Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats

Risk-based surveillance of avian influenza in Australia’s wild birds

John P. Tracey

Invasive Animals Cooperative Research Centre, Vertebrate Pest Research Unit, Industry & Investment NSW, Forest Road, Orange, New South Wales 2800, Australia. Email: john.tracey@industry.nsw.gov.au

Wildlife Research 37(2) 134-144 http://dx.doi.org/10.1071/WR09152
Submitted: 4 November 2009  Accepted: 8 February 2010   Published: 16 April 2010


Context. The epidemiology of avian influenza and the ecology of wild birds are inextricably linked. An understanding of both is essential in assessing and managing the risks of highly pathogenic avian influenza (HPAI).

Aims. This project investigates the abundance, movements and breeding ecology of Australia’s Anseriformes in relation to the prevalence of low-pathogenicity avian influenza (LPAI) and provides risk profiles to improve the efficiency and relevance of wild-bird surveillance.

Methods. Generalised linear models and analysis of variance were used to examine the determinants of Anseriformes abundance and movements in Australia, and the observed prevalence of LPAI in Australia (n = 33 139) and overseas (n = 93 344). Risk profiles were developed using poultry density, estimated LPAI prevalence, the abundance of Anseriformes, and the probability of Anseriformes moving from areas of HPAI epizootics.

Key results. Analysis of Australian wild-bird surveillance data strongly supports other studies that have found the prevalence of LPAI in wild birds to be much lower (1%) in Australia than that in other countries (4.7%). LPAI prevalence was highly variable among sampling periods and locations and significantly higher in dabbling ducks than in other functional groups. Trends in Anseriformes movements, abundance and breeding are also variable, and correlated with rainfall, which could explain low prevalence and the failure to detect seasonal differences in LPAI in wild birds. Virus prevalence of faecal samples was significantly lower, whereas collecting faecal samples was 3–5 times less expensive and logistically simpler, than that of cloacal samples. Overall priority areas for on-going surveillance are provided for Australia.

Conclusions. Previous surveillance has occurred in high-priority areas, with the exception of Mareeba (North Queensland), Brisbane and Darwin, and has provided valuable information on the role of wild birds in maintaining avian influenza viruses. However, several practical considerations need to be addressed for future surveillance.

Implications. Long-term surveillance studies in wild birds in priority areas are required, which incorporate information on bird abundance, age, behaviour, breeding and movements, particularly for dabbling ducks. This is important to validate trends of LPAI prevalence, in understanding the main determinants for virus spread and persistence, and in predicting and managing future epizootics of HPAI in Australia.


Alfonso C. P. Cowen B. S. van Campen H. 1995 Influenza A viruses isolated from waterfowl in two wildlife management areas of Pennsylvania. Journal of Wildlife Diseases 31 179 185

Arzey G. 2004 The role of wild aquatic birds in the epidemiology of avian influenza in Australia. Australian Veterinary Journal 82 377 378

Arzey G. 2005 The role of wild waterfowl in the epidemiology of AI in Australia. Australian Veterinary Journal 83 445 doi:10.1111/j.1751-0813.2005.tb13090.x

Banks J. , and Alexander D. J. (1997). Molecular epidemiology of the H5 and H7 avian influenza viruses submitted to the international reference laboratory, Weybridge. In ‘Fourth International Symposium on Avian Influenza’. (Eds D. E. Swayne and R. D. Slemons.) pp. 105–109. (United States Animal Health Association: Athens, GA.)

Barr D. A. Kelly A. P. Badman R. T. Campey A. R. 1986 Avian influenza on a multi-age chicken farm. Australian Veterinary Journal 63 195 196

Barrett G. , Silcocks A. , Barry S. , Cunningham R. , and Poulter R. (2003). ‘New Atlas of Australian Birds.’ (CSIRO: Canberra.)

Bibby C. J. , Burgess N. D. , Hill D. A. , and Mustoe S. H. (2000). ‘Bird Census Techniques.’ (Academic Press: San Diego, CA.)

Brown J. D. Goekjian G. Poulson R. Valeika S. Stallknecht D. E. 2009 Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Veterinary Microbiology 136 20 26

Brugh M. , and Beck J. R. (1992). Recovery of minority subpopulation of highly pathogenic avian influenza virus. In ‘Proceedings of the Third International Symposium on Avian Influenza’. (Ed. B. C. Easterday.) pp. 166–174. (University of Wisconsin: Madison, WI.)

Bunn C. 2004 Correspondence regarding the role of wild aquatic birds in the epidemiology of avian influenza in Australia. Australian Veterinary Journal 82 4

Calvete C. , and Estrada R. (2000). ‘Epidemiología de Enfermedad Hemorrágica (VHD) y Mixomatosis en el conejo silvestre en el Valle medio del Ebro – Herramientas de gestión.’ (Consejo de Protección de la Naturaleza: Zaragoza, Spain.)

Chen H. Deng G. Li Z. Tian G. Li Y. Jiao P. Zhang L. Liu Z. Webster R. G. Yu K. 2004 The evolution of H5N1 influenza viruses in ducks in southern China. Proceedings of the National Academy of Sciences, USA 101 10 452 10 457 doi:10.1073/pnas.0403212101

Christidis L. , and Boles W. E. (2008). ‘Systematics and Taxonomy of Australian Birds.’ (CSIRO Publishing: Melbourne.)

Clark L. Hall J. 2006 Avian influenza in wild birds: status as reservoirs, and risks to humans and agriculture. Ornithological Monographs 60 3 29 doi:10.1642/0078-6594(2006)60[3:AIIWBS]2.0.CO;2

Delaney S. , and Scott D. (2006). ‘Waterbird Population Estimates.’ 4th edn. (Wetlands International: Wageningen, The Netherlands.)

Dobson A. Meagher M. 1996 The population dynamics of Brucellosis in the Yellowstone National Park. Ecology 77 1026 1036

Downie J. C. Laver W. G. 1973 Isolation of type A influenza virus from an Australian pelagic bird. Virology 51 259 269

Downie J. C. Hinshaw V. S. Laver W. G. 1977 The ecology of influenza. Isolation of type A influenza viruses from Australian pelagic birds. Australian Journal of Experimental Biology and Medical Science 55 635 643 doi:10.1038/icb.1977.62

East I. J. Hamilton S. A. Garner G. 2008 a Identifying areas of Australia at risk of H5N1 avian influenza infection from exposure to migratory birds: a spatial analysis. Geospatial Health 2 203 213

East I. J. Hamilton S. A. Sharp L. A. Garner G. 2008 b Identifying areas of Australia at risk for H5N1 avian influenza infection from exposure to nomadic waterfowl moving throughout the Australo-Papuan region. Geospatial Health 3 17 27

Ellström P. Latorre-Margalef N. Griekspoor P. Waldenström J. Olofsson J. Wahlgren J. Olsen B. 2008 Sampling for low-pathogenic avian influenza A virus in wild Mallard ducks: oropharyngeal versus cloacal swabbing. Vaccine 26 4414 4416

Feare C. 2007 The spread of avian influenza. Ibis 149 424 425 doi:10.1111/j.1474-919X.2007.00711.x

Food and Agriculture Organization of the United Nations (FAO) (2009). ‘Highly Pathogenic Avian Influenza Confirmed Outbreaks.’ Available at http://www.fao.org/avianflu/en/maps.html [verified November 2009].

Ford J. R. 1958 Seasonal variation in populations of Anatidae at the Bibra Lake District, Western Australia. Emu 58 31 41

Fossum O. Jansson D. Etterlin P. Vagsholm I. 2009 Causes of mortality in laying hens in different housing systems in 2001 to 2004. Acta Veterinaria Scandinavica 51 3

Frith H. J. (1982). ‘Waterfowl in Australia.’ Revised edn. (Angus and Robertson: Sydney.)

Gaidet N. Cattoli G. Hammoumi S. Newman S. H. Hagemeijer W. et al 2008 Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathogens 4 e1 000 127 doi:10.1371/journal.ppat.1000127

Gilbert M. Xiao X. Pfeiffer D. U. Epprecht M. Boles S. et al 2008 Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proceedings of the National Academy of Sciences, USA 105 4769 4774 doi:10.1073/pnas.0710581105

Gilmour A. R. , Gogel B. J. , Cullis B. R. , Welham S. J. , and Thompson R. (2002). ‘ASReml User Guide Release 1.’ (VSN International Ltd: Hemel Hempstead, UK.)

Hamilton S. A. East I. J. Toribio J.-A. Garner M. G. 2009 Are the Australian poultry industries vulnerable to large outbreaks of highly pathogenic avian influenza? Australian Veterinary Journal 87 165 174 doi:10.1111/j.1751-0813.2009.00423.x

Haynes L. Arzey E. Bell C. Buchanan N. Burgess G. et al 2009 Australian surveillance for avian influenza viruses in wild birds (July 2005 to June 2007). Australian Veterinary Journal 87 266 272 doi:10.1111/j.1751-0813.2009.00446.x

Henzell R. P. Cunningham R. B. Neave H. M. 2002 Factors affecting the survival of Australian wild rabbits exposed to rabbit haemorrhagic disease. Wildlife Research 29 523 542 doi:10.1071/WR00083

Hinshaw V. S. Wood J. M. Webster R. G. Deible R. Turner B. 1985 Circulation of influenza viruses and paramyxoviruses in waterfowl originating from two different areas of North America. Bulletin of the World Health Organization 63 711 719

Hochachka W. M. Dhondt A. A. 2000 Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Sciences, USA 97 5303 5306

Hulse-Post D. J. Sturm-Ramirez K. M. Humberd J. Seiler P. Govorkova E. A. et al 2005 Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proceedings of the National Academy of Sciences, USA 102 10 682 10 687 doi:10.1073/pnas.0504662102

Hurt A. C. Hansbro P. Selleck P. Olsen B. Minton C. Hampson A. W. Barr I. G. 2006 Isolation of avian influenza viruses from two different transhemispheric migratory shorebird species in Australia. Archives of Virology 151 2301 2309 doi:10.1007/s00705-006-0784-1

Johnson K. P. Sorenson M. D. 1999 Phylogeny and biogeography of dabbling ducks (genus Anas): a comparison of molecular and morphological evidence. The Auk 116 792 805

Keawcharoen J. van Riel D. van Amerongen G. Bestebroer T. Beyer W. E. van Lavieren R. Osterhaus A. Fouchier R. A. M. Kuiken T. 2008 Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerging Infectious Diseases 14 600 607

Kida H. Yanagawa R. Matsuoka Y. 1980 Duck influenza lacking evidence of disease signs and immune response. Infection and Immunity 30 547 553

Kingsford R. T. 2000 Ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia. Austral Ecology 25 109 127

Kingsford R. T. , and Porter J. L. (2006). Waterbirds and wetlands across Eastern Australia. Technical report. Department of the Environment and Heritage, Canberra.

Kirkland P. D. , and Tracey J. P. (2006). Detecting avian influenza in wild birds in New South Wales. Final report to the Department of Agriculture, Fisheries and Forestry, Wildlife and Exotic Disease Preparedness Program. NSW Department of Primary Industries, Orange, NSW.

Lang A. S. Kelly A. Runstadler J. A. 2008 Prevalence and diversity of avian influenza viruses in environmental reservoirs. Journal of General Virology 89 509 519

Liu J. Xiao H. Lei F. Zhu Q. Qin K. et al 2005 Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309 1206 doi:10.1126/science.1115273

Livezey B. C. 1986 A phylogenetic analysis of recent anseriform genera using morphological characters. The Auk 103 737 754

McCallum H. Roshier D. Tracey J. P. Joseph L. Heinsohn R. 2008 Will Wallace’s line save Australia from Avian Influenza? Ecology and Society 13 41 56

Mackenzie J. S. Edwards E. C. Holmes R. M. Hinshaw V. S. 1984 Isolation of ortho- and paramyxoviruses from wild birds in Western Australia and the characterisation of novel influenza A viruses. Australian Journal of Experimental Biology and Medical Science 62 89 99

Mackenzie J. S. , Britten D. , Hinshaw V. S. , and Wood J. (1985). Isolation of avian influenza and paramyxoviruses from wild birds in Western Australia. In ‘Veterinary Viral Diseases: Their Significance in South-east Asia and the Western Pacific’. (Ed. A. J. Della-Porta.) pp. 336–339. (Academic Press: Sydney.)

Malczewski J. (1999). ‘GIS and Multicriteria Decision Analysis.’ (John Wiley and Sons: New York.)

Morton S. R. Brennan K. G. Armstrong M. D. 1990 Distribution and abundance of ducks in the Alligator Rivers region, Northern Territory. Wildlife Research 17 573 590 doi:10.1071/WR9900573

Mukhtar M. M. Rasool S. T. Song D. Zhu C. Hao Q. Zhu Y. Wu J. 2007 Origin of highly pathogenic H5N1 avian influenza virus in China and genetic characterization of donor and recipient viruses. Journal of General Virology 88 3094 3099 doi:10.1099/vir.0.83129-0

Munster V. J. Fouchier R. A. M. 2009 Avian influenza virus: of virus and bird ecology. Vaccine 27 6340 6344 doi:10.1016/j.vaccine.2009.02.082

Munster V. J. Baas C. Lexmond P. Bestebroer T. M. Guldemeester J. et al 2009 Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. Journal of Clinical Microbiology 47 666 673 doi:10.1128/JCM.01625-08

Murray N. (2002). ‘Import Risk Analysis: Animals and Animal Products.’ (Ministry of Agriculture and Forestry: Wellington, New Zealand.)

Nebel S. Porter J. L. Kingsford R. T. 2008 Long-term trends of shorebird populations in eastern Australia and impacts of freshwater extraction. Biological Conservation 141 971 980 doi:10.1016/j.biocon.2008.01.017

Nestorowicz A. Kawaoka Y. Bean W. J. Webster R. G. 1987 Molecular analysis of the hemagglutinin genes of Australian H7N7 influenza viruses: role of passerine birds in maintenance or transmission. Virology 160 411 418 doi:10.1016/0042-6822(87)90012-2

Office International Epizooties (OIE) (2009). Update on highly pathogenic avian influenza in animals (Type H5 and H7). Available at http://www.oie.int/downld/AVIAN%20INFLUENZA/A_AI-Asia.htm [verified November 2009].

Olsen B. Munster V. J. Wallensten A. Waldernstrom J. Osterhaus A. D. M. E. Fouchier R. A. M. 2006 Global patterns of influenza A virus in wild birds. Science 312 384 388 doi:10.1126/science.1122438

Pannwitz G. Wolf C. Harder T. 2009 Active surveillance for avian influenza virus infection in wild birds by analysis of avian fecal samples from the environment. Journal of Wildlife Diseases 45 512 518

Peroulis I. O’Riley K. 2004 Detection of avian paramyxoviruses and influenza viruses amongst wild bird populations in Victoria. Australian Veterinary Journal 82 79 82

Pfeiffer D. U. 2006 Assessment of H5N1 risk and the importance of wild birds. Journal of Wildlife Diseases 43 S47 S50

Pfeiffer D. U. Minh P. Q. Martin V. Epprecht M. Otte M. J. 2007 An analysis of the spatial and temporal patterns of highly pathogenic avian influenza occurrence in Vietnam using national surveillance data. Veterinary Journal 174 302 309

Robinson T. P. Franceschini G. Wint W. 2007 The Food and Agriculture Organisation’s gridded livestock of the world. Veterinaria Italiana 43 745 751

Roche B. Lebarbenchon C. Gauthier-Clerc M. Chang C.-M. Thomas F. Renaud F. van der Werf S. Guégan J.-F. 2009 Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005–2006 epidemics in the Camargue area. Infection, Genetics and Evolution 9 800 805

Röhm C. Zhou N. Suss J. Mackenzie J. Webster R. G. 1996 Characterization of a novel influenza hemagglutinin, H15: criteria for determination of influenza A subtypes. Virology 217 508 516 doi:10.1006/viro.1996.0145

Rose K. , Newman S. , Uhart M. , and Lubroth J. (2006). ‘Wild Bird HPAI Surveillance: Sample Collection from Healthy, Sick and Dead Birds.’ (FAO: Rome.)

Roshier D. A. Robertson A. I. Kingsford R. T. Green D. G. 2001 Continental-scale interactions with temporary resources may explain the paradox of large populations of desert waterbirds in Australia. Landscape Ecology 16 547 556 doi:10.1023/A:1013184512541

Roshier D. A. Robertson A. I. Kingsford R. T. 2002 Responses of waterbirds to flooding in an arid region of Australia and implications for conservation. Biological Conservation 106 399 411 doi:10.1016/S0006-3207(01)00268-3

Roshier D. A. Klomp N. I. Asmus M. 2006 Movements of nomadic waterfowl, grey teal Anas gracilis, across inland Australia – results from satellite telemetry spanning fifteen months. Ardea 94 461 475

Roshier D. Asmus M. Klaassen M. 2008 What drives long-distance movements in the nomadic grey teal Anas gracilis in Australia? Ibis 150 474 484

Sabirovic M. , Wilesmith J. , Hall S. , Coulson N. , and Landeg F. (2006). ‘Outbreaks of HPAI H5N1 Virus in Europe during 2005/2006.’ (International Animal Health Division: London.)

Selleck P. W. Gleeson L. J. Hooper P. T. Westbury H. A. Hansson E. 1997 Identification and characterisation of an H7N3 influenza A virus from an outbreak of virulent avian influenza in Victoria. Australian Veterinary Journal 75 289

Selleck P. W. Arzey G. Kirkland P. D. Reece R. L. Gould A. R. Daniels P. W. Westbury H. A. 2003 An outbreak of highly pathogenic avian influenza in Australia in 1997 caused by an H7N4 virus. Avian Disease 47 806 811

Siengsanan J. Chaichoune K. Phonaknguen R. Sariya L. Prompiram P. et al 2009 Comparison of outbreaks of H5N1 highly pathogenic avian influenza in wild birds and poultry in Thailand. Journal of Wildlife Diseases 45 740 747

Sims L. D. , and Narrod C. (2009). ‘Understanding Avian Influenza.’ (Food and Agriculture Organization of the United Nations: Rome.)

Sims L. D. , and Turner A. J. (2008). Avian Influenza in Australia. In ‘Avian Influenza’. (Ed. D. E. Swayne.) pp. 239–250. (Blackwell Publishing Ltd: Ames, IA.)

Sims L. D. DomèNech J. Benigno C. Kahn S. Kamata A. Lubroth J. Martin V. Roeder P. 2005 Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. The Veterinary Record 157 159 164

Snow L. C. Newson S. E. Musgrove A. J. Cranswick P. A. Crick H. Q. P. Wilesmith J. W. 2007 Risk-based surveillance for H5N1 avian influenza virus in wild birds in Great Britain. The Veterinary Record 161 775 781

Sraml M. Christidis L. Easteal S. Horn P. Collet C. 1996 Molecular relationships within Australasian waterfowl (Anseriformes). Australian Journal of Zoology 44 47 58

Stallknecht D. E. , and Brown J. D. (2008). Ecology of avian influenza in wild birds. In ‘Avian Influenza’. (Ed. D. E. Swayne.) pp. 43–58. (Blackwell Publishing Ltd: Ames, IA.)

Stallknecht D. E. Kearney M. T. Shane S. M. Zwank P. J. 1990 a Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian Diseases 34 412 418 doi:10.2307/1591429

Stallknecht D. E. Shane S. M. Kearney M. T. Zwank P. J. 1990 b Persistence of avian influenza viruses in water. Avian Diseases 34 406 411 doi:10.2307/1591428

Sturm-Ramirez K. M. Hulse-Post D. J. Govorkova E. A. Humberd J. Seiler P. et al 2005 Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? Journal of Virology 79 11 269 11 279 doi:10.1128/JVI.79.17.11269-11279.2005

Tracey J. P. (2005). Targeting surveillance for avian influenza in wild birds: a pilot investigation in New South Wales. Final report to the Department of Agriculture, Fisheries and Forestry, Wildlife and Exotic Disease Preparedness Program. NSW Department of Primary Industries, Orange, NSW.

Tracey J. P. Woods R. Roshier D. West P. Saunders G. R. 2004 The role of wild birds in the transmission of avian influenza for Australia: an ecological perspective. Emu 104 109 124 doi:10.1071/MU04017

Truscott J. Garske T. Chis-Ster I. Guitian J. Pfeiffer D. Snow L. Wilesmith J. Ferguson N. M. Ghani A. C. 2007 Control of a highly pathogenic H5N1 avian influenza outbreak in the GB poultry flock. Proceedings of the Royal Society of London. Series B. Biological Sciences 274 2287 2295 doi:10.1098/rspb.2007.0542

Turner A. J. 1976 The isolation of fowl plague virus in Victoria. Australian Veterinary Journal 52 384

Turner A. J. 2004 The role of wild aquatic birds in the epidemiology of avian influenza in Australia. Australian Veterinary Journal 82 713

Wang J. Vijaykrishna D. Duan L. Bahl J. Zhang J. X. Webster R. G. Peiris J. S. M. Chen H. Smith G. J. D. Guan Y. 2008 Identification of the progenitors of Indonesia 1 and Vietnam avian influenza A (H5N1) viruses from southern China. Journal of Virology. doi:10.1128/JVI.02468-07

Warner S. , Welch A. , Ainsworth C. , Tracey J. P. , Zikesch F. , Saunders G. R. , and Lukins B. (2006). Application of rapid diagnostic tests in the targeted surveillance of avian influenza virus within Victorian wild bird populations. Final Report to the Wildlife and Exotic Disease Preparedness Program. Primary Industries Research Victoria, Melbourne. Available at www.daff.gov.au/__data/assets/pdf_file/0009/581886/ai-wildbirds-vic-august06.pdf [verified November 2009].

Webster R. G. Yakhno M. Hinshaw V. S. Bean W. J. Murti K. G. 1978 Intestinal influenza: Replication and characterization of influenza virus in ducks. Virology 84 268 278 doi:10.1016/0042-6822(78)90247-7

Westbury H. A. (1998). History of high pathogenic avian influenza in Australia and the H7N3 outbreak (1995). In ‘Proceedings of the Fourth International Symposium on Avian Influenza, May 29–31 1997’. (Eds D. E. Swayne and R. D. Slemons.) pp. 23–30. (United States Animal Health Association: Athens, GA.)

Woodall P. F. 1985 Waterbird populations in the Brisbane region, 1972–83, and correlates with rainfall and water heights. Australian Wildlife Research 12 495 doi:10.1071/WR9850495

World Health Organization (WHO) (2009). ‘Areas Reporting Confirmed Occurrence of H5N1 Avian Influenza in Poultry and Wild Birds since 2003. Available at http://gamapserver.who.int [verified November 2009].

Full Text PDF (573 KB) Export Citation Cited By (7)