Rabies and Wildlife Conservation in Africa
World Small Animal Veterinary Association World Congress Proceedings, 2014
Darryn Knobel1, BVSc, PhD; Paul Bessell2, PhD; Michael Grover3, BSc; Bjorn Reininghaus4, DVM
1Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa; 2Roslin Institute, University of Edinburgh, Easter Bush, UK; 3Activating Africa, Hoedspruit, South Africa; 4Mpumalanga Veterinary Services, Department of Agriculture, Rural Development and Land Administration, Thulamahashe, South Africa

Rabies is a fatal disease caused by infection with members of the Lyssavirus genus. These viruses are able to infect a broad range of species, and all mammals including humans are susceptible to the disease. This paper discusses the occurrence of rabies in wild mammal species in Africa, and its implications for their conservation.

The lyssaviruses can be broadly divided into rabies virus (RABV) and the rabies-related viruses. Five species of rabies-related viruses have been isolated from wildlife hosts in Africa: Lagos bat virus (LBV), Duvenhage virus (DUVV), Mokola virus (MOKV), Shimoni bat virus (SHIBV), and Ikoma lyssavirus (IKOV). Bats are the reservoir hosts for LBV, DUVV and SHIBV. These viruses have been isolated from sick and dead bats, and occasionally spill over to terrestrial wildlife hosts. Early isolates of MOKV were made from shrews (Crocidura spp.) and a rodent in western and central Africa, but more recent isolates have been exclusively from domestic animals (cats and dogs) in southern Africa.1 A single isolate of IKOV was obtained from the brain of an African civet (Civettictis civetta) with clinical rabies in the Serengeti National Park of Tanzania.2 Although knowledge of the ecology of rabies-related lyssaviruses in wild mammal hosts is almost certainly hindered by a lack of surveillance, there is no current evidence that these viruses have an impact on host populations in the wild.

Rabies virus in Africa circulates in terrestrial hosts and has not been associated with infections in bats. Although all mammals are susceptible to infection with RABV, certain species are capable of sustained intraspecies maintenance of particular viral variants adapted to those species. The existence of two distinct variants of RABV is well described in southern Africa. The mongoose variant is maintained in yellow mongooses (Cynictis penicillata). Although cross-species transmission to other wild as well as domestic hosts is not uncommon, there is no evidence of extended onward transmission in these other hosts.3 Molecular phylogenetics and anecdotal reports suggest that mongoose rabies has been present in South Africa since at least the early 1800s. In this time, there have been no published reports of rabies causing significant population declines in yellow mongooses. The other RABV variant in southern Africa is associated with members of the Canidae family, specifically domestic dogs, black-backed and side-striped jackals (Canis mesomelas and Canis adustus) and bat-eared foxes (Otocyon megalotis). There is evidence that jackals and bat-eared foxes are capable of maintaining circulation of this canid variant of RABV in specific geographic foci, independent of domestic dogs.4,5 Although not reported in South Africa, rabies outbreaks in bat-eared foxes have been associated with local population declines.6 As yet, there is no substantive evidence of rabies causing significant population declines in jackals. Although the effect of RABV on local populations of maintenance hosts may be concealed by a lack of surveillance in these populations, the general picture that emerges when one considers the ecology of rabies in wild mammal maintenance hosts in southern Africa is that the disease is not of significant concern to the persistence of populations.

Elsewhere in Africa, evidence for the existence of RABV variants adapted to particular wild host species is scant. A report of a divergent rabies virus causing asymptomatic infection and a carrier state in spotted hyaenas (Crocuta crocuta) in the Serengeti ecosystem in Tanzania7 remains to be substantiated through isolation and characterization of the purported variant. A unique scenario has emerged in Namibia, involving rabies among kudu (Tragelaphus strepsiceros), an herbivorous mammal. There is now clear evidence that a variant of RABV, originally introduced through spill-over of a canid variant, is being maintained independently in the Namibian kudu population.8 The initial epidemic of rabies in kudu, from 1977–1985, caused an estimated loss of 20 per cent of the population. Rabies in kudu may therefore be a concern for the conservation of that species in Namibia; however, kudu are abundant and it is believed that the population had attained an unprecedented density in the period prior to the epidemic, which may have contributed to horizontal transmission of the virus. The disease has remained endemic in the kudu population since, with a second, recent peak in cases in 2008. The extended nature of the outbreak suggests that the kudu population in Namibia is able to recover sufficiently in the periods between epidemic peaks.

There is more support for rabies as a threat to the conservation of populations of endangered canids in Africa. Well-documented outbreaks of rabies have caused significant local declines or extinctions in populations of African wild dogs (Lycaon pictus) and Ethiopian wolves (Canis simensis).9,10 It is perhaps notable that these impacts have occurred in already vulnerable populations: small, isolated population or those on the periphery of protected areas. Small populations of endangered canids are more susceptible to stochastic extinction following introduction of disease from more abundant maintenance host populations, and populations on the periphery of protected areas are more likely to contact domestic dogs, the most abundant reservoir host species of RABV in Africa. This suggests that conservation efforts for these species must not focus solely on mitigating the immediate threat of disease through for example vaccination of vulnerable populations, but must naturally focus on creating larger and better connected populations, ideally within a network of protected areas where contact with infected domestic hosts is reduced. Regular vaccination of contiguous populations of domestic dogs against rabies is also warranted, particularly in light of the broader human and animal health benefits of this approach.11

Two case studies illustrate that the conservation impact of rabies in more complex host communities within protected areas is more muted, even in the face of high rabies incidence in contiguous domestic dog populations. In the first case study, in the species-rich Serengeti ecosystem in Tanzania, evidence that domestic dogs are the only maintenance population for RABV has been accumulated. Only a single canid-associated variant circulates among carnivores there, and cross-species transmission events from domestic dogs results in only short-lived chains of transmission in wildlife, with no evidence of persistence.12 An ongoing study in a protected area adjacent to the Kruger National Park (KNP) in South Africa provides similar evidence. There is a high level of surveillance in the reserve, which is open to the KNP on its eastern and southern boundary, and fenced from adjacent human settlements and communal rangelands on its western and northern boundaries. Almost all carcasses of carnivorous or omnivorous wild animals encountered are sent for rabies testing, and domestic dogs entering the reserve are shot and also tested for rabies by fluorescent antibody test at a reference laboratory. Data from 151 dogs that were tested for rabies between January 2009 and March 2014 (State Veterinary records) and for whom accurate coordinates were available, are included in this study. More dogs were shot closer to the fence, gates, camps, rivers, and other water points than expected by chance. Of the 151 dogs tested, 102 (68%) were positive for rabies. Dogs found further into the reserve were significantly more likely to test positive for rabies than dogs found closer to the fence line. Non-rabid dogs were also found significantly closer to neighbouring villages, while rabid dogs were found closer to rivers and access roads. Despite the high rates of incursion of rabies-positive dogs into the reserve, intensive passive surveillance for rabies as a cause of death in wildlife (n = 54 animals tested) has revealed only a single case in a chacma baboon (Papio ursinus). While it may be that the intensive management in this reserve results in the rapid destruction of rabies-infected dogs that enter (before exposures can occur), and in the destruction of the few wild animals that are exposed, the lack of wildlife cases is striking. Together with the evidence from Serengeti, this points to a lack of persistence of RABV in complex host communities.

In conclusion, it appears that with the exception of vulnerable populations of endangered canids, rabies is not of significant conservation concern in Africa. A more substantial problem for the control of rabies on the continent is posed by the maintenance of the canid variant of RABV in wildlife hosts in southern Africa, seemingly independently from cycles in domestic dogs. While it remains apparent that efforts to eliminate this variant from the continent must begin with wide-scale and sustained mass dog vaccination, the prospect of adjunct control strategies in wildlife in specific locations must be considered in the planning stages. The rise of wildlife-associated rabies cases in the USA following the elimination of dog-associated rabies,13 and the apparent decades-long undetected circulation of rabies in ferret badgers in Taiwan,14 should serve as cautionary notes to maintain and intensify rabies surveillance in wildlife alongside efforts to control the disease in dogs.

References

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2.  Marston DA, Horton DL, Ngeleja C, Hampson K, McElhinney LM, Banyard AC, et al. Ikoma lyssavirus, highly divergent novel lyssavirus in an African civet. Emerging Infectious Diseases. 2012;18(4):664–667.

3.  Van Zyl N, Markotter W, Nel LH. Evolutionary history of African mongoose rabies. Virus Research. 2010;150(1–2):93–102.

4.  Sabeta CT, Mansfield KL, McElhinney LM, Fooks AR, Nel LH. Molecular epidemiology of rabies in bat-eared foxes (Otocyon megalotis) in South Africa. Virus Research. 2007;129(1):1–10.

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6.  Maas B. Bat-eared fox behavioral ecology and the incidence of rabies in the Serengeti National Park. Onderstepoort Journal of Veterinary Research. 1993;60(4):389–393.

7.  East ML, Hofer H, Cox JH, Wulle U, Wiik H, Pitra C. Regular exposure to rabies virus and lack of symptomatic disease in Serengeti spotted hyenas. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(26):15026–15031.

8.  Scott TP, Fischer M, Khaiseb S, Freuling C, Hoeper D, Hoffmann B, et al. Complete genome and molecular epidemiological data infer the maintenance of rabies among kudu (Tragelaphus strepsiceros) in Namibia. PLoS One. 2013;8(3):e58739.

9.  Gasgoyne SC, Laurenson MK, Lelo S, Borner M. Rabies in African wild dogs (Lycaon pictus) in the Serengeti region, Tanzania. Journal of Wildlife Diseases. 1993;29(3):396–402.

10. Knobel DL, Fooks AR, Brookes SM, Randall DA, Williams SD, Argaw K, et al. Trapping and vaccination of endangered Ethiopian wolves to control an outbreak of rabies. Journal of Applied Ecology. 2008;45(1):109–116.

11. Cleaveland S, Kaare M, Knobel D, Laurenson MK. Canine vaccination - Providing broader benefits for disease control. Veterinary Microbiology. 2006;117(1):43–50.

12. Lembo T, Hampson K, Kaare MT, Ernest E, Knobel D, Kazwala RR, et al. The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Neglected Tropical Diseases. 2010;4(2):e626.

13. Velasco-Villa A, Reeder SA, Orciari LA, Yager PA, Franka R, Blanton JD, et al. Enzootic rabies elimination from dogs and reemergence in wild terrestrial carnivores, United States. Emerging Infectious Diseases. 2008;14(12):1849–1854.

14. Chiou H-Y, Hsieh C-H, Jeng C-R, Chan F-T, Wang H-Y, Pang VF. Molecular characterization of cryptically circulating rabies virus from ferret badgers, Taiwan. Emerging Infectious Diseases. 2014;20(5):790–798.

  

Speaker Information
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Darryn Knobel, BVSc, PhD
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science
University of Pretoria
South Africa


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