by Barbara Maas*
Disease can be a powerful force affecting the sex and
age structure
of animal populations. This report examines the impact of rabies on
bat-eared fox
groups in the Serengeti National Park.
Bat-eared foxes (Otocyon megalotis) are comparatively small nocturnal canids, which live in two disjunct populations in the eastern and southern parts of Africa (Figure 1 [coming soon!]). Their head, back and the upper part of their legs are a grizzly grey, while their chest and the underside of their body vary from a light buff to a rich honey tone. Other parts of the animal's body, such as the backs of the ears, the lower parts of the legs, the upper side of the tail, as well as a raccoon-like "face-mask" are black, and it is these parts which are most easily visible at night. As suggested by their name, the most outstanding physical features of bat-eared foxes are their phenomenally out-sized ears. These can measure up to 13cm in an animal which stands to an average shoulder height of 30 cm (Kingdon, 1977; Smithers, 1983).
Bat-eared foxes are the only species in the genus Otocyon. The species is set apart from the rest of the Canidae on the basis of several morphological characteristics associated primarily with its dentition. Firstly, bat-eared foxes have between one and four pairs of extra molars, as a result of which they have more teeth than any other heterodont placental mammal (Sclater, 1900). Secondly, a modification of the insertion point of the digastric muscle allows the animals to open and close their jaws up to five times per second.
Although the ears of bat-eared foxes may also serve a thermoregulatory function, their main purpose, like that of the anatomical features described above, seems to lie in facilitating effective prey detection. Bat-eared foxes, to a greater extent than other canids, have virtually given up preying on vertebrates and feed on insects (Nel, 1978; Berry, 1980; Smithers, 1983). Sharp hearing and rapid movement are vital in prey capture. In parts of the southern African population, where wild fruit and berries are available, these may also form a substantial part of the species' diet (Smithers, 1983; Kuntzsch & Nel, 1992).
In the Serengeti, as well as in many parts of southern Africa, Hodotermes mossambicus (a relatively large harvester termite) and dung beetles constitute the most important sources of food for bat-eared foxes (Nel, 1978; Lamprecht, 1979; Malcolm, 1986; Maas, 1993). In my study area both termites and dung beetles were more abundant in areas inhabited by bat-eared foxes than those which were not, and local differences in Hodotermes foraging density were inversely proportional to territory size. Furthermore, Hodotermes foraging hole density was also positively correlated with a variety of demographic and reproductive variables, such as litter size and female recruitment rate (Maas, 1993). One of the main consequences of this unorthodox diet is that in contrast to animals which feed on larger prey, the collection of a sufficient quantity of very small food items is directly dependent on available foraging time. This relationship is intensified during nutritional bottlenecks, which can occur as a result of a reduction in availability (e.g. a drought), an increase in physiological requirements (e.g. during reproduction) or a combination of both.
Rabies occurs in all parts of the African continent. Although the domestic dog is most frequently associated with the transmission and maintenance of rabies in African countries, the number of wildlife cases too is likely to be high. However, reliable information on rabies in African wildlife is scarce, not least because of the enormous practical difficulties associated with effective monitoring. The first documented rabies cases in Tanzania were reported in 1932/33 (see Rweyemamu et al., 1973), but rabies had not been confirmed in the Serengeti National Park until 1986 (Maas, 1993). However, prior to this date there were anecdotal accounts of disease-related mortality in wild dogs (Lycaon pictus) (Schaller, 1972; Malcolm, 1979). Even before that time, Leaky (1969) attributed large fluctuations in the number of bat-eared foxes near his camp to periodic outbreaks of disease. So far wild dogs and bat-eared foxes continue to be the only Serengeti carnivores for which rabies has been confirmed in the laboratory (Gascoyne et al., in press; Maas, 1993). The problem of disease related mortality in Serengeti carnivores is further complicated by the recent occurrence of distemper in the Kenyan Massai Mara Game Reserve (K.Alexander, pers. com.), which is situated to the north of the Park and is part of the same ecosystem. Without laboratory confirmation the clinical symptoms of canine distemper and canine hepatitis are difficult to distinguish from those caused by rabies infections (Macdonald, 1980) and it is thus possible that the problem is even more complex than it appears at first. Certainly, a disease like rabies in the fragile Serengeti ecosystem raises perplexing conservation problems (Macdonald, in press).
Between 1986 and 1989, 90% (N=94) of the mortality suffered by a population of known individual bat-eared foxes was caused by disease (Figure 3). In contrast, the proportion of foxes which were killed by predation or road accidents was negligible (6%). During the four years of the study, two separate disease outbreaks affected the population, the first in 1987 and the second in 1988. The outbreaks were short, lasting for approximately seven weeks in 1987 and five weeks in 1988. All animals submitted for post mortem analysis were diagnosed as rabid. Although only three post mortem examinations could be carried out, it was assumed that animals which disappeared shortly after they had been observed to show clinical symptoms had died of the same cause. The majority of infected animals developed the paralytic form of the disease and did not show any furious symptoms. Instead, an initial stiffness and lack of coordination in the animals' hind limbs progressively developed into complete ataxia. At the same time, the sick foxes grew increasingly weak and sometimes suffered violent convulsions and cramp-like seizures, which affected their entire body and during which they frequently cried out. Other symptoms included conjunctival and scleral congestion, accompanied by varying degrees of discharge from the eyes. However, increased salivation was not observed. Some individuals developed an almost "obsessive" tendency to pick up food items and carry them around in their jaws. Infected foxes soon became too weak to forage and usually died within a week of the onset of clinical symptoms. Animals which showed signs of restlessness were actively avoided by other group members and although this was true also for several animals suffering the terminal stages of paralytic rabies, others received increased amounts of grooming and contact behaviour.
Looking at the study population as a whole, it was found that approximately 20% of all males and cubs (N=19 and N=234 respectively) and about 60% of all females (N=48) were affected by the disease. Furthermore, mortality data presented in Figure 3 show that during the four years of the study, rabies was the major cause of death in both adult and juvenile bat-eared foxes. However, a comparison of proportional adult mortality revealed that in both years the proportion of females which fell victim to the disease was significantly larger than the proportion of males. Further examination of the data showed that in both groups of adults fewer animals died during the 1987 outbreak than during that of the subsequent year. In contrast, the proportion of cubs which died from rabies was the same in both years. The data on male and female rabies-related mortality suggest that in years in which rabies outbreaks occurred, females were at least 11 times more likely to die from rabies than were males.
Although some continue to consider rabies an inevitably fatal disease, the outcome of rabies infections is believed to depend on factors such as virus strain and pathogenicity, dose of infection, host susceptibility and route of transmission (see Baer, 1991). Seropositive animals may be showing subclinical infections or seroconversion may occur in association with recovery from clinical rabies (Andral & Serie, 1957; Fekadu & Baer, 1980; Fekadu et al., 1981). Today ample evidence exists for physiological mechanisms (Martin, 1989) by which exposure to stressors can increase the susceptibility of individuals to infectious disease (Fowler, 1986; Workman & La Via, 1987; Jeppesen, 1988; Wemelsfelder, 1990, see Martin, 1989 for a review). There has also been accumulating evidence which indicates a possible link between immunocompetence and the susceptibility to rabies (Wiktor et al., 1980, quoted in King & Turner, 1992; Sriwanthana et al., 1989; Wandeler, 1991). In 1975, Winkler reported that stress and physical condition can influence the length of the incubation period in foxes. McLean (1975) stated that in raccoons, more females than males were found to have rabies serum neutralising antibodies. He continued to argue that in the same species, latent rabies infections may be reactivated by stress (see also Johnston & Beauregard, 1969), although this view has become increasingly disputed. Nevertheless, female bats are over-represented in rabies samples submitted for examination in the United States (C.Rupprecht, pers. com.), and it was found that in some ungulates, females experience a period of postpartum immunosuppression.
While the 1987 epidemic took place at a time when the cubs were almost fully grown, the 1988 outbreak reached the population in November, when females were in mid-lactation. Furthermore, rainfall in November and thus insect availability was exceptionally low in 1988. November usually marks the early part of the rainy season and brings with it a dramatic increase in insect availability. After four months of dry season during which food supplies became increasingly scarce, the animals are at a nutritional low, a fact which is reflected in their poor physical condition during this time of year. Thus, a delay in the onset of the rainy season signifies a nutritional dilemma at a time when, as a consequence of lactation and the cost of parental care, nutritional demands on adults are greatest. This is particularly relevant, since compared to other canids for which this information is available, the costs of lactation are high in bat-eared foxes (Maas, 1993). It is therefore possible that poor physical condition, aggravated by reduced availability of food and water was associated with higher mortality rates in lactating females in 1988. Restricted access to food, due to lack of rainfall would also affect male bat-eared foxes, and hence may explain the difference in male mortality rates between the two years. However, a judgement on whether greater susceptibility in females, and particularly lactating females, is related to differences in condition, or whether the observed differences are indeed related to the same phenomenon, must be postponed until information on the presence of rabies neutralising anti-bodies, physical condition and immune status are available.
Differences in exposure rather than susceptibility may provide an alternative explanation for the observed intra- and intersexual differences in disease-related mortality. It has been suggested that rabies is sometimes transmitted from one individual to another through social grooming. However, disease transmission through social grooming cannot explain the observed differences in male and female mortality rates, since in bat-eared foxes males are more active groomers than are females. Furthermore, both territorial and antipredator defence are almost exclusively performed by males, and intra- and intergroup aggression is rare in bat-eared foxes. Hence, increased exposure of females through intra- or interspecific antagonistic encounters is also an unlikely explanation for the observed phenomena.
However, rabies transmission from one female to another during communal suckling may provide a possible route of infection, since rabies transmission via maternal milk has been reported in other species (Constantine, 1967; Afshar, 1979). In family groups with more than one breeding female, females always suckle each other's cubs communally. Thus infected cubs may pass the disease on to other females through abrasions on the females' teats.
In most areas where rabies epidemics occur, one species is predominantly involved in maintaining the disease, while others - so called "spill-over species" - are less severely affected. In the Serengeti National Park rabies has so far been confirmed only in bat-eared foxes and wild dogs. The disease is also widespread among the domestic dog population which inhabits the surrounding areas (S.Gascoyne, pers. comm.). It is unlikely, however, that these three species will remain the only ones implicated in the transmission of rabies in the Serengeti ecosystem, once further studies get under way. Gascoyne's work, as well as the present study, emphasise the urgent need for more information on the scale of rabies infection in Serenegti carnivores. More information is necessary in order to identify the role which wildlife species and domestic animals play in the transmission and maintenance of rabies in the area, both in view of its conservation implications and in terms of minimising human exposure.
Andral, L. & Serie, C. 1957. Études experimentales sur la rage en Ethiopie. Ann. Inst. Past., 93: 475.
Baer, G.M. 1991. (ed.) The Natural History of Rabies. Second Edition.
Berry, M.P.S. 1980. Somach contents of bat-eared foxes, Otocyon megalotis, from the northern Transvaal. S. Afr. J. Wildl. Res., 11: 28-30.
Constantine, D.G. 1967. Rabies transmission by air in bats caves. U. S. Dept. Health, Education and Welfare, Public Health Service Publication, 1617: 1-51.
Fekadu, M. & Baer, G.M. 1980. Recovery from clinical rabies of 2 dogs with a rabies virus strain from Ethiopia. Am. J. Vet. Res., 41: 1632-1634.
Fekadu, M., Shaddock, J.H. & Baer, G.M. 1981. Intermittent excretion of rabies virus in the saliva of a dog two and six months after it had recovered from experimental rabies. Am. J. Trop. Med. Hyg., 30: 1113-1115.
Fowler, M.E. 1986. Stress. In: Zoo and Wild Animal Medicine (2nd edition), ed. by M. E. Fowler, Saunders, Philadelphia, pp. 34-35.
Gascoyne, S.C., Laurenson, M.K., Burrows, R., Lelo, S. & Borner, M. In press. Rabies in wild dogs (Lycaon pictus) in the Serengeti Ecosytem. J. Wildl. Dis.
Jeppesen, L.L. 1988. Stress in farmed fur animals. In: Proceedings of the International Congress on Applied Ethology in Farm Animals, Skara. Ed. by J. Unshelm, G. van Putten, K. Zeeb & I. Ekesbo, KTBL, Dalmstadt, Germany, pp. 89-94.
Johnston, D.H. & Beauregard,M. 1969. Rabies epidemiology in Ontario. Bull. Wildl. Dis. Assoc., 5: 357-370.
King, A.A. & Turner,G.S. 1993. Rabies - A Review. J. Comp. Pathol., 108: 1-39.
Kingdon, J. 1977. East African mammals. Vol. III A (Carnivores), Academic Press, London, pp.54-63.
Kuntzsch, V. & Nel, J.A.J. 1992. Diet of bat-eared foxes in the Karoo. Koedoe, 35: 37-48.
Lamprecht, J. 1978. The relationship between food competition and foraging group size in some larger carnivores: a hypothesis. Z. Tierpsychol., 46: 337-343.
Leaky, L.S.B. 1969. Animals of East Africa. National Geographic Society, Washington.
Maas, B. 1993. Behavioural Ecology and Social Organisation of the Bat-eared fox in the Serengeti National Park, Tanzania. Ph.D thesis, University of Cambridge.
Macdonald, D.W. 1980. Rabies in Wildlife; a biologist's perspective. Oxford University Press, Oxford.
Macdonald, D.W. In press. Rabies and wildlife: a conservation problem? Onderstepoort Journal of Veterinary Research.
Malcolm, J.R. 1979. Social organization and communal rearing of pups in African Wild dogs (Lycaon pictus). Ph. D. Thesis, Harvard University.
Malcolm, J. R. 1980 Social organiztion and communal rearing of pups in African wild dogs (Lycaon pictus). Ph. D. thesis, Harvard University, Cambridge, MA.
Martin, P. 1989. Psychoimmunology - relations between brain, behaviour and immune function. In: Whither Ethology?, Vol. 8 of Perspectives in Ethology, ed. by P. P. G. Bateson & P. H. Klopfer, Plenum Press, New York, pp. 173-214.
McLean, R.G. 1975. Racoon rabies. In: The Natural History of Rabies. Ed. by G. M. Baer, Academic Press, New York, pp. 53-77.
Nel, J.A.J. 1978. Notes on the food and foraging behaviour of the bat-eared fox, Otocyon megalotis. Bull. Carnegie Mus. Nat. Hist., 6: 132-137.
Rweyemamu, M.M., Loretu, K., Jacob, H & Gorton, E. 1973. Observations on rabies in Tanzania. Bull. Epizootic Diseases in Africa, 21: 99-102.
Schaller, G.B. 1972. The Serengeti lion: a study of predator-prey relations. University of Chicago Press, Chicago.
Sclater, W.L. 1900. The Fauna of South Africa. Vol. 1, R.H. Potter, London.
Smithers, R.H.N. 1983. The Mammals of the Southern African Subregion. Pretoria, pp. 403-409.
Sriwanthana, B., Hemachuda,T., Griffin,D.E., Manutsathit,S., Tweardy,D. & Phanuphak,P. 1989. Lymphocyte subsets in human encephalitic and paralytic rabies. Acta Neurol. Scand., 80: 287-289.
Wandeler, A.I. 1991. Oral immunization of wildlife. In: The Natural History of Rabies. 2nd edition. Ed. by G. M. Baer, pp. 485-501.
Wemelsfelder, F. 1990. Boredom and laboratory animal welfare. In: The Experimental Animal in Biomedical Research. Ed. by B. Rolin & M. L. Kesel, C. R. C. Press, Florida, pp. 244-272.
* Dr. Barbara Maas undertook this study as part of her doctoral thesis from the University of Cambridge. Currently she is a member of the Wildlife Conservation Research Unit at Oxford, where she is seeking funds for a postdoctoral study of rabies in small canids in the Serengeti.
© 1994 International Union for the Conservation of Nature and Natural Resources
Return to Canid News Table of Contents or CSG Home Page