Neotrop. Helminthol., 7(2), 2013
2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
TRINIBACULUM ALTIPARANAE SP. N., A NEW DACTYLOGYRID SPECIES (MONOGENEA) OF
THE ASTYANAX ALTIPARANAE (OSTEICHTHYES: CHARACIDAE) IN THE PEIXE RIVER,
SOUTHEASTERN BRAZIL
TRINIBACULUM ALTIPARANAE SP. N. UNA NUEVA ESPECIE DE DACTYLOGYRIDO
(MONOGENEA) DE ASTYANAX ALTIPARANAE (OSTEICHTHYES: CHARACIDAE) EN EL
RÍO PEIXE, SUDESTE DE BRASIL
a* a b
Vanessa Doro Abdallah , Rodney Kozlowiski de Azevedo & Reinaldo José da Silva
Abstract
This article describes a new species –Trinibaculum altiparanae sp. n. –found in the gills of the
Astyanax altiparanae Garutti & Britski, 2000. Fish were collected from the Peixe River in the
municipality of Anhembi, State of São Paulo, Brazil, in March 2010. This paper describes the third
species of the genus Trinibaculum. This new species is characterized by having an accessory
structure that does not articulate with the male copulatory organ (MCO). This accessory structure
has a basally bifid, well-curved distal end, tapered with a terminal flabellate piece. The male
copulatory organ is a simple tube with less than one ring coiled counterclockwise; two similar
curved dorsal bars; a ventral bar with concave ends and a posterior projection, a dorsal anchor with
a truncated deep root and a slightly curved shaft, a ventral anchor with a curved shaft and
differently shaped and sized hooks. Those features distinguish the new species from the two other
species previously described in this genus: Trinibaculum braziliensis Kritsky, Thatcher &
Kayton, 1980 was found parasitizing Brycon melanopterus (Cope, 1872) and Trinibaculum
rotundus Karling, Lopes, Takemoto & Pavanelli, 2011 was found parasitizing Schizodon borellii
(Boulenger, 1900).
key words: Ancyrocephalinae - Astyanax altiparanae - monogeneans - State of São Paulo - Trinibaculum altiparanae sp. n.
Suggested citation: Abdallah, VD, Azevedo, RK & Silva, RJ. 2013. Trinibaculum altiparanae sp. n., a new Dactylogyrid species
(Monogenea) of the Astyanax altiparanae (Osteichthyes: Characidae) in the Peixe river, Southeastern Brazil Neotropical
Helminthology, vol. 7, n°2, jul-dec, pp. 211 - 217. .
aUSC- Universidade Sagrado Coração, Bauru, São Paulo, Brasil, 17011-160
bUNESP- Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia, Botucatu, São Paulo, Brasil, 18618-970
E-mail: vanessaabdallah@ig.com.br
211
Abdallah et al.
Trinibaculum altiparanae a new species from Brazil
212
Resumen
Palabras clave: Ancyrocephalinae - Astyanax altiparanae - Estado de São Paulo - monogeneos -
Trinibaculum altiparanae sp. n.
Una nueva especie - Trinibaculum altiparanae sp. n. - se describe de las branquias de Astyanax
altiparanae Garutti & Britski, 2000. Los peces fueron recolectados en el río Peixe en el municipio
de Anhembi, São Paulo, Brasil, en marzo del 2010. Esta es la tercera especie del género
Trinibaculum que se describe. La nueva especie se caracteriza por tener una pieza accesoria no
articulada al órgano masculino copulador (COM), basalmente bífida y curva, el extremo distal
cónico con una pieza terminal flabelada. El órgano copulador masculino es un tubo simple y
envuelto con menos de una vuelta en dirección hacia la izquierda; barras dorsales similares y
curvadas; una barra ventral con extremo cóncavo y con proyección posterior; raíz del áncora
dorsal profunda y truncada y suavemente curvada; áncora ventral curvada y ganchos con diferente
forma y tamaño, que difiere de las otras dos especies previamente descritas en este género:
Trinibaculum braziliensis Kritsky, Thatcher & Kayton, 1980 que parasita a Brycon melanopterus
(Cope, 1872) y Trinibaculum rotundus Karling, Lopes, Takemoto & Pavanelli, 2011 que parasita
Schizodon borellii (Boulenger, 1900).
parasitizing the gill filaments of Schizodon
borellii (Boulenger, 1900) from the upper
Paraná River floodplain by Karling et al. (2011).
According to Kritsky et al. (1980), this genus
differs from all other Ancyrocephalinae because
it possesses two widely separated simple dorsal
bars, a dextroventral vagina, confluent intestinal
crura, and intercecal gonads. Astyanax
altiparanae (Garutti & Britski, 2000), a South
American species with relevant importance, is a
small-sized species (less than 20 cm in length)
found in all environments, but more abundant in
rivers and channel (Agostinho et al. 1997), is
considered a forage, serving as food for large-
sized fish species, in addition to piscivorous
mammals, reptiles, and birds that inhabit the
floodplains of rivers in general (Hann et al.
1997).
This paper provides the description of a new
species of Trinibaculum, a parasite found in the
gills of the A. altiparanae in the State of São
Paulo, Brazil.
In March 2010, eight specimens of A.
altiparanae were collected for the study of
monogeneans found in the Peixe River
Monogeneans are the most speciose and
diversified group of ectoparasites in the
neotropical actinopterygian fish (Cepeda &
Luque, 2010). In Brazil, the parasite fauna has
been described for only 17.3% of the fish
species, indicating that the total parasite
biodiversity of fish in the region is grossly
underestimated at present (Luque & Poulin,
2007). Thus, additional efforts at carrying out
studies on the biodiversity of such parasites are
relevant. The Peixe River (48º06'38”W; 22º
49'53.1”S) is a tributary on the left bank of the
middle Tiete River Basin in the region of Barra
Bonita, State of São Paulo, Brazil. The river
originates in the municipality of Torre de Pedra,
State of São Paulo, in the Basaltic Cuesta
Botucatu Environmental Preservation Area and
2
is a drainage basin corresponding to 584 km
running from North to South (Caramaschi,
1986). The Trinibaculum genus was originally
described by Kritsky et al. (1980) and the type
species (Trinibaculum braziliensis Kritsky,
Thatcher & Kayton, 1980) was recorded
parasitizing the gills of the Brycon melanopterus
(Cope, 1872) in the Januacá Lake near the city of
Manaus, State of Amazonas, Brazil. After that,
the Trinibaculum rotundus (Karling, Lopes,
Takemoto & Pavanelli, 2011) was described
INTRODUCTION
MATERIALS AND METHODS
213
Neotrop. Helminthol., 7(2), 2013
Diagnosis (based on 12 whole-mounted worms,
five stained with Gomori's trichrome and seven
mounted using Gray and Wess' medium) - Body
340 ± 20.9 (309–397; n = 12) long, fusiform,
robust; 86 ± 11.5 (70–94; n = 12) wide near
gonad level. Smooth tegument. Cephalic lobes
moderately developed; cephalic glands not
observed. Eyes 4, posterior pair smaller; eye
granules present near pharynx. Pharynx
spherical, 17 ± 2.6 (13–24; n = 11) in diameter;
short esophagus; intestinal ceca confluent
posterior to testis. Short peduncle; oval haptor
39 ± 5.3 (32–50; n = 12) long, 60 ± 5.1 (53–63; n
= 12) wide. Ventral anchor 37 ± 4.9 (36–39; n
=11) long, with superficial root more developed
than deep root, curved shaft, short point, base 13
± 1.6 (11–18; n = 11) wide. Dorsal anchor 10 ±
0.6 (8–12; n = 11) long, with elongated
superficial root and truncated deep root, slightly
curved shaft and point; base 7 ± 0.9 (6–9; n = 11)
wide. Ventral bar 31 ± 1.9 (29–33; n = 12) long,
slightly V-shaped, with concave ends, striated,
with posterior projection. Similar curved dorsal
bars, 11 ± 1.1 (9–14; n = 18) long. Hooks
different in shape and size, pair 3, 4 and 7 equal,
with curved shaft and point, dilated shank, FH
loop about ¼ of shank length; pairs 1, 2, 5, and 6
equal, with tapered shaft and point, dilated
shank, FH loop about ¾ shank length; hook pairs
3, 4 and 7–17 ± 2.2 (13–20; n = 18) long, pairs 1,
2, 5, and 6–10 ± 1.5 (8–11; n = 18). Gonads
intercecal, overlapping. Testis postgermarian,
subspherical 13 ± 2.1 (10–15; n = 4) in diameter.
Seminal vesicle a simple dilation of vas
deferens; prostatic reservoir saccate. The male
copulatory organ is a simple tube, curved with
less than one ring, counterclockwise, 68 ± 10.6
(51–75; n = 9) long. Accessory piece 19 ± 3.1
(16–22; n = 9) long, non-articulated to MCO,
bifid basally, with different ends, well curved,
distal end tapered with terminal flabellate piece.
Germarium sub-ovate 42 ± 6.9 (35–48; n = 4)
long, 20 ± 2.7 (16–27; n = 4) wide, vagina
dextroventral, heavily sclerotized, handcuff-
shape. Vitellaria dense, random in trunk, but
absent in the regions of the reproductive organs.
Type host - Astyanax altiparanae Garutti and
Britski, 2000 (Characiformes: Characidae).
Site of infestation - Gills.
(22º49'53.1”S; 48º06'38”W) in the municipality
of Anhembi, State of São Paulo, Brazil. Fish
were collected using nylon monofilament gill
nets with mesh sizes of 3 to 14 cm at 3 different
sites on the river: river mouth, pond and river
channel. The nets were deployed at 1700 and
removed at 0700 the following day for a total
exposure time of 14 hours. Each fish was placed
in a separate plastic bag and kept in coolers until
necropsy. The gills were removed and the gill
arches were separated, then placed in a vial and
flooded with hot water (60° C to 70° C). The vial
was vigorously shaken to detach parasites from
the gills. After one hour, absolute alcohol was
added to the vials in order to fixate the
monogeneans, second procedures of Boeger &
Vianna (2006).
Some specimens were stained with Gomori's
trichrome and mounted with Canada balsam and
others were mounted using Gray and Wess'
medium (Humason, 1979) for the study of
sclerotized structures. Differential interference
contrast microscopy (Leica DMLB 5000, Leica
Microsystems, Wetzlar, Germany) was used for
the morphologic examination. Measurements
were obtained using a computerized image
analysis system (LAS, Leica Microsystems).
Measurements (in micrometers) were expressed
as the mean ± standard deviation followed by the
range and the number of specimens measured in
parentheses. The illustrations were made with
the aid of a camera lucida mounted on a Leica
DMLS microscope. Type specimens were
deposited at Instituto Nacional de Pesquisas da
Amazônia (INPA), Manaus, State of Amazonas,
Brazil and at Coleção Helmintológica do
Instituto de Biociências de Botucatu (CHIBB),
Botucatu, São Paulo, Brazil with numbers
Holotype INPA 586, Paratypes INPA 587a, b;
Paratypes CHIBB 052L, 053L and 054L.
Dactylogyridae Bychowsky, 1933
Ancyrocephalinae Bychowsky, 1937
Trinibaculum Kritsky, Thatcher & Kayton, 1980
Trinibaculum altiparanae sp. n.
(Figs. 1A-I; 2A-D)
RESULTS
Figure. 1. Trinibaculum altiparanae sp. n. (A) Whole worm, ventral view. (B) Ventral bar. (C) Vagina. (D) Ventral anchor. (E)
Dorsal anchor. (F) Dorsal bar. (G) Male copulatory complex: MCO and accessory piece. (H) Hook pair 1. (I) Hook pair 3.
Abdallah et al.
Trinibaculum altiparanae a new species from Brazil
214
215
Figure. 2. Trinibaculum altiparanae sp. n. (A) Whole worm, ventral view. (B) Haptor showing ventral anchor (arrow). (C)
Haptor showing striations on ventral bar (arrow) and dorsal anchor and bar (dotted arrow). (D) Haptor showing posterior
projection in ventral bar (arrow).
projections in T. braziliensis), dorsal anchor
with truncated deep root and slightly curved
shaft (dorsal anchor with spine-shaped deep root
and short straight shaft in T. braziliensis), ventral
anchor with curved shaft (ventral anchor with
straight shaft in T. braziliensis), hooks differents
in shape and size (equal in T. braziliensis), shape
of body fusiform (subtriangular in T.
braziliensis) and gonads overlapping (tandem in
T. braziliensis). The new species differs from T.
rotundus in possessing the vagina dextroventral,
heavily sclerotized, handcuff-shape (vagina
dextrolateral slightly sclerotized ending at level
of seminal receptacle in T. rotundus), male
copulatory organ a simple tube, coiled with less
than one ring, counterclockwise (copulatory
organ coiled with 1.5 clockwise rings in T.
rotundus), body fusiform and robust (body disk-
shape with absence of haptor peduncle in T.
Type locality - Peixe River (22º49'53.1”S;
48º06'38”W), municipality of Anhembi, São
Paulo State, Brazil.
Prevalence: 50%
Mean Intensity: 2.4 ± 0.3
Specimens deposited - Holotype INPA 586,
Paratypes INPA 587a, b; Paratypes CHIBB
052L, 053L and 054L.
Etymology - The specific designation
altiparanae refers to the specific name of the
type-host.
Taxonomic discussion - Trinibaculum
altiparanae sp. n. differs from T. braziliensis in
possessing the accessory piece non-articulated
to MCO, bifid basally, well curved, distal end
tapered with terminal flabellate piece (broadly
articulated to proximal portion of male
copulatory organ in T. braziliensis), ventral bar
with posterior projection (without posterior
Neotrop. Helminthol., 7(2), 2013
216
Vazzoler, AEAM, Agostinho, AA & Hahn,
NSA. Planície de inundação do alto rio
Paraná: aspectos físicos, biológicos e
socioeconômicos. Maringá: EDUEM.
p.179-208.
Monogenoidea. In Thatcher, VE. Amazon
Fish Parasites. Sofia: Pensoft Publishers.
p. 42-116. Distribuição da
ictiofauna de riachos das Bacias do Tietê
e do Paranapanema, junto ao divisor de
águas (Botucatu, SP). Tesis de Doctor en
Ecologia e Recursos Naturais,
Universidade Federal de São Carlos, São
Carlos. Three new
species of Demidospermus (Monogenea:
Da c tyl ogy rid a e) par asi tic o n
Brachyplatystoma filamentosum
(Siluriformes: Pimelodidae) from the
Araguaia River, Brazil. Journal of
Parasitology, vol. 96, pp. 869-873.
Ecologia trófica. In: A
planície de inundação do Alto rio Paraná:
aspectos físicos, biológicos e
socioeconômicos. (Eds. Vazzoler, AEAM
Agostinho, AA & Hahn, NSA). pp. 209-
228. Maringá: EDUEM. Animal tissue
techniques. W.H. Freeman Co.,
California.
Trinibaculum
rotundus n. s p. ( Mono gene a,
Ancyrocephalinae), a parasite of
Schizodon borellii (Characiformes,
Anostomidae) from the upper Paraná
River floodplain, Brazil. Helminthologia,
vol. 48, pp. 85-87.
Neotropical Monogenoidea. 3. Five new
species from South America with the
proposal of Tereancistrum gen. n. and
Trinibaculum gen. n. (Dactylogyridae:
Ancyrocephalinae). Acta Amazônica, vol.
10, pp. 411-417. Metazoan parasite
species richness in Neotropical fishes:
Boeger, WA & Vianna, RT. 2006.
Caramaschi, EP. 1986.
Cepeda, PB & Luque, JF. 2010.
Hahn, NS, Andrian, IF, Fugi, R & Almeida,
VLL. 1997.
Humason, GL. (ed). 1979.
Karling, LC, Conceição Lopes, LP, Takemoto,
RM & Pavanelli, GC. 2011.
Kritsky, DC, Thatcher, VE & Kayton, RJ. 1980.
Luque, JL & Poulin, R. 2007.
rotundus), peduncle present (absent in T.
rotundus), ventral bar with posterior projections
(without in T. rotundus) and hooks differents in
shape and size (equal in T. rotundus).
The new species presented here is allocated to
Trinibaculum based on the main characters of
the genus presented by Kritsky et al. (1980) and
Boeger & Vianna (2006), i. e., gonads tandem,
vagina dextro-ventral, ventral bar slightly V-
shaped and dorsal bar double; anterior, posterior
projections absent. However, the Trinibaculum
altiparanae sp. n. presents three characteristics
different of this genus: (i) an accessory piece not
directly articulated to the MCO (also observed in
the Trinibaculum rotundus); (ii) a ventral bar
with posterior projection; and (iii) hooks thet are
different in shape and size - which can be
perfectly justified because Kritsky et al. (1980)
relied on the observation of a single species that
was being described then, the Trinibaculum
braziliensis to make the diagnosis of the genus.
The authors would like to thank Ricardo
Massato Takemoto from UEM (Universidade
Estadual de Maringá) for providing slides of
Trinibaculum rotundus for observation and
comparison with our species and Elisa Pinto de
Oliveira for editing the English. Vanessa D.
Abdallah was supported by a student fellowship
from FAPESP (2009/51726-6), Rodney K. de
Azevedo was supported by a student fellowship
from FAPESP (2010/06564-5), and Reinaldo
José da Silva was supported by a Research
fellowship from CNPq (312590/2009-1) and
FAPESP (2009/53316-0).
ACKNOWLEDGMENTS
BIBLIOGRAPHIC REFERENCES
Agostinho, AA, Júlio Júnior, HF, Gomes, LC,
Bini, LM & Agostinho, CS. 1997.
Composição, abundância e distribuição
espaço-temporal da ictiofauna. In:
Abdallah et al.
Trinibaculum altiparanae a new species from Brazil
Neotrop. Helminthol., 7(2), 2013
Hotspots and the geography of
biodiversity. Parasitology, vol. 134, pp.
865-878.
Correspondence to author/ Autor para
correspondencia:
Vanessa Doro Abdallah
USC- Universidade Sagrado Coração, Bauru, São
Paulo, Brasil. 17011-160
R. Irmã Arminda, 10050 - Vila Brunhari Bauru,
17011-160. Tel.: +55 11 21077297.
E-mail / Correo electrónico:
vanessaabdallah@ig.com.br
Received June 5, 2013.
Accepted September 6, 2013.
217
