 10.1016/j.marpolbul.2010.08.007.
14. Box, G.E.P., Cox, D., An analysis of transformations. J. Roy. Stat. Soc. 26 (1964), 211–252.
15. Bråte, I.L.N., Eidsvoll, D.P., Steindal, C.C., Thomas, K.V., Plastic ingestion by Atlantic cod (Gadus morhua) from the Norwegian coast. Mar. Pollut. Bull. 112 (2016), 105–110, 10.1016/j.marpolbul.2016.08.034.
16. Brewer, D.T., Blaber, S.J.M., Fry, G., Merta, G.S., Efizon, D., Sawdust ingestion by the tropical shad (Tenualosa macrura, Teleostei: Clupeidae): implications for conservation and fisheries. Biol. Conserv. 97 (2001), 239–249, 10.1016/S0006-3207(00)00117-8.
17. Browne, M.A., Galloway, T.S., Thompson, R., Microplastic-an emerging contaminant of potential concern?. Integrated Environ. Assess. Manag. 3 (2007), 559–561, 10.1002/ieam.5630030412.
18. Cervigón, F., Food and Agriculture Organization of the United Nations, R., Fischer, W., Garibaldi, L., Hendrickx, M., Lemus, A.J., Marquez, R., Poutiers, J.M., Robaina, G., Rodriguez, B., Field Guide to the Commercial Marine and Brackish-water Resources of the Northern Coast of South America. first ed., 1993, Food and Agriculture Organization of the United Nations, Rome.
19. 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, 10.1016/j.marpolbul.2011.09.025.
20. Collignon, A., Hecq, J.H., Glagani, F., Voisin, P., Collard, F., Goffart, A., Neustonic microplastic and zooplankton in the north western Mediterranean Sea. Mar. Pollut. Bull. 64 (2012), 861–864, 10.1016/j.marpolbul.2012.01.011.
21. Costa, M.F., Barletta, M., Microplastics in coastal and marine environments of the western tropical and sub-tropical Atlantic Ocean. Environ. Sci. Process. Impacts 17 (2015), 1868–1879, 10.1039/C5EM00158G.
22. Costa, M.F., Silva-Cavalcanti, J.S., Barbosa, C.C., Portugal, J.L., Barletta, M., Plastics buried in the inter-tidal plain of a tropical estuarine ecosystem. J. Coast Res., 2011, 339–343, 10.2112/SI65-206.1.
23. Dantas, D.V., Barletta, M., Costa, M.F., Barbosa-Cintra, S.C.T., Possatto, F.E., Ramos, J.A.A., Lima, A.R.A., Saint-Paul, U., Movement patterns of catfishes (Ariidae) in a tropical semi-arid estuary. J. Fish. Biol. 76 (2010), 2540–2557, 10.1111/j.1095-8649.2010.02646.x.
24. Dantas, D.V., Barletta, M., da Costa, M.F., The seasonal and spatial patterns of ingestion of polyfilament nylon fragments by estuarine drums (Sciaenidae). Environ. Sci. Pollut. Res. 19 (2012), 600–606, 10.1007/s11356-011-0579-0.
25. Davidson, K., Dudas, S.E., Microplastic ingestion by wild and cultured Manila Clams (Venerupis philippinarum) from Baynes Sound, British Columbia. Arch. Environ. Contam. Toxicol. 71 (2016), 147–156, 10.1007/s00244-016-0286-4.
26. de Sá, L.C., Luís, L.G., Guilhermino, L., 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. Environ. Pollut. 196 (2015), 359–362, 10.1016/j.envpol.2014.10.026.
27. Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M., Cyrus, D.P., Nordlie, F.G., Harrison, T.D., The guild approach to categorizing estuarine fish assemblages: a global review. Fish Fish. 8 (2007), 241–268, 10.1111/j.1467-2679.2007.00253.x.
28. Eriksson, C., Burton, H., Origins and biological accumulation of small plastic particles in fur seals from Macquarie Island. Ambio 32 (2003), 380–384, 10.1579/0044-7447-32.6.380.
29. Ferreira, G.V.B., Barletta, M., Lima, A.R.A., Dantas, D.V., Justino, A.K.S., Costa, M.F., Plastic debris contamination in the life cycle of Acoupa weakfish (Cynoscion acoupa) in a tropical estuary. ICES J. Mar. Sci. J. du Cons. 73 (2016), 2695–2707, 10.1093/icesjms/fsw108.
30. Fok, L., Cheung, P.K., Hong Kong at the Pearl River Estuary: a hotspot of microplastic pollution. Mar. Pollut. Bull. 99 (2015), 112–118, 10.1016/j.marpolbul.2015.07.050.
31. Fossi, M.C., Panti, C., Guerranti, C., Coppola, D., Giannetti, M., Marsili, L., Minutoli, R., Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Mar. Pollut. Bull. 64 (2012), 2374–2379, 10.1016/j.marpolbul.2012.08.013.
32. 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. B Biol. Sci. 364 (2009), 2013–2025, 10.1098/rstb.2008.0265.
33. Guebert, F.M., Barletta, M., Ferreira, M., Threats to sea turtle populations in the Western Atlantic : poaching and mortality in small-scale fishery gears. J. Coast Res. 522 (2013), 42–47, 10.2112/SI65-008.1.
34. Güven, O., Gökdağ, K., Jovanović, B., Kideys, A.E., Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ. Pollut. 223 (2017), 286–294, 10.1016/j.envpol.2017.01.025.
35. INMET, Precipitação Acumulada Mensal. [WWW Document], 2014, Inst. Nac. Meteorol. Ministério da Agric. Pecuária e Abast www.inmet.gov.br (accessed 9.20.15).
36. Ivar Do Sul, J.A., Costa, M.F., The present and future of microplastic pollution in the marine environment. Environ. Pollut. 185 (2014), 352–364, 10.1016/j.envpol.2013.10.036.
37. Ivar do Sul, J.A., Costa, M.F., Barletta, M., Cysneiros, F.J.A., Pelagic microplastics around an archipelago of the Equatorial Atlantic. Mar. Pollut. Bull. 75 (2013), 305–309, 10.1016/j.marpolbul.2013.07.040.
38. Ivar do Sul, J.A., Costa, M.F., Silva-Cavalcanti, J.S., Araújo, M.C.B., Plastic debris retention and exportation by a mangrove forest patch. Mar. Pollut. Bull. 78 (2014), 252–257, 10.1016/j.marpolbul.2013.11.011.
39. Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J., Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S., Lange, C.B., Lenihan, H.S., Pandolfi, M., Peterson, C.H., Steneck, R.S., Tegner, M.J., Warner, R.R., Pandolfi, J.M., Historical collapse overfishing of and the recent coastal ecosystems. Science (80-.) 293 (2001), 629–638, 10.1126/science.1059199.
40. Jovanović, B., Ingestion of microplastics by fish and its potential consequences from a physical perspective. Integrated Environ. Assess. Manag. 13 (2017), 510–515, 10.1002/ieam.1913.
41. Lebreton, L.C.M., Greer, S.D., Borrero, J.C., Numerical modelling of floating debris in the world's oceans. Mar. Pollut. Bull. 64 (2012), 653–661, 10.1016/j.marpolbul.2011.10.027.
42. Lebreton, L.C.M., van der Zwet, J., Damsteeg, J.-W., Slat, B., Andrady, A.L., Reisser, J., River plastic emissions to the world's oceans. Nat. Commun., 8, 2017, 15611, 10.1038/ncomms15611.
43. Levene, H., Robust test for equality of variances. Olkin, I., Ghurye, S.G., Hoeffding, W., Madow, W.G., Mann, H.B., (eds.) Contributions to Probability and Statistics: Essays in Honour of Harold Hotelling, 1960, Stanford University Press, Palo Alto, 278–292.
44. Lima, A.R.A., Barletta, M., Costa, M.F., Seasonal-dial shifts of ichthyoplankton assemblages and plastic debris around an equatorial Atlantic Archipelago. Front. Environ. Sci., 4, 2016, 56, 10.3389/fenvs.2016.00056.
45. Lima, A.R.A., Barletta, M., Costa, M.F., Seasonal distribution and interactions between plankton and microplastics in a tropical estuary. Estuar. Coast Shelf Sci. 165 (2015), 213–225, 10.1016/j.ecss.2015.05.018.
46. Lima, A.R.A., Barletta, M., Costa, M.F., Ramos, J.A.A., Dantas, D.V., Melo, P.A.M.C., Justino, A.K.S., Ferreira, G.V.B., Changes in the composition of ichthyoplankton assemblage and plastic debris in mangrove creeks relative to moon phases. J. Fish. Biol. 89 (2016), 619–640, 10.1111/jfb.12838.
47. Lima, A.R.A., Costa, M.F., Barletta, M., Distribution patterns of microplastics within the plankton of a tropical estuary. Environ. Res. 132 (2014), 146–155, 10.1016/j.envres.2014.03.031.
48. Lusher, A.L., Hollman, P., Mendoza-Hill, J., Microplastics in Fisheries and Aquaculture: Status of Knowledge on Their Occurence and Implications for Aquatic Organisms and Food Safety. 2017, FAO, Rome doi:978-92-5-109882-0.
49. 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, 10.1016/j.marpolbul.2012.11.028.
50. Lusher, A.L., O'Donnell, C., Officer, R., O'Connor, I., Microplastic interactions with North Atlantic mesopelagic fish. ICES J. Mar. Sci. 73 (2016), 1214–1225, 10.1093/icesjms/fsv241.
51. Lusher, A.L., Welden, N.A., Sobral, P., Cole, M., Sampling, isolating and identifying microplastics ingested by fish and invertebrates. Anal. Methods 9 (2017), 1346–1360, 10.1039/C6AY02415G.
52. Moore, C.J., Synthetic polymers in the marine environment: a rapidly increasing, long-term threat. Environ. Res. 108 (2008), 131–139, 10.1016/j.envres.2008.07.025.
53. MPA, Boletim Estatístico Da Pesca E Aquicultura 2011. 2011 Brasília.
54. Myers, R.A., Worm, B., Rapid worldwide depletion of predatory fish communities. Nature 423 (2003), 280–283, 10.1038/nature01610.
55. Oehlmann, J., Schulte-Oehlmann, U., Kloas, W., Jagnytsch, O., Lutz, I., Kusk, K.O., Wollenberger, L., Santos, E.M., Paull, G.C., Van Look, K.J.W., Tyler, C.R., A critical analysis of the biological impacts of plasticizers on wildlife. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 2047–2062, 10.1098/rstb.2008.0242.
56. Palmer, M.W., Putting things in even better order: the advantages of canonical correspondence analysis. Ecology 74 (1993), 2215–2230, 10.2307/1939575.
57. Pinkas, L., Oliphant, M.S., Iverson, I.L.K., Food habits of Albacore, Bluefin Tuna, and Bonito in California Waters. Calif. Dep. Fish Game Fish Bull. 152 (1971), 1–105.
58. Pinnegar, J., Jennings, S., O'Brien, C., Polunin, N., Long-term changes in the trophic level of the Celtic Sea fish community and fish market price distribution. J. Appl. Ecol. 39 (2002), 377–390, 10.1046/j.1365-2664.2002.00723.x.
59. Possatto, F.E., Barletta, M., Costa, M.F., Ivar do Sul, J.A., Dantas, D.V., Plastic debris ingestion by marine catfish: an unexpected fisheries impact. Mar. Pollut. Bull. 62 (2011), 1098–1102, 10.1016/j.marpolbul.2011.01.036.
60. Quinn, R., Keough, M., Experimental Design and Data Analysis for Biologists. first ed., 2002, Cambridge University Press, Cambridge.
61. Ramos, J.A.A., Barletta, M., Costa, M.F., Ingestion of nylon threads by gerreidae while using a tropical estuary as foraging grounds. Aquat. Biol. 17 (2012), 29–34, 10.3354/ab00461.
62. Ramos, J.A.A., Barletta, M., Dantas, D.V., Lima, A.R.A., Costa, M.F., Influence of moon phase on fish assemblages in estuarine mangrove tidal creeks. J. Fish. Biol. 78 (2011), 344–354, 10.1111/j.1095-8649.2010.02851.x.
63. 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, 3263, 10.1038/srep03263.
64. Ryan, P.G., Moore, C.J., van Franeker, J. a, Moloney, C.L., Monitoring the abundance of plastic debris in the marine environment. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 1999–2012, 10.1098/rstb.2008.0207.
65. Santillo, D., Miller, K., Johnston, P., Microplastics as contaminants in commercially important seafood species. Integrated Environ. Assess. Manag. 13 (2017), 516–521, 10.1002/ieam.1909.
66. Silva-Cavalcanti, J.S., Silva, J.D.B., França, E.J. de, Araújo, M.C.B. de, Gusmão, F., Microplastics ingestion by a common tropical freshwater fishing resource. Environ. Pollut. 221 (2017), 218–226, 10.1016/j.envpol.2016.11.068.
67. Talsness, C.E., Andrade, A.J.M., Kuriyama, S.N., Taylor, J. a, vom Saal, F.S., Components of plastic: experimental studies in animals and relevance for human health. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 2079–2096, 10.1098/rstb.2008.0281.
68. Taylor, M.L., Gwinnett, C., Robinson, L.F., Woodall, L.C., Plastic microfibre ingestion by deep-sea organisms. Sci. Rep., 6, 2016, 33997, 10.1038/srep33997.
69. Ter Braak, C.J.F., Smilauer, P., CANOCO References Manual and CanocoDraw for Windows User's Guide: Software for Canonical Community Ordination. 2002 [WWW Document] www.canoco.com Version 4.5.
70. Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., Potential for plastics to transport hydrophobic contaminants. Environ. Sci. Technol. 41 (2007), 7759–7764, 10.1021/es071737s.
71. Thompson, R.C., Moore, C.J., vom Saal, F.S., Swan, S.H., Plastics, the environment and human health: current consensus and future trends. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009), 2153–2166, 10.1098/rstb.2009.0053.
72. Thompson, R.C., Olsen, Y., Mitchell, R.P., Davis, A., Rowland, S.J., John, A.W.G., McGonigle, D., Russell, A.E., Lost at sea: where is allthe plastic?. Science (80-.), 304, 2004, 838, 10.1126/science.1094559.
73. Underwood, A.J., Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. first ed., 1997, Cambridge University Press, Cambridge.
74. Underwood, A.J., Chapman, M.G., Browne, M.A., Some problems and practicalities in design and interpretation of samples of microplastic waste. Anal. Methods 9 (2017), 1332–1345, 10.1039/C6AY02641A.
75. Vendel, A.L., Bessa, F., Alves, V.E.N., Amorim, A.L.A., Patrício, J., Palma, A.R.T., Widespread microplastic ingestion by fish assemblages in tropical estuaries subjected to anthropogenic pressures. Mar. Pollut. Bull. 117 (2017), 448–455, 10.1016/j.marpolbul.2017.01.081.
76. Wang, J., Tan, Z., Peng, J., Qiu, Q., Li, M., The behaviors of microplastics in the marine environment. Mar. Environ. Res. 113 (2016), 7–17, 10.1016/j.marenvres.2015.10.014.
77. Williams, M., Zalasiewicz, J., Waters, C.N., Edgeworth, M., Bennett, C., Barnosky, A.D., Ellis, E.C., Ellis, M.A., Cearreta, A., Haff, P.K., Ivar Do Sul, J.A., Leinfelder, R., McNeill, J.R., Odada, E., Oreskes, N., Revkin, A., Richter, D.D.B., Steffen, W., Summerhayes, C., Syvitski, J.P., Vidas, D., Wagreich, M., Wing, S.L., Wolfe, A.P., Zhisheng, A., The Anthropocene: a conspicuous stratigraphical signal of anthropogenic changes in production and consumption across the biosphere. Earth's Futur. 4 (2016), 34–53, 10.1002/2015EF000339.
78. 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, 10.1016/j.envpol.2013.02.031.
79. Zalasiewicz, J., Waters, C.N., Ivar do Sul, J.A., Corcoran, P.L., Barnosky, A.D., Cearreta, A., Edgeworth, M., Galuszka, A., Jeandel, C., Leinfelder, R., McNeill, J.R., Steffen, W., Summerhayes, C., Wagreich, M., Williams, M., Wolfe, A.P., Yonan, Y., The geological cycle of plastics and their use as a stratigraphic indicator of the Anthropocene. Anthropocene 13 (2016), 4–17, 10.1016/j.ancene.2016.01.002.
80. Zhao, S., Zhu, L., Wang, T., Li, D., Suspended microplastics in the surface water of the Yangtze Estuary System, China: first observations on occurrence, distribution. Mar. Pollut. Bull. 86 (2014), 562–568, 10.1016/j.marpolbul.2014.06.032.