First report on Asian fish tapeworm (Bothriocephalus acheilognathi) infection of indigenous mahseer (Tor tambra) from Nagan Raya district, Aceh province, Indonesia

Abstract

First report on Asian fish tapeworm (Bothriocephalus acheilognathi) infection of indigenous mahseer (Tor tambra) from Nagan Raya district, Aceh province, Indonesia. Bulg. J. Vet. Med. (online first). The aim of the present study was to examine the prevalence and intensity of the Asian fish tapeworm, Bothriocephalus acheilognathi on the indigenous mahseer fish Tor tambra. The fish samples were collected from Isiep River, Nagan Raya District as representative of wild population and from aquaculture ponds as representative of captive population. A total of 30 fish samples from Krueng Isep river and 30 fish samples from aquaculture fish ponds were examined in this study. The fish samples were abdominally dissected and the alimentary tracts were taken and perforated. The alimentary contents were placed onto Petri dish and observed for tapeworms. The samples of worm were photographed using stereo microscope. The results showed that the fish samples from aquaculture fishponds were infected by Bothriocephalus acheilognathi with the prevalence and intensity of 53.33% and 8.06, respectively, while no fish from the river was infected by cestoda.

Full text

Bulgarian Journal of Veterinary Medicine, 2015
ONLINE FIRST
ISSN 1311-1477; online at http://tru.uni-sz.bg/bjvm/bjvm.htm
Original article
FIRST REPORT ON ASIAN FISH TAPEWORM (BOTHRIOCEPHALUS
ACHEILOGNATHI) INFECTION OF INDIGENOUS MAHSEER
(TOR TAMBRA) FROM NAGAN RAYA DISTRICT,
ACEH PROVINCE, INDONESIA
Z. A. MUCHLISIN
1
, Z. FUADI
1
, A. M. MUNAZIR
1
, N. FADLI
1
,
W. WINARUDDIN
2
, C. NANDA DEFIRA
3
& A. HENDRI
4
1
Department of Aquaculture, Faculty of Marine and Fisheries, Syiah Kuala Univer-
sity, Indonesia;
2
Faculty of Veterinary Medicine, Syiah Kuala University, Indonesia;
3
Department of Biology, Faculty of Sciences, Syiah Kuala University, Indonesia;
4
Faculty of Marine and Fisheries, Teuku Umar University, Meulaboh, Indonesia
Summary
Muchlisin, Z. A., Z. Fuadi, A. M. Munazir, N. Fadli,
W. Winaruddin, C. Nanda Defira &
A. Hendri, 2015. First report on Asian fish tapeworm (Bothriocephalus acheilognathi)
infection of indigenous mahseer (Tor tambra) from Nagan Raya district, Aceh province,
Indonesia. Bulg. J. Vet. Med. (online first).
The aim of the present study was to examine the prevalence and intensity of the Asian fish tapeworm,
Bothriocephalus acheilognathi on the indigenous mahseer fish Tor tambra. The fish samples were
collected from Isiep River, Nagan Raya District as representative of wild population and from aqua-
culture ponds as representative of captive population. A total of 30 fish samples from Krueng Isep
river and 30 fish samples from aquaculture fish ponds were examined in this study. The fish samples
were abdominally dissected and the alimentary tracts were taken and perforated. The alimentary con-
tents were placed onto Petri dish and observed for tapeworms. The samples of worm were
photographed using stereo microscope. The results showed that the fish samples from aquaculture
fishponds were infected by Bothriocephalus acheilognathi with the prevalence and intensity of
53.33% and 8.06, respectively, while no fish from the river was infected by cestoda.
Key words: Bothriocephalus acheilognathi, cestodes, intensity, keureling, prevalence
INTRODUCTION
Keureling fish or internationally named
mahseer (Tor tambra) is one of the popu-
lar freshwater fish in Indonesia. The fish
has a good taste and higher price in local
and regional markets (Muchlisin et al.
2015). At present, the spawning of this
species has been successfully induced and
it is experimentally cultured in the pond.
However, the keureling fish in captive
conditions is very susceptible to parasites
infestation. Muchlisin et al. (2014) repor-
ted that about 50% of keureling popula-

First report on Asian fish tapeworm (Bothriocephalus acheilognathi) infection of indigenous mahseer …
BJVM, ××, No ×
2
tions in aquaculture ponds were infected
by Lernea sp., Argulus sp. and Trichodina
sp. In addition, the preliminary field ob-
servation revealed that the cultured
mahseer was also infected by cestodes of
the Asian fish tapeworm, Bothriocephalus
acheilognathi. Hence, this is the first re-
port on the Asian fish tapeworm infection
from western part of Indonesia.
The Bothriocephalus acheilognathi
was first described in Japan from intestine
of Acheilognathus rhombea (Yamaguti,
1934) and currently is the common endo-
parasite for freshwater fish worldwide,
particularly cyprinids (Marcogliese, 2008;
Choudhury & Cole, 2011). This worm has
been reported to infest fish in the USA
(Heckmann et al., 1993; Scholz, 1997;
Kuperman et al., 2001), Europe (Marcog-
liese, 2008) and other parts of the world,
koan fish in Iran (Hosseinifard et al.,
2011), some native freshwater fish species
in Mexico (Salgado-Maldonado & Pine-
da-Lopez, 2003). According to Choud-
hury et al. (2013) the grass carp, Cteno-
pharyngodon idella could be considered a
principal host for B. acheilognathi in Pa-
nama and worldwide. Nowadays this
parasite has been categorised as global
freshwater invasive species due to the
success of invasiveness; however, no re-
port from Indonesia was available. Ac-
cording to Ozturk & Ozer (2014) the wide
spread of Asian tapeworm has occurred in
two ways; import-export of exotic cypri-
nids for culture and introduction of grass
carp for controlling macrophytes in differ-
ent region throughout the world (Boomker
et al., 1980).
In general, besides infecting fish, the
cestodes are also likely to infect humans
consuming the infected and improperly
cooked fish (Justine et al., 2012; Yera et
al., 2013). Some species of cestodes infect
men for long period without any symp-
toms (Waeschenbach et al., 2012). The
objective of the present study was to
evaluate the prevalence and intensity of B.
acheilognathi infection on local mahseer
fish from wild and captive population in
Nagan Raya District, Indonesia. This is
the first report for infection of Bothrio-
cephalus acheilognathi in freshwater fish
from Aceh region, Indonesia.
MATERIALS AND METHODS
Study site and time
The study was conducted in Beutong Sub-
district, Nagan Raya, Aceh Province, In-
donesia from December 2013 to February
2014. The wild population sample was col-
lected from Isiep River (04
0
16’51.61”N,
96
0
26’58.53”E), while captive fish were
collected from aquaculture ponds
(4
0
14’50.53’’N, 96
0
26’13.48’’E) in Me-
unasah Krueng village of Nagan Raya.
The laboratory analyses were carry out in
Syiah Kuala University and Brackishwater
Aquaculture Station, Ujung Batee in Ban-
da Aceh and Aceh Besar, respectively.
Sampling
Samplings were conducted during the rainy
season, December 2013. A total of 60 fish
were collected randomly from wild (30
individuals) and captive (30 individuals)
populations using casting nets with two
mesh sizes (1.0 and 2.0 inches). Collected
fish were preserved in ice box (4
o
C) until
transported to laboratory for further analy-
sis. The main water quality parameters such
as dissolved oxygen, pH, temperature and
turbidity were measured ex situ.
Sample preparation and analysis
The fish samples were anaesthetised in a
solution of tricaine methanesulfonate (MS
222), prepared by dissolving 4 g of MS

Z. A. Muchlisin, Z. Fuadi, A. M. Munazir, N. Fadli,
W. Winaruddin, C. Nanda Defira & A. Hendri
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222 in 5 L tap water (Muchlisin et al.,
2004) measured for total length (cm) and
body weight (g), and then submitted to
abdominal dissection using sterile scis-
sors. The alimentary tract were removed,
placed into a jar then perforated with a
needle and the alimentary contents were
placed onto Petri dish and observed for
Asian tapeworm cestodes naked-eye or
using a magnifying glass. The samples of
worm were taken from the Petri dish,
placed onto object glass and two drops of
safranin were added to the sample for
observation under stereo microscope (40–
100× magnification) and photographed.
Identification of cestodes was based on
Khalil et al. (1994).
The prevalence and intensity of
infection were calculated based on Kabata
(1985) as followed: Prevalence=(total of
infected fish/total of examined fish) ×
100%; Intensity=total of parasites/total of
infected fish.
RESULTS
The fish samples from captive system
(ponds) were infected by Bothriocephalus
acheilognathi, while no fish from the wild
population was infected by this worm. A
total of 16 fish samples from the captive
system were infested by B. acheilognathi
resulting in 53.33% prevalence and 8.06
of intensity. A total of 129 tapeworms
were recorded during the study (Table
1).
Fig. 1. Morphology of Asian fish tapeworm
(Bothriocephalus acheilognathi) showing
scolex and proglottids (arrows).
As recorded in this study and accord-
ing to Scholz (1997), B. acheilognathi
had specific characteristics: pyramid-sha-
pe scolex with a pair of bothria, seg-
mented body (proglottids), no neck and no
dorsal or ventral median furrow (Fig. 1).
DISCUSSION
This study revealed that the prevalence of
Asian tapeworm in Tor tambra was rela-
tively higher compared to that in fish from
Bafra Fish Lake, the lower Kizilirmak
Delta, Turkey (Ozturk & Ozer, 2014) and
Labeobarbus aeneus (Bertasso & Avenant-
Table 1. Prevalence and intensity of Asian fish tapeworm Bothriocephalus acheilognathi in the ali-
mentary tract of keureling fish (T. tambra) collected from wild and captive systems
Populations
Parameters
Captive (n=30) Wild (n=30)
Total number of infected fish 16 –
Total number of tapeworms 129 –
Intensity 8.06 –
Prevalence (%) 53.33 –

First report on Asian fish tapeworm (Bothriocephalus acheilognathi) infection of indigenous mahseer …
BJVM, ××, No ×
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Oldewage, 2005). However, the highest
prevalence of Asian tapeworm was re-
ported in Labeobarbus kimberleyensis
(Bertasso & Avenant-Oldewage, 2005),
Cyprinella lutrensis (Heckmann et al.,
1995) and Profundulus hildebrandi from
the endorheic basin of San Cristobal de
las Casas, Mexico (Velazquez-Velazquez
et al., 2011).
We suggest that this was due to the
poor sanitary condition of the pond. Our
field observation indicates that the sludge
from the deposition process of residual
water and unconsumed feed and fish fae-
ces at the pond bottom had reached a
thickness of 20–25 cm. Based on Khalil et
al. (1994), bottom sludge is the appropri-
ate medium for growing of cestode larvae
in the pond. Therefore, the prevalence of
the endoparasite B. acheilognathi in local
mahseer fish (T. tambra) was higher com-
pared to that of ectoparasites as reported
previously by Muchlisin et al. (2014). In
addition, the prevalence of B. acheilog-
nathi has probably a seasonal pattern with
higher prevalence during the summer and
lower in winter as recorded for Schizotho-
rax niger (Zargar et al., 2012). Our study
was conducted during the rainy season
(winter), so, a higher prevalence would be
expected during the dry season in Indone-
sia. Therefore, further study is needed to
evaluate the real prevalence and intensity
of this Asian tapeworm during the diffe-
rent seasons in the region.
The Asian tapeworm was probably in-
troduced accidentally into the Nagan Raya
region with infected common carp (Cy-
prinus carpio) from Java Island, Indone-
sia in 2006 by Local Fisheries Affair
(DKP). The common carp was also sus-
pected as origin of B. acheilognathi infec-
tion in the endangered fish Profundulus
hildebrandi in Mexico (Velazquez-Velaz-
quez et al., 2011).
The study revealed that only fish sam-
pled from aquaculture pond (captive sys-
tem) were infected by tapeworm and no
fish from wild river population had the
tapeworm. According to Williams & Wil-
liams (1996), the Asian tapeworm re-
quires a copepod intermediate host and we
speculate that aquaculture ponds provide
ideal conditions for copepods and tape-
worm transmission as mentioned earlier.
According to Choudhury et al. (2013)
streams are relatively less suitable for co-
pepods growing and therefore B. achei-
lognathi was not found in the fish sample
from stream as recorded in this study.
The Asian tapeworm had infected cy-
prinids in many countries of almost all
continents and this is the first report from
Aceh region, Indonesia. B. acheilognathi
infection impairs fish health, body condi-
tion and growth (Marcogliese, 2008) and
causes great economic losses in hatcheries
and fish farms worldwide (Kuperman et
al., 2001; Zargar et al., 2012). Therefore,
the Asian tapeworm is a potential threat
for aquaculture industry and a special at-
tention to eradicate the invasiveness is
needed.
CONCLUSION
The mahseer fish (T. tambra) sampled
from aquaculture pond in Nagan Raya
district, Indonesia was infected by the
Asian fish tapeworm Bothriocephalus
acheilognathi at a prevalence of 53.33%
and intensity of 8.06, while no fish sample
from the Isiep River wild population was
infected by this worm.
ACKNOWLEDGMENTS
The study was supported by Directorate Gene-
ral of Higher Education (DGHE), Department
of National Education (Diknas), Republic of

Z. A. Muchlisin, Z. Fuadi, A. M. Munazir, N. Fadli,
W. Winaruddin, C. Nanda Defira & A. Hendri
BJVM, ××, No ×
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Indonesia through research grant of Master
Plan Percepatan Pembangunan Ekonomi In-
donesia (MP3EI), therefore the authors thank
DGHE Diknas for supporting this study.
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Correspondence:
Prof. Dr. Muchlisin Z. A., S.Pi, M.Sc
Department of Aquaculture,
Faculty of Marine and Fisheries,
Syiah Kuala University,
Banda Aceh 23111, Indonesia,
e-mail: muchlisinza@unsyiah.ac.id