Abstract
The helminth fauna of eight species of wild ruminants and five species of domestic ruminants sharing common grassland in Mongolia was reviewed. A total of 108 species of helminths, belonging to 40 genera, 23 families, 11 superfamilies, 6 orders and 3 classes were reported in wild and domestic ruminants in Mongolia. Several new host–helminth associations have been recorded. Twenty seven helminth species have been found in certain host species for the first time in Mongolia. These included 2 species of trematodes, 2 species of cestodes and 23 species of nematodes. Helminths that are specific for some of the examined ruminant species were determined. However, wild animals may serve as a reservoir of helminth infections for domestic animals when sharing grassland in Mongolia. The helminth fauna of the ruminants with respect to occurrence, distribution, prevalence and intensity of infection was considered for six geographic regions of Mongolia.
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Introduction
For centuries, livestock was the most important factor contributing to the socio-economic status of the nomadic herdsmen in Mongolia. Approximately 30 million livestock such as goats, sheep, cattle, camels and horses, and 40 other mammalian species are present in Mongolia. Parasitism by helminths is of serious concern in either grazing animal husbandry or wildlife. Several studies have shown that wild-living animals may act as reservoirs of infectious agents (Simpson 2002) and parasites (Badanin 1940; Rodonaâ 1962; Asadov 1963; Petrov 1985; McManus 1996; Kjimtrup et al. 2000) of domesticated animals. Considering the difficulty of access to information on the helminth fauna of wild-living and domestic animals in Mongolia, the aim of this paper is to review the studies on cattle, sheep, goat, yak and camel, and wild ruminants including the maral (Cervus elaphus sibiricus), roe deer (Capreolus pygargus), argali (Ovis ammon), ibex (Capra sibirica), Mongolian gazelle (Procapra gutturosa), goitred gazelle (Gazella subgutturosa), Mongolian saiga (Saiga tatarica mongolica) and wild Bactrian camel (Camelus bactrianus).
Table 1 shows the helminth species found in our studies (Gongoryn 1978; Tazieva et al. 1981; Gongoriin and Kuznetzov 1986; Sharhuu 1986; Sharkhuu 2001). Considering in addition the studies of other authors on the helminth fauna of Mongolian domestic (Kopyrin 1937; Šumakovič 1937; Ivaškin 1955; Namjil 1967; Baatar 1970; Dashzeveg 1973; Sharhuu 1986) and wild ruminants (Baatar 1969; Danzhan 1978; Sharhuu 1986; Ganbold 2000), a total of 108 species of helminths belonging to 3 classes, 6 orders, 11 superfamilies, 23 families and 40 genera were registered. The following helminth species were first described in Mongolia: Moniezia skrjabini in sheep and goats (Baatar 1970); Thelazia ivashkini in cattle (Dashzeveg 1973); Nematodirus changai in the maral (Sharhuu 1986) and Paradictyocaulus gutturosa in the Mongolian gazelle (Danzhan and Ganbold 1999).
Trematode infections were mainly restricted to certain areas in Mongolia, namely, the area of the Depression of Great Lakes, and their biodiversity is very limited. For cestodes, species of the families Anoplocephalidae (39.5%) and Taeniidae (16.1%) were common. The most often recorded helminths were nematodes of the families Trichostrongylidae (55%), Protostrongylidae (7.5%), Setariidae, Habronematidae and Trichuridae (4.5%).
According to their location in the host, 80 species were recovered from the digestive tract, 10 from the lungs, 6 from the chest and abdominal cavities (Setaria altaica, Se. capreola, Se. cervi, Se.digitata, Se. labiato-papillosa, Setaria sp.), 2 from the skin (Stephanofilaria stilesi, Onchocerca sp.), 3 from the lacrymal glands (Thelazia gulosa, Th. ivashkini, Th. skrjabini), and 1 each from the liver (Echinococcus granulosus larva: Echinococcus hydatidosus), the heart (Taenia ovis larva: Cysticercus ovis), the brain and spinal cord (Multiceps multiceps larva: Coenurus cerebralis), the dura mater and pia mater of the brain (Elaphostrongylus panticola), the skeletal muscle (Taenia saginata larva: Cysticercus bovis) and the portal vein (Orientobilharzia turkestanica). Sixty-seven species are parasites of both wild and domesticated ruminants. These helminth species are named common helminths and were determined with similarity indexes of 55.5% in the argali, 33% in the ibex, 46.5% in cattle and the yak, 39.6% in the Mongolian gazelle, 56.5% in the goat and 36.5% in the camel. The higher the similarity index, the closer is the interrelation of helminths between domestic and wild ruminants.
The following species of helminths reported in Mongolia were considered specific to their hosts: Dipetalonema evansi, Dictyocaulus cameli and Nematodirella cameli to the Bactrian camel; Taenia saginata larvae, Thelazia gulosa, Th. ivashkini, Th. skrjabini, Stephanofilaria stilesi, Onchocerca sp. and Dictyocaulus viviparus to cattle and yak; Setaria altaica, Elaphostrongylus panticola and Nematodirus changai to the maral; Setaria capreola, Skrjabinocaulus sofievi, Skrjabinagia kolchida, Ostertagia antipini and Spiculopteragia dagestanica to the roe deer; Spiculocaulus leuckarti and Nematodirus archari to the argali; Skrjabinema caprae, Protostrongylus caprae and Neostrongylus zvetkovi to the ibex, Setaria sp., Paradictyocaulus gutturosa, Skrjabinodera saiga, Nematodirus gazellae and Nematodirella gazelli to the gazelle species.
Although prevalence and intensity of helminth infection were studied in each animal, here the genera of helminths are considered only on the average of the hosts with respect to their occurrence throughout the ecological regions of Mongolia. Information about geography and climatic conditions in each region were reported according to the data given by Gungaadash (1984) and the National Atlas (Anonym 1990). On the basis of our review of the helminth fauna, the existence, distribution, prevalence and intensity of infection in the various geographic regions of Mongolia are detailed below (see Fig. 1).
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1.
High mountains (Huvsgul and Altai)
Long, cold winter lasts in the area. Thirty helminth species, including 5 species of cestodes and 25 species of nematodes, were identified in this region. Haemonchus and Bunostomum spp. (prevalence: 5.4–45.5%; average intensity: 11–689), Oesophagostomum spp. (25–36%; 59–230) and Dictyocaulus spp. (0.8–31.6%; 6–116) were found. Trematodes with fresh-water molluscs as intermediate hosts were not reported.
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2.
Altai pre-mountains
This region includes the Mongol and Gobi-Altai mountain chains with an altitude of 2,000–3,000 m (absolute height 3,500–4,374 m) above sea level. Average annual precipitation is 100–300 mm, January temperature: −25 to −30 °C; July temperature: +17 to +18 °C. Fifty-six species of helminths were registered in this region, 11 species were cestodes, and 45 species were nematodes. Haemonchus, Oesophagostomum and Bunostomum spp. were absent in this region. There were also no trematodes that require fresh-water molluscs in their lifecycle.
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3.
Hangai-Hentii pre-mountain chains
The altitude of this region is 1,500–2,000 m above sea level. Annual precipitation is 200–300 mm on average; the temperatures in January are −25 to −30 °C and in July +15 to +20 °C. Sixty-two helminth species, including 2 trematode, 12 cestode and 48 nematode species, were registered. Paramphistomatidae trematodes and nematodes such as Trichuris (10.4–84%; 5–416), Bunostomum, Chabertia (5.2–83%; 18–390), Oesophagostomum, Ostertagia (50–91.1%; 105–60,000), Marshallagia (50.6–96%; 132–2,620), Haemonchus (28.2–100%; 120–5,660), Cooperia (5–79.1%; 115–21,763), Nematodirus (17–90%; 112–6,953), Dictyocaulus and Protostrongylus spp. were found.
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4.
Steppe
Steppe is found 800–1,200 m above sea level. Average annual precipitation is 120–250 mm; average temperatures are −15 to −20 °C in January and +20 to +25 °C in July. Fifty-five helminth species, including 12 species of cestodes and 43 species of nematodes, were registered in this region. The most common infections were with Chabertia, Ostertagia, Marshallagia and Nematodirus spp. Dictyocaulus infections were rare, and trematodes were not found.
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5.
Semi-desert (semi-arid)
This region is about 1,000–1,500 m above sea level and experiences warmer and drier winters, and hotter and drier summers with, on average, 50–150 mm precipitation. Fifty-three species of helminths, including 3 species of trematodes, 12 species of cestodes and 38 species of nematodes including Bunostomum, Chabertia, Haemonchus, Trichostrongylus (8–60%; 12–50,000), Oesophagostomum, Dictyocaulus and Ostertagia spp. were registered here. The following nematode species were considered as indicators of this region: Nematodirus oiratianus, Trichostrongylus probolurus, Nematodirella cameli and Parabronema skrjabini (40–100%; 34–920). Animals originating from the Depression of Great Lakes in this region had a higher prevalence and intensity of helminth infections, and 42 helminth species were identified. Molluscs, which are the intermediate hosts of Paramphistomum, Liorchis and Orientobilharzia spp., are abundant here.
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6.
Desert
No trematode species, 2 species of cestodes and 25 species of nematodes were recorded in animals from this region. The high temperature and low humidity of air and soil in semi-arid and desert regions are the climatic conditions that are responsible for lower levels of some helminth infections in comparison with other localities (data not shown). The common helminth genus here is Nematodirella (2.6–30%; 90–3,400) in the camel and goats.
Conclusions
In conclusion, the helminth fauna of domestic and wild ruminants in Mongolia is rich, with varying diversity as to occurrence, distribution, prevalence and intensity of infection in the geographic regions. The knowledge of the helminth fauna in relation to hosts and geographical regions is very important, particularly with respect to control measures in domesticated animals.
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Acknowledgements
We would like to express our gratitude to the Veterinary Institute in Ulaanbaatar, Mongolia, the K.I. Skryabin (All-Union) Institute of Helminthology in Moscow, Russia, the Institute of Zoology in Alma-Ata, Kazahstan and the W. Stefański Institute of Parasitology in Warsaw, Poland, for their support, supervision and kindness.
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Sharhuu, G., Sharkhuu, T. The helminth fauna of wild and domestic ruminants in Mongolia—a review. Eur J Wildl Res 50, 150–156 (2004). https://doi.org/10.1007/s10344-004-0050-3
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DOI: https://doi.org/10.1007/s10344-004-0050-3