Incorporating environmental heterogeneity and observation effort to predict host distribution and viral spillover from a bat reservoir.

Predicting the spatial occurrence of wildlife is a major challenge for ecology and management. In Latin America, limited knowledge of the number and locations of vampire bat roosts precludes informed allocation of measures intended to prevent rabies spillover to humans and livestock. We inferred the spatial distribution of vampire bat roosts while accounting for observation effort and environmental effects by fitting a log Gaussian Cox process model to the locations of 563 roosts in three regions of Peru. Our model explained 45% of the variance in the observed roost distribution and identified environmental drivers of roost establishment. When correcting for uneven observation effort, our model estimated a total of 2340 roosts, indicating that undetected roosts (76%) exceed known roosts (24%) by threefold. Predicted hotspots of undetected roosts in rabies-free areas revealed high-risk areas for future viral incursions. Using the predicted roost distribution to inform a spatial model of rabies spillover to livestock identified areas with disproportionate underreporting and indicated a higher rabies burden than previously recognized. We provide a transferrable approach to infer the distribution of a mostly unobserved bat reservoir that can inform strategies to prevent the re-emergence of an important zoonosis.

Ecological determinants of rabies virus dynamics in vampire bats and spillover to livestock.

The pathogen transmission dynamics in bat reservoirs underpin efforts to reduce risks to human health and enhance bat conservation, but are notoriously challenging to resolve. For vampire bat rabies, the geographical scale of enzootic cycles, whether environmental factors modulate baseline risk, and how within-host processes affect population-level dynamics remain unresolved. We studied patterns of rabies exposure using an 11-year, spatially replicated sero-survey of 3709 Peruvian vampire bats and co-occurring outbreaks in livestock. Seroprevalence was correlated among nearby sites but fluctuated asynchronously at larger distances. A generalized additive mixed model confirmed spatially compartmentalized transmission cycles, but no effects of bat demography or environmental context on seroprevalence. Among 427 recaptured bats, we observed long-term survival following rabies exposure and antibody waning, supporting hypotheses that immunological mechanisms influence viral maintenance. Finally, seroprevalence in bats was only weakly correlated with outbreaks in livestock, reinforcing the challenge of spillover prediction even with extensive data. Together our results suggest that rabies maintenance requires transmission among multiple, nearby bat colonies which may be facilitated by waning of protective immunity. However, the likelihood of incursions and dynamics of transmission within bat colonies appear largely independent of bat ecology. The implications of these results for spillover anticipation and controlling transmission at the source are discussed.

Defining New Pathways to Manage the Ongoing Emergence of Bat Rabies in Latin America.

Rabies transmitted by common vampire bats (Desmodus rotundus) has been known since the early 1900s but continues to expand geographically and in the range of species and environments affected. In this review, we present current knowledge of the epidemiology and management of rabies in D. rotundus and argue that it can be reasonably considered an emerging public health threat. We identify knowledge gaps related to the landscape determinants of the bat reservoir, reduction in bites on humans and livestock, and social barriers to prevention. We discuss how new technologies including autonomously-spreading vaccines and reproductive suppressants targeting bats might manage both rabies and undesirable growth of D. rotundus populations. Finally, we highlight widespread under-reporting of human and animal mortality and the scarcity of studies that quantify the efficacy of control measures such as bat culling. Collaborations between researchers and managers will be crucial to implement the next generation of rabies management in Latin America.

Fluorescent biomarkers demonstrate prospects for spreadable vaccines to control disease transmission in wild bats.

Vaccines that autonomously transfer among individuals have been proposed as a strategy to control infectious diseases within inaccessible wildlife populations. However, rates of vaccine spread and epidemiological efficacy in real-world systems remain elusive. Here, we investigate whether topical vaccines that transfer among individuals through social contacts can control vampire bat rabies-a medically and economically important zoonosis in Latin America. Field experiments in three Peruvian bat colonies, which used fluorescent biomarkers as a proxy for the bat-to-bat transfer and ingestion of an oral vaccine, revealed that vaccine transfer would increase population-level immunity up to 2.6 times beyond the same effort using conventional, non-spreadable vaccines. Mathematical models showed that observed levels of vaccine transfer would reduce the probability, size and duration of rabies outbreaks, even at low but realistically achievable levels of vaccine application. Models further predicted that existing vaccines provide substantial advantages over culling bats-the policy currently implemented in North, Central and South America. Linking field studies with biomarkers to mathematical models can inform how spreadable vaccines may combat pathogens of health and conservation concern before costly investments in vaccine design and testing.

Quantifying the burden of vampire bat rabies in Peruvian livestock.

BACKGROUND: Knowledge of infectious disease burden is necessary to appropriately allocate resources for prevention and control. In Latin America, rabies is among the most important zoonoses for human health and agriculture, but the burden of disease attributed to its main reservoir, the common vampire bat (Desmodus rotundus), remains uncertain. METHODOLOGY/PRINCIPAL FINDINGS: We used questionnaires to quantify under-reporting of livestock deaths across 40 agricultural communities with differing access to health resources and epidemiological histories of vampire bat rabies (VBR) in the regions of Apurimac, Ayacucho and Cusco in southern Peru. Farmers who believed VBR was absent from their communities were one third as likely to report livestock deaths from disease as those who believed VBR was present, and under-reporting increased with distance from reporting offices. Using generalized mixed-effect models that captured spatial autocorrelation in reporting, we project 4.6 (95% CI: 4.4-8.2) rabies cases per reported case and identify geographic areas with potentially greater VBR burden than indicated by official reports. Spatially-corrected models estimate 505-724 cattle deaths from VBR in our study area during 2014 (421-444 deaths/100,000 cattle), costing US$121,797-171,992. Cost benefit analysis favoured vaccinating all cattle over the current practice of partial vaccination or halting vaccination all together. CONCLUSIONS: Our study represents the first estimate of the burden of VBR in Latin America to incorporate data on reporting rates. We confirm the long-suspected cost of VBR to small-scale farmers and show that vaccinating livestock is a cost-effective solution to mitigate the burden of VBR. More generally, results highlight that ignoring geographic variation in access to health resources can bias estimates of disease burden and risk.

Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies.

Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.

Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control.

Despite extensive culling of common vampire bats in Latin America, lethal human rabies outbreaks transmitted by this species are increasingly recognized, and livestock rabies occurs with striking frequency. To identify the individual and population-level factors driving rabies virus (RV) transmission in vampire bats, we conducted a longitudinal capture-recapture study in 20 vampire bat colonies spanning four regions of Peru. Serology demonstrated the circulation of RV in vampire bats from all regions in all years. Seroprevalence ranged from 3 to 28 per cent and was highest in juvenile and sub-adult bats. RV exposure was independent of bat colony size, consistent with an absence of population density thresholds for viral invasion and extinction. Culling campaigns implemented during our study failed to reduce seroprevalence and were perhaps counterproductive for disease control owing to the targeted removal of adults, but potentially greater importance of juvenile and sub-adult bats for transmission. These findings provide new insights into the mechanisms of RV maintenance in vampire bats and highlight the need for ecologically informed approaches to rabies prevention in Latin America.