Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem

Abstract

Knowledge of infection reservoir dynamics is critical for effective disease control, but identifying reservoirs of multi-host pathogens is challenging. Here, we synthesize several lines of evidence to investigate rabies reservoirs in complex carnivore communities of the Serengeti ecological region in northwest Tanzania, where the disease has been confirmed in 12 carnivore species.Long-term monitoring data suggest that rabies persists in high-density domestic dog Canis familiaris populations (> 11 dogs km(-2)) and occurs less frequently in lower-density (< 5 dogs km(-2)) populations and only sporadically in wild carnivores.Genetic data show that a single rabies virus variant belonging to the group of southern Africa canid-associated viruses (Africa 1b) circulates among a range of species, with no evidence of species-specific virus-host associations.Within-species transmission was more frequently inferred from high-resolution epidemiological data than between-species transmission. Incidence patterns indicate that spill-over of rabies from domestic dog populations sometimes initiates short-lived chains of transmission in other carnivores.Synthesis and applications. The balance of evidence suggests that the reservoir of rabies in the Serengeti ecosystem is a complex multi-host community where domestic dogs are the only population essential for persistence, although other carnivores contribute to the reservoir as non-maintenance populations. Control programmes that target domestic dog populations should therefore have the greatest impact on reducing the risk of infection in all other species including humans, livestock and endangered wildlife populations, but transmission in other species may increase the level of vaccination coverage in domestic dog populations necessary to eliminate rabies.

Fig. 1

Potential rabies reservoir systems in the Serengeti. CCS, critical community size. In this figure, we use humans as the target population, but for rabies target populations include humans, livestock and endangered wildlife. If the epidemiological situation corresponds to (a), vaccinating domestic dogs would shift the situation first to (c) and finally to an overall community insufficient for rabies maintenance.

Fig. 2

Map of the Serengeti ecological region illustrating the distribution of suspected rabies cases (most were not laboratory-confirmed but diagnosed using epidemiological history and clinical criteria). Tables S2 and S3 in Supplementary material detail confirmed wildlife cases in Serengeti National Park (SNP) and Serengeti (SD) and Ngorongoro (ND) districts. Cases recorded in SNP from January 1995–January 2007 are mapped, whereas only cases from January 2002–January 2007 in SD and ND are mapped because GPS data were not available for the earlier period. Domestic dog cases are shown in black (SD: n = 833; ND: n = 128) and cases in other carnivores as white circles (SD: n = 96; ND: n = 27; SNP: n = 23). Village boundaries are indicated by grey lines. LGCA, Loliondo Game Control Area; NCA, Ngorongoro Conservation Area.

Fig. 3

Wildlife disease monitoring in Serengeti National Park: (a) carnivore reports and (b) samples retrieved for rabies diagnosis. The peak in 1994 coincided with a canine distemper outbreak in lions (Roelke-Parker et al. 1996).

Fig. 4

Incidence of bites by suspected rabid domestic dogs in Serengeti (SD, black line) and Ngorongoro (ND, grey line) districts derived from hospital records. Incidence is shown only for years before the implementation of domestic dog vaccination programmes in the study populations (July 1987–January 1997 in SD and January 1994–December 2003 in ND). No data were available for 6 months during 1993 in SD.

Fig. 5

Suspected rabies cases among carnivore species in (a) Serengeti (n = 929) and (b) Ngorongoro districts (n = 155) monitored by contact tracing from January 2001 to January 2007.

Fig. 6

Phylogenetic tree of nucleoprotein gene sequences (282 bp, 94 deduced amino acids, nucleotide positions 1139–1420 on the SAD B19 genome (Conzelmann et al. 1990) for RABV samples from the study area compared with isolates from other areas of Africa. The tree is constructed using Bayesian phylogenetics under the transitional model of nucleotide evolution with a gamma-shaped distribution of rates across sites (TIM + Γ Posada & Crandall 1998; base frequencies = 0·3253, 0·2134, 0·2360, 0·2253; nucleotide substitution rates = 1·0000, 3·6723, 0·4393, 0·4393, 8·1773, 1·0000; Γ = 0·3390). For samples from the study area, the year of collection is indicated within square brackets. Previously published sequences are designated by strain names (Kissi et al. 1995; Randall et al. 2004). The tree is rooted with isolate 1500AFS, defined as outgroup, representative of the lineage Africa 3. Nodal posterior probabilities > 0·95 are shown. The scale indicates branch-length expressed as the expected number of substitutions per site. *Species not definitively identified.

Fig. 7

The proportion of estimated transmission within and between host types (associated with 1255 suspected rabies cases, 1044 in Serengeti and 211 in Ngorongoro) in Serengeti (light grey) and Ngorongoro (dark grey) districts, with ‘dog’ corresponding to domestic dogs and ‘carnivore’ to domestic cats and wild carnivores. Credibility intervals (95%) are shown for expected transmission within and between host types assuming inter- and intraspecific transmission were equally likely and that livestock are dead-end hosts.