Ecological conditions experienced by bat reservoir hosts predict the intensity of Hendra virus excretion over space and time

Abstract

The ecological conditions experienced by wildlife reservoir hosts affect the amount of pathogen they excrete into the environment. This then shapes pathogen pressure, the amount of pathogen available to recipient hosts over space and time, which affects spillover risk. Few systems have data on both long-term ecological conditions and pathogen pressure, yet such data are critical for advancing our mechanistic understanding of ecological drivers of spillover risk. To identify these ecological drivers, we here reanalyze shedding data from a spatially replicated, multi-year study of Hendra virus excretion from Australian flying foxes in light of 25 years of long-term data on changing ecology of the bat reservoir hosts. Using generalized additive mixed models, we show that winter virus shedding pulses, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations that have been displaced to novel habitats. We next derive the area under each annual shedding curve (representing cumulative virus excretion) and show that pathogen pressure is also affected by the ecological conditions experienced by bat populations. Finally, we illustrate that pathogen pressure positively predicts observed spillover frequency. Our study suggests that recent ecological conditions of flying fox hosts are shifting the timing, magnitude, and cumulative intensity of Hendra virus shedding in ways that shape the landscape of spillover risk. This work provides a mechanistic approach to understanding and estimating risk of spillover from reservoir hosts in complex ecological systems and emphasizes the importance of host ecological context in identifying the determinants of pathogen shedding.

Climate Anomalies and Spillover of Bat-Borne Viral Diseases in the Asia–Pacific Region and the Arabian Peninsula

“…Our study revealed a stronger correlation between climate variability and the spillover pattern of HeV in eastern Australia than NiV in Bangladesh. HeV prevalence in flying foxes in Australia has shown multi-year inter-epidemic periods, suggesting that viral dynamics are not annual, but the ecological drivers and the climate influence behind this pattern remain unclear [ 64 , 65 , 66 ]. Numerous factors including food shortage, low concentration of nectar-based resources, extreme temperatures, dry conditions, phenology of eucalypt forests, physiological stress, flying fox foraging behavior, and use of wintering roosts in urban and agricultural areas were all suggested to be associated with increased HeV shedding in Australian flying foxes [ 18 , 66 , 67 ].…”

“…HeV prevalence in flying foxes in Australia has shown multi-year inter-epidemic periods, suggesting that viral dynamics are not annual, but the ecological drivers and the climate influence behind this pattern remain unclear [ 64 , 65 , 66 ]. Numerous factors including food shortage, low concentration of nectar-based resources, extreme temperatures, dry conditions, phenology of eucalypt forests, physiological stress, flying fox foraging behavior, and use of wintering roosts in urban and agricultural areas were all suggested to be associated with increased HeV shedding in Australian flying foxes [ 18 , 66 , 67 ]. Our logistic regression models and SEM show that seasonal climate factors (monthly temperature), but also multi-annual climate variability (ENSO 3.4 index) and long-trend climate anomalies (land surface temperature anomalies), significantly influence the complex pattern of HeV spillover events in Australia.…”

Viral diversity and zoonotic risk in endangered species

“…First, researchers might consider reproducing recent analyses of the pace of viral discovery (Wille et al 2021; Gibb et al 2022) and testing whether a change to a species’ IUCN Red List status has a downstream effect on research effort, further interrogating our hypothesis that endangered species are subject to an additional and unique form of sampling biases. Further work on the relationship between extinction pressure and disease emergence can also move beyond viral diversity—a crude metric for zoonotic emergence that only minimally captures the transmission process—and examine whether infection prevalence in hosts and shedding into the environment is higher in species facing different kinds of anthropogenic threats (Becker et al 2021). Finally, we suggest that researchers might consider deliberate efforts to better inventory and study the viral fauna of endangered species, both because of the actionable concerns we raise above, and simply to understand these species better.…”

Strategic vaccine stockpiles for regional epidemics of emerging viruses: a geospatial modeling framework

“…In Bangladesh, the emergence of Nipah virus has been driven by the conversion of intact forest into mosaic landscapes, driving the flying fox bat (Pteropus medius) reservoir into farms, where they forage for fruit and date palm sap (McKee et al 2021;Epstein et al 2020). These foraging behaviors create opportunities for human exposure to Nipah virus, and probably coincide with seasonal patterns of winter temperature, food stress, and site selection-a pattern that has been demonstrated more comprehensively for Pteropus bat reservoirs of Hendra virus in Australia (Becker et al 2021;Eby et al 2023;McKee et al 2021;Epstein et al 2020).…”

“…We chose to use the richness of known bat host species as a coarse proxy for viral circulation in reservoirs, and therefore as a reasonable first-principles approximation of risk (Plowright et al 2019). We also explored additional predictors that captured anthropogenic drivers of spillover (McKee et al 2021; Epstein et al 2020; Becker et al 2021), but found that these had poor correspondence to previous outbreaks, and excluded key areas that might be at risk (see Supporting Information).…”