Journal of Threatened Taxa | www.threatenedtaxa.org | 26
November 2020 | 12(15): 17093–17104
ISSN 0974-7907 (Online)
| ISSN 0974-7893 (Print)
doi: https://doi.org/10.11609/jott.5160.12.15.17093-17104
#5160 | Received 11 June
2019 | Final received 16 November 2020 | Finally accepted 18 November 2020
Gastrointestinal helminth and
protozoan infections of wild mammals in four major national parks in Sri Lanka
Chandima Sarani Sepalage 1 & Rupika Subashini Rajakaruna 2
1,2 Department of
Zoology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka.
1 sarani.sepalage91@gmail.com,
2 rupikar@pdn.ac.lk (corresponding author)
Editor: Bahar S. Baviskar,
Wild-CER, Nagpur, India. Date of publication: 26 November
2020 (online & print)
Citation: Sepalage, C.S. & R.S. Rajakaruna (2020). Gastrointestinal helminth and
protozoan infections of wild mammals in four major national parks in Sri Lanka.
Journal of Threatened Taxa 12(15): 17093–17104. https://doi.org/10.11609/jott.5160.12.15.17093-17104
Copyright: © Sepalage & Rajakaruna 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: We did not receive any external funding for this project
Competing interests: The authors declare no competing interests.
Author
details: Chandima Sarani Sepalage is a young zoologist interested in internal parasites of threatened wildlife. She holds a master’s degree and a BSc Hons. in Zoology from the University of Peradeniya, Sri Lanka. Rupika Subashini Rajakaruna is a parasitologist attached to the Department of Zoology University of Peradeniya in Sri Lanka. She is interested in disease ecology of enteric parasites of threatened taxa and how wildlife parasites can be considered in conservation targets of hosts.
Author
contribution: CSS—carried out the field and laboratory work, analysed data and wrote the manuscript; RSR—designed the study protocols, supervised the field and laboratory work, edited the manuscript
Acknowledgements: Authors acknowledge Dr Shanmugasundaram
Wijeyamohan and the park rangers for the assistance
in fecal sample collection.
Abstract: A
cross-sectional, coprological survey of gastrointestinal (GI) parasites of wild
mammals in four major National Parks in Sri Lanka: Wilpattu,
Udawalawe, Wasgamuwa, and
Horton Plains was carried out during November 2016 to August 2017. Fresh fecal samples were collected and analyzed
using sedimentation technique, iodine & saline smears, and Sheather’s sucrose flotation for morphological
identification parasite eggs, cysts, and larvae. A modified salt flotation was carried out for
egg counts. Seventy samples from 10
mammal species: Asian Elephant, Spotted Deer, Water Buffalo, Sambar, Indian
Hare, Asian Palm Civet, Sloth Bear, Wild Boar, Grey Langur, Leopard, and four
unknown mammals (two carnivores, one herbivore and one omnivore) were analyzed. Most were infected (94.3%) with more than one
GI parasites. The highest prevalence of
infection was recorded in Horton Plains (100%), followed by Wasgamuwa
(92.8%), Wilpattu (90.4%) and Udawalawe
(75.0%) with a significant difference among four parks (Chi square test; χ2=35.435;
df=3; p<0.001).
Nineteen species of GI parasites were recorded, of which Entamoeba,
Isospora, Balantidium, Fasciola, Moniezia,
Dipylidium, strongyles, Toxocara,
Trichiurus and hookworms were the most
common. Strongyles
(62.1%) and Entamoeba (80.3%) were the most prevalent helminth and
protozoan infections, respectively.
Overall, there was no difference in the prevalence of protozoans (84.3%)
and helminths (87.1%; χ2=1.0; df=1;
p=0.317). In carnivores, Entamoeba,
Balantidium, Moniezia, strongyles and Strongyloides
were common and in herbivores, Entamoeba, strongyles,
Strongyloides and Toxocara
were common. The quantitative
analysis showed strongyles (17.639 EPG) and Isospora (18,743 OPG) having the highest
infection intensity among helminthes and protozoans,
respectively. This study provides
baseline information of GI parasites and their distribution in wild mammals in
the four national parks. Although the
prevalence of GI infections was high, their intensity shows that they could be
incidental infections. When the
prevalence of an infection is high but the intensity is low, it is unlikely to
be a major health problem leading to the endangerment of a species. Parasitic diseases can not only affect
conservation efforts, but they are also natural selection agents and drive
biological diversification, through influencing host reproductive isolation and
speciation.
Keywords: Cysts,
gastrointestinal parasites, helminthes,
identification, protozoans, wild mammals.
INTRODUCTION
National
parks are established in many countries to protect and conserve nature while
also serving for education, tourism and entertainment (Kaffashi
et al. 2015). National parks in Sri
Lanka were first established 100 years ago to conserve valuable natural
environments (Dahlberg et al. 2010) and are distributed over three climatic
zones; dry zone, wet zone and intermediate zone. Today, there are 35 national reserves
consisting of three strict nature reserves, 26 national parks, five nature
reserves, and one jungle corridor. In
Sri Lanka, the Department of Wildlife Conservation (DWC) is the main government
authority which has the legal power to control national reserves and natural
forests. In these national reserves, a
total of 95 species and subspecies of mammals have been described consisting of
21 endemic species and 12 introduced species (Weerakoon
2012).
Endoparasites
are an important part of studying the disease ecology of wild animals as the
abundance and diversity of parasites can determine the health of a particular
ecosystem (Sallows 2007). Especially, in a natural ecosystem carnivores
occur in lower densities than ruminants, therefore, parasitic infection of
carnivores is a good indicator to understand the health of a specific national
park (Stuart et al. 2017). Moreover,
parasitic infections can vary between sexes, for example male ungulates are
more susceptible to parasitic infections than the females (Dunn 1978; Apio et al. 2006).
Environmental conditions like monsoon rains and soil moisture affect
parasitic transmission and many parasitic diseases are acquired through
contaminated soil and water (Marathe et al.
2002). When food and water are
contaminated with infected feces it can easily spread
the diseases among wild animals in the park (Coffey et al. 2007; Stuart et al.
2017). Parasites can affect the growth
rate, mortality rate, population size and interaction between individuals such
as sexual selection and social behaviors of wild
mammals (Sinclair & Griffith 1979; Sumption & Flowerdew 1985; Freeland
et al. 1986; Marathe et al. 2002).
Ecologists
have recently begun to understand the importance of diseases and parasites in
the dynamics of populations (Altizer et al.
2003). Diseases and parasites were
probably responsible for some extinctions on islands but also on larger land
masses, but the problem has only been identified retrospectively (reviewed in
McCallum & Dobson 1995). On the
other hand endemic pathogens and parasites might play a crucial role in
maintaining the diversity of ecological communities and ecosystems (Karesh et al. 2012).
When the hosts are keystone or dominant species with important functions
in an ecosystem, the effects of diseases on ecological communities can be
particularly pronounced (Preston & Johnson 2010). Patterns of disease emergence in wildlife and
integration of parasitism into community ecology provide information for better
understanding of the roles of parasites in nature. Among these, their role in food webs,
competitive interactions, biodiversity patterns, and the regulation of keystone
species, make it clear that parasites contribute to structuring ecological
communities (Preston & Johnson 2010).
There is
no current literature available on the GI parasites of wild animals in national
parks in Sri Lanka. The present study
was carried out to obtain baseline information of the types, prevalence and
infection intensity of GI parasites in wild mammals in four major national
parks located in three climatic zones of Sri Lanka.
MATERIALS AND METHODS
Study site and study animals
Four
nature reserves were selected. Wilpattu National Park (8.433N & 80.000E), Wasgamuwa National Park (7.716N & 80.933E) and Udawalawe National Park (6.438N & 80.888E) are located
in the dry zone with mean annual temperature of 27.20C, 27.00C,
and 27.50C, respectively.
Horton Plains National Park (6.800N & 80.000E), located in the wet
zone has a mean annual temperature of 13.00C (Figure 1).
The
number of wild mammal species varies among the four parks: 31 species of
mammals in Wilpattu National Park, 43 in Udawalawe National Park, 23 in Wasgamuwa
National Park and 24 in Horton Plains National Park (DWC, Sri Lanka).
Collection of samples
Fresh fecal samples from wild mammals in the four parks were
collected during November 2016 to August 2017.
Approximately, 10–15 g of fecal matter was
collected from each animal that had defecated in the morning between 07.00 and
10.00 h while samples from those that defecate in the afternoon (e.g., Elephant
and Wild Boar) were collected in the late afternoon between 16.00 and 18.00
h. A trained tracker from the DWC
identified the fecal samples. Samples were taken to the laboratory in a
cooler, stored in a refrigerator at 40C and were analyzed
in the parasitology laboratory in the Department of Zoology at the University
of Peradeniya.
Sample analysis
Fecal samples were analyzed
using four methods: (a) sedimentation technique, (b) direct iodine and saline
smears, (c) Sheather’s sucrose flotation, and (d)
modified salt flotation. The eggs of different
species were identified morphometrically under a microscope under 10X
ocular lens and
objective lens of
40X (total magnification
400x). The number of
eggs, cysts/oocysts in 0.5ml were calculated as eggs per gram (EPG) in helminthes and cysts per gram (CPG) or oocysts per gram
(OPG) in protozoans. The length and
width of the eggs were measured under the same 400x magnification (10×40).
Sedimentation technique (Zajac &
Conboy 2012; page 13)
Since
the trematode eggs are relatively large and heavy they were qualitatively
isolated using the sedimentation method.
Approximately, 3g of feces was measured (for
elephants 50g was measured due to the high fiber
content in their feces) and mixed with 50ml distilled
water. Then the suspension was poured
into a test tube and allowed to settle for 5 min. The supernatant was removed and the pellet
was re-suspended in 5ml of distilled water and then allowed to set for another
5 min. Finally, the supernatant was
removed and the sediment layer collected in the bottom of the test tube was
examined after adding one drop of Methylene Blue under 400x magnification.
Direct iodine and saline smears
(Zajac & Conboy 2012; pages 12–13)
A drop
of Lugol’s iodine was placed on a microscopic slide
and a small portion of fecal matter (~ size of head
of a match) was picked up by using a cleaned toothpick and mixed thoroughly
with iodine. Then a drop of saline (1%
solution) was added to the smear, covered using cover slip and was observed under
light microscope at 400x magnification.
Sheather’s sucrose
flotation technique (Zajac & Conboy 2012, pages 4–11)
This
method was used to identify nematode and cestode eggs, coccidian oocysts and
other protozoan cysts in the fecal sample. Approximately, 3g of fecal
sample was measured (again 50g was used for elephant dung samples) and mixed
with 50ml of freshly prepared Sheather’s sucrose
solution (SPG 1.2–1.25) to make a suspension.
The suspension was filtered and poured into cleaned test tube and filled
until a convex meniscus formed at the top of the tube. A cover slip was placed over the meniscus and
left for 20 min. The cover slip was then
placed on a slide and examined under the microscope at 400x magnification.
Modified salt flotation technique
(Zajac & Conboy 2012; pages 4–11)
Modified
salt flotation is a quantitative method to count eggs of nematodes, trematodes
and cestodes and cysts of protozoa.
Approximately, 3g of the sample was transferred into a 15ml clean
centrifuge tube and 14ml of distilled water were added. For elephant dung samples, 50g was
transferred into a 50ml centrifuge tube and 45ml of distilled water were
added. Then the fecal
solution was stirred well with using a glass rod, the tube was centrifuged at
3000G (N/kg)for
20 min. After that, the supernatant was
removed, and the tube was filled again with 14ml (or 45ml) of distilled water
and was centrifuged at 3000G for 20 min.
This procedure was repeated until a clear solution of the supernatant
was obtained. Then the supernatant was
removed and salt solution was added to the butt of the centrifuge tube up to
14ml (or 45ml) level. Again, the tubes
were centrifuged at 3000G for 20 min.
Then the supernatant with the floating parasitic eggs was transferred
into a 15ml clean centrifuge tube and distilled water was added up to the 15ml
level and was centrifuged at 3000G for 10 min.
Then the supernatant was removed and the sediment was pipetted out into
microcentrifuge tubes (Eppendorf®).
These tubes were then centrifuged at 3000G for 10 min. The supernatant was removed leaving about
0.5ml of solution. This was mixed
thoroughly and about 0.1ml of the suspension was placed on and a microscopic
slide. Five such smears were prepared
from each sample and examined using a light microscope. Eggs of different species were identified and
counted and the number of eggs per gram in each sample was calculated. Intensity of infections was calculated using
CPG (cysts per gram), OPG (oocysts per gram) and EPG (eggs per gram) of feces.
RESULTS
Prevalence of parasites
A total
of 70 mammals were examined (Wilpattu = 21, Udawalawe = 8, Wasgamuwa = 28 and
Horton Plains = 13) of which 66 (94.3%) were infected with more than one GI
parasite of protozoans, trematodes, nematodes and cestodes. Among the four parks, the highest prevalence
of GI parasites was observed in the Horton Plains where all the mammals were
infected (100%), followed by Wasgamuwa (92.8%) and
the lowest was Udawalawe (75.0%) with a significant
difference in the prevalence among parks (Chi square test; χ2 = 35.435;
df = 3; p<0.001).
Overall, there was no difference in the prevalence of protozoans (84.3%)
and helminths (87.1%; χ2 = 1.0; df = 1; p
= 0.317).The highest protozoan prevalence was observed in Horton Plains(100%),
followed by Wasgamuwa (85.7%), Wilpattu
(80.9%) and Udawalawe (62.5%). The highest helminth prevalence was observed
from Horton Plains (92.3%), followed by Wasgamuwa
(89.3%), Wilpattu (85.7%) and Udawalawe
(75.0%).
Types of gastrointestinal parasites
Parasites
belong to 19 genera were observed in mammals in the four national parks. Out of which 14 species were identified
(Table 1; Figure 2). The most common
protozoan was Entamoeba (80.3%) observed in the Asian Elephant, Water
Buffalo, Spotted Deer, Asian Palm Civet, Indian Hare, Sloth Bear, Sambar, Wild
Boar, and Grey langur. The most common
helminth were strongyles (62.1%) observed in the
Asian Elephant, Water Buffalo, Asian Palm Civet, Leopard, Sloth Bear, Sambar,
Indian Hare, and Grey Langur. The least
common parasite infections were pinworm, Toxocara,
Diphyllobothrium and Balantidium.
Intensity of Infections
Overall,
the intensity of infection was not high in any GI parasite observed in the four
parks (Table 2). The highest protozoan
infection was observed in the Horton Plains (23.811 CPG) and the highest
helminth infection was observed in Wasgamuwa (18.743
EPG; Table 2).
DISCUSSION
Results
show that the prevalence of GI infections in wild mammals in the four national
parks was high (94.3%). High prevalence
of GI infections are recorded in many national parks: Masai
Mara National Reserve (100%) in Kenya (Engh et al.
2003), Kibale National Park (84%) in Uganda (Bezjian et al. 2008), Serengeti and the Ngorongoro Crater
(97.3%) in Tanzania (Muller-Graf, 1995), Langtang National Park (88.9%) in
Nepal (Achhami et al. 2016). There was a significant difference in the
prevalence among the four parks. Udawalawe had the lowest prevalence GI infections while
Horton Plains had the highest. This
could be due to the period of sampling where it was carried in the dry period
in Udawalawe and in the rainy season in Horton
plains. During rainy periods, the
transmission of parasitic infections is high.
The environmental conditions such as rainfall patterns have a
significant influence on the parasitic transmission in mammals and there is a
strong relationship between the rainfall and the pathogenecity
of GI infection (Marathe et al. 2002; Rosenthal 2010;
Turner et al. 2012; Chattopadhyay & Bandyopadhyay 2013; Stuart et
al. 2017). On the contrary, Wasgamuwa Park was also sampled during the dry season but
had a higher prevalence of infection.
Some studies, however, show that the prevalence of certain GI parasites
is not correlated with rainfall pattern (Gillespie et al. 2004, 2005). For example, Oesophagostomum
is a common infection in baboons in the dry season in Kibale
National forest (Bezjian et al. 2008). The authors point out that this parasite may
resist desiccation due to the lush habitat of the Kibale
National Forest and the presence of the Dura River. It has also been noted that during the dry
season, Oesophagostomum sp. larvae can
avoid adverse weather conditions by arresting their development (Pettifer 1984).
Nevertheless, the sample size in the Udawalawe
Park was small (n = 8) and therefore comparing across parks and drawing
conclusions cannot be done uncritically.
The prevalence of infection did not show any marked seasonal variation
among the four parks.
There
was no difference in the prevalence of helminthes and
protozoans in the four national parks.
The two groups have developed different adaptive strategies for their
survival. Protozoans release large
number of cysts with feces, compared to helminthes. But
helminth egg is resistant to various environmental conditions like high temperature,
high rainfall, desiccation etc (e.g., Toxocara,
Trichiurus) (Okulewicz
et al. 2012) as they have a thick egg shell.
Wilpattu and Udawalawe
parks are located in the dry zone of the country that has high temperatures but
the helminth eggs and protozoan cysts were able to survive those
conditions. Some studies however, show
high prevalence of helminthes than protozoans, have
been reported in wild lions in Tanzania (Muller-Graf 1995) and spotted hyenas
in Masai Mara Reserve, Kenya (Engh
et al. 2003) whereas in captive conditions such as zoological gardens, the
protozoan prevalence is higher than helminthes due to
regular anthelmintic treatments (Dawet et al. 2013)
but may not be the case always (Adeniyi et al. 2015; Aviruppola
et al. 2016).
Prevalence
of parasite infections can lead to evolution of tolerance or resistance in the
host. Tolerance to parasites, or
infection tolerance is the ability of a host to limit the health or fitness
effect of a given infection intensity whereas resistance is the ability of the
host reduce risk of infection. Both
resistance and tolerance are host traits that have evolved to alleviate the
health and fitness effects of infection, but they represent two fundamentally
different strategies to deal with parasites.
The main difference of the two is that resistance reduces the risk of
infection and/or the replication rate of the parasite in the host, whereas
tolerance does not. Tolerance and
resistance lead to different ecological and evolutionary interactions between
hosts and their parasites (Roy & Kirchner 2000; Rausher
2001; Best et al. 2014; Vale et al. 2014).
Roy & Kirchner (2000) show that if hosts evolve resistance, this
should reduce the prevalence of the parasite in the host population and if
hosts evolve tolerance instead, this will have a positive effect on parasite
prevalence.
Among
the GI parasite species observed Entamoeba, Isospora,
and Balantidium were the most common protozoans while Moniezia, Fasciola,
Schistosoma, Dipylidium, Diphyllobothrium, Ascaris,
strongyles, Strongyloides,
Trichostrongylus, Trichiurus,
Toxocara, hookworm, and pinworm infections
were the common helminthes. The diversity of parasite species was highest
in the Wasgamuwa Park and the lowest in the Horton
Plains. Although the prevalence of
infection was highest in the Horton Plains National Park, the diversity of
infection was the lowest. The common GI
parasites for both herbivores and carnivores were Entamoeba and strongyles. Fecal samples of herbivores such as the Asian Elephant Elephas
maximus, Water Buffalo Bubalus arnee, Spotted Deer Axis axis,
Sambar Rusa unicolor, Grey Langur Semnopithecus priam,
and Indian Hare Lepus nigricollis were
infected with Entamoeba, Balantidium, Moniezia,
Fasciola, Trichiurus,
strongyles, Strongyloides,
and Trichostrongylus. Carnivorous such as Leopard Panthera pardus kotiya and other unknown carnivorous species were
infected with Entamoeba, strongyles, Strongyloides,Toxocara, and hookworm.
Herbivores
get the infections through contaminated food or water as most of these GI
parasite eggs, cysts and larvae are associated with pasture. Digenetic trematodes like Fasciola,
and Pharamphistomum have indirect
life cycles where a snail (e.g., Lymnea, Planorbis, Balinus,
Oncomelaria) acts as an intermediate host of
parasite who associate with water bodies.
Cercariae of these trematodes encyst on vegetation where herbivores
feed. Moniezia
is a common cestode of herbivores and it was recorded from all four parks. It was also recorded in an unknown carnivore
in Horton Plains. A recent study on GI
parasites of wild cats reported Moniezia in
four leopards in Horton plains (Kobbekaduwa et al.
2017) and the authors attribute this as an accidental ingestion of oribatid
mites, the intermediate host of Moniezia by
the leopards. The mite lives on
the pasture and enters the mammalian host while feeding. Fasciola,
Moniezia, Strongyloides,
and Trichuris obtained from herbivores in Bhutan (Tandon et al. 2005)
and strongyles, Strongyloides,
Moniezia observed from Musk Deer in Nepal (Achhami et al. 2016).
Balantidium is also transmitted through fecal-oral
route infection via contaminated pasture (Schuster & Ramirez-avila 2008).
Carnivores get infected by GI parasites like Toxocara
mainly by ingesting the intermediate host (Okulewicz
et al. 2012) or by direct penetration like the hookworms. Toxocara is
a common GI parasite of carnivores worldwide.
Studies have shown Grey wolves in Riding mountain National Park of
Canada (Sallows 2007; Stuart et al. 2017) wild Lions
in Tanzania (Muller-Graf 1995), Wolves in northeastern
Poland (Kloch et al. 2005) wild carnivores in Przybyszewskiego (Okulewicz et
al. 2012), and Spotted Hyena samples in Masai Marai Reserve in Kenya (Engh et
al. 2003) as few examples.
Although
the prevalence of infection was high among the mammals, the intensity of most
infections were not high enough to cause serious health problems in these
mammals. Wild mammals have natural
resistance against parasites or live mutually with them, unlike captive
stressful conditions where the animals are more susceptible to parasitic
infections (Borkovcova & Kopriva
2005; Singh et al. 2006a,b; Adeniyi et al. 2015). Free ranging animals can disperse the
parasite throughout the environment, therefore the infections in wild mammals
or free living ones occur in low intensities compared to captive or domestic
mammals (Stuart et al. 2017). Because of
constant stress of captivity makes animals more susceptible to parasitic
infection as the immune system of these captive animals become weak (Gracenea et al. 2002; Cordon et al. 2008). Moreover, some infections in most captive and
domestic mammals has both transplacental and transmammary
transmission which can cause serious damage such as acute and ocular infections
of Toxocara in cubs (Okulewicz
et al. 2012). In some cases parasites
can affect the cellulose digestion of host species, increase the rate of
morbidity and mortality (e.g., Oesophagostomum;
Muehlenbein 2005).
This may depend on the intensity of infection, where some parasites
become less pathogenic even with large number of eggs or cysts (>20,000),
but some become high pathogenic with few eggs or cysts.
This study provides baseline information
of GI parasites and their distribution in wild mammals in the four national
parks. The prevalence of GI infections
was high, nevertheless, their intensity shows that they could be incidental
infections. When the prevalence of an
infection is high but the intensity is low, it is unlikely to be a major health
problem to endanger species.
Mathematical models have shown that parasitic diseases affecting host
mortality maintain equilibrium far below their disease free carrying capacity
(Anderson 1979; McCallum & Dobson 1995).
Highly pathogenic diseases also have minor effect on host
populations. If a disease is detectable
at high prevalence, it is probably mild and unlikely to be a major problem to
an endangered species. Parasitic diseases can affect conservation efforts,
acting as a contributing threat in the endangerment of wildlife hosts, and
occasionally causing severe population declines (de Castro & Bolker 2005; Blehert et al.
2009). The maintenance of host-parasite
relationships in managed wildlife populations can be ultimately beneficial, and
points to a critical role for wildlife parasitologists in conservation efforts
(Gomez & Nichols 2013). Parasites
are also natural selection agents influencing a variety of host attributes,
from phenotypic polymorphism and secondary sexual characters, to the
maintenance of sexual reproduction (Wegner et al. 2003; Lively et al. 2004;
Blanchet et al. 2009). These effects
ultimately drive biological diversification, through influencing host
reproductive isolation and speciation (Summers et al. 2003). Infections are
fundamental to the ecological and evolutionary drivers of biological diversity
and ecosystem organization (Marcogliese 2004). Wildlife parasites should be considered
meaningful conservation targets as important as their hosts as they not only
can affect conservation efforts, but they are also natural selection agents and
drive biological diversification, through influencing host reproductive
isolation and speciation.
Table 1. Prevalence of gastrointestinal parasites of
wild mammals in four national parks in Sri Lanka.
Parasite |
National Park |
|||
Wilpattu |
Udawalawe |
Wasgamuwa |
Horton plains |
|
Entamoeba Isospora Balantidium Moniezia Fasciola Schistosoma Dipylidium Diphyllobothrium Ascaris Strongylus Strongyloide Trichostrongylus Trichiurus Toxocara Hook worm Pin worm Unknown sp 1 Unknown sp 2 Unknown sp 3 |
71.4% 52.4% 14.3% 19.0% 38.1% 4.8% - - 14.3% 57.1% - 19.0% - - - 23.8% 4.8% - - |
83.3% 50% 16.7% 16.7% 33.3% - - - - 83.3% 33.3% 16.7% - - 50% - - - - |
85.7% 35.7% - 39.3% 39.3% 10.7% 32.1% 14.3% 32.1% 57.1% 10.7% 10.7% 10.7% 10.7% - 7.1% - - 3.6% |
92.3% 84.6% - 53.9% - - - - - 61.5% - - 15.4% - 7.7% - 3.8% 15.4% 15.4% |
Table 2. Prevalence and the intensity of parasites
found in wild mammals in four national parks in Sri Lanka.
National Park |
Mammal species (n) |
Parasite |
Prevalence |
Intensity (CPG/EPG/OPG) |
|
Asian Elephant Elephas maximus (1) |
Entamoeba |
100% |
0.020 |
|
Fasciola |
100% |
0.060 |
|
|
Strongyles |
100% |
0.300 |
|
|
Water Buffalo Bubalus arnee (5) |
Entamoeba |
40% |
0.334 |
|
Balantidium |
60% |
0.734 |
|
|
Isospora |
60% |
3.467 |
|
|
Fasciola |
40% |
0.201 |
|
|
Moniezia |
20% |
0.067 |
|
|
Schistosoma |
20% |
0.067 |
|
|
Strongyle |
40% |
0.400 |
|
|
Spotted Deer Axis axis (4) |
Entamoeba |
50% |
0.417 |
|
Isospora |
75% |
0.084 |
|
|
Moniezia |
75% |
0.084 |
|
|
Ascaris |
75% |
0.084 |
|
|
Trichostrongylus |
50% |
4.834 |
|
|
Indian Palm Civet Paradoxurus hermaphroditus (1) |
Entamoeba |
100% |
6.670 |
|
Isospora |
100% |
1.334 |
|
|
Strongyle |
100% |
0.334 |
|
Wilpattu |
Sloth Bear Melursus ursinus (1) |
Entamoeba |
100% |
0.334 |
|
Isospora |
100% |
14.000 |
|
|
Dipylidium |
100% |
10.000 |
|
|
Strongyle |
100% |
14.668 |
|
|
Indian Hare Lepus nigricollis (1) |
Entamoeba |
100% |
1.334 |
|
Moniezia |
100% |
0.334 |
|
|
Sambar Rusa unicolor (3) |
Entamoeba |
100% |
0.778 |
|
Isospora |
100% |
1.222 |
|
|
Fasciola |
100% |
2.889 |
|
|
Ascaris |
66.7% |
0.222 |
|
|
Strongyle |
66.7% |
0.778 |
|
|
Trichiurus |
33.4% |
0.222 |
|
|
Wild Boar Sus scrofa (4) |
Entamoeba |
50% |
0.333 |
|
Isospora |
25% |
0.416 |
|
|
Fasciola |
50% |
0.416 |
|
|
Moniezia |
25% |
0.084 |
|
|
Dipylidium |
25% |
0.084 |
|
|
Strongyles |
75% |
1.000 |
|
|
Unknown sp1 |
100% |
2.084 |
|
|
Unknown omnivore (1) |
Isospora |
100% |
1.000 |
|
Dipylidium |
100% |
7.334 |
|
|
Unknown sp 1 |
100% |
4.334 |
|
|
Unknown sp 2 |
100% |
0.334 |
|
|
Asian Elephant Elephas maximus (1) |
Fasciola |
100% |
0.020 |
|
Strongyle |
100% |
0.960 |
|
|
Water Buffalo Bubalus arnee (1) |
Entamoeba |
100% |
2.000 |
|
Balantidium |
100% |
1.000 |
|
|
Isospora |
100% |
4.667 |
|
|
Strongyle |
100% |
1.334 |
|
|
Grey Langur Semnopithicus priam (1) |
Entamoeba |
100% |
1.000 |
|
Isospora |
100% |
5.334 |
|
|
Strongyle |
100% |
18.668 |
|
Udawalawe |
Strongyloide |
100% |
7.334 |
|
|
Hook worm |
100% |
0.334 |
|
|
Unknown carnivore (1) |
Entamoeba |
100% |
1.000 |
|
Isospora |
100% |
1.667 |
|
|
Strongyle |
100% |
8.334 |
|
|
Strongyloide |
100% |
1.667 |
|
|
Hook worm |
100% |
0.334 |
|
|
Spotted Deer Axis axis (1) |
Entamoeba |
100% |
2.000 |
|
Fasciola |
100% |
0.334 |
|
|
Hook worm |
100% |
0.334 |
|
|
Trichostrongylus |
100% |
1.000 |
|
|
Indian Hare Lepus nigricollis (1) |
Entamoeba |
100% |
2.000 |
|
Moniezia |
100% |
4.000 |
|
|
Strongyle |
100% |
8.000 |
|
|
Asian Elephant Elephas maximus (6) |
Entamoeba |
100% |
2.667 |
|
Isospora |
25% |
0.166 |
|
|
Fasciola |
50% |
0.334 |
|
|
Moniezia |
100% |
1.083 |
|
|
Strongyle |
50% |
1.883 |
|
|
Water Buffalo Bubalus arnee (6) |
Entamoeba |
100% |
3.050 |
|
Isospora |
50% |
0.555 |
|
|
Moniezia |
66.7% |
0.611 |
|
|
Schistosoma |
50% |
0.167 |
|
Wasgamuwa |
Ascaris |
83.3% |
0.889 |
|
|
Strongyle |
66.7% |
0.833 |
|
|
Spotted Deer Axis axis (6) |
Entamoeba |
83.3% |
0.833 |
|
Isospora |
83.3% |
0.833 |
|
|
Unknown sp3 |
16.7% |
0.055 |
|
|
Fasciola |
66.7% |
0.444 |
|
|
Moniezia |
50% |
0.167 |
|
|
Dypylidium |
33.3% |
0.222 |
|
|
Diphyllobothrium |
33.3% |
0.166 |
|
|
Ascaris |
16.7% |
0.167 |
|
|
Trichostrongylus |
50% |
0.500 |
|
|
Asian Palm Civet Paradoxurus hermaphroditus (7) |
Entamoeba |
100% |
1.048 |
|
Isospora |
14.2% |
0.528 |
|
|
Fasciola |
85.7% |
3.667 |
|
|
Dipylidium |
71.4% |
1.000 |
|
|
Diphyllobothrium |
28.5% |
0.190 |
|
|
Strongyle |
100% |
19.667 |
|
|
Strongyloide |
42.8% |
1.381 |
|
Wasgamuwa |
Trichiurus |
42.8% |
1.714 |
|
|
Toxocara |
28.5% |
0.809 |
|
|
Pinworm |
14.2% |
0.407 |
|
|
Leopard Panthera pardus kotiya (1) |
Dipylidium |
100% |
0.334 |
|
Strongyle |
100% |
9.334 |
|
|
Toxocara |
100% |
5.000 |
|
|
Sloth Bear Melursus ursinus (1) |
Dipylidium |
100% |
2.000 |
|
Strongyle |
100% |
1.668 |
|
|
Unknown herbivore (1) |
Entamoeba |
100% |
2.000 |
|
Ascaris |
100% |
0.667 |
|
|
Strongyle |
100% |
0.667 |
|
|
Indian Hare Lepus nigricollis (4) |
Entamoeba |
100% |
15.755 |
|
Isospora |
100% |
45.697 |
|
|
Moniezia |
75% |
2.647 |
|
|
Strongyle |
75% |
12.521 |
|
|
Trichiurus |
50% |
3.014 |
|
|
Unknown sp 3 |
25% |
6.500 |
|
|
Asian Palm Civet Paradoxurus hermaphroditus (1) |
Entamoeba |
100% |
16.000 |
|
Strongyle |
100% |
4.000 |
|
|
Unknown sp 3 |
100% |
2.000 |
|
Horton Plains |
Wild Boar Sus scrofa (2) |
Entamoeba |
50% |
0.333 |
|
Isospora |
100% |
4.667 |
|
|
Strongyle |
100% |
0.667 |
|
|
Unknown sp 1 |
100% |
2.000 |
|
|
Sambar Rusa unicolor (5) |
Entamoeba |
100% |
1.401 |
|
Isospora |
100% |
0.734 |
|
|
Moniezia |
60% |
0.200 |
|
|
Strongyle |
20% |
0.067 |
|
|
Hook worm |
20% |
0.067 |
|
|
Unknown carnivore (1) |
Entamoeba |
100% |
6.000 |
|
Moniezia |
100% |
2.000 |
|
|
Strongyle |
100% |
4.000 |
REFERENCES
Achhami, B.,
H.P. Sharma & A.B. Bam (2016). Gastro-intestinal parasites of Musk
Deer (Moschus chrysogaster
Hodgson, 1839) in Langtang National Park, Nepal. Journal of Institute of
Science and Technology 21(1): 71–75.
Adeniyi, I.C., O.A. Morenikeji & B.O. Emikpe
(2015). The prevalence of gastro-intestinal parasites of
carnivores in university zoological gardens in South West Nigeria. Journal
of Veterinary Medicine and Animal Health 7(4): 135–139.
Altizer, S.,
C.L. Nunn, P.H. Thrall, J.L. Gittleman, J. Antonovics, A.A. Cunningham, A.P. Dobson, V. Ezenwa, K.E. Jones, A.B. Pedersen & M. Poss (2003). Social organization and parasite
risk in mammals: integrating theory and empirical studies. Annual
Review of Ecology, Evolution, and Systematics 34(1): 517–547.
Anderson, R.M. (1979).
Parasite pathogenecity and the depression of the host
population equilibria. Nature 279: 150–152.
Apio, A., M.
Plath & T. Wronski (2006).
Patterns of gastrointestinal parasitic infections in the Bushbuck, Tragelaphus scriptus
from the Queen Elizabeth National Park, Uganda. Journal of Helminthology 80:
213–218.
Aviruppola,
A.M.J.K., R.S. Rajakaruna & R.P.V.J. Rajapakse (2016). Coprological survey of
gastrointestinal parasites of mammals in Dehiwala National Zoological Gardens,
Sri Lanka. Ceylon Journal of Science 45(1): 83–96.
Best, A., A. White & M. Boots
(2014). The co-evolutionary implications of host tolerance. Evolution;
International Journal of Organic Evolution 68: 1426–1435
Bezjian, M.,
T.R. Gillespie, C.A. Chapman & E.C. Greiner (2008). Coprologic evidence of gastrointestinal
helminths of forest baboons, Papioanubis, in Kibale National Park, Uganda. Journal of Wildlife
Diseases 44(4): 878–887.
Blanchet, S., O. Rey, P. Berthier, S.
Lek & G. Loot (2009).
Evidence of parasite mediated disruptive selection on genetic diversity in a
wild fish population. Molecular Ecology 18: 1112–1123.
Blehert, D.S.,
A.C. Hicks, M. Behr, C.U. Meteyer, B.M. Berlowski-Zier, E.L. Buckles, J.T.H. Coleman, S.R. Darling,
A. Gargas, R. Niver, J.C. Okoniewski, R.J. Rudd & W.B. Stone (2009). Bat
white-nose syndrome: an emerging fungal pathogen? Science 323–227.
Borkovcova, M.
& J. Kopirova (2005).
Parasitic helminthes of reptiles (Reptilia)
In South Moravia (Czech Republic). Parasitology Research 95(1): 77–80.
Chattopadhyay, A.K. & S.
Bandyopadhyay (2013). Seasonal variations of EPG levels in gastro-intestinal
parasitic infection in a Southeast Asian controlled locale: a statistical
analysis. Springerplus 2: 2–9.
Coffey, R., E. Cummins, M. Cormican, V.O. Flaherty & S. Kelly (2007).
Microbial exposure assessment of waterborne pathogens. Human Ecological Risk
Assessment 13: 1313–1351.
Cordon, G.P., A.H. Prados, D. Romero, S.M. Moreno, A. Pontes, A. Osuna &
M.J. Rosales (2008) Intestinal parasitism in the animals of the zoological
garden ‘‘Pena Escrita’’ (Almunecar,
Spain). Veterinary Parasitology 156: 302–309.
Dahlberg, A., R. Rohder & K. Sandell (2010). National parks and environmental justice: comparing access rights and
ideological legacies in three countries. Conservation
and Society 8(3): 209–224.
Dawet, A., D.P. Yakubu & H.M. Butu (2013). Survey of gastrointestinal parasites of non-human primates in Jos Zoological Garden. Journal of Primatology 2(1): 1–3.
De Castro, F.
& B.M. Bolker (2005). Parasite establishment
and host extinction in model communities. Oikos 111(3): 501–513.
Dunn, A.M.
(1978). Veterinary Helminthology. 2nd Edition. William Heinemann
Medical Books, London, UK.
Engh, A.L., K.G.
Nelson, R. Peebles, A.D. Hernandez, K.K. Hubbard
& K.E. Holekamp (2003). Coprologic Survey of Parasites of Spotted Hyenas
(Crocuta crocuta)
in the Masai Mara National
Reserve, Kenya. Journal of
Wildlife Diseases 39(1):
224–227.
Freeland, W.J., B.L.J. Delvinqueir&
B. Bonnin (1986). Food and parasitism
of the Cane
Toad, Bufo marinus, in relation to time since colonization. Wildlife Research 13(3): 489–499.
Gillespie, T.R.,
E.C. Greiner & C.A. Chapman (2004). Gastrointestinal parasites of the guenons
of western Uganda. Journal
of Parasitology 90:
1356–1360.
Gillespie, T.R.,
E.C. Greiner & C.A. Chapman (2005). Gastrointestinal parasites of the colobus
monkeys of Uganda. Journal
of Parasitology 91:
569–573.
Gómez, A. &
E. Nichols (2013). Neglected
wild life: parasitic biodiversity as a conservation target. International
Journal for Parasitology:
Parasites and Wildlife 2:
222–227.
Gracenea, M., M.S. Gomez, J. Torres, E. Carne & J. Fernadez-Moran (2002) Transmission dynamics of Cryptosporidium in primates and herbivores
at the Barcelona Zoo: A long-term
study. Veterinary
Parasitology 104: 19–26.
Kaffashi, S., A. Radam, M.N. Shamsudin, M.R. Yacob & N.H.
Nordin (2015). Ecological
Conservation, Ecotourism, and Sustainable Management: The
Case of Penang National
Park. Forests 6: 2345–2370.
Karesh, W.B., A. Dobson, J.O. Lloyd-Smith, J. Lubroth, M.A. Dixon, M. Bennett, S. Aldrich, T. Harrington,
P. Formenty, E.H. Loh & C.C. Machalaba
(2012). Ecology of
zoonoses: natural and unnatural histories. The
Lancet 380(9857): 1936–1945.
Kloch, A., M. Bednarska & A. Bajera (2005). Intestinal macro and microparasites of Wolves (Canis
lupus L.) from north-eastern Poland Recovered by Coprological
Study. Annals of Agricultural and Environmental Medicine 12: 237–245.
Kobbekaduwa, V., C. Fillieux, A. Thududgala, R.P.V.J. Rajapakse
& R.S. Rajakaruna (2017). First record of tapeworm Moniezia
(Cestoda: Anoplocephalidae)
infections in Leopards: coprological survey of gastrointestinal parasites of wild and captive
cats in Sri Lanka. Journal of Threatened Taxa 9(3):
9956–9961. https://doi.org/10.11609/jott.2926.9.3.9956-9961
Lively, C.M., M.F. Dybdahl, J. Jokela, E.E. Osnas & L.F. Delph (2004). Host sex and local
adaptation by parasites in a snail-trematode interaction. The American Naturalist 164: S6–S18.
Marathe, R. R.,
S.S. Goel, S.P. Ranade,
M.M. Jog & M.G. Watwe
(2002). Patterns in abundance
and diversity of fecally dispersed
parasites of tiger in Tadoba National Park,
Central India. BMC Ecology 2: 1–10.
Marcogliese, D.J. (2004). Parasites: small players with
crucial roles in the ecological theater. EcoHealth 1:
151–164.
McCallum, H. & A. Dobson (1995). Detecting disease
and parasite threats to endangered
species and ecosystems. Trends in Ecology and
Evolution 10: 190–194.
Muehlenbein, M.P. (2005). Parasitological analyses of the Male Chimpanzees
(Pantroglodytes schweinfurthii)
at Ngogo, Kibale National
Park, Uganda. American Journal of Primatology 65: 167–179.
Muller-Graf,
C.D.M. (1995). A coprological
survey of intestinal parasites of Wild Lions (Panthera leo) in the Serengeti and
the Ngorongoro Crater, Tanzania, East Africa. The
Journal of Parasitology 81(5):
812–814.
Okulewicz, A., A. Perec-Matysiak, K. Bunkowska & J. Hildebrand (2012). Toxocara canis, Toxocara cati and Toxascaris
leonina in wild and domestic carnivores. Helminthologia 49(1): 3–10.
Pettifer, H.L. (1984). The helminth fauna of the digestive tracts of Chacma
Baboons, Papio ursinus, from different localities in the Transvaal. Onderstepoort Journal of
Veterinary Research 51: 161–170.
Preston, D. & P. Johnson (2010). Ecological Consequences of Parasitism. Nature Education Knowledge 3(10): 47.
Rausher, M.D. (2001). Co-evolution and plant resistance to natural enemies.
Nature 411: 857–864.
Rosenthal, J.
(2010). Climate
Change and Geographic
Distribution of Infectious Diseases. EcoHealth 6:
489-495.
Roy, B.A.
& J.W. Kirchner (2000). Evolutionary
dynamics of pathogen resistance and tolerance. Evolution 54: 51–63.
Sallows, T.A. (2007). Diet preference and parasites of grey wolves in
Riding Mountain National Park of Canada. M.Sc. Thesis. University Manitoba,
Canada.
Schuster,
F.L. & L. Ramirez-avila (2008). Current world status of Balantidium coli. Clinical
Microbiology Reviews 21(4): 626–638.
Sinclair,
A.R.E. & M.N. Griffith (1979). Serengeti: Dynamics of an Ecosystem. Chicago: University of Chicago Press.
Singh, P.,
M.P. Gupta, L.D. Singla, N. Singh & D.R. Sharma (2006a). Prevalence and chemotherapy of gastrointestinal
helminthic infections in wild carnivores of Mahendra
Choudhury Zoological Park, Punjab. Journal of Veterinary Parasitology 20(1):
17–23.
Singh, P.,
M.P. Gupta, L.D. Singla, S. Sharma, B.S. Sandhu & D.R. Sharma (2006b). Parasitic infections in wild herbivores in the Mahendra Choudhury Zoological Park, Chhatbir,
Punjab. Zoo’s Print Journal 21(11): 2459–2461. https://doi.org/10.11609/JoTT.ZPJ.1519.2459-61
Stuart, P., O. Golden, A. Zintl, T.D. Waal, G. Mulcahy, E.
McCarthy & C. Lawton (2017). A coprological survey of parasites
of wild carnivores in Ireland. Parasitology Research: 1–10.
Summers, K., S. McKeon, J. Sellars,
M. Keusenkothen, J. Morris, D. Gloeckner,
C. Pressley, B. Price & H. Snow (2003). Parasitic exploitation as an engine
of diversity. Biological Reviews 78: 639–675.
Sumption , K.J. & J.R. Flowerdew (1985). The
ecological effects of the decline in Rabbits (Oryctolagus
cuniculus L.) due to myxomatosis. Mammal Review 15(4):
151–186.
Tandon, V., P.K. Kar, B. Das, B.
Sharma & J. Dorjee (2005).
Preliminary survey of gastro-Intestinal helminth infection in herbivores
livestock of mountainous regions of Bhutan and Arunachal Pradesh. Zoos’
Print Journal 20(5): 1867–1868. https://doi.org/10.11609/JoTT.ZPJ.1227.1867-8
Turner, W.C., W.D. Versfeld, J.K. Kilian & W.M. Getz (2012). Synergistic
effects of seasonal rainfall, parasites and demography on fluctuations in
springbok body condition. Journal of Animal Ecology 81: 58–69. https://doi.org/10.1111/j.1365-2656.2011.01892.x
Vale, P.F., A. Fenton & S.P.
Brown (2014). Limiting damage during infection: lessons from infection
tolerance for novel therapeutics. Public Library of Science 12:
e1001769.
Weerakoon, D. (2012).
The Taxonomy and Conservation Status of Mammals in Sri Lanka. Available
from: https://www.researchgate.net/publication/268630003 Accessed on 26 December 2019.
Wegner, K.M., T.B.H. Reusch & M. Kalbe (2003).
Multiple parasites are driving major histocompatibility complex polymorphism in
the wild. Journal of Evolutionary Biology 16: 224– 232.
Zajac, A.M. & G.A. Conboy (2012).
Fecal examination for the diagnosis of
parasitism, pp. 3–14. In: Zajac, A.M. & G.A. Conboy (eds.). Veterinary
Clinical Parasitology. John Wiley & Sons, 354pp.