Pathogen spillover driven by rapid changes in bat ecology.

Peggy Eby1,2,3 Alison J Peel2 Andrew Hoegh4 Wyatt Madden5,6 John R Giles7,8 Peter J Hudson9 Raina K Plowright10,11
Affiliations 11 institutions
  1. School of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia.
  2. Centre for Planetary Health and Food Security, Griffith University, Nathan, Queensland, Australia.
  3. Center for Large Landscape Conservation, Bozeman, MT, USA.
  4. Department of Mathematical Sciences, Montana State University, Bozeman, MT, USA.
  5. Department of Microbiology and Cell Biology, Montana State University, Bozeman, MT, USA.
  6. Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, GA, USA.
  7. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
  8. Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA.
  9. Center for Infectious Disease Dynamics, Pennsylvania State University, State College, PA, USA.
  10. Department of Microbiology and Cell Biology, Montana State University, Bozeman, MT, USA. [email protected].
  11. Department of Public and Ecosystem Health, Cornell University, Ithaca, NY, USA. [email protected].

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.

Supporting text Virus Host Location
Chiroptera 371 Ecology 6 Ecosystem 36 Hendra Virus 39 Horses 52 Agriculture 5 Animals 1948 Australia 28 Bayes Theorem 32 Climate 7 Food Supply 3 Forests 10 Humans 1440 Natural Resources 1 Pandemics 108 Public Health 17

Evidence records

3 total
Zoonotic Surveillance
2 records · 1 evidence types
Evidence type
2 records
OVE6534
Key finding

Interactions between land-use change and climate produced persistent bat residency in agricultural areas driving Hendra virus spillover clusters, while flowering pulses in remnant forests reduced spillover occurrence.

Virus
Host
Location
Supporting text

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.

Method
integrative Bayesian network modeling | long-term ecological data analysis
Geographic raw
agricultural areas | remnant forests
OVE6533
Key finding

Bats adopted persistent residency behaviour in response to environmental change, representing an ecological shift relevant to Hendra virus spillover dynamics.

Virus
Host
Location
Supporting text

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.

Method
long-term ecological monitoring | behavioural observation
Geographic raw
subtropical Australia
Country inferred
AUS
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE6532
Key finding

Hendra virus spilled over naturally from Pteropodid bats to horses in subtropical Australia, with repeated clusters documented over 25 years.

Virus
Host
Location
Supporting text

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.

Method
ecological observation | Bayesian network modeling
Study design
long-term ecological monitoring study linking bat behaviour and spillover patterns
Transmission direction
animal-to-animal
Geographic raw
subtropical Australia