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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e55913, enero-diciembre 2023 (Publicado Nov. 17, 2023)
Mercury concentration in larvae of Eustrongylides sp.
(Nematoda: Dioctophymatoidea) from fish of the Brazilian Amazon
Lincoln Lima Corrêa1*; https://orcid.org/0000-0002-6453-4824
Hérlon Mota Atayde1; https://orcid.org/0000-0001-8178-393X
Sandra Layse Ferreira Sarrazin2; https://orcid.org/0000-0002-2884-7655
Ricardo Bezerra de Oliveira2; https://orcid.org/0000-0003-4526-2146
1. Universidade Federal do Oeste do Pará – UFOPA. Avenida Vera Paz, s/n- Salé, CEP 68040-255, Santarém, Pará, Brazil;
lincorre@gmail.com (*Correspondence), herlon.atayde@ufopa.edu.br
2. Universidade Federal do Oeste do Pará – UFOPA. Instituto de Ciências da Educação – ICED. Av. Marechal Rondon
s/n, Caranazal, CEP 68040-070, Santarém, Pará, Brazil; sarrazin@ufpa.br, ricardo.oliveira@ufopa.edu.br
Received 19-VII-2023. Corrected 26-X-2023. Accepted 10-XI-2023.
ABSTRACT
Introduction: Chemical pollution represents a great concern to aquatic organisms, especially fish. Metals enter
the aquatic environment from a variety of sources, including natural biogeochemical cycles and anthropogenic
sources such as industrial and residential effluents, mining and atmospheric sources.
Objective: To describe the Eustrongylides sp. larvae and the interaction with their fish hosts as indicators of
mercury (Hg) contamination in the Brazilian Amazon, and the distribution of Hg in the internal organs of
fish species Hoplias malabaricus and Pygocentrus nattereri collected in oxbow lakes on the Tapajós River, in the
municipality of Santarém, in the state of Pará.
Methods: Total Hg was analyzed using the Direct Hg Analyzer - DMA-80. Concentrations of Hg in Eustrongylides
sp. were compared with those found in the tissues/organs of the hosts H. malabaricus and P. nattereri. Hg con-
centrations in the host/parasite system were statistically compared using Principal Component Analysis. The
bioconcentration factor (BCF) was calculated to assess the bioaccumulation capacity of metals in Eustrongylides
sp. larvae, comparing the concentration of Hg in the parasite with that accumulated in the musculature of
infected hosts.
Results: Hg concentrations in all tissues/organs analyzed were higher in the parasitic species Eustrongylides
sp. larvae when compared with those found in tissues/organs of H. malabaricus and P. nattereri. There was an
inversely proportional relationship, showing that when Eustrongylides sp. larvae are present, the concentration
in the parasite is higher than in the musculature of host fish H. malabaricus and P. nattereri. The BCF of Hg was
found by comparing Eustrongylides sp. larvae/H. malabaricus muscle and was observed during a flood (BCF Hg
= 15 364).
Conclusions: The results confirm the greater bioaccumulative capacity of Eustrongylides sp. compared to its
host. The data indicated the viability of using Eustrongylides sp. larvae in biomonitoring programs. It is worth
mentioning that fish samples for Hg analysis must be free of parasites since their presence can alter the results.
Key words: fish parasites; Tapajós river; bioaccumulator parasite; heavy metals; pollution.
https://doi.org/10.15517/rev.biol.trop..v71i1.55913
AQUATIC ECOLOGY
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e55913, enero-diciembre 2023 (Publicado Nov. 17, 2023)
INTRODUCTION
The fish species Hoplias malabaricus,
known in Brazil as “Traíra” belongs to the
Erythrynidae family with three genera of Char-
aciformes: Erythrinus Scopoli, 1777, Hopleryth-
rinus Gill, 1896, and Hoplias Gill, 1903 (Nelson,
2006). They are carnivores (piscivores) and are
fish widely distributed in the Neotropics, found
in all Brazilian states, covering all watersheds in
South America. This genus can efficiently adapt
to different environmental conditions (Bialetz-
ki et al., 2008). The genus Hoplias comprises
two complexes of species: the Hoplias lacerdae
group, with nine species: Hoplias brasilien-
sis, Hoplias aimara, Hoplias patana, Hoplias
teres Hoplias intermedius, Hoplias microlepis,
Hoplias macrophthalmus, Hoplias australis, and
Hoplias curupira; and the Hoplias malabari-
cus group which, based on cytogenetic and
molecular biology studies, has also been con-
sidered a species complex (Jacobina et al.,
2011; Marques et al., 2013; Santos et al., 2009;
Vitorino et al., 2011).
Another freshwater species, abundant and
widely consumed by riverside populations, is
the Pygocentrus nattereri, known as “Piranha-
caju” or “Piranha-vermelha”. It has a carnivo-
rous food preference from the Serrasalmidae
family, a native, non-endemic, and epiconti-
nental species. They have a reddish color, with
a grayish head and back, and some articles
even record individuals up to 50 cm. Among
the numerous species of Amazonian fish, P.
nattereri stands out for its economic inter-
est in extractive fishing, handicraft making,
aquarium hobby, and the sale of industrialized
products, such as dehydrated piranha soup.
The species P. nattereri has the characteristic
of fish from the Amazonian floodplains due to
RESUMEN
Concentración de mercurio en larvas de Eustrongylides sp. (Nematoda: Dioctophymatoidea)
en peces de la Amazonía brasileña
Introducción: La contaminación química del hábitat acuático representa un gran peligro para organismos acuáti-
cos, especialmente para peces. Los metales ingresan al ambiente acuático desde una variedad de fuentes, incluidos
los ciclos biogeoquímicos naturales y fuentes antropogénicas, como efluentes industriales y residenciales, minería
y fuentes atmosféricas.
Objetivo: Describir las especies de Eustrongylides sp. y la interacción con sus peces hospederos como indicadores
de contaminación por mercurio en la Amazonía brasileña, y la distribución en los órganos internos de las especies
de peces Hoplias malabaricus y Pygocentrus nattereri recolectadas en cochas del Río Tapajós, en el municipio de
Santarém, del estado de Pará.
Métodos: El Hg total se analizó utilizando el Direct Hg Analyzer - DMA-80. Las concentraciones de Eustrongylides
sp. se compararon con las encontrados en los tejidos/órganos de los hospederos H. malabaricus y P. nattereri. Las
concentraciones en el sistema hospedero/parásito se compararon estadísticamente utilizando el análisis de com-
ponentes principales. Se calculó el factor de bioconcentración (BCF) para evaluar la capacidad de bioacumulación
de metales en larvas de Eustrongylides sp., comparando la concentración en el parásito con la acumulada en la
musculatura de los hospederos infectados.
Resultados: Las concentraciones de Hg en todos los tejidos/órganos analizados fueron mayores en las larvas
de la especie parasitaria Eustrongylides sp. en comparación con las encontradas en los tejidos/órganos de H.
malabaricus y P. nattereri. Hubo una relación inversamente proporcional, mostrando que cuando las larvas de
Eustrongylides sp. están presentes, la concentración en el parásito es mayor que en la musculatura de los peces
hospederos H. malabaricus y P. nattereri. El BCF de Hg se encontró comparando Eustrongylides sp. larvas/ mús-
culo H. malabaricus y se observó durante una inundación (BCF Hg = 15 364).
Conclusiones: Los resultados confirman la mayor capacidad bioacumulativa de Eustrongylides sp. en compara-
ción con su hospedero. Los datos indicaron la viabilidad de utilizar larvas de Eustrongylides sp. en programas de
biomonitoreo. Cabe mencionar que las muestras de pescado para análisis de Hg deben estar libres de parásitos ya
que su presencia puede alterar los resultados.
Palabras clave: parásitos de peces; río Tapajós; parásito bioacumulador; metales pesados; contaminación.
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its abundance in scientific fish samplings, thus
being used as an indicator of the stability of
these environments (Freitas & Siqueira-Souza,
2009; Murrieta-Morey & Malta, 2016; Silva et
al., 2014; Siqueira-Souza & Freitas, 2004).
According to studies by Thatcher and
Brites-Neto (1994), adult nematodes that para-
sitize fish inhabit the digestive tract or body
cavities, while in the larval stage, they infect
the muscles. There are four larval stages before
the adult and, in the case of parasitic forms of
fish, the last three are parasitic (Thatcher &
Brites-Neto, 1994). Birds, fish, amphibians, and
reptiles are hosts for nematodes of the genus
Eustrongylides, with birds being definitive hosts
and the others being intermediate or paratenic
hosts (Benigno et al., 2012; Moravec & Kohn,
1993). According to Eiras et al. (2016), these
helminths have zoonotic potential in Brazil, but
no reports have been described in Brazilian ter-
ritory (Barros et al., 2006; Benigno et al., 2012;
Eiras et al., 2018; Fontenelle et al., 2016). Larvae
can be in subcutaneous tissues, liver, mesentery,
and between muscle fibers (Melo et al., 2016).
Pollution directly interacts with parasitism
in complex ways, making it difficult to describe
its effects on disease (Lafferty, 1997). This
interaction becomes clearer in reviews of fish
parasites (Williams & Mackenzie, 2003). Some
pollutants are toxins, which can harm both the
host and its parasites’ immune systems. Some
may even preferentially show higher concen-
trations in parasite tissues than in hosts (Sures,
2008a). However, observations contrary to this
have also been made (Andrews et al., 1988).
These possibilities lead to a diverse set of pre-
dictions about the effect of toxic pollutants on
parasites (Sures et al., 1999).
Specific predictions for some parasites and
pollution are possible. Fish parasites provide
information about water pollution through
both their presence or absence and the para-
sites’ capacity to accumulate heavy metals in
tissues, mainly arsenic, copper, lead, zinc, and
cadmium (Sures & Taraschewski, 1995). Intes-
tinal parasites like Proteocephalus percae and
Acanthocephalus lucii have this ability; their
tissues contain 300 times more of these toxins
than the muscles and liver of their host fish.
The principal source of mercury, Hg, con-
tamination for humans is the intake of fish and
other aquatic organisms. Hg present in fish is
approximately 90 % in the form of methylmer-
cury (MeHg). MeHg is the most toxic chemical
form of Hg for living beings (Crespo-Lopez et
al., 2021). In the Amazon and mainly in the
region surrounding the Tapajós River basin,
the presence of MeHg in fish that commonly
feeds the population has been shown (Lino et
al., 2018). Thus, monitoring MeHg in fish is of
fundamental importance for understanding the
contamination levels in the environment and
humans by this metal.
When ingested, fish can be a relevant vehi-
cle for heavy metal transmission. Some studies
(Albuquerque et al., 2021; Alcala-Orozco et
al., 2020; da Silva-Costa et al., 2022; Lima et
al., 2015; Silva et al., 2019) in fish from Ama-
zonian environments, including in specimens
consumed by indigenous communities (Vas-
concellos et al., 2021), point to the detection
of worrying levels of these metals in species of
commercial interest. Human contamination
by fish gains importance when considering
the preference of Amazonians for this protein
source, to the detriment of others (Barreto-Sa
et al., 2019; Haddad-Junior et al., 2021; Lino et
al., 2018; Lopes et al., 2016). The present study
is the pioneer in describing Eustrongylides sp.
larvae (Nematoda: Dioctophymatoidea) and
the interaction with their fish hosts as indica-
tors of the accumulation of contamination by
HgT (Total Mercury) in the Brazilian Amazon.
It also describes the distribution of HgT in the
internal organs of fish of the species Hoplias
malabaricus and Pygocentrus nattereri collect-
ed, mainly in oxbow lakes in Rio Tapajós, in the
municipality of Santarém, in the state of Pará,
which is a place that suffers negative impact of
anthropic actions due to gold mining above the
Tapajós River, consequently, carrying it to the
area where the collections took place.
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MATERIALS AND METHODS
Collection Location: Fish were collected
by fishing in oxbow lakes of tributaries of
the Tapajós River, in the Amazon Basin, near
the Alter do Chão district of the municipal-
ity of Santarém-Pará, coordinates (2°17’46”
S; 54°53’47.74” W - Quantum GIS version
3.14.15, QGIS Development Team, 2020)
(Fig. 1). Gillnets measuring 30 m in length and
2.5 m in height, and with a mesh size of 30, 35
and 40 mm between knots were used to capture
the fish, along with bait. Collections occurred
concurrently to compare data obtained in two
fish species (H. malabaricus and P. n at t e r -
eri) from the same environment (Fig. 2C, Fig.
2D). The collections took place throughout
the year 2022. Sixteen specimens of H. mala-
baricus and 24 specimens of P. nattereri were
captured. These specimens were obtained in
two hydrological periods: in winter (character-
ized as high waters), collected in the month of
April (six specimens of H. malabaricus and 14
P. nattereri), and in summer (characterized as
dry waters), collected in December (ten speci-
mens of H. malabaricus and ten P. nattereri).
After collection, fishes were euthanized using
clove oil (150 mg/L diluted in water), their total
length (Tl, in centimeters) and whole weight (in
grams) were measured using (for the collection
of the total length, a measuring tape was used
and for the weight a scale was used), then fish
were dissected at the collection site, and sex
determined according to Vazzoler (1996).
Collection of parasites and organs: After
being anesthetized and euthanized, the fish
were examined under a stereomicroscope to
remove all Eustrongylides sp. larvae encapsulat-
ed in musculature (Fig. 2A, Fig. 2B), and these
were separated for the morphometric study.
For morphological identification, we exam-
ined ten specimens of parasites, which were
clarified according to Santin et al., (2009) and
studied by light microscopy, with magnifica-
tion from 100X to 400X, according to Moravec
Fig. 1. Map of Brazil, highlighting the Amazon River Basin. Geographic coordinates (2°17’46” S; 54°53’47.74” W - QGIS
version 3.14.15, QGIS Development Team, 2020).
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and Kohn (1993), after the preparation of
temporary slides. The photomicrographs were
processed in a Zeiss Axioplan microscope with
an Axiocam ERc 5s camera.
The ecological terms used, and the param-
eters of prevalence, abundance, and mean
intensity of infection were calculated according
to those proposed by Bush et al. (1997). These
parameters were calculated using Quantitative
Parasitology 3.0 software (Rozsa et al., 2000),
according to Reiczigel et al. (2019).
All Eustrongylides sp. larvae and the fol-
lowing fish organs (head, kidney, heart, liver,
spleen, small intestine, gonads, and muscles)
were frozen at -20 °C for HgT analysis. Muscle
samples were free of this type of parasite.
HgT analysis: Aliquots weighing between
0.01-0.05 g (wet weight) were analyzed for HgT
concentration. For such analysis, the Direct
Mercury Analyzer – DMA – 80 Tri cell (Mile-
stone – Italy) was used. To ensure the reliability
Fig. 2. A. Encapsulated and B. free larvae of Eustrongylides sp.; Host species, C. Hoplias malabaricus and D. Pygocentrus
nattereri.
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of the results, the certified reference material
BCR-463 Tuna Fish (SIGMA) was used, with
reference values of 2.85 ± 0.16 mgHg/kg and
obtaining values of 2.80 ± 0.07.
Calculation of the bioconcentration fac-
tor (BCF): The Hg bioconcentration factor
(BCF) evaluates the capacity of bioaccumula-
tion of the metal in larvae of Eustrongylides
sp. by comparing the concentration of HgT
accumulated in these larvae with that contained
in the musculature of infected specimens of
H. malabaricus and P. nattereri. The BCF esti-
mate was calculated and analyzed according
to (Schludermann et al., 2003; Sures, 2008b;
Sures et al., 1999). BCF was calculated using the
expressions: BCF = (C[parasite]/C[host tissue]).
Statistical analysis: Comparative analyzes
referring to HgT concentration in Eustron-
gylides sp. larvae related to that of the fish
organs (head kidney, heart, liver, spleen, small
intestine, gonads, and muscle), and between
oxbow lakes were conducted using Principal
Component Analysis (PCA). Spearman’s corre-
lation coefficient was used to test for significant
associations between HgT concentrations in
larvae and host tissues/organs. All statistical
tests were performed using the SPSS 8.0 pro-
gram (Tanaka & Mori, 1997).
RESULTS
Morphological characterization, based on
ten specimens of third instar larvae of Eustron-
gylides sp.: body of larvae filiform, yellow-
ish, 60.17-126.20 mm long and 0.65-1.39 mm
wide. Cuticles distinctly transversely striated.
Three cuticles visible in these stage four larvae:
external cuticle, from the second instar, mid-
dle cuticle from the third instar, and internal
cuticle from the fourth instar. Conical cephalic
extremity. Oral opening small, oval, surrounded
by 12 cephalic papillae arranged in two circles;
each circle formed by two lateral, two subdorsal
and two subventral papillae; inner circle papil-
lae smaller, with pointed apices. Pair of small
lateral amphids like somatic papillae located
immediately anterior to the lateral cephalic
papillae of the outer circle. Four small somatic
sublateral field papillae present between the
inner and outer circles of the cephalic papillae.
Oral cavity 1.77 mm long; esophageal length
12.53-20.15 mm and width 0.27-0.68 mm.
Nerve ring encircling esophagus 23.0-38.2 mm
from anterior end. Blunt posterior extremity,
with slightly elevated region of the anus. Male
larvae: developed caudal sucker with a small
cuticular border around the entire perimeter.
A wide, thick-walled genital tube (ejaculatory
duct) with circular muscles extending anteri-
orly from the rectum, usually with several coils.
Tube curving posteriorly near the esophageal-
intestinal junction and, after a short distance,
expanding into a large hologonic, blunt-ended
testis. Seminal vesicle ends just before the
genital tube. Spicule incompletely sclerotized.
Female larvae: genital primordium consisting
of four regions - thick-walled vagina composed
of cuboidal epithelium, wide genital tube, and
narrow uterus. The genital tube consists of
circular muscles and a thin, narrow lumen,
curving posteriorly and expanding into a large,
conical-tipped hologonic ovary.
Forty fish were collected altogether - 16
H. malabaricus (eight males and eight females)
and 24 P. nattereri (14 males and ten females),
with biometric data length/weight of 37.12 ±
9.99 cm / 528 ± 355.90 g, and 17.95 ± 1.64 cm /
167.83 ± 39.72 g, respectively (Fig. 2C, Fig. 2D).
The larvae Eustrongylides sp. described in this
study are all the third stage (L3). By the abso-
lute numerical distribution of larvae in 27 of
all the collected fish (67 %), the infection rates
obtained were as follows: prevalence of 63 %,
abundance of 1.77, and mean intensity of 2.81
larvae/fish. HgT concentrations found in the
tissues/organs of H. malabaricus and P. nattereri
and in Eustrongylides sp. larvae in hydrological
periods (drought and flood) are shown in Fig.
3 and Fig. 4.
HgT concentrations found in the tissues/
organs of the hosts H. malabaricus and P.
nattereri and the parasites, Eustrongylides sp.
larvae, in the hydrological periods (flood and
drought) are presented in Fig. 3 and Fig. 4.
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The concentrations of HgT were significantly
higher (P < 0.01) in the parasite species when
compared with that quantified in the tissues/
organs of the hosts. PCA showed that the high-
est concentration of parasites occurred in H.
malabaricus, and the highest concentration of
Hg occurred in the gonads of this species. The
second highest HgT index was detected in the
muscles of both fish species investigated here
(Fig. 4).
Spearman’s correlation coefficient (r)
was crucial to determine the significant rela-
tionships between HgT concentrations in
Eustrongylides sp. larvae and the muscles of
H. malabaricus and P. nattereri parasitized by
them. An inversely proportional relationship
was observed, demonstrating that the concen-
tration of the metal in these larvae is always
higher than that detected in the musculature
of these fish (r = -0.076; P ≤ 0.001) (Fig. 5).
The HgT BCF in Eustrongylides sp. larvae was
higher in H. malabaricus specimens collected in
the flood (BCFHg = 15 364).
DISCUSSION
Several studies have discussed the differ-
ent roles that parasitic fish species play in the
aquatic ecosystem. Previously, these organisms
were considered only as a threat to the health
of fish, but currently they have shown several
other functions, such as environmental bio-
indicators or sentinels of pollution of aquatic
Fig. 3. Total mercury (HgT) concentrations found in the
tissues/organs of Hoplias malabaricus and Pygocentrus
nattereri and in Eustrongylides sp. larvae during flood and
drought.
Fig. 4. Total mercury (HgT) concentrations (µg/kg) in the host/parasite system and its characterization by the Principal
Component Analysis (PCA). Highlighted in green are the tissue/organ mercury concentrations of the Hoplias malabaricus
components and in red are the tissue/organ mercury concentrations of the Pygocentrus nattereri components.
8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e55913, enero-diciembre 2023 (Publicado Nov. 17, 2023)
environments (Bush et al., 1997; Heckmann et
al., 2015; MacKenzie, 1999; Morsy et al., 2015;
Poulin, 1992; Santoro et al., 2020; Sures et al.,
1999; Williams and Mackenzie, 2003). Recent
studies have recorded the capacity of intestinal
fish parasites to accumulate high concentra-
tions of heavy metals in their tissues, mainly
species of the phylum Acanthocephala (Sures,
2007; Sures & Siddall, 2003; Vidal-Martínez et
al., 2010) and to a much lesser extent, the spe-
cies of Cestoda (Sures et al., 1999) and Nema-
toda (Morsy et al., 2015; Sures, 2003; Thielen
et al., 2004). Currently, the species of Acan-
thocephala are considered the most efficient
bioaccumulators of heavy metals. According to
Sures (2006), the performance of species from
other groups, such as Nematoda parasites of
fish, needs to be better known.
Studies described by Vidal-Martínez et al.,
(2010) analyzing the average level of lead (Pb)
accumulated in the tissues of the nematode
Anguillicoloides crassus (Kuwahara, Nimi and
Itagaki, 1974), a parasite of the swim bladder
of Anguilla anguilla (Linnaeus, 1758), recorded
that this was lower than what was found in its
host and realized that A. crassus could excrete
heavy metals from a proteinase that degrades
hemoglobin. Other studies carried out with
nematodes reported that the intestinal parasite
Raphidascaris acus (Bloch, 1779) accumulated
more iron (Fe) and zinc (Zn) (respectively, 68.4
and 86.9 times more) than the liver of its host
Esox Lucius ( Linnaeus, 1758) and that the lev-
els of lead (Pb), chromium (Cr) and cadmium
(Cd) in the nematode Philometra ovata (Zeder,
1803), an intestinal parasite, were 160, 431 and
119 times higher in the musculature of its host,
respectively (MacKenzie, 1999).
Studies focusing on HgT in Amazonian
fish have recently been described by Barbosa et
al., (2003) and Dórea et al., (2004). Neverthe-
less, analyses with Hg concentration in para-
sites, particularly Eustrongylides sp. larvae do
not exist in the scientific literature. Nematoda
larvae of the Anisakidae family (Railliet and
Henry, 1912) bioaccumulated lower concentra-
tions of lead (Pb) and copper (Cu) than the host
Dicentrarchus labrax (Linnaeus, 1758) (da Silva-
Costa et al., 2022). The present study showed
that Eustrongylides sp. larvae were all the third
stage (L3) and that their HgT concentrations
were higher than in the tissues/organs of the
H. malabaricus and P. nattereri hosts. The study
also showed that the ability of Eustrongylides
sp. to bioconcentrate HgT appears to be related
to the site where the host’s infection occurred.
However, the Eustrongylides sp. larvae in H.
malabaricus have a more evolved spoliation
mechanism since they accumulated more HgT
when compared to the Eustrongylides sp. larvae
of P. nattereri. However, other factors must be
involved, such as the development stage and the
feeding aspect of the host species.
The present study detected negative cor-
relation for the concentration of HgT, charac-
terizing it as bioaccumulated in Eustrongylides
sp. larvae when compared with muscle con-
centrations in H. malabaricus and P. nattereri
hosts. It seems that the time factor has not deci-
sively influenced the concentration of metals
in the Eustrongylides sp. larvae in that specific
case. This negative correlation observed can be
attributed to the kinetics of absorption and the
excretion of these metals in this species. Future
investigations should reach further elucidation.
Although the Eustrongylides sp. larvae ana-
lyzed contained high concentrations of HgT,
the reproducibility of individuals within the
host were not affected. It may suggest that
Fig. 5. Spearman’s correlation coefficient of total mercury
(HgT) concentrations in Eustrongylides sp. larvae, when
compared with concentration in the musculature of host
fish Hoplias malabaricus and Pygocentrus nattereri (r =
-0.076; P ≤ 0.001).
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these parasites have their own detoxification
mechanisms. Thus, further investigation and
data analysis on free life stages and their expo-
sure to mercury contamination is needed. The
results of the present study evidenced HgT
concentrations in the muscle and gonads of H.
malabaricus and P. nattereri, especially in the
latter organ, which had the highest concentra-
tion among all the organs analyzed. Regarding
the gonads/roe of Amazonian fish, scientific
articles rarely mention anything about con-
sumption habits. When this occurs, however,
there are no qualitative or quantitative details
such as preferred species or ingested quantities.
Eating roe is a common practice of the local
population, which means a higher transfer of
this heavy metal to consumer individuals.
Using parasites as bioaccumulators of
heavy metals is more efficient than using their
definitive hosts. Sures et al., (1999) report in
their study, that the parasitic species reduce
the levels of metals in the tissues of their hosts,
masking the actual results. The high BCF HgT
values found in the present study were similar
in both collection periods - flood and drought.
The highest values occurred in the dry season,
possibly due to the reduction of the flooded
area of the lakes and the consequent higher
accumulation of metals in the area. The data
obtained in the present study indicate that the
Eustrongylides sp. larvae have more efficient
mechanisms for capturing and accumulating
heavy metals than H. malabaricus and P. n a t -
tereri. This HgT uptake and bioaccumulation
kinetics by Eustrongylides sp. is still not well
known, but it was evident that the parasitic
species showed higher concentrations of HgT.
Thus, parasitic infections of fish must be
considered when using environmental moni-
toring programs. Otherwise, the levels of pol-
lutants in the hosts may, as investigated by
(Sures, 2008b), be erroneously detected and
therefore, can invalidate the model. This proce-
dure is essential to use the parasite/host system
in ecotoxicological studies. Data in the present
work indicate the importance of considering
the influence of fish parasite species in bio-
monitoring programs.
The present work showed the greater bio-
accumulative capacity of Eustrongylides sp.
compared to its host H. malabaricus and P. n a t -
tereri. This feature enabled it to be a potential
sentinel organism, which could provide reliable
information on pollution or the availability of
heavy metals in aquatic environments.
The present study is the first in the Ameri-
cas that used larvae of a parasitic nematode on
fish muscle as bioindicators of HgT accumu-
lation. The results showed the viability of its
use, mainly for biomonitoring sensitive aquatic
environments in the Brazilian Amazon. Other
studies of HgT concentration in fish also rec-
ommend verifying that analyzed fish tissue is
free of parasites since HgT concentration in
the nematodes can be higher than in fish tis-
sue. However, further studies on the kinetics of
HgT absorption in Eustrongylides sp. and fish
are needed.
Ethical statement: the authors declare that
they all agree with this publication and made
significant contributions; that there is no con-
flict of interest of any kind; and that we fol-
lowed all pertinent ethical and legal procedures
and requirements. All financial sources are fully
and clearly stated in the acknowledgments sec-
tion. A signed document has been filed in the
journal archives.
ACKNOWLEDGMENTS
The author Lincoln Lima Corrêa would
like to express his gratitude for the guaranteed
and financial support granted by the CAPES/
FAPESPA project N. 06/2015 - Process n°
88881.160660/2017-01. Sandra Layse Ferreira
Sarrazin would like to thank Fundação de
Amparo à Pesquisa no Pará- FAPESPA project
PPP/22.
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