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Session VI: Disease and health service

Reindeer (Rangifer tarandus) and yak (Bos (Poephagus) grunniens):
Disparate animal species—similar environment, management and parasite problems?

P.J. Waller

SWEPAR, National Veterinary Institute, SE-751 89 Uppsala, Sweden


Reindeer (Rangifer tarandus) inhabit most of the circumpolar land areas not covered by permanent ice in the Palaearctic (Eurasian) and Nearctic (American) regions of the northern hemisphere. In the northern areas of Sweden, Norway and Finland (Fennoscandia), home to the Saami people, reindeer are a crucial resource and large populations are maintained under semi-domesticated situations. There has been departure somewhat from the transhumance type of management in recent years, but still these animals are herded extensively on alpine pastures and browse, in accordance with the seasonal availability of feed. In many ways, this approximates the management systems for yak (Bos grunniens) in the cold, high altitude areas of central Asia. Therefore, it is not suprising that similar species of parasites (both internal and external), with similar features and rank order of importance are found in these two quite different animal species. The warble fly (Hypoderma spp) is generally regarded as the most important parasite of both reindeer and yak. The immature stages cause considerable stress to the animal through the migratory activities, and economic loss due to damage of the hide following the emergence of the pre-pupal stages. For reindeer, the incidence of infection can exceed 95% of the herds. Hypodermosis, particularly of the white yak populations in the Tianzhu region of China, is a particularly serious disease with prevalence of infection approximating 100% and responsible for great losses in productivity. Gastro-intestinal nematode parasites are also important in both reindeer and yak. In reindeer, the abomasal parasite Ostertagia gruehneri is the most common and economically important. Yak have been shown to harbour a range of nematode species, similar to those found in cattle in the cool temperate regions of the world, with Ostertagia spp considered to be one of the most important internal parasites. Control of these parasites is essential if economic losses are to be reduced, or avoided, for both reindeer and yak production. This poses many logistical and practical problems which are not associated with control of parasites in more sedentary systems of livestock management—such as for cattle, sheep and goats.

Keywords: External parasites, internal parasites, reindeer, yak


The reindeer genus Rangifer comprises only one species, R. tarandus living in the northern hemisphere, both in the Palaearctic (Eurasian) and Nearctic (American) areas (Banfield 1961). It inhabits most of the circumpolar land areas not covered by permanent ice. The southern most reindeer (apart from those introduced to the southern hemisphere) graze in China (50 ) and the northern most on Svalbard, Greenland and arctic islands of Canada (Oksanen 1999). There is some controversy as to the number of subspecies of reindeer, with a range between 7 and 12. It seems that one of the most important reasons for the evolution of subspecies has been the separation of the Asian and American continents and the concomitant occurrence of a series of glacial periods (Oksanen 1999). The Nearctic wild reindeer is called the caribou.

The current estimate of the total reindeer population of the world is nearly 8 million animals, with half of them semi-domesticated (Staaland and Nieminen 1993). About 20% of the semi-domesticated reindeer are in Fennoscandia (Finland, Sweden and Norway) and 75% in Russia. The remaining 5% are found in North America and Greenland, and on arctic and sub-antartic islands (Oksanen 1999).

The main reindeer product is meat, but also hides are an important source of income. In Russia, reindeer are still an important draft animal. They are also milked and used for riding at some locations (Nieminen 1995). Velvet antler constitute the major reindeer product in Alaska for sale to Asian markets (Nieminen and Muhonen 1996).

Within the Fennoscandian region, reindeer husbandry is almost entirely associated with the indigenous Saami people. Management is under a co-operative system, whereby animals are owned by individual herders, but they graze communally. The number of animals has increased rapidly in recent years, largely due to changed management techniques which include winter supplementary feeding, antiparasitic treatment and motorised herding. This has placed considerable demands on the sustainability of this industry, not least of which is the pressure on the environment induced by overgrazing (Oksanen 1999).

The adaptations of the yak (Bos (Poephagus) grunniens) to extremely cold climatic conditions are rather similar to those of the reindeer. In addition, there are other physiological adaptations (large heart, lungs and high erythrocyte count), which enable this species to tolerate low oxygen content of high altitude regions (Sasaki 1994). Their habitat is limited to the mountains and plateaus of the Asian highlands, inter-connected mountainous areas of the Himalaya, Pamir, Kun Lun, Tien Shan and Altai mountains (RangaRao et al. 1994). The world population is in the order of 15 million animals, with approximately 90% found within the P.R. of China (Rongchang et al. 1994). There are several native strains or types of yak and this animal can interbreed with cattle, with the hybrids referred to as dzomo (female) and dzo (male). This has now become a common practice for the purposes of increasing meat and particularly milk production, but it results in sterility of the male hybrids (Rongchang et al.1994). Yak are known universally as being an important pack animal in these cold, high mountain regions, but they also produce a range of valuable products, such as meat, milk, hide, hair and dung (used as fuel).

Because both reindeer and yak are the sole animal species of economic importance that survive in their respective regions, they are irreplaceable resources to the local communities. Therefore, factors that adversely affect the productivity of these animals, which potentially can be minimised, are of great importance. Of these, macroparasites (internal and external) are likely to be the most important disease organisms, which limit animal productivity at the extreme latitudes and altitudes of the world.

Parasites—Impact on production

Establishing with any degree of certainty, the financial penalty of parasite infection in a given livestock system is extremely difficult—some would say impossible. A much more relevant approach is to attempt to assess the avoidable losses from parasitic infections, simply because it is totally unrealistic to expect suppression (or eradication) of parasites from any grazing livestock situation (Perry and Randolph 1999). This would particularly apply to extensive, communal grazing activity that typifies the way in which reindeer, or yak, are managed.

It is a common belief amongst reindeer owners that the obvious parasites (larval stages of the oestrid flies—warbles, throat bots) are part of the 'normal' appearance of their animals and these, together with the cycles in weather and vegetation, are an inseparable part of reindeer management ecosystem (Oksanen 1999). Nevertheless, attempts to estimate the costs of parasites to reindeer productivity have been made and these range from 20–30% (Nordkvist 1967; Saval'ev 1968). Irrespective of this, reindeer owners are now obviously of the opinion that parasites are a cause of preventable losses in production. This is clearly illustrated by the fact that approximately 75% of all reindeer in Fennoscandia are treated at least once per year with anthelmintic (Oksanen 1999).

It would seem that the effects of parasites, particularly hypodermosis, are even more severe in yak. Studies involving many thousands of yak, where comparisons were made between either treated and untreated animals grazing communally, showed that milk and meat production was increased by 20–30%, and hide damage and mortality were greatly reduced, in the treated animals (Yanhong 1994). Hypodermosis was also attributed to be a significant factor in the cause of high mortality of yak in Bhutan (Choudhuri 1970). The Tianzhu White yak—a rare, mild tempered, native strain of yak found largely in the Gansu Province of China, is particularly susceptible to warble attack, with almost all animals infected at any one time (Yanhong 1994).

Whilst these very limited studies which attempt to estimate productivity/costs of parasites to reindeer and yak industries, are directed entirely towards the obvious parasites (warbles and throat bots), absolutely no information of the penalties of the more cryptic gastro-intestinal and pulmonary nematodes of reindeer and yak exists. However, based on analogy with economic assessments of the cost of internal parasitism in other grazing ruminants (cattle and sheep), these costs are likely to be substantial. This is based on the fact that immunity in grazing livestock to nematode parasites is slow to develop, is dependent on a good nutritional state and pick-up of infective stages from pasture is more-or-less a continuous process. As a consequence, parasites are ubiquitous throughout all the extensively grazed regions of the world and virtually all animals are infected almost all of the time (Waller 1997a).

Parasites of importance

Theory predicts that the most pathogenic parasites are generally rare and thus have little impact on host populations, compared with less pathogenic parasites that may be abundant and therefore suppress host populations to a greater extent (Anderson and May 1978; May and Anderson 1978).

External parasites

The most notable insect parasites of reindeer and yak, excluding harassment by blood sucking insects, are lice and the oestrid flies. Of the latter, the warble fly Hypoderma/ Oedemagena tarandi (for reindeer) and Hypoderma lineatum (for yak) are generally considered the most important, but possibly this is due to the fact that most studies (see above) have been directed towards this pest. H. lineatum is the common warble fly of cattle. The throat bot, Cephenomyia trompe, may also be important in reindeer, but very little is known about this parasite.

The life cycle of Hypoderma is very similar for all species of this genus. Female flies lay eggs on the hairs of the host, especially on the feet, during the summer months. The larvae hatch, crawl down the hair follicle and penetrate the skin, to commence an extensive somatic migratory phase in the connective tissue of the animal. They finally reach their predilection sites, which is the subcutaneous tissue of the back of the animal, where they mature to the 3rd instar larvae. During winter they perforate the skin of the animal to breathe. In spring, the mature larvae emerge, drop to the ground where they bury themselves, pupate and the imagos emerge about one month later, depending on the prevailing weather conditions (12 ≡ 50 days; 27°C ≡ 10 days; Nilssen 1997). Hypoderma has a specific attraction for light coloured animals; thus this fly particularly troubles white reindeer and yak.

Internal parasites

For reindeer, the brainworm, Elaphostrongylus rangiferi, is considered to be the most important, but this could be simply due to the fact that, apart from warble fly, most is known about this parasite (Oksanen 1999). This parasite has been responsible for severe outbreaks of meningoencephalitis after warm summer weather (Handeland and Slettbakk 1994). Very little is known about the lungworm, Dictyocaulus eckertii, of reindeer, but it can be present in large numbers in emaciated reindeer calves during late winter (A. Oksanen, personal communication). With regards to the gastro-intestinal nematodes, the abomasal species (particularly Ostertagia gruehneri) has been reasonably well studied but mainly in wild reindeer populations on Svalbard (Halvorsen and Bye 1999). The intestinal nematode fauna, such as Trichostrongylus spp, Moniezia spp, Nematodirus and Nematodirella spp may also be important. Quantitative data suitable for epidemiological investigations and the development of strategic control methods are lacking almost entirely for most of the parasites of reindeer (O. Halvorsen, personal communication).

A number of studies on the gastro-intestinal nematode fauna of yak have been performed (Liu 1994; RangaRao et al. 1994). As expected, a comprehensive array of species have been reported, representing the range of important nematode, trematode and cestode species commonly found in bovine and ovine hosts, some being apparently yak-specific. With regards to nematode parasites, it appears that Trichostrongylus spp, Ostertagia spp, Cooperia spp are the most dominant species (Ranga Rao et al. 1994). This observation is in accord to the most abundant nematode parasite species of ruminant livestock found in the temperate regions of the world (Anderson and Waller 1983). Thus, it is reasonable to assume that the epidemiology and principles of control of these parasites in yak would be broadly similar to gastro-intestinal parasites of cattle.

Methods of control

These have been directed primarily at the control of insect pests, particularly Hypoderma spp.


Prior to the advent of the effective parasiticides, various management procedures were carried out with varying degrees of adoption for reindeer management systems in the Palaearctic region (Oksanen 1999). Warbles were often removed mechanically from infected reindeer by compressing them between the thumb and the forefinger in spring. However, this procedure was extremely laborious and an alternative, effective mechanical method of individual animal treatment was to suffocate the larval stages by applying thick emulsions, e.g. creosote or tar, to the backs of animals.

Because of their specific attraction to light coloured reindeer, warble fly females were lured to alight on white hides, where they were easily killed. Early knowledge of the seasonal dynamics of H. tarandi, led to the development of some ingenious management procedures. For example, resting herds of reindeer in wet, swampy regions in early summertime was carried out with the specific purpose of causing a lot of the emerging larvae to drown. Another practice was to drive herds considerable distances (>50 km) after calving in early summer and not returning to the calving ground until late autumn, to deprive the adult flies with suitable hosts. Dark sheds for housing and the use of smoke screens as repellents during the warm summer months are also traditional methods used to combat this important pest problem in reindeer.

I am not aware of any published information with regards to the control of warbles in yak by non-chemical methods. However, it is possible that one, or a number, of these approaches have been used.


With the advent of the modern insecticides (DDT, hexachlorethane, chlorophos and pyrethrin etc.), mass spraying of animals was tested in Russia. One trial showed that the use of 12.5 kg for each of pure DDT and hexachlorethane on a herd of 1000 reindeer during one summer season increased their performance by 5–6 kg/animal and improved the quality of the hides (Savelv 1968). Clearly these are impressive performance data, but one wonders at what cost to the environment? Fortunately, the questionable economics and the impracticality of such mass treatment (if not the environmental impact) have precluded widespread adoption of these mass insecticide treatment procedures.

Chemical treatment against the larval stages of warbles started to become popular following the advent of the systemically applied organophosphate drugs. Drugs such as famphos, trichlorfon and fenthion have been reported as being effective against the larval stages of both warbles and throat bots of reindeer (Nieminen et al. 1980; Nordkvist 1980) and fenthion has been used against warbles in yak with good success (Yanhong 1994).

However the treatment of the larval stages of these flies took a quantum leap forward with the marketing of the macrocyclic lactone (ML) drugs, most notably ivermectin. These drugs have a very broad range of activity and extraordinary potency against both internal and external parasites—as a consequence they are often termed endectocides. Not only do these drugs have an exceedingly potent activity against nematode parasites at dose levels many magnitudes less than for the other broad-spectrum anthelmintics, but they have quite extraordinary potency against Hypoderma spp. For example, the dose rate of ivermectin for most livestock species is 200 μg/kg liveweight, with the dose-limiting species being the gastro-intestinal nematodes (cf. range of ≡ 5–50 mg/kg for the other modern broad-spectrum anthelmintics), represents major overkill for warble larvae. A high efficacy was reported at a dose of 0.2 μg/kg of the injectable formulation against H. lineatum in cattle—one thousandth of the recommended dose rate for nematode parasites (Drummond 1984).

A series of studies have been conducted on the control of internal and external parasites of reindeer using the ML anthelmintics, principally by Oksanen and co-workers (Oksanen et al. 1992; Oksanen et al. 1993; Oksanen 1996; Oksanen et al. 1998) who have suggested that the most efficacious product is seemingly the subcutaneous injectable formulation of ivermectin. These workers have also evaluated other ML formulations. For example, moxidecetin was shown not to have comparable efficacy as ivermectin (Oksanen and Nieminen 1998). Doramectin had 100% efficacy against warbles and throat bots, but this drug was not evaluated against internal parasites (Oksanen and Nieminen 1996). However, it could be expected to have equi-potency with ivermectin against these.

Although no off-label recommendations can be made for any drugs, it is almost certain that the ML anthelmintics would have similar, extremely high levels of efficacy against internal and external parasites of yak. The recommended dose rate to domestic ruminants is the same (i.e. 200 μg/kg for all the commercial MLs for subcutaneous injection and oral administration, and 500 μg/kg as a pour-on application). Although the topical (percutaneous) application has a lot of obvious attractions, this formulation was found to be not as effective as the subcutaneous administration in reindeer (Oksanen et al. 1993; Oksanen et al. 1995). This was attributed to the dense hair covering, thick skin and large subcutaneous fat deposits of the reindeer, which would limit drug bioavailability. The same factors are likely to militate against high efficacy of pour-on formulations of MLs in yak. It is also important to recognise that there are considerable differences within ruminants in the metabolism and pharmacokinetics of the MLs (McKellar and Benchaoui 1996), thus extrapolations of expected efficacy against similar parasites between animal species must be made with caution.

Parasite treatment strategies

Strategic treatment—Getting the best out of the drug

To maximise the effect of any anti-parasiticide treatment, it is important to link this with the seasonal ottlenecks in the parasite populations, when either the greatest proportion of the population will be exposed to the drug treatment and/or the potential for immediate re-infection is low. Also, every effort should be made to treat the whole host population, which serve as the main reservoir for the parasite population(s). This maximises the benefit of the drug treatment. This is sound in theory, but often difficult in practice, particularly in communal-type grazing systems, which typify reindeer and yak production.

However, it is now recognised that a particularly important time to treat reindeer, from a parasite epidemiology standpoint, is at the time when the animals are gathered in early winter. The parasites are particularly vulnerable, as they have evolved to over-winter almost entirely inside the animals. The warble and throat bot populations consist almost entirely of larval stages within the host and nematode parasites accumulate inside the animals, often in the hypobiotic (arrested) stage of development. Therefore, it is obvious that treatment at this time with a broad-spectrum anthelmintic (a ML) is an extremely sound strategy. This has been now widely accepted by the owners of reindeer in Fennoscandia and thus within a co-operative, almost universal agreement to treat with a ML anthelmintic at winter gathering, is commonplace (Oksanen 1999).

It would seem that the general epidemiological pattern of internal and external parasites of yak would be similar to those of the reindeer. That is, accumulation as larval stages within the animals as the main means of over-winter survival. Therefore treatment of animals at the beginning of winter not only causes a major disruption in the magnitude of the continuing parasite populations in the following year, but also removes potentially damaging parasite populations within the animal. These over-wintering populations compete for the precious nutritional resources of the animal when climatic conditions are extreme.

A word of warning—On resistance

It must be remembered that every time a drug is used, a strong selection pressure is placed on the target parasite population. Any survivors, and these can be exceedingly few with the modern drugs now available, have a great survival advantage. Resistance has been shown to be genetically determined and thus survivors will pass on resistance genes to successive generations. It could be argued that, because of the extreme sensitivity of Hypoderma spp to the ML drugs, resistant genes would be non-existent in this important parasite of reindeer and yak. I am not so certain. High levels of ML resistance have been shown to develop in other fly species (Scott et al. 1991).

One potent selector for the development of anthelmintic resistance is high frequency of treatment (Waller 1997b). Thus it could also be argued that treatment of reindeer and yak very infrequently (1–2 times each year) would not impose a strong selection pressure for the development of resistance. Unfortunately this also does not appear to be the case. Occasional strategic treatments have been shown to be potent selectors of resistance in situations where almost the entire parasite populations are within the animal (Besier 1997).

Although ML resistance by the target pest species has not been reported in reindeer or yak, it occurs for other pest parasite species—both flies (Scott et al. 1991) and to a range of both sheep and cattle nematode parasites (Rolfe 1997; Sangster 1999). Of particular concern with regards to all the cases of macrocyclic lactone resistance is that resistance seems to be a single major gene effect. This means that once resistance occurs, it increases rapidly and to a very high level (Le Jambre 1996), where dose levels many magnitudes higher than the recommended dose rate of the drug have no effect on resistant individuals.

I do not wish to conclude this presentation by sounding alarmist. However it must always be remembered that the development of resistance to a particular drug (group) is an inevitable evolutionary consequence in any given target pest species. Rather sadly, this has been shown time and time again (Waller 1994). It is important that reindeer and yak owners are made aware of this potential and for them to use other means of parasite control, both chemical and non-chemical, that are practical, affordable and effective to safeguard against the occurrence of this phenomenon.


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