EcoHealth

, Volume 13, Issue 1, pp 26–38 | Cite as

Landscape Utilisation, Animal Behaviour and Hendra Virus Risk

  • H. E. Field
  • C. S. Smith
  • C. E. de Jong
  • D. Melville
  • A. Broos
  • N. Kung
  • J. Thompson
  • D. K. N. Dechmann
Original Contribution

Abstract

Hendra virus causes sporadic fatal disease in horses and humans in eastern Australia. Pteropid bats (flying-foxes) are the natural host of the virus. The mode of flying-fox to horse transmission remains unclear, but oro-nasal contact with flying-fox urine, faeces or saliva is the most plausible. We used GPS data logger technology to explore the landscape utilisation of black flying-foxes and horses to gain new insight into equine exposure risk. Flying-fox foraging was repetitious, with individuals returning night after night to the same location. There was a preference for fragmented arboreal landscape and non-native plant species, resulting in increased flying-fox activity around rural infrastructure. Our preliminary equine data logger study identified significant variation between diurnal and nocturnal grazing behaviour that, combined with the observed flying-fox foraging behaviour, could contribute to Hendra virus exposure risk. While we found no significant risk-exposing difference in individual horse movement behaviour in this study, the prospect warrants further investigation, as does the broader role of animal behaviour and landscape utilisation on the transmission dynamics of Hendra virus.

Keywords

Hendra virus Emerging disease Flying-fox Bat Horse Landscape Behaviour Risk 

References

  1. Allworth A, O’Sullivan J, Selvey L, Sheridan J (1995) Equine morbillivirus in Queensland. Communicable Diseases Intelligence 19:575.Google Scholar
  2. Anon (2012) Management and restoration of flying-fox camps: guidelines and recommendations. SEQ Catchments Ltd. http://www.seqcatchments.com.au/programs/biodiversity-priority-species-and-habitats-flying-foxes. Accessed Jan 12, 2015.
  3. Baldock FC, Douglas IC, Halpin K, Field H, Young PL, Black PF (1996) Epidemiological investigations into the 1994 equine morbillivirus outbreaks in Queensland, Australia. Singapore Veterinary Journal 20:57–61.Google Scholar
  4. Berger A, Scheibe KM, Eichhorn K, Scheibe A, Streich J (1999) Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii) measured through one year under semi-reserve conditions. Applied Animal Behaviour Science 64:1–17.CrossRefGoogle Scholar
  5. Biosecurity Queensland (2012) Fruiting and Flowering Trees. Brisbane: The Department of Agriculture, Forestry & Fisheries. Queensland Government. http://www.daff.qld.gov.au/__data/assets/pdf_file/0010/69580/fruiting-and-flowering-trees.pdf. Accessed Dec 18, 2014.
  6. Biosecurity Queensland (2014) What is Hendra Virus. Brisbane: The Department of Agriculture, Forestry & Fisheries. Queensland Government. http://www.daff.qld.gov.au/animal-industries/animal-health-and-diseases/a-z-list/hendra-virus/general-information/what-is-hendra-virus. Accessed Dec 28, 2014.
  7. Birt P, Hall LS, Smith GC (1997) Ecomorphology of teh tongues of Australian Megachiroptera (Chiroptera: Pteropodidae). Australian Journal of Zoology 45:369–384.CrossRefGoogle Scholar
  8. Bostock PD, Holland AE (2010) Census of the Queensland Flora. Brisbane: Queensland Herbarium Biodiversity and Ecosystem Sciences, Department of Environment and Resource Management, pp. 1–320.Google Scholar
  9. Chua K, Koh C, Hooi P, Wee K, Khong J, Chua B, et al. (2002) Isolation of Nipah virus from Malaysian Island flying foxes. Microbes Infect 4:145–151.CrossRefPubMedGoogle Scholar
  10. Churchill S (2008) Australian Bats, Sydney: Allen & Unwin.Google Scholar
  11. Cochran WW (1980) Wildlife telemetry. In: Wildlife Management Techniques Manual, Schemnitz SD (editor), Washington, DC: The Wildlife Society, pp 507–520.Google Scholar
  12. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449.CrossRefPubMedGoogle Scholar
  13. de Jong CE, Field HE, Tagtag A, Hughes T, Dechmann D, Jayme S, et al. (2013) Foraging behaviour and landscape utilisation by the endangered golden-crowned flying fox (Acerodon jubatus), The Philippines. PLoS One 8:e79665.CrossRefPubMedGoogle Scholar
  14. de Jong CE, Jonsson N, Field H, Smith C, Crichton EG, Phillips N, et al. (2005) Collection, seminal characteristics and chilled storage of spermatozoa from three species of free-range flying fox (Pteropus spp.). Theriogenology 64:1072–1089.CrossRefPubMedGoogle Scholar
  15. Epstein JH, Field HE (2011) Disease surveillance in free-ranging bat populations: challenges and logistical considerations. In: Investigating the Role of Bats in Emerging Zoonoses: Balancing Ecology, Conservation and Public Health Interest, Newman SH, Field HE, Epstein JH, de Jong CE (editors), Rome: Food and Agriculture Organization of the United Nations, pp 47–62.Google Scholar
  16. Field H, Crameri G, Kung N, Wang L (2012) Ecological aspects of Hendra virus. Current Topics in Microbiology and Immunology 359:11–23.PubMedGoogle Scholar
  17. Field H, Kung N (2011) Henipaviruses—unanswered questions of lethal zoonoses. Current Opinion in Virology 1:658–661.CrossRefPubMedGoogle Scholar
  18. Field H, Young P, Yob JM, Mills J, Hall L, Mackenzie J (2001) The natural history of Hendra and Nipah viruses. Microbes and Infection 3:307–314.CrossRefPubMedGoogle Scholar
  19. Field HE (2005) The ecology of Hendra virus and Australian bat lyssavirus. In: Ph.D. thesis, Brisbane: The University of Queensland.Google Scholar
  20. Field HE, De Jong C, Melville D, Smith C, Smith I, Broos A, et al. (2011) Hendra virus infection dynamics in Australian fruit bats. PLoS One 6:e28678.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fogarty R, Halpin K, Hyatt AD, Daszak P, Mungall BA (2008) Henipavirus susceptibility to environmental variables. Virus Research 132:140–144.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goldspink LK, Edson DW, Vidgen ME, Bingham J, Field HE, Smith CS (2015) Natural Hendra virus infection in flying-foxes—tissue tropism and risk factors. PLoS One 10(6):e0128835. doi:10.1371/journal.pone.0128835.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hall L (2009) A Wild Australia Guide: Bats. Queensland: Steve Parish Publishing.Google Scholar
  24. Hall L, Richards G (2000) Flying Foxes: Fruit and Blossom Bats of Australia. Malabar: Krieger Publishing.Google Scholar
  25. Halpin K, Hyatt AD, Fogarty R, Middleton D, Bingham J, Epstein JH, et al. (2011) Pteropid bats are confirmed as the reservoir hosts of Henipaviruses: a comprehensive experimental study of virus transmission. American Journal of Tropical Medicine and Hygiene 85:946–951.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Halpin K, Young PL, Field HE, Mackenzie JS (2000) Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. Journal of General Virology 81:1927–1932.CrossRefPubMedGoogle Scholar
  27. Hanna JN, McBride WJ, Brookes DL, Shield J, Taylor CT, Smith IL, et al. (2006) Hendra virus infection in a veterinarian. Medical Journal of Australia 185:562–564.PubMedGoogle Scholar
  28. Jonsson NN, Johnston SD, Field H, de Jong C, Smith C (2004) Field anaesthesia of three Australian species of flying fox. Veterinary Record 154:664–664.CrossRefPubMedGoogle Scholar
  29. Markus N, Hall L (2004) Foraging behaviour of the black flying-fox (Pteropus alecto) in the urban landscape of Brisbane, Queensland. Wildlife Research 31:345–355.CrossRefGoogle Scholar
  30. Marsh GA, Haining J, Hancock TJ, Robinson R, Foord AJ, Barr JA, et al. (2011) Experimental infection of horses with Hendra virus/Australia/horse/2008/Redlands. Emerging Infectious Diseases 17:2232–2238.CrossRefPubMedPubMedCentralGoogle Scholar
  31. McFarlane R, Becker N, Field H (2011) Investigation of the climatic and environmental context of Hendra virus spillover events 1994–2010. PLoS One 6(12):e28374. doi:10.1371/journal.pone.0028374.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Murray K, Selleck P, Hooper P, Hyatt A, Gould A, Gleeson L, et al. (1995) A morbillivirus that caused fatal disease in horses and humans. Science 268:94–97.CrossRefPubMedGoogle Scholar
  33. O’Sullivan JD, Allworth AM, Paterson DL, Snow TM, Boots R, Gleeson LJ, et al. (1997) Fatal encephalitis due to novel paramyxovirus transmitted from horses. Lancet 349:93–95.CrossRefPubMedGoogle Scholar
  34. Palmer C, Price O, Bach C (2000) Foraging ecology of the black flying fox (Pteropus alecto) in the seasonal tropics of the Northern Territory, Australia. Wildlife Research 27:169–178.CrossRefGoogle Scholar
  35. Palmer C, Woinarski JCZ (1999) Seasonal roosts and foraging movements of the black flying fox (Pteropus alecto) in the Northern Territory: resource tracking in a landscape mosaic. Wildlife Research 26:823–838.CrossRefGoogle Scholar
  36. Parry-Jones KA, Augee ML (1992) Movements of grey-headed flying foxes (Pteropus poliocephalus) to and from a cology site on the central coast of New South Wales. Wildlife Research 19:331–340.CrossRefGoogle Scholar
  37. Playford EG, McCall B, Smith G, Slinko V, Allen G, Smith I, et al. (2010) Human Hendra virus encephalitis associated with equine outbreak, Australia, 2008. Emerging Infectious Diseases 16:219–223.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, et al. (2011) Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proceedings of the Royal Society of London B. 278:3703–3712.CrossRefGoogle Scholar
  39. Queensland Herbarium (2011) Regional Ecosystem Description Database (Version 6.0b, updated January 2011), Brisbane: Queensland Government Department of Environment and Resource Management. https://www.qld.gov.au/environment/plants-animals/plants/ecosystems/descriptions/. Accessed Oct 18, 2011.
  40. Richards GC (1995) A review of ecological interactions of fruit bats in Australian ecosystems. Symposia of the Zoological Society of London 67:79–96.Google Scholar
  41. Roberts BJ, Catteral CP, Eby P, Kanowski J (2012) Latitudinal range shifts in Australian flying-foxes: a re-evaluation. Austral Ecology 37:12–22.CrossRefGoogle Scholar
  42. Scanlan J, Kung N, Selleck P, Field H (2014) Survival of Hendra virus in the environment—modelling the effect of temperature. EcoHealth. doi: 10.1007/s10393-014-0920-4
  43. Selvey L, Sheridan J (1994) Outbreak of severe respiratory disease in humans and horses due to a previously unrecognised paramyxovirus. Communicable Diseases Intelligence 18:499.Google Scholar
  44. Selvey LA, Wells RM, McCormack JG, Ansford AJ, Murray K, Rogers RJ, et al. (1995) Infection of humans and horses by a newly described morbillivirus. Medical Journal of Australia 162:642–645.PubMedGoogle Scholar
  45. Smith CS, Skelly C, Kung N, Roberts BJ, Field HE (2014) Flying-fox species diversity—a spatial risk factor for Hendra virus infection in horses in eastern Australia. PLoS One 9:1–7.Google Scholar
  46. Smith I, Broos A, de Jong C, Zeddeman A, Smith C, Smith G, et al. (2011) Identifying hendra virus diversity in pteropid bats. PLoS One 6:e25275.CrossRefPubMedPubMedCentralGoogle Scholar
  47. USA Department of Defense (2008) Global Positioning System Standard Positioning Service Performance Standard, 4th ed. http://www.gps.gov/technical/ps/2008-SPS-performance-standard.pdf. Accessed Aug 06, 2015.
  48. Westbury HA, Hooper PT, Brouwer SL, Selleck PW (1996) Susceptibility of cats to equine morbillivirus. Australian Veterinary Journal 74:132–134.CrossRefPubMedGoogle Scholar
  49. Williamson M, Hooper P, Selleck P, Gleeson L, Daniels P, Westbury H, et al. (1998a) Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Australian Veterinary Journal 76:813–818.CrossRefPubMedGoogle Scholar
  50. Williamson MM, Hooper PT, Selleck PW, Gleeson LJ, Daniels PW, Westbury HA, et al. (1998b) Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Australian Veterinary Journal 76:813–818.CrossRefPubMedGoogle Scholar
  51. Young PL, Halpin K, Selleck PW, Field H, Gravel JL, Kelly MA, et al. (1996) Serologic evidence for the presence in pteropus bats of a paramyxovirus related to equine morbillivirus. Emerging Infectious Diseases 2:239–240.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Association for Ecology and Health 2015

Authors and Affiliations

  • H. E. Field
    • 1
    • 2
  • C. S. Smith
    • 1
  • C. E. de Jong
    • 1
  • D. Melville
    • 1
  • A. Broos
    • 1
  • N. Kung
    • 1
  • J. Thompson
    • 3
  • D. K. N. Dechmann
    • 4
  1. 1.Queensland Centre for Emerging Infectious Diseases, Biosecurity Queensland, Department of Agriculture and FisheriesBrisbaneAustralia
  2. 2.EcoHealth AllianceNew YorkUSA
  3. 3.Queensland Herbarium, Department of Environment and Heritage ProtectionBrisbaneAustralia
  4. 4.Max Planck Institute for OrnithologyRadolfzellGermany

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