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Iranian J Parasitol: Vol. 8, No.3, July -Sep 2013, pp.423-429
423 Available at: http://ijpa.tums.ac.ir
Original Article
Seasonal and Geographic Distribution of Cercarial Infection in
Lymnaea gedrosiana
(Pulmunata: Lymnaeidae) In North West
Iran
Abbas IMANI-BARAN 1, *Mohammad YAKHCHALI 2, Reza MALEKZADEH-VIAYEH 3,
Ali FARAHNAK 4
1. Dept. of Pathobiology, Parasitology Division, Faculty of Veterinary Medicine, Tabriz University, Tabriz, Iran
2. Dept. of Pathobiology, Parasitology Division, Faculty of Veterinary Medicine, Nazlu campus, Urmia University, Urmia, Iran
3. Artemia and Aquatic Animals Research Institute, Urmia University, Urmia, Iran
4. Dept. of Parasitology and Mycology, School of Public Health, Medical Sciences of Tehran University, Tehran, Iran
Received 11 Feb 2013
Accepted 19 May 2013
Abstract
Background:
Trematodes are a diverse group of endoparasites which require
molluscan and vertebrate animals as intermediate and definitive hosts in their life
cycle. The present study was carried out to determine the diversity and geographic
distribution of infection with trematodes’cercariae in the snail Lymnaea gedrosiana
from north-west Iran.
Methods:
A total number of 6759 Lymnaeidae snails were collected from 28 snail
habitats; of these L. gedrosiana was the prevalent snail (74.37%) which examined
for cercarial infection by shedding method.
Results:
The overall infection rate was 8.03%. The most frequent trematodes
cercariae in the snail were xiphidiocercariae (81.98%), furcocercariae (32.26%),
echinostome cercariae (5.19%), and monostome cercariae (1.24%). The highest
infection rate in L. gedrosiana (100%) was with echinostome cercariae from
Golestaneh in autumn.
Conclusion:
Due to the important role of pond snails in transmission of cercariae
to fish as a source of zoonotic diseases, it is essential to estimate the distribution
and abundance of the snails and the rate of their infection with different trema-
todes’ cercariae, and establish control programs in each region.
Keywords
Cercariae,
Lymnaea gedrosiana,
Iran
*Correspondence
Email:
m.yakhchali@urmia.ac.ir
Iranian Society of Parasitology
http:// isp.tums.ac.ir
Iranian J Parasitol
Open access Journal at
http:// ijpa.tums.ac.ir
Tehran University of Medical
Sciences Publication
http:// tums.ac.ir
Imani-Baran et al.: Seasonal and Geographic Distribution …
Available at: http://ijpa.tums.ac.ir 424
Introduction
igenian trematodes have compli-
cated life cycles in which molluscs
play the key role as intermediate
hosts for part of their developmental stages.
In this regard, freshwater snails, in particular
those from the order Basomamtophora, have
substantial contribution to development and
transmission of parasitic flukes. For instance,
some 20 species of cercariae have been iso-
lated from the lymnaeid snails of Lymnaea pere-
gra (Muller, 1774) (1). Snail-mediated diseases
are among the major groups of helminthic dis-
eases caused by trematode parasites. However,
the main snail species involving in the trans-
mission of flukes vary in different geo-
graphical regions.
Freshwater snails have been studied in dif-
ferent Iranian provinces including Fars,
Khoozestan and Mazandaran (2-5). L.
gedrosiana (Annandale and Prashad, 1919) has
been reported to be a prefered intermediate
host for a number of parasitic helminths such
as Fasciola gigantica (Cobbold, 1855) (6),
Ornitobilharzia turkestanicum (Skrjabin, 1913) (2,
7), and Trichobilharzia spp. (3). It was also
found that L. gedrosiana had a considerable role
in the transmission of zoonotic diseases such
as cercarial dermatitis (1.1% in South-West
and 0.05% in North of Iran), fasciolosis
(0.35%), Plagiorchids infections (0.1%), and
Clinostomum infections (0.2%) in Iran (3, 6, 8-
10). Therefore, examination of the snails
makes it possible to gain information about
the degree to which they are responsible for
infection distribution. This is also the keystone
for identifying the trematode fauna in the are-
as of interest.
To date, no large-scale study has been car-
ried out on the distribution and abundance of
L. gedrosiana and its contribution to the
transmition of cercarial infection in north-
western Iran. Thus, the aim of this study was
to elucidate the seasonal and regional inci-
dence of L. gedrosiana and its rate of cercarial
infections in the region.
Material and Methods
Study area
West Azerbaijan Province is located in
north-west of Iran (35°46´ to 39°58´ in lati-
tude and 44°3´ to 47°23´ in longitude) (Fig. 1).
Fig.1: Map of the collected Lymnaea gedrosiana with
cercariae infection in West Azerbaijan province,
Iran (1. Ziveh, 2. Osaloo, 3. Najafabad, 4. Esm-
jondi, 5. Urmia-Goushji Road, 6. Shorgul, 7.
Eslamabad, 8. Gargulug, 9. Shabanlu, 10. Darlak,
11. Gugarchingaleh, 12. Garehbagh, 13. Garehag-
haj, 14. Esmailkandi, 15. Marganlar)
Excluding the Lake Urmia, this semi-humid
and temperate province has an area of
37,608 km² elevating 1,332m above sea level.
The climate of the province is largely influ-
enced by the rainy winds of the Atlantic
Ocean and Mediterranean Sea; the maximum
temperature reaches 34°C in July, while mini-
mum temperature may be –16°C in January.
Annual precipitation varies between 300 and
800 mm with large yearly and monthly fluctua-
tions. Generally, the province witnesses two
rainy seasons, the first from March to May
and the second in October-November (5).
Three are numerous water bodies and reser-
voirs with relatively appropriate environmen-
tal conditions in West Azarbaijan province
D
Iranian J Parasitol: Vol. 8, No.3, July -Sep 2013, pp.423-429
425 Available at: http://ijpa.tums.ac.ir
where suitable habitats are provided for pond
snails (5).
Snail
collection
A total of 28 perennial and seasonal fresh-
water snails habitats were monitored from
May to December 2010 (Fig.1). The habitats
included various water-body types, i.e. wet-
lands, ponds, rivers, canals, springs, swamps,
pools, streams and ditches, located in both
mountainous and low-land areas of north,
central and south parts of the province. Snail
sampling was undertaken by searching each
site for 15 minutes using a standard flat wire
mesh scoop with a mesh size of 2mm (11, 12).
The collected snails were placed in plastic
screw cap containers containing the water of
snail habitat and transferred alive to the labo-
ratory for species identification using the
morphological keys provided by Mansoorian
(13) and Pfleger (1). The identified snails were
kept alive in an aquarium at optimal condi-
tions to be investigated for their cercarial in-
fection.
Collection of cercariae from the infected
snails
The identified snails as L. gedrosiana were
transferred to the Parasitology Museum of the
Tehran Faculty of Veterinary Medicine for
detailed characterization and verification. The
snails were then placed individually in flat-bot-
tomed glass vials (height 7.5 cm, diameter 2.5
cm) containing filtered pond water and ex-
posed to a 100-W light bulb at a distance of
15cm for 4-6 hours for cercarial shedding (14).
The snails which did not shed cercariae on the
first exposure were re-exposed on the second
day. Cercariae were characterized by morpho-
logical and biometrical examinations as de-
scribed by Frandsen and Christensen (15).
Statistical evaluation
Data were analyzed by SPSS statistical pro-
gram (version 14, SPSS Inc., Chicago, IL,
USA) using the non-parametric Chi-square
test with confidence interval of 95%. Proba-
bility of < 0.05 was regarded as significant.
Results
Snails
Of the total of 6759 collected Lymnaeidae
snails, L. gedrosiana was the predominant spe-
cie (74.37%) observed in 18 out of the 28 in-
vestigated water bodies (Fig. 1). The snail was
found mainly in the stagnant or slow-moving,
clear to slightly turbid waters with aquatic
plants cover. During the course of this study,
the seasonal and geographical distributions of
L. gedrosiana were significantly different (P =
0.0001). However, there was no significant
differences in the distributions for the snail in
Ziveh (P = 0.816) and Gogarchinghaleh (P =
0.677). The snails counts were significantly
higher in summer than in autumn (P =
0.0001) (Table1).
Table 1: Association between regional and sea-
sonal distribution of Lymnaea gedrosiana population
in northwestern Iran (n=5026)
Place
Season
P
Summer
Autumn
Ziveh
38
36
0.816
Najafabad
181
0
0.0001
Shorgol
156
121
0.035
Ghargologh
30
15
0.025
Shabanlu
222
154
0.0001
Gogarchinghaleh
188
180
0.677
Gharahaghaj
344
406
0.024
Esmailkandy
372
175
0.0001
Marganlar
294
0
0.0001
Diversity and abundance of cercariae
From the 3673 identified L. gedrosiana snails,
8.03% were infected with cercariae of differ-
ent trematodes (Table 2). The infections were
observed throughout the study period, but the
largest number of the infected snails was ob-
served between June and August (Table 3).
Identified cercariae and their respective contri-
bution to the total snail infection rate were as
follows: xiphidiocercariae 81.98%, furcocerca-
riae 32.26%, echinostome cercariae 5.19%,
and monostome cercariae 1.24% (Table 2).
Xiphidiocercariae and monostome cercariae
Imani-Baran et al.: Seasonal and Geographic Distribution …
Available at: http://ijpa.tums.ac.ir 426
were found only in the snails sampled from
north part of West Azarbaijan province, while
echinostome cercariae and furcocercariae were
absent from the snails sampled in the central
part of the province. All examined snails
(100%) from Golestaneh in autumn were in-
fected with echinostome cercariae, and the
snails sampled from Gharahaghaj in summer
had the highest infection rate with
xiphidiocercariae (76.81%) (Table 3).
Table 2: Geographical distribution of cercariae infection in examined Lymnaea gedrosiana snails of northwes-
tern Iran (n=3673)
Ccercariae
Place
Snail
No. of
examined snails
Prevalence
(%)
Xiphidiocercariae
Shorgul
277
2.17
Gharahaghaj
750
81.98
Marganlar
294
10.2
Gharahbaagh (Zanoil)
278
2.88
Gharahbaagh (Jamgoli)
242
0.83
Furcocercariae
Marganlar
294
5.44
Gargulug
30
10.02
Echinostome cercariae
Shorgul
Zarineh-roud
277
31
3.61
32.26
Golestaneh
Shorgul
318
277
5.19
3.61
Marganlar
294
3.43
Darlak
60
1.67
Monostome cercariae
Gargulug
30
1.24
Gharahbaagh (Kefi)
261
1.15
Total
-
3673
8.03
Table 3: Seasonal distribution of cercarial infection in examined Lymnaea gedrosiana snails of northwestern Iran (n=403)
Ccercariae
Place
Season
Snail
No. of examined snails
Prevalence (%)
Xiphidiocercariae
Shorgul
Summer
156
3.85
Gharahaghaj
Summer
344
76.81
Gharahaghaj
Autumn
406
5.17
Marganlar
Summer
294
10.24
Gharahbaagh (Zanoil)
Autumn
278
2.88
Gharahbaagh (Jamgoli)
Autumn
242
0.83
Furcocercariae
Shorgul
Summer
156
4.49
Shorgul
Autumn
121
2.48
Marganlar
Summer
294
5.44
Gargulug
Summer
30
10.02
Echinostome cercariae
Zarineh-roud
Golestaneh
Golestaneh
Summer
Summer
Autumn
31
75
243
32.26
30.6
100
Shorgul
Summer
156
3.85
Shorgul
Autumn
121
3.31
Marganlar
Summer
294
3.44
Darlak
Summer
60
1.67
Monostome cercariae
Gargulug
Gharahbaagh (Kefi)
Summer
Autumn
30
261
6.67
1.15
Iranian J Parasitol: Vol. 8, No.3, July -Sep 2013, pp.423-429
427 Available at: http://ijpa.tums.ac.ir
Discussion
Lymnaeidae snails are of medical and veteri-
nary importance since they are required, as
intermediate hosts, to complete the life cycle
of trematode species. They are distributed
throughout the world and are known as the
vectors of more than 71 species belonging to
13 trematode families (16). A considerable
body of research has explored the potential
role of lymnaeid snails in transmitting the in-
fectious parasitic trematodes worldwide (17-
19). However, intra-molluscan trematode par-
asitism is frequently associated with the altera-
tion of a host's growth, fecundity or survival
(20), and its susceptibility to trematodes (21).
In the present study, L. gedrosiana was found to
be a predominant pond snail in the region.
This finding was in accordance with previous
reports from Iran (4,5,13,22,23). Furthermore,
in consitence with several earlier studies (2, 4,
13, 24), in this study the highest population
density of L. gedrosiana was recorded in sum-
mer.
Until present, only a few studies have been
carried out on the diversity and abundance of
cercarial infection in the pond snails of Iran. For
instance, cercarial infection in L. gedrosiana was
reported from Khoozestan province (3, 25), in
Galba truncatula (Müller, 1774) from Khoozestan
and Kurdestan provinces (26), and in L.
gedrosiana and L. palustris (Müller, 1774) from
northern Iran (6, 9, 10). The snail L. gedrosiana is
found to be a general intermediate host for four
groups of cercariae in the studied region. Several
studies have confirmed the simultaneous infec-
tion of L. gedrosiana with echinostome cercariae
(Echinostomatidae), furcocercariae (O. tur-
kestanikum and Trichobilharzia spp.), mon-ostome
cercariae (Notocotylidae), and xip-hidocercariae
(Plagiorchiidae) (2, 3, 24) in Iran. Sharif et al. (10)
found that L. gedrosiana in northern Iran were
also infected with the same cercariae types. Loy
and Haas (27) isolated the larvae of 18
trematode species from L. stagnalis in Germany.
Faltynkova et al. (18) identified 24 trematode
species comprising 19 cercariae in L. stagnalis, of
which the dominant cercariae were those be-
longing to three species of Echinoparyphium
aconiatum, Opisthioglyphe ranae, and Plagiorchis elegans.
Immani-Baran et al. (28) found the infection of
L. auricularia snails in North West Iran with two
groups of fluke’s cercariae, i.e. furcocercariae
and echinostomcercariae.
Seasonality that is mirrored by changes in
environmental variables can intervene in
snail's ecology and influence the larval devel-
opment of a trematode inside its host snail. It
may also affect cercarial shedding (the release
of cercariae from the host snail in nature).
However, the influence of environmental ele-
ments on cercarial shedding is trematode-
specific (29). The optimal reproduction of L.
gedrosiana in northwestern Iran occurs in early
summer (June-July) (2, 4). Similarly, the high-
est cercariael infection rates in lymnaeid snails
of the region were observed between June and
September, while Sharif et al. (10) recorded
the maximum infection rates in late summer
(August-September). Thus, it can be anticipat-
ed that both snail's propagation and their in-
fection with trematodes are correlated with
seasonal variations. Farahnak et al. (30) noted
that various ecological factors such as season
and water temperature, pH and dissolved oxy-
gen influence the emergence of cercariae from
the snails and their release inside the water
resources.
Conclusion
With regard to the importance of farm ani-
mal health in national economy, it is essential
to study the diversity, distribution and abun-
dance of the intermediate hosts of infectious
trematodes, mainly freshwater snails. L. gedro-
siana is a common pond snail in West Azarbai-
jan province which has shown the capacity for
vectoring diverse cercarial species. Results of
this study and those of the related investiga-
tions can assist in collecting data on the eco-
logical relevance of the snails distribution and
the pattern of transmission of digenian
trematodes by the snails and finally, in preven-
Imani-Baran et al.: Seasonal and Geographic Distribution …
Available at: http://ijpa.tums.ac.ir 428
tion and control of the following disease out-
breaks.
Awknowlegments
This study was supported financially by the
Urmia University, Iran. The authors acknowl-
edge the support and interest of the technical
members of the Artemia and Aquatic Animals
Research Institute, Central Lab of Faculty of
Urmia Veterinary Medicine and Malacology
Laboratory at Urmia University, Iran. The au-
thors declare that there is no conflict of inter-
est.
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