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Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Neotropical Helminthology
Neotropical Helminthology, 2025, vol. 19 (1), 121-129
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
PARASITES OF THE WHITE MULLET,
MUGIL CUREMA
VALENCIENNES,
1836 (MUGILIFORMES: MUGILIDAE), FROM SANTA CATARINA STATE,
SOUTHERN BRAZIL
PARÁSITOS DE LA LISA BLANCA,
MUGIL CUREMA
VALENCIENNES,
1836 (MUGILIFORMES: MUGILIDAE), DEL ESTADO
DE SANTA CATARINA, SUR DE BRAS
IL
Rosiléia Marinho de Quadros
1,2*
, Aline Brum Figueredo Ruschel
3
,
Jary André Carneiro Júnior
2
,
Pedro Volkmer de Castilho
4
, Renata Assis Casagrande
1
&
Ricardo Bassini-Silva
5*
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20251911972
Universidad Nacional
Federico Villarreal
Volume 19, Number 1 (jan - jun) 2025
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
T is study investigates the parasitic fauna of
Mugil curema
Valenciennes, 1836 (Mugilidae) from Laguna, southern
Santa Catarina, Brazil, being the f rst parasitological survey of this species in the region. A total of 52 specimens were
examined for ecto- and endoparasites. T e external examination revealed Ergasilidae specimens and copepod eggs on the
gills, while the monogenean
Metamicrocotyla macracantha
(Alexander, 1954) was identif ed. Internal prospection showed
the presence of the acanthocephalan
Neoechinorhynchus curemai
Noronha, 1973, and one unidentif ed digenean from
1
Departamento de Medicina Veterinária, Centro de Ciências Agroveterinárias, Universidade do Estado de Santa Catarina
(Cav - Udesc), Lages, SC, Brazil; e-mail: rosileia.quadros@udesc.br,
rosileia@uniplaclages.edu.br,
e-mail: renata.casagrande@
udesc
2
Laboratório de Zoologia e Parasitologia, Universidade do Planalto Catarinense (UNIPLAC), Lages, SC, Brazil; e-mail:
jary@uniplaclages.edu.br
3
Departamento de Aquicultura da UFSC, vinculada ao Laboratório de Piscicultura Marinha (LAPMAR), Universidade
Federal de Santa Catarina (UFSC), Florianópolis, SC, Brazil; e-mail: aline.brum@ufsc.br
4
Departamento de Engenharia de Pesca e Ciências Biológicas, Universidade do Estado de Santa Catarina (UDESC), Laguna,
SC, Brazil. e-mail: pedro.castilho@udesc.br
5
Laboratório de Coleções Zoológicas, Instituto Butantan, São Paulo, SP, Brazil; e-mail: ricardo.bassini@gmail.com
* Corresponding author: rosileia.quadros@udesc.br
Rosiléia Marinho de Quadros:
https://orcid.org/0000-0003-2801-0289.
Aline Brum Figueredo Ruschel:
https://orcid.org/0000-0002-5801-2317
Jary André Carneiro Júnior:
https://orcid.org/0000-0001-8625-0542
Pedro Volkmer de Castilho:
https://orcid.org/0000-0002-9939-7807
Renata Assis Casagrande:
https://orcid.org/0000-0001-6845-6344
Ricardo Bassini-Silva:
https://orcid.org/0000-0002-9568-4120
122
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Marinho de Quadros
et al.
the family Haploporidae. Histopathological analysis revealed hepatic lesions and mild infammation in intestinal tissue.
Tese fndings underscore the importance of parasites in
M. curema
, contributing to the ecological understanding of
parasitism in marine fsh and its potential implications for human health and environmental monitoring.
Keywords:
Environmental indicators
–
Fish health – Histopathology – Parasitology
–
Southern Brazil
RESUMEN
Este estudio investiga la fauna parasitaria de
Mugil curema
Valenciennes, 1836 (Mugilidae) de Laguna, en el sur de Santa
Catarina, Brasil, siendo el primer relevamiento parasitológico de esta especie en la región. Se examinaron un total de 52
ejemplares en busca de ecto e endoparásitos. El examen externo reveló la presencia de ejemplares de Ergasilidae y huevos
de copépodos en las branquias, mientras que se identifcó el monogeneo
Metamicrocotyla macracantha
(Alexander, 1954).
La prospección interna mostró la presencia de acanthocephala
Neoechinorhynchus curemai Noronha, 1973
y de un digeneo
no identifcado de la familia Haploporidae. El análisis histopatológico reveló lesiones hepáticas e infamación leve en el
tejido intestinal. Estos hallazgos resaltan la importancia de los parásitos en
M. curema
, contribuyendo a la comprensión
ecológica del parasitismo en peces marinos y sus posibles implicancias para la salud humana y el monitoreo ambiental.
Palabras clave:
Indicadores ambientales – Salud de los peces – Histopatología – Parasitología – Sur de Brasil
INTRODUCTION
Te family Mugilidae Jarocki, 1822 consists of 20 genera
and 78 valid species (Froese & Pauly, 2024), with a
wide geographic distribution, occurring in tropical and
subtropical regions worldwide, particularly along coastal
areas and estuaries (Falkenberg
et al.,
2021). In Brazil, the
only genus of this family recorded is
Mugil
L., 1758, which
includes six species:
Mugil brevirostris
Miranda-Ribeiro,
1915;
Mugil curema
Valenciennes, 1836;
Mugil curvidens
Valenciennes, 1836;
Mugil incilis
Hancock, 1830;
Mugil
liza
Valenciennes, 1836; and
Mugil rubrioculus
Harrison,
Nirchio, Oliveira, Ron & Gaviria, 2007 (Fischer
et al.
,
2011; Nascimento
et al.,
2022).
According to the FAO (2022), mugilids are among
the most produced fsh in global coastal and marine
aquaculture, ranking just behind two species: Atlantic
salmon,
Salmo salar
L., 1758 (Salmoniformes:
Salmonidae) and milkfsh,
Chanos chanos
Forsskål, 1775
(Gonorynchiformes: Chanidae). Te production of
farmed mugilids reached 291.2 thousand tons in 2020,
marking a 125% increase over the previous fve years
(FAO, 2022). Brazil is recognized as one of the largest
producers of mullet worldwide (FAO, 2015; Santos
et al
.,
2021).
Among the species found in the country,
M. curema
stands out due to its high demand, refected not only in
fshing statistics but also in its signifcance as a farmed
species. Tis species displays pelagic behavior and is found
in a variety of habitats, including sandy shores, coastal
pools, brackish lagoons, estuaries, and muddy bottoms
(Moutinho & Alves, 2014). In its natural environment,
M. curema
has a diverse diet, feeding on algae, particularly
diatoms, and zooplankton.
Fish parasites represent an important component of
aquatic biodiversity, as fsh are directly afected by their
environment or indirectly through their hosts (Mehana
et al.,
2020). Tese parasites are notably diverse and
abundant compared to other vertebrate classes, likely
due to evolutionary processes that have fostered a close
association with a wide range of invertebrates over time
(Dezfuli & Scholz, 2022). Understanding the biological
dynamics of marine populations and species is closely
linked to the study of evolutionary processes that govern
the history of biodiversity (Broglia & Kapel, 2011).
Te family Mugilidae, with its broad distribution and
diverse species, plays a signifcant role in both natural
ecosystems and global aquaculture. Additionally, the
study of fsh parasites provides valuable insights into
aquatic biodiversity, as evidenced by various studies
on
Mugil
species, which have revealed a wide range of
parasites. Tis diversity was summarized by Falkenberg
et al
. (2022), who highlighted that the most extensively
studied regions in Brazil are the Northeast and Southeast.
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
In this context, the present study aims to assess the
occurrence of parasites in
M. curema
, representing the
frst parasitological investigation of this species in Laguna,
a municipality in southern Santa Catarina, where fshing
and fsh consumption hold great economic and historical
importance.
Figure 1.
Location of Tesoura Beach, Laguna Municipality, Santa Catarina State, Brazil.
MATERIAL AND METHODS
Host specimens’ collection
Te study was conducted in the municipality of Laguna
(28° 28’ 57’’ S, 48° 46’ 53’’ W), located in the southern
state of Santa Catarina (Figure 1). With a population of
just over 50,000 inhabitants, the region’s main economic
activities are fshing, commerce, and tourism. A total of
52
M. curema
specimens were studied, all commercially
sold at the Tesoura Beach, a small stretch of beach
approximately 150 meters long, situated within the Barra
Beach Mole.
Tese specimens, which had an average length of 40±55
cm and an average weight of 150±380 grams, were
purchased from local fshermen between November
2019 and March 2020. After being kept refrigerated, the
specimens were transported to the Zoology Laboratory at
the State University of Santa Catarina (UDESC), located
in Laguna Municipality.
Parasitological analyses
External and internal examinations were conducted at
the Microbiology and Parasitology Laboratory at the
Department of Fisheries Engineering and Biological
Sciences, University of the State of Santa Catarina
(UDESC). Te inspection began with the oral, nasal, and
opercular cavities. Skin mucus samples were then scraped
using a microscope slide, and the contents were analyzed
under a Nikon Eclipse optical microscope. While, the
gills were removed through a lateral incision of the
opercula and examined fresh under an Olympus SZ61
stereomicroscope.
In addition, a ventral incision was made from the
operculum to near the anus to expose the abdominal
cavity, muscle tissue fragments were placed in Petri dishes
and examined under the same stereomicroscope for the
detection of zoonotic nematodes. Te intestinal content
was also transferred to Petri dishes and inspected for
acanthocephalans, nematodes, cestodes and trematodes.
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et al.
Preparation and identifcation of the helminthofauna
Acanthocephalans and nematodes were fxed in AFA
solution (70% ethanol, 5% formalin, and 2% glacial
acetic acid), then preserved in 70% ethanol for later
identifcation. Trematodes were stained following the
protocol by Amato
et al.
(1991), and their identifcation
was based on internal parasite structures, observed using
a Nikon Eclipse optical microscope coupled with a
Canon EOS R8 camera. For species-level identifcation
of the Monogenea specimen, we followed the studies of
Hendrix (1994) and Kohn
et al.
(1994). Te identifcation
of Acanthocephala was based on the work of Martins
et al.
(2000), while the classifcation of the Trematoda
family followed the studies of Tatcher (1978) and
Andres
et al.
(2018). All parasites are deposited in the
didactic collection of the Laboratory of Zoology and
Parasitology at the Universidade do Planalto Catarinense
(UNIPLAC), in Lages, Santa Catarina, Brazil.
Histopathological analyses
Following standard histopathological procedures, liver
and intestinal samples were collected and preserved in
formalin (10%), prepared with destilated water, for these
analyses. Tese organs were subjected to dehydration in a
graded ethanol series, clarifed in xylene, and embedded
in parafn at 60°C. Tissue sections were stained with
Harris hematoxylin and eosin (HHE) for subsequent
examination under a Nikon Eclipse optical microscope.
All histopathological analysis was conducted at the
Pathology Laboratory of the Department of Veterinary
Medicine at the University of the State of Santa Catarina
(UDESC), Lages, Santa Catarina, Brazil.
Ethis acpects:
Te fsh were obtained directly from
the fshermen at their beach sales. Ethics approval Not
applicable.
RESULTS
Parasites’ identifcation
After completing all the processes described above, a total
of 18
M. curema
specimens were found to be parasitized.
Among these, copepod eggs were observed in the gills
of nine individuals, along with two unidentifed adult
specimens of Ergasilidae (Copepoda: Cyclopoida). In
another
M. curema
specimen, a digenetic trematode of
the family Haploporidae Nicoll, 1914 (Platyhelminthes:
Trematoda) was found, a family commonly associated
with fsh of the genus
Mugil
. Additionally, in the gills of
one
M. curema
specimen,
Metamicrocotyla macracantha
(Alexander, 1954) (Monogenea: Mazocraeidea:
Microcotylidae) was identifed (Figure 2). Furthermore,
three specimens of
Neoechinorhynchus curemai
Noronha,
1973 (Acanthocephala: Neoechinorhynchidae) were
recovered from the intestines examined.
Figure 2
. Microscope image of the
Metamicrocotyla macracantha
(Alexander, 1954) (Monogenea: Mazocraeidea:
Microcotylidae) collected from the gills of the white mullet,
M. curema
. A – General view of the endoparasite; B –
Close up of the anterior region; B
1
– Close up of the genital atrium; C – Close up of the posterior region. Scale bar: A
1.5 mm, B, B
1
and C 0.5 mm.
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Te species
M. macracantha
is characterized by an
elongated, lanceolate body, measuring 15.2 mm in length
and 4 mm in width, dorsoventrally fattened and tapering
anteriorly. Te apical glands have ducts extending up to
the level of the pharynx. Te buccal opening is median,
subterminal, and ventral, located between the anterior
extremity and the pharynx. It has two latero-median
suckers (0.7 mm in length × 0.6 mm in width), situated
between the buccal opening and the pharynx. Te
intestinal ceca are long. Te haptor measures 1.8 mm in
length and 1.3 mm in width, featuring 21 pairs of clamps
arranged in two longitudinal rows along the body. Te
clamps are composed of dark structures (sclerites). Te
genital opening is median and ventral, located at the level
of the cecal bifurcation, and armed with atrial spines
(0.6 mm in length × 0.1 mm in width), organized into
two bilateral groups arranged in two parallel rows (six
anterior and eleven posterior). Te testes are elongated
and numerous (3.3 mm in length × 1.7 mm in width).
Te vitelline gland extends from the cecal bifurcation to
the anterior end of the haptor. Eggs were not observed.
While, the species
N. curemai
, which is host-specifc, is
characterized by a cylindrical trunk that is wider in the
anterior third, a short proboscis armed with two large
hooks and three circles of smaller hooks, and elliptical
eggs, consistent with the specimens examined in this
study.
Although the study involved the identifcation of several
parasites, high-quality images are available only for
M.
macracantha
. Images of the other listed parasites were not
obtained due to limitations in the collection process or
viewing conditions. However, morphological descriptions
and bibliographic references were rigorously followed,
ensuring the accuracy of the identifcation.
Histopathological analyses
Te liver samples with light-colored spots and ulcerative
lesions were analyzed and histopathologically revealed
the presence of larval migration (Figure 3A) and
areas of moderate to severe, difuse hepatocellular
degeneration. In the intestinal samples, the presence of
parasites was observed in the submucosa, surrounded
by a mild infammatory reaction, with a predominance
of macrophages (Figure 3B).
Unfortunately, it was not
possible to identify the causative agent of the lesions
described above, requiring further studies.
Figure 3.
Histopathological images of the
M. curema
’s liver and intestine.
A -
Cross section of the
intestinal muscle.
B -
Cross section of the liver parenchyma. Black arrows show the endoparasite. All
images in HE stains. Scale bar: 200 µm.
DISCUSSION
Fish parasites, especially those in marine environments,
can cause signifcant economic losses and pose public
health concerns. Despite this, specifc studies on parasite
diversity, particularly nematodes in marine fsh from the
Americas, are scarce, with most research focusing on
isolated cases of particular species (Pereira & González-
Solís, 2022). In the present study, the absence of
ectoparasites on the body surface may be attributed to
the capture method, as the friction between the fsh and
the net could dislodge these parasites. Tis hypothesis is
supported by the fnding of parasites in the gills, an area
protected from such mechanical efects.
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Marinho de Quadros
et al.
While gill parasites typically exhibit low diversity and
density, their interactions are often reported as isolated
incidents. However, the coexistence of monogeneans
on gills is well documented, with some studies, such as
this one, reporting the presence of copepods alongside
monogeneans (Baker
et al
., 2005). For
M. curema
, the
only record of coinfection by Monogenea and ergasilids
on the gills of this species in Brazil comes from Falkenberg
et al
. (2021), who found evidence suggesting interactions
between these parasites in this species in northeastern
Brazil. In the present study, we identifed ergasilid
copepods and the monogenean species
M. macracantha
on the gills of
M. curema
.
Ergasilid copepods, which predominantly inhabit the
gills, can cause infammatory reactions, increased mucus
production, changes in gill flament anatomy, and
cellular infltration. In some cases, these changes can lead
to hyperplasia, potentially afecting host growth, fertility,
and survival (Cavalcanti
et al
., 2005; Mentz
et al
.,
2016).
Herein, only two complete copepod specimens
were identifed, with the remaining samples being
eggs, making it difcult to observe any signifcant gill
alterations. Similar fndings were reported in
M. curema
specimens from the northern region of Santa Catarina,
where ergasilid specimens were also found on the gills of
M. curema
specimens (Gueretz
et al
., 2022).
Regarding to the monogenean species collected, we were
able to identifed up to species level as
M. macracantha
, a
monogenean from the family Metamicrocotylidae, which
has been sparsely documented in Brazil, particularly in
M. liza
(Kohn
et al
., 1994; Cohen
et al
., 2004). Known to
parasitize the gills of marine fsh, particularly those of the
genus
Mugil
, this parasite can cause gill lamella hyperplasia
in cases of massive infection, thereby interfering with ion
absorption and gas exchange (Mentz
et al.,
2016). While
this parasite has been previously reported in other
Mugil
species in various regions (Vidal-Martínez
et al
., 2017),
this study presents the frst record of
M. macracantha
in
M. curema
from southern Brazil.
Additionally, the present study identifed
N. curemai
acanthocephalans in the intestines of three specimens.
Tis species has also been reported in
M. curema
from
the northern region of Santa Catarina, with a prevalence
of 3.39%, further supporting the fndings of this study
(Gueretz
et al
., 2022).
Mugil
species are catadromous,
their migratory behavior could explain the distribution
of
N. curemai
across coastal and estuarine environments
(Cavalcanti
et al
., 2012; Gueretz
et al
., 2022).
Acanthocephalans are signifcant in ecological studies
because they can accumulate contaminants, making
them valuable indicators of environmental quality (Sures,
2008; Roohi
et al
., 2015). Fish, being highly susceptible to
pollutants through diet or living in degraded ecosystems,
often harbor high concentrations of metals in the tissues
of acanthocephalans, suggesting the environmental
conditions to which they are exposed (Abdallah
et al
.,
2019). Te relationship between fsh, parasites, and
contaminants provides an efective means of assessing
ecosystem health. As biological indicators, fsh parasites
can refect the ecology of their hosts, including migration
patterns, feeding habits, and population structures
(Mehana
et al.
, 2020).
Digeneans from the family Haploporidae, which primarily
parasitize herbivorous or omnivorous fsh, are common
in marine ecosystems. In Brazil, these parasites have been
recorded in several
Mugil
species (Eiras
et al
., 2016; Andres
et al
., 2018). Te present study adds to the knowledge
of these trematodes, though taxonomic identifcation
remains incomplete due to limited specimen availability
and morphological challenges. Similarly, the histological
analysis of hepatic tissue revealed larvae resembling
Ascocotyle longa
metacercariae, a zoonotic parasite. While
precise identifcation could not be made, previous studies
in
M. curema
have also reported the presence of
A. longa
larvae in muscle tissue (Namba
et al.
, 2012; Gueretz
et
al
., 2022). Digenean trematodes may not be immediately
concerning due to their typically asymptomatic nature,
due the fact that their potential pathogenic efects are still
debated and dependent on various factors as parasite type,
host condition, and the presence of intermediate hosts
(Aly
et al.,
2020). However, these fndings contribute to
the growing understanding of digenean trematodes and
their potential implications for fsh health, highlighting
the need for further research to clarify the pathogenicity
and ecological roles of these parasites.
In conclusion, this study contributes important insights
into the diversity of parasitic fauna in
M. curema
and
highlights the ecological interactions between fsh
and their parasites.
Te fndings not only expand the
knowledge of parasitic species in Brazilian marine
ecosystems but also emphasize the role of parasites as
indicators of environmental health. Continued research
is crucial to further understand these interactions and
their implications for both fsh health and human safety,
particularly in relation to zoonotic parasites in fsh
consumed by humans.
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Author contributions: CRediT (Contributor Roles
Taxonomy)
RMQ
= Rosiléia marinho de Quadros
ABFR
= Aline Figueredo Ruschel
JACJ
= Jary André Carneiro Júnior
PVC
= Pedro Volkmer de Castilho
RAC
= Renata Assis Casagrande
RBS
= Ricardo Bassini-Silva
Conceptualization:
RMQ
Data curation:
RMQ
Formal Analysis:
RMQ, ABFR, PVC, RAC, RBS
Funding acquisition:
RMQ
Investigation:
RMQ, ABFR, PVC, RAC, RBS
Methodology:
RMQ, PVC, JACJ
Project administration:
RMQ, RBS
Resources:
RMQ, PVC
Software:
RMQ, ABFR, JACJ, PVC, RAC, RBS
Supervision:
RMQ
Validation:
RMQ, RBS
Visualization:
RMQ, RBS
Writing – original draft:
RMQ, ABFR, JACJ, PVC,
RAC, RBS
Writing - review & editing:
RMQ, RBS
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Received April 18, 2025.
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