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Unravelling the stomach contents of fish and crab species from Cananéia, São Paulo: Are they eating plastic?

Abstract

Plastic pollution represents a threat to marine ecosystems and has therefore been gaining space in the realm of public interest. In this study, we investigated the ingestion of food and non-food items (i.e., plastic particles) by fish and crabs. These animals are commonly collected by trawling with a double-ring net along the coast of Cananéia, state of São Paulo, Brazil; some of them are consumed as food by the local population. Fish and crab stomachs were removed and dissected, and their contents were examined under a stereoscopic microscope with an image-capturing system. The presence or absence of plastic was also registered. We examined 139 specimens of 16 fish species and 143 specimens of four crab species. The most frequent food items found in fish were unidentified food, followed by crustaceans, molluscs, polychaetes, and other fish; in crabs, the items were unidentified food, followed by crustaceans, molluscs and fish. Plastic particles were found in all fish species, representing 47.5% of the individuals analysed. In crabs, the incidence of plastic was lower, occurring in only two species (5% in Callinectes danae and 3% in C. ornatus). Only four fish species analysed had previous records of plastic ingestion in the scientific literature. The high incidence of microplastics in our study is worrying because they negatively affect the animals’ lives and can be transferred through the tropic web to top predators, including humans, through the ingestion of contaminated animals.

Keywords
Human exposure; Commercial fish; Plastic fibres; Anthropogenic influence

INTRODUCTION

Globally, approximately 50% of the 300 million tonnes of plastic produced per year are intended for a single use before being discarded, resulting in a growing burden of waste that can contaminate rivers and the ocean (Galloway et al., 2017aGalloway, T.S.; Cole, M. & Lewis, C. 2017a. Interactions of microplastic debris throughout the marine ecosystem. Nature ecology & evolution, 1(5), 1-8. https://doi.org/10.1038/s41559-017-0116.
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There has also been a great deal of concern regarding microplastics, which are defined as plastic particles < 5 mm and are currently the most abundant type of plastic in the ocean (Borriello & Rose, 2022Borriello, A. & Rose, J.M. 2022. The issue of microplastic in the oceans: Preferences and willingness to pay to tackle the issue in Australia. Marine Policy, 135: 1-9, 104875. https://doi.org/10.1016/j.marpol.2021.104875.
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The global concern for plastic’s damaging impact on all life forms is increasing steadily (Barrowclough & Birkbeck, 2022Barrowclough, D. & Birkbeck, C.D. 2022. Transforming the Global Plastics Economy: The Role of Economic Policies in the Global Governance of Plastic Pollution. Social Sciences, 11(1): 26. https://doi.org/10.3390/socsci11010026.
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) and consequently impacting the ecological functionality of keystone species and trophic levels (e.g., bioturbation, nutrient cycling) (Boerger et al., 2010Boerger, C.M.; Lattin, G.L.; Moore, S.L. & Moore, C.J. 2010. Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin , 60(12): 2275-2278. https://doi.org/10.1016/j.marpolbul.2010.08.007.
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; Galloway et al., 2017bGalloway, T.S.; Dogra, Y.; Garrett, N.; Rowe, D.; Tyler, C.R.; Moger, J.; Lammer, E.; Landsiedel, R.; Sauer, U.G.; Scherer, G.; Wohlleben, W.; & Wiench, K. 2017b. Ecotoxicological assessment of nanoparticle-containing acrylic copolymer dispersions in fairy shrimp and zebrafish embryos. Environmental Science: Nano, 4(10): 1981-1997. https://doi.org/10.1039/C7EN00385D.
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). Microplastic ingestion by different aquatic animals can alter the feeding behaviour, lower lipid storage, and reduce growth and reproduction outputs, also reducing the offspring’s quality and increasing oxidative stress (Browne et al., 2013Browne, M.A.; Niven, S.J.; Galloway, T.S.; Rowland, S.J. & Thompson, R.C. 2013. Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Current Biology, 23(23): 2388-2392. https://doi.org/10.1016/j.cub.2013.10.012.
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). This phenomenon has been increasingly documented in many groups, such as fish, crustaceans, mammals, and others (Gall & Thompson, 2015Gall, S.C. & Thompson, R.C. 2015. The impact of debris on marine life. Marine Pollution Bulletin , 92(1): 170-179. https://doi.org/10.1016/j.marpolbul.2014.12.041.
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, Nicastro et al., 2018Nicastro, K.R.; Savio, R.L.; McQuaid, C.D.; Madeira, P.; Valbusa, U.; Azevedo, F.; Casero, M.; Lourenço, C. & Zardi, G.I. 2018. Plastic ingestion in aquatic-associated bird species in southern Portugal. Marine Pollution Bulletin , 126: 413-418. https://doi.org/10.1016/j.marpolbul.2017.11.050.
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). Still, nanoparticles of contaminated microplastic can go from the gut to the cell membranes, causing cell deregulation (Mattsson et al., 2017Mattsson, K.; Johnson, E.V.; Malmendal, A.; Linse, S.; Hansson, L.A. & Cedervall, T. 2017. Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Scientific reports, 7(1): 1-7. https://doi.org/10.1038/s41598-017-10813-0.
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). Recently studies have shown microplastic occurrence at the cellular level in human placenta (Ragusa et al., 2021Ragusa, A.; Svelato, A.; Santacroce, C.; Catalano, P.; Notarstefano, V.; Carnevali, O.; Papa, F.; Rongioletti, M.C.A.; Baiocco, F.; Draghi, S.; D’Amore, E.; Rinaldo, D.; Matta, M. & Giorgini, E. 2021. Plasticenta: First evidence of microplastics in human placenta. Environment International , 146: 106274. https://doi.org/10.1016/j.envint.2020.106274.
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) and blood (Leslie et al., 2022Leslie, H.A.; van Velzen, M.J.; Brandsma, S.H.; Vethaak, D.; Garcia-Vallejo, J.J. & Lamoree, M.H. 2022. Discovery and quantification of plastic particle pollution in human blood. Environment International , 163: 1-8, 07199. https://doi.org/10.1016/j.envint.2022.107199.
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).

Some cases of plastic ingestion by marine organisms have already been published in Brazil. In fish species, for example, polymers were observed in the gastric content of the Atlantic bigeye Priacanthus arenatus Cuvier 1829, collected from a stretch of the Santa Catarina coast (Garopaba) in southern Brazil (Cardozo et al., 2018Cardozo, A.L.; Farias, E.G.; Rodrigues-Filho, J.L.; Moteiro, I.B.; Scandolo, T.M. & Dantas, D.V. 2018. Feeding ecology and ingestion of plastic fragments by Priacanthus arenatus: What’s the fisheries contribution to the problem? Marine Pollution Bulletin , 130: 19-27. https://doi.org/10.1016/j.marpolbul.2018.03.010.
https://doi.org/10.1016/j.marpolbul.2018...
). Miranda & Carvalho-Souza (2016Miranda, D.D.A. & de Carvalho-Souza, G.F. 2016. Are we eating plastic-ingesting fish? Marine Pollution Bulletin , 103(1-2): 109-114. https://doi.org/10.1016/j.marpolbul.2015.12.035.
https://doi.org/10.1016/j.marpolbul.2015...
) addressed the same phenomenon for two species, Scomberomorus cavalla (Cuvier 1829) and Rhizoprionodon lalandii (Valenciennes 1839), in north-eastern Brazil. Furthermore, Dantas et al. (2020Dantas, N.C.; Duarte, O.S.; Ferreira, W.C.; Ayala, A.P.; Rezende, C.F. & Feitosa, C.V. 2020. Plastic intake does not depend on fish eating habits: Identification of microplastics in the stomach contents of fish on an urban beach in Brazil. Marine Pollution Bulletin , 153: 1-8, 110959. https://doi.org/10.1016/j.marpolbul.2020.11095.
https://doi.org/10.1016/j.marpolbul.2020...
) detected plastic ingestion by seven fish species in Ceará, and Macieira et al. (2021Macieira, R.M.; Oliveira, L.A.S.; Cardozo-Ferreira, G.C.; Pimentel, C.R.; Andrades, R.; Gasparini, J.L.; Sarti, F.; Chelazzi, D.; Cincinelli, A.; Carvalho Gomes, L. & Giarrizzo, T. 2021. Microplastic and artificial cellulose microfibers ingestion by reef fishes in the Guarapari Islands, southwestern Atlantic. Marine Pollution Bulletin , 167: 1-8, 112371. https://doi.org/10.1016/j.marpolbul.2021.112371.
https://doi.org/10.1016/j.marpolbul.2021...
) reported the ingestion of such particles by seven coral reef fish species in Guarapari Islands, both of these areas in Brazil. In contrast, reports of polymers in the digestive content of decapod crustaceans in the country are still very scarce. Records are only available for the fiddler crab Uca (Minuca) rapax (Smith, 1870) (Brenneck et al., 2015Brennecke, D.; Ferreira, E.C.; Costa, T.M; Appel, D.; da Gama, B.A. & Lenz, M. 2015. Ingested microplastics (> 100 μm) are translocated to organs of the tropical fiddler crab Uca rapax. Marine Pollution Bulletin , 96(1-2): 491-495. http://doi.org/10.1016/j.marpolbul.2015.05.001.
http://doi.org/10.1016/j.marpolbul.2015....
) and spider crab Libinia ferreirae Brito Capello, 1871, along the Cananéia coastline, in the state of São Paulo, Brazil (Gonçalves et al., 2019Gonçalves, G.R.L.; Negreiros-Fransozo, M.L.; Fransozo, A. & Castilho, A.L. 2019. Feeding ecology and niche segregation of the spider crab Libinia ferreirae (Decapoda, Brachyura, Majoidea), a symbiont of Lychnorhiza lucerna (Cnidaria, Scyphozoa, Rhizostomeae). Hydrobiologia, 847(4): 1013-1025. https://doi.org/10.1007/s10750-019-04158-0.
https://doi.org/10.1007/s10750-019-04158...
); more detailed studies regarding the environment and species in different Brazilian regions are still scarce. No studies on the interaction of plastic with the regional biota had ever been carried out in the coastal region of São Paulo that is being assessed in the present study; this demonstrates a research gap regarding plastic ingestion by key species from both an ecological and economic perspective. In 2017, 12,380 tonnes of coastal fish were captured in the state of São Paulo (Ávila-da-Silva et al., 2019Ávila-da-Silva, A.O.; Carneiro, M.H.; Mendonça, J.T.; Bastos, G.C.C.; Miranda, L.V.; Ribeiro, W.R. & Santos S. 2019. Produção Pesqueira Marinha e Estuarina do Estado de São Paulo Julho a Setembro de 2019. Informe Pesqueiro de São Paulo, (68): 1-4.); of these, 1,913 tonnes were captured in the Cananéia region.

Considering that Brazil is the fourth largest plastic-consuming country on the planet (Wit et al., 2019Wit, W.; Hamilton, A.; Scheer, R.; Stakes T. & Allan S. 2019. Solucionar a poluição plástica: transparência e responsabilização. Suíssa, WWF - Fundo Mundial para a Natureza.) and that less than 40% of the Brazilian population benefits from garbage collection services and an adequate sewage treatment infrastructure (SNIS, 2014Sistema Nacional de Informações sobre Saneamento (SNIS). 2014. Diagnóstico dos Serviços de Água e Esgotos - 2104 (Diagnoses of water and wastewater services - 2014). Ministério das Cidades (Ministery of Cities), Brasília. Available: Available: http://antigo.snis.gov.br/diagnostico-anual-agua-e-esgotos/diagnostico-ae-2014 . Access: 04/02/2020.
http://antigo.snis.gov.br/diagnostico-an...
), a study investigating microplastics’ real impacts on organisms’ health is urgently needed along with efforts to prevent them from afflicting these same organisms. This problem is compounded when contaminated animals are ingested whole (Nelms et al., 2019Nelms, S.E.; Barnett, J.; Brownlow, A.; Davison, N.J.; Deaville, R.; Galloway, T.S.; Lindeque, P.K.; Santillo, D. & Godley, B.J. 2019. Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory? Scientific Reports, 9(1): 1-8. https://doi.org/10.1038/s41598-018-37428-3.
https://doi.org/10.1038/s41598-018-37428...
). Microplastic accumulation and biomagnification in top predators like humans have been discussed (Carbery et al., 2018Carbery, M.; O’Connor, W. & Palanisami, T. 2018. Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environment International, 115: 400-409. https://doi.org/10.1016/j.envint.2018.03.007.
https://doi.org/10.1016/j.envint.2018.03...
). However, studies on this topic are still recent, and therefore little is known about it. Microplastic ingestion could be responsible for generating many diseases, and it is estimated that plastic can cause cancer and endocrine disruptions in addition to reducing human fertility (Swan & Colino, 2021Swan, S.H. & Colino, S. 2021. Count down: how our modern world is threatening sperm counts, altering male and female reproductive development, and imperiling the future of the human race. New York, Scribner.). Thus, regarding the problem posed by plastic, our study is the first to describe food items and the occurrence of plastic in marine fish and crab species of Cananéia in the state of São Paulo, Brazil.

MATERIAL AND METHODS

Study area

The region of Cananéia, off the coast of the state of São Paulo, Brazil (Fig. 1), and adjacent marine areas have a rich diversity of fauna and flora, which is of great importance for conservation efforts (Diegues, 1987Diegues, A.C. 1987. Conservação e desenvolvimento sustentado de ecossistemas litorâneos no Brasil. Secretaria do Meio Ambiente, São Paulo, Brasil. UNESCO. (1999) World Heritage Nomination - IUCN Technical Evaluation Atlantic Forests (southeast) (Brazil). UNESCO.). In 1993, the Atlantic Forest biome, prevalent in the region, was designated as a Biosphere Reserve (UNESCO, 2005United Nations Educational, Scientific and Cultural Organization (UNESCO). 2005. World Network of Biosphere Reserves - SC/EES - June 2005. The MAB Program. UNESCO.). The mangrove area in Cananéia has also gained global recognition as the third-largest productive marine ecosystem in the South Atlantic due to its well-conserved environmental resources (Mendonça et al., 2010Mendonça, J.T.; Verani, J.R. & Nordi N.N. 2010. Evaluation and management of blue crab Callinectes sapidus (Rathbun, 1896) (Decapoda - Portunidae) fishery in the Estuary of Cananéia, Iguape and Ilha Comprida, São Paulo. Brazil Brazilian Journal of Biology, 70: 37-45.). Cananéia was also named a World Natural Heritage Site in 1999 due to its importance in scientific research, conservation of human values and traditional culture based on the sustainability of the development standards employed (UNESCO, 1999United Nations Educational, Scientific and Cultural Organization (UNESCO). 1999. World Heritage Nomination - IUCN Technical Evaluation Atlantic Forests (southeast) (Brazil). UNESCO.). However, Cananéia has been undergoing an increase in population density and an intensification of fishing activities, which are the livelihood of many of the region’s families (Mendonça & Katsuragawa, 2001Mendonça, J.T. & Katsuragawa, M. 2001. Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995-1996). Acta Scientiarum. Biological Sciences, 23: 535-547.).

Figure 1
Sampling station in the Cananéia region, state of São Paulo, Brazil.

Sampling

Specimens were collected in Cananéia’s neighbouring oceanic areas (around 25°04′43″S, 47°50′34″W) in September 2019, seven kilometres from the coast, at depths between 11 and 15 metres. Collections were performed with a shrimp trawl (mesh size: 20 mm knot-to-knot at the body and 15 mm at the cod end) and a double rig net.

Immediately after trawling, we hand-picked the fish and crabs and transferred them to an isothermal box with ice; they were then kept in a freezer until they underwent analysis at a laboratory. This procedure followed the methods provided by Williams (1981Williams, M.J. 1981. Methods for analysis of natural diet in portunid crabs (Crustacea: Decapoda: Portunidae). Journal of Experimental Marine Biology , 52(1): 103-113.) to ensure that the digestion of the stomach contents was impeded.

Fish specimens were identified to the lowest taxonomic level possible with a specialist’s help, and crabs were identified in accordance with Melo (1996Melo, G.A.S. 1996. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. São Paulo, Plêiade. FAPESP.). The analysed species of crabs and fish were fixed in 10% formalin and formaldehyde solution and subsequently conserved in 70% ethanol. Vouchers of each fish specimen were deposited in the laboratory collection of the Centre for Research in Biology Ecology and Crustacean Farming [Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos (NEBECC)] at the Zoology Department of the “Júlio de Mesquita Filho” University, Botucatu, São Paulo (NEBECC#00221 lot 1 to NEBECC#00236 lot 16).

Stomach content analyses

The stomach of fish and crabs were dissected, cut, and the contents were then washed in a Petri dish with distilled water and examined under a stereoscopic microscope (Zeiss® Stemi SV6) with an image capture system (Zeiss Stemi 2000-C). We used a modified version of the quantitative scoring method developed by Hyslop (1980Hyslop, E.J. 1980. Stomach contents analysis - a review of methods and their application. Journal of Fish Biology, 17(4): 411-429.), Williams (1981Williams, M.J. 1981. Methods for analysis of natural diet in portunid crabs (Crustacea: Decapoda: Portunidae). Journal of Experimental Marine Biology , 52(1): 103-113.), and Mantelatto & Christofoletti (2001Mantelatto, F.L.M. & Christofoletti, R.A. 2001. Natural feeding activity of the crab Callinectes ornatus (Portunidae) in Ubatuba Bay (São Paulo, Brazil): influence of season, sex, size and molt stage. Marine Biology, 138(3): 585-594.) to calculate the proportion of ingesta in each prey category. To minimise the food identification error, the items were classified in major taxa. Most of the food bits were macerated or were in an advanced digestion stage; therefore, it was not possible to identify them at the levels of genus or species. The presence or absence of plastic particles was visually examined as in Barros et al. (2020Barros, M.S.F. & dos Santos Calado, T.C. 2020. Plastic ingestion lead to reduced body condition and modified diet patterns in the rocky shore crab Pachygrapsus transversus (Gibbes, 1850) (Brachyura: Grapsidae). Marine Pollution Bulletin, 156: 1-7, 111249. https://doi.org/10.1016/j.marpolbul.2020.111249.
https://doi.org/10.1016/j.marpolbul.2020...
), through the criteria established by Norén (2007Norén, F. 2007. Small Plastic Particles in Coastal Swedish Waters. Sweden, KIMO Sweden, KIMO Sweden Göteborg.) for identifying plastic particles, that is, the absence of visible cellular or organic structures; the fibre needed to be equally thick throughout all its length, clear, and with a homogeneous colour. Only the particles that followed all the criteria were considered to be anthropogenic material, i.e., plastic. The plastic particles found were counted, photographed, and measured. Some measurements were implemented to minimise sample contamination by microplastics via air-borne particles or on the surface of the equipment. Sterile containers were used for sample collection; all apparatuses used in the laboratory and all of the surfaces in it were wiped down with 70% ethanol prior to the commencement of any work. In addition, a Petri dish filled with distilled water was kept in the laboratory to monitor air contamination during sample analysis (Torre et al., 2016Torre, M.: Digka, N.; Anastasopoulou, A.; Tsangaris, C. & Mytilineou, C. 2016. Anthropogenic microfibres pollution in marine biota. A new and simple methodology to minimise airborne contamination. Marine Pollution Bulletin , 113(1-2): 55-61. https://doi.org/10.1016/j.marpolbul.2016.07.050.
https://doi.org/10.1016/j.marpolbul.2016...
).

RESULTS

We examined 16 fish species that were grouped according to their feeding behaviour: a) pelagic/benthic fish - Peprilus crenulatus Cuvier, 1829; b) pelagic fish - Chloroscombrus chrysurus (Linnaeus, 1766) and Trichiurus lepturus Linnaeus, 1758; c) benthic fish - which encompass all the other fish, along with four species of omnivorous benthic crabs. In total, 139 fish and 143 crab stomachs were sampled, and their contents were analysed. Figure 2 shows the occurrence of food items for each species.

Figure 2
The coloured circle represents the food items, and the black and white circle represent the absence and presence of anthropogenic plastic material found in 16 marine fish (benthic fish, pelagic/benthic fish and pelagic fish) and four crab species in the region of Cananéia, São Paulo, Brazil (CR = crustaceans; SE = sediment; MO = mollusc; FI = fish; FO = foraminiferans; PO = polychaetes; BR = bryozoans. N = number of fish analysed. UD = Unidentified).

The unidentifiable (UD) item was the predominant food item (52%), followed by crustaceans (29%), fish (4%), and sediment (4%). The other items were unrepresentative (Fig. 2). It is noteworthy that some species such as Menticirrhus martinicensis (Cuvier, 1830), Stellifer brasiliensis (Schultz, 1945), Polydactylus virginicus (Linnaeus, 1758), Isopisthus parvipinnis (Cuvier, 1830), Oligoplites saurus (Bloch & Schneider, 1801), and T. lepturus did not present UD as the most predominant food item; for them, crustaceans, fish, and molluscs were more predominant.

Crabs also had UD as their predominant food item (47%), followed by crustaceans (32%), molluscs (13%), and fish (7%). The other items were unrepresentative (Fig. 2). For Hepatus pudibundus (Herbst, 1785) and Callinectes sapidus Rathbun, 1896, the occurrence of crustaceans, fish and molluscs was higher than UD food items.

Microplastics were recorded for all fish species analysed (47.5% specimens). However, for crabs, the plastic was only found in Callinectes ornatus Ordway, 1863 and Callinectes danae Smith, 1869, two of the four crustacean species analysed (3% of individuals) (Fig. 2). One to three fragments of plastic were registered per fish with an average fragment size of 1.97 mm (ranging from 0.05 to 5.43 mm), for crabs the average fragment size was of 1.80 mm (ranging from 0.14 to 3.24 mm). Plastic microfibres were the most abundant item, representing 78% of the fragments found, in the colours blue (76%), black (19%), red (5%), and transparent (1.5%). Moreover, blue microplastic particles were found (22%) (Fig. 3). Table 1 shows the details for each species. During the analysis process, the controlled Petri dishes did not show contamination by participles in suspension in the air of the laboratory.

Figure 3
Representation of the plastic found in the specimens analysed. (A) largest plastic fibres found in Polydactylus virginicus stomach; (B) plastic particle and fibres found in the fish’s stomach Paralonchurus brasiliensis.

Table 1
Abundance and length of microplastics ingested by 16 fish species and two crabs species from Cananéia, São Paulo.

DISCUSSION

This study reports the food items ingested by different species of fish and crabs along the coastline of Cananéia, a region surrounded by an area designated for environmental protection and characterised by the presence of widespread subsistence fishing activity by the local population (Mendonça et al., 2013Mendonça, J.T.; Da Graça-Lopes, R. & De Azevedo, V.G. 2013. Estudo da CPUE da pesca paulista dirigida ao camarão sete-barbas entre 2000 e 2011. Boletim do Instituto de Pesca , 39(3): 251-261.; Mendonça, 2015Mendonça, J.T. 2015. Caracterização da pesca artesanal no litoral sul de São Paulo, Brasil. Boletim do Instituto de Pesca, 41(3): 479-492.). In addition, we detected the occurrence of plastic, i.e., anthropogenic material, in the fish and crab stomachs. Of the 20 species analysed in this study, only the crabs H. pudibundus and C. sapidus had no plastic fragments in their stomachs. The occurrence of anthropogenic material suggests that other species from this region and of different trophic levels have most likely ingested plastic. Therefore, we emphasise the importance of studies geared toward estimating the number of plastic particles being ingested by species of the biota along the Brazilian coastline in order to show the different levels of impact on the environment and marine life in these sites. We also found that preserved conservation areas surrounding the Cananéia region have not prevented plastic entrance into the marine environment. In conservation areas, plastic pollution can be less concentrated but not absent since plastic particles can be transported to different regions via air, rain, wind, currents, rivers, and streams (Rochman, 2018Rochman, C.M. 2018. Microplastics research - from sink to source. Science, 360(6384): 28-29. https://doi.org/10.1126/science.aar7734.
https://doi.org/10.1126/science.aar7734...
; Lim, 2021Lim, X.Z. 2021. Microplastics are everywhere - but are they harmful? Nature, 593(7857): 22-25. https://doi.org/10.1038/d41586-021-01143-3.
https://doi.org/10.1038/d41586-021-01143...
).

All the fish analysed in our study ingested plastic particles, regardless of their feeding behaviour, and this was to be expected since plastic can be found anywhere in the ocean. Microplastics have been shown to move from the marine surface to the sediments (Gago et al., 2018Gago, J.; Carretero, O.; Filgueiras, A.V. & Viñas, L. 2018. Synthetic microfibers in the marine environment: a review on their occurrence in seawater and sediments. Marine Pollution Bulletin , 127: 365-376. https://doi.org/10.1016/j.marpolbul.2017.11.070.
https://doi.org/10.1016/j.marpolbul.2017...
). Low‐density plastics eventually reach the seafloor through density‐modification due to biofouling or integration into zooplankton faecal matter (Cole et al., 2016Cole, M.; Lindeque, P.K.; Fileman, E.; Clark, J.; Lewis, C.; Halsband, C. & Galloway, T.S. 2016. Microplastics alter the properties and sinking rates of zooplankton faecal pellets. Environmental Science & Technology , 50(6): 3239-3246. https://doi.org/10.1021/acs.est.5b05905.
https://doi.org/10.1021/acs.est.5b05905...
). Microplastic ingestion probably occurs during normal fish feeding activities, as evidenced by our results, which showed that pelagic, demersal, and benthic species had plastic in their stomach content. Plastic intake/contamination occurred independently of the trophic guild, which is in line with the findings of Dantas et al. (2020Dantas, N.C.; Duarte, O.S.; Ferreira, W.C.; Ayala, A.P.; Rezende, C.F. & Feitosa, C.V. 2020. Plastic intake does not depend on fish eating habits: Identification of microplastics in the stomach contents of fish on an urban beach in Brazil. Marine Pollution Bulletin , 153: 1-8, 110959. https://doi.org/10.1016/j.marpolbul.2020.11095.
https://doi.org/10.1016/j.marpolbul.2020...
). We were not able to identify which species is most susceptible to microplastic ingestion based on their feeding habits. However, omnivores and predators can ingest more microplastics as a result of their wider range of diet sources, which can lead to a transfer of microplastics from prey to predator (Dantas et al., 2020Dantas, N.C.; Duarte, O.S.; Ferreira, W.C.; Ayala, A.P.; Rezende, C.F. & Feitosa, C.V. 2020. Plastic intake does not depend on fish eating habits: Identification of microplastics in the stomach contents of fish on an urban beach in Brazil. Marine Pollution Bulletin , 153: 1-8, 110959. https://doi.org/10.1016/j.marpolbul.2020.11095.
https://doi.org/10.1016/j.marpolbul.2020...
). The higher occurrence of microplastics in fish could be related to their behaviour of eating whole or large pieces of prey as opposed to crabs that lacerate their prey into small pieces; however, this hypothesis requires further tests. Studies on species with different eating habits in different food chains need to be performed carefully to understand the magnitude of the microplastic problem on marine life since organisms have contact with plastic particles independent of their food behaviour.

Our study showed a qualitative food habit for fish and crab species, being the first one to present these results for the fish Eugerres brasilianus (Cuvier, 1830), Haemulopsis corvinaeformis (Steindachner, 1868), P. virginicus, O. saurus, and P. crenulatus. We detected differences between the diets of the following species: E. brasilianus and H. corvinaeformis displayed a preference for molluscs (such as bivalves) and sediment, while P. virginicus and O. saurus had a diet comprising predominantly crustaceans. These fish have demersal/benthic behaviour and are predators of benthos resources.

We were unable to identify food items ingested by P. crenulatus due to the species’ accelerated digestion process. This species was reported to associate with jellyfish (Lawley & Faria-Jr., 2018Lawley, J.W. & Faria-Jr., F. 2018 First record of association between Tamoya haplonema (Cnidaria: Cubozoa) and stromateid fish, with a review on interactions between fish and cubozoan jellyfishes. Plankton and Benthos Research, 13(1): 32-38. https://doi.org/10.3800/pbr.13.32.
https://doi.org/10.3800/pbr.13.32...
), suggesting that the fish may feed off jellyfish tissue and/or even the jellyfish’s food. Jellyfish tissue can be digested quickly; this has to do with the jellyfish’s biochemical composition, with more than 90% of water, a high proportion of proteins, low C:N ratio, and an absence of hard structures, it is therefore easily degraded (Hsieh & Rudloe, 1994Hsieh, Y.P. & Rudloe, J. 1994. Potential of utilizing jellyfish as food in Western countries. Trends in Food Science & Technology, 5(7): 225-229. https://doi.org/10.1016/0924-2244(94)90253-4.
https://doi.org/10.1016/0924-2244(94)902...
; Marques et al., 2021Marques, R.; Rufino, M.; Darnaude, A.M.; Carcaillet, F.; Meffre, M. & Bonnet, D. 2021. Jellyfish degradation in a shallow coastal Mediterranean lagoon. Estuarine, Coastal and Shelf Science, 261: 1-12, 107527. https://doi.org/10.1016/j.ecss.2021.107527.
https://doi.org/10.1016/j.ecss.2021.1075...
). In addition, the food that is poached from the jellyfish has already undergone the initial stages of digestion, so its final digestion is faster.

Seven of the fish species analysed here had already been registered based on the occurrence of microplastic in their stomachs: Conodon nobilis (Linnaeus, 1758), C. chrysurus, Cathorops spixii (Agassiz, 1829), H. corvinaeformis, O. saurus, S. brasiliensis, and Trichiurus lepturus Linnaeus, 1758 (Dantas et al., 2012Dantas, D.V.; Barletta, M. & Costa, M.F.D. 2012. The seasonal and spatial patterns of ingestion of polyfilament nylon fragments by estuarine drums (Sciaenidae). Environmental Science and Pollution Research, 19: 600-606. https://doi.org/10.1007/s11356-011-0579-0.
https://doi.org/10.1007/s11356-011-0579-...
; Silva et al., 2018Silva, J.D.; Barletta, M.; Lima, A.R. & Ferreira, G.V. 2018. Use of resources and microplastic contamination throughout the life cycle of grunts (Haemulidae) in a tropical estuary. Environmental Pollution , 242: 1010-1021. https://doi.org/10.1016/j.envpol.2018.07.038.
https://doi.org/10.1016/j.envpol.2018.07...
; Vendel et al., 2017Vendel, A.L.; Bessa, F.; Alves, V.E.N.; Amorim, A.L.A.; Patrício, J. & Palma, A.R.T. 2017. Widespread microplastic ingestion by fish assemblages in tropical estuaries subjected to anthropogenic pressures. Marine Pollution Bulletin , 117(1-2): 448-455. https://doi.org/10.1016/j.marpolbul.2017.01.081.
https://doi.org/10.1016/j.marpolbul.2017...
; Pegado et al., 2018Pegado, T.S.S.; Schmid, K.; Winemiller, K.O.; Chelazzi, D.; Cincinelli, A.; Dei, L. & Giarrizzo, T. 2018. First evidence of microplastic ingestion by fishes from the Amazon River estuary. Marine Pollution Bulletin , 133(1): 814-821. https://doi.org/10.1016/j.marpolbul.2018.06.035.
https://doi.org/10.1016/j.marpolbul.2018...
; Dantas et al., 2020).

Crustaceans, like shrimps and crabs, use plant and organic matter accumulated in sediment as a food resource (Willems et al., 2016Willems, T.; De Backer, A.; Kerkhove, T.; Dakriet, N.N.; De Troch, M.; Vincx, M. & Hostens, K. 2016. Trophic ecology of Atlantic seabob shrimp Xiphopenaeus kroyeri: Intertidal benthic microalgae support the subtidal food web off Suriname. Estuarine, Coastal and Shelf Science , 182: 146-157. https://doi.org/10.1016/j.ecss.2016.09.015.
https://doi.org/10.1016/j.ecss.2016.09.0...
). This can increase the crab’s chance of indirectly ingesting plastics that are coated by biofilm (community of microorganisms) accumulated in the environment, which mistakenly understand this material to be food of high nutritional value. In terms of the crabs analysed in our study, there are reports of plastic occurrence only for C. ornatus (Santana et al., 2017Santana, M.F.M.; Moreira, F.T. & Turra, A. 2017. Trophic transference of microplastics under a low exposure scenario: insights on the likelihood of particle cascading along marine food-webs. Marine pollution bulletin , 121(1-2): 154-159.). However, it is noteworthy that the ingestion occurred under laboratory conditions (see Santana et al., 2017 for more details). Thus, our study is the first to find evidence of plastic ingestion by C. ornatus under natural conditions. In light of our findings, we recommend that studies that seek to understand possible connections between food habits and plastic ingestion through trophic transfer be conducted.

The most frequent type of plastic we found was blue microfibre, as in many other studies conducted in marine environments (Duncan et al., 2017Duncan, E.M.; Botterell, Z.L.R.; Broderick, A.C.; Galloway, T.S.; Lindeque, P.K.; Nuno, A. & Godley, B.J. 2017 A global review of marine turtle entanglement in anthropogenic debris: a baseline for further action. Endangered Species Research, 34: 431-448. https://doi.org/10.3354/esr00865.
https://doi.org/10.3354/esr00865...
; Compa et al., 2018Compa, M.; Ventero, A.; Iglesias, M. & Deudero, S. 2018. Ingestion of microplastics and natural fibres in Sardina pilchardus (Walbaum, 1792) and Engraulis encrasicolus (Linnaeus, 1758) along the Spanish Mediterranean coast. Marine Pollution Bulletin , 128: 89-96. https://doi.org/10.1016/j.marpolbul.2018.01.009.
https://doi.org/10.1016/j.marpolbul.2018...
; Suaria et al., 2020Suaria, G.; Achtypi, A.; Perold, V.; Lee, J.R.; Pierucci, A.; Bornman, T.G.; Aliani, S. & Ryan, P.G. 2020. Microfibers in oceanic surface waters: A global characterisation. Science Advances, 6(23): eaay8493. https://doi.org/10.1126/sciadv.aay8493.
https://doi.org/10.1126/sciadv.aay8493...
). These fibres are usually shed during the manufacturing and laundry processes and reach rivers and oceans mostly through sewage (Henry et al., 2019Henry, B.; Laitala, K. & Klepp, I.G. 2019. Microfibres from apparel and home textiles: prospects for including microplastics in environmental sustainability assessment. Science of the Total Environment , 652: 483-494. https://doi.org/10.1016/j.scitotenv.2018.10.166.
https://doi.org/10.1016/j.scitotenv.2018...
). Some fish species eat microplastic particles because they confuse them with their natural food items. Ory et al. (2017Ory, N.C.; Sobral, P.; Ferreira, J.L. & Thiel, M. 2017. Amberstripe scad Decapterus muroadsi (Carangidae) fish ingest blue microplastics resembling their copepod prey along the coast of Rapa Nui (Easter Island) in the South Pacific subtropical gyre. Science of the Total Environment , 586: 430-437. https://doi.org/10.1016/j.scitotenv.2017.01.175.
https://doi.org/10.1016/j.scitotenv.2017...
) reached this understanding because they found blue plastic in the stomachs of Decapterus muroadsi (Temminck & Schlegel, 1844); the natural prey of D. muroadsi is a blue copepod that tends to live on the surface of the water, where the blue plastic particles are also found due to their lower density. These fish may confuse these particles with food. In our study, some fish representants of Carangidae, the same family studied by Ory et al. (2017), such as C. chrysurus and O. saurus, can have similar behaviours, thereby justifying the incidence of blue plastic ingestion. Blue nylon fibres (debris) are commonly found in the environment, facilitating accidental ingestion by animals. Dantas et al. (2020Dantas, N.C.; Duarte, O.S.; Ferreira, W.C.; Ayala, A.P.; Rezende, C.F. & Feitosa, C.V. 2020. Plastic intake does not depend on fish eating habits: Identification of microplastics in the stomach contents of fish on an urban beach in Brazil. Marine Pollution Bulletin , 153: 1-8, 110959. https://doi.org/10.1016/j.marpolbul.2020.11095.
https://doi.org/10.1016/j.marpolbul.2020...
) found that blue polyester is the most common microfibre ingested by fish analysed in Brazil. The other blue microplastic particles found in our study could be a synthetic blue pigment used in the composition of paints and the coating of certain types of plastic, which are widely employed in the packaging industry (Lewis, 2004Lewis, P.A. 2004. Organic colorants. In: Charvat, R.A. (Org.). Coloring of Plastics: Fundamentals. Hoboken, New Jersey, John Wiley & Sons. p. 100-126.); Dantas et al. (2020) found these particles in Brazilian fish. All these plastic types, as well as their means of insertion, could be taking place in the region of Cananéia due to the improper disposal of garbage and sewage and fishing activity (loss or undue disposal of fishing gear). These activities need to be monitored since the population in this region increases by 10 times during the high season (summer) (Becegato, 2007Becegato, J.L. 2007. Impacto ambiental antrópico na APA (Área de Proteção Ambiental) da 506 Ilha Comprida (SP), da Pré-História à atualidade. Dissertação de Mestrado em 507 Análise Geoambiental. Universidade de Guarulhos.), increasing the disposal of materials.

Many studies have shown that plastic ingestion causes significant damage to animals (e.g.,Watts et al., 2015Watts, A.J.; Urbina, M.A.; Corr, S.; Lewis, C. & Galloway, T.S. 2015. Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environmental Science & Technology , 49(24): 14597-14604. https://doi.org/10.1021/es501090e.
https://doi.org/10.1021/es501090e...
; Lönnstedt & Eklöv, 2016Lönnstedt, O.M. & Eklöv, P. 2016. Environmentally relevant concentrations of microplastic particles influence larval fish ecology. Science, 352(6290): 1213-1216. https://doi.org/10.1126/science.aad8828.
https://doi.org/10.1126/science.aad8828...
). Watts et al. (2015Watts, A.J.; Urbina, M.A.; Corr, S.; Lewis, C. & Galloway, T.S. 2015. Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environmental Science & Technology , 49(24): 14597-14604. https://doi.org/10.1021/es501090e.
https://doi.org/10.1021/es501090e...
) showed that crustaceans contribute to breaking down microplastics when ingesting these particles, making smaller plastic particles available in the environment. It is noteworthy that the smaller the particles, the greater the risk they offer (Mattsson et al., 2017Mattsson, K.; Johnson, E.V.; Malmendal, A.; Linse, S.; Hansson, L.A. & Cedervall, T. 2017. Brain damage and behavioural disorders in fish induced by plastic nanoparticles delivered through the food chain. Scientific reports, 7(1): 1-7. https://doi.org/10.1038/s41598-017-10813-0.
https://doi.org/10.1038/s41598-017-10813...
) since they are more easily ingested (Pozo et al., 2019Pozo, K.; Gomez, V.; Torres, M.; Vera, L.; Nuñez, D.; Oyarzún, P.; Mendoza, G.; Clarke, B.; Fossi, M.C.; Bainic, M.; Přibylová, P. & Přibylová, P. 2019. Presence and characterization of microplastics in fish of commercial importance from the Biobío region in central Chile. Marine Pollution Bulletin , 140: 315-319. https://doi.org/10.1016/j.marpolbul.2019.01.025.
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; Foekema et al., 2013Foekema, E.M.; De Gruijter, C.; Mergia, M.T.; van Franeker, J.A.; Murk, A.J. & Koelmans, A.A. 2013. Plastic in North Sea Fish. Environmtal Science Technology, 47(15): 8818-8824. https://doi.org/10.1021/es400931b.
https://doi.org/10.1021/es400931b...
). Microplastic accumulation in the animal body generates bioaccumulation of plastic and subsequent biomagnification (Rochman et al., 2013Rochman, C.M.; Hoh, E.; Hentschel, B.T. & Kaye, S. 2013. Long-term field measurement of sorption of organic contaminants to five types of plastic pellets: implications for plastic marine debris. Environ Science & Technology, 47(3): 1646-1654. https://doi.org/10.1021/es303700s.
https://doi.org/10.1021/es303700s...
; Perez-Venegas et al., 2018Perez-Venegas, D.J.; Seguel, M.; Pavés, H.; Pulgar, J.; Urbina, M.; Ahrendt, C. & Galbán Malagón, C. 2018. First detection of plastic microfibers in a wild population of South American fur seals (Arctocephalus australis) in the Chilean Northern Patagonia. Marine Pollution Bulletin , 136: 50-54. https://doi.org/10.1016/j.marpolbul.2018.08.065.
https://doi.org/10.1016/j.marpolbul.2018...
; Nelms et al., 2019Nelms, S.E.; Barnett, J.; Brownlow, A.; Davison, N.J.; Deaville, R.; Galloway, T.S.; Lindeque, P.K.; Santillo, D. & Godley, B.J. 2019. Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory? Scientific Reports, 9(1): 1-8. https://doi.org/10.1038/s41598-018-37428-3.
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); higher bioaccumulation is found in top predators, including humans (Carbery et al., 2018Carbery, M.; O’Connor, W. & Palanisami, T. 2018. Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environment International, 115: 400-409. https://doi.org/10.1016/j.envint.2018.03.007.
https://doi.org/10.1016/j.envint.2018.03...
; Au et al., 2017Au, S.Y.; Lee, C.M.; Weinstein, J.E.; van den Hurk, P. & Klaine, S.J. 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.
https://doi.org/10.1002/ieam.1907...
). Different species that ingest plastic are sought after fishing resources; this increases the probability of plastic ingestion by humans (e.g.,Neves et al., 2015Neves, D.; Sobral, P.; Ferreira, J.L. & Pereira, T. 2015. Ingestion of microplastics by commercial fish off the Portuguese coast. Marine pollution bulletin, 101(1): 119-126. https://doi.org/10.1016/j.marpolbul.2015.11.008.
https://doi.org/10.1016/j.marpolbul.2015...
; Digka et al., 2018Digka, N.; Tsangaris, C.; Torre, M.; Anastasopoulou, A. & Zeri, C. 2018. Microplastics in mussels and fish from the Northern Ionian Sea. Marine Pollution Bulletin , 135: 30-40. https://doi.org/10.1016/j.marpolbul.2018.06.063.
https://doi.org/10.1016/j.marpolbul.2018...
; Hara et al., 2020Hara, J.; Frias, J. & Nash, R. 2020. Quantification of microplastic ingestion by the decapod crustacean Nephrops norvegicus from Irish waters. Marine Pollution Bulletin , 152: 110905. https://doi.org/10.1016/j.marpolbul.2020.110905.
https://doi.org/10.1016/j.marpolbul.2020...
). We included fish species with commercial importance in our study: Micropogonias furnieri (Desmarest, 1823), E. brasilianus, P. crenulatus, O. saurus, Genidens barbus (Lacepède, 1803), M. martinicensis, and T. lepturus; these last two species, in particular, are of significant commercial importance (Martins & Haimovici, 1997Martins, A.S. & Haimovici, M. 1997. Distribution, abundance and biological interactions of the cutlassfish Trichiurus lepturus in the southern Brazil subtropical convergence ecosystem. Fisheries Research, 30(3): 217-227.; Braun & Fontoura 2004Braun, A.S. & Fontoura, N.F. 2004. Reproductive biology of Menticirrhus littoralis in southern Brazil (Actinopterygii: Perciformes: Sciaenidae). Neotropical Ichthyology, 2: 31-36.). In addition, the blue crabs C. sapidus and C. danae have some commercial importance.

Regarding the species analysed in our study, none of them was recorded as threatened species in FishBase (https://fishbase.net.br, accessed on August 12th 2022). Nevertheless, such data is non-existent for some species, such as P. crenulatus, G. barbus, C. spixii, and Aspistor luniscutis (Valenciennes, 1840). Furthermore, quite a bit of the information found in the database has not been updated since 2009, and it therefore is obsolete; this is the case for M. furnieri. Our results reinforce the urgency of the need for further studies to shed light on the stability of populations of many species, given the pollution of the environment by different components, mainly plastic, fishing-induced pressures, and climate change.

CONCLUSION

This is the first study to document microplastic ingestion for nine fish and four crab species in their natural environments in Cananéia, São Paulo, Brazil. We found that unidentifiable food, crustaceans, molluscs, fish, and sediment are the most common items ingested by the species studied. Microplastics were found in different species that share the same environment. All of the fish species sampled in Cananéia were found to have ingested microplastics; this is independent of their habitat and feeding behaviours. Only two crab species did not present microplastics in the stomach. As previously reported, blue microplastic fibres were the most frequent microplastics in our study. The highest incidence of microplastic contamination was found in a region surrounded by preserved areas. Since a low number of individuals and species were analysed, this research in the Cananéia coast and mangrove areas should be extended to obtain more information and evidence of microplastic contamination and intake by the organisms in question. Research regarding plastic contamination is essential for guiding the Brazilian environmental authorities to create strategies for sustainable management of marine, coastal, and mangrove ecosystems in both the region and the country as a whole. Guidelines and laws should be created, and companies that use plastics should collect and reuse such material. Also, industry changes are necessary to start using natural and biodegradable products. We know this is a big challenge for Brazil; nevertheless, changes need to be implemented in this century if we want life on the planet to have a chance.

ACKNOWLEDGMENTS

We appreciate permission by “Instituto Chico Mendes de Conservação da Biodiversidade” (ICMBio) to collect the bycatch of commercial shrimps.

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  • FUNDING INFORMATION:

    Financial support that GRLG receives from the São Paulo Research Foundation (FAPESP, Projects 2018/01659-0, 2019/00105-3).
  • Published with the financial support of the “Programa de Apoio às Publicações Científicas da Universidade de São Paulo”

Edited by

Edited by:

Murilo Nogueira de Lima Pastana

Publication Dates

  • Publication in this collection
    27 Feb 2023
  • Date of issue
    2023

History

  • Received
    12 Apr 2022
  • Accepted
    31 Oct 2022
  • Published
    23 Jan 2023
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