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Inorganic contamination in roadkill birds in Northeast Brazil

Contaminação inorgânica em aves atropeladas no Nordeste do Brasil

Abstract

Wildlife roadkill surveys in Brazil often focus on birds, as they are one of the main groups affected by road accidents. In addition roadkill, anthropogenic litter also contributes to a significant number of bird fatalities every year. The present study aimed to investigate the stomach contents and possible contamination by inorganic material of birds killed on a federal highway that crosses the Serra de Itabaiana National Park in the state of Sergipe, Brazil. Monitoring and data collection were carried out from January to June 2022, with a motorcycle at an average speed of 60 km/h. The collected animals were transported to the Institute of Technology and Research, located at the Tiradentes University, Sergipe, Brazil, and a plastic material was identified. The plastic material found was subjected to Fourier Transform Infrared Spectroscopy (FTIR), which showed a similar wavenumber to a polymer in the polypropylene chain, very common in plastic packaging. The presence of plastics and metals in the intestinal contents of Caracara plancus and Crotophaga ani is noteworthy, as they have a greater tendency to ingest plastics due to their generalist diet. Plastic contamination in Progne chalybea and Nyctidromus albicollis probably occurred through bioaccumulation, from the consumption of insects contaminated by microplastics.

Keywords
Bird feeding; Microplastic; Spectroscopy; Residue; Ingestion; Stomach contents

Resumo

As pesquisas sobre atropelamentos de animais silvestres no Brasil geralmente se concentram nas aves, pois elas são um dos principais grupos afetados por acidentes rodoviários. Além dos atropelamentos, o lixo antropogênico também contribui para um número significativo de mortes de aves todos os anos. O presente estudo teve como objetivo investigar o conteúdo estomacal e possível contaminação por material inorgânico de aves atropeladas em uma rodovia federal que atravessa o Parque Nacional da Serra de Itabaiana, no estado de Sergipe, Brasil. O monitoramento e a coleta de dados foram realizados no período de janeiro a junho de 2022, com uma motocicleta a uma velocidade média de 60 km/h. Os animais coletados foram transportados para o Instituto de Tecnologia e Pesquisa situado na Universidade Tiradentes, Sergipe, Brasil, onde foi identificado um material plástico. O material plástico encontrado foi submetido à espectroscopia no infravermelho com transformada de Fourier (FTIR), que mostrou número de onda semelhante a um polímero da cadeia do polipropileno, muito comum em embalagens plásticas. Chama a atenção a presença de plásticos e metais no conteúdo intestinal de Caracara plancus e Crotophaga ani, pois apresentam maior tendência à ingestão de plásticos devido à dieta generalista. A contaminação plástica em Progne chalybea e Nyctidromus albicollis provavelmente ocorreu por bioacumulação, a partir do consumo de insetos contaminados por microplásticos.

Palavras-chave
Alimentação de pássaros; Microplástico; Espectroscopia; Resíduo; Ingestão; Conteúdo do estômago

Introduction

The running over of animals is one of the main negative impacts in the suppression of fauna in the biotic environment, as it endangers populations of entire species, causing a decline or even extinction (Gumier-Costa and Spencer 2009GUMIER-COSTA, F., SPERBER, C.F. 2009. Atropelamentos de vertebrados na Floresta Nacional de Carajás, Pará, Brasil. Acta Amazon., 39:459–466. https://doi.org/10.1590/S0044-59672009000200027.
https://doi.org/10.1590/S0044-5967200900...
, Winton et al. 2020WINTON, S.A., BISHOP, C.A., LARSEN, K.W. 2020. When protected areas are not enough: low-traffic roads projected to cause a decline in a northern viper population. Endanger. Species Res., 41:131–139. https://doi.org/10.3354/esr01017.
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). According to the Brazilian Center for Road Ecology Studies, it is estimated that, in Brazil, around 15 animals are killed by vehicles per second, totaling 475 million per year, of which approximately 90% are small-sized. The northeastern region of Brazil concentrates 9% of the total recorded roadkill in the country (CBEE 2019CBEE 2019. Centro Brasileiro de Estudos em Ecologia de Estradas, Sistema Urubu https://sistemaurubu.com.br/dados/ (last access in 07/nov/2022).
https://sistemaurubu.com.br/dados/...
).

In Brazil, birds represent a significant proportion of vertebrates killed by vehicles, being among the groups with the highest presence in studies on roadkill in various states of Brazil (Silva et al. 2019SILVA, L.M., SOUSA, F.A., VIEIRA, T.C., MORAIS, C.R. 2019. Levantamento de animais vertebrados atropelados em trechos das rodovias MG-352 e MG-190. Reva GeTeC, 8:42–63., Miranda et al. 2021MIRANDA, J.E.S., SANTOS, A., SOUZA, W.F. 2021. Atropelamento de animais silvestres na rodovia go-060 entre Iporá e Arenópolis, estado de Goiás. Braz. J. Develop., 7:51664–51671. https://doi.org/10.34117/bjdv.v7i5.30275.
https://doi.org/10.34117/bjdv.v7i5.30275...
, Vasconcelos et al. 2021VASCONCELOS, A.R.P., SILVA, E.I., CARVALHO, A.V. 2021. Evaluation of run-over of wild animals on BR-153, trecho Guaraí-Tabocão. Res. Soc. Develop., 10:e332101523834-e332101523834. https://doi.org/10.33448/rsd-v10i15.23834.
https://doi.org/10.33448/rsd-v10i15.2383...
, Favretto 2022FAVRETTO, M.A. 2022. Atropelamento de vertebrados no Planalto de Santa Catarina, Sul do Brasil. Biodivers. Bras., 12:1–8. https://doi.org/10.37002/biobrasil.v12i2.1998.
https://doi.org/10.37002/biobrasil.v12i2...
). This quantity may be underestimated, as bird carcasses tend to degrade more rapidly due to their size (Henry et al. 2021HENRY, D.A.W., COLLINSON-JONKER, W.J., DAVIES-MOSTERT, H.T., NICHOLSON, S.K., ROXBURGH, L., PARKER, D.M. 2021. Optimizing the cost of roadkill surveys based on an analysis of carcass persistence. J. Environ. Manag., 291:112664. https://doi.org/10.1016/j.jenvman.2021.112664.
https://doi.org/10.1016/j.jenvman.2021.1...
), making it difficult to keep accurate records, in addition to the fact that many become trapped in the structure of the vehicles.

Souza et al. (2022)SOUZA, L.A.C., ARAÚJO SOUSA, E.S., FIGUEIRA, S.V., REIS, A.D.B.G., SILVA, B.P.A., ALVES, F.M., PARANAIBA, W.C.R.B., SANTOS, T.P., PONTES, S.R.L., OLIVEIRA E SILVA, G.F., 2022. Levantamento de fauna atropelada na GO 050, trecho Trindade-Campestre de Goiás. Vita et Sanitas, 16:120–132. in a survey carried out on the GO 050 highway, in the state of Goiás, Brazil, identified the association between large amounts of trash on the sides of the highway and roadkill wildlife occurring on these stretches. Subsequently, Marques et al. (2023)MARQUES, A.P., NETO, L.L., CARMO, M.E.R., LOPES, S.C. 2023. Levantamento dos impactos ambientais causados pela construção e uso de rodovias. Rev. Multidiscip. do Nordeste Mineiro, 4(1). associate the irregular disposal of garbage through the windows of vehicles that travel on highways and associated the accumulation of garbage on the sides of the highway with run-overs and intoxication of these animals due to ingestion of plastic.

The ingestion of plastic waste by wildlife has become common (Sá et al. 2018SÁ, L.C., OLIVEIRA, M., RIBEIRO, F., ROCHA, T.L., FUTTER, M.N. 2018. Studies of the effects of microplastics on aquatic organisms: what do we know and where should we focus our efforts in the future? Sci. Total Environ., 645:1029–1039. https://doi.org/10.3354/esr01017.
https://doi.org/10.3354/esr01017...
, Zhu et al. 2019ZHU, L., WANG, H., CHEN, B., SUN, X., QU, K., XIA, B. 2019. Microplastic ingestion in deep-sea fish from the South China Sea. Sci. Total Environ., 677:493–501. https://doi.org/10.1016/j.scitotenv.2019.04.380.
https://doi.org/10.1016/j.scitotenv.2019...
). It is estimated that about 55% of birds with habits associated with freshwater environments and 56% of seabirds have plastic and/or microplastics in their digestive tracts (Gall and Thompson 2015GALL, S. C., THOMPSON, R. C. 2015. The impact of debris on marine life. Mar. Pollut. Bull., 92:170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041.
https://doi.org/10.1016/j.marpolbul.2014...
, Holland et al. 2016HOLLAND, E.R., MALLORY, M.L., SHUTLER, D. 2016. Plastics and other anthropogenic debris in freshwater birds from Canada. Sci. Total Environ., 571:251–258. https://doi.org/10.1016/j.scitotenv.2016.07.158.
https://doi.org/10.1016/j.scitotenv.2016...
). The ingestion of anthropogenic waste by birds can pose the risk of perforations and intestinal blockages in animals (Henry et al. 2021HENRY, D.A.W., COLLINSON-JONKER, W.J., DAVIES-MOSTERT, H.T., NICHOLSON, S.K., ROXBURGH, L., PARKER, D.M. 2021. Optimizing the cost of roadkill surveys based on an analysis of carcass persistence. J. Environ. Manag., 291:112664. https://doi.org/10.1016/j.jenvman.2021.112664.
https://doi.org/10.1016/j.jenvman.2021.1...
). The present study aimed to investigate plastic contamination in the stomach contents of bird roadkill on a section of BR-235 in the state of Sergipe, Brazil.

Material and Methods

The Serra de Itabaiana National Park (10°45’59” S; 37°20’14” W) has a total area of 8.024.79 hectares (ICMBio 2005ICMBIO 2005. Instituto Chico Mendes de Conservação da Biodiversidade, PARNA Serra de Itabaiana https://www.icmbio.gov.br/portal/unidadesdeconservacao/biomas-brasileiros/mataatlantica/unidades-de-conservacao-mata-atlantica/2211-parna-serra-de-itabaiana (last access in 29/jul/2020).
https://www.icmbio.gov.br/portal/unidade...
), with a tropical climate and predominance of the Atlantic Forest biome (ICMBio 2005ICMBIO 2005. Instituto Chico Mendes de Conservação da Biodiversidade, PARNA Serra de Itabaiana https://www.icmbio.gov.br/portal/unidadesdeconservacao/biomas-brasileiros/mataatlantica/unidades-de-conservacao-mata-atlantica/2211-parna-serra-de-itabaiana (last access in 29/jul/2020).
https://www.icmbio.gov.br/portal/unidade...
). It is crossed by the federal highway BR-235 for about four kilometers. The BR-235 highway has 2.093 km starting in the state of Sergipe and ending in the state of Pará. The stretch that crosses the state of Sergipe from west to east is approximately 120 kilometers long, passing through seven municipalities in Sergipe until reaching the state of Bahia.

Collections were carried out on the 37 km stretch between the municipalities of Aracaju (zero kilometer) and Areia Branca, where the Serra de Itabaiana National Park is located. The sampled stretch is surrounded by fragments of Atlantic Forest and anthropized areas (pastures, residences, sugarcane, and corn plantations, among others) and was covered by motorcycle, at an average speed of 60 km/h (Oliveira et al. 2021OLIVEIRA, S.L., BASTOS, R.P., LACERDA, K.A.P. 2021. How does the evaluation speed interfere in the registry number of animated animals? Braz. J. Develop., 7:63045–63065. https://doi.org/10.34117/bjdv7n6-605.
https://doi.org/10.34117/bjdv7n6-605...
), twice a month, between January and June 2022.

The collected bird roadkill was identified (Piacentini et al. 2015PIACENTINI, V.Q., ALEIXO, A., AGNE, C.E., MAURÍCIO, G.N., PACHECO, J.F., BRAVO, G.A., BRITO, G.R.R., NAKA, L.N., OLMOS, F., POSSO, S., SILVEIRA, L.F., BETINI, G.S., CARRANO, E., FRANZ, I., LEES, A.C., LIMA, L.M., PIOLI, D., SCHUNCK, F., AMARAL, F.R., BENCKE, G.A., COHN-HAFT, M., FIGUEIREDO, L.F.A., STRAUBE, F.C., CESARI, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Rev. Bras. Ornitol., 23:91–298., Pacheco et al. 2021PACHECO, J.F., SILVEIRA, L.F., ALEIXO, A., AGNE, C.E., BENCKE, G.A., BRAVO, G.A., BRITO, G.R.R., COHN-HAFT, M., MAURÍCIO, G.N., NAKA, L.N., OLMOS, F., POSSO, S.R., LEES, A.C., FIGUEIREDO, L.F.A., CARRANO, E., GUEDES, R.C., CESARI, E., FRANZ, I., SCHUNCK, F., PIACENTINI, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee—second edition. Ornithol. Res., 29:94–105. https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
), photographed, and georeferenced with the help of the Timestamp Camera® application (Susamp Infotech, Surat, India). The collected carcasses that were not crushed or in an advanced stage of decomposition were placed in sealed plastic bags and transported to the Institute of Technology and Research in a thermal bag for biometric and laboratory analyses.

In the laboratory, the birds were subjected to biometric measurement: total length (from the tip of the tail to the beak), wingspan (from the tip of the right wing to the tip of the left wing), and weight, for which a tape measure and electronic scale were used. Then, the carcasses were necropsied for organ removal and analysis, the gizzard contents were washed with running water, sieved, and classified with the help of a microscope and a stereomicroscope. The sieved content was stored in 70% ethyl alcohol.

All materials, without identification of origin, were weighed and then subjected to oxidative processing for organic material degradation. After the application of 20 mL of a 0.005 M aqueous solution of Fe II sulfate, used as a catalyst added to the solid residue, 20 mL of 35% hydrogen peroxide was added to the mixture. The material was kept at rest at room temperature for five minutes, and then mixed in a heated magnetic stirrer at 60°C for 30 minutes, covered with a watch glass. The solution was then sieved to remove the plastic fragments resulting from the oxidation process (Maynard et al. 2021MAYNARD, I.F.N., BORTOLUZZI, P.C., NASCIMENTO, L.M., MADI, R.R., CAVALCANTI, E.B., LIMA, A.S., JERALDO, V.L.S., MARQUES, M.N. 2021. Analysis of the occurrence of microplastics in beach sand on the Brazilian coast. Sci. Total Environ., 771:144777. https://doi.org/10.1016/j.scitotenv.2020.144777.
https://doi.org/10.1016/j.scitotenv.2020...
). The plastic material obtained was subjected to Fourier Transform Infrared Spectroscopy (FTIR) on an Agilent FTIR Cary 630 spectrometer (Agilent Technologies Inc., Santa Clara USA), in a partner laboratory.

The metallic fragment found after cleaning the adhered organic material was weighed and subjected to a magnetism test.

For the present study, the project was authorized by the Biodiversity Authorization and Information System – SISBIO, under number 79209-1 and registered in the National System for Management of Genetic Heritage and Associated Traditional Knowledge – SisGen (registration ADDECD3).

Results

The stomach contents of four bird species, which were run over on the Sergipe stretch of the BR 325 highway, were analyzed: Crested Caracara – Caracara plancus (Miller, 1777) (Falconiformes, Falconidae), Smooth-Billed Ani – Crotophaga ani Linnaeus, 1758 (Cuculiformes, Cuculidae), Grey-Breasted Martin – Progne chalybea (Gmelin, 1789) (Passeriformes, Hirundinidae), and Common Pauraque – Nyctidromus albicollis (Gmelin, 1789) (Caprimulgiformes, Caprimulgidae). The species Cr. ani, P. chalybea, and N. albicollis had predominantly insect content, comprising eight orders and four families. Due to insect fragmentation, it was not possible to identify them at the species level.

The plastic residues found in the stomachs of N. albicollis, P. chalybea, and Cr. ani were similar to filaments and were classified as microplastics because they were smaller than 5 mm. However, due to the small size of the fragments, their weight could not be determined (Figure 1a).

Figure 1
Residues removed from the stomachs of Progne chalybea and Caracara plancus collected on the stretch of the BR-235 highway in Sergipe, Brazil, between January and June 2022. A) Microplastic residue removed from the stomach contents of Progne chalybea. B and C) Residues removed from the stomach of Caracara plancus: plastic material (B); metallic fragment (C).

The plastic residue fragments removed from the stomach of C. plancus were classified as macroplastics (above 5 mm) (Figure 1b), weighing 0.982 mg, and the metallic fragments were characterized as similar to aluminum, non-magnetic, weighing 0.0102 mg (Figure 1c).

The plastic residue found in C. plancus, according to spectroscopic analysis, presented waves of 3.400 cm–1, 2.200–2.840 cm–1, 1.300–1.500 cm–1, with a spectrum similar to polypropylene (Figure 2).

Figure 2
Number of waves obtained from the plastic material removed from the stomach of Caracara plancus and subjected to Fourier Transform Infrared Spectroscopy (FTIR).

Discussion

The plastic content found in C. plancus was probably the main cause of the animal’s stomach distension, due to the entanglement of plastic and organic matter. The absence of apparent trauma in the body suggests that plastic may be associated with the animal’s death or vulnerability. The coloration of plastic residues has become an important topic to consider, as many species of animals are visual predators, that is, they forage selectively and are attracted to certain colors and shines (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. Mar. Pollut. Bull., 60:2275–2278. https://doi.org/10.1016/j.marpolbul.2010.08.007.
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, Chen et al. 2019CHEN, Q., ALLGEIER, A., YIN, D., HOLLERT, H. 2019. Leaching of endocrine disrupting chemicals from marine microplastics and mesoplastics under common life stress conditions. Environ. Int., 130:104938. https://doi.org/10.1016/j.envint.2019.104938.
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). Accordingly, blue and/or transparent plastic material represent the most commonly ingested by animals (Zhan et al. 2020ZHANG, D., CUI, Y., ZHOU, H., JIN, C., YU, X., XU, Y., LI, Y., ZHANG, C. 2020. Microplastic pollution in water, sediment, and fish from artificial reefs around the Ma’an Archipelago, Shengsi, China. Sci. Total Environ., 703:134768. https://doi.org/10.1016/j.scitotenv.2019.134768.
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, Carlin et al. 2020CARLIN, J., CRAIG, C., LITTLE, S., DONNELLY, M., FOX, D., ZHAI, L., WALTERS, L. 2020. Microplastic accumulation in the gastrointestinal tracts in birds of prey in central Florida, USA. Environ. Pollut., 264:114633. https://doi.org/10.1016/j.envpol.2020.114633.
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).

Caracara plancus has the most diverse diet among all 65 species of falconids, feeding on carcasses, arthropods (Formoso et al. 2019FORMOSO, A.E., AGÜERO, L., SAUTHIER, D.E.U. 2019. Diet of the Southern Caracara in a near-shore insular system in southern Patagonia, Argentina. J. King Saud Univ. Sci., 31:1339–1343. https://doi.org/10.1016/j.jksus.2018.10.001.
https://doi.org/10.1016/j.jksus.2018.10....
), vertebrates (Villalobos and Bagno 2012VILLALOBOS, M.P., BAGNO, M.A. 2012. Avian frugivores feeding on Mauritia flexuosa (Arecaceae) fruits in Central Brazil. Rev. Bras. Ornitol., 20:26–29.), in addition to consuming fruits, and may actively assist in seed dispersal (Paula et al. 2020PAULA, W.S., SOUZA, R.N., SANTOS, E.G. 2020. Fruit consumption and seed dispersal of Caryocar brasilense (Caryocaraceae) by Caracara plancus (Falconidae). Braz. J. Biol., 81:1127–1128. https://doi.org/10.1590/1519-6984.234498.
https://doi.org/10.1590/1519-6984.234498...
). The ingestion of plastic and metallic fragments by C. plancus generates various assumptions, such as the presence of this material in common foraging areas (Derraik 2002DERRAIK, J.G.B. 2002. The pollution of the marine environment by plastic debris: a review. Mar. Pollut. Bull., 44:842–852. https://doi.org/10.1016/S0025-326X(02)00220-5.
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, Foekema et al. 2013FOEKEMA, E.M., GRUIJTER, C., MERGIA, M.T., VAN FRANEKER, J.A., MURK, A.J., KOELMANS, A.A. 2013. Plastic in North Sea fish, Environ. Sci. Technol., 47:8818–8824. https://doi.org/10.1021/es400931b.
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), which may lead to its accidental ingestion during predation (Rossi et al. 2019ROSSI, L.C., SCHERER, A.L., PETRY, M.V. 2019. First record of debris ingestion by the shorebird American Oystercatcher (Haematopus palliatus) on the Southern coast of Brazil. Mar. Pollut. Bull., 138:235–240. https://doi.org/10.1016/j.marpolbul.2018.11.051.
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; D’Souza et al. 2020D’SOUZA, J.M., WINDSOR, F.M., SANTILLO, D., ORMEROD, S.J. 2020. Food web transfer of plastics to an apex riverine predator. Glob. Chang. Biol., 26(7):3846–3857. https://doi.org/10.1111/gcb.15139
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). Metal, in turn, can attract the bird’s attention due to the color or shine caused by the reflection of light (Holland et al. 2016HOLLAND, E.R., MALLORY, M.L., SHUTLER, D. 2016. Plastics and other anthropogenic debris in freshwater birds from Canada. Sci. Total Environ., 571:251–258. https://doi.org/10.1016/j.scitotenv.2016.07.158.
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; Seif et al. 2018SEIF, S., PROVENCHER, J.F., AVERY-GOMM, S., DAOUST, P.Y., MALLORY, M.L., SMITH, P.A. 2018. Plastic and non-plastic debris ingestion in three gull species feeding in an urban landfill environment. AECT, 74:349–360. https://doi.org/10.1007/s00244-017-0492-8.
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), some species of birds use materials with vibrant and metallic colors for ornamentation (Sergio et al. 2011SERGIO, F., BLAS, J., BLANCO, G., TANFERNA, A., LÓPEZ, L., LEMUS, J.A., HIRALDO, F. 2011. Raptor nest decorations are a reliable threat against conspecifics. Science, 331:327–330. https://doi.org/10.1126/science.1199422.
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).

The FTIR spectrum obtained in the analysis of the sample found in the stomach of C. plancus is similar to the spectrum of polypropylene, as presented in the work of Karthik et al. (2018)KARTHIK, R., ROBIN, R.S., PURVAJA, R., GANGULY, D., ANANDAVELU, I., RAGHURAMAN, R., RAMESH, R. 2018. Microplastics along the beaches of southeast coast of India. Sci. Total Environ., 645:1388–1399. https://doi.org/10.1016/j.scitotenv.2018.07.242.
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About 62% of all plastic products in the world are produced from polypropylene (PP) and polyethylene (PE) (Boenel et al. 2021BOENEL, M., VOBIS, G., SOLANS, M. 2021. Actinobacterias degradadoras de polipropileno. Rev. Int. Contam. Amb., 37:577–588. https://doi.org/10.20937/rica.54004.
https://doi.org/10.20937/rica.54004...
), polypropylene is a polymer widely used in various segments of industry, as it presents chemical, physical, and mechanical properties that allow its application in fabrics, films, bottles, food packaging, automotive products, among others (Maddah 2016MADDAH, H.A. 2016. Polypropylene as a promising plastic: a review. Am. J. Polym. Sci., 6:1–11. https://doi.org/10.5923/j.ajps.20160601.01.
https://doi.org/10.5923/j.ajps.20160601....
).

Progne chalybea and N. albicollis are exclusively insectivorous birds. P. chalybea captures insects in the air column (Sick 1997SICK, H. 1997. Ornitologia brasileira. Editora Nova Fronteira., Helms et al. 2016HELMS, J.A., GODFREY, A.P., AYMES, T., BRIDGE, E.S. (2016). Predator foraging altitudes reveal the structure of aerial insect communities. Sci. Rep., 6:1–10. https://doi.org/ 10.1038/srep28670.
https://doi.org/10.1038/srep28670...
) in short flights or during migration, and can feed on various types of insects during its life (Kelly et al. 2013KELLY, J.F., BRIDGE, E.S., FRICK, W.F., CHILSON, P.B. 2013. Ecological energetics of an abundant aerial insectivore, the Purple Martin. PLoS ONE, 8: e76616. https://doi.org/10.1371/journal.pone.0076616.
https://doi.org/10.1371/journal.pone.007...
). N. albicollis is a nocturnal bird that feeds during short flights from a perch. Both species have short and wide beaks, characteristics that allow foraging for insects during flight (Sick 1997SICK, H. 1997. Ornitologia brasileira. Editora Nova Fronteira.). The microplastic filaments found in the stomach contents analyzed in both species, due to their small size, may be associated with insects that, in some way (internal or external), transported the material from the anthropic area to eventual predation (Edo et al. 2021EDO, C., FERNÁNDEZ-ALBA, A.R., VEJSNÆS, F., VAN DER STEEN, J.J., FERNÁNDEZ-PIÑAS, F., ROSAL, R. 2021. Honeybees as active samplers for microplastics. Sci. Total Environ., 767:144481. https://doi.org/10.1016/j.scitotenv.2020.144481
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; Zhu et al. 2023ZHU, J., WU, P., ZHAO, N., JIANG, S., ZHU, H., JIN, H. 2023. Microplastics in terrestrial insects, long-horned beetles (Coleoptera: Cerambycidae), from China. Sci. Total Environ., 888:164197.).

Some studies explain contamination by microplastics in insectivorous birds through bioaccumulation, due to the fact that the annual production of plastics varied from 1.5 million tons in 1950 to 335 million tons in 2016 (Sá et al. 2018SÁ, L.C., OLIVEIRA, M., RIBEIRO, F., ROCHA, T.L., FUTTER, M.N. 2018. Studies of the effects of microplastics on aquatic organisms: what do we know and where should we focus our efforts in the future? Sci. Total Environ., 645:1029–1039. https://doi.org/10.3354/esr01017.
https://doi.org/10.3354/esr01017...
, Li et al. 2015LI, H.X., GETZINGER, G.J., FERGUSON, P.L., ORIHUELA, B., ZHU, M., RITTSCHOF, D. 2015. Effects of toxic leachate from commercial plastics on larval survival and settlement of the barnacle Amphibalanus amphitrite. Environ. Sci. Technol., 50:924–931. http://dx.doi.org/10.1021/acs.est.5b02781.
https://doi.org/10.1021/acs.est.5b02781...
), a factor that increases the dispersion of microplastics among habitats, facilitating the contamination of insects and their predators.

Ameixa et al. (2018)AMEIXA, O.M.C.C., SOARES, A.O., SOARES, A.M.V.M., LILLEBØ, A.I. 2018. Ecosystem services provided by the little things that run the world. In Selected Studies in Biodiversity (B. Şen, & O. Grillo, eds.). IntechOpen. p. 267–302. http://dx.doi.org/10.5772/intechopen.74847.
https://doi.org/10.5772/intechopen.74847...
categorize the ecosystem services provided by insects and the effects of contamination of these services by microplastics. In a study developed by Windsor et al. (2019)WINDSOR, F.M., RILLEY, R.M., TYLER, C.R., ORMEROD, S.J. 2019. Microplastic ingestion by riverine macroinvertebrates. Sci. Total Environ., 646:68–74. https://doi.org/10.1016/j.scitotenv.2018.07.271.
https://doi.org/10.1016/j.scitotenv.2018...
in Wales, specimens of Ephemeroptera from the families Baetidae and Heptageniidae and Trichoptera from the family Hydropsychidae were collected, showing concentrations of 0.14 microplastics per mg of tissue in 50% of the samples studied. Yang et al. (2015)YANG Y., YANG, J., WU, W.M., ZHAO, J., SONG, Y., GAO, L., YANG, R., JIANG, L. 2015. Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 1. Chemical and physical characterization and isotopic tests. Environ. Sci. Technol., 49:12080–12086. https://doi.org/10.1021/acs.est.5b02661.
https://doi.org/10.1021/acs.est.5b02661...
can also be cited for their results regarding the ability of Tenebrio molitor larvae to ingest expanded polystyrene plastic as its sole source of food.

Some insects are already using microplastics as a substrate for egg deposition (Goldstein et al. 2012GOLDSTEIN, M.C., ROSENBERG, M., CHENG, L. 2012. Increased oceanic microplastic debris enhances oviposition in an endemic pelagic insect. Biol. Lett., 8:817–820. http://dx.doi.org/10.1098/rsbl.2012.0298.
https://doi.org/10.1098/rsbl.2012.0298...
). Al-Jabaichi et al. (2019) observed mosquito larvae that, during aquatic larval development, ingested microplastic particles and remained with the material until the adult stage, thus transporting the material from water to air and soil, contaminating new environments. Larvae of the mosquito Culex pipiens, an insect with larval development in the soil, can consume microplastic particles of approximately 2 μm, which are transferred throughout the larval stages until the adult stage (Al-Jaibachi et al. 2018AL-JAIBACHI, R., CUTHBERT, R.N., ROSS, N., CALLAGHAN, A. 2018. Up and away: ontogenic transference as a pathway for aerial dispersal of microplastics. Biol. Lett., 14:20180479. https://doi.org/10.1098/rsbl.2018.0479.
https://doi.org/10.1098/rsbl.2018.0479...
).

Morelli et al. (2020)MORELLI, F., BENEDETTI, Y., MØLLER, A.P. 2020. Diet specialization and brood parasitism in cuckoo species. Ecol. Evol., 10:5097–5105. https://doi.org/10.1002%2Fece3.6263.
https://doi.org/10.1002%2Fece3.6263...
associates social parasitism with the dietary specialization of various species of Cuculiformes. However, Cr. ani does not show dietary specialization, feeding mainly on larger insects such as those of the Orthoptera order, eggs of other birds, small vertebrates (Repenning et al. 2009REPENNING, M, BASSO, H.C.P., ROSSONI, J.R., KRÜGEL, M.M., FONTANA, C.S. 2009. Análise comparativa da dieta de quatro espécies de cucos (Aves: Cuculidae), no sul do Brasil. Zoologia 26:443–453. https://doi.org/10.1590/S1984-46702009000300008.
https://doi.org/10.1590/S1984-4670200900...
), as well as fruits and seeds foraging the ground (Hughes 1997HUGHES, J.M. 1997. Cuculiformes: Cuculidae. Coccyzus minor (Mangrove Cuckooo). In The Birds of North America no. 299 (A. Poole & F. Gill, eds.). Cornell Laboratory of Ornithology. p.1–20.). In this study, this species presented plastic filaments in the stomach contents, and, because it is a generalist species, accidental plastic consumption may be facilitated.

Conclusion

The present study provides results on plastic polymer contamination in birds that are not well studied in this regard, since the group most affected by plastic ingestion is still that of seabirds. Caracara plancus and Cr. ani, due to their generalist feeding habits, are susceptible to the consumption of various inorganic materials. The polypropylene ingested by the birds in this study is used in the manufacture of grain bags, fertilizers, plastic films, packaging, among others, which may explain its presence in rural areas. Metals were also found in the stomach of C. plancus, and many bird species are attracted to shiny objects and collect them for nesting or ingestion.

The plastic materials found in the species P. chalybea and N. albicollis are a warning of the presence of microplastics in insects as well, suggesting a potential trophic transfer of this material throughout the food chain. Microplastics are transported between environments, as they are carried from aquatic environments to distant areas by insects or even by wind action, and considering that P. chalybea is a migratory and insectivorous bird, it can transport plastic materials for several kilometers, contaminating distant areas from the place of origin after the bird’s death or predation.

Therefore, there is a great need for expanding studies on the degree of microplastic dispersion in the wild and in synanthropic environments, on how this dispersion occurs, and on the degree of toxicity that plastic contamination causes in different taxonomic groups, as well as its influence on heterotrophic cycles.

Acknowledgments

The authors would like to acknowledge the collaboration of Álvaro Silva Lima, PhD, and Tairan Eutímio dos Santos, M.S., from the Food Analysis Laboratory (ITP), for their contributions to the FTIR Spectrophotometry analysis. They also would like to acknowledge Francisco José Zorzenon, M.S., from the Reference Unit of the Laboratory of Urban Pests, at the Biological Institute of São Paulo, for verifying the identification of insect fragments. DASB and JKSS acknowledge, respectively, the Coordination for the Improvement of Higher Education Personnel (CAPES – Financial Code 001) and the Brazilian National Council for Scientific and Technological Development (CNPq) for the scholarships granted. This work was financed with resources from the public notice CAPES/FAPITEC/SE n. 11/2016 PROEF.

Data Availability

Supporting data are available at: <https://data.scielo.org/dataset.xhtml?persistentId=doi:10.48331/scielodata.T8LQHM>.

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Edited by

Associate Editor
Carlos Joly

Publication Dates

  • Publication in this collection
    07 June 2024
  • Date of issue
    2024

History

  • Received
    30 Jan 2024
  • Accepted
    09 May 2024
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