Parasitological
Communication
Biosci. Biotech. Res. Comm. 11(2): 187-194 (2018)
Description of intestinal parasites found in some
snakes of Al-Diwaniyah, Iraq
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
Department of Biology, Faculty of Education, University of Al-Qadisiyah, Al-Diwaniyah, Iraq
ABSTRACT
A survey of parasites was conducted in 130 snakes collected from ve sites of Al-Diwaniyah Province (City Center,
Afak, East Hamzah, Al-Badair and Nafer districts of Iraq. The snakes belong to 8 species of two families Colubridae
and Biodae, which contain Platyceps ventromaculatus, P. rogers, Malpolon monspesslana, Sapalerosophis clifordi,
Dolichophis mesopotamicus, Rhynchocalamus melanocephalu, Eryx jaculus and Natrix tessellate. Eighty-three sam-
ples of snakes 63.84% were infected with ve species of internal parasites which include two protozoans, Isospora sp.
and Cryptosporidium sp, two species of nematodes Kalicephalus sp. and Strongyloides sp. and one species of cestode
Oochoristica tandani. Through the site of intestinal parasites in the digestive tract was mostly small intestine, higher
percentage of them were detected in other parts of digestive tract. Results also showed that single parasitic infections
were most common in comparison to other infections. This is the rst survey of intestinal parasites from snakes in
Iraq where detailed description of the intestinal parasites are reported for the rst time from snakes of Iraq.
KEY WORDS: SNAKES, REPTILE, INTESTINAL PARASITES, IRAQ
187
ARTICLE INFORMATION:
*Corresponding Author: Sadiya.anah@qu.edu.iq
Received 27
th
March, 2018
Accepted after revision 19
th
June, 2018
BBRC Print ISSN: 0974-6455
Online ISSN: 2321-4007 CODEN: USA BBRCBA
Thomson Reuters ISI ESC / Clarivate Analytics USA and
Crossref Indexed Journal
NAAS Journal Score 2018: 4.31 SJIF 2017: 4.196
© A Society of Science and Nature Publication, Bhopal India
2018. All rights reserved.
Online Contents Available at: http//www.bbrc.in/
DOI: 10.21786/bbrc/11.1/1
INTRODUCTION
Al-Diwaniyah province, (180 KM south of Baghdad) is
one of the southern provinces and its territory is part
of the plain sedimentary Iraqi, which is characterized
by the simple decline from north-west to the south and
south-east also show minor differences and other local
in the surface of the province because of several fac-
tors, most important process of wind sedimentation and
can be explained nature by dividing the province. The
rst part consists of the ood plain, which includes most
areas of the province and the area of the shallow and
semi-shallow depressions, which the second part repre-
sents, the third part which is located in the sand dunes
area. Such as the districts of Afak and AL-Badir, and the
fourth part, which is represented by the sandy area and
188 DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
covers the southwestern part of the province in the area
between the west of the Euphrates River and the Western
administrative boundaries of the province, (Al-Janabi &
Ghaleb, 1992).
There are about 2,900 species of snakes spread in all
countries except the North and South Poles, the Hawai-
ian Islands, Ireland and New Zealand. The anatomical
and physiological behavior of the scale diaphragms in
the body is the easiest way to distinguish between these
species, (Vitt & Caldwell, 2013 McAllister et al. (2015).
Some of these species are venomous and some other
nonvenomous. The poison is mainly used to kill prey or
defend itself. Snakes are not at all harmful and many
of them are highly bene cial to human beings as they
feed on rats and mice and their skin is of great value as
it enters in the illegal manufacture of bags and shoes. In
addition, the venom of some snakes is used in preparing
antidotes for poisoning, (Pasi, 1992; Caswell et al., 2014,
Yimming et al. (2016).
Reptiles, including snakes, are exposed to a variety of
pathogens, which may be bacterial, fungal, viral, para-
sitic agents. There are many studies have indicated that
snakes are the intermediary or de nitive hosts for many
of the internal parasites, such as round worms such as
Angusticaecum sp, Porocephalus crotali, capillaria sp. as
well as intestinal protozoa such as Eimeria sp., Isospora
sp., Caryospora sp., Tyzzeria sp, (Klingenberg, 2000 Parc
2008, Rataj et al., 2011).
Cryptosporidium sp. is an intermediate host of Toxo-
plasma sp. (Duszynski & Upton, 2009), as well as it is
a blood parasite similar to Plasmodium, Haemoproteus
mesnili and Haemoproteus balli (Telford, 2009; Jacob-
son, 2007). It is also affected by external parasites, most
notably ticks such as Amblyomma sp. and mites like
Ophionyssus natricis (Rataj et al., 2011; Pietzsch et al.,
2006 McAllister et al. (2015).
According to our literature review, despite of wide
distribution of these snakes in Iraq, there is not much
comprehensive and adequate published data about
intestinal parasites of these snakes. Therefore the cur-
rent study was conducted to prepare list of intestinal
parasites of these snakes in Iraq.
MATERIAL AND METHODS
EXAMINATION OF COLLECTED SNAKES AND
THEIR PARASITES
The dead snakes were kept in the refrigerator at 7° C and
dissected within seven days while living species were
anesthetized with ether after the removal of the fangs
(Fontenot & Font, 1996). Then process of snakes dissec-
tion was carried out according to the method of Jacob-
son, (1978), where the snakes were placed on a large
piece of cork designed for this purpose. Then they were
opened from abdominal side, starting from annual slit
towards the fore front. The digestive tract and its com-
ponents were then removed by sharp scissors in a sterile
Petri dish to look for intestinal worms. It was also exam-
ined near the yellow sac around the pancreas adjacent
to the stomach as well as the liver and lungs. In case of
isolation of intestinal worms, it was washed with water
and kept in containers of %70 ethyl alcohol, then added
drops of glycerin. For the purpose of clari cation and
con rmation, use of acetocarmine dye was carried out
to pigment tapeworms, trematoda, and acanthocephalus.
Nematodes were placed in lactophenol solution and then
observed on a clean glass slide using Canada’s balsam
(Chaiyabutr & Chanhome, 2002).
For the study of intestinal protozoa a sample of the
stool was examined in direct smears with the use of some
illustrative pigments such as iodine and Zell-Nelson. All
intestinal parasites were examined under low and high
magni cations (10x,40x) and necessary measurements
were taken using ocular and stage micrometer. Identi-
cation of parasites was carried out using characters
described by Rataj et al., (2011).
FIGURE 1. Some species of snakes.
STATISTICAL ANALYSIS
The results were analysed by Completely Randomized
Design (CRD) which was adopted as a one-way and two-
way laboratory experimental design, as well as a com-
parison of the averages using a Least Signi cant Differ-
ence (LSD) under probability level of P ≤ 0.05
RESULTS
Of the 130 snakes samples examined,83 snakes, 63.84%
were found to be infected with different species of par-
asites (Table 1) and ve species of intestinal parasites
were recorded which included two species of protozoans
one species of cestoda and two species of nematode. The
results show that the distribution of intestinal parasites
in digestive tract of snakes, tapeworms was found only in
the large and small intestine being 80 and 50 % respec-
BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ 189
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
tively, while nematodes, Kalicephalus sp. were found in
three different places of the gastrointestinal tract, stom-
ach, small and large intestine being 31.82, 52.27 and
20.45% respectively. Strongyloides sp, was found only
in the small intestine at a rate of 100%. Isospora sp.
was recorded in stomach, small and large intestine being
42.86, 85.71 and 9.52% respectively. Similarly, Crypto-
sporidium spp. was recorded only in the small and large
intestine being 28.57 and 75%, respectively.
The statistical analysis showed no signi cant differ-
ences in infection rates according to species parasites,
while signi cant differences in infection rates were
found according to location of infection, (Table 2). It is
clear from (Fig. 12) that the highest incidence of intesti-
nal parasites was in single infections with one species of
parasite with 65.62 % dominance , followed by binary
infections with 36.14 %, while triple infections (three or
more parasites) ranked 7.22 %. Signi cant differences
were found in the types infection at the probability level
(P ≤ 0.05).
1.
Isospora sp
.(Henyon,1923)
Species of intestinal protozoa were recorded in smears
prepared from all snakes except P. roger‘s and Rhyncho-
calamus melanocephalus. In the isolates from stomach,
small and large intestinal ,the immature cysts of Isos-
pora sp. were detected, being oval with one end was
having rounded boundary, and the other was thin and
had a wall consisting of two thin layers and was with
a micropyle at the high end, which was about 19-20
33 x 20 micrometers. The life cycle of this parasite was
of direct nature and the host was perhaps infected by
mature cysts along with food or water contamination,
(Fig.2)
Table 1. Number & percentage of snakes infected with internal parasites.
Species of snakes (n=130)Species of parasites
R.melanocephalus
(n=1)
D.mesopotamicus
(n=15)
N.tessellata
(n=19)
S.clifordi
(n=11)
E.jaculus
(28)
M.monspessulana
(n=13)
P.roger s
(n=1)
P.ventromacultus
(n=42)
S.I*N(%)S.I*N(%)S.I*N(%)S.I*N(%)S.I*N(%)S.I*N(%)S.I*N(%)S.I*N(%)
00(0)12(13.33)211(57.89)00(0)12(7.14)00(0)00(0)2.85(11.90)Oochoristica tandani
00(0)12(13.33)1.427(36.84)13(27.27)1.6621(75)11(7.69)00(0)1.2010(23.81)Kalicephalus sp.
0(0)000(0)00(0)00(0)12(7.14)00(0)00(0)11(2.38)Strongyloides sp.
00(0)3.303(20)42(10.53)1.754(36.36)102(7.14)32(15.38)00(0)3.308(19.05)Isospora sp.
00(0)2.504(26.67)27(36.84)1.205(45.45)23(10.7)1.254(30.77)00(0)2.405(11.90)Cryptosporidium spp.
To compare the severity infection between parasites species=1.26
To compare the severity infection between snakes species=1.26
To compare the infection rate between parasites species=14.40
To compare the infection rate between snakes species=N.S
LSD(P≤0.05)
F.calculated:7.03 F.table:2.32
F.calculated:3.32 F.table:2.32
F.calculated:4.12 F.table:2.32
F.calculated:2.15 F.table:2.23
*S.I: Severity of infection
FIGURE 2. Cysts of Isospora sp. (100x)
2.
Cryptosporidium spp.
(Tyzzer, 1907)
The cyst of Cryptosporidium spp isolated from small
and large intestinal of all types of snakes except the
two species P. roger’s and R. melanocephalus showed
cysts which were spherical or oval-shaped, containing
eight spores with double-walled being about 5.1 x 4.5
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
190 DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS
Table 2. Number &infection rate of intestinal parasites in digestive tract in snakes.
Site of infectionNumber of
parasites
Species of parasites
Large intestineSmall intestinestomach
%n%n%n
501080160020Oochoristica tandani
31.821452.272320.45944Kalicephalus sp.
00103003Strongyloides sp.
42.86985.71189.52221Isospora sp.
28.57875210028Cryptosporidium spp.
To compare the infection rate according to species of parasites =N.S
To compare the infection rate according to site of infection =33.98
LSD(P≤0.05)
F.calculated:0.31 F.table:3.83 (to species parasites)
F.calculated:20.91 F.table:4.45 (to site infection)
micrometers and were characterized by having a direct
life cycle, (Fig. 3).
FIGURE 3. Cysts of Cryptosporidium spp.(100x)
3.
Oochoristica tandani
(Luhe, 1898)
This species of cestoda was found in both the large and
small intestines of P. ventromaculatus, E.jaculus, N.
tessellata and D. mesopotamicus which were tall and
thin worms with a length of about 90 mm and a width
of 0.77 mm. The head was equipped with four suckers
without spines followed by the neck area consisting of
40 immature proglottids followed by mature proglot-
tids, after about 10 pieces of the gravid proglottids, were
18 proglottids and all types of proglottids had length
greater than the width by about 4 times. The ovary con-
sisted of 5-4 lobes while number of testes had 37-45
test, both ventral longitudinal excretory ducts and nar-
row dorsal ducts showed small anastomosing branches
( g. 4, 5 & 6).
4.
Kalicephalus sp.
(Rudolphi, 1819)
This nematode worm had the highest percentage of
isolated intestinal worms, it was found in all species
of snakes except Platyceps rogers and Rhynchocala-
mus melanocephalus, and was found in both the large
FIGURE 4. Oochoristica tandani
FIGURE 5. Immature
proglottids
FIGURE 6. Mature proglottids
Scolex(100x)
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ 191
and small intestines as well as stomach, this nematoda
female had short, strong worms with a white color that
did not exceed 6 mm in length. The mouth was equipped
with four pyramid cuticular structures, it had esopha-
gus funnel shaped containing three small teeth and with
strong kaitinine lining, excretory pore was near to pos-
terior end, uterine branches were opposed or parallel
and were full of eggs with posterior end being conical,
( g. 7,8 & 9).
mm and white color and was covered with a soft layer
of cuticle. The oral cavity was small and followed by a
cylindrical shaped esophagus. The uterus had a thin wall
and was lled with eggs that appeared in the shape of
two tubes full of eggs (Fig.10,11 & 12).
FIGURE 7. Anterior end of Kali-
cephalus sp. female(100x)
FIGURE 8. Eggs of Kali-
cephalus sp. female(100x)
FIGURE 9. Posterior end of Kali-
cephalus sp. female(100x)
5.
Strongyloides sp.
(Grassi, 1879)
This nematode worm was found in the small intestines
of only two species of snakes: P. ventromacu- latus and
Eryx jaculus. The isolated female length was about 3.5
FIGURE 10. Anterior
end of Strongyloides sp.
female(100x)
FIGURE 11. Eggs of two
tubes (100x)
FIGURE 12. Posterior end of
Strongyloides sp. female(100x)
DISCUSSION
The results of the present study indicate that the total
infection rates of snakes were 63.84 %, which is lower
than that recorded by Chaiyabutr & Chanhome (2002)
in Thaland, Santora et al., (2013) in southern Italy and
Nasiri et al., (2014) being 75,95 and 73.56 % respec-
tively, and is higher than that recorded by Dusen et
al., (2010) in the north-west of Turkey and Rataj et al.,
(2011) in Scandinavia, which amounted to 27.27 and 47
% respectively. The different recorded ratios (above and
below) may be due to the variation of the number of
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
192 DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS
specimens examined, their species, sizes and sources of
food, as well as their location and the nature of their
livelihood, as well as some of the research was con-
ducted on the captive snake and some on wild species,
some of them on aquatic species.
In this study, there were ve species of intestinal par-
asites, the intestinal protozoa was the most widespread,
the reason for this was that most of the snakes were
subjected to pressure conditions of cages. In the case
of infection a of single snake it was put to the cysts of
spores with waste, which led to the pollution of cages
and water sources, as well as the fact that these parasites
had a direct life cycle. A high incidence of nematode
infection was observed compared to tapeworms, this
is consistent with Chaiyabutr & Chanhome’s study of
(2002) in Thailand, Santos et al., (2006) in Iberian Penin-
sula and Dusen et al., (2010) in the north-west of Turkey
and Ribas et al., (2010) in the north-east of Spain and of
Fontenot & Font’s (1996) in south-eastern Louisiana in
aquatic vipers, which pointed to a higher incidence of
tapeworms compared to nematodes.
This is due to the availability of intermediate hosts
which play a major role in the incidence of tapeworms.
Also observed was that the number of intestinal para-
sites located in the intestines is much higher than the
numbers present in the stomach and large intestine may
be due to the fact that the intestinal environment suit-
able for the parasites because of the integration of the
physiological characteristics of the food in addition to
its presence in a soluble and ready for absorption and
this is consistent with Santora et al., (2013) and Dusen
(2010).
The results of the current study showed that the inci-
dence of one species of parasite was the highest percent-
age compared with binary and triple infections. The rea-
son for this may be due to the living and environmental
competition between the parasites of the host.
The results of the study indicate that snakes of
medium size are most susceptible to parasitic infections,
reaching the highest level within the group which ranged
between 50 - 100 cm. This result is consistent with the
reports of Santora et al., (2013) and Capizzi et al., (2008).
This may be due to the fact that medium-sized snakes
are more active than small and large species and there-
fore have a wide food diversity, Small snakes are always
inactive and poorly nourished. While few infection in
large snakes due to having evolution immune system
(Santora et al., 2013; Capizzi et al., 2008; Poulin, 2007).
Parasitic infection occurs under the in uence of a bio-
logical agents which include host, parasite and carrier,
such as host species, genus and feeding nature (Osgood
& Schall, 2004).
This study indicated only one species of tapeworm
was found, which was found in the small and large
intestine. It was recorded in only four species of snakes:
Platyceps ventromaculatus, Eryx jaculus, Natrix tessel-
lata and D. mesopotamicus, being 11.9, 7.14, 57.89 and
%13.3, respectively. It is worth mentioning this species is
not only in snakes, as it was previously recorded in Iraq
by Al-Hashimi (2006) in Al-Anbar in his study of Iraqi
reptiles. It has been isolated by King & Babero (1974)
in Australian Kangaroo Dipodomys ssp. in Nevada by
Bursey et al., (1996) in the Australian lizards called
Moloch horridus and Rataj et al., (2011) in Scandinavia
from lizards and Bursey et al. (1996) pointed to the pres-
ence of more than 74 species, which is concerned with
the infection of different species of reptiles, Their life
cycle is indirect and requires beetles and some insects as
an intermediate host to complete their life cycle. While
Kalicephalus sp. was one of the most common nema-
todes recorded during the current study, it was found
in the stomach, small and large intestine and has been
isolated from most species of snakes and the highest per-
centage was in the Eryx jaculus, which was 75% and the
lowest in Malpolon monspesslana, which amounted to
7.69%, while Strongyloides sp. was found only in two
species of snakes, Platyceps ventromaculatus and Eryx
jaculus with a percentage of 2.38 and 7.14 respectively.
This species was universally recorded in snakes by Fon-
tenot & Font (1996) in South-East Louisiana in group of
aquatic snakes at a rate of 4 % and Rataj et al., (2011) in
Scandinavia snakes and turtles at a rate 3.7 %.
Protozoa included two species such as Isospora sp.
and Cryptosporidium spp Isospora spp which were
recorded in most species of snakes. The highest per-
centage was the S. clifordi, which was 36.36 % and the
infection was obtained by swallowing the cysts contain-
ing spores with contaminated water and food, which
is globally registered in snakes by Asmundsson et al.,
(2001) in Ecuador and Chaiyabutr & Chanhome (2002)
in Thailand and McAllister et al. (2015) in Oklahoma.
FIGURE 13. Types of infection & percentage of infected
snakes with intestinal parasites.
Hadi M. Hamaza AL-Mayali and Sadiya Aziz Anah
BIOSCIENCE BIOTECHNOLOGY RESEARCH COMMUNICATIONS DESCRIPTION OF INTESTINAL PARASITES FOUND IN SOME SNAKES OF AL-DIWANIYAH, IRAQ 193
Cryptosporidium spp. was recorded in six species of
snakes and highest percentage was registered in S. cli-
fordi, which was % 45.45. This nding agrees with that
of Brower & Cran eld (2001) who have shown similar
data in snakes of Animal Farm Zoo in Baltimore, Mary-
land USA. Our present study of the histological changes
caused by the parasite considerably agrees with that of
Kuroki et al., (2008) in Japan and Rataj et al., (2011)
in Scandinavia and Yimming et al., (2016) in Thailand.
This protozoa was recorded in 57 different species of
reptiles, including 40 species of snakes, 15 species of
lizards, and 2 turtles (Xiao et al.,2004). The incidence
of species without apparent disease in mammals and
birds (Ramirez et al., 2004) with the exception of C.
serpentis, which leads to clear pathological symptoms
such as abdominal bloating, low weight and lethargy
of infected animals,This species is concerned with rep-
tiles only (Fayer et al., 1997). The infection with Crypto-
sporidium is obtained by swallowing cysts containing
spores with water and food or through contaminated
soils, (Rosenthal,1997).
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