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 ( 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.
- Award ID(s):
- 1716698
- NSF-PAR ID:
- 10390340
- Editor(s):
- Becker, Daniel
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 17
- Issue:
- 5
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0268549
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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. -
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Abstract Context Environmental change impacts natural ecosystems and wildlife populations. In Australia, native forests have been heavily cleared and the local emergence of Hendra virus (HeV) has been linked to land-use change, winter habitat loss, and changing bat behavior.
Objectives We quantified changes in landscape factors for black flying foxes (
Pteropus alecto ), a reservoir host of HeV, in sub-tropical Queensland, Australia from 2000–2020. We hypothesized that native winter habitat loss and native remnant forest loss were greatest in areas with the most human population growth.Methods We measured the spatiotemporal change in human population size and native ‘remnant’ woody vegetation extent. We assessed changes in the observed
P. alecto population and native winter habitats in bioregions whereP. alecto are observed roosting in winter. We assessed changes in the amount of remnant vegetation across bioregions and within 50 km foraging buffers around roosts.Results Human populations in these bioregions grew by 1.18 M people, mostly within 50 km foraging areas around roosts. Remnant forest extent decreased overall, but regrowth was observed when policy restricted vegetation clearing. Winter habitats were continuously lost across all spatial scales. Observed roost counts of
P. alecto declined.Conclusion Native remnant forest loss and winter habitat loss were not directly linked to spatial human population growth. Rather, most remnant vegetation was cleared for indirect human use. We observed forest loss and regrowth in response to state land clearing policies. Expanded flying fox population surveys will help better understand how land-use change has impacted
P. alecto distribution and Hendra virus spillover. -
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Abstract Pathogens can spill over and infect new host species by overcoming a series of ecological and biological barriers. Hendra virus (HeV) circulates in Australian flying foxes and provides a data‐rich study system for identifying environmental drivers underlying spillover events. The frequency of spillover events to horses has varied interannually since the virus was first discovered in 1994. These observations suggest that HeV spillover events are driven, in part, by environmental factors, including loss of flying fox habitat and climate variability.
We explicitly examine the impact of environmental variation on the risk of HeV spillover at three spatial scales relevant to this system. We use a dataset of 60 spillover events and boosted regression tree methods to identify environmental features (including concurrent and lagged temperature, rainfall, vegetation indices, land cover, and climate indices) at three spatial scales (1‐km, 20‐km, 100‐km radii) associated with horse contacts and reservoir species ecology.
We find that temperature, local (1‐km radius) human population density, and landscape (100‐km radius) forest cover and pasture are the most influential environmental features associated with HeV spillover risk. By including multiple spatial scales and temporal lags in environmental features, we can more accurately quantify risk across space and time than with models that use a single scale. For example, high quality vegetation at the local scale and within a foraging radius (20‐km) in the concurrent month and previous years, combined with poorer quality vegetation at the landscape scale in the concurrent month increase risk of HeV spillover. These and other environmental associations likely influence the dynamic foraging behaviour of reservoir flying foxes and drive contacts that facilitate spillover into horse populations.
Synthesis and application : Current management of HeV spillover focuses on local‐scale interventions – primarily through vaccination and detection of infected horses. Our study finds that HeV spillover risk is also driven by environmental changes over much larger scales and demonstrates management practices would benefit from incorporating landscape interventions alongside local interventions. -
Understanding environmental factors driving spatiotemporal patterns of disease can improve risk mitigation strategies. Hendra virus (HeV), discovered in Australia in 1994, spills over from bats (Pteropus sp.) to horses and thence to humans. Below latitude - 22, almost all spillover events to horses occur during winter, and above this latitude spillover is aseasonal. We generated a statistical model of environmental drivers of HeV spillover per month. The model reproduced the spatiotemporal pattern of spillover risk between 1994 and 2015. The model was generated with an ensemble of methods for presence–absence data (boosted regression trees, random forests and logistic regression). Presences were the locations of horse cases, and absences per spatial unit (2.7 9 2.7 km pixels without spillover) were sampled with the horse census of Queensland and New South Wales. The most influential factors indicate that spillover is associated with both cold-dry and wet conditions. Bimodal responses to several variables suggest spillover involves two systems: one above and one below a latitudinal area close to - 22. Northern spillovers are associated with cold-dry and wet conditions, and southern with cold-dry conditions. Biologically, these patterns could be driven by immune or behavioural changes in response to food shortage in bats and horse husbandry. Future research should look for differences in these traits between seasons in the two latitudinal regions. Based on the predicted risk patterns by latitude, we recommend enhanced preventive management for horses from March to November below latitude 22 south.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0268549
