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 threat 1 . Many correlational studies associate spillover with changes in land use or other anthropogenic stressors 2,3 , although the mechanisms underlying the observed correlations have not been identified 4 . 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.
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The Ecology of Nipah Virus in Bangladesh: A Nexus of Land-Use Change and Opportunistic Feeding Behavior in Bats
Nipah virus is a bat-borne paramyxovirus that produces yearly outbreaks of fatal encephalitis in Bangladesh. Understanding the ecological conditions that lead to spillover from bats to humans can assist in designing effective interventions. To investigate the current and historical processes that drive Nipah spillover in Bangladesh, we analyzed the relationship among spillover events and climatic conditions, the spatial distribution and size of Pteropus medius roosts, and patterns of land-use change in Bangladesh over the last 300 years. We found that 53% of annual variation in winter spillovers is explained by winter temperature, which may affect bat behavior, physiology, and human risk behaviors. We infer from changes in forest cover that a progressive shift in bat roosting behavior occurred over hundreds of years, producing the current system where a majority of P. medius populations are small (median of 150 bats), occupy roost sites for 10 years or more, live in areas of high human population density, and opportunistically feed on cultivated food resources—conditions that promote viral spillover. Without interventions, continuing anthropogenic pressure on bat populations similar to what has occurred in Bangladesh could result in more regular spillovers of other bat viruses, including Hendra and Ebola viruses.
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- Award ID(s):
- 1716698
- NSF-PAR ID:
- 10295543
- Date Published:
- Journal Name:
- Viruses
- Volume:
- 13
- Issue:
- 2
- ISSN:
- 1999-4915
- Page Range / eLocation ID:
- 169
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Does the structure and connectivity of host populations influence the dynamics and evolution of their pathogens? This topical question is the essence of research investigating the ecology of a
Pteropus fruit bat and its zoonotic Nipah virus (NiV) published by Olival et al. in this issue ofMolecular Ecology . Questioned less overtly, but nonetheless implicit to the study, is “what are the mechanisms underpinning intraspecific host–pathogen congruence (IHPC) of genetic structure?”. Olival et al. investigated the phylogeographical structure ofPteropus medius and NiV isolates across Bangladesh, from areas inside and outside of the Nipah belt—an area where most human spillover events occur. A high degree of host panmixia was discovered, with some population differentiation east of the Nipah belt. NiV genetic structure was congruent with the host. The authors attributed the panmixia and structuring, respectively, to (a) the highly vagile nature ofP. medius , and (b) possible differences between bioregions within and outside the Nipah belt. Other potential explanatory mechanisms were acknowledged, including hybridization and transmission mode. This study makes a valuable contribution to a growing body of literature examining IHPC. This has implications not only for pathogen spillover to humans and domestic animals, but more generally for thinking about the mechanisms that underlie patterns of host and pathogen genetic associations. -
Sampling reservoir hosts over time and space is critical to detect epizootics, predict spillover and design interventions. However, because sampling is logistically difficult and expensive, researchers rarely perform spatio-temporal sampling of many reservoir hosts. Bats are reservoirs of many virulent zoonotic pathogens such as filoviruses and henipaviruses, yet the highly mobile nature of these animals has limited optimal sampling of bat populations. To quantify the frequency of temporal sampling and to characterize the geographical scope of bat virus research, we here collated data on filovirus and henipavirus prevalence and seroprevalence in wild bats. We used a phylogenetically controlled meta-analysis to next assess temporal and spatial variation in bat virus detection estimates. Our analysis shows that only one in four bat virus studies report data longitudinally, that sampling efforts cluster geographically (e.g. filovirus data are available across much of Africa and Asia but are absent from Latin America and Oceania), and that sampling designs and reporting practices may affect some viral detection estimates (e.g. filovirus seroprevalence). Within the limited number of longitudinal bat virus studies, we observed high heterogeneity in viral detection estimates that in turn reflected both spatial and temporal variation. This suggests that spatio-temporal sampling designs are important to understand how zoonotic viruses are maintained and spread within and across wild bat populations, which in turn could help predict and preempt risks of zoonotic viral spillover.more » « less
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Global changes in response to human encroachment into natural habitats and carbon emissions are driving the biodiversity extinction crisis and increasing disease emergence risk. Host distributions are one critical component to identify areas at risk of viral spillover, and bats act as reservoirs of diverse viruses. We developed a reproducible ecological niche modelling pipeline for bat hosts of SARS-like viruses (subgenus Sarbecovirus ), given that several closely related viruses have been discovered and sarbecovirus–host interactions have gained attention since SARS-CoV-2 emergence. We assessed sampling biases and modelled current distributions of bats based on climate and landscape relationships and project future scenarios for host hotspots. The most important predictors of species distributions were temperature seasonality and cave availability. We identified concentrated host hotspots in Myanmar and projected range contractions for most species by 2100. Our projections indicate hotspots will shift east in Southeast Asia in locations greater than 2°C hotter in a fossil-fuelled development future. Hotspot shifts have implications for conservation and public health, as loss of population connectivity can lead to local extinctions, and remaining hotspots may concentrate near human populations.more » « less
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Abstract The spatial organization of populations determines their pathogen dynamics. This is particularly important for communally roosting species, whose aggregations are often driven by the spatial structure of their environment.
We develop a spatially explicit model for virus transmission within roosts of Australian tree‐dwelling bats (
Pteropus spp.), parameterized to reflect Hendra virus. The spatial structure of roosts mirrors three study sites, and viral transmission between groups of bats in trees was modelled as a function of distance between roost trees. Using three levels of tree density to reflect anthropogenic changes in bat habitats, we investigate the potential effects of recent ecological shifts in Australia on the dynamics of zoonotic viruses in reservoir hosts.We show that simulated infection dynamics in spatially structured roosts differ from that of mean‐field models for equivalently sized populations, highlighting the importance of spatial structure in disease models of gregarious taxa. Under contrasting scenarios of flying‐fox roosting structures, sparse stand structures (with fewer trees but more bats per tree) generate higher probabilities of successful outbreaks, larger and faster epidemics, and shorter virus extinction times, compared to intermediate and dense stand structures with more trees but fewer bats per tree. These observations are consistent with the greater force of infection generated by structured populations with less numerous but larger infected groups, and may flag an increased risk of pathogen spillover from these increasingly abundant roost types.
Outputs from our models contribute insights into the spread of viruses in structured animal populations, like communally roosting species, as well as specific insights into Hendra virus infection dynamics and spillover risk in a situation of changing host ecology. These insights will be relevant for modelling other zoonotic viruses in wildlife reservoir hosts in response to habitat modification and changing populations, including coronaviruses like SARS‐CoV‐2.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/v13020169
