English
French
Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.).
Abstract: Anthropogenic environmental change is often implicated in the emergence of new zoonoses from wildlife; however, there is little mechanistic understanding of these causal links. Here, we examine the transmission dynamics of an emerging zoonotic paramyxovirus, Hendra virus (HeV), in its endemic host, Australian Pteropus bats (fruit bats or flying foxes). HeV is a biosecurity level 4 (BSL-4) pathogen, with a high case-fatality rate in humans and horses. With models parametrized from field and laboratory data, we explore a set of probable contributory mechanisms that explain the spatial and temporal pattern of HeV emergence; including urban habituation and decreased migration-two widely observed changes in flying fox ecology that result from anthropogenic transformation of bat habitat in Australia. Urban habituation increases the number of flying foxes in contact with human and domestic animal populations, and our models suggest that, in addition, decreased bat migratory behaviour could lead to a decline in population immunity, giving rise to more intense outbreaks after local viral reintroduction. Ten of the 14 known HeV outbreaks occurred near urbanized or sedentary flying fox populations, supporting these predictions. We also demonstrate that by incorporating waning maternal immunity into our models, the peak modelled prevalence coincides with the peak annual spill-over hazard for HeV. These results provide the first detailed mechanistic framework for understanding the sporadic temporal pattern of HeV emergence, and of the urban/peri-urban distribution of HeV outbreaks in horses and people.
Publication Date: 2011-05-11 PubMed ID: 21561971PubMed Central: PMC3203503DOI: 10.1098/rspb.2011.0522Google Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- N.I.H.
- Extramural
- Research Support
- Non-U.S. Gov't
- Research Support
- U.S. Gov't
- Non-P.H.S.
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research explores how the changes in lifestyle and ecology of fruit bats or flying foxes caused by human activity may contribute to the emergence of the Hendra virus, a dangerous pathogen affecting both humans and horses. The study uses data-based models to associate urban habituation and decline in bat migration with increased contact with human populations and reduced immunity, respectively, which can lead to more intense virus outbreaks.
Anthropogenic Environmental Change and Zoonoses
- The study begins by acknowledging the impact of anthropogenic (human-led) environmental changes on the emergence of new zoonoses, diseases that can be transmitted from animals to humans. However, it notes that there is insufficient understanding of the precise mechanisms through which these links occur.
- The zoonosis of interest here is the Hendra virus (HeV), a highly dangerous pathogen that can be found in Australian Pteropus bats and can be transmitted to humans and horses.
- The researchers highlight the need for more in-depth study of the transmission dynamics of this virus to understand how and why it emerges.
Role of Urban Habituation and Migration Change
- Urban habituation refers to the adaptation of wildlife to living in urban areas. This adaptation has been observed in flying foxes, and the study suggests that it increases the contact between these bats and human populations.
- Additionally, the transformation of bat habitats as a result of human activity has led to decreased migratory behaviour, which the researchers hypothesize could contribute to diminished population immunity and consequently more severe outbreaks of HeV following its local reintroduction.
Supporting Evidence and Prediction Verification
- The researchers validate their predictions by noting that ten of the fourteen observed HeV outbreaks occurred close to urbanized or stationary flying fox populations.
- The study also uses models accounting for waning maternal immunity to show that the timing of the highest predicted prevalence of the virus correlates with the peak annual risk for HeV transmission, known as spill-over hazard.
Significance of the Research
- The findings of this research put forth a detailed understanding of how the emergence of the Hendra virus is linked to the changing ecological behaviour of flying foxes due to human activities.
- This study provides a fundamental framework for understanding the irregular, mainly urban/peri-urban, occurrence of HeV outbreaks in horses and humans, which can guide future research and mitigation strategies.
Cite This Article
APA
Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, Daszak P.
(2011).
Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.).
Proc Biol Sci, 278(1725), 3703-3712.
https://doi.org/10.1098/rspb.2011.0522 Publication
Researcher Affiliations
- Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA. rplowright@gmail.com
MeSH Terms
- Animals
- Australia
- Bayes Theorem
- Chiroptera / virology
- Ecosystem
- Epidemics
- Hendra Virus
- Henipavirus Infections / epidemiology
- Henipavirus Infections / immunology
- Henipavirus Infections / transmission
- Humans
- Population Dynamics
- Zoonoses / epidemiology
- Zoonoses / virology
Grant Funding
- R01 TW005869 / FIC NIH HHS
- R01-TW05869 / FIC NIH HHS
References
This article includes 69 references
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases.. Nature 2008 Feb 21;451(7181):990-3.
- Morse S. S. 1993. Examining the origins of emerging viruses. In Emerging viruses (ed. Morse S. S.), pp. 10u201328 New York, NY: Oxford University Press
- Weiss RA, McMichael AJ. Social and environmental risk factors in the emergence of infectious diseases.. Nat Med 2004 Dec;10(12 Suppl):S70-6.
- Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens.. Emerg Infect Dis 2005 Dec;11(12):1842-7.
- Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JR, Dobson AP, Hudson PJ, Grenfell BT. Epidemic dynamics at the human-animal interface.. Science 2009 Dec 4;326(5958):1362-7.
- Plowright R. K., Sokolow S. H., Gorman M. E., Daszak P., Foley J. E. 2008. Causal inference in disease ecology: investigating ecological drivers of disease emergence. Front. Ecol. Environ. 6, 420u201342910.1890/070086 (doi:10.1890/070086)
- Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: important reservoir hosts of emerging viruses.. Clin Microbiol Rev 2006 Jul;19(3):531-45.
- Dobson AP. Virology. What links bats to emerging infectious diseases?. Science 2005 Oct 28;310(5748):628-9.
- Halpin K, Hyatt AD, Plowright RK, Epstein JH, Daszak P, Field HE, Wang L, Daniels PW. Emerging viruses: coming in on a wrinkled wing and a prayer.. Clin Infect Dis 2007 Mar 1;44(5):711-7.
- Mackenzie JS, Chua KB, Daniels PW, Eaton BT, Field HE, Hall RA, Halpin K, Johansen CA, Kirkland PD, Lam SK, McMinn P, Nisbet DJ, Paru R, Pyke AT, Ritchie SA, Siba P, Smith DW, Smith GA, van den Hurk AF, Wang LF, Williams DT. Emerging viral diseases of Southeast Asia and the Western Pacific.. Emerg Infect Dis 2001;7(3 Suppl):497-504.
- Murray K, Selleck P, Hooper P, Hyatt A, Gould A, Gleeson L, Westbury H, Hiley L, Selvey L, Rodwell B. A morbillivirus that caused fatal disease in horses and humans.. Science 1995 Apr 7;268(5207):94-7.
- Daszak P., et al. & H. E. R. G. H 2006. The emergence of Nipah and Hendra virus: pathogen dynamics across a wildlife-livestock-human continuum. In Disease ecology: community structure and pathogen dynamics (eds Collinge S., Ray C.), pp. 186u2013201 Oxford, UK: Oxford University Press
- Field H, Young P, Yob JM, Mills J, Hall L, Mackenzie J. The natural history of Hendra and Nipah viruses.. Microbes Infect 2001 Apr;3(4):307-14.
- Hsu VP, Hossain MJ, Parashar UD, Ali MM, Ksiazek TG, Kuzmin I, Niezgoda M, Rupprecht C, Bresee J, Breiman RF. Nipah virus encephalitis reemergence, Bangladesh.. Emerg Infect Dis 2004 Dec;10(12):2082-7.
- Eby P. 1991. Seasonal movements of gray-headed flying-foxes, Pteropus poliocephalus (chiroptera, Pteropodidae), from 2 maternity camps in northern New-South-Wales. Wildlife Res. 18, 547u201355910.1071/WR9910547 (doi:10.1071/WR9910547)
- Markus N., Hall L. 2004. Foraging behaviour of the black flying-fox (Pteropus alecto) in the urban landscape of Brisbane, Queensland. Wildlife Res. 31, 345u201335510.1071/WR01117 (doi:10.1071/WR01117)
- Parry-Jones K. A., Augee M. L. 1992. Movements of gray-headed flying foxes (Pteropus poliocephalus) to and from a colony site on the central coast of New South Wales. Wildlife Res. 19, 331u201334010.1071/WR9920331 (doi:10.1071/WR9920331)
- Vardon M. J., Tidemann C. R. 1998. Reproduction, growth and maturity in the black flying-fox, Pteropus alecto (Megachiroptera: Pteropodidae). Aust. J. Zool. 46, 329u201334410.1071/ZO98023 (doi:10.1071/ZO98023)
- Halpin K, Hyatt AD, Fogarty R, Middleton D, Bingham J, Epstein JH, Rahman SA, Hughes T, Smith C, Field HE, Daszak P. Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission.. Am J Trop Med Hyg 2011 Nov;85(5):946-51.
- Halpin K, Young PL, Field HE, Mackenzie JS. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus.. J Gen Virol 2000 Aug;81(Pt 8):1927-1932.
- Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus).. Proc Biol Sci 2008 Apr 7;275(1636):861-9.
- Eby P., Richards G., Collins L., Parry-Jones K. 1999. The distribution, abundance and vulnerability to population reduction of a nomadic nectarivore, the grey-headed flying-fox Pteropus poliocephalus in New South Wales, during a period of resource concentration. Aust. Zool. 31, 240u2013253
- Hall L., Richards G. 2000. Flying foxes: fruit and blossom bats of Australia. Australian natural history series. Sydney, Australia: University of New South Wales Press Ltd
- Woinarski J. C. Z., Whitehead P. J., Bowman D. M. J. S., Russell-Smith J. 1992. Conservation of mobile species in a variable environment: the problem of reserve design in the northern territory, Australia. Global Ecol. Biogeogr. Lett. 2, 1u20131010.2307/2997325 (doi:10.2307/2997325)
- Noble I., et al. 1996. Land resources. In Australia: state of the environment 1996. Collingwood, Australia: CSIRO Publishing
- Eby P. 2000. The results of four synchronous assessments of relative distribution and abundance of grey-headed flying-fox Pteropus poliocephalus. In Proc. Workshop to Assess the Status of the Grey-headed Flying Fox in New South Wales (eds Richards G., Hall L.), pp. 66u201377 Canberra, Australia: Australian Bat Society; See http://batcall.csu.edu.au/abs/ghff/ghffproceedings.pdf
- Eby P. 2002. National count of grey-headed flying-foxesu2014July 27 & 28, 2002. Report to Environment Australia, Queensland Parks and Wildlife Service, NSW National Parks and Wildlife Service, Victoria Department Natural Resources and Environment
- Eby P. 2003. National count of grey-headed flying-foxesu2014April 12 & 13, 2003. Report to Environment Australia, Queensland Parks and Wildlife Service, NSW National Parks and Wildlife Service, and Victoria Department Natural Resources and Environment
- Eby P. 2004. National count of grey-headed flying-foxesu2014April 3 & 4, 2004. Report to the Department of Environment and Heritage, Canberra
- Birt P. 2004. Mutualistic interactions between the nectar-feeding little red flying fox Pteropus scapulatus (Chiroptera: Pteropodidae) and flowering eucalypts (Myrtaceae): habitat utilisation and pollination. PhD thesis, University of Queensland, Brisbane, Australia
- Roberts B. J. 2005. Habitat characteristics of flying fox camps in south-east Queensland. B Sc. (Hons) thesis, Griffith University, Nathan, Queensland, Australia
- Shilton L., Latch P., McKeown A., Pert P., Westcott D. 2008. Landscape-scale redistribution of a highly mobile threatened species, Pteropus conspicillatus (Chiroptera, Pteropodidae), in response to Tropical Cyclone Larry. Austral Ecol. 33, 549u201356110.1111/j.1442-9993.2008.01910.x (doi:10.1111/j.1442-9993.2008.01910.x)
- McDonald-Madden E., Schreiber E. S. G., Forsyth D. M., Choquenot D., Clancy T. F. 2005. Factors affecting grey-headed flying-fox (Pteropus poliocephalus: Pteropodidae) foraging in the Melbourne metropolitan area, Australia. Austral Ecol. 30, 600u201360810.1111/j.1442-9993.2005.01492.x (doi:10.1111/j.1442-9993.2005.01492.x)
- Parry-Jones K., Augee M. 2001. Factors affecting the occupation of a colony site in Sydney, New South Wales by the grey-headed flying-fox Pteropus poliocephalus (Pteropodidae). Austral Ecol. 26, 47u201355
- Parry-Jones K. A., Augee M. L. 1991. Food selection by gray-headed flying foxes (Pteropus poliocephalus) occupying a summer colony site near Gosford, New South Wales. Wildlife Res. 18, 111u201312410.1071/WR9910111 (doi:10.1071/WR9910111)
- Tidemann C. R., Nelson J. E. 2004. Long-distance movements of the grey-headed flying fox (Pteropus poliocephalus). J. Zool. Lond. 263, 141u201314610.1017/S0952836904004960 (doi:10.1017/S0952836904004960)
- Catterall C., Storey R., Kingston M. B. 1997. Reality versus rhetoric: a case study monitoring regional deforestation. In Conservation outside nature reserves (eds Hale P., Lamb D.), pp. 367u2013377 Brisbane, Australia: Centre for Conservation Biology, Queensland
- McIlwee A. P., Martin L. 2002. On the intrinsic capacity for increase of Australian flying-foxes (Pteropus spp., Megachiroptera). Aust. Zool. 32, 76u2013100
- Field H. 2005. The ecology of Hendra virus and Australian bat lyssavirus. PhD thesis, School of veterinary science, The University of Queensland, Brisbane, Australia
- Anderson R., May R. 1991. Infectious diseases of humans. Oxford, UK: Oxford University Press
- Kermack W. O., McKendrick A. G. 1927. A contribution to the mathematical theory of epidemics. Proc. R. Soc. Lond. A 115, 700u201372110.1098/rspa.1927.0118 (doi:10.1098/rspa.1927.0118)
- Black F. L. 1991. Epidemiology of paramyxoviridae. In The paramyxoviruses (ed. Kingsbury D. W.), pp. 509u2013536 New York, NY: Plenum Press
- Coyne MJ, Burr JH, Yule TD, Harding MJ, Tresnan DB, McGavin D. Duration of immunity in dogs after vaccination or naturally acquired infection.. Vet Rec 2001 Oct 27;149(17):509-15.
- Fraser K. B., Martin S. J. 1978. Measles virus and its biology. New York, NY: Academic Press
- Birt P., Markus N. 1999. Notes on the temporary displacement of Pteropus alecto and P. poliocephalus by P. scapulatus within a daytime campsite. Aust. Mammal. 21, 107u2013110
- Markus N. 2002. Behaviour of the black flying fox Pteropus alecto. I. Territoriality and courtship. Acta Chiropterol. 4, 153u2013166
- Halpin K. 2000. Genetic studies of Hendra virus and other novel paramyxoviruses. St. Lucia: Department of Microbiology and Parasitology, University of Queensland
- Nelson J. E. 1965. Movements of Australian Flying Foxes (Pteropodidae: Megachiroptera). Aust. J. Zool. 13, 53u20137310.1071/ZO9650053 (doi:10.1071/ZO9650053)
- Ratcliffe F. N. 1931. The flying fox in Australia (Pteropus). Commonwealth Counc. Sci. Ind. Res. Bull. 53, 1u201381
- Ratcliffe F. N. 1932. Notes of the fruit bats (Pteropus spp.) of Australia. J. Anim. Ecol. 1, 32u20135710.2307/993 (doi:10.2307/993)
- Palmer C. 1997. Ecology of the black flying-fox, Pteropus alecto in the seasonal tropics of the Northern Territory: resource tracking in a landscape mosaic and role in seed dispersal. Darwin, Australia: Northern Territory University
- Palmer C., Woinarski J. C. Z. 1999. Seasonal roosts and foraging movements of the black flying fox (Pteropus alecto) in the Northern Territory: resource tracking in a landscape mosaic. Wildlife Res. 26, 823u201383810.1071/WR97106 (doi:10.1071/WR97106)
- Grenfell B, Harwood J. (Meta)population dynamics of infectious diseases.. Trends Ecol Evol 1997 Oct;12(10):395-9.
- Keeling MJ, Gilligan CA. Metapopulation dynamics of bubonic plague.. Nature 2000 Oct 19;407(6806):903-6.
- Grenfell BT, Bju00f8rnstad ON, Kappey J. Travelling waves and spatial hierarchies in measles epidemics.. Nature 2001 Dec 13;414(6865):716-23.
- Dobson A, Foufopoulos J. Emerging infectious pathogens of wildlife.. Philos Trans R Soc Lond B Biol Sci 2001 Jul 29;356(1411):1001-12.
- Pulliam JR. Viral host jumps: moving toward a predictive framework.. Ecohealth 2008 Mar;5(1):80-91.
- Woolhouse ME, Haydon DT, Antia R. Emerging pathogens: the epidemiology and evolution of species jumps.. Trends Ecol Evol 2005 May;20(5):238-44.
- Duncan A., Baker G. B., Montgomery N. 1999. The action plan for Australian bats. Canberra, Australia: Environment Australia
- Field HE, Breed AC, Shield J, Hedlefs RM, Pittard K, Pott B, Summers PM. Epidemiological perspectives on Hendra virus infection in horses and flying foxes.. Aust Vet J 2007 Jul;85(7):268-70.
- van der Ree R., McDonnell M. J., Temby I., Nelson J., Whittingham E. 2006. The establishment and dynamics of a recently established urban camp of flying foxes (Pteropus poliocephalus) outside their geographic range. J. Zool. 268, 177u201318510.1111/j.1469-7998.2005.00005.x (doi:10.1111/j.1469-7998.2005.00005.x)
- Hooper PT, Gould AR, Russell GM, Kattenbelt JA, Mitchell G. The retrospective diagnosis of a second outbreak of equine morbillivirus infection.. Aust Vet J 1996 Sep;74(3):244-5.
- O'Sullivan JD, Allworth AM, Paterson DL, Snow TM, Boots R, Gleeson LJ, Gould AR, Hyatt AD, Bradfield J. Fatal encephalitis due to novel paramyxovirus transmitted from horses.. Lancet 1997 Jan 11;349(9045):93-5.
- Cummings DA, Irizarry RA, Huang NE, Endy TP, Nisalak A, Ungchusak K, Burke DS. Travelling waves in the occurrence of dengue haemorrhagic fever in Thailand.. Nature 2004 Jan 22;427(6972):344-7.
- Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. Seasonality and the dynamics of infectious diseases.. Ecol Lett 2006 Apr;9(4):467-84.
- Hosseini PR, Dhondt AA, Dobson A. Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches.. Proc Biol Sci 2004 Dec 22;271(1557):2569-77.
- Begon M, Hazel SM, Baxby D, Bown K, Cavanagh R, Chantrey J, Jones T, Bennett M. Transmission dynamics of a zoonotic pathogen within and between wildlife host species.. Proc Biol Sci 1999 Oct 7;266(1432):1939-45.
- Swinton J., Harwood J., Grenfell B. T., Gilligan C. A. 1998. Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations. J. Anim. Ecol. 67, 54u20136810.1046/j.1365-2656.1998.00176.x (doi:10.1046/j.1365-2656.1998.00176.x)
- Rahman SA, Hassan SS, Olival KJ, Mohamed M, Chang LY, Hassan L, Saad NM, Shohaimi SA, Mamat ZC, Naim MS, Epstein JH, Suri AS, Field HE, Daszak P. Characterization of Nipah virus from naturally infected Pteropus vampyrus bats, Malaysia.. Emerg Infect Dis 2010 Dec;16(12):1990-3.
Citations
This article has been cited 148 times.Secure Payments
Satisfaction Guarantee
We offer a 60-day guarantee to ensure you are completely satisfied.
Fast & Free Shipping
We provide fast and free shipping on all orders over $40.