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. 2024 Feb 14;48(1):134–140. doi: 10.1007/s12639-024-01652-8

Gastrointestinal parasites of the wild ungulates (Mammalia: Cetartiodactyla) in the Hemis National Park, Ladakh, India

Jigmet Zazay 1,✉, Bilal A Bhat 1, Hidayatullah Tak 1, Arif Nabi Lone 1
PMCID: PMC10908697  PMID: 38440757

Abstract

We evaluated the gastrointestinal parasitic prevalence and intensity of wild ungulates in the Hemis National Park of Ladakh by examining their fresh faecal samples. A total of 327 fresh faecal samples from three wild ungulates, blue sheep Pseudois nayaur (n = 127), Ladakh urial Ovis vignei vignei (n = 110), and Himalayan ibex Ibex siberica (n = 90) were collected between June 2021 and May 2022. The techniques of flotation and sedimentation were used to find parasite eggs and oocysts from the faecal samples. Out of 327 samples examined, 165 samples were infected with gastrointestinal parasites making an overall prevalence of 50.45%. Seven parasitic taxa, including one protozoan (Eimeria spp.), five nematodes (Nematodirus spp., Strongyloides spp., Haemonchus sp., Trichuris sp., and Trichostrongylus spp.), and one cestode (Monezia spp.), were found during the current investigation. Mixed infection was reported in 36 (11%) of the total examined samples. The prevalence of gastrointestinal parasites was found to be highest in blue sheep (55.11%), followed by Ladakh urial (49.09%) and Himalayan ibex (45.55%). The highest prevalence was recorded in the summer (64.42%), and the lowest in the winter (33.82%). A significant difference in parasitic prevalence was observed across seasons in each of the three wild ungulate hosts. However, there was no significant difference in the prevalence of parasites between these hosts.

Keywords: Prevalence, Mixed infection, Eggs per gram, Wild ungulates, Trans-Himalayas

Introduction

Gastrointestinal (GI) parasites are among the most widespread parasites that can infect the gastrointestinal tract (GIT) of humans and other animals (Inácio et al. 2022). The different parasitic genera residing in the GIT of ungulates are known to cause debilitating diseases resulting in reduced food consumption and mortality thus causing huge economic losses (Waller 2006). Pathogens and parasites are among the growing threats to wild ungulate populations (Hart et al. 2018). The common parasites that infect wild ungulates include coccidian, nematodes, cestodes and trematodes (Komáromy 2010). It is often seen that wild ungulate species are affected by the parasites and pathogens of domestic ruminants when they share the habitat (Verheyden et al. 2020).

The mountain ranges of Ladakh harbour eight species of wild ungulates, of which three species, blue sheep Pseudois nayaur, Ladakh urial Ovis vignei vignei and Himalayan ibex Ibex siberica are reported from the Hemis National Park (HNP) (Mishra 2001). In addition to these three wild ungulates, the Tibetan argali Ovis ammon hodgsonii has been occasionally reported in the HNP by earlier workers (Bhatnagar et al. 2001; Namgail et al. 2007). Blue sheep has been listed as the Least Concern while Ladakh urial and Himalayan ibex are listed as Near-Threatened (IUCN 2023). Blue sheep is distributed across the Tibetan plateau and its surrounding mountain ranges, while Himalayan ibex is distributed in the mountains of Trans-Himalayas (Ahmad 2023). Ladakh urial is endemic to Ladakh and neighbouring Gilgit-Baltistan (Khara et al. 2021).

Although the distribution, conservation status and habitat ecology of the wild ungulates of Ladakh have been studied (Fox et al. 1991; Namgail 2001; Khara et al. 2021), the data on the status of gastrointestinal parasitic infections in these wild hosts, however, is not available. Against this backdrop, the present study has been undertaken in the HNP of Ladakh where some wild ungulates are known to share the habitat with the livestock and this mixed aggregation can facilitate the transmission of gastrointestinal parasites among them. The baseline data on the prevalence and intensity of gastrointestinal parasites infecting wild ungulates of the HNP is, therefore, required and necessary for comparison and future monitoring.

Material and methods

Study area

HNP (34° 09.844″ N and 77° 03.506″ E), with an area of 4450 km2 is located to the south of Leh city at an altitudinal range of 3000 to 6000 m asl (Jamwal et al. 2019). The park is bounded by Sumdah Valley in the north, Markha, and Shang Valley in the south, and Rumbakh in the northwest (Jackson et al. 2003). The area experiences highly fluctuating weather conditions. In summer, the temperature varies from 30 °C in the sun to 4 °C in the shade. In winter, the temperature ranges from 0 °C during the day and drops below − 15 °C to − 20 °C at night. Heavy snowfall in the winter leads to the closure of passes in most of the area (Chandola 2012; Jamwal et al. 2019).

Vegetation is predominantly alpine and steppe in nature. Shrub lands cover less than 5% of the total land area. Grasses, sedges, and herbaceous plants are the main vegetation types, covering less than 15% of the total area (Fox et al. 1991). Dominant plant species within the park include woundwort (Stachys tibetica), cinquefoils (Potentilla spp.), worm-weeds (Artemisia spp.), Rhubarb (Rheum spp.), Himalayan knotweed (Bistorta spp.), and Ephedra (Ephedra spp.). Seabuckthorn (Hippophae salicifolia), willows (Salix spp.) and myricaria (Myricaria elegans) occupy the humid valley basin while wild rose (Rosa webbiana) occupy the gentle slopes. Poplars (Populus spp.) are cultivated in the valley bottoms up to 3700 m altitude (Chandola 2012; Jamwal et al. 2019).

Sample collection and examination

Faecal samples of three wild ungulates i.e., blue sheep, Ladakh urial and Himalayan ibex were collected from 22 sampling sites of the HNP between June 2021 and May 2022. The sites have been selected in a way to cover all habitat types along the altitudinal gradient. During our survey, no Tibetan argali was sighted in the study area. Samples were collected after the sighted animals had moved from the grazing area by using gloves to avoid contamination. Only fresh samples, soft and unfrozen in winter and moist and glistening in summer were collected. Adhering soil was brushed away from faecal pellets and 5–10 pellets per sample were placed in 15 ml airtight vials containing 10% formalin. Preserved samples were brought to the Wildlife Research Laboratory, Department of Zoology, University of Kashmir for analysis. The presence of protozoan cysts and GIT helminth eggs was examined by floatation and sedimentation techniques (Demelash et al. 2016). Identification of the eggs was done on the basis of morphology and size with the help of a standard key (Soulsby 1982). The number of eggs and oocysts counted on the McMaster slide was multiplied by 100 and expressed as helminth eggs per gram (EPG) of faeces and protozoan oocysts per gram (OPG) of faeces (Zajac and Conboy 2012). The prevalence of parasites in the hosts was calculated by the number of infected samples divided by the number of examined samples (Thrusfield 2007). The mean EPG and range of parasites were calculated using Microsoft Excel 2018.

Statistical analysis

The chi-square test was used to observe the differences in parasites across seasons in each host using R software 4.2.2. Kruskal Wallis test was used to evaluate the differences in GI parasitic prevalence among three wild ungulates. The confidence level was held at 95% with a p value < 0.05 for significance.

Results

A total of 327 faecal samples of three wild ungulates, blue sheep (n = 127), Ladakh urial (n = 110) and Himalayan ibex (n = 90) were examined for GI parasites. Out of these, 165 samples were infected with seven different genera of parasites consisting of one protozoan (Eimeria spp.), five nematodes (Nematodirus spp., Strongyloides spp., Trichuris sp., Haemonchus sp., Trichostrongylus spp.) and one cestode (Moniezia spp.).

Overall prevalence

The overall prevalence of GI parasites was 50.45%. Eimeria was found to have the highest prevalence in all three wild ungulate hosts, with an overall prevalence of (18.65%). Among helminths, nematodes were recorded with a higher prevalence (16.20%) than cestodes (4.58%). The highest prevalence was observed in blue sheep (55.11%), followed by Ladakh urial (49.09%) and Himalayan ibex (45.55%). Both blue sheep and Ladakh urial were infected with four genera of parasites. The parasites present in blue sheep were Eimeria spp. (20.47%) Nematodirus spp. (8.66%), Strongyloides spp. (7.87%) and Moniezia spp. (6.29%) while Ladakh urial was infected with Eimeria spp. (17.27%), Trichuris sp. (10.90%), Haemonchus sp. (5.45%) and Moniezia spp. (6.36%). The Himalayan ibex was infected with three genera of parasites Eimeria spp. (18.88%), Nematodirus spp. (8.88%) and Trichostrongylus spp. (5.55%) (Fig. 1).

Fig. 1.

Fig. 1

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Overall percentage prevalence of GI parasites in wild ungulates of Hemis National Park between June 2021 and May 2022

Mixed infections

Mixed infections were reported from 36 samples (11%) of the total samples of three wild ungulates. Various combinations of mixed infections reported in blue sheep were Eimeria and Moniezia spp. (5.51%); Eimeria, Moniezia and Nematodirus spp. (3.93%); Eimeria, Strongyloides and Moniezia spp. (2.36%). Ladakh urial was infected with mixed combinations of Eimeria and Moniezia spp. (3.63%); Haemonchus and Eimeria spp. (2.72%) and Trichuris and Eimeria spp. (2.72%). The Himalayan ibex was infected with Eimeria and Nematodirus spp. (6.66%); Eimeria and Trichostrongylus spp. (3.33%) and Eimeria, Nematodirus and Trichostrongylus spp. (2.22%). (Table 1).

Table 1.

Mixed infections of (GI) parasites in the wild ungulates of HNP between June 2021 and May 2022

Blue sheep (n = 127) Ladakh urial (n = 110) Himalayan ibex (n = 90)
Mixed parasites  + ive samples (%) Mixed parasites  + ive samples (%) Mixed parasites  + ive samples (%)

Eimeria spp.

Moniezia spp.

 7(5.51)

Eimeria spp.

Moniezia spp.

 4 (3.63)

Eimeria spp.

Nematodirus spp.

 6 (6.66)

Eimeria spp.

Moniezia spp.

Nematodirus spp.

 5(3.93)

Eimeria spp.

Haemonchus sp.

 3 (2.72)

Eimeria spp.

Trichostrongylus spp.

 3 (3.33)

Eimeria spp.

Strongyloides spp.

Moniezia spp.

 3(2.36)

Eimeria spp.

Trichuris sp.

 3 (2.72)

Eimeria spp.

Nematodirus spp.

Trichostrongylus spp.

 (2.22)
Total 15 (11.81) 10 (9.09) 11 (12.22)
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Seasonal prevalence

The prevalence was highest in the summer (64.42%) followed by autumn (51.13%), spring (44.77%) and winter (33.82%). A significant seasonal difference in the GI parasitic prevalence was observed in each host: blue sheep (χ2 = 11.94; p = 0.007), Ladakh urial (χ2 = 8.074; p = 0.044) and Himalayan ibex (χ2 = 8.65; p = 0.034). There was, however, no significant difference in the prevalence of parasites among the three hosts (H = 0.24; p = 0.88) and no significant difference (H = 1.14; p = 0.56) was seen in the seasonal prevalence of parasites across these hosts (Fig. 2).

Fig. 2.

Fig. 2

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Seasonal prevalence of GI parasites in wild ungulates between June 2021 and May 2022

Eggs per gram (EPG)

Among the three host species, the highest mean EPG was observed in blue sheep followed by Ladakh urial and Himalayan ibex. Among different parasites, the highest mean EPG and range were those of Eimeria spp. in all three ungulate species i.e. 309.99 (50–600) in blue sheep, 204.16 (50–400) in Ladakh urial, and 123.33 (50–166.66) in Himalayan ibex, while the lowest mean EPG and range were for Strongyloides spp. 93.33 (50–200) in blue sheep, Trichuris sp. 88.88 (50–166.66) in Ladakh urial and Trichostrongylus spp. 66.66 (50–66.66) in Himalayan ibex (Table 2).

Table 2.

Mean Eggs per gram (EPG) and ranges of (GI) parasites in the wild ungulates of HNP between June 2021 and May 2022

GIT parasites GIT parasitic group Blue sheep
Infected samples (n = 70)
Mean intensity (Range)		 Ladakh urial
Infected samples (n = 54)
Mean intensity (Range)		 Himalayan ibex
Infected samples (n = 41)
Mean intensity (Range)
Eimeria spp. Protozoa 309.99 (50–600) 204.16 (50–400) 123.33 (50–166.66)
Nematodirus spp. Nematode 158.33 (50–350) – 84.99 (50–166.66)
Strongyloides spp. 93.33 (50–200) – –
Haemonchus sp. – 94.44 (50–183.33) –
Trichuris spp. – 88.88 (50–166.66) –
Trichostrongylus spp. – – 66.66 (50–66.66)
Moniezia spp. Cestode 233.33 (50–600) 142.58 (100–250) –
Mixed parasites 297.22 (100–533.33) 266.66 (100–566.66) 219.68 (100–300)
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Discussion

During the present study, seven genera of gastrointestinal parasites belonging to Protozoa (one) Nematoda (five) and Cestoda (one) were reported. The overall prevalence and oocyst per gram (OPG) of Eimeria spp. were highest in all three wild ungulates of the HNP. Our results are in consonance with those of Ostrowski et al. (2009) and Ashraf et al. (2022). This may be due to the transmitted ‘oocyst’ stage of these parasites which can withstand stressors and remain in the infective stage for a long period of time Eimeria spp. are responsible for causing diarrhoea, loss of appetite, and even death in severe cases (Kennedy 2001). Among helminths, the prevalence of nematodes was higher (16.20%) than cestodes (4.58%). A similar observation has been made by different workers in other wild ungulates (Lone et al. 2016; Bhat et al. 2022; Dar et al. 2022). This is because most of the nematodes have a direct life cycle that does not require an intermediate host. However, their life cycle also involves partial development outside the host and is transmitted by feeding on contaminated food, water and soil. Usually, it is the L3 stage of nematodes at which the parasite assumes its form to invade the host (Soulsby1982; Walker and Morgan 2014; Figueiredo et al. 2020).

The overall prevalence of gastrointestinal parasites in the wild ungulates of the HNP was 50.45% which is lower as compared to the prevalence reported in other mountain ungulates of similar landscapes i.e., 100% in Tibetan antelope in Qinghai China, 50–87% in blue sheep in different reserves of Spiti valley India, 83.45% in Afghan urial and 68.22% in Suleiman markhor of Pakistan (Ahmad 2020; Cao et al. 2020; Iyer et al. 2022) The higher prevalence of parasites (55.5%) in the blue sheep as compared to the other two ungulates could be due to its wide distribution and sharing of a habitat with the livestock (sheep and goat) in some areas of the HNP while Ladakh urial and Himalayan ibex have limited ranges within the national park. Similar studies have been carried out in other Trans-Himalayan regions and it is reported that the parasite load was higher in wild ungulates that grazed in the same pasture with domestic livestock (Iyer et al. 2022). This finding suggests that parasites may be transmitted between wild and domestic ungulates (Barone et al. 2020; Khanyari et al. 2021).

Our study reported that among nematodes, Nematodirus spp. is present in both blue sheep and Himalayan ibex. The probable reason for the presence of Nematodiruss spp. in the Himalayan ibex is that it forms an overlap zone with some populations of blue sheep during the scarcity of food. This may be a possible reason for the cross transmission of GI parasites between these two hosts. Nematodirus is not associated with clinical diseases but in some European countries, Nematodirus battus is responsible for causing springtime diarrhoea in ungulates (Soulsby 1982; Zajac et al. 2020). The low prevalence and intensity of Strongyloides spp. in blue sheep and Trichostrongylus spp. in Himalayan ibex may be attributed to the fact that a dry and cold environment is not favourable to the Strongyloides eggs’ proliferation while Trichostrongylus produces only a few hundred eggs (Gardner et al. 2004; Stien et al. 2002).

Trichuris sp. and Haemonchus sp. were reported only in Ladakh urial with a prevalence of (10.90%) and (5.45%) respectively, as compared to Trichuris sp. in Siberian ibex (21.4%) and Argali of Mongolia (7.1%), Trichuris sp. (16.30%) and Haemonchus sp. (73.91%) in Punjab urial in Pakistan (Kenny et al. 2009; Bajwa et al. 2019). The difference in prevalence in different areas may be due to variations in climate; especially for the Haemonchus sp. as their prevalence is mostly reported in areas with high relative humidity, rainfall and ambient temperature which favour their development. Heavy infection with Haemonchus sp. led to anaemia and can even cause the death of the host however, in arid regions, the threat of Haemonchus sp. to the ruminant is quite low and their clinical symptoms are very rare (Cao et al. 2020; Zajac et al. 2020).

During the present study, Moniezia spp. were reported only in blue sheep and Ladakh urial. The presence of this parasite genus in the ruminant may be due to the consumption of oribatid mites that contain mature cysticercoid stages (Rizwan et al. 2023). The complete absence of Monezia spp. in the Himalayan ibex could be associated with the absence of an intermediate host (oribatid moth) as their preferred cliff habitat is relatively drier and less vegetated. The infections caused by Monezia spp. are generally asymptomatic and harmless but heavy infection may result in blockage of the intestine, diarrhoea, and weight loss (Zvinorova et al. 2016). No trematodes were recorded in our study. This may be due to the absence of molluscs (intermediate hosts), as their survival and development are influenced by the climate and environmental conditions of the area (Kusiluka and Kambarage 1996).

The high prevalence of parasites observed during summer (June–August) in our study area may be associated with relatively higher rainfall in summer as compared to other seasons which provides a moist environment for larval development while the low infection observed during winter could be associated with precipitation in the form of snowfall resulting in the drying out of faecal pellets causing the minimum chances of infection (Lone et al. 2016; Molla and Bandyopadhyay 2016). The mixed infections were reported in 36 samples belonging to blue sheep (n = 15, 11.81%), Ladakh urial (n = 10, 9.09%) and Himalayan ibex (n = 11, 12.20%). Earlier research shows that the diseases caused by mixed infections are more severe than the infection caused by any single species as they cause damage to the immune system of the host and thus render the animals susceptible to other diseases (Talpur et al. 2009; Wang et al. 2006).

The average intensity for eggs per gram (EPG) reported in our study is very low as compared to those reported by earlier workers in other mountain ungulates (Ostrowski et al. 2009; Lone et al. 2016; Bhat et al. 2022). The low EPG may be due to the freezing dry and cold climatic conditions prevailing in our study area, the segregated population of wild ungulates, the low density of the livestock population in the vast area of the HNP and the presence of anthelminthic plant species like Artemisia spp., Nepeta spp., Potentilla spp., Rheum spp. and Salix spp. which they graze on.

Conclusion

Although the intensity of parasites reported in our study was very low, i.e., less than 500 EPG at which the host shows no clinical symptoms, still there is a possibility that parasitic load may increase with increasing density of livestock which can act as a potential risk for these wild ungulate populations. The highest parasite prevalence in blue sheep, highlights the role of habitat sharing with livestock in parasitic transmission. Effective control measures would involve periodic anthelmintic treatments, regulated livestock grazing and maintaining healthy habitat conditions to keep the parasitic load at minimum.

Acknowledgements

We are thankful to the University Grants Commission (UGC) for providing grants under the UGC-JRF fellowship scheme. The authors duly acknowledge the Department of Zoology, University of Kashmir for providing laboratory and other facilities. Our sincere thanks go to the Department of Wildlife Protection Leh Ladakh for providing the necessary permission for the smooth conduct of this work.

Funding

This research was funded by University Grants Commission.

Declarations

Conflict of interest

On behalf of all authors, the corresponding author declares no conflict of interest.

Ethical approval

During the present study, non-invasive methods based on faecal examination were employed.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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