Pathogen spillover driven by rapid changes in bat ecology

Abstract

During recent decades, pathogens that originated in bats have become an increasing public health concern. A major challenge is to identify how those pathogens spill over into human populations to generate a pandemic threat1. Many correlational studies associate spillover with changes in land use or other anthropogenic stressors2,3, although the mechanisms underlying the observed correlations have not been identified4. One limitation is the lack of spatially and temporally explicit data on multiple spillovers, and on the connections among spillovers, reservoir host ecology and behaviour and viral dynamics. We present 25 years of data on land-use change, bat behaviour and spillover of Hendra virus from Pteropodid bats to horses in subtropical Australia. These data show that bats are responding to environmental change by persistently adopting behaviours that were previously transient responses to nutritional stress. Interactions between land-use change and climate now lead to persistent bat residency in agricultural areas, where periodic food shortages drive clusters of spillovers. Pulses of winter flowering of trees in remnant forests appeared to prevent spillover. We developed integrative Bayesian network models based on these phenomena that accurately predicted the presence or absence of clusters of spillovers in each of the 25 years. Our long-term study identifies the mechanistic connections between habitat loss, climate and increased spillover risk. It provides a framework for examining causes of bat virus spillover and for developing ecological countermeasures to prevent pandemics.

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

“…Connecting such data with changing ecology of wildlife further requires studies of abiotic and biotic correlates and host behaviour and demography at similar or biologically meaningful spatial and temporal scales (Becker, Washburne, et al, 2019; Lunn et al, 2021; Ostfeld et al, 2006). Here, the ecological conditions that predict HeV shedding from flying foxes were derived from data collected over approximately 25 years and from diverse sources (Eby & Law, 2008; Eby et al, 1999; Lunn et al, 2021) (Eby et al, 2022a). Although collecting this kind of ecological data will accordingly present logistical difficulties, the growth of national research networks, global community consortiums and remote sensing, among other large‐scale efforts, should facilitate similar approaches to link spatiotemporal data on both host ecology and infection (Dietze et al, 2018).…”

“…We paired HeV urine pool prevalence data within our study region with long‐term data on flying fox ecology. As described in full in Eby et al (2022a), we used data held by Australian state governments, flying fox surveys conducted between 1998–2005 and 2012–2019, records held by local land managers and experienced observers, and direct observation by the authors to characterise the ecological conditions experienced by bat populations over time (Eby & Law, 2008; Eby et al, 1999; Lunn et al, 2021). Roosts were classified as belonging to their historic winter range (and, thus, where bats rely on native winter dietary plants) or to newly established overwintering regions (and, thus, where native food is less available).…”

“…To lastly test whether annual AUC (as an approximation of pathogen pressure) positively predicts spillover frequency, we collated data on the location and date of all known HeV cases in horses in our study region between 2012 and 2014 (Plowright et al, 2015). As described in full in Eby et al (2022a), these data were obtained from government notices (i.e. New South Wales Department of Primary Industries, Queensland Department of Agriculture and Fisheries; Business Queensland), ProMED, local media reports and personal communications.…”

“…All HeV shedding data and flying fox abundance data used in this analysis are freely available from the Queensland government (CC BY 4.0; https://www.data.qld.gov.au/dataset/hev-infection-flying-foxes-easternaustralia). Original ecological covariate data and HeV spillover data (provided to the nearest town for anonymity) presented in Eby et al (2022a) are available from the Cornell University eCommons Digital Repository: https://doi.org/10.7298/3dbp-t721 (Eby et al, 2022b), https://doi.org/10.7298/kdht-sp38 (Eby et al, 2022c), and https://doi.org/10.7298/tb5p-dr98 (Eby et al, 2022d). Those data subset to the flying fox roosts analyzed here are provided in Table 1 and Table S4, respectively.…”

“…The relationships between food shortages and HeV shedding thus remain poorly understood, especially in the context of changing ecological conditions experienced by bat hosts. Recent work suggests such ecological changes have increased the HeV spillover frequency (Eby et al, 2022a) (Eby et al, 2020; Peel et al, 2017), but the mechanisms linking food shortages and shifts in bat behaviour with virus shedding remain unresolved.…”