335
RESEARCH NOTE / NOTA CIENTÍFICA
RHINOXENUS BULBOVAGINATUS (MONOGENEA, DACTYLOGYRIDAE) PARASITE OF THE
NASAL CAVITIES OF SALMINUS HILARII (CHARACIFORMES, CHARACIDAE) IN A
NEOTROPICAL RIVER, SP, BRAZIL
RHINOXENUS BULBOVAGINATUS (MONOGENEA, DACTYLOGYRIDAE) PARÁSITO DE LA
CAVIDAD NASAL DE SALMINUS HILARII (CHARACIFORMES, CHARACIDAE) EN UNA RÍO
NEOTROPICAL, SP, BRASIL
1* 2 1 1
Rodrigo Bravin Narciso , Heleno Brandão , Fábio Hideki Yamada & Reinaldo José da Silva
Abstract
Keywords: Ancyrocephalinae - Freshwater fish - Neotropical region - "Tabarana"
Suggested citation: Narciso, RB, Brandão, H, Yamada, FH & Silva, RJ. 2013. Rhinoxenus bulbovaginatus (Monogenea,
Dactylogyridae) parasite of the nasal cavities of Salminus hilarii (Characiformes, Characidae) in a neotropical river, SP, Brazil.
Neotropical Helminthology, vol. 7, n°2, jul-dec, pp. 335 - 339.
1 UNESP - Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia,
Laboratório de Parasitologia de Animais Silvestres/LAPAS, CEP 18618-970, Botucatu, SP, Brazil. *e-mail: rodrigobtu7@gmail.com
2Departamento de Biologia, Universidade Federal do Paraná/UFPR, Setor Palotina, Palotina, PR, Brazil
Neotrop. Helminthol., 7(2), 2013
2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
The aim of study is to report for the first time the occurrence of Rhinoxenus bulbovaginatus
infesting the nasal cavity of Salminus hilarii from the Taquari River, São Paulo State, Brazil.
Rhinoxenus bulbovaginatus was originally described parasitizing the nasal cavities of Salminus
brasiliensis from the Paraná River. Rhinoxenus spp. are monogenean parasites from the nasal
cavities of Characiformes fishes in the Neotropical region. To date, eight species of Rhinoxenus
were described in seven different hosts. This study broadens the range of hosts parasitized with
monogeneans of nasal cavities.
Resumen
Palabras clave: Ancyrocephalinae - Peces de agua dulce - Neotropicales - "Tabarana".
El objetivo del trabajo es registrar una nueva ocurrencia de Rhinoxenus bulbovaginatus en la
cavidad nasal de Salminus hilarii del río Taquari, Estado de São Paulo, Brasil. Rhinoxenus
bulbovaginatus fue originalmente descrita parasitando cavidades nasales en Salminus
brasiliensis del río Paraná. Rhinoxenus spp. son monogéneos parásitos de las cavidades nasales
de los peces Characiformes en la región Neotropical. Hasta la fecha, ocho especies de Rhinoxenus
fueron descritas en siete especies hospederas. El presente estudio amplía el rango de hospederos
parasitados con monogéneos de las cavidades nasales.
in 5% formalin, and stored in 70% alcohol.
Afterwards the monogeneans were mounted
unstained in Grey & Wess medium to study the
sclerotized structures (Eiras et al., 2006).
Measurements in micrometers are expressed as
the mean followed by the range and number (n)
of specimens measured in parentheses. The
terminology specific to Rhinoxenus follows
Kritsky et al. (1988a). Ecological terms were
used according to Bush et al. (1997). The image
capture were made using a differential
interference contrast microscope (Leica DM
5000B). Voucher helminth specimens were
deposited in the Coleção Helmintológica do
Instituto de Biociências (CHIBB), of the
Universidade Estadual Paulista/UNESP from
Botucatu, São Paulo State, Brazil.
Rhinoxenus bulbovaginatus Boeger,
Domingues & Pavanelli (1995)
(Fig. 1)
Measurements based on five specimens
mounted in Grey & Wess medium: Body
fusiform 571 (301.5-860.4; n=2) long, 138.9
(111.6-166.3; n=2) wide, divided in cephalic
region, trunk and haptor; dorsoventrally
flattened. Cephalic lobes poorly developed.
Four pairs of head organs, cephalic glands not
observed. Four eyes, usually equidistant, and
members of posterior pair large than those of
anterior pair. Pharynx spherical, 60.6 (n=1) in
diameter. Haptor trapezoidal, lacking peduncle.
Ventral anchor 102.8 (100.5-105.2; n=6) long,
base 15.7 (13.2-17.4; n=4) wide. Ventral bar
trapezoidal 40.2 (36.5-44; n=2) long, 9 (8.9-9.1;
n=2) wide. Dorsal haptoral spike 106.35 (101.3-
105.6; n=6) long. Seven pairs of hooks with
Ancyrocephalinae distribution, hook pair 2
lying on 2 bilateral lobes outside haptor, 37 (30-
42.3; n-9) long. Male copulatory organ, with
about 2 counter-clock rings, first ring 27.6 (26-
29.3; n=2) in diameter. Accessory piece 39.2
(32.2-46.3; n=2) long, 19 (18.3-19.8; n=2) wide,
articulated with the base of male copulatory
organ. Vagina sclerotized, sinistral, simple tube,
loop ended at distal bulb. Reproductive organs
The genus Rhinoxenus, proposed by Kritsky et
al. (1988a), includes monogeneans parasites of
the nasal cavities of Characiformes fishes. To
date, eight species have been described in this
genus: Rhinoxenus piranhus Kritsky, Boeger &
Thatcher, 1988 (type species) in Pygocentrus
nattereri Kner, 1858; R. arietinus Kritsky,
Boeger & Thatcher, 1988 in Schizodon fasciatus
Spix & Agassiz, 1829; R. nyttus Kritsky, Boeger
& Thatcher, 1988 in S. fasciatus; R.
bulbovaginatus Boeger, Domingues &
Pavanelli, 1995 in Salminus brasiliensis
(Cuvier, 1816); R. anaclaudiae Domigues &
Boeger, 2005 in Triportheus cf. nematurus
(Kner, 1858); R. curimbatae Domigues &
Boeger, 2005 in Prochilodus lineatus
Valenciennes, 1837; R. guianensis Domigues &
Boeger, 2005 in Curimata cyprinoides
Linnaeus, 1766; R. euryxenus Domigues &
Boeger, 2005 in Serrasalmus marginatus
Valenciennes, 1837.
Rhinoxenus spp. are Ancyrocephalinae
monogeneans characterized by a pair of dorsal
haptor spikes, lack of a dorsal bar, and hooks pair
2 lying on two lateral lobes of the trunk (Kritsky
et al., 1988a). Rhinoxenus bulbovaginatus was
first described parasitizing the nasal cavities of
Salminus maxillosus (=Salminus brasiliensis)
from the Paraná River, Paraná State, Brazil. This
monogenean species differs from the congeners
because of the morphology of the male
copulatory complex, vagina, and ventral anchor
(Boeger et al.,1997).
This study is the first record of R.
bulbovaginatus infecting Salminus hilarii
(Characidae) from the Taquari river, Upper
Paranapanema River, São Paulo State, Brazil.
Five specimens of S. hilarii were collected from
April 2011 to July 2012, in the Taquari River,
Jurumirim reservoir (23°12'17'' S; 49°13'19''
W), São Paulo State, Brazil. The monogeneans
were removed from the nasal cavities and fixed
INTRODUCTION
Narciso et al.
Rhinoxenus of the nasal cavities of Salminus
MATERIAL AND METHODS
RESULTS
336
Site of infection: Nasal cavities.
Voucher numbers: CHIBB 120L, 121L and
122L.
Prevalence: 60% (3 of 5 fishes examined).
Mean Intensity of infection: 2 parasites per
parasitized host.
not observed. Vitellaria scattered throughout the
trunk.
Taxonomic summary
Type host: Salminus hilarii Valenciennes, 1850
Type locality: Taquari River, Upper
Paranapanema River, São Paulo State, Brazil.
RESULTS
Neotrop. Helminthol., 7(2), 2013
Figure 1. Specimen of Rhinoxenus bulbovaginatus parasite of nasal cavity of Salminus hilarii from Taquari river, São Paulo
State, Brazil: (A) total view; (B) Copulatory complex and vagina (arrow); (C) Dorsal haptoral spikes; (D) Ventral anchors and bar
(arrow). Scale bars: 100 µm (A); 20 µm (B, C, and D).
337
Narciso et al.
Rhinoxenus of the nasal cavities of Salminus
Table 1. Morphometry (in µm) of Rhinoxenus bulbovaginatus parasite of nasal cavity of Salminus hilarii from
Taquari river, São Paulo State, Brazil.
Measurements Boeger et al. (1995) Preset Study
Body
Length 441 (430-454; n=4) 571 (301.5-860.4; n=2)
Width 160 (115-190; n=4) 138.9 (111.6-166.3; n=2)
Pharynx diameter 41-43 (n=2) 60.6 (n=1)
Haptor
Length 100 - 105 (n=2) -
Width 102-110(n=2) -
Ventral anchor
Length 113 (110-119; n=8) 102.8 (100.5-105.2; n=6)
Width 26 (23-29; n=9) 15.7 (13.2-17.4; n=4)
Dorsal haptorial spike
Length 119 (115-122; n=5) 106.35 (101.3-105.6; n=6)
Bar
Length 42 (35-54; n=8) 40.2 (36.5-44; n=2)
Width - 9 (8.9-9.1; n=2)
Hook
pair 2 31 (29-33; n=3) -
Other hooks 41 (29-52; n=16) 37 (30-42.3; n-9)
Male copulatory organ
First ring diameter - 27.6 (26-29.3; n=2)
Acessory piece
Length - 39.2 (32.2-46.3; n=2)
Width - 19 (18.3-19.8; n=2)
Testis
Length 95 (81-118; n=3) -
Width 24 (25-27; n=3) -
Germarium
Length 82 -102 (n=2) -
Width 27-32 (n=2) -
The specimens of R. bulbovaginatus found in S.
hillarii showed morphology very similar to the
specimens collected in S. brasiliensis (Kritsky et
al., 1988a), excepted for ventral anchor width,
which is bigger (Table 1). However, it was
suggested that this is a common individual
variation rather than some morphological
changes associated with biological aspects of the
host.
The main morphological characteristic that
differs R. bulbovaginatus from it congeneric
species is the vagina is sclerotized with distal
loop and bulb. To date, this monogenean species
have been reported parasitizing the nasal
cavities only in S. brasiliensis. Thus this study
suggests the specificity of R. bulbovaginatus
with fishes of Salminus genus. Moreover, this
study is the first record of R. bulbovaginatus in S.
hilarii broadening the range of the geographical
distribution and occurrence of the genus
According to Boeger et al. (1995) two genera of
Dactylogyridae are known as parasites of the
nasal cavities of Characiformes fishes of the
Neotropical region: Rhinonastes Kritsky et al.,
(1988b), and Rhinoxenus Kritsky, Boeger &
Thatcher, 1988. However, Urocleidoides naris
Rosim, Mendoza-Franco & Luque, 2011 (Rosim
et al., 2011) was recently described in the nasal
cavities of Hoplias malabaricus (Bloch, 1794)
from the Cuiabá River, Brazil. Monogenean
species of the genus Rhinoxenus are parasites of
the nasal cavity of Characiformes fishes of the
families Characidae, Anostomidae,
Prochilodontidae, Curimatidae (Domingues &
Boeger, 2005), which is corroborated in this
study due to the report of first occurrence of R.
bulbovaginatus in a characid fish of Taquari
river, Brazil.
DISCUSSION
338
2º ed., Eduem, Maringá, Brasil.
Neotropical Monogenea. 11.
Rhinoxenus, new genus (Dactylogyridae
Ancyrocephalinae) with descriptions of
three new species from the nasal cavities
of Amazonian Characoidea. Proceedings
of the Biological Society of Washington,
vol. 101, pp. 87-94.
Rhinonastes pseudocapsaloideum
n. gen., n. sp. (Dactylogyridae,
Ancyrocephalinae), a nasal parasite of
Curimatã, Prochilodus nigricans Agassiz
(Cypriniformes, Prochilodontidae), in
Brazil. The Journal of Parasitology, vol.
74, pp. 695-698.
New and previously described
species of Urocleidoides (Monogenoidea:
Dactylogyridae) infecting the gills and
nasal cavities of Hoplias malabaricus
(Characiformes: Erythrinidae) from
Brazil. The Journal of Parasitology, vol.
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Kritsky, DC, Boeger, WA & Thatcher, VE.
1988a.
Kritsky, DC, Thatcher, VE & Boeger, WA.
1988b.
Rosim, DF, Mendoza-Franco, EF & Luque, JL.
2011.
Neotrop. Helminthol., 7(2), 2013
Rhinoxenus in freshwater fishes from
Neotropical region.
The authors thank the Coordenação de
Aperfeiçoamento Pessoal de Nível Superior
(AUX-PE-PNPD 3005/2010) and the Fundação
de Amparo a Pesquisa do Estado de São Paulo
(2012/20150-4 and 2011/22603-3) and Aline
Angelina Acosta for the English review.
ACKNOWLEDGEMENTS
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Rhinoxenus bulbovaginatus n. sp.
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Correspondence to author/ Autor para
correspondencia:
Rodrigo Bravin Narciso
Laboratório de Parasitologia de Animais
Silvestres/LAPAS, Departamento de Parasitologia,
Instituto de Biociências, Universidade Estadual
Paulista/UNESP, CEP 18618-970, Botucatu, SP,
Brazil.
E-mail / Correo electrónico:
rodrigobtu7@gmail.com
Received September 13, 2013.
Accepted November 9, 2013.
339
