STUDIES ON PARASITIC DISEASES AMONG WILD AND

SCVMJ, XII (2) 2007
171
STUDIES ON PARASITIC DISEASES AMONG WILD AND
CULTURED EEL FISH (Anguilla anguilla)
Ahmed M. M. El-Ashram
Fish Diseases Dept., Central Lab. For Aquaculture Research (El-Abbassa),
Agriculture Research Center, Egypt.
ABSTRACT
Three years study was performed for the detection of parasitic diseases in the
cultured and wild eel (Anguilla anguilla). A total number of 800 eel specimens
(400 wild fish from lakes and 400 cultured ones from commercial fish farms in
El-Sarkia, Kafr El-sheikh and El-Beharah provinces was collected and subjected
to clinical signs, postmortem and parasitological examinations. Also trials for
the treatment of some parasitic diseases were evaluated. The total prevalence of
parasitic infection was 78.1% among the examined fish. The rate in wild and
cultured eels was 72.5 and 83.8%, respectively. The total rate of Trichodina
species, Ichthyophthirius multifiliis, Myxidium giardi, Myxobolus dermatobius,
monogeneans, Eimeria, Anguillicola crassus, Anisakiid larvae, cestodes and
Ergasilus species infections was 31.25, 2.5, 12.8, 22.5, 48.8, 0.5, 78.1, 0.4, 8.9
and 19 % respectively. The detected monogenetic trematodes and its total
prevalence were Pseudodactylogyrus species (31.3%), Dactylogyrus species
(10%), Gyrodactylus species (4.4%) and Quadriacanthus species (3.1%). The
total rate of Proteocephalus species, Cyathocephalus species and unidentified
cestode infection was 6.9, 1.9 and 0.1 % respectively. The clinical signs and
postmortem changes associated with each infection were recorded. Our results
showed that formalin and praziquental at concentration of 0.25 ppm and 10mg/L
for 1 hr was effective for controlling trichodinosis and pseudodactylogyrosis,
respectively. With the aid of the radiographic method, the A. crassus infection
and changes in the gasbladder of infected eel specimens can be monitored
successfully. Electrophoretic analysis of adult Anguillicola crassus proteins in
SDS-PAGE revealed a series of bands were illustrated. Levamisole at
concentrations of 1 or 2mg/L for 24 or 48 hr showed promising result in the
treatment of anguillicolosis.
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INTRODUCTION
Aquaculture is the fastest growing
segment of both the world and Egypt
agriculture industry. The development
of sustainable, economically and environmentally aquaculture production
will be vital and benefit for many sectors throughout the country and for
global food security. Movement of aquatic animals with a high market value
is necessary for development of aquaculture on both subsistence and commercial level. However, the introduction of new species increases the
probability of introducing new pathogens, which can have dir consequences on aquaculture (Woo, 1995).
In recent years, eel (Anguilla anguilla) is a fish of growing commercial
value allover the world because of its
nutritional and medicinal values. Eel
culture expanded considerably in Egypt.
Diseases are a crucial factor which
inhibits the expansion of aquaculture.
A wide variety of parasitic agents have
been recorded as significant problems
in eel's aquaculture (Gosper, 1996;
Barker and Cone, 2000; Agullar et
al., 2005 and McKinnon, 2006).
Parasites causing little apparent damage in feral fish populations may
become causative agents of diseases of
great importance in farmed fish leading to pathological changes, decrease
of fitness or reduction of market value
of fish (Woo, 1995; Paperna, 1996
and Scholz, 1999).
Ahmed El-Ashram
The potential ecological impacts of
introducing eel on other fish species
may be significant as they may introduce pathogens and parasites to which
other fish species were previously unexposed.
In Egypt, major gaps still exist in
the knowledge of eel parasitic diseases. So, there is a great requirement
for research for additional knowledge
of exotic diseases that may be of
future significance for the industry. A
need exists to further evaluate the
aquaculture potential of eels and to
develop appropriate culture technologies. The aim of the present study
was to through light on parasitic
diseases of eels (Anguilla anguilla)
under egyptian conditions. Furthermore, trials for treatment of certain
parasitic diseases was evaluated.
MATERIAL & METHODS
Fish specimens
A total number of 800 fish specimens of eels (A. anguilla) weighing 10
to 275 gm (400 wild fish from Egyptian lakes and the other 400 cultured
from commercial fish farms in ElSarkia, Kafr El-sheikh and El-Beharah
provinces) were sampled from over 3
consecutive years, on several occasions in the period between January
2004 to December 2006.
In the laboratory, the fish specimens were maintained alive in tanks
supplied with dechlorinated and aerated
SCVMJ, XII (2) 2007
tap water. The clinical and postmortem examinations were performed as
described by Lucky (1977).
Parasitological examinations were
performed according to Lucky (1977);
Ash and Oriel (1987) and Buchmann
(1988). Parasites were processed by
standard methods for light or scanning
electron microscopy (Alvarez et al.,
1995). Identification of the collected
parasites was performed based on
Lom and Dykova (1992); Moravec
(1994); Hoffmann (1999) and Buchmann and Bresciani (2001).
The Radiodiagnostic technique of
infected eels with Anguillicola crassus
was performed as described by Beregi
et al., (2001) and Szekely et al., (2005).
Eels with uninfected gas-bladder were
used as control. After radiography,
eels were killed and examined by
conventional parasitological methods.
Three samples of adult A. crassus
were collected a live from naturally
infected eels and washed in phosphate
buffered saline, pH 7.2. Electrophoresis for protein prepared from Anguillicola crassus was performed according to Laemmli (1970).
Trials for treatment of anguilliculosis
Fifty naturally infected eels (weight
25-45gm) were randomly divided into
five equal groups and distributed in
well aerated glass aquaria supplied
with dechlorinated tap-water and polypropylene tube serving as hiding
place. After acclimatizatio the fish to
173
laboratory conditions for 2 weeks, LLevamisole HC1 was used as bath
treatment to evaluate the curative dose
against Anguillicola crassus. The first
group was designated as control. The
second and third ones were treated
with levamisole at concentration of
1mg/l for 24 and 48hr., respectively.
The fourth and fifth groups were
subjected to Levamisole at concentration of 2mg/l for 24 and 48hr.,
respectively. During treatment the eels
were not fed. The eels were killed and
the gasbladder was dissected and
examined for A. crassus immediately
after treatment by 24 hr as described
by Taraschewski et al. (1988), Hartmann (1989) and Geets et al., (1992).
Mortality and behavior of eels during
and after treatment were recorded.
Trials for treatment of Trichodinosis
Twenty eel specimens suffering from
Trichodina species infection were divided into two groups with 10 individuals each and kept in glass aquaria as
mentioned before for treatment from
Trichodina species infection. The first
group was left as a control. The
second one was treated with formalin
at concentration of 0.25 ppm as
described by Woo (1995).
Trials for treatment of Pseudodactylogyrosis
Before the trial commenced, the
presence of Pseudodactylogyrus species on gills was confirmed in 10 randomly sampled fish, obtained from a
174
stock showing 100% prevalence of
Pseudodactylogyrus infection. Forty
infested eel were equally divided into
two groups. The first kept as nontreated control. The second one was
exposed to Praziquental at concentration of 10mg/L for 1 hr according to
Paperna (1996). All fish specimens
were examined for the presence of
Pseudodactylogyrus on gills, clinical
abnormalities and mortalities were
recorded.
RESULTS
The total prevalence of parasitic
infection was 78.1% among the examined fish. The prevalence of parasitic
infection in wild and cultured eels was
72.5 and 83.8%, respectively (Table, 1).
Trichodiniasis:
Mass mortalities associated with
Trichodinosis were recorded during
acclimation in freshwater ponds. The
total prevalence of trichodinosis was
31.25%. The prevalence of Trichodina
species infection was 12.5 and 50% in
both wild and cultured eels respectively (Table, 2). Fish exhibited lethargy, respiratory distress, frayed fins and
epidermal erosion. Trichodina species
was detected in gills and skin. Heavily
infested eels had grayish coat due to
increased secretion of mucus (Fig. 1).
Microscopically, masses of Trichodina species were observed in gills and
skin scraping (Fig. 1). From a safety
point of view, no mortality was
Ahmed El-Ashram
recorded in the treated group with
formalin. While the mortality rate was
30% in the non-treated one (Table, 3).
Trichodina was found dead and disappeared from the treated eel. All clinical abnormalities were disappeared from
the treated fish and returned to normal
behavior.
White spot disease
No white spot infection was recorded among wild eel. The prevalence
among cultured eel was 5% (Table, 2).
Clinically, the infected eel showed loss
of appetite, respiratory distress and
increased mucus secretion. Adult Ichthyophthirius multifiliis (Fig. 1) was
detected on the gills and skin of
infected eel in freshwater farms, characterized by a horseshoe-shaped macronucleus and a small round micronucleus.
Myxidium giardi infection (Myxidium
dermatitis)
The total prevalence of Myxidium
giardi infection was 12.8%. The prevalence rate in wild and cultured eel was
4.3 and 21.3% respectively (Table, 2).
Myxidium was detected infecting the
skin and gills. Clinically infected eels
showed small white spots scattered on
the skin (1-4mm in diameter) (Fig. 2).
They might undergo rupture and left
ulcer at site of infestation. Also, dark
discoloration, weak swimming and rubbing against hard objects were recorded. The macroscopic cyst rendered
fish unsightly and unmarketable. In
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case of heavy gills infestation, respiratory distress and growth impairment
were recorded. Microscopically black
cysts were observed in gills containing
spores. The black colour may be due
to accumulation of melanomacrophages. Spores were spindle in shape
with both ends pointed (Fig. 2). There
was a polar capsule. The length of the
spores was 8.0-13.8µm and the width
was 6.5-8.9 µm.
Myxobolus dermatobius infection
(Fig. 3):
The total prevalence of Myxobolus
infection was 22.5%. A higher rate
was recorded in cultured eel (37.5%)
than the wild one (7.5%) (Table, 2).
Myxobolus infection was noticed in
the skin (Fig. 3). Whitish nodules (13mm) located in the subcutaneous
tissues of eel fins. A milky material
was noticed when the infected tissue
was pressed between two slides.
Rupture of the cyst led to hemorrhage
and ulcer. Melanomacrophages were
found around the infected area (Fig.
3). Spores were almost circular in
front view (6.3-7µm). The polar
capsules measured 2.8-3.5µm. It not
contained filament coils. The iodinophilous vacuole was absent.
Eimeria species infection (Fig. 4):
The prevalence of Eimeria infection
was very rare (0.5%). It is only reported
in cultured fish (1%) (Table, 2). Neither
clinical signs nor mortalities were recorded in the infected fish. Unsporulated
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oocyst of Eimeria sp. was spherical,
12.5 µm in diameter. The wall of
oocyst was double layer and the
distance between the two layers was
0.5µm.
Gill Monogeneans
The total prevalence of gills monogeneans was 48.8%. A higher rate was
recorded in cultured eels (71.5%) than
in wild one (26%) (Table, 4). The
detected monogenetic trematodes with
its total prevalence were Pseudodactylogyrus species (31.3%), Dactylogyrus species (10%), Gyrodactylus
species (4.4%) and Quadriacanthus
species (3.1%) (Table, 5) (Fig. 5).
Clinically, heavily infected eels showed excessive mucus, loss of appetite,
respiratory distress and emaciation.
Gills were congested.
Microscopically, the monogeneans
were found attached to the gill
filaments. Pseudodactylogyrus species
measures 0.9-2.2 mm long and 0.1-0.3
mm wide. There were four pigmented
light receptors at the anterior end. The
ventral hamuli are prominent. While
the dorsal hamuli are small. Pseudodactylogyrus has 14 marginal hocks in
the haptor. Dactylogyrus species was
characterized by four anterior eye
spots and a sucker anteriorly. The
caudal end has haptor with one or two
large hooks surrounded by up to 16
smaller hocklets. The total length of
the worms was about 400µ. Gyrodactylus species was characterized by
176
absence of the eyes spots, viviparous
and one pair of anchor firmly attached
by two bars. Quadriacanthus species
showed an elongated body with four
head organs. Haptor has two pairs of
anchors of different shape and size.
Ventral anchors were smaller than
dorsal one but similar in shape and
with more developed point.
Praziquental at concentration of
10mg/l for 1 hr had deleterious effect
on Pseudodactylogyrus parasite. All of
the treated fish were returned to normal state within 7 days post treatment.
The mortality among the treated and
non-treated groups was 10 and 35%,
respectively (Table, 6).
Anguilliculosis
The total prevalence of anguilliculosis caused by Anguillicola crassus
infection in the examined samples was
78.1%. Its rate in wild and cultured
eels was 72.5 and 83.8 %, respectively
(Table, 7). The intensity was ranged
from 1-40.
The clinical signs and postmortem
changes associated with anguilliculosis were loss of appetite, emaciation,
reduced swimming ability and slight to
severe abdominal distension (Fig., 6).
Red swollen anus was recorded as pathognomonic criteria for eels infected
with A. crassus (Fig., 7). Generally,
the gills were congested with excessive mucus secretion on the body
surface. The infected gasbladder had
turbid wall as the result of thickening,
Ahmed El-Ashram
inflammation and fibrosis. The gasbladder with worms looks like sausage
appearance. Also, showed intensive
pigment accumulation and stomach
like to touch. Upon incision, many round worms flow in chocolate like masses and bloody exudates were seen
(Fig., 6). The pneumatic duct became
markedly inflamed, enlarged and red
in colour. Rupture of the gas bladder
was recorded in few cases especially
in heavy infected one. Therefore, the
infected eels lose the functionality of
their swimbladder, which means that
they cannot maintain their depth and
also are likely to die on exposure to
high pressure.
The adult worm of dracunculoid
nematode (A. crassus) live in the gas
bladder lumen and fed on their host's
blood. Its body is darkly coloured,
fusiform and tapering at both ends.
The buccal capsule is well sclerotized,
its anterior rim bearing one row of 2128 teeth. The oesophagus was cylindrical with anterior musculature, posterior glandular part and expanded at
its posterior half. The nerve ring situated at the border of the first and
second third of esophagus. While the
excretory pore lies near the junction of
esophagus and intestine. Intestine is
dark, straight and broad. There are
three large rectal glands. Tail is conical and short (Fig., 8).
Female: It measures 9.25-69.0 mm
long with maximum width 0.8-4.6
SCVMJ, XII (2) 2007
mm. The buccal capsule measures
0.01-0.03 mm long and 0.01-0.07 mm
width. The esophagus is 0.62-1.9 mm
long and the maximum width 0.160.35 mm. The excretory pore opens at
0.70-1.19 mm from the anterior
extremity. The vulva is prominent,
cone-shaped and situated posteriorly at
2.21-6.5 mm from the posterior extremity. Ovarian tubes extend from a
short distance below esophagus till the
region anterior to rectal glands. The
uterus occupies the most of the body
containing eggs and larvae. The rectal
glands measures 0.14- 0.4 X 0.08-0.24
mm. The anus opens on well developed papillae like projection. The tail
is conical and measures 0.19-0.4 mm
(Fig., 8).
Male: It measures 17.8-45.7 mm long
and 0.6-3.3 mm wide. Its anterior end
is similar to that of the female. The
excretory pore open at 0.6-0.8 mm
from the anterior extremity. Testes are
ovoid and located near the tail end.
The posterior end is bifurcate into two
parts. The cloaca opens on a prominent process which measures 0.040.09 mm. The rectal glands measures
0.2-0.4X0.06-0.11 mm. There are five
pairs of caudal papillae; two pre-anal
and three post-anal. The tail is conical
and measures 0.10-0.25 mm long.
Radiodiagnostic examination
The size of the fish and its gasbladder is proportionally related. The
gasbladder of healthy eels is clearly
177
outlined and a full air filled lumen on
the radiographs. The gasbladder gives
a homogenous radiographic shadow
under the spinal column (Fig. 9). On
the other hand, the infected eels showed deformity and non-homogenous
area in the shadow of the gasbladder
according to the intensity of infection
because it is not completely filled with
worms. While no radiographic shadow
and no area containing air was detected when the lumen of the gasbladder
was entirely filled with worms (Fig. 9).
Radiographic examination was confirmed by the dissection of the examined
fish. The gasbladder of non-infected
eels is transparent and thinned walled.
On dissection, the gasbladder of these
eels proved to be free from infection
or infected as in radiographic examination.
The application of bath treatment
of Levamisole HC1 medicine of both
concentrations 1 or 2mg/l for 24 or 48
hr led death of adult and preadult
nematodes lived in the lumen of the
gasbladder at 24 hr examination post
treatment. The eggs and newly hatched larvae (L2) of Anguillicola
crassus showed no signs of reaction to
the drug. In the control group, eels
contained adult and pre-adult parasites
of A. crassus without any signs of
harm to them. Therefore, the treatment
of eels with drug several times will be
necessary and should be at 4 weeks
after the first application to kill the
178
newly emerged preadult and adult
stages. The break down of the life
cycle should be carried out by controlling the intermediate hosts which is
impossible under culture system. No
signs of toxicity were recorded among
the treated eels.
Electrophoretic analysis of sonicated adult A. crassus proteins in SDSPAGE revealed a series of bands with
different molecular weights illustrated
in Table, (8) and Fig. (10).
Anisakidae larvae (Fig., 11):
The total prevalence of Anisakiid
larvae was 0.4%. Anisakiid larvae
were detected in the abdominal cavity
of wild eel only (0.8%) (Table, 7). No
clinical abnormalities and postmortem
lesions were observed in the infected
fish. The total length of free Anisakiid
larvae is 0.22-0.34mm, their maximum width being 0.02-0.03mm.
Oesophagus is provided with a long
ventriculus. Also, it is characterized
by the presence of prominent boring
tooth. An anal gland is present. Cuticle
was characterized by fine transverse
striations.
Cestodiasis (Fig. 12&13):
The total prevalence was 8.9%. No
infection was recorded in the wild
fish, while it was 17.8% in cultured
ones (Table, 9). The total prevalence
of Proteocephalus species, Cyathocephalus species and unidentified cestode
species infection was 6.9, 1.9 and 0.1
% among the total examined fish,
Ahmed El-Ashram
respectively (Table, 10). The causative agents isolated from diseased
fish were Proteocephalus species,
Cyathocephalus species and unidentified cestode species (Fig. 12 & 13).
All of them were living in intestine.
Pathological effects would be related
to the number of parasites per fish.
Heavily infected fish had distended
abdomen and emaciation. The intestine of infected fish showed severe
hemorrhagic enteritis and mechanical
obstruction as well as upsetting fish
general condition.
Crustaceans
The total prevalence of gills copepods (Ergasilus species) was 19 %.
The prevalence among the wild and
cultured eels was 4.3 and 33.8%,
respectively (Table, 11). The crustacean parasite was detected in gills of
eel. The infested gills showed elongated yellowish white nodules and a
great amount of thick mucus secretion
(Fig. 14). Also, there were respiratory
distress and congested gills at the early
of infection which turned pale later on.
SCVMJ, XII (2) 2007
179
Table (1): The total prevalence of parasitic diseases among the examined eels.
Type of fish
Number of examined fish
Number of infested fish
%
Wild
400
290
72.5
Cultured
400
335
83.8
Total
800
625
78.1
Table (2): The prevalence of protozoal parasites in both wild and cultured eels.
Type of fish
Trichodina
Number of
examined fish
I. multifiliis
No.
%
No.
%
Myxidium
giardi
No.
%
Myxobolus
dermatobius
No.
%
12.5
0
0
17
4.3
30
Eimeria sp.
No.
%
7.5
0
0
Wild
400
50
Cultured
400
200
50
20
5
85
21.3
150
37.5
4
1
Total
800
250
31.3
20
2.5
102
12.8
180
22.5
4
0.5
Table (3): Treatment of the eels infested with Trichodina species disease by
using formalin.
Fish group
Agent
Treated
Control
Formalin
-
Number of
infested fish
10
10
Number of dead
fish
0
3
Mortality rate
0
30
Table (4): The prevalence of monogenetic trematodes among the examined eels.
Type of fish
Number of examined fish
Number of infested fish
%
Wild
Cultured
400
400
104
286
26
71.5
Total
800
390
48.8
Table (5): Prevalence of monogenetic trematodes in wild and cultured eels.
Type of fish
Wild
Cultured
Total
Number of
examined fish
400
400
800
Pseudodactylogyrus
Gyrodactylus
Quadriacanthus
No.
%
No.
Dactylogyrus
%
No.
%
No.
%
50
200
250
12.5
50
31.3
28
52
80
7
13
10
11
24
35
2.8
6
4.4
15
10
25
3.8
2.5
3.1
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Ahmed El-Ashram
Table (6): Mortality rate of laboratory trial for the use of Praziquental
against Pseudodactylogyrus infection.
Fish group
Agent
Treated
Control
Praziquental
-
Number of infested
fish
20
20
Number of dead
fish
2
7
Mortality rate
10
35
Table (7): The prevalence of A. crassus and Anisakis larvae among the
examined eels.
Type of fish
Wild
Cultured
Total
Number of examined
fish
No.
A. crassus
%
Anisakis larvae
No.
%
400
400
800
290
335
625
72.5
83.8
78.1
3
0
3
0.8
0
0.4
Table (8): Molecular weights of protein banding patterns of A. crassus.
BN
1
2
3
4
5
6
7
8
9
10
11
12
13
RF
0.167
0.207
0.228
0.285
0.395
0.421
0.513
0.628
0.657
0.723
0.778
0.813
0.873
MW
205.000
97.400
66.000
29.000
-
BN= Band number
Sample1
190.989
173.633
165.162
144.195
110.960
104.297
83.773
63.701
59.450
50.802
44.564
41.000
35.540
Sample2
190.989
173.633
165.162
144.195
110.960
104.297
83.773
63.701
59.450
50.802
44.564
41.000
35.540
RF=Relative front
Sample3
190.989
173.633
165.162
144.195
110.960
104.297
83.773
63.701
59.450
50.802
44.564
41.000
35.540
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181
Table (9): The prevalence of cestodes among the examined eels.
Type of fish
Number of examined fish
Number of infested fish
%
Wild
Cultured
Total
400
400
800
0
71
71
0
17.8
8.9
Table (10): The prevalence of cestode species among the examined eels.
Type of fish
Number of
examined fish
400
400
800
Wild
Cultured
Total
Proteocephalus species
No.
%
0
55
55
0
13.8
6.9
Cyathocephalus
species
No.
%
0
15
15
0
3.8
1.9
Unidentified
species
No.
%
0
1
1
0
0.3
0.1
Table (11): The prevalence of Ergasilus species in both wild and cultured eels.
Type of fish
Number of examined fish
Number of infested fish
%
Wild
400
17
4.3
Cultured
400
135
33.8
Total
800
152
19
182
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Fig. (1): (A) Eel specimen infected with external parasite. (B) gill of infected specimen with
Trichodina species (C) Trichodina sp. (D) Ichthyophthirius multifiliis.
Fig. (2): (A) Eel specimen infected with Myxidium species showing white spot on skin. (B)
Myxidium species cysts from gills surrounded with melanomacrophages. (C) Light
micrograph of cyst. (D) Fresh spores of Myxidium species.
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183
Fig. (3): (A) Fins of eel showing white nodules due to infestation with Myxobolus species
(B) Melanomacrophages surrounding infestation. (C) Light micrograph of cyst. (D) Fresh
preparation of mature Myxobolus species spores (E) Front view of stained spores. (X 1000)
(F) Scanning electron micrograph of fresh Myxobolus spore.
Fig. (4): Eimeria sp. in intestinal scraping.
184
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Fig. (5): Gills Monogeneans. (A) Pseudodactylogyrus species. (B) Dactylogyrus species. (C)
Gyrodactylus species. (D) Quadriacanthus species.
Fig. (6): (A) Anguilla anguilla naturally infected with Anguillicola crassus showing
swollen of abdomen. (B) Eel showing turbid wall of gasbladder. (C) Gasbladder heavy
infected with A. crassus (D) A. crassus in Petridish. (E) Gasbladder occupied by single A.
crassus.
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185
Fig. (7): Eel specimens infected with Anguillicola crassus showing red swollen anus.
Fig. (8): (A) Adult Anguillicola crassus (A) Anterior end. (B) Male posterior end. (C)
Female posterior end. X120. (D) Scanning electron micrograph of A. crassus teeth inside
buccal capsule. (E) Hatched second stage larva inside a loose cuticular sheath.
186
Ahmed El-Ashram
Fig. (9): Radiograph of the gasbladder of eel (lateral view). (A) clearly outlined gasbladder.
(B) Radiographic shadow of worms in the cranial part of gasbladder (partial shadow). (C)
The gasbladder is packed with worms and no radiographic shadow.
Fig. (10): Coomassie blue stained SDS-PAGE of adult A. crassus. M, molecular weight
markers indicated in kDa.
SCVMJ, XII (2) 2007
187
Fig. (11): Anisakis species larvae (A) Anterior end. (B) Posterior end
Fig. (12): Proteocephalus species infection. (A) Intestine of eel heavily infected with cestode.
(B) unstained scolex. (C) Stained scolex. (D) Mature segment.
188
Ahmed El-Ashram
Fig. (13): (A) Cesode infection in mouth after death of eel. (B) Cyathocephalus species
scolex. (C) Cyathocephalus species mature segment. (D) & (E) Unidentified cestode.
Fig. (14): (A) Gill of eel infested with Ergasilus species. (B) Ergasilus species in Petri dish.
(C) Ergasilus species, adult female attached to gills.
SCVMJ, XII (2) 2007
DISCUSSION
There is a general decline in eel
production worldwide (McKinnon,
2006). Eels are susceptible to a
number of diseases and parasites
(Gosper 1996). During the last decades, a greater attention had paid to
the problems posed by parasites and
their importance for fishery even at
sub-clinical levels, leading to constraints in the productivity of aquaculture (Scholz, 1999). The good identification of the parasitic agents infesting fishes under the egyptian conditions usually is the first step to control
infestation or even prevent its reoccurrence. However, there is a less
knowledge of parasitic diseases observed in farmed eels than of other
significant aquaculture species in Egypt.
There is a requirement for research in
the parasitic diseases of the farmed
eels for addition knowledge of exotic
diseases that may be of future significance for the industry.
Besides direct losses caused by
mortality, parasites may have considerable impact on growth and behavior
of fish, their resistance to other stress
factors, susceptibility to predation and
reduction of marketability (Woo, 1995;
Barker 1997 and Scholz, 1999).
The total prevalence of infection
was 78.1% among the examined eels,
with a higher rate in cultured eels
(83.8%) than in wild one (72.5 %).
Barker (1997) recorded that the total
rate of parasitic infection was 43 to
48%. Agullar et al., (2005) found that
the total rate of parasitic infection
among eels collected from Ulla and
Tea River in Spain was 99.4 and
99.6% respectively. Woo (1995);
Barker (1997) and Barker and Cone
(2000) mentioned that the prevalence
189
differed according to weight, length,
sampling sites and water quality.
However, Barker and Cone (2000)
and Agullar et al., (2005) mentioned
that fish farms provide an ideal
conditions for transmission of infectious diseases.
Ectoparasitic protozoan diseases
are the most important parasitic diseases of cultured fishes (Woo, 1995).
Production of eel in Egypt is depending on the collection of glass eels or
elvers caught along the Egyptian coasts. Parasites were introduced to the
farm with such wild eels and under
aquaculture conditions, these parasites
increased in numbers and cause heavy
mortalities. Trichodina had previously
been reported from eels (Madsen et
al., 2000; and Agullar et al., 2005).
The total prevalence of trichodinosis was 31.25%. A higher rate of
infection was recorded in cultured fish
(50%) than in the wild one (12.5%).
Woo (1995) mentioned that the ciliates
occurred in low number in feral fish.
Barker (1997) recorded that the total
prevalence of gill parasites was 56 to
57%. On the contrary, El-Dosoky,
(2007) reported a higher prevalence in
wild eel (36.4%) than in cultured one
(20.6%). A lower rate was noticed by
Agullar et al. (2005) in Ulla and Tea
River (9.9 and 1.5% respectively).
Clinically, the infected fish showed
respiratory distress, frayed fins and
epidermal erosion. Heavily infested
eels had grayish coat due to increased
secretion of mucus. Similar clinical
abnormalities were noticed by Woo
(1995); Madsen et al. (2000a); Madsen
et al. (2000b); Buchmann and Bresciani
(2001) and El-Dosoky (2007).
190
Regarding the treatment of the
infected fish, it is obvious that formalin led to complete disappearance
of Trichodina species. The mortality
rate was 30% in the non-treated group.
All infected fish became normal in
behavior. Similar result had mentioned
by Woo (1995); Paperna (1996) and
Madsen et al. (2000b).
Ichthyophthiriasis is one of the most
serious infectious diseases leading to
considerable losses due to mortality or
decreased yield in non-lethal infections as reported in cultured eel (Scholz, 1999). White spot disease was
only recorded in cultured eel (5%). On
the contrary, Agullar et al. (2005)
observed that the prevalence of I.
multifiliis was 23.5 to 30.5% in wild
eels. The infected eel showed loss of
appetite and heavy mucus secretion. I.
multifiliis was detected in the gills and
skin of infected eel. Such findings
were met by Woo (1995); Paperna
(1996) and Scholz (1999).
Myxidium is a wide spread myxozoan parasite of cultured fishes leading to severe economic losses (Woo,
1995). The total prevalence of Myxidium species infection was 12.8%. The
rate in wild and cultured eel was 4.3
and 21.3% respectively. Silva et al.
(1993) reported that the prevalence of
Myxidium was 54% in the gills and
skin of A. anguila. El-Dosoky (2001)
isolated Myxidium from skin only with
a rate of 4.2 and 0% in wild and
cultured eels respectively. Agullar et
al., (2005) noticed a prevalence of
95%. El-Dosoky (2007) recorded that
the prevalence of Myxidium species
was 6.3 and 15.9% in cultured and
wild eel, respectively. Kristmundsson
and Helgason (2007) recorded M.
giardi in a high prevalence (30.0 to
93.3%). They noticed that Myxidium
Ahmed El-Ashram
giardi most heavily infected the gills,
but kidneys and various other organs
were also frequently infected.
Clinically infected eels showed small
whit spots scattered on the skin, ulcer
and respiratory distress. The macroscopic cyst rendered fish unsightly and
unmarketable. Similar observations were
recorded by Egusa (1992); Gosper
(1996); El-Dosoky (2001) and Kristmundsson and Helgason (2007).
Microscopically black cysts were observed in gills containing spores. The
black color may be due to accumulation of melanomacrophages. Spores
were spindle in shape and both ends
were pointed. Similar morphological
criteria were noticed by Woo (1995);
Paperna (1996) and El-Dosoky (2001).
The prevalence rate of Myxobolus
infection was 22.5%. A higher one
was recorded in cultured eel (37.5%)
than the wild one (7.5%). Agullar et
al. (2005) found that the prevalence of
Myxobolus ranged 26.5 to 34.5%.
Kristmundsson and Helgason (2007)
detected Myxobolus from fins with a
prevalence of 3.3 to 6.6%. Clinically,
whitish nodules (1-3mm) located in
the subcutaneous tissues of eel fins
which ruptured left ulcer. Similar pictures were noticed by Woo (1995);
Paperna (1996) and El-Dosoky (2001)
who mentioned that the rupture of
dermal and branchial cysts caused intense hemorrhaging and facilitated secondary bacterial invasion. On the
other hand, Copland (1982) recorded
the infection with Myxobolus dermatobius from stomach and intestine of
eel.
The prevalence of Eimeria infection was rare (0.5%). It is only reported in cultured fish (1%). Kristmundsson and Helgason (2007) found
SCVMJ, XII (2) 2007
Eimeria anguillae on rare occasions.
On the contrary, Agullar et al. (2005)
detected Eimeria species in wild eel
with a prevalence of 2.5 to 3.7%.
Unsporulated oocyst of Eimeria sp.
was spherical, 12.5 µm in diameter.
The wall of oocyst was double layered
with 0.5µm between the two layers.
Similar morphological characters were
reported by Lom and Dykova (1992).
Infection with helminthes are quite
common in both wild and cultured fish
and may cause problems in aquaculture (Scholz, 1999). The monogenean parasites are serious pests of anguillid eels. Heavy infestation retarded
production in eels rearing facilities by
causing morbidity and mortality (Barker and Cone, 2000 and Hayward et
al., 2001).
The total prevalence of gill monogeneans was 48.8%. A higher rate was
recorded in cultured eels (71.5%) than
in wild one (26%). Barker (1997) reported that the prevalence of monogenea among the examined eels was
5-18%. Sures and Street (2001) recorded that the prevalence of Pseudodactylogyrus species was 89.5 to 94.3%
in River Rhine. Sobecka and PileckaRapacz (2003) found that the prevalence of P. anguillae was 82% among
the examined wild eel. Agullar et al.,
(2005) observed that the prevalence of
Pseudodactylogyrus species infection
was 30.2 to 56% among the wild eels.
On the other hand, El-Dosoky, (2007)
191
recorded that the prevalence of Pseudodactylogyrus species and Dactylogyrus species infection among cultured and wild eels was 22.2,43.1 and
9.0,20.5%, respectively. Heavily infected eels showed excessive mucus,
loss of appetite and respiratory distress. Microscopically, the monogeneans were found attached to the gill
filaments. Similar pictures were previously described by Buchmann et al.,
(1987); Buchmann (1988); Cone and
Marcogliese (1995); Barker and
Cone (2000); Sobecka and PileckaRapacz (2003) and El-Dosoky (2007)
who found that the intense infection of
monogenean parasites often result in
gill hyperplasia, increased gill mucus
production, physical distortion of the
gill filaments, and respiratory failure.
Moreover, various species of Monogenea can serve as vectors for viral
and bacterial pathogens of fish (Cusack and Cone, 1986).
Our results showed that praziquental in a concentration of 10mg/l for
1 hr was an effective agent in controlling Pseudodactylogyrus species
infection. These results were in agreement with those mentioned by Woo
(1995) and Paperna (1996).
Anguillicolois is widely recognized
as one of the most important economically damaging disease affecting eels
culture allover the world. The introduction of blood feeding nematode, A.
crassus, into Europe in the 1980s
192
occurred through importation of
infected Japanese eels from East Asia
and later became established in North
Africa (Kirk, 2003 and Moravec et
al., 2005). The genus Anguillicola
comprises five species (Moravec et
al., 1994). A. crassus is the most
important species infecting eel. Amer
and El-Ashram (2006) detected A.
novaezelandiae for the first time from
eels in Egypt.
The total prevalence of A.
crassus infection was 78.1%. The rate
in wild and cultured eels was 72.5 and
83.8 %, respectively. Nearly similar
result was recorded by Ercüment et
al. (2005) ranged 72.41 to 82.86%.
The prevalence of A. crassus infection was higher than that reported by
El-Dosoky, (2001); Evans et al.,
(2001); Crean et al., (2003); Agullar
et al., (2005) and El-Dosoky (2007)
were 9.9, 55.5, 66, 66.5 and 75.17%,
respectively. A higher rate (100%)
was noticed by Molnar et al., (1993).
However, Kristmundsson and Helgason (2007) recorded no A. crassus
infection in Iceland. They mentioned
that low winter temperature of most
Icelandic freshwater systems would
seriously hamper a successful development of A. crassus.
Anguillicolois caused mass mortalities of eel in Lake Balaton during
1991 and 1995 and in Lake Gnarpurt
(Molnar et al., 1993 and McKinnon,
2006). Eels displayed clinical signs of
Ahmed El-Ashram
infection including, distended and red
anus. Ruptured gasbladders were recorded in heavily infected fish. Similar
clinical signs were recorded by Evans
et al., (2001); El-Dosoky (2001); Kirk
(2003); Amer and El-Ashram (2006)
and El-Dosoky (2007). Crean et al.
(2003) and El-Dosoky (2007) observed that the anal redness may provide
a simple, non-invasive diagnostic tool
for A. crassus infection. The adverse
effect of dracunculoid nematode (A.
crassus) is due to blood sucking feeding, occlusion of the lumen and migration of the larvae (Kirk, 2003). This
nematode possesses many characteristics seen in successful colonizers as a
high reproductive potential, low degree of intermediate specificity and infectivity in fresh and marine water and
infect all sizes (Gosper, 1996).
Concerning the morphological characters of A. crassus, these were similar to those mentioned by Moravec,
(1994) and El-Dosoky, (2001).
The great potential of radiodiagnostic methods in fish medicine as
an aid in the diagnosis of infection was
suggested by Beregi et al., (2001). Our
results showed that the radiodiagnostic
method appeared to be a useful tool in
the diagnosis of anguilliculosis. The
method is based on the radiodiagnostic
principle that organs filled with air are
radiotransparent and thus readily discernible as dark areas on the radiograph
(negative contrast) (Beregi et al., 1998).
The gasbladder of healthy eels is
clearly outlined and a full air filled
lumen on the radiographs. The infe-
SCVMJ, XII (2) 2007
cted eels showed deformity and nonhomogenous area in the shadow of the
gasbladder according to the intensity
rate because it is not completely filled
with worms. While no radiographic
shadow and no area containing air was
detected when the lumen of the gasbladder was entirely filled with worms.
Radiographic examinations were confirmed by the dissection of the examined fish. Similar pictures were
obtained by Beregi et al., (2001); ElDosoky (2001); Szekely et al., (2005)
and El-Dosoky (2007).
Controlling of fish diseases is one
of the most important tasks in aquaculture. Basically, there are two ways
of controlling anguillicolosis (Hartmann, 1989 and Geets et al., 1992). The
first method is the use of therapeutic
treatment of infested eels with anthelmintics. Our results showed that the
application of bath treatment with Levamisol at concentrations of 1mg/l for
24 or 48 hr or 2mg/l for 24 or 48 hr
led to a complete cure of eels from
anguillicolosis. Similar results were
recorded by Taraschewski et al.,
(1988); Hartmann (1989); Geets et
al., (1992) and El-Dosoky (2007) who
found that Levamisol was the most
effective drug, can bring about the complete recovery of eels. Secondly, eliminate the intermediate host so that
the life cycle of the parasites cannot be
completed. Complete eradication of
the intermediate host was impossible
under natural conditions (Geets et al.,
1992). Hartmann (1989) recommended a second treatment under freshwater condition scheduled about 3
weeks after the first, and possibly
other treatments later at longer time
intervals. Hartmann (1989) noticed
that some of the nematodes are able to
regenerate after suffering sublethal
193
damage. Bath treatment was the best
method since eels that did not feed
could also be treated (Geets et al.,
1992). Kennedy and Fitch (1990)
suggested that the best approach to
limit the spread of A. crassus is
through legislation regulating import
and export of eels.
Regarding the electrophoretic protein pattern of A. crassus, the present
study revealed a series of bands with
different molecular weights which may
be will be helpful in the diagnosis and
development of new vaccine against
parasites (Scholz, 1999).
Fish Anisakiid larvae are nematode
stages of cosmopolitan distribution with
a wide range of hosts (Woo, 1995).
The total prevalence of Anisakiid
larvae was 0.4%. Anisakiid larvae
were found in the abdominal cavity of
wild eel only (0.8%). Neither clinical
signs nor postmortem lesions were
recorded in the infected fish. Agullar
et al., (2005) reported 0.3% as a
prevalence of A. simplex in wild eel.
Kristmundsson and Helgason (2007)
found one specimen of a third-stage
larva of Anisakis simplex in the visceral cavity of one marine eel.
The total prevalence of cestode infection was 8.9%. No infection was
recorded in the wild fish, while it was
17.8% in cultured ones. The total rate
of Proteocephalus species, Cyathocephalus species and unidentified cestode infection was 6.9, 1.9 and 0.1 %
among the total examined fish, respectively. Barker (1997) recorded that
the total prevalence of Proteocephalus
was rare (2-3%). Kristmundsson and
Helgason (2007) observed that the
cestode Proteocephalus macrocephalus (16.6%) was common in eels.
Sures and Street (2001) recorded that
the prevalence of Proteocephalus spe-
194
cies was 15.8% in River Rhine. Agullar et al., (2005) mentioned that
cestode infection was 1% among the
examined eels. On the contrary, ElDosoky (2001) detected cestode infection among wild and cultured eels at
rate of 18 and 13% respectively.
Stefansson (2000) studied the diet of
eels and found the tendency for
smaller eels to eat proportionally more
of small crustaceans, which are vital in
the life cycle of cestode.
Cestode infecting cultured eels was
reported to cause intestinal tissue destruction, mechanical blockage and nutrient absorption at the expense of the
host in heavily infected fish. This was
in accordance with Woo (1995); Paperna (1996) and El-Dosoky (2001).
The crustacean Ergasilus species
frequently parasitize gills of eels causing significant damage to host. The
total prevalence of gills copepods was
19 %. The rate among the wild and
cultured eels was 4.3 and 33.8%, respectively. Barker (1997) reported that
the rate of gill copepod was 5 to 23%.
While, Agullar et al., (2005) noticed
that the prevalence of Ergasilus was
1.5 to 3.5% in Spain. On the other
hand, El-Dosoky (2001 and 2007)
failed to detect crustacean infections
among the examined eels. Barker and
Cone (2000) found that the prevalence
of Ergasilus and Pseudodactylogyrus
species among wild eels was related to
stream flow, pH and temperature. The
infested gills showed elongated yellowish white nodules and a great amount of thick mucus secretion. Similar
clinical signs and postmortem changes
were noticed by Woo (1995); Paperna (1996) Barker and Cone (2000)
who mentioned that heavy infection of
Ergasilus cause severe hemorrhaging
Ahmed El-Ashram
and gill inflammation associated with
attachment and feeding of parasites.
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Taraschewsk, H.; Renner, C. and
Mehlhorn, H. (1988): Treatment of
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in the air bladder of eels. Parasitol.
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Woo, P.T.K. (1995): Fish diseases and
disorders. CABI Publish., London, U.K.
‫‪198‬‬
‫‪Ahmed El-Ashram‬‬
‫الملخص العربى‬
‫دراسات على األمراض الطفيلية فى أسماك الثعبان (أنجويال أنجويال) البرية والمستزرعة‬
‫أحمد محمد محمود األشرم‬
‫قسم أمراض األسماك – المعمل المركزي لبحوث الثروة السمكية (العباسة) – مركز البحوث الزراعية‪.‬‬
‫أجريت هذه الدراسة علي عدد ‪ 088‬عينة سمكية من أسماك الثعبان بواقع ‪ 088‬عينة تم تجميعها‬
‫من بحيرات (برية) و عددد ‪ 088‬عيندة أردر تدم تجميعهدا مدن المد ارس الةدمكية (مةدز رعة) بمحافظدات‬
‫الشرقية والبحيرة وكفر الشيخ‪ .‬أسزمرت هذه الراسة لمدة ثالثة أعوام وذلك لدراسة األمراض الطفيلية الزي‬
‫تصيبها‪ .‬كذلك أجريت بعض المحاوالت العالجية لبعض األمراض‪ .‬كانت نةدبة األادابة الكليدة للطفيليدات‬
‫المخزلفة هى ‪ .% 1087‬حيث كانت النةبة فى األسدماك البريدة والمةدز رعة هدى ‪ % 0.80 , 1.87‬علدى‬
‫الزددددوالى‪ .‬كانددددت نةددددبة األاددددابة الكليددددة بعدددددو الزريكودينددددا‪ ,‬األكثيوفثريددددا‬
‫مددددالزيفيال ‪ ,‬ميجدددد ديم‪,‬‬
‫المكةوبولس‪ ,‬الديدان المثقوبة وحيدة العائل‪ ,‬األيميريا‪ ,‬األنحيوليكوال كرازيس‪ ,‬يرقات األنيةداكس‪ ,‬ديددان‬
‫شددريطية واألرجةدديليس هددى ‪ 088 ,880 ,1087 ,887 ,0080 ,..87 ,7.80 , .87 ,.78.7‬و ‪%78‬‬
‫علدددى الزدددوالي‪ .‬أظهدددرت الدراسدددة ان الديددددان المثقوبدددة وحيددددة العائدددل الزدددى تصددديل أسدددماك الثعبدددان هدددى‬
‫سدددددودوداكزيلوجير‬
‫(‪ ,)%.78.‬داكزيلدددددوجير‬
‫(‪ ,)%78‬جيدددددروداكزيلس (‪ )%080‬وكوادريكانةددددديس‬
‫(‪ .)%.87‬بينت الدراسة ان الديدان الشريطية الزى تم ع لها وتشخيصها مع نةدبة األادابة كاندت كالزدالى‪:‬‬
‫بروتيوسيفليس (‪ ,)%988‬سياثوسيفاليس (‪ )%788‬وغير معروفة ‪ .)%887‬تم تةجيل العالمدات المريدية‬
‫االكلينيكية والزغيرات المصاحبة لكدل مدرض علدى حددة‪ .‬أشدارت النزدائا ان الفورمدالين عندد تركيد ‪88.7‬‬
‫ج ء فدى المليدون والبرازيكونزيدل (‪ 78‬ملجدم ‪/‬لزدر) لمددة سداعة لهمدا القددرة فدى قزدل افيلدي الزريكوديندا و‬
‫سودوداكزيلوجير‬
‫على الزوالى‪ .‬ظهر جليدا مد ن الدراسدة ان أسدزخدام أشدعة أكدس يةداعد فدى الكشد‬
‫عدن‬
‫األاابة بطفيل األنحيوليكوال كرازيس والزغيرات المصاحبة لهذه االاابة فى المثانة الهوائيدة‪ .‬كمدا أمزددت‬
‫الدراسة لزشمل عملية الزفريد الكهربائي لطفيل األنحيوليكوال كرازيس‪ .‬أويحت الدراسة مد تدثثير عقدار‬
‫الليفامي ول القاتل بالنةبة لطفيل األنحيوليكوال عند تركي ‪ 7‬أو ‪ .‬ملجم‪/‬لزر لمدة ‪ .0‬أو ‪ 00‬ساعة‪.‬‬

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