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ISSN 1984-2961 (Electronic)
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Original Article
Braz J Vet Parasitol 2023; 32(4): e008323 | https://doi.org/10.1590/S1984-29612023055
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Metazoan parasites of Hoplias aff. malabaricus,
Trachelyopterus galeatus and Schizodon borellii (Osteichthyes)
from the Protected Area and its main tributary, Brazil
Metazoários parasitos de Hoplias aff. malabaricus, Trachelyopterus galeatus e
Schizodon borellii (Osteichthyes) da Área de Proteção Ambiental e seu principal
afluente, Brasil
Wagner Toshio Hasuike1,2* ; Gabriela Michelan1,2; Isabela Sales Quagliato3; Heleno Brandão3; Ricardo Massato Takemoto1,2
1Programa de Pós-graduação em Biologia Comparada, Universidade Estadual de Maringá – UEM, Maringá, PR, Brasil
2Núcleo de Pesquisa em Limnologia Ictiologia e Aquicultura – NUPELIA, Universidade Estadual de Maringá – UEM, Maringá, PR, Brasil
3Programa de Pós-graduação em Recursos Naturais e Sustentabilidade, Universidade Tecnológica Federal do Paraná – UTFPR,
Santa Helena, PR, Brasil
How to cite: Hasuike WT, Michelan G, Quagliato IS, Brandão H, Takemoto RM. Metazoan parasites of Hoplias aff. malabaricus,
Trachelyopterus galeatus and Schizodon borellii (Osteichthyes) from the Protected Area and its main tributary, Brazil. Braz J Vet Parasitol
2023; 32(4): e008323. https://doi.org/10.1590/S1984-29612023055
Received May 17, 2023. Accepted August 1, 2023.
*Corresponding author: Wagner Toshio Hasuike. E-mail: Hasuike.wt@gmail.com
Abstract
A study of the parasite-host interactions was conducted in the protected area popularly known as the
“Refúgio Biológico de Santa Helena” and its tributary, the São Francisco Falso River. For each of the three host species,
Schizodon borellii, Hoplias aff. malabaricus, and Trachelyopterus galeatus, 30 fish were collected from 2018 to 2019.
A total of 2172 parasites were identified among the three host species. Among these, the Monogenea class had the
highest number of species, with 26 taxa, followed by Copepoda with eight taxa, Digenea with six taxa, and Cestoda and
Nematoda with one taxon each. Eleven new records of infection/infestation were found among the host species such
as Urocleidoides paradoxus, Urocleidoides ramentacuminatus, Rhinoxenus arietinus, Mymarothecioides sp. (Monogenea),
Ergasilus cf. bryconis, Lernaea devastatrix, and Brasergasilus sp. (Copepoda) parasitizing S. borellii. Trinigyrus sp.,
Vancleaveus sp. (Monogenea), Gamispinus diabolicus (Copepoda) present in T. galeatus, and Gamidactylus jaraquensis
(Copepoda) present in H. aff. malabaricus. This study contributes to the record of parasite species occurrence in the
vicinity of a protected area and helps fill gaps in the knowledge of fish parasitic fauna in the Neotropical region.
Keywords: Helminths, crustaceans, Actinopterygii, Atlantic Forest, São Francisco Falso River.
Resumo
Foi realizado um estudo das interações parasitas-hospedeiros na área de proteção popularmente conhecida como
“Refúgio Biológico de Santa Helena” e seu afluente, o Rio São Francisco Falso. Para cada uma das três espécies
hospedeiras, Schizodon borellii, Hoplias aff. malabaricus e Trachelyopterus galeatus, foram coletados 30 peixes
entre 2018 e 2019. Foi identificado um total de 2.172 parasitos entre as três espécies hospedeiras. Dentre estes,
a classe Monogenea apresentou o maior número de espécies, com 26 táxons, seguida por Copepoda com oito
táxons, Digenea com seis táxons, e Cestoda e Nematoda com um táxon cada. Foram encontrados onze novos
registros de infecção/infestação entre as espécies hospedeiras tais como Urocleidoides paradoxus, Urocleidoides
ramentacuminatus, Rhinoxenus arietinus, Mymarothecioides sp. (Monogenea), Ergasilus cf. bryconis, Lernaea devastatrix e
Brasergasilus sp. (Copepoda) parasitando S. borellii. Trinigyrus sp., Vancleaveus sp. (Monogenea), Gamispinus diabolicus
(Copepoda) presentes em T. galeatus, e Gamidactylus jaraquensis (Copepoda) em H. aff. malabaricus. Este estudo
contribui para o registro da ocorrência de espécies de parasitos nas proximidades de uma área protegida,
e ajuda a preencher lacunas no conhecimento da fauna parasitária de peixes na região Neotropical.
Palavras-chave: Helmintos, crustáceos, Actinopterygii, Mata Atlântica, Rio São Francisco Falso.
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New records of parasites
Introduction
South America has the highest diversity of freshwater fish in the world (Reisetal., 2016; Birindelli & Sidlauskas, 2018).
The orders Characiformes and Siluriformes have the highest species richness, with approximately four thousand valid
species (Frickeetal., 2023). Hoplias aff. malabaricus Bloch, 1794, Schizodon borellii Boulenger, 1900 (Characiformes),
and Trachelyopterus galeatus Linnaeus, 1766 (Siluriformes) are commonly found in the Paraná–Paraguay River basins,
especially after the flooding of the Sete Quedas waterfall (Júlio etal., 2009; Reis etal., 2016; Ota etal., 2018;
Reisetal., 2020).
Fish have been on Earth for a long time compared to other vertebrates and have provided more niches for
invertebrates to conquer, being responsible for hosting more species of parasites than any other vertebrate
group (Thatcher, 2006). Over the years, several authors have attempted to estimate parasite biodiversity
and have estimated that one-third of the total species on Earth are parasites (Poulin & Morand, 2004;
Luqueetal., 2017).
Despite these uncertain estimates, efforts have been made in the form of catalogs on ictioparasitology in
the Neotropical Region, including those on Monogenea (Cohenetal., 2013), Digenea (Kohnetal., 2007), Cestoda
(Rego, 2000; Justoetal., 2017; Alvesetal., 2017), Nematoda (Moravec, 1998; Luqueetal., 2011), Acanthocephala
(Santosetal., 2008), Isopoda (Thatcher, 2000), Copepoda (Luqueetal., 2013), and all parasitological groups such
as the study by Eirasetal. (2010). Notably, these host species, such as S. borelli, have previously been studied in
other locations (Machadoetal., 1996; Lacerdaetal., 2007; Karlingetal., 2011; Karlingetal., 2014), and T. galeatus
(Pavanelli & Santos, 1990; Kohnetal., 2011; Yamadaetal., 2017; Yamadaetal., 2021) and H. aff. malabaricus, which
are considered the most studied hosts in various regions of Brazil (Giãoetal., 2020; Limaetal., 2022; Dinizetal., 2022;
Buenoetal., 2022; Duarteetal., 2023).
With increasing development of human activities, new challenges have emerged as mitigation
measures for biodiversity conservation arising from changes in the biotic and abiotic environments
(Kueffer & Kaiser-Bunbury, 2014). Areas created as environmental protection, is a way to keep intact this
diversity of organisms, and transform unmanaged lands into well-managed entities that maintain this diversity
(Rylands & Brandon, 2005). Conducting species surveys plays an important role in maintaining and understanding
this biodiversity, assisting in a geographical analysis or changes in the composition of the biota (Wilson, 1988).
With increasing research on global biodiversity in freshwater environments, it is becoming increasingly evident
that parasites are a fundamental part of this diversity. Thus, they have been the least quantified group of
organisms, despite playing fundamental roles as integral components of food webs and ecosystem functions, are
significant in quantity and richness, therefore, they should not be neglected (Marcogliese, 2004; Thatcher, 2006;
Laffertyetal., 2008; Timi & Poulin, 2020; Williamsetal., 2022).
Considering the lack of ictioparasitological studies in the protected area and its main tributary, the São Francisco
Falso River, this study aimed to provide the first record of parasite interactions with the hosts H. aff. malabaricus,
T. galeatus and S. borellii. In addition to providing parasitological and ecological data on parasite diversity in this
new study environment.
Material and Methods
Study area and host collection
The area of protection, referred to in the study region as the “Refúgio Biológico de Santa Helena”, was created
in 1984 and has an area of 1,482.05 hectares (142.1 km2) and a perimeter of 30 km (Kliver, 2010). According to the
same author, this ecosystem is located entirely in the municipality of Santa Helena, State of Paraná, and is isolated
by an excavated canal with a concrete bridge and a gate for controlling the entry and exit of people, thus making
it an artificial island.
The São Francisco Falso River was chosen to represent the area of influence of the aforementioned Conservation
Unit owing to its important contribution to the formation of the Itaipu Reservoir, which is one of the largest
floodplains in the municipality of Santa Helena, Paraná. This river has a watercourse of 127.04 km (Fronza, 2019),
an area of 1,554 km2, a perimeter of 227.62 km, and covers the municipalities of Céu Azul, Diamante do Oeste,
Matelândia, Ramilândia, Santa Helena, Santa Tereza do Oeste, São José das Palmeiras, São Pedro do Iguaçu, and
Vera Cruz do Oeste (Limaetal., 2015).
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New records of parasites
The fish species studied were selected because they had the highest numerical representation within the
collections. Thirty individuals of each fish species collected in the project were selected for parasitological studies.
Sampling points were distributed around the “Refúgio Biológico de Santa Helena” (RBSH) along the course of the
São Francisco Falso River (RSFF), totaling eight (8) sampling points (RBSH1: -24°51’15.12”S-54°21’21.12”W; RBSH2:
24°49’39.97”S-54°21’27.63”W; RBSH3: 24°48’30.50”S-54°21’5.33”W; RSFF1: 24°51’41.90”S-54°17’18.50”W; RSFF2:
24°53’14.14”S-54°13’6.60”W; RSFF3: 24°53’53.84” S-54°13’15.12”W; RSFF4: 24°53’18.56”S-54°13’30.32”W; RSFF5:
24°55’7.38”S-54°12’11.87”W) (Figure1).
Representative specimens of the fish were deposited in the fish collections of Nupélia: H. aff. malabaricus
(NUP:23044), S. borelli (NUP:23037), and T. galeatus (NUP:23107).
Parasitological analysis
The following infection/infestation sites were analyzed: nasal cavities, gill filaments, intestine, eyes, heart, urinary
bladder, and musculature. All host necropsy procedures, preservation, and parasite preparation were performed
according to Eirasetal. (2006).
Representative specimens were deposited at the Helminthological Collection of the Oswaldo Cruz Institute
(CHIOC) and the Helminthological Collection of the Institute of Biosciences at Unesp Botucatu (CHIB).
Data analysis
To test the sufficiency of the samples, the species accumulation curve was calculated using the iNEXT package
(Hsiehetal., 2016) was used. The ggplot2 package by (Wickham, 2016) was used to generate the parasite richness
graphs. The ecological descriptors (Abundance, Prevalence, Mean abundance and Mean intensity) were calculated
according to the method described by Bushetal. (1997). The parasitic diversity index was calculated using the
Brillouin calculation (HB), and the Berger–Parker index (d) was used for parasitic dominance. All analyses were
performed using the R software (R Core Team, 2020).
Figure 1. Brazilian map showing the sampling sites in the Refúgio Biológico de Santa Helena (RBSH) and Rio São Francisco Falso (RSFF),
State of Paraná. (QGIS Geographic Information System. Open Source Geospatial Foundation Project).
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New records of parasites
Results
In the study, 40 parasite taxa and 2172 specimens were found, divided among the groups (Monogenea, Digenea,
Cestoda, Nematoda, and Copepoda), present in the three host species analyzed in this study (see Tables1,2and3).
All host individuals were parasitized by at least one parasite species.
Although the available literature indicates that 30 individuals are adequate for parasitological studies, as shown
in Figure2, the species accumulation curve for S. borellii did not show stability, whereas the other two species
reached stability with the amount collected.
Among the host species, H. aff. malabaricus had the highest parasite richness, with 19 taxa, followed by S. borellii
with 14 taxa, and T. galeatus with nine taxa (Figure3).
The results obtained through the Brillouin index (HB) showed that H. aff. malabaricus had the highest diversity,
followed by T. galeatus and S. borellii. The Berger-Parker index (d) showed that T. galeatus had the highest species
dominance, followed by S. borellii and H. aff. malabaricus (Table4).
Table 1. Total diversity of parasite species found in the host: Schizodon borellii.
Parasite species SI A P (%) MA ± SE MII ± SE NIR
Monogenea
Jainus piava CHIOC- 39770 G 142 30.0 4.7 ± 16.8 15.7 ± 28.7
Urocleidoides paradoxus CHIOC- 39779 a-d G 24 16.6 0.8 ± 2.5 4.8 ± 4.8 X
Urocleidoides ramentacuminatus CHIOC-39780 a-d G 14 30.0 0.4 ± 0.8 1.5 ± 0.7 X
Rhinoxenus arietinus CHIOC- 39772 a-d NC 32 33.3 1.0 ± 2.6 3.2 ± 3.8 X
Tereancistrum parvus CHIOC- 39774 G 5 13.3 0.1 ± 0.4 1.25 ± 0.5
Tereancistrum paranaenses CHIOC- 39773 a-c G 3 10.0 0.1 ± 0.3 1.0
Mymarothecioides sp. G 7 3.3 0.2 ± 0.1 7.0 X
Dactylogyridae gen. sp.1 G 1 3.3 0.03 ± 0.1 1.0
Dactylogyridae gen. sp.3 G 45 30.0 1.5 ± 2.7 5.0 ± 2.8
Digenea
Austrodiplostomun compactum (metacercariae) CHIOC- 39771 E 1 3.3 0.03 ± 0.1 1.0
Copepoda
Gamispatulus schizodontis CHIBB 702L-703L NC 164 60.0 5.4 ± 8.8 9.1 ± 9.9
Ergasilus cf. bryconis G 16 20.0 0.5 ± 1.5 2.6 ± 2.7 X
Lernaea devastatrix CHIBB 693L; 694L e 695L G 6 13.3 0.2 ± 0.5 1.5 ± 0.5 X
Brasergasilus sp. NC 1 3.3 0.03 ± 0.1 1.0 X
SI: site of infection; G: gills; NC: nasal cavity; E: eyes; A: abundance; P (%): prevalence; MA: mean abundance; MII: mean intensity of infection;
SE: standard error; NIR: new infection/infestation record.
Table 2. Total diversity of parasite species found in the host: Trachelyopterus galeatus.
Monogenea SI A P (%) MA ± SE MII ± SE NIR
Cosmetocleithrum laciniantun CHIOC-39764 a-d G 622 90.0 20.7 ± 20.2 23 ± 20
Cosmetocleithrum baculum CHIOC-39766 a-d G 33 53.0 1.1 ± 1.5 2.0 ± 1.5
Cosmetocleithrum galeatum CHIOC- 39767 a-c G 68 66.6 2.2 ± 2.9 3.5 ± 3.0
Cosmetocleithrum spathulatum CHIOC- 39768 a-c G 318 93.0 10.6 ± 10.1 11.3 ± 10.1
Vancleaveus sp. G 2 6.6 0.06 ± 0.2 1.0 X
Trinigyrus sp. G 1 3.3 0.03 ± 0.1 1.0 X
Digenea
Microrchis oligovitellum CHIOC- 39765 a-b I 24 50.0 0.8 ± 0.9 1.6 ± 0.6
Cestoda
Cangatiella arandasi CHIOC-39769 I 3 10.0 0.1 ± 0.3 1.0
Copepoda
Gamispinus diabolicus CHIBB 704L-705L -706L NC 33 40.0 1.1 ± 1.8 2.7 ± 2.0 X
SI: site of infection; G: gills; NC: nasal cavity; I: intestine; A: abundance; P (%): prevalence; MA: mean abundance; MII: mean intensity of infection;
SE: standard error; NIR: new infection/infestation record.
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New records of parasites
Table 3. Total diversity of parasite species found in the host: Hoplias aff. malabaricus.
Monogenea SI A P (%) MA ± SE MII ± SE NIR
Anacanthorus sp.1 G 2 6.6 0.06 ± 0.2 1.0
Anacanthorus sp.2 G 1 3.3 0.03 ± 0.1 1.0
Anacanthorus sp.3 G 4 3.3 0.13 ± 0.5 2.0 ± 1.4
Urocleidoides brasiliensis CHIOC-39775 a-b G 8 10.0 0.26 ± 0.9 2.6 ± 2.0
Urocleidoides cuiabai CHIOC-39776 a-b G 151 73.0 5 ± 5.1 6.8 ± 4.8
Urocleidoides paranae CHIOC- 39778 a-d G 35 13.0 1.16 ± 4.9 8.7 ± 12.2
Urocleidoides naris CHIOC- 39777 a-f NC 6 10.0 0.2 ± 0.7 2.0 ± 1.7
Urocleidoides sp.1 G 82 70.0 2.8 ± 3.2 4.0 ± 3.2
Urocleidoides sp.2 G 8 6.6 0.2 ± 1.2 4.0 ± 4.2
Dactylogyridae gen.sp.1 G 15 13.0 0.5 ± 1.4 3.75 ± 1.5
Dactylogyridae gen.sp.2 G 66 50.0 2.2 ± 3.0 4.4 ± 3.0
Digenea
Austrodiplostomum compactum (metacercariae) CHIOC-39783 E 9 20.0 0.9 ± 0.7 1.5 ± 0.8
Clinostomum dimorphum (metacercariae) H/I 7 20.0 0.2 ± 0.5 1.1 ± 0.4
Clinostomum sp. (metacercariae) CHIOC -39784 I 2 6.6 0.06 ± 0.3 1.0
Phyllodistomum sp. CHIOC- 39786 a-b UB 8 10.0 0.2 ± 0.9 2.6 ± 2.0
Nematoda
Contracaecum sp. (larvae) CHIOC- 39785 I 10 13.0 0.2 ± 1.2 1.1 ± 3.0
Copepoda
Gamidactylus jaraquensis CHIBB 698L - 699L NC 43 53.0 1.4 ± 1.8 2.68 ± 1.8 X
Gamispatulus schizodontis CHIBB 700L - 701L NC 37 33.0 1.2 ± 2.7 3.7 ± 3.7
Lernaea devastatrix CHIBB 696L e 697L G 96 53.0 3.2 ± 5.1 6.0 ± 5.8
Lernaea devastatrix NC 7 20.0 0.2 ± 0.6 1.5 ± 0.8
SI: site of infection; G: gills; H: heart; NC: nasal cavity; I: intestine; UB: urinary bladder; E: eyes; A: abundance; P (%): prevalence; MA: mean abundance;
MII: mean intensity of infection; SE: standard error; NIR: new infection/infestation record.
Figure 2. Accumulation curve of parasite species by hosts collected.
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New records of parasites
Discussion
The Class Monogenea was the most expressive of the groups, with high parasite richness and abundance
(61.9% of the parasites found), which may be related to some factors, the environment in which their hosts live,
such as lakes or power plant reservoirs, which are characterized as lentic; thus, the specify, due their monoxenic
life cycle, the free-swimming larvae can find their host more easily (Lizamaetal., 2006). In addition, this group
is considered to be the richest and most diverse among fish parasites which are highly specific to their hosts
(Poulin & Morand, 2004; Kuchtaetal., 2020).
Crustaceans were the second most diverse group in this study, accounting for 19% of the samples. Among
the groups of metazoan parasites in freshwater fish, crustaceans Branchiura, Copepoda, and Isopoda stand
out for their importance and diversity (Tavares-Diasetal., 2015). These three groups represent a large part
of the parasitic crustacean fauna in the Neotropical region and deserve attention because they highly impact
their hosts which are found mainly in fish farms or natural environments (Pavanellietal., 2013). Ergasilids
represent the fourth largest family of freshwater copepods, with over 60 species in the freshwater region of
Brazil (Luqueetal., 2013). Among those found in this study, G. schizodontis has a generalist habit, as it occurs
in a variety of hosts and has been reported in four families: Anostomidae, Erythrinidae, Pimelodidae and
Serrasalmidae (Narciso & Silva, 2020).
Table 4. Brillouin index (HB) and Berger-Parker index (d), among the hosts species.
Host Brillouin index (HB) Berger-Parker index(d)
Schizodon borellii 0.45 ± 0.39 0.74 ± 1.22
Trachelyopterus galeatus 0.80 ± 0.25 2.41 ± 2.13
Hoplias aff. malabaricus 1.05 ± 0.39 0.37 ± 0.31
Figure 3. Total richness by parasite groups in each host species.
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New records of parasites
Digenea was the third most diverse group (14.3% of the samples found) and was the most recorded group
in helminthological survey studies (Pavanellietal., 1997; Takemoto et al., 2009; Lehunetal., 2020), as these
parasites exploit fish as intermediate or definitive hosts in their life cycle. A parasitological survey conducted by
Ramosetal. (2013) on infection and distribution of Austrodiplostomum compactum in Brazil, demonstrated that
there is a wide range of fish species that are parasitized by A. compactum, encompassing the orders Characiformes,
Perciformes, Siluriformes, and Gymnotiformes and, according to Yamadaetal. (2008), the parasite presents a
wide variety of intermediate hosts, thus presenting low specificity or “preference” to the various intermediate
hosts already recorded.
In host fish, the diversity and richness of parasites are influenced by the set of species present in the
environment, and most endoparasites are acquired by the trophic route, whereas the habitat, behavior, age,
and sex of the hosts are important for ectoparasite infestation (Guidellietal., 2003). The results obtained
from the low prevalence and abundance of some species of endoparasites found in this study are interesting,
and according to Overstreet (1997), the absence of parasites in a particular host indicates that the life cycle
of the parasite is impaired. In this case, transmission between the mollusk (first intermediate host) and fish
(second intermediate host) in the form of cercariae may not occur in this environment, making it impossible
to close the cycle.
The Brillouin’s index (HB) calculation results showed two important findings. First, S. borellii, in which parasitic
14 taxa were found, showed a lower HB index than the T. galeatus, in which nine taxa were found (see Table4).
The difference in the HB index is because some species, such as Dactylogyridae gen. sp.1 (Monogenea), A. compactum
(Digenea), and Brasergasilus sp. (Copepoda), occurred only once in the S. borellii sample and influenced the value
of the diversity index. Second, it may be related to the number of hosts collected; as shown in Figure2, the
sample number of the host S. borellii was not stabilized in the species accumulation curve and probably did not
demonstrate its real diversity. Hoplias aff. malabaricus was expected to have the highest parasite composition
(19 taxa), mainly if we considered the behavior and trophic level of the host, as addressed by Poulin & Leung (2011).
Species such as Vancleaveus sp. and Trinigyrus sp. (Monogenea) present in T. galeatus and Mymarothecioides
sp. (Monogenea) and Brasergasilus sp. (Copepoda) present in S. borellii had their first record of occurrence, but in
low abundance and prevalence (below 10%). According to Bushetal. (1990), this type of case can be considered
accidental if parasite indices are low. It is also important to highlight that this study is the first record of the occurrence
of the remaining species: Urocleidoides ramentacuminatus, U. paradoxus, Rhinoxenus arietinus (Monogenea),
Ergasilus cf. bryconis, Gamispinus diabolicus, Gamidactylus jaraquensis and Lernaea devastatrix (Copepoda). Thus, this
study contributes to the knowledge of the occurrence of these parasitic species in fish of the families Anostomidae,
Erythrinidae, and Auchenipteridae both in terms of their location and geographic distribution, providing new
information for future studies on parasite diversity.
Acknowledgements
The authors are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) – process
n. 402670/2016-7, for the support provided to the current study; to Instituto Chico Mendes de Conservação
da Biodiversidade (ICMBio), for authorizing the sample collection; to the Environmental Police of Santa Helena
County/ PR, for the support provided in scientific expeditions; to the members of Grupo de Estudo em Ictiologia
Neotropical (GEIN), and to Universidade Tecnológica Federal do Paraná – UTFPR, Santa Helena Campus, for providing
the infrastructure to develop the study.
The authors are also grateful to Núcleo de Pesquisa em Limnologia Ictiologia e Aquicultura-NUPELIA- Universidade
Estadual de Maringá-UEM, for providing the infrastructure for this work to be carried out. The authors are also
grateful to CAPES for the resources used in this work.
Ethics declaration
The fish species in this study were collected during the expeditions of the project entitled: “Levantamento
da Ictiofauna, Biologia Populacional, Dieta e Dispersão de Parasitos de Peixes na Área de Influência do Refúgio
Biológico de Santa Helena/PR” - Universal CNPq: 402670/ 2016-7, authorized by ICMBIO via SISBIO: no. 57181-1
and by the ethics and animal use committee of CEUA) of UTFPR under protocol number: 2016-031 and SISGEN
with registration number: A6AE4EF.
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Conflict of interest
The authors declare that they have no conflict of interest.
References
Alves PV, de Chambrier A, Scholz T, Luque JL. Annotated checklist of fish cestodes from South America. ZooKeys 2017; 650(650):
1-205. http://dx.doi.org/10.3897/zookeys.650.10982. PMid:28331385.
Birindelli JLO, Sidlauskas BL. Preface: how far has neotropical ichthyology progressed in twenty years? Neotrop Ichthyol 2018;
16(3): e180128. http://dx.doi.org/10.1590/1982-0224-20180128.
Bueno RMR, Leite LAR, Pelegrini LS, Abdallah VD, Azevedo RK. Biodiversity of the metazoan parasites of Hoplias malabaricus
(Bloch, 1794) from the Jacaré-Pepira River, Tietê-Jacaré River Basin, São Paulo State, Brazil. Bol Inst Pesca 2022; 48: e702.
http://dx.doi.org/10.20950/1678-2305/bip.2022.48.e702.
Bush AO, Aho JM, Kennedy CR. Ecological versus phylogenetic determinants of helminth parasite community richness.
Evol Ecol 1990; 4(1): 1-20. http://dx.doi.org/10.1007/BF02270711.
Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolisetal. revisited. J Parasitol 1997;
83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
Cohen SC, Justo MCN, Kohn A. South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro:
Oficina de Livros; 2013.
Diniz MFBG, Sousa WBB, Carvalho MNM, Yamada FH. Metazoan parasite community of Hoplias malabaricus
(Characiformes, Erythrinidae) in a stream of Caatinga domain, Brazil. Ann Parasitol 2022; 68(3): 453-460. http://dx.doi.org/10.17420/
ap6803.451. PMid:36502608.
Duarte R, Santos-Clapp MD, Brasil-Sato MC. Metazoan endoparasites of Hoplias malabaricus (Bloch, 1794) (Actinopterygii: Erythrinidae)
from upper and middle São Francisco river basin, Minas Gerais State, Brazil. Parasitol Res 2023; 122(2): 645-659. http://dx.doi.
org/10.1007/s00436-022-07768-1. PMid:36574009.
Eiras JC, Takemoto RM, Pavanelli GC, Adriano EA. Diversidade dos parasitas de peixes de água doce do Brasil. Maringá: Clichetec; 2010.
Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. 2nd ed. Maringá:
Eduem; 2006.
Fricke R, Eschmeyer WN, Van der Laan R. Eschmeyer’s catalog of fishes: genera, species, references [online]. San Francisco: California
Academy of Sciences; 2023 [cited 2023 Apr 15]. Available from: http://researcharchive.calacademy.org/research/ichthyology/
catalog/fishcatmain.asp
Fronza FL. Determinação do potencial erosivo do solo nas bacias dos rios São Francisco Falso e São Francisco Verdadeiro, região oeste
do estado do Paraná [thesis]. Medianeira: Universidade Tecnológica Federal do Paraná; 2019.
Gião T, Pelegrini LS, Azevedo RK, Abdallah VD. Biodiversity of parasites found in the trahira, Hoplias malabaricus (Bloch, 1794),
collected in the Batalha River, Tietê-Batalha drainage basin, SP, Brazil. An Acad Bras Cienc 2020; 92(2): e20180610. http://dx.doi.
org/10.1590/0001-3765202020180610. PMid:32556046.
Guidelli GM, Isaac A, Takemoto RM, Pavanelli GC. Endoparasite infracommunities of Hemisorubim platyrhynchos (Valenciennes,
1840) (Pisces: Pimelodidae) of the Baía River, Upper Paraná River floodplain, Brazil: specific composition and ecological aspects.
Braz J Biol 2003; 63(2): 261-268. http://dx.doi.org/10.1590/S1519-69842003000200011. PMid:14509848.
Hsieh TC, Ma KH, Chao A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol
2016; 7(12): 1451-1456. http://dx.doi.org/10.1111/2041-210X.12613.
Júlio HF Jr, Tós CD, Agostinho ÂA, Pavanelli CS. A massive invasion of fish species after eliminating a natural barrier in the upper
rio Paraná basin. Neotrop Ichthyol 2009; 7(4): 709-718. http://dx.doi.org/10.1590/S1679-62252009000400021.
Justo MCN, Fernandes BMM, Knoff M, Cárdenas MQ, Cohen SC. Checklist of Brazilian Cestoda. Neotrop Helminthol 2017; 11(1): 187-282.
Karling LC, Bellay S, Takemoto RM, Pavanelli GC. A new species of Jainus (Monogenea), gill parasite of Schizodon borellii
(Characiformes, Anostomidae) from the upper Paraná river floodplain, Brazil. Acta Sci Biol Sci 2011; 33(2): 227-231.
http://dx.doi.org/10.4025/actascibiolsci.v33i2.6168.
Karling LC, Lopes LPC, Takemoto RM, Pavanelli GC. New species of Tereancistrum (Dactylogyridae) monogenean parasites of
Schizodon borellii (Characiformes, Anostomidae) from Brazil, and emended diagnosis for T.parvus. Acta Sci Biol Sci 2014; 36(3):
365-369. http://dx.doi.org/10.4025/actascibiolsci.v36i3.20216.
Kliver SM. Plano de manejo área de relevante interesse ecológico Santa Helena ARIE-SH Refúgio Biológico Santa Helena RBSH. Santa
Helena: Nattural Engenharia Ambiental; 2010.
Braz J Vet Parasitol 2023; 32(4): e008323 9/10
New records of parasites
Kohn A, Fernandes BM, Cohen SC. South American trematodes parasites of fishes. Rio de Janeiro: Fundação Oswaldo Cruz; 2007.
Kohn A, Moravec F, Cohen SC, Canzi C, Takemoto RM, Fernandes BMM. Helminths of freshwater fishes in the reservoir of the
Hydroelectric Power Station of Itaipu, Paraná, Brazil. Check List 2011; 7(5): 681-690. http://dx.doi.org/10.15560/7.5.681.
Kuchta R, Řehulková E, Francová K, Scholz T, Morand S, Šimková A. Diversity of monogeneans and tapeworms in cypriniform fishes
across two continents. Int J Parasitol 2020; 50(10-11): 771-786. http://dx.doi.org/10.1016/j.ijpara.2020.06.005. PMid:32687912.
Kueffer C, Kaiser-Bunbury CN. Reconciling conflicting perspectives for biodiversity conservation in the Anthropocene. Front Ecol Evol
2014; 12(2): 131-137. http://dx.doi.org/10.1890/120201.
Lacerda ACF, Takemoto RM, Lizama MAP, Pavanelli GC. Parasitic copepods in the nasal fossae of five fish species (Characiformes) from
the upper Paraná River floodplain, Paraná, Brazil. Acta Sci Biol Sci 2007; 29(4): 429-435. http://dx.doi.org/10.4025/actascibiolsci.v29i4.887.
Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP,etal. Parasites in food webs: the ultimate missing links. Ecol Lett
2008; 11(6): 533-546. http://dx.doi.org/10.1111/j.1461-0248.2008.01174.x. PMid:18462196.
Lehun AL, Hasuike WT, Silva JOS, Ciccheto JRM, Michelan G, Rodrigues AFC,etal. Checklist of parasites in fish from the upper
Paraná River floodplain: an update. Rev Bras Parasitol Vet 2020; 29(3): e008720. http://dx.doi.org/10.1590/s1984-29612020066.
PMid:32935771.
Lima FS, Melo HPS, Camargo LMA, Takemoto RM, Menguetti DUO, Virgilio LR. Helminth parasites of Hoplias malabaricus
(Bloch, 1794) in areas of Brazilian Amazon with different degree of deforestation. Conjecturas 2022; 22(2): 460-484.
http://dx.doi.org/10.53660/CONJ-714-806.
Lima VR, Fujita DS, Fujita RH. Caracterização fluvio-morfométrica da Bacia Hidrográfica do Rio São Francisco Falso, estado do
Paraná. Rev Norte Cient 2015; 10(1): 71-86.
Lizama MAP, Takemoto RM, Pavanelli GC. Influence of the seasonal and environmental patterns and host reproduction on
the metazoan parasites of Prochilodus lineatus. Braz Arch Biol Technol 2006; 49(4): 611-622. http://dx.doi.org/10.1590/S1516-
89132006000500011.
Luque JL, Aguiar JC, Vieira FM, Gibson DI, Santos CP. Checklist of Nematoda associated with the fishes of Brazil. Zootaxa 2011;
3082(1): 1-88. http://dx.doi.org/10.11646/zootaxa.3082.1.1.
Luque JL, Pereira FB, Alves PV, Oliva ME, Timi JT. Helminth parasites of South American fishes: current status and characterization as
a model for studies of biodiversity. J Helminthol 2017; 91(2): 150-164. http://dx.doi.org/10.1017/S0022149X16000717. PMid:27855726.
Luque JL, Vieira FM, Takemoto RM, Pavanelli GC, Eiras JC. Checklist of Crustacea parasitizing fishes from Brazil. Check List 2013;
9(6): 1449-1470. http://dx.doi.org/10.15560/9.6.1449.
Machado MH, Pavanelli GC, Takemoto RM. Structure and diversity of endoparasitic infracommunities and the trophic level of
Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Mem Inst Oswaldo Cruz 1996; 91(4):
441-448. http://dx.doi.org/10.1590/S0074-02761996000400010. PMid:9070406.
Marcogliese DJ. Parasites: small players with crucial roles in the ecological theater. EcoHealth 2004; 1(2): 151-164. http://dx.doi.
org/10.1007/s10393-004-0028-3.
Moravec F. Nematodes of freshwater fishes of the Neotropical Region. Academia: Publishing House of the Academy of Sciences of
the Czech Republic; 1998.
Narciso RB, Silva RJ. Two Gamispatulus Thatcher & Boger, 1984 (Cyclopoida: Ergasilidae) from Schizodon intermedius Garavello &
Britski (Actinopterygii: Anostomidae), with description of a new species. Zootaxa 2020; 4803(3): 463-482. http://dx.doi.org/10.11646/
zootaxa.4803.3.3. PMid:33056005.
Ota RR, Deprá GC, Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised,
annotated and updated. Neotrop Ichthyol 2018; 16(2): e170094. http://dx.doi.org/10.1590/1982-0224-20170094.
Overstreet RM. Parasitological data as monitors of environmental health. Parassitologia 1997; 39(3): 169-175. PMid:9802064.
Pavanelli GC, Machado MH, Takemoto RM. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: Vazoller
AESM, Agostinho AA, Hahn NS, editors. A planície de inundação do alto Rio Paraná: aspectos físicos, biológicos e socioeconômicos.
Maringá: Eduem; 1997. p. 307-329.
Pavanelli GC, Santos MHM. Cangatiella arandasi, gen. n. sp. n (Cestoda-Proteocephalidae), parasito de Parauchenipterus
galeatus (Siluriformes-Auchenipteridae) do Rio Paraná, PR. Rev Bras Zool 1990; 7(4): 535-539. http://dx.doi.org/10.1590/S0101-
81751990000400012.
Pavanelli GC, Takemoto RM, Eiras JC. Parasitologia de peixes de água doce do Brasil. Maringá: Eduem; 2013.
Poulin R, Leung TLF. Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 2011; 166(3):
731-738. http://dx.doi.org/10.1007/s00442-011-1906-3. PMid:21249395.
Braz J Vet Parasitol 2023; 32(4): e008323 10/10
New records of parasites
Poulin R, Morand S. Parasite biodiversity. Washington: Smithsonian Institution; 2004.
Ramos IP, Franceschini L, Zago AC, Zica ÉOP, Wunderlich AC, Carvalho ED, etal. New host records and a checklist of fishes
infected with Austrodiplostomum compactum (Digenea: Diplostomidae) in Brazil. Rev Bras Parasitol Vet 2013; 22(4): 511-518.
http://dx.doi.org/10.1590/S1984-29612013000400010. PMid:24473875.
Rego AA. Cestode parasites of neotropical teleost freshwater fishes. In: Salgado-Madonado G, Aldrete ANG, Vidal-Martínez VM,
editors. Metazoan parasites in the Neotropics: a systematic and ecological perspective. Ciudad de México: Instituto de Biología de
la Universidad Nacional Autónoma de México; 2000. p. 135-154.
Reis RB, Frota A, Deprá GC, Ota RR, Graça WJ. Freshwater fishes from Paraná state, Brazil: an annotated list, with comments
on biogeographic patterns, threats, and future perspectives. Zootaxa 2020; 4868(4): 451-494. http://dx.doi.org/10.11646/
zootaxa.4868.4.1. PMid:33311378.
Reis RE, Albert JS, Di Dario F, Mincarone MM, Petry P, Rocha LA. Fish biodiversity and conservation in South America. J Fish Biol
2016; 89(1): 12-47. http://dx.doi.org/10.1111/jfb.13016. PMid:27312713.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing [software]. Vienna:
R Development Core Team; 2020 [cited 2020 Nov 23]. Available from: https://www.r-project.org/
Rylands AB, Brandon K. Brazilian protected areas. Conserv Biol 2005; 19(3): 612-618. http://dx.doi.org/10.1111/j.1523-
1739.2005.00711.x.
Santos CP, Gibson DI, Tavares LE, Luque JL. Checklist of Acanthocephala associated with the fishes of Brazil. Zootaxa 2008;
1938(1): 1-22. http://dx.doi.org/10.11646/zootaxa.1938.1.1.
Takemoto RM, Pavanelli GC, Lizama MDLA, Lacerda ACF, Yamada FH, Moreira LHA,etal. Diversity of parasites of fish from the
Upper Paraná River floodplain, Brazil. Braz J Biol 2009;69(2 Suppl): 691-705. http://dx.doi.org/10.1590/S1519-69842009000300023.
PMid:19738975.
Tavares-Dias M, Dias-Júnior MBF, Florentino AC, Silva LMA, Cunha AC. Distribution pattern of crustacean ectoparasites of freshwater
fish from Brazil. Rev Bras Parasitol Vet 2015; 24(2): 136-147. http://dx.doi.org/10.1590/S1984-29612015036. PMid:26154954.
Thatcher VE. Amazon fish parasites. Moscow: Pensoft Publishers; 2006.
Thatcher VE. The isopod parasites of South American fishes. In: Salgado-Madonado G, Aldrete ANG, Vidal-Martínez VM, editors.
Metazoan parasites in the Neotropics: a systematic and ecological perspective. Ciudad de México: Instituto de Biología de la Universidad
Nacional Autónoma de México; 2000. p. 193-226.
Timi JT, Poulin R. Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 2020; 50(10-11): 755-761. http://dx.doi.
org/10.1016/j.ijpara.2020.04.007. PMid:32592807.
Wickham H. Ggplot2: Elegant graphics for data analysis. Houston: Springer; 2016. https://doi.org/10.1007/978-3-319-24277-4_9.
Williams MA, Faiad S, Claar DC, French B, Leslie KL, Oven E,etal. Life history mediates the association between parasite abundance
and geographic features. J Anim Ecol 2022; 91(5): 996-1009. http://dx.doi.org/10.1111/1365-2656.13693. PMid:35332535.
Wilson EO. Biodiversity. Washington DC: National Academy of Sciences; 1988.
Yamada FH, Moreira LHA, Ceschini TL, Takemoto RM, Pavanelli GC. Novas ocorrências de metacercária de Austrodiplostomum
compactum (Lutz, 1928) (Platyhelminthes: Digenea) parasito de olhos de peixes da bacia do rio Paraná. Rev Bras Parasitol Vet
2008; 17(3): 163-166. http://dx.doi.org/10.1590/S1984-29612008000300010. PMid:19245765.
Yamada POF, Yamada FH, Silva RJ, Anjos LA. A new species of Cosmetocleithrum (Monogenea, Dactylogyridae), a gill parasite of
Trachelyopterus galeatus (Siluriformes, Auchenipteridae) from Brazil, with notes on the morphology of Cosmetocleithrum striatuli.
Comp Parasitol 2017; 84(2): 119-123. http://dx.doi.org/10.1654/1525-2647-84.2.119.
Yamada POF, Yamada FH, Silva RJ. Three new species of Cosmetocleithrum (Monogenea: Dactylogyridae) gill parasites of
Trachelyopterus galeatus (Siluriformes: Auchenipteridae) in Southeastern Brazil. Acta Parasitol 2021; 66(2): 436-445. http://dx.doi.
org/10.1007/s11686-020-00282-3. PMid:33074465.