Rabies in African Wild Dogs (Lycaon pictus) in the Madikwe Game Reserve

M. Hofmeyr, J. Bingham, E. P. Lane, A. Ide, and L. Nel

Madikwe Game Reserve, North West Parks Board, PO Box 4124, Rustenburg 0300, South Africa (Hofmeyr); Rabies Unit, Onderstepoort Veterinary Institute, Private Bag X5, Onderstepoort 0110, South Africa (Bingham); Department of Pathology, Faculty of Veterinary Science, University of Pretoria, Private Bag X4, Onderstepoort 0110, South Africa (Lane and Ide); and Department of Microbiology and Plant Pathology, Biological and Agricultural Sciences, University of Pretoria, Pretoria 0002, South Africa (Nel)

Key Words: African wild dog, Lycaon pictus, Rabies

Introduction

The African wild dog (Lycaon pictus) is an endangered canid species, which formerly occupied most of the non-forested areas of sub-Saharan Africa. Currently, this species occurs only in localised areas of this range. ¹² African wild dogs are nomadic, highly social canids and form packs of up to 28 individuals with an average of around 8 - 12 members. ^3,9 The main prey consists of antelope, which they mostly hunt down co-operatively. Packs are strictly hierarchical, each with a dominant (alpha) male and female. Usually only the alpha individuals breed, although the other members help to raise the young by bringing them food and by defending them. The average litter sizes is 7 - 10, although up to 19 may be born. ¹²

The distribution and numbers of wild dogs recently have declined drastically for unknown reasons. However, habitat loss, conflict with man and persecution, competition with other carnivores, road kills, loss of genetic diversity and infectious disease may be involved. ⁶ Of the latter, rabies and canine distemper have been reported to cause high mortality in free ranging packs of wild dogs. Rabies decimated packs in the Serengeti, Tanzania⁷ and the Masai Mara, Kenya⁸ and was thought to have contributed to the extinction of wild dogs in these areas. ⁵ Canine distemper eliminated a pack of 12 wild dogs from the Chobe National Park, Botswana in 1994. ¹ This presentation describes a rabies outbreak in a wild dog pack in Madikwe Game Reserve in the Northwestern Province of South Africa and the attempts to control it.

Case Report

Three wild caught, adult, male and three captive-bred adult female wild dogs were translocated to Madikwe Game Reserve in 1994 and in 1995, respectively. The dogs formed a coherent free-living pack, successfully breeding in 1996 and again in July 1997 so that in September 1997 there were six adults (three males and three females), six yearlings, and 12 pups. The males were vaccinated for rabies at the time of capture by a single intramuscular dose of vaccine (Dec 1994). Radio collars were attached to some of the dogs at, or soon after, the time of their release. At no time did the dogs attempt to break out of the reserve, which is bounded by an electric fence.

The first unusual sign, on 14 September 1997, was a change of the pack's male status and the absence of the old alpha male. However, his radio signal could be detected in the vicinity of their den and it was presumed he was inside. By 20 September the pack, without the old alpha male, had left the den and the following day his body, too decomposed for pathological examination, was retrieved from the den. On 24 September one of the yearling females killed all twelve pups, eating three of them. Over the following 21 days this yearling female and six of the remaining dogs died or were euthanased in extremis following observed periods of illness. Only three of the dogs, all yearlings, have survived to date.

All observed affected dogs showed disorientation, lethargy, and ataxia. In addition, inappetance, unusual wariness of vehicles, progressive paralysis, and terminal flaccid paralysis were noted. The period between onset of signs and death varied between one and six days. Aggression was noticed in only two dogs. The first yearling to be affected actively sought and killed all the pups, although no aggression was displayed towards the other pack members. The third-ranking adult female became unusually bold and eventually challenged the alpha female's status. She showed intermittent aggression towards the other dogs, which elicited retaliation.

Macroscopic lesions were not present on full necropsy of two dogs. Rabies was confirmed in the three adult females and two subadults by the fluorescent antibody test on brain material. Rabies virus was isolated from salivary gland in one of four of these cases, where salivary gland suspension was tested by intracerebral inoculation into three-week-old mice. Formalin-fixed salivary gland from the fifth case contained immunoperoxidase-stained rabies antigen. Carcasses of the two remaining adult males were not retrieved and a diagnosis of rabies was made on clinical signs only. Sections of the brains of ten of the pups killed by the affected yearling lacked rabies antigen on immunoperoxidase staining.

Immediately after the loss of the pups, the dogs no longer showed any inclination to hunt. They appeared depressed and lethargic. As it was thought that this was due to lack of food, they were fed with impala carcasses.

During October and November 1997 six jackals (Canis mesomelas) exhibiting abnormal behaviour were reported within the pack’s home range. One was confirmed rabid by the fluorescent antibody test on brain material. Other vector species were not reported with rabies in the Madikwe area before the outbreak in the wild dogs.

On the first of October, immediately after rabies was diagnosed, the surviving seven dogs were confined in a 1ha holding boma at Madikwe for observation and vaccinated with inactivated rabies vaccine at the dose of one ml given IM in the Biceps femurus during immobilsation with zolitol and xylazine. Despite vaccination, three dogs died of rabies 16 – 21 days after they were placed in the boma. One yearling died during immobilisation and was diagnosed negative for rabies. Two of the three surviving dogs were released back into the wild after 10 months. The third dog was successfully integrated into another breeding program at another site.

The three survivors were vaccinated at intervals and their serum tested in cell culture for neutralising antibodies. ⁴ Antibody titres were present soon after the primary vaccination but declined despite booster vaccinations (Table 2). This phenomenon is worth further investigation and may indicate why the adult males and other wild dogs^2,8 were susceptible to rabies despite having been vaccinated.

The rabies viruses obtained from the wild dogs were compared with typical South African rabies virus isolates from Canidae from various geographic locations, Pasteur virus,¹³ and a typical rabies virus isolate of the biotype associated with hosts belonging to the Viverridae family. The phylogeny was based on the sequencing and alignment of an 850 nt region of the virus genomes, which included the G-L intergenic domain. ¹⁰ A phylogenetic tree subsequently was constructed by the neighbour-joining method. ¹¹ Nucleic acid sequence comparisons demonstrated that the jackal isolate and those obtained from the wild dogs were virtually identical and clearly distinguished from other typical South African canid rabies virus isolates. Cumulatively, our results strongly suggest that jackals are the principle host species of the rabies cycle and transmitted the infection to the to the wild dog pack. Our supposition is that the alpha male brought the infection into the pack, considering that he was the first to die.

It has been argued that intervention during an outbreak may have increased the susceptibility of the wild dogs to rabies infection. ² In this outbreak, vaccination probably saved three of the dogs. Table 1 strongly suggests that the dogs, which died following vaccination, did not shed virus, while those that died before vaccination had virus in the salivary glands. Therefore, vaccination may have reduced or eliminated virus shedding from uninfected animals, thus reducing the risk of infection to other members of the pack. It was felt that euthanasia of affected dogs was important in prevention of excessive contact of healthy dogs with infected ones. The alternative possibilities of early isolation of affected dogs was rejected on the grounds that it would cause unnecessary stress, which could mask clinical signs and interfere with monitoring. We feel that rapid and effective intervention in an infected pack is important in preventing dissemination of the disease to all members in the pack.

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