ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2019, 13(1), ene-jun:17-23.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
OCCURRENCE OF BRAGA NASUTA SCHIOEDTE & MEINERT (1881) (ISOPODA, CYMOTHOIDAE)
PARASITIZING THE ORNAMENTAL FISH HYPHESSOBRYCON EQUES (STEINDACHNER, 1882)
(CHARACIDAE) FROM A BRAZILIAN RIVER
OCURRENCIA DE BRAGA NASUTA SCHIOEDTE & MEINERT (1881) (ISOPODA, CYMOTHOIDAE)
PARASITANDO EL PECE ORNAMENTAL HYPHESSOBRYCON EQUES (STEINDACHNER, 1882)
(CHARACIDAE) DE UN RIO BRASILEÑO
1Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brasil.
2Programa de Pós-graduação e Ciências Biológicas (Zoologia), Instituto de Biociências, UNESP.
Laboratório de Parasitologia de Animais
Silvestres (LAPAS), Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista (UNESP), Rua
Prof. Dr. Antonio Celso Wagner Zanin, s/n°, CEP 18618-689. Botucatu, SP, Brasil. Phone: +55 (14) 3880 0522. E-mail:
Corresponding Author: rodrigoparasitologia@gmail.com
1,2 1 1 1
Rodrigo Bravin Narciso ; Gabriela Peres de Oliveira ; Aline Angelina Acosta & Reinaldo José da Silva
ABSTRACT
Keywords: Crustacea – Freshwater – Malacostraca – Mato Grosso do Sul State
Cymothoidae is the most common family of parasitic isopods found in fishes from Brazil. Among
freshwater cymothoids, the genus Braga has seven species already recorded for this country. Braga
nasuta Schioedte & Meinert (1881) was originally described from the coast of Brazil, however, it has
already been recorded parasitizing freshwater fishes from Amazonas, Bahia, São Paulo, and Pará States.
An adult male of B. nasuta was recorded for the first time parasitizing the ornamental fish,
Hyphessobrycon eques (Steindachner, 1882) sampled in the “Reserva Particular do Patrimônio Natural”
Cisalpina, Mato Grosso do Sul State, Brazil. This study also represents the first record of this parasitic
isopod in the Central-West region of Brazil. The occurrence of parasitic isopods on a highly appreciated
and exported fish like H. eques increases the concern about the potential introduction of these parasites to
importing countries.
Neotropical Helminthology
17
Volume13,Number1(jan-jun2019)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Auspiciado por:
INTRODUCTION
18
RESUMEN
Palabras clave: Crustacea - Agua dulce - Malacostraca - Mato Grosso do Sul
Cymothoidae es la familia más común de isópodos parásitos encontrados en peces de Brasil. Entre los
cimotoideos de agua dulce, el género Braga con siete especies ya registradas en el país. Braga nasuta
Schioedte & Meinert (1881) fue originalmente registrada por la primera vez en la Costa de Brasil, pero ya
se ha registrado en peces de agua dulce en los estados brasileños de Amazonas, Bahia, São Paulo y Pará.
Un macho adulto de B. nasuta fue registrado por primera vez parasitando el pez ornamental,
Hyphessobrycon eques (Steindachner, 1882) muestreado en la Reserva Particular de Patrimonio Natural
Cisalpina, Mato Grosso do Sul, Brasil. Este estudio también representa el primer registro de ese isópodo
parásito en la región Centro-Oeste del Brasil. El registro de isópodos parásitos en una especie de pez muy
apreciada y exportada como H. eques aumenta la preocupación del potencial de introducción de estos
parásitos a los países importadores.
parasites can cause expressive damages to their
hosts. Especially on the gills, these parasites can
cause compression and destruction of tissues,
blood loss, and decreasing of breathing capacity,
which may affect hosts' metabolism and lead to a
decrease in their growth rate (Carvalho et al., 2004;
Eiras et al., 2010). Furthermore, these parasites can
increase the mortality rate or even act as vectors for
other fish diseases, particularly those caused by
virus and bacteria (Tavares-Dias et al., 2014).
The genus Braga Schiöedte & Meinert, 1881
includes freshwater cymothoids, with seven
species described: Braga amapaensis Thatcher,
1996, Braga bachmanni Stadler, 1972, Braga
brasiliensis Schiöedte & Meinert, 1881, Braga
cichlae Schiöedte & Meinert, 1881, Braga
fluviatilis Richardson, 1911, Braga nasuta
Schiöedte & Meinert, 1881, and Braga patagonica
Schiöedte & Meinert, 1884 (Schiöedte & Meinert,
1881). Except for B. bachmanni that was described
from Ancistrus cirrhosus (Valenciennes, 1836) in
Argentina (Stadler, 1972), all other species have
already been recorded parasitizing fishes in Brazil
(Luque et al., 2013). Species from this genus are
usually found associated with the tongue or the
opercular cavity of their hosts (Thatcher, 2006).
Hyphessobrycon eques (Steindachner, 1882) is a
small neotropical characid, which has diurnal
activity anolis widely distributed in Amazon and
Paraguay-Paraná River basins (Carvalho & Del-
Claro, 2004). Popularly known as “serpa tetra”,
“jewel tetra” or ”matogrossinho”, this species is
highly appreciated in aquiariofilism due to its
Teleosts harbor a great quantity and variety of
invertebrate parasites, being recorded host-parasite
associations with parasites from different taxa, as:
Protozoa, Ciliophora, Cnidaria (Myxozoa),
Platyhelminthes (Trematoda, Cestoda, and
Monogenea), Nematoda, Acanthocephala,
Arthropoda (Copepoda, Branchiura, Isopoda,
Pentastomida, and Acari), Annelida (Hirudinea)
and Mollusca (Bivalvia) (Thatcher, 2006;
Pavanelli et al., 2013). Parasitic crustaceans,
represented mainly by the subclasses Copepoda
and Branchiura, and the order Isopoda are among
the most relevant parasites of Brazilian freshwater
fishes (Eiras et al., 2010).
Isopods are dorso-ventrally flattened crustaceans
found in marine, freshwater, and terrestrial
habitats. They are characterized by having a free
thorax (= pereon) with seven free segments (=
pereonites) each bearing a pair of similar legs (=
pereopods) (Thatcher, 2006). Parasitic isopods
have from four to seven pairs of walking legs
modified for grasping and each of these is provided
with a stout claw-like dactyl (Thatcher, 2006).
Currently, 53 species and 21 genera of parasitic
isopods are known from Brazilian fishes and most
of them belong to the family Cymothoidae Leach,
1818 (Luque et al., 2013).
The knowledge about the impacts of isopods on the
health of fishes is still scarce (Tavares-Dias et al.,
2014). Nevertheless, the presence of these
Narciso et al.
Neotropical Helminthology, 2019, 13(1), ene-jun
exuberant red color (Fujimoto et al., 2013). Despite
being an important species for the aquarium fishery
industry, there is little information about the
parasite fauna of H. eques (Acosta & Silva, 2015).
Fujimoto et al. (2013) and Acosta & Silva (2015)
are the only two assessment of its parasitic fauna
reporting the occurrence of cysthacanths
(Acanthocephala) of Quadrigyrus nickoli Schmidt
& Hugghins, 1973 and Hysterothylacium sp. larvae
(Nematoda), respectively.
We present herein the first report of B. nasuta
(Isopoda: Cymothoidae) parasitizing the
ornamental fish, H. eques sampled in the “Reserva
Particular do Patrimônio Natural (RPPN)”
Cisalpina, Mato Grosso do Sul State, Brazil.
Specimens of H. eques (n = 30) were collected
under the Permanent License for the Collection of
Zoological Material (SISBio 60640-1) in January
2018 in a stream (21°19'53.70"S; 51°56'39.91"W)
in the RPPN Cisalpina, Mato Grosso do Sul State,
Brazil. Fish were collected using sieve nets. Hosts
were individually stored in plastic bags and
transported to the laboratory for parasitological
analyses. Oral cavity, gill chamber, and body
surface of fish were examined for isopods using a
stereo microscope. The Isopod was stored in vials
with 70% ethanol. Morphological analysis and
photomicrographs of the parasite were obtained
using Leica Application Suite 3.7.0 software in
Leica M125 stereomicroscope.
The identification of the isopod was based on
descriptions and identification keys proposed by
Lemos de Castro (1959), Lemos de Castro & Silva
(1985), and Thatcher (2006). The parasite voucher
was deposited in the “Coleção Helmintológica do
Instituto de Biociências de Botucatu (CHIBB)” at
São Paulo State University (UNESP), Botucatu,
São Paulo State, Brazil (CHIBB 8521).
This study was approved by the Ethics Committee
in Animal Experimentation of the Institute of
Biosciences of the São Paulo State University
(Unesp) under the protocol number 942/2017.
19
MATERIAL AND METHODS
Neotropical Helminthology, 2019, 13(1), ene-jun
RESULTS
Thirty specimens of H. eques were examined for
crustacean parasites. Only one isopod adult male
was found parasitizing one fish specimen
(prevalence = 1/30 or 3.3%). The ectoparasite was
identified as belonging to Braga based on the
presence of the following: (i) body symmetrical
longer than wide (5.6 mm long, and 2.6 mm wide)
(Fig. 1A); (ii) cephalon not immersed in pereonite
1; (iii) all seven pairs of pereopods prehensile and
provided with stout claw-like dactyls (Fig. 1B);
(iv) pleopods multilaminate; and (v) pleon slightly
immersed in pereonite 7 (Figs. 1-2).
The male was identified as belonging to the species
B. nasuta by the presence of following features: (i)
cephalon truncated anteriorly; (ii) pereopod 7 with
a dactyl shorter and weaker than others; (iii) merus
of pereopod 7 with a distal tooth near the
articulation with carpus; (iv) pleotelson triangular,
ending in a small and sharp tip (Fig. 2C); and (v)
uropod extending beyond the apex of pleotelson
and with exopod slightly longer than endopod.
The present study report for the first time the
occurrence of B. nasuta infesting H. eques. The
ectoparasite identification was confirmed based on
the main morphological characteristics presented
by Lemos de Castro (1959), Lemos de Castro &
Silva (1985), Thatcher (2006), and Thatcher et al.
(2009).
Hyphessobrycon eques is a Neotropical fish widely
distributed along the Amazon and Paraná-
Paraguay River basins (Carvalho & Del-Claro,
2004). In Brazil, its occurrence in other rivers, such
as the Upper Paraná River may be related to the
introduction of this species through aquarists
(Pavanelli & Graça, 2007). This small characid
presents a diurnal activity and an opportunistic
foraging tactic, which consist in following
substrate grubbers (Carvalho & Del-Claro, 2004).
A dispite this species is highly appreciated as an
aquarium fish, given its peculiar red color
(Fujimoto et al., 2013), there is relatively little
DISCUSSION
Braga nasuta in an ornamental sh from Brazil
20
information about its biology and behavior in the
wild (Carvalho & Del-Claro, 2004).
Likewise, the literature about its parasitic fauna is
still scarce. Up to date, there are only two reports
about metazoan parasites associated with this
species. Fujimoto et al. (2013) recorded for the first
time the occurrence of Quadrigyrus nickoli
cystacanths (Acanthocephala, Quadrigyridae) in
the stomach and intestine of H. eques sampled in
Chumucuí River, Pará State, Brazil. Acosta & Silva
(2015) recorded Hysterothylacium sp. larvae
(Nematoda, Anisakidae) in the intestine and
coelomic cavity of H. eques sampled in the
Paranapanema River, São Paulo State, Brazil.
Hence, the present study is the first report of an
ectoparasitic isopod on H. eques, and the first
report of B. nasuta from Mato Grosso do Sul State,
Brazil.
Figure 1. Braga nasuta Schioedte & Meinert (1881), adult male. (A) Dorsal view; (B) Ventral view; (C) Lateral view.
Narciso et al.
Neotropical Helminthology, 2019, 13(1), ene-jun
21
Studies regarding the parasitic fauna of ornamental
fishes have gained importance over the last few
years, not only because these parasites have the
potential to affect their hosts' biology, and as a
consequence resulting in economic losses for both
breeders and hobbyists (e. g.: increased fish
mortality, decreased fish grow rate, treatment
costs, etc.) (Piazza et al., 2006; Tavares-Dias et al.,
2009), but also due to increased concern with the
potential for the introduction of diseases and
parasites through the importation and exportation
of these fishes (Tavares-Dias et al., 2009). The
introduction of a new parasite may lead to deep
changes in the native fauna due to decreasing of
native species recruitment, alterations in the
trophic structure, species extinction, or even by
modifications upon evolutionary pressures,
resulting in decreased quality of fishery resources
(Lacerda et al., 2013).
Many crustaceans, mainly copepods, have been
considered as invasive species worldwide
(Johnson et al., 2004; Piasecki et al., 2004). The
lernaeid copepod Lernaea cyprinacea (Linnaeus,
1758) is considered one of the most important
invasive parasites on fishes. This species has been
reported infesting numerous fishes, including both
native and exotic species throughout the world
(Piasecki et al., 2004). In Brazil, L. cyprinacea was
th
introduced at the beginning of 20 century via the
importation of the common carp, Cyprinus carpio
Linnaeus, 1758 with several reports in both farmed
and wild fish throughout the country (Piasecki et
al., 2004). The presence of the cymothoids B.
nasuta, which exhibits a monoxenous life-cycle
and protandrous hermaphroditism (Thatcher,
2006), in a very largely exported and appreciated
ornamental species like H. eques, increases the
concern about the potential for the introduction of
Figure 2. Braga nasuta Schioedte & Meinert (1881), adult male. (A) Cephalon, dorsal view; (B) Cephalon, ventral view; (C)
Pleon, dorsal view; (D) Pleon, ventral view.
Neotropical Helminthology, 2019, 13(1), ene-jun Braga nasuta in an ornamental sh from Brazil
these parasites to importing countries. Therefore, it
is recommended to intensify measures when
exporting H. eques and other ornamental fishes in
order to avoid the spread of parasitic isopods as B.
nasuta to other locations.
The parasitic cymothoid B. nasuta was originally
proposed from a single specimen (female) by
Schioedte & Meinert (1881) for the Brazilian coast.
Later, Lemos de Castro (1959) considered the
statement of Schioedte & Meinert (1881) that B.
nasuta is a marine species, as vague and probably
wrong, since two other specimens (males) were
found in freshwater. Braga nasuta shows
distribution restricted to the Brazilian territory with
reports for Amazonas, Bahia, São Paulo and Pará
States (Thatcher, 2006; Jesus et al., 2017). In
relation to hosts, B. nasuta was reported originally
for Hypostomus sp. (Siluriformes, Loricariidae)
(Thatcher, 2006) and, more recently, parasitizing
fingerlings of Arapaima gigas (Schinz, 1822)
(Osteoglossiformes, Arapaimidae) (Jesus et al.,
2017).
The main features used to identify the male
cymothoid (reported herein) to species level were
the morphology of cephalon, pleotelson, uropod,
and pereopods, and the color pattern of the dorsal
segments. This specimen exhibits the same
morphology and body color proposed and
illustrated by Lemos de Castro (1959). However, it
differs from the male specimens reported by Jesus
et al. (2017) for fingerlings of A. gigas (see Fig. 3 in
Jesus et al., 2017). Our specimen differs from those
of A. gigas by presenting: (i) large cephalon in
relation to the total body length (vs relative size of
cephalon to the total body length smaller); (ii)
cephalon truncated anteriorly (vs rounded
anteriorly); (iii) uropod extending beyond the apex
of pleotelson (vs smaller than the pleotelson); (iv)
exopod longer than endopod (vs similar in size); (v)
pleotelson triangular and wider than long (vs
rounded and as long as wide). Our specimen also
differs by presenting median pereon stripe and the
posterior stripe of each pereonite thinner (vs
thicker stripes). Because of these differences, we
believe that the specimens found on A. gigas
belong to another species of the genus Braga.
This study reported for the first the time infestation
of H. eques from Mato Grosso do Sul State, Brazil,
with B. nasuta and contributes to expanding the
22
knowledge about the geographical distribution and
the list of fishes parasitized by this isopod in this
country.
The authors thank the Conselho Nacional de
Desenvolvimento Científico e Tecnológico CNPq-
PROTAX (440496/2015-2) and FAPESP
2016/50377-1 for the financial support given to the
study. R. B. Narciso was supported by CNPq
(132844/2018-4) and R. J. da Silva was supported
by (CNPq, 307808/2014-9).
ACKNOWLEDGEMENT
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(Characiformes, Characidae). Brazilian
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