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ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2021, 15(2), jul-dic:217-223.
RESEARCH NOTE / NOTA CIENTÍFICA
1
Universidade Federal do Maranhão, Pinheiro, Maranhão, Brazil.
2
Universidade Estadual do Maranhão, São Luís, Maranhão, Brazil.
3
Núcleo de Estudos Morfofisiológicos Avançados (NEMO), Universidade Estadual da Região Tocantina do Maranhão
(UEMASUL), Imperatriz, MA, Brazil.
*Corresponding author: danilo.correa@ufma.br
Márcia Mirella Silva Mello: https://orcid.org/0000-0001-6521-9175
Carine Almeida Miranda Bezerra: https://orcid.org/0000-0003-4842-1595
Diego Carvalho Viana: https://orcid.org/0000-0002-3302-9892
Danilo Francisco Corrêa Lopes: https://orcid.org/0000-0001-8711-3881
12
Márcia Mirella Silva Mello; Carine Almeida Miranda Bezerra;
31*
Diego Carvalho Viana & Danilo Francisco Corrêa Lopes
ABSTRACT
Between March and July 2019, 11 fish belonging to the species
Cichlasoma zarskei
Ottoni, 2011 (Acará),
Serrasalmus aff. rhombeus
Linnaeus, 1766 (Piranha),
Trachelyopterus galeatus
Linnaeus, 1766
(Bagrinho) and
Hoplias malabaricus
Bloch, 1794 (Traíra) in the Pericumã river basin, Maranhão, Brazil
were evaluated. Stomach, intestine and eye samples were taken for parasite analysis. Parasites belonging
to the groups were identified: nematodes, genus
Contracaecum
sp.; Cystacanth of acantocephala; and
larva of cestoda. In this research it was possible to report new associations in the host-parasite
relationship, such as the first record of the genus
Contracaecum
sp. in the species
C. zarskei
, a parasite that
presents zoonotic potential when infected raw or undercooked fish is consumed. The knowledge about the
parasitofauna of the fish community in the Pericumã river basin, Maranhão, Brazil is expanded through
this study, with the registration of new species of helminths described for the region.
Neotropical Helminthology
217
doi:10.24039/rnh20211521280
IDENTIFICATION OF PARASITIC FAUNA IN FISHES OF THE PERICUMÃ RIVER BASIN IN THE
STATE OF MARANHÃO, BRAZIL
IDENTIFICACIÓN DE LA FAUNA PARASITARIA EN PECES DE LA BACIA DEL RIO PERICUMÃ
EM EL ESTADO DE MARANHÃO, BRASIL
D
D
D
D
Keywords
: Brazil -
Contracaecum
– Endoparasite – Maranhão – Nematoides – Zoonoses
image/svg+xml
218
Brazil has a large variety of fish species,
accounting for approximately 20% of all
freshwater fishes in the world and 55% of
freshwater fishes in the neotropical region. The
country has a greater diversity of families of
endemic freshwater fishes compared to families of
marine fishes, with an estimated 2600 to 3100
species belonging to families that only inhabit
freshwater environments (Reis
et al
., 2003;
Buckup
et al
., 2007; Froese & Pauly, 2019). In the
state of Maranhão (northeast region of Brazil),
studies have addressed the parasitism of fishes in
natural and artificial (farms) environments, but few
studies conducted in the state have investigated the
parasite-host relationship and associated diseases
in fishes (Bezerra
et al
., 2020; Nascimento
et al
.,
2021). In the region known as the Maranhense
Lowlands in the state of Maranhão, fishes are part
of the diet of the population and many local
communities depend on the production and sale of
catches as the principal means of supporting the
family, demonstrating the economic importance of
the activity (Bernadi, 2005). In this context,
parasites of these fishes can cause high mortality
rates, reducing the size of the landings and the
commercial value of the catch (Bastos-Gomes
et
al
., 2017).
Despite the importance of fishing activities and the
occurrence of parasites of fishes of economic
interest, few investigations have addressed the
parasitic fauna of freshwater fishes in the region of
INTRODUCTION
the Maranhense Lowlands (Rodrigues
et al
., 2017).
Thus, studies on the ecology, morphology and
zoonotic potential of fish parasites are needed.
The aim of the present study was to characterize the
parasitic fauna of the species
Cichlasoma zarskei
Ottoni, 2011,
Serrasalmus aff. rhombeus
Linnaeus,
1766,
Trachelyopterus galeatus
Linnaeus, 1766
and
Hoplias malabaricus
Bloch, 1794 from the
Pericumã River in the Maranhense Lowlands, state
of Maranhão, Brazil.
This study was conducted in the main channel of
the Pericumã River in the state of Maranhão,
Brazil, at three points where artisanal fishing is
performed: Cachoeira – P1 (coordinates:
2°41'13.15" S 45°7'14.78" W); Juçareira – P2
(2°30'28.22" S 45°4'26.04" W); and Comporta – P3
(2°27'53.08" S 45°1'56.38" W). A total of 81
individuals were acquired from local fishermen
between March and July 2019. The individuals
were packed in ice and sent to the Environmental
Chemistry Lab (AMBIO) of the Fishery
Engineering Department of Universidade Federal
do Maranhão (UFMA), Pinheiro campus, where
data were collected from each individual on total
length (TL), standard length (SL) and total weight
(WT). The project received authorization from the
SISBIO Authorization and Information System in
Biodiversity (process number: 58236). Parasites
were collected using the method established by
RESUMEN
Palavras-Chave
: Brasil –
Contracaecum
– Endoparásito – Maranhão – Nematodes – Zoonosis
Entre marzo y julio de 2019, 11 peces pertenecientes a las especies
Cichlasoma zarskei
Ottoni, 2011
(Acará),
Serrasalmus aff. rhombeus
Linnaeus, 1766 (Piranha),
Trachelyopterus galeatus
Linnaeus, 1766
(Bagrinho) y
Hoplias malabaricus
Bloch, 1794 (Traíra) en la cuenca del río Pericumã, Maranhão, Brasil
fueron evaluados. Se tomaron muestras de estómago, intestino y ojos para el análisis de parásitos. Se
identificaron parásitos pertenecientes a los grupos: nematodos, género
Contracaecum
sp.; cistiacanto de
acantocéfalo, y larva de céstoda. En esta investigación fue posible reportar nuevas asociaciones en la
relación huésped-parásito, como el primer registro del género
Contracaecum
sp. en la especie
C. zarskei
,
parásito que presenta potencial zoonótico cuando se consume pescado infectado crudo o con poca
cocción. El conocimiento sobre la parasitofauna de la comunidad de peces en la cuenca del río Pericumã,
Maranhão, Brasil se amplía a través de este estudio, con el registro de nuevas especies de helmintos
descritos para la región.
Silva Mello
et al.
MATERIAL AND METHODS
Neotropical Helminthology, 2021, 15(2), jul-dic
image/svg+xml
taxonomic organization and identification of the
helminths was performed using taxonomic keys
and specific original works for each parasite,
following Campbell & Beveridge (1994) and Palm
(1999) for Cestoda, Moravec (1998) for Nematoda
and other studies on taxonomy on the specific level
for the other parasites. The specimens studied were
deposited in the 'Coleção Helmintológica do
Instituto Oswaldo Cruz (CHIOC 39718; CHIOC
39719; CHIOC 39173; CHIOC 39174; CHIOC
39175; CHIOC 39176; CHIOC 39177; CHIOC
39178).
Ethical aspects
This investigation was subject to ethical norms that
facilitated the minimization of possible harm to the
specimens, breeding grounds and technical
personnel involved in the identification of the
samples to generate new knowledge without
violating established ethical principles for these
cases. All the authors involved in the investigation,
publication and dissemination of the results are
responsible for the reliability and accuracy of the
data (DHAMM, 2013).
Twenty-nine tissues were analyzed, including
stomachs, intestines, celomatic cavity and eyes, of
the following species:
C. zarskei
,
S. aff. rhombeus
,
T. galeatus
and
H. malabaricus
(Table 1). These
species were chosen due to their economic
importance and abundance in the region, as they
are commonly sold and consumed by the local
population.
219
Eiras
et al
. (2006). Each fish was submitted to
necropsy for the analysis of the viscera, eyes and
gastrointestinal tract at a total of four infection
sites: eyes, stomach, intestine and mesentery.
Helminths were transferred to Petri dishes for
fixation according to the different techniques
employed for each group and studied under a light
microscope.
Nematodes were fixed in 70% ethyl alcohol for the
relaxation of the specimens and conserved in the
same solution, whereas acanthocephalans were
fixed in 70% ethyl alcohol. Cestodes were placed
in Petri dishes with water and maintained
refrigerated for 24 hours for the relaxation of the
scolex and extroversion of the tentacles. The
specimens were subsequently sent for
identification at the Morphophysiology Laboratory
of the State University of the Tocantina Region of
Maranhão, Brazil. Cestodes were transferred to
70% ethyl alcohol, stained with alcoholic
hydrochloric acid-carmine, dehydrated in an
increasing series of ethyl alcohol (70%, 80%, 90%
and absolute), cleared with phenol and Faia's
creosote or methyl salicylate and mounted on
slides with Canada balsam. Nematodes were
cleared in phenol and mounted on slides for
examination (Pavanelli
et al
., 2008).
Acanthocephalans were stained with Meyer's
paracarmine for a variable time until impregnation
of the dye, differentiated in 2% hydrochloric acid
for the removal of excess dye, dehydrated in an
increasing ethyl alcohol series (70%, 80%, 90%
and absolute for 30 minutes each), diaphanized in
increasing concentrations of clove oil (10%, 50%
and 100%) for a variable time and mounted on
slides with Canada balsam (Oliveira, 2019). The
RESULTS AND DISCUSSION
Table 1.
List of helminths and infection sites of endoparasites of fishes collected from Pericumã River, state of
Maranhão, Brazil.
Host
Parasit
e
Infection site
Cichlasoma
zarskei
Contracaecum
sp. larva (N=1)
Mesent
ery
Trachelyopterus galeatus
Contracaecum
sp. larva (N=1)
Cestoda larva (N=1)
Mesentery
Hoplias malabaricus
Contracaecum
sp. larva (N=4)
Mesentery
Serrasalmus aff. rhombeus
Contracaecum
sp. larva (N=1)
Intestin
e
Capillaridae
gen. sp. f
a
m
(N=2)
Intestin
e
Acanthocephal
a
,
C
y
stacant
h
(N=1)
Stomach
Parasitic fauna in fishes of the Pericumã river basin in Brazil
Neotropical Helminthology, 2021, 15(2), jul-dic
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220
Among the helminths analyzed in the present
study,
Contracaecum
sp. was found in seven of the
eleven samples, which may be associated with the
low parasitic specificity of this nematode
(Gonçalves
et al
., 2016). In a previous study,
Oliveira (2019) also found that
Contracaecum
sp.
was abundant among all host species, found in the
mesentery and intestinal lumen of the fish species
Serrasalmus spilopleura
Kner, 1858,
H.
malabaricus
,
Cichla monoculus
Spix, 1831 and
Serrasalmus rhombeus
Linnaeus, 1766 caught in
the lower stretch of the Jari River in the state of
Amapá. Rodrigues
et al
. (2017) reported a higher
mean intensity, dominance coefficient and
coefficient of variation for the genus
Contracaecum
located in the mesentery of
H.
malabaricus
collected from open markets and
directly from fishermen in the city of São Bento,
which is located in the microregion of the
Maranhense Lowlands.
Numerous variables can determine the existence of
endoparasites, especially infecting forms, which
are obtained directly through the diet of the host
(Mesquita
et al.,
2011; Tavares-Dias
et al
., 2013).
Indeed, the diet of fishes can be inferred by
parasites disseminated in this manner. The fishes of
the present study occupy an intermediate position
in the trophic chain, serving as food for birds and
piscivorous aquatic mammals, which then become
the definitive hosts of species of
Contracaecum
(Neves
et al
., 2013; Bittencourt
et al
., 2014;
Tavares-Dias
et al
., 2014).
Contracaecum
sp.
depreciates the catch and, when affecting young
fishes, the larvae can cause death or invade the
heart region, cause changes to the stomach wall and
compromise the musculature (Germano &
Germano, 2008).
In the present study,
Serrasalmus aff. rhombeus
presented parasitic variety. This may have been
influenced by the trophic level of this fish, as
carnivorous fishes can become infected with
different nematoid larvae when feeding on
previously infested smaller fishes and are therefore
more prone to infections by
Contracaecum
sp.
(Benigno
et al
., 2012; Meneguetti
et al
., 2013;
Alcantara
et al
., 2015; Gonçalves
et al
., 2016).
Moreover, taking into consideration that most
endoparasites are related to a specific ecological
niche and diet, a high diversity of parasitic fauna in
a host specific indicates a varied diet of another
host. Therefore, this variety of parasitic species
suggests that the host population consumed a
diversity of prey items in the habitat (Neves
et al
.,
2013; Tavares-Dias
et al
., 2013; Bittencourt
et al
.,
2014; Tavares-Dias
et al
., 2014).
Adult capillariids (females containing eggs) were
found in the stomach of
Serrasalmus aff.
rhombeus
, suggesting that this fish species may be
considered the definitive host. However, the
lifecycle of capillariids has not yet been fully
clarified (Pereira
et al.
, 2020; Pelligra
et al
., 2020).
According to Moravec (1994), these organisms
have a direct lifecycle, but there is the possibility of
having intermediate hosts, such as annelids or
crustaceans. Capillariids can be found in the
digestive tube or several other organs of fishes.
Specimens of the family Capillariidae were found
in the stomach and intestine of freshwater fishes in
studies conducted in the São Francisco River in the
state of Minas Gerais and floodplain lakes in the
state of Amazonas, respectively (Morais, 2011).
Some capillariids are pathogenic and have the
capacity for accentuated infection that can cause
the death of the host (Moravec, 1994; Moravec,
1998).
A representative of the phylum Acanthocephala
was found in only one individual, parasitizing
Serrasalmus aff. rhombeus
. The specimen was
found in the cystacanth (infecting larval) stage and,
thus, its classification could not be determined.
Paratenic hosts may also be part of the life cycle of
acanthocephalans by feeding on an intermediate
host that is not part of the diet of the definitive host
and are then consumed by the definitive host,
thereby completing the cycle. However, some
fishes tend to be infected accidentally when
feeding on organisms that harbor cystacanths
(Eiras
et al
., 1995; Goater
et al.,
2014).
Regarding the cestoid larva found in the stomach of
T. galeatus
, this may be considered its intermediate
or paratenic host. In the carrier, more serious harm
can be found when the parasites use more efficient
attachment structures, which can cause significant
harm to the host intestine and high infection
intensities can cause intestinal occlusion, which
can lead to the death of the host (Pavanelli
et al
.,
2008).
There is a certain absence of cases of zoonoses
Silva Mello
et al.
Neotropical Helminthology, 2021, 15(2), jul-dic
image/svg+xml
221
transmitted by fishes in the Amazon region of the
state of Maranhão. However, this scenario is
directly influenced by the insufficiency of reports
of this type of parasitosis. Indeed, there is a need to
improve the networks of data on parasitic diseases
from water bodies so that tropical diseases do not
continue being omitted (Corrêa & Pinheiro, 2017).
Further studies involving molecular biology are
needed to broaden knowledge on the parasite
community of fishes of the Pericumã River.
The authors are grateful to the Laboratory of
Helminth Parasites of Fishes (LHPP), FIOCRUZ
for the contribution to the analyses of the samples.
Competing Interests
The authors declare no conflicts of interest
regarding the publication of this paper.
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Acta Parasitologica, vol. 59, pp. 158-164.
Received October 18,2021.
Accepted December, 11, 2021.
Parasitic fauna in fishes of the Pericumã river basin in Brazil
Neotropical Helminthology, 2021, 15(2), jul-dic