Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 March 2021 | 13(3): 17889–17894
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.5682.13.3.17889-17894
#5682 | Received 05 January 2020 | Final
received 18 March 2021 | Finally accepted 19 March 2021
Parasitic infection in captive
wild mammals and birds in Bangabandhu Sheikh Mujib Safari Park, Cox’s Bazar,
Bangladesh
M. Najmul
Hossain 1, Anita Rani Dey 2, Nurjahan Begum 3
& Thahsin Farjana
4
1 Veterinary Surgeon, Central
Veterinary Hospital, 48-Kazi Alauddin Road, Dhaka
1000, Bangladesh.
2–4 Department of Parasitology,
Bangladesh Agricultural University, Mymensingh 2202, Bangladesh.
1 niazcvasubd@gmail.com, 2 anitadey@bau.edu.bd
(corresponding author), 3 nurjahanpara@yahoo.com, 4 tfarjanamunni@yahoo.com
Editor: Priya J.Gawande,
Nagpur Veterinary College, Nagpur, India. Date
of publication: 26 March 2021 (online & print)
Citation: Hossain, M.N., A.R. Dey, N. Begum & T. Farjana (2021). Parasitic infection in captive
wild mammals and birds in Bangabandhu Sheikh Mujib Safari Park, Cox’s Bazar,
Bangladesh. Journal of Threatened Taxa 13(3): 17889–17894. https://doi.org/10.11609/jott.5682.13.3.1788-17894
Copyright: © Hossain et al. 2021. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: National Science
and Technology (NST) of Bangladesh.
Competing interests: The authors
declare no competing interests.
Author details: Md. Najmul Hossain is a field veterinarian and engaged in disease
diagnosis and treatment. Anita Rani Dey is
an Associate Professor of Parasitology, Bangladesh Agricultural University,
Mymensingh-2202, Bangladesh and works on epidemiology, anthelmintic resistance
and molecular biology of parasites of livestock and poultry. Nurjahan Begum
is a Professor of Parasitology, Bangladesh Agricultural University,
Mymensingh-2202, Bangladesh and her interest is to work on molecular biology of
blood protozoa. Thahsin Farjana is a Professor of
Parasitology, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh
and her interest on biology of arthropods vectors.
Author contribution: ARD and NB conceptualized and
designed the study. MNH collected
samples. MNH and ARD identified
parasites and analyzed the data. MNH, TF and ARD drafted the paper and made
final revisions. NB and TF made critical revision of the manuscript. All the authors read the final version of the
manuscript and approved it.
Acknowledgements: The authors acknowledge National
Science and Technology (NST) of Bangladesh for granting the research fund. Sincere thanks to the authority of
Bangabandhu Sheikh Mujib Safari Park for sample collection.
Abstract: We investigated the infection
rate of gastrointestinal (GI) parasite eggs and premature stages from different
wild animals and birds in Bangabandhu Sheikh Mujib Safari Park, Dulahazra, Cox’s Bazar.
A total of 56 fecal samples were collected
from 24 species during July to November 2012 using modified Stoll’s ova
dilution technique. Coprology analysis
revealed that the overall rate of parasitic infection was 78.6%, of which 51.8%
were helminths and 35.7% protozoa. The
identified parasites were Paramphistomum spp.
(7.1%), Fasciola spp. (5.4%), strongyles (26.8%), Ascaris spp. (3.6%), Strongyloides spp. (7.1%), Dictyocaulus
spp. (5.4%), Trichuris spp. (3.6%), Capillaria
spp. (5.4%), Heterakis spp. (3.6%), and Balantidium
coli (35.7%). Mixed infection
(21.4%) was observed in nine animals, including co-infection with Balantidium
coli and strongyles in Tiger Panthera
tigris, Sambar Deer Rusa
unicolor and Pig-tailed Macaque Macaca nemestrina, Strongyloides
spp., Trichuris spp. and larvae of Dictyocaulus
spp. in Capped Langur Trachypithecus pileatus, Balantidium coli and Capillaria spp. in Clouded Leopard Neofelis nebulosa, Fasciola spp. and Balantidium coli in Spotted
Deer Axis axis, Ascaris spp. and strongyles in African Elephant Loxodonta
africana, Strongyloides
spp. and Heterakis spp. in Peafowl Pavo cristatus and Heterakis spp. and strongyles
co-infection in Great Pied Hornbill Buceros
bicornis.
It is concluded that GI parasites were prevalent in this safari
park. Further epidemiological
investigation is necessary for controlling parasitic infection.
Keywords: Ascaris, Balantidium coli, Capillaria, Dictyocaulus,
Fasciola, GI parasites, Heterakis,
infections, Paramphistomum, strongyles, Strongyloides,
Trichuris.
INTRODUCTION
Conservation of wildlife in many parts of the world is
associated with zoological gardens (Parsani et al.
2001a). Zoo populations are unique and
important sources for studying wildlife and their habitats, and to preserve
endangered species through captive breeding and reintroduction programs
(Schulte-Hostedde & Mastromonaco
2015). Parasitic diseases constitute a
major problem for these animals while in captivity (Rao & Acharjyo 1984). In
nature, practically no animal is free from parasitic infection, but they often
develop resistance from low grade infections.
Captive animals are vulnerable to GI parasites, which often cause severe
illness or death. Common GI parasites of
captive birds and mammals include nematodes, trematodes, cestodes and
protozoa. It is possible to eliminate
these parasites by giving proper attention to feeding, water and maintenance of
hygiene, husbandry practices, disease prophylaxis and treatment in
captivity. Usually, captive animals do
not show alarming signs of parasitism if regular deworming practices are
carried out (Parsani et al. 2001a).
The study of wildlife while in captivity has
contributed greatly to our current biological knowledge. Zoos, wildlife breeding centers
and research institutions are playing a vital role in this respect. Investigations on endoparasitic
fauna are important for the study of their prevalence and geographical
distribution (Zasityte & Grikienciene
2002). In Bangladesh, very few
zoological gardens, safari parks and eco parks have been established which act
as an important source of recreation for people of all ages. Among them,
safari park is the wildlife park where visitors can observe freely roaming
animals from protected vehicles (Chipperfield 1975). There have been few comprehensive studies on
the prevalence of intestinal parasites in animals in zoological gardens of
Bangladesh (Raja et al. 2014). The
present study aimed to identify GI parasites and their present status in birds
and mammals of Bangabandhu Sheikh Mujib Safari Park.
MATERIALS AND METHODS
Study area
This study was conducted at Bangabandhu Sheikh Mujib
Safari Park, Dulahazra, Cox’s Bazar, Bangladesh. The samples were examined in the laboratory,
Department of Parasitology, Bangladesh Agricultural University, Mymensingh.
Study period
The study was conducted from July to November 2012.
Selection of animals
A total of 56 samples were collected from species
including: Tiger Panthera tigris (4), Lion Panthera
leo (4), Asiatic Black Bear Ursus
thibetanus (4), Clouded Leopard Neofelis nebulosa
(3), Black Fox Vulpes vulpes (1), Hog Deer Axis
porcinus (4), Sambar Rusa
unicolor (4), Spotted Deer Axis axis (4),
Hippopotamus Hippopotamus amphibious
(2), African Elephant Loxodonta africana (3), Wildebeest Connochaetes
taurinus (4), Gayal Bos
frontalis (2), Langur Semnopithecus sp.
(2), Capped Langur Trachypithecus pileatus (3), Monkey Macaca
fascicularis (2), Hoolock Gibbon Hoolock hoolock (2), Pig-tailed Macaque Macaca
nemestrina (1), Emu Dromaius
novaehollandiae (1), Peafowl Pavo
cristatus (2), Guinea Fowl Numida
meleagris (1), Great Pied Hornbill Buceros bicornis
(1), Indian Pond Heron Ardeola grayii (1), and Vulture Aegypius
monachus (1).
Collection and preservation of samples
Fecal samples were collected with the help of animal caretakers
in the early morning from the floor to prevent contamination. Each sample was placed in a polythene bag
containing 10% formalin. The opening
edge of the bag was tightly closed and samples were labeled
according to species with a marker.
Coprological examination
All samples were examined at the laboratory,
Department of Parasitology, Bangladesh Agricultural University,
Mymensingh. The samples were processed
for microscopic examination. The ova/
cysts/ larvae of different parasites were identified according to Stoll’s ova
dilution technique to determine eggs per gram (EPG) or cyst per gram (CPG) of feces as described by Soulsby
(1982).
Micrometry of ova and cyst
The sizes (length by width) in μm
of ova, cysts and larvae of identified parasites were measured (Cable 1965).
RESULTS
Overall infection rate of GI parasites in animals
The overall rate of parasitic infection was 78.6%
(44), where helminths and protozoan infection were 51.8% (29) and 35.7% (20),
respectively (Table 1). Identified
parasites included protozoa Balantidium coli (35.7%); nematodes strongyles (26.8%), Ascaris spp. (3.6%), Dictyocaulus spp. (5.4%), Strongyloides
spp. (7.1%), Trichuris sp. (3.6%), Capillaria
spp. (5.4%), and Heterakis spp.
(3.6%); and trematode Fasciola spp. (5.4%) and
Paramphistomum spp. (7.1%) (Table
2). Results indicated that helminth
infection were more common than protozoan infection.
Infection rate of mixed infection in animals
Mixed infection (21.4%) was observed in nine animals:
Tiger, Sambar Deer and Pig-tailed Macaque (Balantidium coli and strongyles), Capped Langur (Strongyloides
spp., Trichuris spp. and larvae of Dictyocaulus
spp.; Strongyloides spp.,
Trichuris spp. and larvae of Dictyocaulus
spp.), Clouded Leopard (Balantidium coli and Capillaria
spp.), Spotted Deer (Fasciola spp.
and Balantidium coli), Elephant (Ascaris spp. and larvae of strongyles), Peafowl (Strongyloides
spp. and Heterakis spp.),
Great Pied Hornbill (Heterakis spp. and
strongyles) (Table 3).
Infection rate of GI parasites in carnivores
Among carnivores, 68.8% (11/16) animals were positive
for GI parasites, of which 62.5% (10/16) were found positive for protozoa and
18.8% (3/16) samples were positive for helminthes. The detected parasites of carnivores included
strongyles (12.5%), Capillaria
spp. (6.3%) and Balantidium coli (62.5%). No parasite was
found in Black Fox.
Infection rate of GI parasite in herbivores
Among herbivores, 100% animals were positive for GI
parasites. Among them, 30.4% and 78.3%
samples were found positive for protozoa and helminthes,
respectively. The isolated parasites
were Fasciola spp. (13.0%), Paramphistomum spp. (17.4%), strongyles
(43.5%), Balantidium coli (30.4%), Ascaris spp. (8.7%), and Capillaria spp. (4.4%).
Infection rate of GI parasite in non-human primates
Among primates, 70.0% animals were positive for GI
parasites of which 30.0% and 50.0% samples were found positive for protozoa and
helminthes, respectively. The detected parasites were Strongyloides spp. (30.0%), Dictyocaulus spp. (30.0%) and Trichuris
spp. (20.0%), strongyles (20.0%), and
Balantidium coli (30.0%).
Infection rate of GI parasite in birds
Among birds, 42.6% samples were positive for GI
parasites. No samples were found
positive for protozoa. The identified
parasites were Strongyloides spp.
(14.3%), Heterakis spp. (28.6%), Capillaria spp. (14.3%) and strongyles
(14.3%).
Intensity of infection of GI parasites in different
animals
In the present study, intensity of different parasites
in different animals was also measured.
The mean EPG/ CPG were calculated.
The highest CPG (cyst per gram) was found in Pig-tailed Macaque for Balantidium
coli as 500. The highest EPG (egg
per gram) was found in Capped Langur for Strongyloides
spp. (1200).
Micrometry of egg/cyst of different GI parasites in
different animals
The sizes (length by width) in µm of egg/cyst of
different GI parasites were measured in the present study (Table 4).
DISCUSSION
The objective of zoological gardens is to protect
endangered animal species and to evaluate needs for protecting
biodiversity. It helps to gain an
accurate and updated knowledge of different diseases that affect wild and
exotic animals when in captivity (Mitchell et al. 2009). In case of parasitic infection, animal
keepers and visitors play an important role of mechanical vector of parasites
and improper feeding systems can enhance the parasitic infection (Nasiri & Jameie 2019).
Overall 78.6% animals were found to be infected with
GI parasites, which was close to the previous finding of Raja et al. (2014) at
Dhaka Zoo in Bangladesh (78.7%) and slightly higher than the earlier reports of
Opara et al. (2010) and Corden et al. (2008) in
Nigeria (76.6%) and Spain (72.5%), respectively. The variation may be due to climatic
condition, husbandry practice and feeding management of the study area. Environmental contamination could be through
contaminated water or fodder, and even zoo workers have also been reported to
play a role in transmission by acting as vectors and transmitting parasites
through their shoes, clothes, hands, food, or with working tools (Adetunji 2014; Otegbade & Morenikeji 2014).
The infection rate of helminths infection (51.8%) was
found higher than protozoan infection (35.7%).
This is similar with the report of Parsani et
al. (2001a) who revealed that 57.1% animals were positive for helminths
infection and 18.8% for protozoa in Rajkot Municipal Corporation Zoo. The present study also confirms the report of
Varadharajan & Kandasamy (2000) who recorded that
58.0% animals were positive for helminths infections and 6.0% were positive for
protozoan infections. In this study,
nematode and protozoan infection were commonly found due to its direct life
cycle involving no intermediate host and transmitted by oro-fecal
route through contaminated feed, water, and soil and have the potential to
accumulate in a captive environment. A
few trematode infections and no cestode infection was recorded because of their
indirect life cycle (Parsani et al.
2001b). In this park, animals and birds
are reared in protective enclosure giving less chance of accessibility to the
intermediate hosts of trematodes and cestodes.
In the present study, mixed infection observed in
different animals and birds. The mixed
infection in deer was recorded by Kanungo et al. (2010) in majority of the deer. Mutani et al.
(2003) reported that 58.5% monkeys were infected with at least three parasite
species and only 34.0% with one and two parasite species. This suggests that there is a fairly high
rate of transmission of the parasites observed between individuals either
because of the monkeys’ gregarious nature or because of suitable environmental
conditions (Mutani et al. 2003). The finding of mixed infection in this study might
be due to presence of all aged animals in the same cages, feeding management
and improper disposal of feces.
In this study, it is indicated that 68.8% carnivores
were positive for GI infection. This
finding is lower than the report of Muller-Graf (1995) and Lim et al. (2008)
who reported that the prevalence was 97.3% and 89.3%, respectively. The differences may be due the subspecies of
tigers in this study which are different from the previous. Also the geographical factors and
environmental factors are responsible for this variation.
In this study, 100% herbivores were positive for GI
parasites. This finding is absolutely
higher than the all previous findings. Wahed (2004) reported that 44.4% herbivores were positive
with GI parasites. The high prevalence
of Fasciola sp. (13.5%) and Strongyloides spp. (11.5%) in deer was
recorded by Mandalet al. (2002). The infection with Fasciola
sp. in deer was also observed by Maia (2001), Vengušt
(2003), Chroust & Chroustova
(2004), and Novobilsky et al. (2007). Comparatively, however, higher prevalence
rate of Fasciola spp. in deer was recorded by
Kanungo et al. (2010) as 20% at Dhaka Zoo and 19.1% at Dulahazara Safari Park.
This difference might be due to location of animal cages, availability
of intermediate hosts near the cages, and the source of feeds. The probable cause of Fasciola
spp. infection was strongly connected with mud snails that live on the edges of
drains and act as intermediate host (Vengust
2003). Another important factor was the
green grass and leaves supplied to deer from outside of the zoo, which may be
contaminated with metacercaria (Kanungo et al. 2010). At Bangabandhu Sheikh Mujib Safari Park, the
chance of contamination is also higher as the cage is located at marshy land
and the grass supplied to the deer is also taken from the outside.
Among primates, 70% of animals were infected with GI
parasites. This result is much lower
than that of Mutani et al. (2003) who revealed the
overall infection rate was 88.7%. On the
other hand, lower prevalence rate in primate was recorded by Lim et al.
(2008) and Stuart et al. (1990) as 54.5% and 48%, respectively. The present study also confirmed that among
the infected primate, there was a lower occurrence of protozoa (20%) than
helminth (40%) which is against the earlier report of Lim et al. (2008) who
recorded as 35.4% protozoa and 19.1% helminths. Balantidium coli were the most
prevalent intestinal parasite detected in primates. This finding is an agreement with the earlier
report of Levecke et al. (2007). Actually, Balantidium coli are common
protozoa of animals having a wide host range and possess a simple direct life
cycle. The appearance of these parasites
can be explained by the simplicity of their life cycle, the low infective dose,
the short pre-patent period and ability to survive in the environment.
CONCLUSIONS
Though there are some coprology studies of GI
parasites that have been done in wild animals in different zoos in Bangladesh,
this is the first investigation on GI parasites in animals in Bangabandhu
Sheikh Mujib Safari Park. Routine
monitoring of the presence of parasites in animals and birds are imperative in
assisting good management and implementation of preventive and control measures
against the spread of infectious parasitic diseases among animals within the
park or to humans.
Table
1. Infection rate of GI parasites in
different animals at Bangabandhu Sheikh Mujib Safari Park.
|
Type
of animal |
No.
of sample examined |
Protozoa infected
(%) |
Helminth infected
(%) |
Mixed
infected (%) |
Total infected*
(%) |
|
Carnivores |
16 |
10 (62.5) |
3 (18.8) |
2 (12.5) |
11(68.8) |
|
Herbivores |
23 |
7 (30.4) |
18 (78.3) |
4 (17.4) |
23 (100) |
|
Primates |
10 |
3 (30.0) |
5 (50.0) |
4 (40.0) |
7 (70.0) |
|
Birds |
7 |
0 (0.0) |
3 (42.9) |
2 (28.6) |
3 (42.9) |
|
Total |
56 |
20
(35.7) |
29
(51.8) |
12
(21.4) |
44
(78.6) |
*
Total no. of animals/ birds affected is less than the summation of individual
infection because same animal/ bird was infected with more than one type of
gastro-intestinal parasites
Table
2. Infection rate of GI parasites in different animals in Bangabandhu Sheikh
Mujib Safari Park.
|
Types
of parasites |
Name
of the parasites |
No.
of case |
Infection
rate (%) |
Intensity
of infection (EPG/CPG) |
|
Protozoa |
Balantidium
coli |
20 |
35.7 |
100–500 |
|
Trematode |
Paramphistomum spp. |
04 |
7.1 |
100–300 |
|
Fasciola spp. |
03 |
5.4 |
100–200 |
|
|
Nematode |
strongyles |
15 |
26.8 |
100–1200 |
|
Ascaris
spp. |
02 |
3.6 |
200–400 |
|
|
Strongyloides spp. |
04 |
7.1 |
100–1200 |
|
|
Dictyocaulus spp. |
03 |
5.5 |
600–700 |
|
|
Trichuris
spp. |
02 |
3.6 |
300 |
|
|
Capillaria spp. |
03 |
5.4 |
100–700 |
|
|
Heterakis spp. |
02 |
3.6 |
100–200 |
Table
3. Mixed infection in different animals in Bangabandhu Sheikh Mujib Safari
Park.
|
Name
of animals |
Name
of parasites |
No.
of case |
|
Tiger,
Sambar Deer and Pig-tailed Macaque |
Balantidium
coli and strongyles |
3 |
|
Capped
Langur |
Strongyloides spp.,
Trichuris spp. and larvae of Dictyocaulus
spp. |
2 |
|
Strongyloides spp.,
and larvae of Dictyocaulus spp. |
1 |
|
|
Clouded
Leopard |
Balantidium
coli and Capillaria
spp. |
1 |
|
Spotted
Deer |
Fasciola
spp. and Balantidium coli |
1 |
|
Elephant |
Ascaris
spp. and strongyles |
2 |
|
Peafowl |
Strongyloides
spp. and Heterakis spp. |
1 |
|
Great Pied
Hornbill |
Heterakis
spp. and strongyles |
1 |
Table
4. Micrometry of egg/ cyst of different parasites.
|
Name
of parasites |
Size
in µm |
|
Balantidium
coli |
50 x 70 |
|
Paramphistomum spp. |
160 x 90 |
|
Fasciola spp. |
87 x 43.5 |
|
strongyles |
72.5 x 43.5 |
|
Strongyloides spp.
|
58 x 29 |
|
Ascaris
spp. |
70 x 50 |
|
Capillaria spp. |
45 x 25 |
|
Heterakis spp. |
70 x 45 |
|
Trichuris
spp. |
79 x 36 |
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