(Note: this is
from the 1990 version the action plan
Click
here for the 2004 version of the
Canid Action Plan)
(from Foxes, Wolves, Jackals, and
Dogs,
the IUCN/SSC Canid Specialist Group's 1990 Action Plan)
Having considered two significant sources of mortality amongst canids, namely predator control and the fur harvest, it seems appropriate to mention that many canid populations are subject to serious outbreaks of disease. To date there is no complete review of the impact of diseases on canids worldwide, but there are sufficient snippets of information to suggest that disease may be an important factor in many populations, and may even regulate some (see, for example, the report of Hersteinsson's work on arctic foxes, Chapters 6 and 11). Reports vary from distemper in the bat-eared foxes of the Serengeti to leishmaniasis in the crab-eating zorro and hoary zorro of Brazil (Lainson et al. 1969). However, most notorious, probably most widespread, and certainly best studied is rabies.
Here, we will illustrate the potential importance of disease in canid conservation by reviewing briefly the example of rabies amongst red foxes in Europe. This example serves to emphasise two points: a) that there are substantial management problems concerning species which are not endangered and b) that modern techniques offer ecologically exciting solutions to wildlife disease problems.
The wild species implicated as vectors of rabies vary regionally, but worldwide the one mammalian family most commonly involved is the Canidae (Macdonald and Voigt 1985). There are at least occasional reports of most species of canid contracting rabies, and some members of the family are significant vectors, sometimes the major wildlife vector, in many regions. For example, golden jackals in north Africa, lndia, and, along with wolves, in the Middle East; black-backed jackals in parts of Southern Africa; arctic foxes in the far north, raccoon dogs in Eastern Europe and Asia; and red foxes throughout Europe and much of North America. Outbreaks of rabies have been implicated in losses of endangered species such as African wild dogs, and raise substantial fears concerning relict populations such as the Simien jackal [= Ethiopian wolf].
Rabies is a viral disease, generally transmitted when saliva is 'injected' into a susceptible animal that is bitten by an infectious one. Although all mammals can contract rabies, species differ in their susceptibility and in the symptoms they show. Raccoons and some mongooses, for example, are amongst those that can survive the disease and become immune. Red foxes, in contrast, are highly susceptible, and once infected have little or no chance of survival.
There are different strains of rabies virus, more or less specific to groups or species. For example, although cats are highly susceptible to the domestic dog's strain, they are not especially susceptible to the red fox strain. Foxes are very susceptible to their own strain, but not very susceptible to cat or dog strains. Except in Yugoslavia and Turkey, where the dog strain exists in wolves, Europe is swamped with the vulpine form. The existence of these strains of virus may explain many previously puzzling aspects of epidemiology. For example, this may explain why foxes in Denmark and the Netherlands remain free of rabies in regions where serotine bats are infected.
The history of rabies and its control in Europe illustrates important lessons for canid conservation. Rabies has come and gone in Europe throughout recorded history (whether it was dog or fox strain is generally unknown, although in Britain during recorded history rabies occurred almost exclusively in dogs). Coincident with the turmoil of the Second World War, the twentieth-century epidemic erupted in Poland and subsequently spread steadily across Europe in foxes. Since 1939, rabies has spread some 1,400 km westward, the front wave advancing between 20-60 km per annum (Toma and Andral 1977). On average, and with much variation, there has been an advance of about 4.8 km per month, interspersed with occasional leaps forward of up to 100 km (e.g. in 1982 in Yugoslavia, a focus erupted in Croatia, some 400 km ahead of the front wave). The toll has been fantastic. For instance, in 1982, 13,971 rabid red foxes were recorded in the 11 central European countries where sylvatic rabies predominates. Nobody knows what proportion of rabid foxes are reported, but it is likely to be very low; Braunschweig (1982) guessed that it would be between 2- 10%.
When rabies penetrates a new area, the foxes suffer an epizootic outbreak. With the fox population approximately decimated, the incidence of the disease dwindles and remains low during a 'silent' phase for two or three years. Thereafter, secondary peaks recur, often at intervals of 3-5 years following the first epizootic. Over a wide area, these cycles in reported case-incidence are out of phase with each other, giving the impression that the foci of enzootic rabies move around. Superimposed upon this inter-annual periodicity in the incidence of reported rabies is a seasonal pattern. There is a peak in cases in late winter, and a trough in mid-summer. There is similar seasonality in the monthly velocity with which the front line of the disease advances. In Germany, for instance, the spring increase in velocity is detected in February, whereas the incidence starts to increase about a month later (Bogel et al. 1976). Another pattern in the behaviour of the disease concerns its victims: in May-June, subadult foxes compose a smaller proportion of those reported dying from rabies than they do of those dying from other causes. In contrast, subadult males are disproportionately common in the sample dying from rabies in the autumn, whereas adult females are disproportionately common in such samples in spring.
Many of the characteristics of rabies epizootics can be interpreted in terms of fox biology (reviewed, for example, by Macdonald 1980 and Macdonald and Voigt 1985). Such links make it a priority to study the behaviour of those canids involved in rabies transmission, both in order to understand the behaviour of the disease, and to predict the consequences of attempts to manage it. For example, the behaviour of the disease in Europe can be related to the behaviour of foxes. The inter-annual periodicity of the disease reflects the population dynamics of the vector. After a fresh epizootic has swept through an area, some 60-80% of susceptible foxes will have perished. The result is that there are insufficient survivors to sustain the outbreak, which then peters out. Thereafter, the recurring enzootic waves of disease indicate that fox populations have recovered sufficiently to support further outbreaks. The late winter peak in incidence coincides with the social disruption and territorial incursions associated with the dispersal of subadults, competition for territories and the chaos of courtship. The disease front appears to chart a route through habitats characterised by high fox populations, probably spreading from one territory to the next during clashes between residents.
However, spread between neighboring foxes cannot be the whole story, because all else being equal it would lead to slower advance of the disease front where territories are smaller and populations generally larger, whereas, if anything, the opposite is the case. Some leaps forward by the disease may be caused by the minority of foxes showing the notorious "furious" form of rabies, in which berserk, fearless individuals travel aimlessly. However, these symptoms are rare in foxes (although quite common in dogs), and the rabid foxes studied in the wild have behaved rather normally until they were overtaken by terminal paralysis (Andral et al. 1982). The speed at which the disease spreads is probably much influenced by the footloose, adversarial lifestyle of itinerant foxes and the dispersal of cubs. Johnston and Beauregard (I 969) hypothesized that not only did the fox's behaviour in winter increase the likelihood of exposure to rabies, but also the stressed condition of dispersing subadults might further increase their susceptibility to infection (see also Artois and Aubert 1982).
The persistence of rabies, and the success of attempts to control it depend fundamentally on a measure known as the contact rate. The contact rate for a population is the average number of susceptible individuals infected by each diseased animal (see Bailey 1975). Contact rate is not constant, but a complicated function of the social organisation and density of the vectors, and thus of the frequency of meetings between them. Contact rate must be 1.0 or greater in order for rabies to remain enzootic (May 1983). It is straightforward to see that understanding rabies in canid populations demands an understanding of factors affecting contract rate. However in the stochastic world of complex animal populations, measurement of contact rate is notoriously difficult. This is largely because the frequency with which individuals meet, and hence the potential contact rate of the disease, is a reflection of their population density, social organisation, and their ecology.
Assuming that fox population density, and therefore perhaps contact rate, are determined partly by resource availability, various authors have sought to relate the behaviour of rabies to habitat charactersitics. The assumption is that habitat characteristics are correlated with the abundance of fox food (Macdonald et al. 1981). Although this approach is weakened by its inability to cope with cyclical variations in prey populations or, directly, with mortality pressures, it has shown some promise (e.g. Harris and Rayner 1986). For example, Jackson (1979) found that the velocity of the epizootic varied between land classes. Ross (1981) found a clear association between the velocity of the rabies epizootic in France and the presence of limestone bedrock. A plausible, but untested, explanation for associations of this sort is that the habitat features in question support high densities of foxes which have a high contact rate.
The intention of control policies for wildlife rabies is, ultimately, to reduce contact rate below 1.0, thereby breaking the chain of infection. Thus the traditional European approach has pivoted on the principle that the disease would die out if enough foxes could be killed so that numbers among the survivors were so low that the average infectious individual died before it infected a susceptible one. This policy has been pursued across Europe by armies of game and forest rangers, aided by hunters, who have both shot foxes and gassed them (pumping Cyclone B into their dens, or spooning in powder which gives off hydrocyanic gas). An important aim has been to reduce the numbers of infected foxes so that the threat to humans was reduced. Across Europe the numbers of foxes slaughtered annually in anti-rabies campaigns are unknown, but it must run into many thousands. Similar tolls have been commonplace amongst canids in many parts of the world. An often quoted but still poignant set of statistics is that summarising the arguably unsuccessful 1953 campaign in Alberta: in 18 months the approximate toll was 50,000 red foxes, 35,000 coyotes, 4,200 wolves, 7,500 lynx, 1,850 bears, 500 striped skunks and 164 cougars (Ballantyne and O'Donoghue 1954).
The starkly obvious question is whether the effort put into killing foxes in the attempt to eradicate rabies has succeeded. It has probably reduced the number of cases of rabid foxes somewhat, and temporarily reduced fox density (which rabies also does very swiftly). It may have protected man, but it has conspicuously failed to eradicate the disease, or even to slow its progress across Europe. One exception to this gloomy answer is the case of peninsular Denmark where, on three separate occasions, rabies has been eradicated within two breeding seasons by surprisingly rudimentary methods (gassing dens with stirrup pumps, supplemented in West Jutland by poisoning with strychnine at feeding sites) (Westergaard 1982). Of course, one would expect the great variation reported in canid behaviour and population densities from region to region to complicate the control of animals whose population dynamics are anyway rather resilient. One consequence of variation in fox population density between habitats is that baiting schemes may need to be adapted to widely different numbers of foxes (see Macdonald 1977, p. 89), and this requires a flexible stratagem which can be adjusted to local circumstances.
The high intrinsic rate of increase that typifies fox populations militates against attempts to reduce their numbers by killing them. The complicated nature of their social system weakens the argument that reducing fox numbers is likely to lead to a concommittant reduction in social contact amongst the survivors. For these reasons, some ecologists have argued that killing foxes was unlikely to reduce contact rate sufficiently, and for sufficiently long, to eradicate rabies, or even to control it very effectively (Macdonald 1987). The same ecological principles suggest that an alternative, oral vaccination, is more likely to succeed (Bacon 1985). The possibility of controlling rabies by vaccinating them against rabies became a serious possibility with the publication of preliminary results by Steck et al. in 1982. The idea is to vaccinate foxes against rabies, thereby reducing the number of susceptibles in the population not by killing them, but by making them immune. This approach also circumvents the possible counterproductive consequences of destabilising the foxes' social system. Considering the destabilising effects of killing schemes on fox society, Macdonald (1987) argues that the proportion of the fox population that must be killed to eradicate the disease is likely to be different from, and larger than, the proportion that must be immunized to achieve the same end. Furthermore, there is now mounting evidence that vaccination can be cheaper, and it is obviously more humane. Most compelling of all, it appears to work.
The first pilot studies were undertaken in Switzerland in 1978 and involved monitoring the progress of fox rabies up the arms of Y-shaped valleys. At the entrance to one arm of each Y, every effort was made to kill foxes, whereas at the entrance to the other arm of the valley, chickens' heads loaded with oral vaccine were scattered. The foxes ate the chickens' heads and inoculated themselves. Subsequently, rabies spread among the surviving foxes in the arm of the valley where others had been killed, but was stopped in tracks by the barrier of healthy, inoculated foxes (Steck et al. 1982).
Early misgivings about the risks of vaccine-induced rabies in non-target species arose because the vaccine used (SAD ERA) was a "live attenuated virus vaccine"--that is, a live rabies virus prepared so as to reduce greatly its virulence. These fears have largedly been quelled by the development of a safer, more efficient live vaccine (SAD-B19). Added to this, new possibilities have emerged: genetic engineering his produced what may turn out to an even better vaccine. A relatively innocuous virus called Vaccinia (the orthopox virus used in the eradication of smallpox) has its genetic composition manipulated to incorporate elements Of the rabies virus. The resulting "recombinant Vaccinia" has sufficient traits of the real rabies virus that, when eaten by foxes, it stimulates immunity to the disease (Blancou et al.1986). So far only preliminary trials have been completed in the field (in Belgium by Professor P.P. Pastoret) of the recombinant vaccine, but massive field trials have now been completed using the attenuated live virus vaccine. These trials, in Switzerland, West Germany, Italy, Austria, Luxembourg, Belgium, and France, have been impressively successful. Meanwhile, the search is on for other genetically engineered vaccines. Furthermore, other ideas may have a role.: Bacon and Macdonald (1980) proposed supplementing oral vaccination with baits containing birth control agents, thereby slowing the surge of unvaccinated recruits into the population every breeding season.
Kappeler et al. (1988) report that between 1978 and 1985 they distributed more than 600,000 SAD ERA vaccine baits throughout an area of 45,000 sq km in Switzerland. The result: aside from some inaccessible parts of the Jura Mountains, rabies has been virtually eliminated from Switzerland. Schneider and Cox (1988) similarly reported massive trials between 1983 and 1987 involving placement of more than five million vaccine baits over 60% of West Germany. The result was that 72% of foxes killed by hunters in those areas had eaten the baits and expressed antibodies against rabies-i.e. the baits gave protection from rabies to almost three quarters of the fox population. Not only has rabies almost disappeared from the vaccinated area of southern Germany (and persisted elsewhere, where traditional methods were employed), but not one case of vaccine-induced rabies was found there (three such cases occurred in Switzerland).
The advances in vaccine technology bring real prospects that oral vaccination of foxes will lead to the eradication of rabies as a disease of European wildlife within a decade. This offers significant lessons for canid conservation. Vaccination may offer a good solution to limiting rabies in other canids, including rare species; there are proposals, for example, to distribute oral vaccine against rabies to silver-backed jackals in Zimbabwe. Vaccination may also present prophylactic protection for rare species if an epidemic threatens; the precarious circumstances of Simien jackals and African wild dogs immediately come to mind.
| Canid Action Plan Table of Contents | CSG homepage | References |
© 1990 International Union for the Conservation of Nature and Natural Resources