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Water Air Soil Pollut (2021) 232:29

https://doi.org/10.1007/s11270-020-04964-6

Plastic Ingestion by Commercial and Non-Commercial


Fishes from a Neotropical River Basin
Felipe P. Lima & Valter M. Azevedo-Santos &
Viviane M. R. Santos & Ana P. Vidotto-Magnoni &
Cláudio L. Soares & Felipe V. Manzano &
André B. Nobile

Received: 30 August 2020 / Accepted: 21 December 2020


# The Author(s), under exclusive licence to Springer Nature Switzerland AG part of Springer Nature 2021

Abstract The pollution of Brazilian freshwater ecosys- belonging to five species contained plastic in their
tems by plastic began to appear in the scientific literature stomachs. The synthetic polymers were determined to
only in this century. We provide herein reports of plastic be polyethylene (PE) and polypropylene (PP). Three of
ingestion by members of the ichthyofauna in the Paraíba the species had not previously been reported to consume
do Sul River basin. Our study area comprised the plastic in natural ecosystems. In addition, at least three
Simplício Hydroelectric Complex, located in the middle of the five species are commercially valuable. Our work,
section of the Paraíba do Sul River. Fish specimens were together with other published records, raises to 46 the
caught with gillnets and the stomach contents examined number of Brazilian freshwater fish species known to
using a stereomicroscope and, when necessary, a com- have ingested plastic particles. Implementation of poli-
pound microscope. Out of a total of 218 individual cies at the river basin level are needed to avoid plastic
stomachs from 19 species examined, six individuals pollution in the Paraíba do Sul and tributaries in the
southeastern Brazil.

F. P. Lima : A. B. Nobile
Ictiológica Consultoria Ambiental ME-LTDA, Rua Primo Keywords Fourier-transformed infrared spectroscopy .
Paganini, 990 – Casa C, Botucatu, SP 18.608-190, Brazil Freshwater . Microplastic . Paraíba do Sul River .
Pollution . Stomach
V. M. Azevedo-Santos (*)
Universidade Estadual Paulista - UNESP, Departamento de
Zoologia, Instituto de Biociências, R. Prof. Dr. Antônio Celso
Wagner Zanin, 250 - Distrito de Rubião Junior, Botucatu, SP, 1 Introduction
Brazil
e-mail: valter.ecologia@gmail.com
Globally, animals are known to ingest synthetic polymers
V. M. R. Santos (Avery-Gomm et al. 2013; Denuncio et al. 2011;
Universidade Federal de Ouro Preto-UFOP, Departamento de Desforges et al. 2015; Lusher et al. 2015; Nelms et al.
Química, Instituto de Ciências Exatas e Biológicas, Campus
2016). Azevedo-Santos et al. (2019a) showed that fish
Morro do Cruzeiro, Ouro Preto, MG 354000-000, Brazil
representing many trophic guilds contained some type of
A. P. Vidotto-Magnoni plastic in their gastric systems. New reports of plastic
Departamento de Biologia Animal e Vegetal, Universidade ingestion by commercial and non-commercial freshwater
Estadual de Londrina – UEL, Rodovia Celso Garcia Cid - PR-445,
fish indicate continually increasing rates of occurrence
Km 380, Londrina, PR 86.057-970, Brazil
(e.g., Andrade et al. 2019; Urbanski et al. 2020). Consid-
C. L. Soares : F. V. Manzano ering the diversity of fishes (see Fricke and Eschmeyer
Furnas Centrais Elétricas S.A., Av. Graça Aranha, 26 - Centro, Rio 2020), and the high levels of plastic pollution in most
de Janeiro, RJ 20.030-000, Brazil
aquatic ecosystems (Blettler et al. 2018, 2019), we believe
29 Page 2 of 8 Water Air Soil Pollut (2021) 232:29

that the true number of freshwater fish species ingesting 2019), we hypothesized that fishes of the Paraíba do Sul
plastic is far greater than currently known. River basin are also ingesting plastic fragments. In this
The Paraíba do Sul River basin is located in a highly work, we record plastic particles in the stomachs of
populated and industrialized region including parts of commercially and ecologically important fishes of this
three southeastern Brazil states. Therefore, this basin is Neotropical River basin.
one of Brazil’s most imperiled. During collections in the
middle Paraíba do Sul River, we captured several plastic
fragments drifting in the river (A. B. Nobile et al. un-
published data). Based on the presence of these frag-
ments and motivated by several records of plastic inges-
tion by fishes in Brazilian waterbodies (e.g., Urbanski
et al. 2020; Silva-Cavalcanti et al. 2017; Andrade et al.

Fig. 1 Locations of fish collections in the Paraíba do Sul River basin


Water Air Soil Pollut (2021) 232:29 Page 3 of 8 29

2 Material and Methods 2.4 Analyses of Anthropogenic Fragments

2.1 Study Area To confirm the anthropogenic particles were plastic as


well as to determine their composition, we used Fourier-
The Paraíba do Sul River headwater is located in the transformed infrared spectroscopy (hereafter FTIR) with
Serra da Bocaina, southeastern Brazil (Pereira et al. spectra ranging from 500 to 4000 cm−1. For analysis, we
2006). The river flows ~1200 km east (Salomão et al. used a Thermo Scientific Nicolet 380 FTIR. The IR
2001), emptying into the Brazilian coast near the mu- spectra obtained and the main vibration bands were
nicipality of São João da Barra, Rio de Janeiro State reproduced through the Horizon program and used to
(Pereira et al. 2006). It passes through the municipality classify the chemical composition of each plastic particle.
of Volta Redonda, an urban area with a large steel plant, To determine the size of fragments found in the
as well as several other municipalities with chemical, stomachs, we followed Moore (2008), who classified
food, and textile industries that deliver untreated indus- particles < 5 mm as micro. We determined the color of
trial and urban effluents to the river (Araujo et al. 2003; the plastics visually, looking at the tonality that predom-
Pinto et al. 2006). For many years, the basin has been inated in the particle.
altered by local- and regional-extent anthropogenic
pressures and stressors (e.g., Araujo et al. 2003; Pinto
et al. 2006; Vitule et al. 2015). 3 Results
Our study area comprised the Simplício Hydroelec-
tric Complex (UHE Simplício-Queda Única), located in We examined the stomach contents of 218 specimens
the middle Paraíba do Sul River basin. The fourteen comprising 19 species (Table 1; Table S2). We found
sites were located in reservoirs and rivers (Fig. 1; six plastic particles (determined through FTIR) in the
Table S1). stomachs of six individuals belonging to the species

Table 1 Number of stomachs examined (NSE) and frequency of


occurrence (FO%) of stomachs with plastic fragments (see also
2.2 Fish Sampling
Table S2 and Table S3)

Fishes were collected from November 2016 to August Species NSE FO%
2017. Collections were conducted through an agreement
Astyanax cf. lacustris (Lütken 1875) 1 –
with the Instituto Brasileiro do Meio Ambiente e dos
Astyanax bimaculatus (Linnaeus 1758) 22 –
Recursos Naturais Renováveis (IBAMA). Individuals
were caught with gillnets (3 to 18-cm mesh between Psalidodon fasciatus (Cuvier 1819) 2 –
opposite knots). Nets were installed at the sites at dusk Geophagus brasiliensis (Quoy & Gaimard 1824) 1 –
and retrieved at dawn after fishing for 14 h. Hoplias malabaricus (Bloch 1794) 1 –
Hoplosternum littorale (Hancock 1828) 3 33.3
Hypostomus affinis (Steindachner 1877) 2 –
2.3 Gastric Analysis Hypostomus auroguttatus Kner 1854 1 100.0
Hypostomus sp. 1 –
For gastric analysis, a scalpel incision was made from Hypomasticus copelandii (Steindachner 1875) 6 –
the anus to the isthmus. Usually, when dissecting a fish, Megaleporinus conirostris (Steindachner 1875) 1 –
most of the stomachs are empty. Therefore, from the Oligosarcus hepsetus (Cuvier 1829) 36 –
specimens collected, we only examined stomachs with Pachyurus adspersus Steindachner 1879 2 –
food present. Afterwards, the stomach contents were Pimelodus fur (Lütken 1874) 27 –
transferred to Petri dishes and examined with a stereo- Pimelodus maculatus Lacepède 1803 61 3.3
microscope and, when necessary, a compound micro- Plagioscion squamosissimus (Heckel 1840) 26 3.9
scope. Possible plastics as well as natural organic matter Prochilodus lineatus (Valenciennes 1837) 2 –
were separated from each other visually and washed Rhamdia quelen (Quoy & Gaimard 1824) 5 –
with 70% ethanol, which enabled us to assess consump- Trachelyopterus striatulus (Steindachner 1877) 18 5.6
tion rates.
29 Page 4 of 8 Water Air Soil Pollut (2021) 232:29

Fig. 2 Plastic materials found among the stomach contents of fish species from the Paraíba do Sul River basin (see also Figure S1)

Hypostomus auroguttatus, Hoplosternum littorale, 4 Discussion


Pimelodus maculatus, Plagioscion squamosissimus,
and Trachelyopterus striatulus (Fig. 2; Table 1). Site We found plastic fragments in the stomachs of five fish
S10 presented three individuals that had ingested syn- species from the Paraíba do Sul River basin. Our
thetic polymers. Single individuals with plastic in the work — together with other published records
stomach were captured in sites S1, S8, and S9. Five of (Table 2) — elevate to 46 the number of Brazilian
the six fish with plastic fragments in the stomach were freshwater fish species known to ingest plastic particles.
captured in the reservoir region. We highlight that three species in our study (i.e.,
The fragments of synthetic polymers found in the fish Hypostomus auroguttatus, Plagioscion
stomachs were microplastics of four colors: blue (two squamosissimus, Trachelyopterus striatulus) had not
particles), green (two), gray (one), and pink (one) (Fig. been previously reported (sensu Azevedo-Santos et al.
2). We determined that the microplastics ingested were 2019a) as consuming plastic in natural ecosystems.
polyethylene (PE) and polypropylene (PP) (Figure S1). Previous reports exist only for Hoplosternum littorale,
Water Air Soil Pollut (2021) 232:29 Page 5 of 8 29

Table 2 Fish species reported to have ingested plastic particles in citations received by Andrade et al. (2019) and Silva-Cavalcanti
Brazilian freshwater ecosystems. The table is based on a search in et al. (2017). Orders and families of the species may be found in
the reference list of Azevedo-Santos et al. (2019a), new searches Table S3
following the methodology of the same authors, and consulting

Species Watershed Individuals Individuals with References


analyzed plastic in gastric
content

Acnodon normani Gosline 1951 Xingu 4 1 Andrade et al. (2019)


Aequidens tetramerus (Heckel 1840) Guamá 5 – Ribeiro-Brasil et al. (2020)
Astyanax lacustris (Lütken, 1875) Uruguay 61 11 Santos et al. (2020)
Bryconamericus aff. iheringii (Boulenger 1887) Ivaí 14 7 Garcia et al. (2020)
Bryconops melanurus (Bloch 1794) Guamá 5 – Ribeiro-Brasil et al. (2020)
Carnegiella strigata (Günther 1864) Guamá 5 – Ribeiro-Brasil et al. (2020)
Characidium aff. zebra Eigenmann 1909 Ivaí 5 1 Garcia et al. (2020)
Copella arnoldi (Regan 1912) Guamá 5 – Ribeiro-Brasil et al. (2020)
Crenicichla regani Ploeg 1989 Guamá 5 – Ribeiro-Brasil et al. (2020)
Curimatella lepidura (Eigenmann & Eigenmann 1889) Apodi-Mossoró 67 – Oliveira et al. (2020a)
Hemigrammus unilineatus (Gill 1858) Guamá 5 – Ribeiro-Brasil et al. (2020)
Hoplias malabaricus (Bloch 1794) Guamá 5 – Ribeiro-Brasil et al. (2020)
Hoplosternum littorale (Hancock 1828) Sorocaba; Pajeú 73 41 Oliveira et al. (2020b);
Silva-Cavalcante et al.
(2017)
Hypostomus ancistroides (Ihering 1911) Ivaí 9 2 Garcia et al. (2020)
Hypostomus cf. strigaticeps (Regan 1908) Ivaí 21 2 Garcia et al. (2020)
Iguanodectes rachovii Regan 1912 Guamá 5 – Ribeiro-Brasil et al. (2020)
Iheringichthys labrosus (Lütken, 1874) Uruguay 29 10 Santos et al. (2020)
Laimosemion strigatum (Regan 1912) Guamá 6 – Ribeiro-Brasil et al. (2020)
Mastiglanis cf. asopos Bockmann 1994 Guamá 5 – Ribeiro-Brasil et al. (2020)
Megalechis thoracata (Valenciennes 1840) Guamá 5 – Ribeiro-Brasil et al. (2020)
Metynnis guaporensis Eigenmann 1915 Xingu 11 3 Andrade et al. (2019)
Myloplus rhomboidalis (Cuvier 1818) Xingu 1 1 Andrade et al. (2019)
Myloplus rubripinnis (Müller & Troschel 1844) Xingu 15 2 Andrade et al. (2019)
Myloplus schomburgkii (Jardine 1841) Xingu 6 1 Andrade et al. (2019)
Nannacara taenia Regan 1912 Guamá 5 – Ribeiro-Brasil et al. (2020)
Ossubtus xinguense Jégu 1992 Xingu 19 10 Andrade et al. (2019)
Piabarchus stramineus (Eigenmann 1908) Ivaí 16 6 Garcia et al. (2020)
Pimelodella geryi Hoedeman 1961 Guamá 5 – Ribeiro-Brasil et al. (2020)
Polycentrus schomburgkii Müller & Troschel, 1849 Guamá 6 – Ribeiro-Brasil et al. (2020)
Pristobrycon cf. scapularis (Günther 1864) Xingu 14 6 Andrade et al. (2019)
Prochilodus brevis Steindachner 1875 Apodi-Mossoró 33 – Oliveira et al. (2020a)
Prochilodus lineatus (Valenciennes 1837) Tietê 32 23 Urbanski et al. (2020)
Psalidodon fasciatus (Cuvier 1819) Sorocaba 36 1 Oliveira et al. (2020b)
Psalidodon aff. paranae (Eigenmann 1914) Ivaí 30 8 Garcia et al. (2020)
Pygocentrus nattereri Kner 1858 Xingu 4 3 Andrade et al. (2019)
Rhamdia quelen (Quoy & Gaimard 1824) Sorocaba 5 2 Oliveira et al. (2020b)
29 Page 6 of 8 Water Air Soil Pollut (2021) 232:29

Table 2 (continued)

Species Watershed Individuals Individuals with References


analyzed plastic in gastric
content

Rineloricaria pentamaculata Langeani & de Araujo 1994 Ivaí 24 7 Garcia et al. (2020)
Serrasalmus eigenmanni Norman 1929 Xingu 6 2 Andrade et al. (2019)
Serrasalmus manueli (Fernández-Yépez & Ramírez 1967) Xingu 7 1 Andrade et al. (2019)
Serrasalmus rhombeus (Linnaeus 1766) Xingu 9 2 Andrade et al. (2019)
Tometes ancylorhynchus Andrade, Jégu & Giarrizzo 2016 Xingu 5 2 Andrade et al. (2019)
Tometes kranponhah Andrade, Jégu & Giarrizzo 2016 Xingu 63 12 Andrade et al. (2019)

from Brazilian waters, and Pimelodus maculatus, from Plastic ingestion by Paraíba do Sul River basin fishes
Argentina (Pazos et al. 2017; Silva-Cavalcanti et al. is likely a consequence of pollution from multiple urban
2017). Because this is not the first time that these two areas, indicating the need for a broad policy. In fact, it is
species were reported to have ingested plastic in fresh- insufficient for a city in the lower portion of the Paraíba
water ecosystems, we believe that both may exhibit the do Sul basin to adopt strict measures to avoid pollution
same behavior in other polluted rivers (e.g., Tietê) where if cities upriver do not do likewise. Similar to other
they occur. disturbances (Azevedo-Santos et al. 2019b), plastic
According to Markic et al. (2020), the absence of drifts downriver and fragments by abrasion, eventually
plastic in stomachs may be related to the low number of reaching areas where progressive pollution policies are
specimens examined (fewer than ten). We did not con- implemented (including coastal cities). Thus, plastic
firm plastic ingestion by several fish species (e.g., pollution requires implementation of actions (e.g., in
Geophagus brasiliensis, Hoplias malabaricus, Azevedo-Santos et al. 2021) across entire Paraíba do
Megaleporinus conirostris, Psalidodon fasciatus) in Sul River basin.
ou r stu dy. Fo r the se sp ec ies, howe ve r, w e
only examined a small number of stomachs (in some
Supplementary Information The online version contains sup-
cases only one; Table 1). Therefore, we recommend that
plementary material available at https://doi.org/10.1007/s11270-
new assessments in the Paraíba do Sul River basin 020-04964-6.
should occur and include more individuals of each
species, especially focusing on those that did not have
plastic particles in their stomachs in our study.
When compared with fish species of other regions Acknowledgments We thank FURNAS Centrais Elétricas S.A.
for understanding the importance of disclosing environmental
(e.g., Amazon River basin; see Table 2), we found
consultancy data resulting from the analysis of biological material
relatively few individuals with plastic in their stomachs and ichthyofauna monitoring of UHE Simplício - Queda Única.
from the Paraíba do Sul River basin. However, the We wish to thank Robert M. Hughes and James A. Nienow, for a
species recorded herein are commercially important, critical revision of the manuscript.
such as H. auroguttatus, P. maculatus, and
Code Availability None.
P. squamosissimus (F. P. Lima et al. personal observa-
tion). Some studies have already shown that plastics are
harmful to fishes (Ding et al. 2018). Plastics have been Data Availability None.
reported to interfere with digestion, and can fill animal
stomachs with undigestible components that lead to Compliance with Ethical Standards
starvation or low growth (Sigler 2014). In addition, fine
Conflict of Interest The authors declare that they have no
particles can be transferred to muscle tissue (Zitouni conflict of interest.
et al. 2020), which could possibly impact human
consumers.
Water Air Soil Pollut (2021) 232:29 Page 7 of 8 29

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