Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 February 2020 | 12(3): 15370–15374
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5050.12.3.15370-15374
#5050 | Received 08 May 2019 | Final received
12 January 2020 | Finally accepted 23 January 2020
Prevalence and seasonal variation
of gastrointestinal parasites among captive Northern Pig-tailed Macaque Macaca leonina (Mammalia:
Primates: Cercopithecidae)
Phoebe Lalremruati
1 & G.S. Solanki 2
1,2 Department of Zoology, Mizoram
University, Aizawl, Mizoram 79004, India
1 phoebemamteii@gmail.com, 2 drghanshyam.solanki@gmail.com
(corresponding author)
Abstract: A study on the prevalence and
seasonal variations of gastrointestinal parasites of 12 captive Pig-tailed
Macaques Macaca leonina
housed at Aizawl Zoological Park, Mizoram, India, was conducted. Fresh stool samples were collected on a
monthly basis from the study animals was grouped for two seasons—summer
(April–June 2017) and monsoon (July–September 2017). Samples were stored in 10% formalin until
further processing. Three methods—direct
smear, faecal floatation, and faecal sedimentation were used. Two categories of parasites—protozoa and
nematodes were recorded. Balantidium
coli, a protozoa, Strongyle, Ascaris
lumbricoides, Trichiuris trichiura, and nematode parasites were recorded in
different stages. Out of 71 samples
analysed, 63 samples (88.73%) were positive with ova of gastrointestinal
parasites. The prevalence of Balantidium
coli was highest with 38.23% and 56.75%, followed by Strongyle
35.29% and 37.83% in summer and monsoon season, respectively. A variation on the prevalence of
gastrointestinal parasites was assessed using chi squared tests between monsoon
season and summer season. Variation was
found to be significant (χ 2=20.569, P˂0.05 and χ 2=10.857,
P˂0.05). The overall prevalence of
gastrointestinal parasites was higher during monsoon season (91.89%) than
summer season (85.29%).
Keywords: Aizawl Zoological Park, Ascaris
lumbricoides, Balantidium coli, India, Mizoram, Strongyle,
Trichiuris trichiura.
Editor: Rajeshkumar G. Jani, Anand Agricultural
University, Anand, India. Date of publication:
26 February 2020 (online & print)
Citation: Lalremruati, P. & G.S. Solanki (2020). Prevalence and seasonal variation
of gastrointestinal parasites among captive Northern Pig-tailed Macaque Macaca leonina
(Mammalia: Primates: Cercopithecidae). Journal of Threatened Taxa 12(3): 15370–15374. https://doi.org/10.11609/jott.5050.12.3.15370-15374
Copyright: © Lalremruati
& Solanki 2020. 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: Present study
was financially
supported by Department of Science &
Technology, GoI,
through Inspire
fellowship to first author.
Competing interests: The authors
declare no competing interests.
Acknowledgements: We thank the chief wildlife
warden, Department of Environment, Forests and Climate Change, for supporting
our research. We express our gratitude
to the Department of Zoology, Mizoram University for providing infrastructure
for the research. We also thank
Department of Science and Technology, New Delhi for providing INSPIRE
Fellowship to perform this research.
Non-human primates are susceptible to a
variety of diseases caused by infection with gastrointestinal parasites, both
in the wild and in captivity (Kuntz 1982).
Captive animals are supposed to have low prevalence of parasites as
anti-helminthic measures are practiced, however, infestation may be more due to
unhygienic conditions of cages. Crowding
of animals in cage, type of food and feeding practices are key factors in the
development of endoparasites in zoo animals (Malan et al. 1997; Mul et al. 2007; Sanchez et al. 2009). The majority of primate pathogens culminate
in chronic, sub-lethal infections (Goldberg et al. 2008) and parasite
infections with low immune system can trigger deterioration of health (Glaser
& Kiecolt-Glaser 2005; Coe 2011). Gastrointestinal parasite infected animals
exhibit symptoms like watery diarrhea, hemorrhage, and dysentery; the animals
may also develop renal infections that eventually lead to death (Levecke et al. 2007).
Parasite load may affect the fitness of the host, influencing the
survival and reproduction of the infected individuals (Boyce 1990; Hudson 1992;
van Vuren 1996; Hilser et
al. 2014). Knowledge about the profile
of gastrointestinal parasites and their intensity in primates may help the zoo
managers in developing better management plans to maintain the health of this
threatened species, and to ensure local survival. This study is an attempt on captive
Pig-tailed Macaque Macaca leonina to understand the parasitic profile of this
threatened primate species so that the zoo authorities may undertake
appropriate measures for prevention of parasite infection for this species and
also for primates in general.
Materials and Methods
Study site
The study was conducted at Aizawl Zoological
Park that covers an area of 65ha and is situated 14km away from Aizawl, the
state capital. The zoo maintains seven
species of primates, which includes four species of Vulnerable (VU) primates,
such as, Stump-tailed Macaque Macaca arctoides, Northern Pig-tailed Macaque Macaca leonina, Bengal
Slow Loris Nycticebus bengalensis,
and Capped Langur Trachypithecus pileatus, one Near Threatened (NT) species,
Assamese Macaque Macaca assamensis,
one Endangered (EN) primate, Western Hoolock Gibbon Hoolock hoolock, and one Least Concern (LC) primate,
Rhesus Macaque Macaca mulatta.
Subjects
The Northern Pig-tailed Macaques study group
included a total of 12 individuals, seven males and five females. They live in an enclosure of 850m2
area with two adjacent indoor rooms which can be opened or closed by sliding
doors. They are fed with fruits and
vegetables every day. Water is available
ad libitum. For the control of parasitic
infection, piperazine hydrazine liquid
61% is used by the zoo authorities. The
piperazine hydrazine liquid is mixed with water which is given to the monkeys
for drinking. This treatment is done
once in three months as recommended by the veterinarian.
Faecal sample collection
This study was conducted during April
2017–September 2017. Fresh stool samples
were collected each month from the study group and grouped into two seasons
summer (April–June 2017) and monsoon (July–September 2017) for meaningful
inference. Animals were in captive
conditions, hence monthly variations were not cognizable. Samples were examined macroscopically for the
presence of larval or adult of various parasites at different stages. Samples were collected in the morning hours
and were stored in 10% formalin at the sampling site for further processing as
per the procedures mentioned by Gillespie (2006). The collection tubes labeled with date and
time of collection were shaken vigorously to homogenize sample and storage
solution.
This study was undertaken with the permission
of the Chief Wildlife Warden, Department of Environment, Forest and Climate
Change under the permission number A.33011/4/2011-CWLW/Vol.II/388-89.
Sample processing
Three methods as recommended by Gillespie
(2006) were used for the identification of parasitic infection, i.e., direct
smear, faecal floatation, and faecal
sedimentation
Direct Smear: A thin smear of faecal material with normal saline was prepared on a slide
and observed under the microscope.
Faecal floatation: Approximately 1g of faeces was placed
into a 15ml centrifuge tube. The tube
was filled 2/3rd with de-ionised water and
homogenized with a wooden spatula, then centrifuged for 10min at 1,800rpm. The supernatant was decanted and the faeces was re-suspended in sodium nitrate (NaNO3)
solution. The tube was filled to the
meniscus with NaNO3 and a cover slip was placed on the mouth of the
tube and left for 10min. The cover slip
was removed and placed on a labelled slide.
Single slide for each individual sample was observed under a microscope
with 10X and 40X magnifications.
Presence of parasitic helminths and protozoa were observed and
photographed.
Faecal sedimentation: One gram of the preserved faecal
sample was homogenized in a centrifuge tube, topped up and thoroughly mixed
with 7–10 ml of 10% formal saline solution which also served as the
fixative. The resulting suspension was
strained into a clean centrifuge tube using a fine sieve to remove debris. Three milliliters of diethyl ether was then
added. The mixture was stoppered, mixed,
and centrifuged for 3min at 2,000rpm.
Debris and fat which formed a floating plug were dislodged using an
applicator stick and the supernatant was discarded. Using a Pasteur pipette, a drop each of the
remaining sediment was transferred to a clean glass microscope slide to make a
wet smear. Lugol’s
iodine solution (0.15%) was used to stain the slide. Sediments were further screened and analysed for identification of parasites and their
different stages.
Chi-square test was used to assess the
variation on the prevalence of each gastrointestinal parasite between winter
and summer seasons. Chi-square test was
carried out with SPSS version 18.0.
Results
The study animals were found to be infected
with two major groups of parasites: protozoa and nematodes. Four species of
parasites, namely, Balantidium coli (protozoa), and Strongyle,
Ascaris lumbricoides, and Trichiuris
trichiura (nematodes), were recorded. Photos of the ova of all species recorded are
given on Image 1. Out of the total 71
samples analyzed during the study, 63 samples (88.73%) were found to be
positive with ova of gastrointestinal parasites, however, seasonal variations
in the rate of infestation and different parasite species recorded also
varied. In summer, out of 34 faecal samples, 85.29% were infected with parasites. In this season, protozoan infestation was
found to be more (38.23%) and among nematodes, infection with Trichiuris trichiura (35.29%)
was highest, followed by Strongyle (26.47%),
and Ascaris lumbricoides (23.53%).
The overall prevalence of gastrointestinal parasites was higher during
monsoon season (91.89%) than summer season (85.29%). In the monsoon season, the rate of infection
with Balantidium coli was high (56.75%), followed by Strongyle
and Trichiuris trichiura
(37.83% and 37.83%, respectively) and Ascaris lumbricoides (27.02%). Seasonal comparison of prevalence (%) of all
four types of parasites is given in Figure 1.
The prevalence of Balantidium coli was also highest in both the
seasons, followed by the whipworm Trichiuris
trichiura.
On comparing the prevalence of infection
between the summer and monsoon seasons, it was found that infection with Balantidium
coli and Strongyle was significantly
higher during monsoon season than summer season (χ 2=20.569, P˂0.05
and χ 2=10.857, P˂0.05, respectively). There was, however, no significant variation
on the prevalence of Ascaris lumbricoides and Trichiuris
trichiura between the two seasons (χ 2=3.611,
P=0.164 and χ 2=3.782, P=0.151, respectively).
Discussions
Several parasitic infections have been
reported in non-human primates, both in captivity (Levecke
et al. 2007; Cordon et al. 2008; Nath et al. 2012; Barbosa et al. 2015; Margono et al. 2015) and in the wild (Legesse
& Erko 2004; Parr 2013; Kouassie
et al. 2015). The prevalence observed in
the present study (88.73%) was higher than that reported by Opara
et al. (2010) in captive animals, with prevalence rates of 62.5% and 61.5%,
respectively. Parasitic diseases are
reported to be common to zoo animals in tropical countries due to the climatic
factors that favor the development of parasites such as light, temperature, and
humidity (Opara et al. 2010). The two groups of parasites were also
reported in Belgium Zoo in prosimians, old world monkey, new world monkeys, and
some apes (Levecke et al. 2007). The protozoa and nematodes are highly
prevalent even in wild non-human primates (Kouassi et
al. 2015). The present study also
indicates high prevalence of protozoa (Balantidium coli) in both the
seasons as compared to nematodes (Figure 1), which is similar to the study
conducted by Levecke et al. (2007) in Belgium on
captive primates. Trematodes and
cestodes were not detected in this study.
This could be because these parasites require an intermediate host for
their transmission and that are less likely in the captive environment (Atanaskova et al. 2011).
Attendants of enclosures of these animals
could act as vehicles for cross transmission.
Also, the animals serve as potential reservoirs that could transmit
gastro-intestinal parasites to zoo keepers and possibly to visitors. This study further shows the need for an
anti-helminthic program such as early season treatments to prevent infection in
animals under captivity, regular passive surveillance for parasitic infections,
and effective treatment programs.
Moreover, it has been observed that confinement of wild animals in zoo
makes them more prone to different parasitic infections despite proper
attention for feeding, water, and maintenance of hygiene in captivity (Kashid et al. 2002).
The nematodes and some coccidian parasites have a direct life cycle,
without any intermediate host and are transmitted by feco-oral
route through contaminated feed, water, and soil and have the potential to
accumulate in a captive environment (Thawait et al.
2014). The environmental contamination
could be through contaminated water or fodder, and 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).
Based on this study, it is recommended that upgraded and more effective
regular preventive as well as prophylactic measures are needed to be included
in the management schedule of these animals at regular interval. Physical and chemical based hygiene are also
needed as a part of management programs for captive animals.
For figure
& image - - click here
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