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Rabies in Zimbabwe: Reservoir Dogs and the Implications for Disease Control

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Rabies in Zimbabwe: Reservoir Dogs and the Implications for Disease Control Rabies in Zimbabwe: reservoir dogs and the implications for disease control C. J. Rhodes1*, R. P. D. Atkinson2, R. M. Anderson1 and D. W. Macdonald2 1WellcomeTrust Centre for the Epidemiology of Infectious Disease, and 2Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Using detailed ¢eld study observations of the side-striped jackal (Canis adustus) and a simple stochastic model of the transmission dynamics of the virus and host demography, we discuss the epidemiology of rabies virus infection in the jackal population of Zimbabwe. Of the two jackal species in Zimbabwe, the other being the black-backed jackal (Canis mesomelas), the bulk of noti¢ed rabies cases are in side-striped jackals. Speci¢cally, we show that the side-striped jackal population itself does not seem able to support rabies infection endemically, i.e. without frequent reintroduction from outside sources of infection. We argue that this is probably because the overall average jackal population density is too low to maintain the chain of infection. This study suggests that the disease is regularly introduced to jackals by rabid dogs from populations associated with human settlements. Given the rapidly rising dog population in Zimbabwe, estimates are derived of the future incidence of jackal rabies based on di¡erent dog-vaccination scenarios. Keywords: rabies; jackals; mathematical model transmission of rabies in this context (Gascoyne et al. 1. INTRODUCTION 1993b; Macdonald 1993). Furthermore, a greater preva- Rabies is a communicable disease capable of infecting all lence of rabies infection would have an impact on the mammals. The viral pathogen concentrates in cerebral agricultural sector of many African countries, as stock and nervous tissues, and upon succumbing to infection animals are currently lost each year owing to rabies the host often exhibits marked behavioural changes. In infection acquired from itinerant rabid canids (Bingham humans, the clinical symptoms of rabies, and the virtual 1995a). certainty of death following the emergence of these symp- Using a combination of detailed ¢eld-observation data toms, have made this disease one of the most feared in the and simple mathematical models this paper analyses the world. particular form of rabies epidemics in Zimbabwe. The Historically, in Europe, domestic dogs have been the large population of domestic dogs appears to act as the main vector of the disease to man, although in recent primary self-sustaining reservoir of the rabies virus. It is years the red fox (Vulpes vulpes) has acted as the primary possible that other species of animal can then acquire disease reservoir (Blancou et al. 1991). The population infection through interaction with the dog population. biology of foxes and the dynamics of fox rabies in Europe Typically, this results in temporally sporadic and spatially have been topics of extensive study, and ultimately this has localized outbreaks of rabies in other species, commonly led to e¡ective disease eradication and containment jackals in some parts of southern Africa. Jackals, which strategies which are generally based on oral vaccination our calculations suggest are unable to support rabies ende- of foxes (Anderson et al. 1981; Smith & Harris 1991; White mically (i.e. without frequent reintroduction from outside et al. 1995). Risk of exposure to humans has been consider- sources of infection), might then in their turn infect other ably reduced by the availability of e¡ective vaccines for wild and domestic animals, with welfare, conservation and domesticated dogs and cats. economic consequences before the disease dies out among Rabies is also present in the diverse mammalian popu- them. Using the mathematical model, it is possible to lations of Africa (Swanepoel et al. 1993), which is home to explore the potential variation that uncertainty in some some of the world's most endangered canid species of the ecological parameters can induce. (Gascoyne et al. 1993a; Sillero-Zubiri et al. 1996). Our ¢ndings support the conclusion of recent studies on However, at present, the complex epidemiology of rabies rabies infection in the dog populations of the Serengeti in Africa is not so well-understood as that in Europe. region of Tanzania (Cleaveland 1995; Cleaveland & Dye Serious outbreaks of rabies infection could jeopardize 1995) where it was shown that dogs are the most likely conservation programmes aimed at preserving species reservoir of the disease. Furthermore, our model predicts which are currently on the threshold of extinction, so it is an increasing dog population in Zimbabwe will lead to important that a better understanding is reached of the an increasing incidence of jackal rabies, and we outline the e¡ect of di¡erent dog-vaccination strategies on the *Author for correspondence ([email protected]). incidence of the disease in jackals. Phil. Trans. R. Soc. Lond. B (1998) 353, 999^1010 999 & 1998 The Royal Society Received 12 November 1996 Accepted 10 June 1997 1000 C. J. Rhodes and others Jackal rabies in Zimbabwe average lifespan of such animals is three to four years. 2. FIELD STUDY OBSERVATIONS The main cause of death on the study site was accidental Ecological parameters (per capita birth rate, per capita snaring in traps where edible species were the intended death rate, carrying capacity and contact rate) were target. For those animals that survive beyond six months, derived from a year-long study of side-striped jackals but which fail to secure a territory, we estimate life expec- (Canis adustus) on 150 km2 of commercial farmland tancy to be 1^2 years. centred 40 km south-west of Harare, Zimbabwe. Unless otherwise stated, all further discussion of jackals in this (c) Home range size and movements paper pertains to the side-striped jackal. The site consists The territories of males and females do not di¡er in size, of Brachystegia-dominated savannah woodland (`miombo'), nor is there a seasonal di¡erence in territory size. We esti- and low-lying, seasonally £ooded, natural grassland. Both mated territory size using 200 mÂ200 m grid cells. Over a habitat types occupy approximately 40% of the total area year the mean territory area used by jackals was and are used by grazing animals. Arable land, comprising 1224Æ92.3 hectares (range 1056^1672 ha.). Over a period planted grass leys, ploughed and fallow ¢elds, and tobacco of four nights each jackal covered a mean of 33% (range and maize crops, occupies the remaining 20%. The study 23^41%) of the mean yearly territory. Over one night site is typical of commercial farmland around Harare. jackals covered a mean of 14% of the mean yearly and The main ecological study techniques were trapping 48% of the mean four-night territory. and radio-tracking. Jackals were trapped using humanely Over a 12-hour-night the average minimum distance modi¢ed leg-hold traps (Victor Soft-catch size 11 , Wood- 2 moved by each jackal was 10.3Æ2.4 km (range 3.4^ stream Corporation Inc., Lititz, Pennsylvania, USA), 31.7 km). This is the sum of straight line distances baited with putrid meat. Once caught, jackals were ¢tted between positions of the jackal at successive ¢xes. The with radio-collars operating at a frequency of 173 MHz actual distance travelled will be somewhat greater than (Biotrack, Wareham, Dorset, UK). A total of ten males this ¢gure suggests. Jackals travel approximately and nine females were trapped and intensively radio- 1.4Æ0.4 km h71, but can run at approximately 20 km h71 tracked from a four-wheel drive vehicle using a Mariner (R. P. D. Atkinson, personal observation). Radar M57 receiver, and a hand-held directional four- element Yagi aerial. A radio-¢x was taken every 10 min (d) Population density and the jackals' positions were located on a map of the The jackal population size and the structure of the study study site overlaid by a grid. Each jackal was tracked for area were estimated using intensive trapping, radio- 8 h a night for three nights, and all night (12 h) for one tracking and night-time sightings. The population of resi- night, after which we started a four-night tracking session dent, territory-holding adults was estimated to be 20^ on the next jackal. A total of four nights was su¤cient to 30 100 km2. The total jackal population of the study identify at least 80% of the area currently in use, by the area was estimated at 60^90 jackals 100 km2 during the minimum convex polygon method (Stickel 1954). All- breeding season, giving a peak density of between 80 and night tracking was done to get complete pictures of total 120 jackals 100 km2 when helpers and itinerants are nightly distance travelled. On every ¢x, data were included. collected on the proximity of neighbouring radio-collared jackals to the focal jackal. In total, we radio-tracked jackals for over 1700 h and took over 10 000 radio-¢xes 3. A MODEL FOR JACKAL RABIES (R. P. D. Atkinson and D. W. Macdonald, unpublished Kingdon (1997) suggests the side-striped jackals occupy data). a similar ecological niche to red foxes in Europe, an obser- To obtain estimates of the demography of the study vation supported by our data and Atkinson's (1996), and population, records of all jackals seen were kept while like foxes they are susceptible to infection with the rabies radio-tracking, whether they were radio-collared or not. virus. Figure 1 shows the annual incidence of reported The age and group size of the jackals, and whether they cases of jackal rabies in Zimbabwe (Foggin 1988; were seen in or out of home ranges of known jackals, were Bingham 1992; Bingham 1995). recorded for this purpose. Jackals live in family groups that exist within territorial boundaries and juveniles disperse annually to establish (a) Birth rate new territories or take over the gaps left in the social The estimated birth rate is 5.4 pups per pair, born hierarchy by adult mortality.
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