Echinococcosis in Foxes of Tibetan Plateau

Chapter Four

Echinococcosis in Foxes of the Tibetan Plateau

4.1 Introduction

Until the recent publication of a paper in 2005 (Xiao et al) Echinococcus multilocularis was known as the 'fox tapeworm'. This Cestode is recognised as the most serious pathogenic zoonosis of all helminthic diseases REF. Today there are two recognised species which can collectively be named fox tapeworms; Echinococcus multilocularis REF and Echinococcus shiquicus REF. The latter of the two species has a restricted distribution. The fox definitive host species Vulpes ferrilata Hodgson (1842) from which the life cycle was first described is found only in the high plateau regions of Tibet, China, Nepal and India hence the parasites' known distribution. As yet this parasite has not been shown to infect man.

The former species Echinococcus multilocularis has a more widespread distribution covering the northern hemisphere across Europe, America and Asia. The parasites' range is not surprising as its natural definitive host is the red fox Vulpes vulpes REF; the most successful canine with a geographical distribution covering nearly the entire holartic region. REF book red fox

Both species of parasite have the potential to infect a range of different hosts and indeed E.multilocularis has been shown to infect a number of wild canids and small mammals (see TABLE>>>>CHAPT>>). The prevalence of E.shiquicus in foxes is not yet known and only a limited number of studies have been carried out. In addition to this, although E.multilocularis may be a well documented parasite, much less is known about specific infection rates in Chinese foxes and the true distribution of the parasite across the Tibetan plateau.

The importance and relevance of monitoring the changing status of these two parasites in wildlife populations is critical in understanding the transmission mechanisms of AE and the wildlife cycle of E.shiquicus.

In order to understand parasite transmission patterns it is first critical to be aware of the host/landscape on which they are found and how it is maintained in wildlife. The initial part of this chapter reviews the biology of the fox definitive hosts with reference to the Tibetan plateau in terms of their habitat, diet and behaviour.

4.1.1 Vulpes ferrilata (Hodgson, 1842)

Distribution and Habitat

The Tibetan fox, or sand fox to which it is sometimes referred is widespread across the Tibetan plateau and found in India, China and Nepal (Schaller, 1998 REF)


Within China- the focus of the current thesis- the Tibetan fox range encompasses the whole Tibet Autonomous region, southern Xinjiang, south-west Qinghai and north-east of Sichuan provinces. A survey of 43 counties of Tibet autonomous region estimated their population to be 37,000 (Piao et al, 1989 in REF online book) and further studies have shown that the population is REF. Its limitation in home range appears to be due to its habitat requirements of elevations exceeding 3000metres up to approximately 5300metres (REF) a direct association with the habitat requirements of the small mammals on which it predates. At these altitudes the fox predominantly uses grasslands and other low level vegetation where small mammal populations are abundant. In essence, as with a majority of mammals, this fox habitat utilization is probably governed by food availability (REF).

A recent study by Wang et al (2007) looked specifically into landcover use by the Tibetan fox. It was shown that they were located significantly more in grassland (composed of herbaceous plants with >60% ground coverage and height no higher than 20cm) than in other habitat types e.g. shrubland. They conclude that the habitat use pattern of Tibetan foxes can be explained by the demand of food and their antipredation strategy. It is believed that the domestic dog is the most important natural enemy of foxes; up to 16 fox deaths directly caused by stray dogs were reported by the group. The significance of this in terms of the current study is great. It accentuates the fact that there is competition and overlap in habitat use favoured by dogs and foxes thus exacerbating the potential transmission of Echinococcus spp. to man, dogs being the link between wildlife AE reservoir and humans (Craig et al, 2004). Other predators include man (for the fur trade),

The choice of the Tibetan fox to utilise open pasture seems to be a compromise; the overlap in habitat use is a risk for attack but it is suggested that these places would allow for earlier detection of predators compared to more dense vegetation cover (Wang, 2008). More detailed studies of fox biology are essential in determining their impact and effect on transmission of disease to other animals and humans.


The principal diet of the Tibetan fox is Ochotona curzoniae, the black lipped Pika (Schaller and Ginsberg, 2004; Lui et al, 2008, Raoul et al, unpublished). This lagomorph species is endemic to the Tibetan Plateau and has been described as a keystone species for biodiversity (Smith and Foggin, 1990). Pika's are diurnal and spend time foraging and digging (Arthur et al, 2008). This species is of extreme importance in terms of this research as it has shown to harbour the metacestode stages of E.multilocularis and E.shiquicus. The In recent times, much research into the small mammal assemblages ALSO THE NUMBER AND TYPE OF CYSTS...........Liu et al (2009) looked at the diet of the Tibetan fox in Qinghai Province. By analysing scats at two time points they were able to examine if fluctuating numbers of Pika's affected their importance in the fox diet. Results showed that although there was a difference in seasonal Pika density, this did not affect the fox diet. IMPORTANCE


It was concluded that large ungulates and mammals probably represented scavenging on carrion due to the relatively small size of the fox compared to those animals. Unfortunately they did not differentiate between other rodent species and Tibetan foxes have previously been shown to predate on various rodent species (Pitymus, Alticola, Cricetulus and Microtus) (Schaller and Ginsberg, 2004). Giradoux and Raoul (unpublished) carried out a separate analysis of fox scats. The consensus remained that the main prey is the Pika with Microtine species being the second most frequently detected in samples. Microtines are known intermediate hosts for E.multilocularis. To date they have not been sho


It is suggested that mating occurs in February with 2 -5 young born after a three month gestation period (Schaller and Ginsberg, 2004). The foxes are usually seen alone hunting or foraging. As Ochotona are diurnal, foxes tend to hunt during daylight hours

Livestock grazing, plateau pikas and the conservation of avian biodiversity on the Tibetan plateau Anthony D. Arthur a, Roger P. Pech a 1, Chris Davey a Jiebu b, Zhang Yanming c and Lin Hui d

They are social animals that tend to be spatially clumped ([Smith and Wang, 1991] and [Zong et al., 1991]) and can reach very high population densities of >350ha-1 (Wang et al. 1997). They are typically diurnal and interact with their environment through foraging and digging activities and by recycling nutrients, which contributes to plant community dynamics; as prey for a suite of top predators; and by constructing burrows that are used as shelter and nest sites by other species (Zhang, 2002 Y. Zhang, Characteristics of social behavior and adaptation to the alpine extreme environment in plateau pikas (Ochotona curzoniae), The Chinese Academy of Sciences, Beijing (2002). [Zhang, 2002][Lai and Smith, 2003], [Zhang et al., 2005] and [Bagchi et al., 2006]).

Schaller G.B. and Ginsberg J.R. (2004) Tibetan fox pp148-151. In Canids:foxes, wolves, jackals and dogs: status survey and conservation action plan. Editors; Claudio S, Hoffmann M. Macdonald D.W. Published: Gland, Switzerland: IUCN

A.T. Smith and J.M. Foggin, The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau, Animal Conservation 2 (1999), pp. 235-240

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