Comparative Clinical Pathology

https://doi.org/10.1007/s00580-018-2739-9

ORIGINAL ARTICLE

The first report of Nematode (Contracaecum) and two Acanthocephala

(Serrasentis sagittifer, Tenuiosentis niloticus) in Persian Gulf’s Japanese
threadfin bream (Nemipterus japonicus)
Ahmad Nematollahi 1 & Parisa Shahbazi 1 & Mohammad F. Abbasi 2 & Saeid Ghaemmaghami 3 & Iraj Mobedi 4

Received: 31 October 2017 / Accepted: 26 April 2018

# Springer-Verlag London Ltd., part of Springer Nature 2018

Abstract
In this study, 649 Japanese threadfin bream (Nemipterus japonicus) were captured from the Persian Gulf and necropsied. The
helminths of each organ were cleared by clearing solutions and stained by proper staining methods. Identification of the parasites
was conducted according to identification keys. Totally, 109 (17%) of fishes were infected with parasites, and infection in
intestine was higher than in other organs. In the present study, one Nematode (Contracaecum), two Acanthocephala
(Serrasentis sagittifer, Tenuiosentis niloticus), and three larvae were isolated. Although Serrasentis sagittifes was reported in
previous studies in Iran, Tenuiosentis niloticus and Contracaecum are reported for first time in Iranian fishes.

Keywords Contracaecum . Serrasentis sagittifer . Tenuiosentis niloticus . Nemipterus japonicas . Persian Gulf

Introduction Africa, all parts of the Persian Gulf, and North Coast of the
Oman Sea (Russell 1990). This fish is one of the major species
Japanese thread fin bream, Nemipterus japonicas, is a demer- in the south of the Red Sea and the Suez Canal (Ben-Tuvia and
sal species with the distribution ranging from Indian Ocean to Grofit 1973). The first hunt of this species from the
Pacific Ocean. It can be seen in the Red Sea, East coast of Mediterranean Sea in 2005 apparently resulted in migration
from the Red Sea through the Suez Canal. The fish has been
seen in the Mediterranean Sea (Golani and Sonin 2006). It is a
* Ahmad Nematollahi
demersal aquatic species living as a herd on coastal areas with
anemat@tabrizu.ac.ir
the sandy and muddy seabed at a depth of 5 to 80 m. The
Parisa Shahbazi thread bream are considered as fish food in many parts of
p_shahbazi@tabrizu.ac.ir the world and are taken commercially by hook and line and
Mohammad F. Abbasi bottom trawl (Puentes-Granada et al., 2004). The biology of
abbassi@yahoo.com Nemipterus japonicus has been studied by many authors in
different regions, including Saudia Arabia (Bakhsh 1996),
Saeid Ghaemmaghami
Ghaemmaghami@gmail.com India (Rajkumar et al. 2003; Manojkumar 2004; Kerdgari
et al. 2009), and Egypt (Amine 2012; El-Haweet 2013).
Iraj Mobedi
mobedi@tu.ac.ir
Wide body, pulvinate dorsal, lack of spine in the posterior
part of the head, and lack of scales are the characters of
1
Department of Pathobiology, Faculty of Veterinary Medicine, Nemipterus japonicas. The dorsal fins have ten spines and
University of Tabriz, Tabriz, Iran nine soft connected rays without cut or incision between hard
2
Department of Clinical Science, Faculty of Veterinary Medicine, and soft rays. Ventral fins have one spine and five soft rays.
Shahid Bahonar University of Kerman, Kerman, Iran Anal fins have three spines and seven soft rays. The caudal fin
3
Department of Food Hygiene and Aquatics, Faculty of Veterinary is forked, and the upper part of upper edge becomes elongated
Medicine, Islamic Azad University of Shabestar Branch, and makes a yellow string. There is a red spot at the origin of
Shabestar, Iran the lateral line and 1–3 yellow longitudinal stripes are above it.
4
Department of Parasitology, Faculty of Medicine, University of Furthermore, 7–9 longitudinal stripes are below lateral line,
Tehran, Tehran, Iran

Fig. 1 The map of sampling area
and a yellow stripe is along the belly. Lateral scales are usually
yellow. Pectoral fins are long. Ventral fins are also long, and
their insertion reaches the base of the anal fin (Russell 1990;
Bakhsh 1996; Amine 2012).
Few studies are known about parasites fauna of Nemipterus
japonicas, and only one report is concerned with parasites of
Serrasentis sagittifer in Iran (Ghaemmaghami et al. 2008).
The aim of this study was to investigate Nematode and
Acanthocephalan species in Nemipterus japonicus of the
Persian Gulf.
Material and methods
The study area was the Bushehr Coast located on the Northern
Coast of the Persian Gulf (Fig. 1). From October 2015 to
September 2016, totally 649 fishes (including 182 male, 396
female, and 71 immature) were monthly captured and
transported to the laboratory along with ice.
In the laboratory, weight, body length, and sex of fishes
were recorded. Fishes were examined only for internal
Table 1 Distribution of isolated helminthes in the organs of fishes
Infected organs Outer surface of Inner surface of
alimentary system alimentary system
No. (%) 62(43.35) 40 (27.97)
Comp Clin Pathol
parasites. Each fish was opened, and the abdominal cavity
was cut, and the intestine was separated from the other visceral
organs and placed in PBS. The intestines were fully examined,
and the helminthes were studied with stereomicroscope.
The obtained worms were washed in 0.6% saline solution
and relaxed in water for 2 h at 4 °C and fixed in ethyl alcohol
70%. Then, the worms were examined by means of light mi-
croscope after being clarified in clearing solution.
Identification of the worm’s species was undertaken by using
the available literature, based on their morphological features
(Moravec 1994; Anderson 2000). Moreover, measurements of
characteristics of fishes were performed by using a camera
lucida.
Results
In this study, 649 fishes (including 182 male, 396 female, and
71 immature) were collected. Totally, 109 (17%) of fishes
were found infected with helminthes. Parasites were found
in 32 of 182 (17.58%) male fishes and 51 of 396 (12.87%)
female fishes and in 26 of 71(36.6%) immature fishes. This
difference was statistically significant (P < 0.05).
Infection in intestine was higher than in other organs.
Totally, 143 helminthes were isolated from different organs
of the fishes. Table 1 shows distribution of isolated helminthes
in organs of fishes.
Infection to parasites is recorded in all seasons, but the
highest prevalence of parasites was in the autumn and winter
(Fig. 2). Statistical analysis results showed that this difference
is not significant.
In the present study, one Nematode (Contracaecum) and
two Acanthocephala (Serrasentis sagittifer, Tenuiosentis
niloticus) were isolated.
Survey of species
Tenuisentis niloticus
Family Tenuisentidae (Van Cleave, 1936)
Genus Tenuisentis (Van Cleave, 1936)
Tenuisentis niloticus (Meyer, 1932; Van Cleave, 1936)
Trunk is cylindrical and is elongated with an unremarkable
anterior trunk cone. There is an ovoid swelling in posterior of
trunk. Proboscis is long and cylindrical. The proboscis consists
Male genital Ovary Liver Abdominal cavity Swim bag Total
gonads
3 (2.09) 6 (4.19) 3 (2.09) 27 (18.88) 2 (1.39) 143 (100)
Comp Clin Pathol

26.61% 26.61%
24.77%
22.1%
Rate of infecon

Spring Summer Autmn Winter

Seasons
Fig. 4 Tenuisentis niloticus
Fig. 2 Distribution of isolated parasites in seasons

of just 1 row of hook with 8 obvious projections and 16 rows pore opens below interlaid. The muscular esophagus is cylin-
on posterior part, with 30–33hooks in each (Figs. 3 and 4). drical with short globular ventricles connected to a posterior
Serrasentis sagittifer ventricular appendix. Females and males are 32 and 24 mm in
Family Rhadinorhynchidae (Southwell & Macfie, 1925) length, respectively (Azhar et al. 2011) (Figs. 7 and 8).
Subfamily Serrasentinae (Petrochenko, 1956)
Genus Serrasentis (Van Cleave, 1923)
Serrasentis sagittifer (Linton, 1889) Discussion
Distinctive rows of spines (combs) are on the ventral sur-
face of their body in adult and encysted stages. The proboscis In the present study, prevalence of infection to helminths was
is short, bulbous, and expended on the anterior end and cov- 17%, and the highest prevalence was observed in the autumn
ered with numerous uniform spines (16–24 longitudinal rows and winter. Furthermore, one Nematode (Contracaecum) and
of 14–18 hooks each). Females are 6.0–130 mm, males are two Acanthocephala (Serrasentis sagittifer, Tenuiosentis
8.6–75.0 mm, juvenile females are 4.0–6.4 mm, and juvenile niloticus) were isolated.
males are 2.6–4.2 mm in length (Figs. 5 and 6). In contrast to the previous studies representing many spe-
Contracaecum (sp.) cies of Nematodes from different localities of the Persian Gulf
Family Anisakidae (Skerjabin, 1945)
Subfamily Anisakinae(Chabaud, 1965)
Genus Contracaecum (Railliet & Henry, 1912)
The body of adult Contracaecum is yellowish, coiled, taper-
ing at each end of the body, and covered with thick, transparent,
and striated cuticle showing transverse folds. Mouth is provid-
ed with three round lips and two marked flanges at corners of
each labium. The three hook-shaped interlabia are well devel-
oped, wide at base, and slightly shorter than the lip. Excretory

Fig. 3 The proboscis of Tenuisentis niloticus Fig. 5 Schematic view of Serrasentis sagittifer sagittifer

Fig. 6 Head of Serrasentis
(AL-Kawari et al. 1996; Kardousha 2016), in this study, only
one Nematode parasite (Contraececum) was detected. Adel
et al. (2013) isolated three Contracaecum larvae from 16%
of 100 Scomberomorus specimens collected from five differ-
ent regions of the Persian Gulf.
Barson and Marshall (2004) examined 202 Claris
gariepinus collected from Chivero lake, Zimbabwe, from
November 2000 to May 2002. In this study, 42.6% infection
with Contracaecum larva was reported.
Aydogdu et al. (2011) collected 65 fishes including
Capoeta antalyensis, Aphanius mento, and Pseudophoxinos
battalgil in Antalya, Turkey. They found three Nematodes,
including Contracaecum larvae, Rhabdochona denudate,
Fig. 7 Schematic view of the head and esophagus of Contracaecum
Comp Clin Pathol
Fig. 8 Head and esophagus of Contracaecum
and Eustrongylides excisus. Contracaecums was isolated from
abdominal cavity of Pseudophoxinos battalgil and Amphanius
mento. In this study, 10 fishes from 21 examined fishes were
infected to parasites, and infection rate was 47.6%.
Contracaecum was not reported in previous studies in
Iranian fishes, and this is the first report from Contracaecum
in Iranian fishes.
In the present study, two species of Acanthocephala para-
sites have been recorded from the Japanese threadfin bream
(Nemipterus japonicus). One of them was reported in Iranian
fishes (Nemipterus japonicus). Ghaemmaghami et al. (2008)
conducted one study on 50 Nemipterus japonicus of the
Persian Gulf and reported Serrasentis sagittifes found in the
abdominal cavity and different organs of inspected fishes.
There are many reports about Serrasentis sagittifes.
Chandra (2006) found 290 different parasite species from
Bangladesh fishes and Serrasentis sagittifes species that was
called Bhetki in local language was one of them.
Tenuisentis niloticus was not reported in previous studies in
Iranian fishes. Although this parasite is recorded in some stud-
ies in the world, Akinsanya et al. (2007) reported Tenuisentis
niloticus in 20 specimens of Gymnarchus niloticus and in 18
specimens of Heterotis niloticus collected from Lekki lagoon
in Nigeria, and the parasites were isolated from the surface of
the intestine of fishes.
Although distribution of Japanese threadfin bream
(Nemipterus japonicus) is reported from different regions of
the Indian Ocean, and the biology of the mentioned fish is
studied by many authors, studies about infection to the para-
sites are rare in different regions of the world. Infection to
Trematode and Nematodes was recorded in family
Nemipteridae only in two studies about parasites infections
of fish in the Persian Gulf.
Compliance with ethical standard
The study was performed under the approval of the state committee on
animal ethics, Tabriz University, Tabriz, Iran (No: 4687/63- Date:
Aug 2015).
Comp Clin Pathol
Conflict of interest All authors have received research grants from
University of Tabriz, Iran, and declare that they have not conflict of
interest.
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