Coprological study of gastrointestinal parasites of captive animals at Rangpur Recreational Garden and Zoo in Bangladesh
Most. Monjila Khatun 1, NurjahanBegum 2, Md. Abdullah Al Mamun 3,
Md. Motahar Hussain Mondal 4 & Md. Shakif-Ul-Azam5
1,2,3,4 Department of Parasitology, Faculty of
Veterinary Science, Bangladesh Agricultural University, Mymensingh-2202,
Bangladesh
5 Scientific Officer,
Dhaka Zoo, Mirpur, Dhaka, Bangladesh
1 vet_kmonjila@yahoo.com, 2 nurjahanpara@yahoo.com,3 mamun.dvm@gmail.com (corresponding author), 4 mmhmondal@yahoo.com,5 shakif78@gmail.com
doi: http://dx.doi.org/10.11609/JoTT.o3093.6142-7
Editor: UlrikeStreicher, Wildlife Veterinarian / Wildlife
Management Consultant, Danang, Vietnam. Date
of publication: 26 July 2014 (online & print)
Manuscript details: Ms #
o3093 | Received 30 July 2013 | Final received 06 May 2014 | Finally accepted
08 July 2014
Citation: Khatun, M.M., N. Begum, M.A.A. Mamun,
M.M.H. Mondal & M. Shakif-Ul-Azam (2014). Coprological study of
gastrointestinal parasites of captive animals at RangpurRecreational Garden and Zoo in Bangladesh. Journal
of Threatened Taxa 6(8): 6142–6147; http://dx.doi.org/10.11609/JoTT.o3093.6142-7
Copyright: © Khatunet al. 2014. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Funding: The study was funded jointly by the first author and
the Department of Parasitology, Bangladesh Agricultural University,
Mymensingh, Bangladesh.
Competing Interest: The
authors declare no competing interests.
Acknowledgements: The authors are
very grateful to the Deputy Curator of RangpurRecreational Garden and Zoo for giving permission to collect fecal samples from the zoo. Sincere
gratitude also to the animal workers for their cordial support and technical
assistance during the sample collection. Special
thanks to the Head, Department of Parasitology, Bangladesh Agricultural
University, Mymensingh 2202, Bangladesh for his kind
assent to use the laboratory.
For figures, images, tables -- click here
Zoological gardens display wild animals
for aesthetic, recreational, educational and conservation purposes (Varadharajan & Pythal1999). One of their goals is to
preserve rare and endangered species and in many parts of the world, parks and
zoological gardens play an important role in species conservation (Parsani et al. 2001). In their natural habitat, wild
animals have large areas available to them. Their exposure to parasitic infections
is, therefore, fairly low and they have consequently a low genetic resistance
against parasitic infections. When
groups of these wild animals are kept in confined spaces in zoological gardens,
the problem of parasitic infections can aggravate and pose a serious threat to
the animals, occasionally causing sudden local fatalities (Muoriaet al. 2005).
The occurrence of parasites in animals
housed in zoos varies according to the type of husbandry, parasite prophylaxis
and type of parasitic treatment. Usually, captive animals in the zoo do not show alarming signs of
parasitism if deworming is carried out regularly (Parsaniet al. 2001). Zoological gardens
however are often located near city centers, where
space is limited and many captive animal species are housed in close proximity
to each other. Because of these space limitations, animals in these facilities
succumb more frequently to parasitic infections, which can pose a serious
health threat (Hoberg et al. 2008). In addition in captivity animals are
often under considerable stress, which further diminishes their resistance to
parasitic infections.
In Bangladesh, a few zoological gardens,
safari parks and eco parks have been established which act as an important
source of recreation for people of all ages. Until this date only few detailed and
comprehensive studies have been conducted on the prevalence of the
gastrointestinal parasites in animals housed in these facilities. Therefore, this study attempts to
determine the occurrence and prevalence of gastrointestinal parasites in zoo
animals at Rangpur Recreational Garden and Zoo in
Bangladesh.
Study
period, site and animals: This study was conducted during April and September 2011 at Rangpur Recreational Garden and Zoo whichis located at Rangpur, in northern Bangladesh. It is the smaller one of two government
zoos and was established in 1991, comprises an area of 20.7 acres and houses a
total number of over 200 animals including mammals, reptiles and birds. The study included the carnivores,
nonhuman primates and herbivores housed at the zoo. A total of 45 samples were
collected. The samples were
collected once from each animal listed in Table 1.
Sampling
and parasitological examination: With the assistance of the animal caretakers individual fresh fecal samples were collected. Because of the small number of animals,
it was possible to associate each sample with a known individual. In the case of the tigers and lions, the
individual animal was kept separately overnight and with the help of animal
caretaker the sample was collected the next morning. For spotted deer, individual samples
were collected immediately after defecation when the deer were supplied with
feed. Attention was paid when a
deer defecated, then its sex was identified and the fresh fecalsample was collected from the floor. Sample collection from hippopotamus, sambar, water buck and hyena was easy due to presence of only one
animal in each cage. In python, the
samples were collected separately from the animals bedding. It was easy because there were only two
pythons in a large cage that were far from each other. In the case of the
nonhuman primates (Rhesus Macaque and Olive Baboon) the individual sample was
collected by keeping the animal separate the previous day with the help of
caretaker.
The fecal sample
was placed in a polythene bag containing 10% formalin and the sample was marked
according to species and sex, and finally examined in the laboratory. The ova, cysts, oocystand larvae of different parasites were identified according to the morphology
and quantitative estimation was done by employing Stoll’s ova
counting technique (Soulsby 1982).
Results: A total of 45 fecalsamples of different animals were examined for the presence of gastrointestinal
parasites. The overall prevalence
of parasitic infection was 60% (27/45) with 35.6% (16/45) of helminth infections and 24% (11/45) of protozoicinfections. Results indicated that helminths infections were more common than protozoic infections in carnivores and herbivores, whereas
in primates protozoicinfection was more common than helminth infection
(Table 2).
At least one intestinal parasite was
identified in the fecal sample of each animal except
in the bears, pythons, the water buck and olive
baboons. Mixed infection was
observed in three species, including Rhesus Monkey (Trichuris sp. + Balantidium coli),deer (Strongyloides sp. + Coccidia) and lion (Toxascaris leonina + Spirometrasp.) (Table 4). 72.7% (8/11) of the carnivores were found positive for gastrointestinal
parasites of which 9.1% (1/11) were protozoa, whereas 63.6% (7/11) were helminths (Table 2). Parasites identified in carnivores comprised Toxascaris leonina, Spirometra sp., Toxocara cati and Balantidium coli. Lions were
found infected with Toxascaris leonina (100%, 4/4) and Spirometrasp. (25%, 1/4). Tigers were found
infected with Toxocara cati(100%, 2/2) (Table 3).
Of the herbivores 50% (13/26) of the
animals were positive for gastrointestinal parasites of which 19.2% (5/26) were
protozoa and 30.8% (8/26) were helminths (Table
2). Parasites identified in
herbivores were Fasciola sp., Moniezia benedeni, Strongyloides sp., Dictyocaulus sp., stomach worm, Coccidia and Balantidium coli.
In the primates, 75% (6/8) of the animals
were positive for gastrointestinal parasites of which 62.5% (5/8) were protozoa
and 12.5% (1/8) were helminths (Table 2). The species identified were Balantidium coli and Trichuris sp. and were found in Rhesus Macaque.
In this study, the sex related prevalence
could only been assessed in deer as only in this species a suitable sample size
was available. Here the prevalence
of gastrointestinal parasites was higher in females (50%) than in males (33.3%)(Table 5).
As not enough samples of each species were
available mean egg per gram of feces (EPG), ova per
gram of feces (OPG), cyst per gram of feces (CPG) and larvae per gram of feces(LPG) were not calculated. So the
results presented in Table 6 simply show the lowest and the highest numbers
found in any sample. The highest
infection rate was found for Balantidiumcoli with 1400 CPG in Rhesus monkey, followed by a rate of 700 CPG in
hippopotamus, and a rate of 300 CPG in hyena and sambardeer.
Discussion: It has to be pointed out that the number
of animals in the study was very low and the results, though they are
interesting, are statistically irrelevant and rather anecdotical.
60% of the animals at Rangpur Recreational Garden and
Zoo were found positive for gastrointestinal parasites. Other authors reported similar (Parsani et al. 2001), higher (Oparaet al. 2010, Corden et al. 2008) or lower prevalences (Chakraborty &
Islam 1996; Lim et al. 2008), but prevalence always ranged between 40.4 and
76.6%.
In all animals, except primates, the
prevalence of helminth infections was higher than the
prevalence of protozoic infections, an observation
also confirmed in other studies (Varadharajan & Kandasamy 2000; Parsani et al. 2001). The high prevalence of helminths encountered in the survey can be explained by thefavorable climatic conditions, which support
prolonged survival of infectious nematode larvae. The finding of mixed infections might be
due to presence of animals of all age groups in the same cages, the feeding
management and improper disposal of feces.
In the present study 72.7% of the
carnivores were found positive for gastrointestinal parasites. Lower (50%) and higher
(97.3% and 89.3%) infection rates were found by other authors(Muller-Graf 1995; Lim et al. 2008). The main parasite found in carnivores weretapeworm Spirometra sp. It has been stated a long time ago that
tapeworms were common among zoo animals (Chauhan et
al. 1973). Spirometrasp. however, though the most common parasite in wild lions (Barutzkiet al. 1985; Ghoshal et al. 1988), has not been
reported in zoo lions until 1995 (Muller-Graf 1995). Occurrence of Spirometra depends on feeding management and availability of intermediate hosts in the
corresponding areas. Two
intermediate hosts are required to complete the life cycle of Spirometra sp. The first intermediate hosts are
crustaceans and snakes; birds, mammals etc. are the second intermediate host (Soulsby 1982). So, the presence of Spirometrasp. in the lion of Rangpur Recreational Garden and
Zoo might be due to ingestion of contaminated beef.
In this study, no gastrointestinal
parasite was recorded in bear. This
might be due to the feeding management, deworming and sample size. Bears are provided with a mixture of
properly boiled ingredients. Heat
destroys most of the ova or cyst of gastrointestinal parasites and might be the
reason for absence of gastrointestinal parasites in bear in our study.
In this study 43.5% of the spotted deer
were positive for gastrointestinal parasites, which is lower than the
prevalence recorded by Kanungo et al. 2010
(75%). 13% of the spotted deer were
found positive for Fasciola sp. This is
lower than the rate of Fasciola sp. in deer
recorded by Kanungo et al. (2010) at Dhaka Zoo (20%)
and at Dulahazara Safari Park (19.1%). This difference might be due to location
of animal cages, availability of intermediate hosts near the cages and the
source of feeds. The occurrence of Fasciola sp. infection in Dhaka and Dulahazara was suspected to be connectedwith mud snails that live on the edges of the drains and act as intermediate
hosts. Most of the deer cages at
Dhaka zoo are located near the lake of the zoo. Moreover, the grass and leaves supplied
to the deer are collected outside of the zoo and might be contaminated with metacercaria of trematodes (Kanungo et al. 2010). But at Rangpur Zoo the chance of contamination
is low as the deer enclosures are located far from the lake of the zoo and the
grass supplied to the deer is cultivated at the zoo.
In sambar only Balantidium coli was recorded, which was
different from other studies (Singh et al. 2009), which found a large number of
gastrointestinal parasites including strongyles, Strongyloides sp., Coccidia, Fasciola sp., Amphistomesand Trichuris sp. This difference might be due to the
number of samples examined and the housing and feeding management of the
zoo. Only one sambaris kept at Rangpur Recreational Garden and it has
been reared in captivity and the chance for contamination from another
individual and the environment was low. Singh’s findings (2009) are made in a
group of sambar in a free range area at Mechendra Choudhry Park, where
the animals take to water readily and swim with the body submerged, which might
expose them to infectiuos stages of parasites leading
to higher parasitic prevalence in the species. Moreover, the moderate temperature range
and the higher humidity at the park lead to the formation of a permanent mud
area favorable to the survival of eggs and
free-living stages of parasites (Singh et al. 2009).
Among the primates 75% animals were
positive for gastrointestinal parasite infection. This result is much lower than the
prevalence of 88.7% reported by Mutani et al. (2003),
but higher than prevalences recorded by Lim et al.
(2008) (54.5%) and Stuart et al. (1990) (48%). In accordance with other studies (Gomez
et al. 1996; Leveck et al. 2007; Lim et al. 2008) we
found a higher prevalence of protozoa (62.5%) than of helminths(12.5%) in this animal group. The
occurrence of these parasites can be explained by the simplicity of their life
cycle, the low infective dose, the short prepatentperiod and ability to survive in the environment. Balantidiumcoli, which was commonly found in our study, has a wide host range and
possesses a simple direct life cycle and its occurrence in
primates has been previously confirmed by Lim et al. (2008) and Gomez et al.(2000). Trichuris sp., which was found
in the primates in this study, has been found by many authors (Lim et al. 2008;
Singh et al. 2009) and is assumed to be the most common helminth in primates (Corden et
al. 2008).
The present study did not find
gastrointestinal parasites in Olive Baboon. Other studies however found baboons
usually infected with various helminths (Nasher 1988; Murray et al. 2000; Mutaniet al. 2003). The fact that we did
not find any parasites might be the result of the number of samples, the
animals’ immune status and health condition, the deworming regime, hygienic
management and low density of the animals in the enclosure.
In our study, sex related prevalence was
only assessed in deer, as only here a suitable sample size was available. Here the prevalence of gastrointestinal
parasites was higher in females (50%) than in males (33.3%). Although, the cause of the higher
parasitic infection rate in females is not known, it can be hypothesized that
pregnancy, lack of feed supplements during gestation and lactation, hormonal
influences and stress factors during gestation, parturition and lactation may
lead to an increased susceptibility for parasites. Llyod (1983)
reported higher level of prolactin and progesterone hormones make an individual
more susceptible to any infection.
Conclusion: This is the first documentation of
gastrointestinal parasites of captive animals at RangpurRecreational Garden and Zoo. The
high prevalence of these parasites emphasizes the importance of controlling
these parasites in order to safeguard the health of the housed animals and of
humans working with these animals. More studies of parasitic infections are essential to understand the
epidemiology of parasitism and also to better prevent parasitic infections.
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