Regular exposure to rabies virus and lack of symptomatic disease in Serengeti spotted hyenas

Abstract

We report a previously unrecognized complexity to the ecology of rabies in wildlife. Rabies-specific virus-neutralizing antibodies in spotted hyenas, the most numerous large carnivore in the Serengeti ecosystem (Tanzania, East Africa), revealed a high frequency of exposure of 37.0% to rabies virus, and reverse transcriptase (RT) PCR demonstrated rabies RNA in 13.0% of hyenas. Despite this high frequency, exposure neither caused symptomatic rabies nor decreased survival among members of hyena social groups monitored for 9 to13 years. Repeated, intermittent presence of virus in saliva of 45.5% of seropositive hyenas indicated a “carrier” state. Rabies isolates from Serengeti hyenas differed significantly (8.5% sequence divergence) from those isolated from other Serengeti carnivores, suggesting that at least two separate strains circulate within the Serengeti carnivore community. This finding is consistent with the fact that exposure in hyenas increased with age and social status, following a pattern predicted by intraspecific age and social-status-dependent oral and bite contact rates. High seroprevalence of rabies, low basic reproductive rate of the virus (R ₀) of 1.9, a carrier state, and the absence of symptomatic rabies in a carnivore in an ecosystem with multihost and multistrain maintenance has not been previously demonstrated for rabies. Because of the substantial differences between the hyena viral isolates and those from canids and viverrids in the Serengeti, it is unlikely that spotted hyenas were the source of rabies virus that killed several African wild dog packs in the Serengeti ecosystem in the 1990s.