ORIGINAL ARTICLE /ARTÍCULO ORIGINAL
FIRST RECORD OF UNITUBULOTESTIS PELAMYDIS (TREMATODA:
DIDYMOZOIDAE) AND SPHYRIOCEPHALUS TERGESTINUS (CESTODA:
SPHYRIOCEPHALIDAE) IN EASTERN PACIFIC BONITO, SARDA CHILIENSIS
(PERCIFORMES: SCOMBRIDAE) IN PERU
PRIMER REGISTRO DE UNITUBULOTESTIS PELAMYDIS (TREMATODA:
DIDYMOZOIDAE) Y SPHYRIOCEPHALUS TERGESTINUS (CESTODA:
SPHYRIOCEPHALIDAE) EN EL BONITO DEL PACÍFICO, SARDA CHILIENSIS
(PERCIFORMES: SCOMBRIDAE) EN PERÚ
1,2 1,2 2,3 1 4 2
Jhon Chero ; Celso Cruces ; José Iannacone ; Gloria Sáez ; Lidia Sanchez ; David Minaya ;
2 5 6
Lorena Alvariño ; Carlos Mendoza-Vidaurre & José Luis Luque
1 Laboratorio de Parasitología. Facultad de Ciencias Naturales y Matemática (FCNNM). Universidad Nacional Federico
Villarreal (UNFV). El Agustino, Lima, Perú.
2 Laboratorio de Ecología y Biodiversidad Animal (LEBA). Facultad de Ciencias Naturales y Matemática (FCNNM).
Universidad Nacional Federico Villarreal (UNFV). El Agustino, Lima, Perú.
3 Facultad de Ciencias Biológicas. Universidad Ricardo Palma (URP). Santiago de Surco, Lima, Perú.
4Departamento de Protozoología Helmintología e Invertebrados Afines. Museo de Historia Natural, Universidad Nacional
Mayor de San Marcos (UNMSM). Javier Prado, Lima, Perú.
5 Laboratorio de Análisis Clínico Moraleslab SAC. Morales, San Martín, Perú.
6 Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro – UFRRJ,
Seropédica, RJ, Brasil.
Neotropical Helminthology, 2015, 9(2), jul-dec: 313-323.
ABSTRACT
Keywords: fish parasite - Sarda chiliensis - Sphyriocephalus tergestinus - Unitubulotestis pelamydis - Peru.
This study aims to report Unitubulotestis pelamydis (Taschenburg, 1879) (Trematoda:
Didymozoidae) and Sphyriocephalus tergestinus Pintner, 1913 (Trypanorhyncha:
Sphyriocephalidae) in Eastern Pacific bonito Sarda chiliensis (Cuvier) (Scombridae) from
Chorrillos, Lima, Peru (12º09'23” S, 77º01'55” W). One hundred specimens of S. chiliensis were
collected, 17 and 32 specimens were infected with U. pelamydis and S. tergestinus postlarvae in
the gill filaments and stomach, respectively. The total prevalence was 49%. The total mean
intensity of infection and abundance were 3.51 (1-12) and 1.72 (0-12), respectively. This is the
first record of U. pelamydis and S. tergestinus postlarvae in Peru.
313
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
RESUMEN
Palabras clave: fish parasite - Sarda chiliensis - Sphyriocephalus tergestinus - Unitubulotestis pelamydis - Perú.
Este estudio tuvo como objetivo registrar Unitubulotestis pelamydis (Taschenburg, 1879)
(Trematoda: Didymozoidae) y Sphyriocephalus tergestinus Pintner, 1913 (Trypanorhyncha:
Sphyriocephalidae) en el bonito del Pacífico Sarda chiliensis (Cuvier, 1832) (Scombridae) en
Chorrillos, Lima, Perú (12º09'23 "S, 77º01'55" W). Se colectaron cien especímenes de S.
chiliensis, 17 y 32 especímenes fueron infectados con U. pelamydis y S. tergestinus en los
filamentos branquiales y el estómago, respectivamente. La prevalencia total fue de 49%. La
intensidad y la abundancia media total de la infección fueron de 3,51 (1-12) y 1,72 (0-12),
respectivamente. Este es el primer registro de U. pelamydis y S. tergestinus en Perú. Además, S.
chiliensis es un nuevo huésped para ambos endoparásitos.
INTRODUCTION
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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015
Eastern Pacific bonito, Sarda chiliensis
(Cuvier, 1832) is an epipelagic neritic fish
distributed from Colombia to Chile and
assessed by IUCN as Least Concern, but its
current population trend is decreasing
(Ancieta, 1964; Chirichigno & Vélez, 1998;
Collette et al., 2011). This species is very
common in coastal zone of Punta Aguja (Peru)
and Iquique (Chile) (Chirichigno & Vélez,
1998). Collette & Nauen (1983) indicated that
Eastern Pacific bonito S. chiliensis is a marine,
pelagic-neritic, oceanodromous and
subtropical species. Length at first maturity is
47 cm. Also, the validity of the subspecies S.
chiliensis chiliensis status is not supported by
the molecular data (Viñas et al., 2010).
Scarce records of parasites of S. chiliensis are
registered in the South Pacific (Tantaleán &
Huiza, 1994; Pérez et al., 1999; Kohn et al.,
2007; Muñoz & Olmos, 2008; Cohen et al.
2013). In this paper, we present the first record
of two endoparasites species, Unitubulotestis
pelamydis (Taschenburg, 1879) and
Sphyriocephalus tergestinus Pintner, 1913 in
Eastern Pacific bonito from Peru.
MATERIAL AND METHODS
Chero et al.
Between January 2013 and December 2014,
100 specimens of S. chiliensis were
necropsied, from the coast of Chorrillos, Lima,
Perú (12º09'23” S, 77º01'55” W), to study their
parasites. Trematodes and cestodes were
extracted from the gills and stomach,
respectively. The parasites obtained were
placed in petri dishes with saline, fixed and
pr e s er v e d i n et h a no l ( 70 % ) . F o r
morphological study, the parasites were
stained with Semichon's acetocarmine and
mounted in Canada balsam for examination as
whole mounts. The parasites were analyzed
and measured using a Microscope leica -
DM500 with camera LEICA - ICC50 HD
Software LAS (Leica Application Suite)–EZ
vers ión 1.8 0, 2 009 , Sw itzer tla nd.
Measurements were made in millimeters
(mm). The taxonomic determination of the
parasites was in accordance with the diagnosis
proposed by Nikolaeva (1980) for trematodes
and Costa et al. (2003) for cestodes. Scolex and
hook measurements follow Palm (1999), Palm
& Walter (2000) and Costa et al. (2003). The
terminology of larval cestodes follows Chervy
(2002). The ecological descriptors of
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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015
slightly sharp. Cuticle thin and smooth. Oral
sucker terminal, 0.230-0.259 (0.244±0.02)
long by 0.225-0.263 (0.246±0.02) wide with
poorly developed muscles. Pharynx 0.199-
0.260 (0.233±0.03) long by 0.176-0.223
(0.202±0.02) wide. Short esophagus. Intestinal
blind long, sinuous, reaching the posterior end
of the body. Acetabulum absent. One tubular,
long, sinuous testicle, located in the anterior
end of the body; with the narrower posterior
end, 1.385-2.631 (1.901±0.65) long by 0.282-
0.907 (0.586±0.31) wide. Ovary tubular.
vitelline gland tubular and single. Uterus very
long, with long handles, occupying almost the
entire length of the body. Eggs elliptical, rather
thin-shelled and embryonated, 0.013-0.017
(0.015±0.002) long by 0.00 -0.010
(0.009±0.001) wide.
Host: Sarda chiliensis Eastern Pacific bonito.
Site of infection: Encysted in pairs on the gill
filaments.
Locality: Chorrillos, Lima, Peru, 12º09'23” S,
77º01'55” W.
Specimens deposited: Voucher MUSM-
UN M S M 3 2 48 . Vo u ch e r CP Y M P-
UNFV178a-c.
Mean Intensity of infection: 3.65.
Prevalence: 17%.
Remarks: Yamaguti (1953) erected the genus
Unitubulotestis, with the original description
of Unitubulotestis carangis Yamaguti, 1953 of
the region pharynx-branchial from Carax sp.
(Carangidae) in Indonesia. This genus is
characterized by a single tubular, long and
winding testicle, caeca simple reach close to
posterior extremity, and gland-cells may
surround anterior parts of alimentary system
(Bray et al., 2008). Unitubulotestis pelamydis
(Taschenburg, 1879) was initially described as
Didymozoon pelamydis by Taschenberg
(1879). Later, Ishii (1935) transferred D.
pelamydis to genus Nematobothrium.
Subsequently, Nikolaeva (1980) considered N.
pelamydis within the genus Unitubulotestis,
based on the presence of a single testicle.
parasitism (prevalence, abundance and mean
intensity of infection) were calculated
according to Bush et al. (1997).
Part of the collected material is deposited in the
Helminthological Collection and Related
Invertebrates of the Museum of Natural
History at the San Marcos University (MUSM-
UNMSM) and in Scientific Collection of
Protozoa and Metazoan Parasites of the
Federico Villarreal University (CPMP-
UNFV), Peru.
The mean total length and weight of the fish
analyzed were 39.94 ± 2.98 (32 48) cm and
645.74 ± 161.15 (425-1100) g, respectively.
Seventeen and thirty-two S. chiliensis
chiliensis specimens were infected by U.
pelamydis (prevalence = 17%) and S.
tergestinus postlarvae (prevalence = 32%),
respectively. One hundred and seventy one
endoparasites were collected in the studied
specimens and the total prevalence was 49%.
The total mean intensity of infection and
abundance were 3.51 (1-12) and 1.72 (0-12),
respectively.
Phylum Platyhelminthes Minot, 1876
Class Trematoda Rudolphi, 1808
Subclass Digenea Carus, 1863
Order Plagiorchiida La Rue, 1957
Family Didymozoidae Monticelli, 1888
Genus Unitubulotestis Yamaguti, 1953
Unitubulotestis pelamydis (Taschenburg,
1879)
(Figure 1)
Description (Based on 6 adult specimens
colored, mounted and five specimens
measured): Trematodes with long body,
cylindrical, filiform and hermaphrodite; with
yellowish color, due to the presence of eggs,
35-51 (44±5.1) long, with a maximum width of
2.074-2.295 (2.180.11); posterior end
RESULTS
First record of Unitubulotestis and Sphyriocephalus
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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Chero et al.
mounted and five specimens measured): Body
5.94-11.2 (9.40±2.07) mm long. Scolex
craspedote with two circular bothridia, 1.28-
1.55 (1.42±0.13) mm in diameter. Four armed
tentacules, 1.50-1.70 (1.61±0.07) mm in
length. The apical portion of each tentacle is
armed with four hooks in the center, these
hooks measured 0.024-0.025 (24.67±0.5) mm
long. The metabasal armature is composed of
approximately 16-18 longitudinal rows of
curved and point falciform shaped hooks.
These hooks measured 0.054-0.068
(0.068±0.051) mm long. The hooks
arrangement in the metabasal armature was in
spiral rows. The basal armature has about 30-
32 rows of falciform shaped hooks, smaller
than those of the metabasal armature,
measured 0.027-0.029 (0.028±0.014) mm
long. Pars vaginalis and pars bulbosa short.
The sheaths of the tentacles are curved and not
sinuous.
Host: Sarda chiliensis Eastern Pacific bonito.
Site of infection: Stomach.
Locality: Chorrillos, Lima, Peru 12º09'23” S,
77º01'55” W.
Specimens deposited: Voucher MUSM-
U N M S M 3 2 4 9 . Vo u c h e r C P Y M P -
UNFV179a-d.
Mean Intensity of infection: 3.41.
Prevalence: 32%.
Remarks: The specimens described in this
paper show the scolex similar to those
described in the genus Sphyriocephalus
Pintner, 1913. This genus is characterized by
having a scolex craspedote with velum. Two
deep, oval bothridia encircled by thickened
rims. Tentacules short and armature
homeoacanthous. Pars vaginalis and pars
bulbosa short (Heinz & Dailey, 1974;
Beveridge & Campbell, 1996).
The genus Sphyriocephalus has not previously
been reported from Peruvian waters (Table 1)
(Tantaléan & Huiza, 1994). The specimens
studied here are in accordance with the
Furthermore, He mentions that U. sardae,
initially described as N. sardae by MacCallum
& MacCallum (1916) and transferred to the
genus Unitubulotestis by Yamaguti (1953), is
synonymous of U. pelamydis. Seven species
currently are recognized, they are: U. carangis
(Type-species); Unitubulotestis istiophorusi
Nikolaeva & Dubina, 1985; Unitubulotestis
laymani Nikolaeva & Parukhin, 1971;
Unitubulotestis maris Caballero & Caballero,
1971; Unitubulotestis parupenei Yamaguti,
1970; Unitubulotestis pelamydis (=
Unitubulotestis sardae) (Taschenburg, 1879)
and Unitubulotestis spilonotopteri Yamaguti,
1970 (Yamaguti, 1953; Yamaguti, 1970;
Nikolaeva, 1981; Nikolaeva & Dubina, 1985;
Bray et al., 2008). All species are registered in
buccal and branchial tissues, body-cavity and
mesenteries of carangid, istiophorid,
scombrid, mulled and exocoetid fishes (Bray et
al., 2008).
In South America, U. pelamydis (= U. sardae)
has been registered on the gill filaments of
Sarda sarda (Bloch, 1793) off the coast of
Brazil (Hsu, 1968; Justo & Kohn, 2005; Alves
& Luque, 2006; Kohn et al. 2007). In Peru,
Unitubulotestis sp. has been registered on the
gill filaments of S. chilensis and in the
operculum of Scomber japonicus Houttuyn,
1782 from North Zone (Tantaleán & Huiza,
1994). However, species of the genus
Unitubulotestis in the Peruvian coast are
unknown (Gómez del Prado-Rosas et al.,
2007); U. pelamydis is the first species
recorded and a new record to the South Pacific.
Also, S. chilensis is a new host.
Clase Cestoda Rudolphi, 1808
Subclase Eucestoda Southwell, 1930
Orden Trypanorhyncha Diesing, 1863
Familia Sphyriocephalidae Pintner, 1913
Género Sphyriocephalus Pintner, 1913
Sphyriocephalus tergestinus Pintner, 1913
(Figura 2-4)
Description (Based on 10 postlarvae colored,
DISCUSSION
317
description given by Costa et al. (2003) for
postlarvae of S. tergestinus, except that the
length of tentacles, hooks of the metabasal and
basal armature in our specimens was slightly
greater. However, based on the number of rows
of hooks in the metabasal armature, circular
bothridia (Costa et al., 2003) and the size of the
bulbs (about twice as long as wide) these
postlarvae are tentatively attributed to S.
tergestinus.
The S. tergestinus postlarvae had been
recovered of six marine fishes of five families
of two different orders (Anguilliformes,
Gadiformes and Perciformes) (Table 1). While
adults have been recovered of three sharks:
Alopias vulpinus (Bonnaterre, 1788)
(Alopiidae); Euprotomicrus bispinatus (Quoy
& Gaimard, 1824) (Dalatiidae) and Isurus
oxyrinchus Rafinesque, 1810 (Lamnidae)
from the Mediterranean and Pacific coast of
Japan (Dollfus, 1942; Gómez, 1983). This
indicates that S. tergestinus has low host
specificity both at the postlarvae and adult
stage (Costa et al., 2003).
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 First record of Unitubulotestis and Sphyriocephalus
Sphyriocephalus tergestinus postlarvae is a
new record to the South America. Also, S.
chilensis is a new host.
Sarda chiliensis from the coast of Chorrillos
were highly parasitized by U. pelamydis and S.
tergestinus. These two specimens are
described for the first time off the Pacific coast
of South America. Adults of U. pelamydis had
showed histopathological effect by fusion of
secondary lamellae of gills in the regions near
the cyst and severe damage in the tissue where
many cysts are present in S. sarda (Marino et
al., 2003; Justo et al., 2013).
In this report, S. tergestinus postlarvae showed
moderate values of prevalence in S. chiliensis,
similar to those obtained for Conger conger
Linnaeus 1758 by Costa et al. (2006). Santos et
al. (2009) suggested that S. tergestinus, can be
used as biological tags to discriminate stocks
of A. carbo. A congeneric species the
Table 1. Fish species reported as hosts of Sphyriocephalus tergestinus postlarvae in the world. All parasites were
found in the stomach of the fish. n= number of specimens examined.
Host Family n Prevalence
(%) Country Reference
Anguilliformes
Conger conger Linnaeus 1758 Congridae 64 26,6 Portugal Costa et al. (2009)
Gadiformes
Macruronus novaezelandiae (Hector, 1871) Merlucciidae - - Australia Beveridge & Campbell (1996)
Perciformes
Aphanopus carbo Lowe, 1838 Trichiuridae 90 5,6 Portugal Costa et al. (1996)
Aphanopus carbo Lowe, 1839 Trichiuridae 135 5,9 Portugal Costa et al. (2003)
Aphanopus carbo Lowe, 1840 Trichiuridae 578 5,9 Portugal Santos et al. (2009)
Brama dussumieri Cuvier, 1831 Bramidae 19 10,5 Indonesia Jakob & Palm (2006)
Lepidopus caudatus (Euphrasen, 1788) Trichiuridae 36 5,6 * Klimpel et al. (2006)
Sarda chiliensis Cuvier, 1832 Scombridae 100 32 Peru Present study
Thunnus alalunga (Bonnaterre, 1788) Scombridae - - USA Love & Moser (1983)
* Referred to as the Great Meteor Seamount (North Atlantic).
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Figure 1. Photomicrograph of Unitubulotestis pelamydis in Sarda chiliensis from Peru. A: Anterior end. B: Posterior end. C:
Testicle.
319
Figure 2. Photomicrograph of Sphyriocephalus tergestinus in Sarda chiliensis from Peru.
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 First record of Unitubulotestis and Sphyriocephalus
plerocercoid cestode Sphyriocephalus viridis
(Wagener, 1854) was selected as suitable for
use as biological tags of the swordfish Xiphias
gladius Linnaeus, 1758 (Garcia et al., 2011).
All specimens of S. chiliensis surveyed for
parasites in this research are less than 48 cm
length and are juveniles because they reach
sexual maturity over 47 cm length (Collete &
Nauen, 1983).
This is the first record of U. pelamydis and S.
tergestinus postlarvae in Peru. Also, Eastern
Pacific bonito S. chiliensis is a new host for
both endoparasites.
320
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Chero et al.
Figure 3. Photomicrograph of Sphyriocephalus tergestinus in Sarda chiliensis from Peru. A: Tentacles. B: Anterior end of the
tentacle. C: Metabasal armature. D: Basal armature.
321
Figure 4. Hook from metabasal armature of Sphyriocephalus tergestinus.
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 First record of Unitubulotestis and Sphyriocephalus
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Received November 18, 2015.
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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 First record of Unitubulotestis and Sphyriocephalus