Award Abstract # 1716698
CNH-L: Dynamics of Zoonotic Systems: Human-Bat-Pathogen Interactions

NSF Org: DEB
Division Of Environmental Biology
Recipient: MONTANA STATE UNIVERSITY
Initial Amendment Date: August 18, 2017
Latest Amendment Date: August 18, 2017
Award Number: 1716698
Award Instrument: Standard Grant
Program Manager: Paco Moore
fbmoore@nsf.gov
 (703)292-5376
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: September 1, 2017
End Date: August 31, 2022 (Estimated)
Total Intended Award Amount: $1,650,000.00
Total Awarded Amount to Date: $1,650,000.00
Funds Obligated to Date: FY 2017 = $1,650,000.00
History of Investigator:
  • Raina Plowright (Principal Investigator)
    rplowright@gmail.com
  • Elizabeth Shanahan (Co-Principal Investigator)
  • Olivier Restif (Co-Principal Investigator)
  • Liam McGuire (Co-Principal Investigator)
  • Nita Bharti (Co-Principal Investigator)
Recipient Sponsored Research Office: Montana State University
216 MONTANA HALL
BOZEMAN
MT  US  59717
(406)994-2381
Sponsor Congressional District: 01
Primary Place of Performance: Montana State University
PO Box 173520, 109 Lewis Hall
Bozeman
MT  US  59717-3520
Primary Place of Performance
Congressional District:
01
Unique Entity Identifier (UEI): EJ3UF7TK8RT5
Parent UEI:
NSF Program(s): DYN COUPLED NATURAL-HUMAN
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1691, 9150, 9278
Program Element Code(s): 169100
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Increases in the frequency of human-wildlife interaction have led to the emergence of new zoonoses, which are infectious diseases that are transmitted from animals to humans. Zoonoses are a major threat to biosecurity and public health. Bats are home to some of the highest-profile emerging zoonoses, including Ebola, Marburg, Nipah, and Hendra viruses, and severe acute respiratory syndrome coronavirus (SARS). Transmission from bats to humans often occurs when bats abandon natural habitats to take advantage of resources associated with human settlements. This project will investigate how habitat loss causes bat migration into populated developed areas, which leads to increased bat-human encounters and increased disease transmission. The research will focus on Hendra virus, a bat borne pathogen in Australia, to study the interactions among changing landscapes, loss of natural habitats, humans, bats, and pathogens. A surge of bat movement into towns and cities in eastern Australia has led to increased negative bat-human interactions, and increased mortality of horses and humans from Hendra virus. An ultimate goal of the research is to identify and mitigate the specific interacting factors responsible for increased disease incidence and poor health outcomes. The research team includes investigators at ten academic institutions and a non-profit organization. The project will train U.S. students and postdoctoral researchers, improve science communication and policies that protect wildlife and human health, and will build greater research capacity among national and international collaborators. Methods and results will be generalizable to numerous countries in which similar zoonotic events occur, but that have limited resources for biological surveillance, disease prevention, and responding to outbreaks.

This project will address the hypotheses that the root cause of negative bat-human interactions is the loss of habitat needed to sustain bats' nomadic feeding ecology, and that some management decisions (e.g., destruction of roost sites, not vaccinating horses) may exacerbate conflict, spillover, and habitat loss. The research integrates theory and field data spanning ecology, physiology, epidemiology, political science, anthropology, veterinary medicine, behavioral ecology, and mathematical modeling. Data will be collected on land-use change and the physiology, energetics, and movement of bats; mechanistic models will be used to examine how the relations among these variables influence bats' use of urban areas. The researchers will conduct field and modeling studies on the dynamics of bat viruses to help predict future instances of virus spillover. They will additionally use narratives, collaboratively produced by researchers and local communities, to conduct experiments on risk perceptions and decisions about bat nuisance, virus spillover, and vaccination. Ultimately, the project will lead to an evidence-based program for reversing the negative human-wildlife interactions that lead to epidemics and loss of wildlife. It will also lead to a framework for public education and engagement that is endorsed by local communities and is embedded in ecological restoration initiatives.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 80)
Almberg, Emily S. and Manlove, Kezia R. and Cassirer, E. Frances and Ramsey, Jennifer and Carson, Keri and Gude, Justin and Plowright, Raina K. "Modelling management strategies for chronic disease in wildlife: Predictions for the control of respiratory disease in bighorn sheep" Journal of Applied Ecology , v.59 , 2021 https://doi.org/10.1111/1365-2664.14084 Citation Details
Altizer, Sonia and Becker, Daniel J. and Epstein, Jonathan H. and Forbes, Kristian M. and Gillespie, Thomas R. and Hall, Richard J. and Hawley, Dana M. and Hernandez, Sonia M. and Martin, Lynn B. and Plowright, Raina K. and Satterfield, Dara A. and Streic "Food for contagion: synthesis and future directions for studying host?parasite responses to resource shifts in anthropogenic environments" Philosophical Transactions of the Royal Society B: Biological Sciences , v.373 , 2018 10.1098/rstb.2017.0102 Citation Details
Andrews, Kimberly R. and Adams, Jennifer R. and Cassirer, E. Frances and Plowright, Raina K. and Gardner, Colby and Dwire, Maggie and Hohenlohe, Paul A. and Waits, Lisette P. "A bioinformatic pipeline for identifying informative SNP panels for parentage assignment from RAD seq data" Molecular Ecology Resources , v.18 , 2018 https://doi.org/10.1111/1755-0998.12910 Citation Details
Annand, Edward J. and Horsburgh, Bethany A. and Xu, Kai and Reid, Peter A. and Poole, Ben and de Kantzow, Maximillian C. and Brown, Nicole and Tweedie, Alison and Michie, Michelle and Grewar, John D. and Jackson, Anne E. and Singanallur, Nagendrakumar B. "Novel Hendra Virus Variant Detected by Sentinel Surveillance of Horses in Australia" Emerging Infectious Diseases , v.28 , 2022 https://doi.org/10.3201/eid2803.211245 Citation Details
Banerjee, Arinjay and Baker, Michelle L. and Kulcsar, Kirsten and Misra, Vikram and Plowright, Raina and Mossman, Karen "Novel Insights Into Immune Systems of Bats" Frontiers in Immunology , v.11 , 2020 10.3389/fimmu.2020.00026 Citation Details
Baranowski, K. and Faust, C.L. and Eby, P. and Bharti, N. "Quantifying the impacts of Australian bushfires on native forests and gray-headed flying foxes" Global Ecology and Conservation , v.27 , 2021 https://doi.org/10.1016/j.gecco.2021.e01566 Citation Details
Baranowski, Kelsee and Taylor, Teairah and Lambert, Brian and Bharti, Nita "Application of Reflectance Ratios on High-Resolution Satellite Imagery to Remotely Identify Eucalypt Vegetation" Remote Sensing , v.12 , 2020 https://doi.org/10.3390/rs12244079 Citation Details
Becker, Daniel_J and Albery, Gregory_F and Kessler, Maureen_K and Lunn, Tamika_J and Falvo, Caylee_A and Czirják, Gábor_Á and Martin, Lynn_B and Plowright, Raina_K and Fenton, ed., Andy "Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence" Journal of Animal Ecology , v.89 , 2020 https://doi.org/10.1111/1365-2656.13166 Citation Details
Becker, Daniel J. and Crowley, Daniel E. and Washburne, Alex D. and Plowright, Raina K. "Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses" Biology Letters , v.15 , 2019 10.1098/rsbl.2019.0423 Citation Details
Becker, Daniel J. and Czirják, Gábor Á. and Rynda-Apple, Agnieszka and Plowright, Raina K. "Handling Stress and Sample Storage Are Associated with Weaker Complement-Mediated Bactericidal Ability in Birds but Not Bats" Physiological and Biochemical Zoology , v.92 , 2019 10.1086/701069 Citation Details
Becker, Daniel J. and Eby, Peggy and Madden, Wyatt and Peel, Alison J. and Plowright, Raina K. and Ostfeld, ed., Richard "Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts" Ecology Letters , v.26 , 2022 https://doi.org/10.1111/ele.14007 Citation Details
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PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

 

SUMMARY:

We are the first group to predict spillovers of an emerging bat-borne virus. Our work shows how viruses pass from bats to people and provides a method to predict and prevent spillover. Contrary to previous studies that have correlated viral spillover with deforestation and the distribution of reservoir hosts, our work provides spatial and temporal data to identify the mechanistic drivers of spillover. Moreover, our work reveals a solution to preventing spillover: protect and restore the forests that provide food for bats in winter. We integrated social science to empirically identify the narratives that would motivate people to adopt this preventative solution.

OUTCOMES:

We show that spillover is driven by interactions between winter habitat loss and climate-driven food shortages. We were able to predict spillovers of Hendra virus, based on the environmental conditions experienced by bats, and the location of bats. 

We brought together more than 25 datasets to describe the dynamics of Hendra virus that included information on bat behavior, distributions, reproduction and food availability, along with records of climate, habitat loss and environmental conditions. We used Bayesian network models to identify the mechanisms and correctly predicted the presence or absence of clusters of spillover in every year over the past 25 years. We showed that the loss of winter habitat was the key trigger to the emergence of Hendra virus and showed that when remnant winter forest produced abundant nectar, the bats left agricultural areas to feed in these patches of native forest, and spillover stopped. Our work suggests that regeneration of winter habitat should be an effective solution to spillover. This work was published in Nature (Eby et al. 2022, doi.org/10.1038/s41586-022-05506-2).

We used data on ecological history of bat populations, to show that only bats that have been displaced to novel habitats excreted more virus in winter. However, after a food shortage, all bat populations shed more virus, especially the bats in novel overwintering habitats. These results were recently published in Ecology Letters (Becker et al. 2022, doi.org/10.1111/ele.14007) and show an important mechanism linking land-use change, habitat loss, and spillover. 

We discovered that the amount of virus excreted by bats, rather than the proportion of bats excreting virus, is more important for explaining spillover patterns. Low-prevalence of Hendra virus outside of high risk periods may be non-infectious RNA shedding and may not contribute to spillover risk. Moreover, when bats shed more virus, such as after food shortages, they synchronously excreted a community of paramyxoviruses in a pulse (Peel et al. 2019). Given the novel way bats excrete viruses, we developed new methods and frameworks for modeling the dynamics in bats (Glennon et al. 2019, Giles et al. 2021, Hoegh et al. 2021, Lunn et al. 2021a, 2021b, 2021c). 

We worked with local and national restoration groups to incorporate bat winter habitat restoration into their activities. With collaborators, we developed and launched a free, online, archive of habitat restoration sites to increase the extent and viability of key winter habitat on the ALA BioCollect platform. This novel initiative provides a tool for restoration practitioners and has received wide support within Australia?s ecological restoration community.

We studied the narratives that change people's attitudes to bats, bat management, and spillover mitigation. We found that stories with characters and photographic images are more effective than information-only messages at mobilizing support for different forms of bat management, including habitat restoration (Guenther and Shanahan 2020). We also found that the more complex One-Health risk message leads not only to greater policy support for preventative measures, but also to greater support for a wider array of policy interventions. We are now working to incorporate these narratives in advocating for ecological countermeasures to spillover. Our findings also include data on an individual's primary source of information on Hendra virus, attitudes towards bats and Hendra virus vaccination to inform risk communication efforts. 

Our work is now influencing pandemic response and funding policies. Pronounced focus on medical countermeasures (e.g., detection, vaccination, and therapeutics) risks exclusion of spillover countermeasures, due to the erroneous perception of spillover as unsolvable, complex, and unclear. Our work on Hendra virus counters these concerns by showing spillover can be predicted and prevented by addressing underlying drivers of spillover cascades. Our empirical social science identified the narratives that will be most effective at encouraging adoption of preventative (rather than reactive) policies.  

This project supported 6 PhD students (5 female), 1 MS student (female), 5 postdocs (2 female), and 9 undergraduates (7 female). We published 73 papers in peer-reviewed journals, and multiple papers are in-review or preparation. We had over 68 media engagements and then >360 headlines that featured our paper in Nature, including in the New York Times, NPR, Nature News, and Le Monde. We engaged with community and policy-makers, and gave over 75 presentations to scientific audiences, policy-makers, and the general public.

 

 


Last Modified: 01/28/2023
Modified by: Raina K Plowright

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