© 2002 Mammal Society, Mammal Review, 32, 12–25

The role of the Badger (Meles meles) in rabies epizootiologyand the implications for Great Britain

G. C. SMITHCentral Science Laboratory, Sand Hutton, York YO41 1LZ, UK,E-mail: g.smith@csl.gov.uk, Tel: 01904 462056, Fax: 01904 462111

ABSTRACTThe occurrence of a wildlife rabies epizootic in Britain remains a very unlikely event, but itis important to examine all the possible consequences of such an event. Here, I examine thepossible role of the European Badger (Meles meles) in such an epizootic. The populationdensity of Badgers in Britain is much higher than that in Europe, and appears to haveincreased substantially over the last decade or so. The population parameters and epizooti-ology of rabies in the Badger are reviewed in comparison with the Fox (Vulpes vulpes) andother species. Mustelids appear to be very susceptible to rabies, with the smaller mustelidsbecoming aggressive, although Badgers do not appear to show heightened aggression wheninfected. Badger populations on the continent become severely reduced when rabies arrivesin the area, and circumstantial evidence strongly suggests that Badgers can easily transmitthe virus. Preliminary models support the idea that the Badger could be a very significantsecondary host, especially in the initial rabies outbreak. The population recovery rate of theBadger suggests that it is unlikely to become a primary host, although short-term epizooticsin the Badger population are likely. The potential for controlling rabies in the Badger is alsoexamined.

Keywords: Badger, disease control, Great Britain, Meles meles, rabies

INTRODUCTIONRabies is a fatal viral disease caused by an RNA Lyssavirus. The disease is maintained in anumber of different species, mostly mammalian carnivores, including Dogs Canis familiarisand Cats Felis catus. The most common form of disease transmission is by exposure to infec-tious saliva, either via wounds or, rarely, mucosal membranes (Krebs, Wilson & Childs, 1995).Following a variable incubation period ranging from a few days to several months (depen-dent upon the route of infection, viral strain, species infected and dose), symptoms occur foronly a few days and are followed by death (Baer, 1991). Such symptoms are generally char-acterized as ‘furious’, with overt aggressive behaviour, or ‘dumb’, with little aggression butincreasing paralysis. Virus is usually present in the saliva during the symptomatic period, andmay also be present for a number of days prior to the onset of any signs (Blancou, Aubert& Artois, 1991). The symptoms generally become progressively more severe, eventually result-ing in paralysis and death (George et al., 1980; Krebs et al., 1995). Radio-tracking studies ofinfected free-ranging Red Foxes (Vulpes vulpes) have shown that, during the last few daysbefore death, the animals may lose their sense of space and time, exhibiting activity at unusual

Mammal Rev. 2002, Volume 32, No. 1, 12–25. Printed in Great Britain.

Correspondence: G. C. Smith, Central Science Laboratory, Sand Hutton, York YO41 1LZ, UK (E-mail: g.smith@csl.gov.uk, Tel: 01904 462056, Fax: 01904 462111).

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times of day and being more likely to leave their territories temporarily (Andral et al., 1982;Artois & Aubert, 1985). It is this change in behaviour that is thought to be responsible forthe transmission of rabies between Fox social groups.

Rabies is usually regarded as having a single-species reservoir with spill-over to other dead-end hosts. Red Fox rabies occurs in Europe and on the Canada–US border (Blancou et al.,1991), Striped Skunk (Mephitis mephitis) rabies in the central United States and California(Charlton, Webster & Casey, 1991), and Raccoon (Procyon lotor) rabies along the easternseaboard States (Winkler & Jenkins, 1991). However, rabies virus has been isolated fromnumerous eutherian host species (Johnston & Beauregard, 1969; Wandeler et al., 1974b;Barnard, 1979) and limited investigations of marsupials have shown them also to be suscep-tible (Statham, 1992). In Europe during the current rabies enzootic, cases in animals otherthan Foxes have been reported to be proportional to the number of Fox cases, and disappearin parallel with, or shortly after, the disappearance of Fox rabies (Wandeler et al., 1974b)(Fig. 1). However, short secondary chains of infection have been noted in non-vector species.In North America three Foxes were reported dying of rabies, probably of bat origin (Daoust,Wandeler & Casey, 1996), and other cases of bat-induced rabies in terrestrial animals havealso been recorded, although rarely (Webster, Casey & Charlton, 1989). An analysis of 191cases of rabies in martens (mostly Stone Marten Martes foina) suggested that, due to theclose correlation between cases, short chains of infection may occur in martens for approxi-mately 3–4 months (Bögel, Schaal & Moegle, 1977). Rabid martens and Weasels (Mustelanivalis) are aggressive, but salivary titre of virus was lower than that recorded in either Foxesor Badgers (Meles meles) (Wandeler et al., 1974a; Förster, 1978), and this lower viral excre-tion may inhibit longer chains of infection. African mustelids are also known to carry rabies,and the Honey Badger (Mellivora capensis) is reported to be one of the most dangerous rabidanimals to deal with (Barnard, 1979).

In eastern Europe a new picture has emerged over the last decade with the spread of rabiesinfection in a different canid, the Raccoon Dog (Nyctereutes procyonoides). In 1988 an out-

Fig. 1. The reported cases of rabies in Foxes (open columns) and Badgers (solid columns) in selected countries in Europe.

break of rabies in Finland produced notified cases in 48 Raccoon Dogs (out of 228 submit-ted), 12 Red Foxes (out of 89 submitted) and two Badgers (out of 15 submitted) (Nyberget al., 1992), and in 1992 Raccoon Dogs accounted for 9% of all wildlife cases in Poland (Lis,1996). In more recent years the number of rabid Raccoon Dogs in Lithuania has oftenapproached half the number of rabid Fox cases (WHO, 1998–99). These data suggest thatFox rabies may be easily transmitted to some other species, and may possibly be transmittedamong these other species in some circumstances.

In the UK the Fox is widespread and abundant, and often occurs in urban areas (Harris& Rayner, 1986) which may account for over 10% of the national population (Harris et al.,1995). As a result, Fox rabies introduced into the UK would be likely to spread quickly if itwere not rapidly eradicated (Murray, Stanley & Brown, 1986; Smith & Harris, 1989). TheBadger is more patchily distributed across Britain, with areas of highest density in south-western parts of England (Cresswell, Harris & Jefferies, 1990; Wilson, Harris & McLaren,1997). It is also in southern England where rabies introduction is most likely (Harris et al.,1992). Although a rabies introduction to British wildlife remains very unlikely, it is impor-tant to examine the consequences of such an event in order to be in the best position to eradicate the outbreak. Computer models suggest that a wildlife rabies epizootic in Foxes inBritain can be controlled, but disease eradication may take many months (Smith, 1995). Thepossible involvement of the Badger in a British rabies outbreak has already been raised (Macdonald, 1995; Morgan, 1995). Because high Badger densities occur where the risk ofintroduced disease is highest, it is worth reviewing the factors that would contribute to theBadger being a possible rabies host, and methods of Badger control. Other problems with arabies epizootic in Britain, such as the role of domesticated companion animals, will not beconsidered, as many of these additional problems are not significantly different from thosein Europe.

COMPARATIVE POPULATION DYNAMICSFoxes are distributed in small family units with a variable but relatively high proportion offemales breeding (Lloyd et al., 1976; Harris, 1979; Lloyd, 1980; Harris & Smith, 1987).

One litter is produced each year, the average size being about 4.7 cubs (Lloyd et al., 1976;Harris & Smith, 1987) although some studies have reported mean litter sizes of up to eight (Englund, 1980; Voigt, Tinline & Broekhoven, 1985). Fox productivity has been esti-mated at 1.0–1.8 cubs per adult per year (Lloyd et al., 1976; Anderson et al., 1981), with apotential maximum of 2.3 per adult per year (assuming a litter size of 4.7 and a 50 :50 sex ratio) (Harris & Smith, 1987). The per capita annual mortality rate of the Fox can vary from 0.7 in urban populations (Harris & Smith, 1987) to between 0.56 and 1.1 in ruralpopulations (calculated from Lloyd, 1980). By using median figures for natality and mortal-ity, an average potential annual growth rate, r (natality – mortality), of about 0.6–0.7 is produced.

Badgers generally live in larger groups with more restricted breeding by females. Socialgroup size in one study in the UK was highly variable and had been recorded at up to 27individuals, although the average was only 8.8 (Rogers et al., 1997). The national averagesocial group size is about six adults (Kruuk & Parish, 1982; Cresswell et al., 1990) but on the continent group sizes of about three adults are commonly recorded (3.2 adults: van Wijngaarden & van de Peppel, 1964; 2.5 adults: Pelikán & Vackar, 1978; 3.7 adults: Wiertz,1993; 1.3–3.0 adults: Goszczynski & Skoczynska, 1996). Where an increase in Badger popu-lation size occurred in Poland, this was caused mostly by an increase in the number of groups,and not by an increase in average group size (Goszczynski & Skoczynska, 1996). In Britain

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up to four litters may be produced in a social group, but one litter is more common(Woodroffe & Macdonald, 1995; Smith et al., 2001).

Estimates of litter size in the Badger vary around three cubs born (3.2 cubs: van Wijngaarden & van de Peppel, 1964; 2.7 cubs: Neal & Cheeseman, 1996; three cubs:Goszczynski & Skoczynska, 1996). Thus the maximum breeding potential of Badgers, assum-ing a 50 :50 sex ratio and a litter size of three, is 1.5 per adult. Actual estimates of produc-tivity in Great Britain are much lower: 0.2–0.9 young per adult per year (Cheeseman et al.,1987; Cresswell et al., 1992; Rogers et al., 1997). With an estimated 3.7 adult Badgers persocial group and assuming an average of one litter of three cubs per group, the annual pro-ductivity in Britain would be 0.8 per adult. Assuming six adults per social group in Britainwould imply an annual productivity of 0.5 per adult. Annual Badger recruitment, as mea-sured in Poland, gave a figure of between 0.22 and 1.3 young per adult (Goszczynski &Skoczynska, 1996). These productivity figures are therefore about half that of the Fox. Percapita annual Badger mortality estimated from one long-term study is in the order of 0.5,including pre-capture mortality (Rogers et al., 1997; Wilkinson et al. 2000), which combineswith fecundity rates to give an annual growth rate of up to 0.3. Therefore Badger produc-tivity may be about half that of the Fox. This fits well with previous estimates of the intrin-sic growth rates (r) of the Fox and Badger at 0.5 and 0.2, respectively (Anderson et al., 1981;Anderson & Trewhella, 1985).

Fox density is relatively uniform over rural England, with numbers in the south-west beingapproximately 1–2 adults per km2 (Harris et al., 1995). However, local Badger density canreach more than 25 adults per km2 (Cheeseman et al., 1987), although numbers are usuallybetween 2.6 and 3.4 adults per km2 in the south-west (Thornton, 1988; Harris et al., 1995).At Woodchester Park, Gloucestershire, Badger density has more than doubled over the last15 years (Rogers et al., 1997) and a recent survey reported a significant increase in numbersthroughout Britain during this period (Wilson et al., 1997). Therefore, average Badger densitymay be at least double that of Foxes in south-west England, and may easily be five to 10times as high in some places.

The slower growth rate of Badgers will therefore mean that, following a rabies epizooticduring which many Badgers may die, the population will require a longer time period torecover to above the threshold carrying capacity, before a second epizootic can occur. Giventhe difference in the intrinsic growth rates between Badgers and Foxes we may expect thatsuch an interval will be about double that seen in Foxes: about 6–10 years if the rabies epizootic were sustained purely in a Badger population.

The social structure of Badger populations in the UK would also have an effect on diseasespread. Only brief contact (antagonistic biting or facial licking) may be required for rabiesspread, and this level of contact is likely to be very high within social groups. Radio-tracking has been used to calculate within- and between-group contact probabilities for the Fox (White & Harris, 1994; White, Harris & Smith, 1995; Baker & Harris 2000) but nocomparable data have been analysed for the Badger. This work has shown that, for Foxes,within-group contact rates are very high, particularly during winter. Between-group contactsare much less common, but radio-tracking suggested that the highest contact rates occurredin winter, and the frequency of bite wounding suggested that the maximum contact periodwas during winter and into spring (White & Harris, 1994; White et al., 1995). This highbetween-group contact rate in winter is probably primarily due to males seeking extra-territorial mating opportunities.

Given that Badgers in any territory may use a number of different setts, individual contactprobabilities may be slightly lower in Badger social groups than within groups of Foxes.

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However, as the number of Badgers in a social group is greater than the number of Foxes,the overall number of secondary infections within a social group may be at least as high inBadgers as in Foxes.

Spatial spread of rabies occurs by two means: neighbour-to-neighbour infection and inter-territorial movement (temporary or permanent dispersal) of infected animals. Both Foxesand Badgers are territorial at moderate to high densities, and interterritorial contacts arelikely to occur on a regular basis (although there will be seasonal differences). The greatestcontact rate should be during the mating season. For Foxes this is usually from January toFebruary (Lloyd, 1980), whereas for Badgers the peak for mating is post-partum in spring,although another smaller peak occurs in autumn (Cresswell et al., 1992).

Dispersal of Foxes is frequent, occurs generally between October and March and mostlyin subadults (Harris & Trewhella, 1988). Dispersal rates have been measured between 26%and 32% for subadult female Foxes and between 73% and 100% for subadult males (Mulder,1985; Harris & Trewhella, 1988), and dispersal distance is negatively related to populationdensity (Trewhella, Harris & MacAllister, 1988).

In undisturbed high-density Badger populations, annual dispersal rates have been calculated as 5–9% for males and 0.5–11% for females (Woodroffe, Macdonald & da Silva,1995; Rogers et al., 1998). These dispersal rates may be greater in low-density populations(Cheeseman et al., 1988; Christian, 1994; Woodroffe et al., 1995) but dispersal rates of similarmagnitude to those seen in the Fox have not been recorded. Males and females generallyappear to disperse similar distances, generally just one or two territories (Cheeseman et al.,1988; Rogers et al., 1998), although some evidence exists for a greater dispersal distance infemales (Woodroffe et al., 1995). Rogers et al. (1998) recorded that males (on a temporary orpermanent basis) are more likely to move between social groups than females.

We can therefore speculate that, given the reduced dispersal rates and distances seen inBadgers, geographical spread of the disease may be less rapid than that seen in Foxes,although behavioural changes resulting from the onset of clinical symptoms may adjust this.

THE EUROPEAN BADGER AS A RABIES HOSTIn any enzootic or large-scale epizootic, the number of infectious primary hosts will be large(over time and space for enzootic, localized for epizootic, situations). As a result of occa-sional interspecies infection, some animals of most species will become infected with the virus.In Europe, where the main reservoir is the Red Fox, which accounts for 89.6% of all wildlifecases, other infected species include the Badger (2.1%), other mustelids (2.7%), deer (4.3%)and other species (1.3%) (Blancou et al., 1991; WHO, 1978–99). Over a period of 11 yearsthe Badger accounted for 9.4% of all rabies cases in Italy (Civardi, 1991). Ahead of the rabiesfront Badgers accounted for 0.5% of the reported cases of rabies, and 2.3% behind the front(Bögel et al., 1976); in the final phase of the epizootic mustelids accounted for 9% of all cases,suggesting to the authors that short chains of rabies infection may have been occurring inmustelids (Moegle & Knorpp, 1978). During the start of the European epizootic at the begin-ning of the Second World War, numerous cases of rabies in Foxes and Badgers were detectedin Poland (Steck et al., 1968). Rabid Badgers are also not uncommon in areas with dog-mediated rabies (e.g. Jordan: Al-Qudah et al., 1997).

The Badger may be the second most frequently infected wildlife species (Artois et al., 1991),and rabies is considered to be a common cause of their mortality in some European coun-tries (Ruprecht, 1996). There is also likely to be under-reporting for a number of reasons.First, because the primary wildlife host of rabies in Europe is the Fox, people would be morelikely to submit Foxes for examination. Secondly, rabid Badgers may be less aggressive and

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more secretive than Foxes and thus less likely to be seen (Moegle & Knorpp, 1978). Thirdly,although truly urban Foxes are rare in Europe, suburban populations have been recorded ina number of cities (e.g. Warsaw: Goszczynski, 1979; Saarbrücken, Germany: Weber, 1982;Copenhagen and Århus: Nielsen, 1990) whereas urban or suburban Badger populations havenot been recorded as often (urban Badgers were recorded in Copenhagen before 1936 andare still found in the surrounding area but probably only about 60 or so animals: Aaris-Sørensen, 1987; Foxes, Badgers and Raccoon Dogs are reported to have declined in thesuburbs of Vilnius, Lithuania: Baranauskas, 1992). The greater proximity of Foxes to humansmust also increase their probability of being reported when rabid. Lastly, Foxes are a legiti-mate target for pest control and hunting, whereas Badgers are legally protected in an increas-ing number of European countries (Griffiths & Krystufek, 1993; Griffiths & Thomas, 1997).

In addition to a reporting bias, the low relative density of Badgers in Europe, comparedwith Foxes, is likely to result in fewer cases of rabies. Graf, Wandeler & Lüps (1996) demon-strated that the low density of Badgers in Switzerland (0.5 per km2) was not due to foodacting as a limiting factor, but they could not demonstrate whether rabies, or rabies control,was a limiting factor.

In an enzootic situation, Badgers have been recorded as constituting 4% of all wildliferabies cases (Wandeler et al., 1974b), and associated mortality may reduce the populationdensity by 90% (Schwierz & Wachendörfer, 1981) during an epizootic. Only Fox and Badgerpopulations appear to be substantially reduced by a rabies epizootic (Wandeler et al., 1988).Such a dramatic reduction in population density suggests that rabies may spread rapidlywithin the Badger population, at least locally, and such localized chains of infection havebeen observed occasionally in Europe (Wandeler et al., 1994). Moegle & Knorpp (1978)reported that Badger populations fall to about 10% of their initial density after the arrivalof a rabies epizootic, suggesting that the Badger population is more severely depressed thanthe Fox population. Wachendörfer & Schwierz (1980) showed that the Badger populationdensity, as measured by hunting returns, was reduced to at least 50% and in some cases aslow as 16% of the original size due to rabies; when gassing of dens was carried out to controlrabies the Badger population fell to a mean of 10% of the original size, and in some areasto below this level.

Sixty per cent of Badgers killed within a rabies enzootic area because of abnormal behav-iour were found to be rabid, and the rabies virus was isolated from 44% of all Badgers founddead (Wandeler et al., 1974b). These figures are suggestive of a localized epizootic outbreakin the Badger population, as disease prevalence in secondary, incidental, hosts would beexpected to be very low. Between 1952 and 1970 the hunting bag for Badgers in Hesse,Germany, decreased from 0.1 to 0.004 animals shot per km2, whereas the numbers of othermustelids killed actually increased (Wandeler et al., 1974b). This reduction in the hunting bagalso suggests that some intraspecific transmission to Badgers may have occurred, althoughrabies control measures are also responsible for killing Badgers.

Steck & Wandeler (1980) reported that, in Switzerland between 1967 and 1978, 77% of allrabies cases were in the Fox and 4.2% in the Badger. In the first 6 months of the Swiss epi-zootic, Badgers constituted 2.7% of cases (and Foxes 89.0%), whereas in the last 6 monthsthey constituted 6.7% (and Foxes 66.2%). Local clusters of rabies were seen in the Badger,but not in other wild species, both in front and behind the rabies front wave, thus ‘suggest-ing short chains of infection among this species’ (Steck & Wandeler, 1980).

Data compiled from the quarterly issues of Rabies Bulletin Europe (WHO, 1978–99) showthat the annual peak of cases in Foxes occurs during the first quarter of the year (Fig. 2). InBadgers the peak is during the second quarter. This delay could be due to the increased level

of interspecific infection from Foxes during the first quarter, followed by the incubationperiod in Badgers. Alternatively, the increased activity of Badgers during post-partumoestrous and consequent enhanced transmission of rabies may account for this peak. Rabiesinfection in other mustelids shows less seasonal variation, with peak numbers of cases beingreported in the third quarter.

In an account of the status of the Badger across Europe (Griffiths & Thomas, 1997), manycountries reported a marked decline in numbers due to rabies and its control (Badgers wereoften targeted during lethal control strategies). Evidence of digging for Foxes to control rabieswas found at 12% of Badger setts visited in the Netherlands (van Wijngaarden & van dePeppel, 1964). In the Federal State of Hesse, rabies reduced the Badger population by anaverage of 50%, and up to 84% in some areas. Further reduction occurred following gassingof Fox earths (Schwierz & Wachendörfer, 1981). There is now evidence in some countries ofan increase in Badger numbers following the cessation of lethal control and the reduction ofrabies incidence (Griffiths & Thomas, 1997). Hunting records from west Germany showed ahunting bag of 21000 in 1959–60, when rabies began to spread into west Germany, followedby a decrease of an order of magnitude during the 1960s and 1970s, and a steady increaseto 18 500 in 1991–92 (Griffiths & Thomas, 1997). Such an increase in the hunting bag hasalso been reported elsewhere (Guthörl, 1990). The increase in numbers of Badgers caughtalso coincides with the wide-scale use of vaccines to control rabies in Foxes.

Wachendörfer & Frost (1992) reported that, of 254 cases of post-exposure treatment ofrabies in humans in Switzerland, cats were responsible for 75%, Foxes 12% and mustelids11%. Moegle & Knorpp (1978) reported that of 101 rabid Badgers, only three were reportedto be aggressive to humans, whereas of 200 rabid martens, 40 cases of aggressive behaviourtowards humans occurred. It is likely, therefore, that only a small number of the mustelid-induced post-exposure cases in humans would have been due to Badgers. George et al. (1980)reported that 43% of rabid Foxes became aggressive and 11% exhibited the furious phase ofthe disease. The Badger is reported to lose its fear of people and not seek to return to its settwhen disturbed, to become aggressive and attack cows, dogs and people, and to make fre-quent loud calls (Sykes-Andral, 1982). Thus, even given equal number of rabid Foxes andBadgers, human contact is still much more likely with Foxes.

THE BADGER AS A POTENTIAL RABIES VECTOR IN THE UKFox density in England averages about 1.5 adults per km2 (Harris et al., 1995). On the conti-nent, Fox density has been estimated at 0.43–1.8 adults per km2 (Bögel et al., 1974; Lloydet al., 1976; Goszczynski, 1989). Therefore British Fox density may be up to three times that

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Fig. 2. The seasonal incidence ofrabies cases in Foxes (opencolumns), Badgers (solid columns)and other mustelids (hatchedcolumns) in Europe, as reportedby the WHO.

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seen in Europe. Average Badger density throughout England is estimated at 1.5 adults per km2 (Harris et al., 1995), while estimates in many continental countries are in the orderof 0.1–0.99 per km2 (Griffiths & Thomas, 1993). Thus English Badger density averagesbetween two and 10 times that seen in Europe, but locally may be more than 20 times as dense.

The hunting index suggests that European Fox density may have doubled during the declineof enzootic rabies (Müller, 1995), therefore the average Fox population density during therabies enzootic should be about half that seen in Britain. This would suggest that enzooticrabies in England may result in 3–10% of wildlife cases occurring in the Badger, all otherthings being equal (up to five times the frequency seen on the continent), and during the epi-zootic phase Badgers may therefore constitute up to 20% of cases.

Successful infection of a new wildlife species by the rabies virus depends upon five steps.The first step is an initial infection. Given the percentage of rabid Badgers reported on thecontinent, initial infection rates are likely to be significant. The rate of interspecific diseasetransfer could be in the order of 1% in continental Europe, in comparison to the rate ofspread in Foxes; thus for every 100 Fox-to-Fox infections there would be one Fox-to-Badgerinfection. This figure is purely an educated guess, as either detailed field studies or modellingof comparative infection in both species would be required to get an estimate in the rightorder of magnitude. If this figure were much higher, we would expect to see frequent localextinction of the Badger, and if very much lower many local populations would have escapedthe effects of rabies. In the UK such interspecific spread should be no more than 5–10%,given the higher Badger density.

The second step for successful infection of the Badger as a reservoir host is the suscepti-bility of the animals to infection. There appear to be no direct laboratory experiments onBadger susceptibility, but given the high population depression of Badgers in Europe, andthe frequency of reporting rabid Badgers, we can assume that susceptibility is relatively high:perhaps of a similar magnitude to that seen in the Fox. This is unusual, as for vulpine rabiesother carnivores (e.g. cats and dogs) may be up to 106 times more resistant (Blancou & Aubert,1997), although Red and Gray Foxes (Urocyon cinereoargenteus) appear to be equally sus-ceptible to rabies (Bell & Moore, 1971). Also supporting the possibility of the Badger beingvery susceptible to Fox rabies is the fact that other mustelids are known to be very suscepti-ble to rabies infection. The Weasel can produce a virus titre in saliva similar to that in theFox after a few passages, although the originally lower virus titre, combined with a shortperiod of virus excretion, may explain the lack of a secondary rabies epizootic in this species(Förster, 1978).

The third step required for the maintenance of rabies infection in the Badger populationis successful excretion of rabies virus from the salivary glands of the host. Data from 759rabid Foxes and 68 rabid Badgers showed that 93% of Foxes and 83% of Badgers show infec-tion of the salivary gland, whereas in the Stone Marten, another commonly infected mustelid,only 50% show salivary infection (Wandeler et al., 1974a).

There is some limited evidence that susceptibility is linked to virus excretion. Thus a speciesthat demonstrates a high virus titre in the salivary glands may be assumed to be quite sus-ceptible to rabies when compared with a species that does not produce much virus in saliva.For example, the domestic Cat requires a very high virus inoculation to succumb to rabies,and tends to exhibit no salivary excretion or a reduced level of excretion of virus (Artoiset al., 1984).

The fourth step is a sufficiently high titre of virus excretion. Salivary gland tissue has ahigh titre of virus in Foxes (103.4 MLD50; MLD50 is the dose required to kill 50% of infectedmice) and is even higher in Badgers (103.5 MLD50), but is significantly lower in Stone Martens

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(101.5 MLD50) (Wandeler et al., 1974a). The above two facts together suggest that viral excre-tion in Badgers is 112% that seen in Foxes (excretion ¥ titre).

Finally, for infection to persist in the population, the average contact rate between sus-ceptible and infectious animals must be greater than unity. This is undoubtedly true withinBadger social groups, which tend to be larger than social groups of Foxes. Between-groupspread may also be greater than unity in the Badger, but may be relatively low given the appar-ent secretive nature of rabid Badgers. An additional complicating factor is the probableincreased interterritorial movement rate when a large proportion of the population isremoved during a disease epidemic. Such a factor has been hypothesized for Badger popu-lations that are artificially reduced by culling (Swinton et al., 1997), and this may lead to anincreased contact rate between infected animals.

MODELLING RABIES IN THE BADGERA number of models have been produced to examine the spread of rabies in Foxes (Anderson et al., 1981; Murray et al., 1986; Smith & Harris, 1989; Smith & Harris, 1991;Smith, 1995; Artois, Langlais & Suppo, 1997; Thulke et al., 1997) and a number of modelshave been produced to examine disease spread (bovine tuberculosis) in Badger populations(Anderson & Trewhella, 1985; Bentil & Murray, 1993; Ruxton, 1996; Smith, Cheeseman &Clifton-Hadley, 1997). Rhodes et al. (1998) used a simple single-species model of rabies inthe Side-striped Jackal (Canis adustus), but with the addition of an input variable for the fre-quency of contact with rabid domestic dogs. This input is necessary to prevent rabies preva-lence from dropping below the threshold density for the disease to persist in the Jackal. Thisdemonstrated that the Side-striped Jackal was not a primary rabies host, but that an enzooticof rabies in dogs was necessary for the disease to survive. This is the only published modelof a rabies epizootic in a secondary wildlife host; models of Badgers as hosts for rabies havenot been produced. It is therefore necessary to construct a simple two-species model (Foxesand Badgers) to examine the potential consequences of a rabies outbreak on the British mainland.

A preliminary non-spatial differential equation model was written (G.C. Smith, unpub-lished data) in STELLA (High Performance Systems Inc., Hanover, New Hampshire, USA)that combined the population parameters of a Fox–rabies model (Anderson et al., 1981) anda Badger model (Anderson & Trewhella, 1985). This model assumes that Badger productiv-ity is lower than that of Foxes, and that Badgers are equally effective in transmitting thedisease. The model predicts that in the initial outbreak the Fox and Badger populations areboth depressed by a similar amount. If the transmission from Fox to Badger is very low (<1%of Fox–Fox rates) then the Badger maintains a low level of endemic disease: a classical sec-ondary host. As the relative interspecies transmission increases, then the slower recovery ofthe Badger leads to outbreaks with a periodicity of about two times the cycle length seen in the Fox. If the interspecies transmission is increased to about 10% of the Fox–Fox rate,then the Badger cycle length follows that of the more dominant Fox cycle. However, duringthe initial epizootic phase the actual number of rabid Badgers is very similar to the numberof rabid Foxes, assuming both populations are at roughly equal densities. This modellingapproach will be examined in detail elsewhere.

RABIES CONTROL IN THE BADGERIn the UK, current contingency plans for rabies control policy involve the distribution ofpoison baits to kill Foxes in an area up to a 19-km radius around any focal incident (Harriset al., 1992), and rabies vaccine may be distributed in a ring around this (Smith, 1995). Given

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the potentially reduced rate of spread of rabies in the Badger population, if any lethal controlis instigated it may be required over a smaller area. The control of rabies in the Badger doesnot have to mirror the strategy for Fox control, because Badger setts can be targeted directly.

In a captive study of six Badgers, vaccinated with the ERA recombinant rabies vaccine,half subsequently died following challenge (Brochier et al., 1989). During a 6-month fieldtrial of the Tubingen Fox baits, containing SAD-B19 rabies vaccine, only 13% of 16 Badgers(compared with 66% of Foxes) were judged to have sufficient antibodies to have serocon-verted (Nyberg et al., 1992). Guittre, Artois & Flamand (1992) orally vaccinated threeBadgers with the SAG1 avirulent rabies vaccine and all three survived challenge. Masson et al.(1996) orally vaccinated five Badgers with the SAG2 vaccine, and antibody titre suggestedthat three might have been able to resist challenge against rabies. Studies have demonstratedthat three commonly used rabies vaccines had similar efficiencies in protecting Foxes againstrabies (Artois et al., 1993), so it may be unlikely that a different rabies vaccine can be foundthat is more effective in the Badger unless specifically prepared.

These studies suggest that perhaps only half of all Badgers that consume vaccine baits willbecome immunized. There is some evidence for a low level of bait uptake by Badgers (7–33%),when the baits are presented in the manner prescribed for Fox control during a rabies outbreak (G.C. Smith, unpublished data). If this level of bait uptake occurred during theabove field trial, and only about half of all Badgers consuming bait seroconverted, then wewould expect 16–17% of all Badgers to be able to resist rabies. This is very similar to the 13%seroconversion rate found by Nyberg et al. (1992).

Although Badgers, and other non-target species, may consume poisonous baits designedfor the Fox, specific targeting of Badgers during a rabies outbreak may be needed under somecircumstances. Such specific targeting would increase the proportion of Badgers that takebait. Additionally, fast-acting poison would prohibit bait monopolization by a few animals,and would thus increase the proportion consuming bait. The limitation of vaccination as ameans to reduce rabies in the Badger population strongly suggests that direct culling may berequired in the event of a wildlife rabies outbreak in areas of high Badger density. As bothculling and vaccination are likely to be performed by using baits, more work is required toinvestigate methods to improve bait uptake in Badgers, and further modelling is required inorder to help predict the spatial spread and ability to control rabies in a two-species outbreak.However, it must be remembered that the chance of a wildlife rabies introduction in Britainremains very low, and that the involvement of the Badger would only be short term.

ACKNOWLEDGEMENTSI would like to thank Jan Whitby for providing me with her original review, and RichardDelahay, Chris Cheeseman and an anonymous referee for commenting on an earlier draft.

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Submitted 28 March 2000; returned for revision 20 December 2000; revision accepted 26 January 2001