The persistence of a SIR disease in a metapopulation: Hendra virus epidemics in Australian black flying foxes (Pteropus alecto)
Jaewoon Jeong
A B D and Hamish McCallum C
+ Author Affiliations
- Author Affiliations
A Environmental Futures Research Institute, Griffith University, Brisbane, Qld 4111, Australia.
B Present address: Centre for Veterinary Epidemiological Research, Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, C1A 4P3, Canada.
C Environmental Futures Research Institute and School of Environment and Science, Griffith University, Southport, Qld 4222, Australia.
D Corresponding author. Email: jjeong@upei.ca
Australian Journal of Zoology 69(1) 1-11 https://doi.org/10.1071/ZO20094
Submitted: 19 November 2020 Accepted: 14 April 2021 Published: 24 May 2021
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
Understanding how emerging viruses persist in bat populations is a fundamental step to understand the processes by which viruses are transmitted from reservoir hosts to spillover hosts. Hendra virus, which has caused fatal infections in horses and humans in eastern Australia since 1994, spills over from its natural reservoir hosts, Pteropus bats (colloquially known as flying foxes). It has been suggested that the Hendra virus maintenance mechanism in the bat populations might be implicated with their metapopulation structure. Here, we examine whether a metapopulation consisting of black flying fox (P. alecto) colonies that are smaller than the critical community size can maintain the Hendra virus. By using the Gillespie algorithm, stochastic mathematical models were used to simulate a cycle, in which viral extinction and recolonisation were repeated in a single colony within a metapopulation. Given estimated flying fox immigration rates, the simulation results showed that recolonisation occurred more frequently than extinction, which indicated that infection would not go extinct in the metapopulation. Consequently, this study suggests that a collection of transient epidemics of Hendra virus in numerous colonies of flying foxes in Australia can support the long-term persistence of the virus at the metapopulation level.
Keywords: black flying fox, Hendra virus, infection dynamics, metapopulation, reservoir hosts, stochastic model, viral invasion, viral persistence.
References
Bartlett, M. S. (1957). Measles periodicity and community size. Journal of the Royal Statistical Society. Series A (General) 120, 48–70.| Measles periodicity and community size.Crossref | GoogleScholarGoogle Scholar |
Breed, A. C., Breed, M. F., Meers, J., and Field, H. E. (2011). Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus) – implications for disease risk management. PLoS One 6, e28816.
| Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus) – implications for disease risk management.Crossref | GoogleScholarGoogle Scholar | 22194920PubMed |
Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V., and Schountz, T. (2006). Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19, 531–545.
| Bats: important reservoir hosts of emerging viruses.Crossref | GoogleScholarGoogle Scholar | 16847084PubMed |
Cross, P. C., Lloyd-Smith, J. O., Johnson, P. L. F., and Getz, W. M. (2005). Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations. Ecology Letters 8, 587–595.
| Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations.Crossref | GoogleScholarGoogle Scholar |
Edson, D., Field, H., McMichael, L., Jordan, D., Kung, N., Mayer, D., and Smith, C. (2015). Flying-fox roost disturbance and Hendra virus spillover risk. PLoS One 10, e0125881.
| Flying-fox roost disturbance and Hendra virus spillover risk.Crossref | GoogleScholarGoogle Scholar | 26625128PubMed |
Foley, J. E., Foley, P., and Pedersen, N. C. (1999). The persistence of a SIS disease in a metapopulation. Journal of Applied Ecology 36, 555–563.
| The persistence of a SIS disease in a metapopulation.Crossref | GoogleScholarGoogle Scholar |
Giles, J. R., Eby, P., Parry, H., Peel, A. J., Plowright, R. K., Westcott, D. A., and McCallum, H. (2018). Environmental drivers of spatiotemporal foraging intensity in fruit bats and implications for Hendra virus ecology. Scientific Reports 8, 9555.
| Environmental drivers of spatiotemporal foraging intensity in fruit bats and implications for Hendra virus ecology.Crossref | GoogleScholarGoogle Scholar | 29934514PubMed |
Gillespie, D. T. (2007). Stochastic simulation of chemical kinetics. Annual Review of Physical Chemistry 58, 35–55.
| Stochastic simulation of chemical kinetics.Crossref | GoogleScholarGoogle Scholar | 17037977PubMed |
Grenfell, B., and Harwood, J. (1997). (Meta)population dynamics of infectious diseases. Trends in Ecology & Evolution 12, 395–399.
| (Meta)population dynamics of infectious diseases.Crossref | GoogleScholarGoogle Scholar |
Hagenaars, T., Donnelly, C., and Ferguson, N. (2004). Spatial heterogeneity and the persistence of infectious diseases. Journal of Theoretical Biology 229, 349–359.
| Spatial heterogeneity and the persistence of infectious diseases.Crossref | GoogleScholarGoogle Scholar | 15234202PubMed |
Halpin, K., Young, P., Field, H., and Mackenzie, J. (2000). Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. The Journal of General Virology 81, 1927–1932.
| Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus.Crossref | GoogleScholarGoogle Scholar | 10900029PubMed |
Hanski, I. (1999). ‘Metapopulation Ecology.’ (Oxford University Press: Oxford.)
Hanski, I., and Gilpin, M. E. (1997). ‘Metapopulation Biology.’ (Academic Press: Cambridge, MA.)
Haydon, D. T., Cleaveland, S., Taylor, L. H., and Laurenson, M. K. (2002). Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 1468–1473.
| Identifying reservoirs of infection: a conceptual and practical challenge.Crossref | GoogleScholarGoogle Scholar | 12498665PubMed |
Jesse, M., Ezanno, P., Davis, S., and Heesterbeek, J. (2008). A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: movement and epidemic duration. Journal of Theoretical Biology 254, 331–338.
| A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: movement and epidemic duration.Crossref | GoogleScholarGoogle Scholar | 18577388PubMed |
Keeling, M. J. (2000). Metapopulation moments: coupling, stochasticity and persistence. Journal of Animal Ecology 69, 725–736.
| Metapopulation moments: coupling, stochasticity and persistence.Crossref | GoogleScholarGoogle Scholar |
Keeling, M. J., and Rohani, P. (2008). ‘Modeling Infectious Diseases in Humans and Animals.’ (Princeton University Press: Princeton.)
Levins, R. (1969). Some demographic and genetic consequences of environmental heterogeneity for biological control. Bulletin of the Entomological Society of America 15, 237–240.
| Some demographic and genetic consequences of environmental heterogeneity for biological control.Crossref | GoogleScholarGoogle Scholar |
Lu, Z., Schukken, Y. H., Smith, R. L., and Grohn, Y. T. (2013). Using vaccination to prevent the invasion of Mycobacterium avium subsp paratuberculosis in dairy herds: a stochastic simulation study. Preventive Veterinary Medicine 110, 335–345.
| Using vaccination to prevent the invasion of Mycobacterium avium subsp paratuberculosis in dairy herds: a stochastic simulation study.Crossref | GoogleScholarGoogle Scholar | 23419983PubMed |
Meade, J., Van der Ree, R., Stepanian, P. M., Westcott, D. A., and Welbergen, J. A. (2019). Using weather radar to monitor the number, timing and directions of flying-foxes emerging from their roosts. Scientific Reports 9, 10222.
| Using weather radar to monitor the number, timing and directions of flying-foxes emerging from their roosts.Crossref | GoogleScholarGoogle Scholar | 31308411PubMed |
Metcalf, C. J. E., Hampson, K., Tatem, A. J., Grenfell, B. T., and Bjornstad, O. N. (2013). Persistence in epidemic metapopulations: quantifying the rescue effects for measles, mumps, rubella and whooping cough. PLoS One 8, e74696.
| Persistence in epidemic metapopulations: quantifying the rescue effects for measles, mumps, rubella and whooping cough.Crossref | GoogleScholarGoogle Scholar |
Peel, A. J., Pulliam, J. R. C., Luis, A. D., Plowright, R. K., O’Shea, T. J., Hayman, D. T. S., Wood, J. L. N., Webb, C. T., and Restif, O. (2014). The effect of seasonal birth pulses on pathogen persistence in wild mammal populations. Proceedings of the Royal Society B: Biological Sciences 281, 20132962.
| The effect of seasonal birth pulses on pathogen persistence in wild mammal populations.Crossref | GoogleScholarGoogle Scholar | 24827436PubMed |
Pineda-Krch, M. (2008). GillespieSSA: implementing the Gillespie stochastic simulation algorithm in R. Journal of Statistical Software 25, 1–18.
| GillespieSSA: implementing the Gillespie stochastic simulation algorithm in R.Crossref | GoogleScholarGoogle Scholar |
Pineda-Krch, M. (2010). GillespieSSA: Gillespie’s stochastic simulation algorithm (SSA). R package version 0.5-4. Available at https://CRAN.R-project.org/package=GillespieSSA
Plowright, R. K. (2007). The ecology and epidemiology of Hendra virus in flying foxes. Ph.D. Thesis, University of California, Davis, USA.
Plowright, R., Foley, P., Field, H., Dobson, A., Foley, J., Eby, P., and Daszak, P. (2011). Urban habituation, connectivity, and stress synchrony: Hendra virus emergence from flying foxes (Pteropus spp.). EcoHealth 7, S36–S37.
Plowright, R. K., Eby, P., Hudson, P. J., Smith, I. L., Westcott, D., Bryden, W. L., Middleton, D., Reid, P. A., McFarlane, R. A., Martin, G., Tabor, G. M., Skerratt, L. F., Anderson, D. L., Crameri, G., Quammen, D., Jordan, D., Freeman, P., Wang, L. F., Epstein, J. H., Marsh, G. A., Kung, N. Y., and McCallum, H. (2015). Ecological dynamics of emerging bat virus spillover. Proceedings of the Royal Society B: Biological Sciences 282, 20142124.
| Ecological dynamics of emerging bat virus spillover.Crossref | GoogleScholarGoogle Scholar | 25392474PubMed |
Plowright, R. K., Peel, A. J., Streicker, D. G., Gilbert, A. T., McCallum, H., Wood, J., Baker, M. L., and Restif, O. (2016). Transmission or within-host dynamics driving pulses of zoonotic viruses in reservoir–host populations. PLoS Neglected Tropical Diseases 10, e0004796.
| Transmission or within-host dynamics driving pulses of zoonotic viruses in reservoir–host populations.Crossref | GoogleScholarGoogle Scholar | 27489944PubMed |
Roberts, B. J., Catterall, C. P., Eby, P., and Kanowski, J. (2012). Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS One 7, e42532.
| Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management.Crossref | GoogleScholarGoogle Scholar | 22880021PubMed |
Tait, J., Perotto-Baldivieso, H. L., McKeown, A., and Westcott, D. A. (2014). Are flying-foxes coming to town? Urbanisation of the spectacled flying-fox (Pteropus conspicillatus) in Australia. PLoS One 9, e109810.
| Are flying-foxes coming to town? Urbanisation of the spectacled flying-fox (Pteropus conspicillatus) in Australia.Crossref | GoogleScholarGoogle Scholar | 25295724PubMed |
Towsey, J. (2017). Pteropus alecto Sunshine Coast. Available at https://www.movebank.org/panel_embedded_movebank_webapp
Tran-Thi, C.-G., Choisy, M., and Zucker, J. D. (2016). Quantifying the effect of synchrony on the persistence of infectious diseases in a metapopulation. In ‘Computing, and Communication Technologies, Research, Innovation, and Vision for the Future (RIVF), 2016 IEEE RIVF International Conference’. pp. 229–234. (IEEE.)
Vardon, M. J., and Tidemann, C. R. (2000). The black flying-fox (Pteropus alecto) in north Australia: juvenile mortality and longevity. Australian Journal of Zoology 48, 91–97.
| The black flying-fox (Pteropus alecto) in north Australia: juvenile mortality and longevity.Crossref | GoogleScholarGoogle Scholar |
Vynnycky, E., and White, R. (2010). ‘An Introduction to Infectious Disease Modelling.’ (Oxford University Press: Oxford.)
Wang, H. H., Kung, N. Y., Grant, W. E., Scanlan, J. C., and Field, H. E. (2013). Recrudescent infection supports Hendra virus persistence in Australian flying-fox populations. PLoS One 8, e80430.
| Recrudescent infection supports Hendra virus persistence in Australian flying-fox populations.Crossref | GoogleScholarGoogle Scholar | 24312221PubMed |
