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Neotrop. Helminthol., 7(1), 2013
2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HIRUDINELLA VENTRICOSA (TREMATODA) PARASITIZING MAKAIRA NIGRICANS AND
ACANTHOCYBIUM SOLANDRI FROM NEOTROPICAL REGION, BRAZIL
HIRUDINELLA VENTRICOSA (TREMATODA) PARASITANDO MAKAIRA NIGRICANS Y
ACANTHOCYBIUM SOLANDRI DE LA REGIÓN NEOTROPICAL, BRASIL
Abstract
In January 2002, were caught 11 Makaira nigricans Lacepède, 1802 (Istiophoridae) and two
Acanthocybium solandri (Cuvier, 1832) (Scombridae) off Cabo Frio municipality, Rio de Janeiro
State, Brazil. We collected digenetic trematodes from the stomach of some of these fishes. We
studied these trematodes with optical and scanning electron microscopy and identified them as
Hirudinella ventricosa (Pallas, 1774) Baird, 1835. This is the first report of this species in A.
solandri in the Brazilian coast, and in M. nigricans in South America.
Keywords: Acanthocybium solandri - Brazil - Hirudinella ventricosa - Makaira nigricans - Neotropical region.
Suggested citation: Felizardo, NN, Knoff, M, Torres, EJL, Pimenta, EG, Amorim, AF & Gomes, DC. 2013. Hirudinella
ventricosa (Trematoda) parasitizing Makaira nigricans and Acanthocybium solandri from neotropical region, Brazil.
Neotropical Helminthology, vol. 7, N°1, jan-jun, pp. 75 - 82.
1Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz - IOC, Rio de Janeiro, RJ, Brasil
2Laboratório de Biologia de Helmintos Otto Wucherer, Universidade Federal do Rio de Janeiro - UFRJ, Rio de Janeiro, RJ, Brasil
3Curso de Engenharia Ambiental, Universidade Veiga de Almeida - UVA, Cabo Frio, RJ, Brasil
4Agência Paulista de Tecnologia dos Agronegócios - APTA, Instituto de Pesca - IP, Santos, SP, Brasil
1 1* 2 3
Nilza Nunes Felizardo , Marcelo Knoff Eduardo José Lopes Torres , Eduardo Gomes Pimenta , Alberto Ferreira de
, 4 1
Amorim & Delir Corrêa Gomes
Resumen
En enero del 2002, fueron capturados 11 Makaira nigricans Lacepède, 1802 y dos Acanthocybium
solandri (Cuvier, 1832) en la costa del municipio de Cabo Frio, Rio de Janeiro, Brasil. Del
estómago de algunos de estos peces fueron colectados trematodos digenéticos. Después del
análisis macroscópico y microscópico de la morfología y la morfometría de las estructuras
externas e internas de los helmintos, mediante estereoscópio, microscopio de campo claro, de
cortes histológicos coloreados con hematoxilina-eosina, y microscopio electrónico de barrido, los
especímenes fueron identificados como pertenecientes a la especie Hirudinella ventricosa
(Pallas, 1774) Baird, 1835. Este es el primer reporte de esta especie en A. solandri en la costa
brasileña, y en M. nigricans en América del Sur.
Palabras clave: Acanthocybium solandri - Brasil - Hirudinella ventricosa - Makaira nigricans - región Neotropical.
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Hirudinella parasitizing Makaira and Acanthocybium Felizardo et al.
The present study had as the starting point the
Marlin Project (Pimenta et al., 2001) aimed to
study the biology of sport fishing in the
municipality of Cabo Frio, Rio de Janeiro,
Brasil, in competitions sponsored by Iate Clube
de Cabo Frio. This project consisted of
researchers from Grupo de Estudos de Pesca
(GEPESCA); Coordenação de Programas de
Pós-Graduação em Engenharia (COPPE),
Universidade Federal do Rio de Janeiro;
Instituto de Pesca de São Paulo (IP-SP); The
Billfish Foundation (TBF); International
Comission for Conservation of Atlantic Tunas
(ICCAT); students of biology and correlated
sciences and off shore sports fishermen. On this
occasion were caught some blue marlin,
Makaira nigricans Lacepède, 1802, and wahoo,
Acanthocybium solandri (Cuvier, 1831). In the
stomach contents of these fish was found a
species of worm, that was collected and
preserved for identification.
Makaira nigricans is the largest billfish, length
reaches around 5.0 m and about 820 Kg, being
target in sport fishing and appreciated as food
(Figueiredo & Menezes, 2000; Pimenta et al.,
2001; Froese & Pauly, 2012). Acanthocybium
solandri (Cuvier, 1831) reaches 2.10 m in length
and 83 kg, their meat is commercialized fresh or
canned. Both are pelagic fish, migratory and
oceanic, known as agile swimmers, inhabit
tropical and subtropical seas. In the Brazilian
coast occurs mainly in running waters in the
Southeast. Their diets consist mainly of fish like
tuna, dolphinfish, flying fish and squid
(Figueiredo & Menezes, 2000; Pimenta et al.,
2001; Froese & Pauly, 2012).
Therefore the aim of this study was to identify
stout digenetic trematodes found in the stomachs
of M. nigricans and A. solandri, from off shore
sport fishing, providing new data on the
morphology and morphometry through
observation of whole specimens in a
stereomicroscope and scanning electron
microscope, and of histological sections in a
bright field microscope.
INTRODUCTION
In January 2002 were caught 11 Makaira
n i g r i c a n s Lacepède, 1802 and two
Acanthocybium solandri (Cuvier, 1832) off
Cabo Frio municipality, Rio de Janeiro State,
Brazil (22º52'46"S, 42º01'07"W), by fishermen,
during the off shore sport fishing tournament of
the “Iate Club do Rio de Janeiro”. These fishes
were necropsied and their stomachs collected
and labeled. In the stomach content from both
fish was found a species of digenetic trematode.
The helminths were fixed and preserved
according to the usual technics in helminthology
(Eiras et al., 2006), after they were analyzed by
stereosmicroscopic, and a specimen was
included in paraffin and sectioned at 7 µm of
thickness and stained with hematoxylin and
eosin (HE) for histological study of internal
structures of taxonomic interest. Observations
were made using a Zeiss stereomicroscope and a
Z e i s s A x i o p h o t m i c r o s c o p e a n d
photomicrographs were taken with a Canon
digital camera attached. Measurements are
presented in millimeters (mm) and were made
with the aid of an Olympus BX 41 microscope
with a micrometric ocular. Range of
measurements is presented followed by the
mean in parentheses. For the study of scanning
electron microscopy (SEM), a specimen was
dehydrated in a graded ethanol series (20º-100º
GL) for one h each step, critical-point dried in
CO , mounted on metallic stubs and coated with
2
gold (20-25 nm deposited). The sample was
examined under FEI Quanta 250 scanning
electron microscope, operating at 25 kV. The
taxonomic classification was made according to
Gibson (2002). Comparison was made with a
specimen of H. ventricosa deposited in the
“Coleção Helmintológica do Instituto Oswaldo
Cruz” (CHIOC), Fiocruz, Rio de Janeiro State,
Brazil, under the number 32140 CHIOC. The
terminology adopted for forebody and hindbody
follows the pattern used by Manter (1970).
Representative specimens preserved in ethanol
70 ºGL and histological sections of a specimen
were included in CHIOC under no. 34884-
34887, and 37.808a-d. Parasitological
MATERIAL AND METHODS
Neotrop. Helminthol., 7(1), 2013
parameter of intensity of infection follows Bush
et al. (1997).
The analyse of the stomach contents from two of
11 M. nigricans (Istiophoridae) and from the two
A. solandri (Scombridae) necropsied fishes
were found a total of 17 helminth specimens (8
from M. nigricans and 9 from A. solandri), with
3-5 and 2-7 of range of infection, respectively,
belonging to a species of adult digenetic
trematode identified beneath.
Hemiuroidea Looss, 1899 in part
(Hirudinellidae Dollfus, 1932)
Hirudinellidae Dollfus, 1932
Hirudinella ventricosa (Pallas, 1774) Baird,
1835 (Figs. 1-8).
Main morphological characteristics: Body stout,
elongate or keyhole-shaped. Body surface
strongly marked with transverse folds and
wrinkles, papillae mainly present in forebody.
Forebody is narrower and shorter than hindbody.
Oral sucker sub-terminal, well developed, opens
directly into the pharinx. Pharinx well
developed ans oesophagus short. Ventral sucker,
well developed, higher than oral sucker. Gut-
caeca fused subterminally, forming cyclocoel.
Uroproct present. Testes two, small, oblique, in
anterior hindbody, pre-ovarian. Seminal vesicle
thin-walled, tubular, convoluted, in the
forebody, antero-dorsally to anterior margin of
ventral sucker; pars prostatica, tubular,
convoluted, surrounding the distal seminal
vesicle. Ejaculatory duct long, muscular,
surrounded by 'cirrus-sac' muscular, opens in a
genital atrium. Genital pore midventral, close to
the midle of forebody, with small aperture.
Ovary oval, post-testicular, in anterior
hindbody; Mehlis' gland present. Uterus mainly
intercaecal, coils extending posteriorly from
ovary to near posterior limit of vitellarium;
metratermo opens into the genital atrium,
imediataly posterior to ´cirrus'. Eggs small,
numerous. Vitellarium, composed of convoluted
tubules, in two lateral fields, caecal, between
levels of testes and mid-hindbody. Excretory
pore, terminal present.
The morphometric data of specimens of H.
ventricosa are presented in Table 1.
RESULTS
Table 1. Morphometric data (mm) of specimens of H. ventricosa from Makaira nigricans and Acanthocybium
solandri off the coast of Cabo Frio, State of Rio de Janeiro, Brazil.
Hosts M. nigricans* M. nigricans** A. solandri**
Body length 17.4 15.5-27.5 (21.6) 28-59 (29.7)
Body depth or width 5.2 6-7 (6.8) 7-22 (15.8)
Forebody 4.3 3-4 (3.6) 4-11 (7.3)
Hindbody 10.4 7-17 (12.2) 18-45 (25.9)
Oral sucker 1.4 x 1.5 1-1.2 (1.1) x 1 1-2.5 (1.7) x 1-3 (2.1)
Ventral sucker 4.6 x 2.8 5-7(5.8) x 4-7 (5.6) 4-7 (5.4) x 3-6.5 (5.1)
Pharynx 1.3 x 1.1 - -
Testes (depth) 0.5 x 2.2 - -
Ovary (depth) 0.4 x 0.9 - -
Eggs 0.03 x 0.02 - -
*Measurements from specimens of histological sections (length x depth).
** Measurements from specimens preserved in ethanol 70 ºGL (length x width).
77
Hirudinella parasitizing Makaira and Acanthocybium Felizardo et al.
Figure 1. Hirudinella ventricosa from Acanthocybium solandri. Scale bar = 1 mm.
Figure 2. Hirudinella ventricosa from Makaira nigricans. Scale bar = 1mm.
78
Neotrop. Helminthol., 7(1), 2013
Figures 3-4. Hirudinella ventricosa from Makaira nigricans, histological sections in HE. Fig. 3. Entire worm at mid longitudinal
section: oral sucker (OS), pharynx (Ph), ventral sucker (VS), one of the testes (T), seminal vesicle (SV), pars prostatica (PP),
'cirrus-sac' (CS), ovary (O), atrium (A), uroproct (UR). Scale bar = 5 mm. Fig. 4. Detail of forebody and anterior portion of
hindbody of the species, oral sucker (OS), pharynx (Ph), ventral sucker (VS), one of the testes (T), seminal vesicle (SV), pars
prostatica (PP), 'cirrus-sac' (CS), ovary (O), metraterm (M), atrium (A), genital pore (GP). Scale bar = 1.5 mm.
79
Hirudinella parasitizing Makaira and Acanthocybium Felizardo et al.
80
Figures 5-8. Hirudinella ventricosa from Makaira nigricans by SEM. Fig 5. Entire worm latero-ventral view. Scale bar = 2.5
mm. Fig. 6. Details of forebody surface: oral sucker (OS), genital pore (GP), ventral sucker (VS). Scale bar = 1.5 mm. Fig 7.
Forebody, detail of tegument near of oral sucker (OS) and genital pore (GP) showing folds, wrinkles and papillae. Fig. 8. Detail of
wrinkles surrounded excretory pore (EP). Scale bars of figs. 7 and 8 = 0.5 mm.
The collected specimens in M. nigracans and A.
solandri of the present study are in accordance
with the morphological and morphometric data
of species H. ventricosa found in most previous
descriptions from several marine fish, mainly
scombroids (Nigrelli & Stunkard, 1947; Gibson,
1976; Fernandes & Kohn, 1984). Other records
have indicated greater lengths from 80 to 170
mm and widths of 30 to 40 mm in fixed
specimens, demonstrating a wide range in body
size (Gibson & Bray, 1977; Romeo et al., 2005).
The SEM held in this study showed body
papillate mostly in forebody and add new details
of genital and excretory pores beyond previous
observations (Nigrelli & Stunkard, 1947;
Gibson & Bray, 1977).
Hirudinella ventricosa was reported in M.
nigricans from Puerto Rico (Williams Jr &
Bunkley-Williams, 1996), and for A. solandri by
Manooch and Hogart (1983) collected in the
Gulf of Mexico and in the States of Florida and
DISCUSSION
Neotrop. Helminthol., 7(1), 2013
North Carolina, Atlantic coast of the United
States; Romeo et al. (2005) recorded in the
Mediterranean Sea, Italy; Kohn et al. (2007)
listed it in Galapagos and Venezuela, and a
further six species of scombroids in South
America, also in Coryphaena hippurus
(Diesing, 1850), Coryphaenidae, in Brazilian
coast. This is the first record of that species in A.
solandri, on the Brazilian coast, and in M.
nigricans in South America.
This study was limited to research with the
parasites of hosts provided by Marlim Project,
which follows the recommendations of the
International Commission for Conservation of
Atlantic Tunas.
Records of H. ventricosa showed it occuring in
various populations of migratory marine fish,
mainly scombroid, suggesting it such as a
biomarker able in identification of these fish
populations (Manooch & Hogart, 1983;
Eggleston & Bochenek, 1990; Mosquera et al.,
2003). The finding of this helminth in M.
nigracans and A. solandri in the present study
corroborates with these records, showing these
helminths have a preference with the large
migratory fishes.
The authors are grateful to Heloisa Maria Diniz
of “Serviço de Produção e Processamento de
Imagens /IOC/FIOCRUZ”, for assisting with
preparation of plates of figures, and to
Wanderley de Souza of CENABIO III (Centro
de microscopia of Universidade Federal do Rio
de Janeiro) for facilitate the use of SEM.
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Received January 21, 2013.
Accepted March 11, 2013.
*Correspondence to author/ Autor para
correspodencia:
Marcelo Knoff
Laboratório de Helmintos Parasitos de Vertebrados,
Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil
4365, CEP 21045-900 Manguinhos, Rio de Janeiro,
RJ, Brasil. Phone: 55(21)2562-1462
E-mail/correo electrónico:
knoffm@ioc.fiocruz.br
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