Parasite/Disease / Status prior to 2000 / Timeline / Locality / Hosts and impact / Dynamics / Cause(s) / Notes
MICROPARASITES
Viruses
A(H5N1)1-3 / Only one avian influenza outbreak in wild birds documented
Highly pathogenic H5N1 first isolated from poultry in 1996
H5N1 hypothesised to have been selected for by exposure to multiple species in markets / 2002
2003-4
2005
2005-9 / Hong Kong
South-East Asia
Qinghai Lake(China)
Eurasia and Africa / Individual mortality in multiple species
Individual mortality in multiple species
Mortality of 6345 individuals of multiple waterbird species (including migratory)
Individual mortality and mass die-offs of multiple species / New strainA(H5N1) in wild birds
Local spatial spread of A(H5N1)
First mass die-off
Continental spatial spread of HPAIA(H5N1) / Emergencefrom domestic poultry
Spread via wild bird dispersal and human movement of domestic and wild birds
New, more lethal, H5N1 variant - Highly Pathogenic avian influenza HPAIA(H5N1)
Spread via wild bird dispersal/ migration and human movement of domestic and wild birds / The human health threat of H5N1 means that there is a unusually large amount of wildlife surveillance data, confirming this as an emergence
Avian pox4-7 / Widespread avian disease found in a large number of bird families with some (e.g. Phasianidae, Emberizidae) seeming more susceptible than others / 2000-9 / Galapagos Islands / Multiple finch species with gross lesions / Increasing prevalence, from 0% in 2000 to 10% in 2009 / Correlated with interannual variation in innate immune function3
Hypothesised link to food supply variation / May be a snap-shot of longer-term normal disease dynamics
Implicated as a major factor in avian declines and extinctions in Hawaii; introduced to the Galapagos in the late 1890s / 2002-4 / Fuerteventura
(Canary Islands) / Short-toed larks (Calandrellarufescens) and Berthelot’s Pipits (Anthusberthelotti) with gross lesions / Unusually high prevalence (up to 60%; suggested to be an epizootic) / Hypothesised link to heavy flea infestation in wild birds and poultry on farms
Hypothesised link to poor nutrition; utilising low-protein diet provided for goats on farms / May be a snap-shot of longer-term normal disease dynamics
Highly variable prevalence, from individual cases to epizootics / 2006-10 / England / Multiple tit species with gross lesions / Significant spatial spread of ‘Paridae pox’ strain from an origin in south-east England / Incursion from central Europe or Scandinavia / May be a snap-shot of longer-term normal disease dynamics
Usutu virus8-12 / First identified in South Africa in 1959
Reported from several other African countries including Senegal, Central African Republic, Nigeria, Uganda, Burkina Faso, Cote d'Ivoire, and Morocco / 2001-2
2005-12 / Austria
Seven other European countries / Die-offs of Eurasian blackbird (Turdusmerula), barn swallows (Hirundorustica), house sparrow (Passer domesticus) and blue tit (Paruscoeruleus); also mortality of 5 captive great grey owls (Strixnebulosa)
Eurasian blackbird die-offs; individual mortality in multiple other species / First report of Usutu virus outside Africa
Local spatial spread / Emergence via introduction from Africa by wild bird migration
Local spread via wild bird dispersal / Seroconversion without disease in countries such as the UK suggests that the virus is circulating widely in Europe withoutalways causing disease impacts; suggests other factors such as vectorial capacity may be limiting
West Nile virus
Lineage 113-16 / Old-world distribution prior to 1999, when reported as a cause of multiple species die-offs in New York State, USA; strain closely related to a strain first detected in Israel in 1998
Pathogen pollution to the USA believed to be via the air transport of an infected person or other avian or mammalian host; range expanded to four states in 1999 / Ongoing 2000
2001
2002
2003-2012
2001
2002-4 / USA; 12 states
USA; 27 states
USA; 44 states
All USA apart from Alaska and Hawaii
Canada; Ontario
Seven provinces / Die-offs of multiple species; individual cases of mortality in others; American crows (Corvusbrachyrhynchos) particularly susceptible; blue jay (Cyanocittacristata) and magpie (Pica hudsonia) mortalities became more prominent from 2003 onwards, as the virus moved westwards
Dead bird surveillance recovered mostly American crows / Continental spatial spread
Range from East to West coast
Continental spatial spread
Local spatial spread
Local spatial spread from USA
Range from Alberta to Nova Scotia / Wild bird dispersal; transmissionhighest in urbanized and agricultural habitats, in part because the hostsand vectors of WNV are abundant in human-modified areas; virus quickly adapted to infect local mosquito vectors more efficiently than the originally
introduced strain / Original establishment in USA in 1999 hypothesised to be facilitated by high mosquito numbers
Also expanded range into central and south America from 2001 onwards, but with only individual cases of bird mortality
2008-11 / Italy / Individual mortality in multiple species
(First human cases for ten years) / Unusually high prevalence; suggested to be an epizootic / Hypothesised link to favourable climatic conditions for vectors / Increase in human cases in multiple European countries through 2000s
May be a snap-shot of longer-term normal disease dynamics.
West Nile virus
Lineage 217-19 / Associated with a wide distribution of endemic transmission in Africa; not known to cause significant mortality / 2004
2008
2010 / Hungary
Austria
Greece / Individual cases of mortality in multiple bird species
Individual cases of mortality in multiple bird species
Individual cases of mortality in multiple bird species / First report of West Nile virus Lineage 2 outside Africa
Local spatial spread
Local spatial spread / Emergence via introduction from Africa by wild bird migration
Wild bird dispersal
Wild bird dispersal / Hypothesised that favourable climatic conditions for vectors may have contributed to persistence; a second Lineage 2 strain has been reported as a cause of human cases in Russia in 2007 & 2010
Bacteria
Avian cholera20 / Probably occurs worldwide in domestic birds; reports in wild birds are considerably more limited in global distribution / 2000 / Korea / Mass die-off (>10,000) of Baikal teal (Anasformosa) / First report in wild birds in eastern Asia / Crowding/stress at over wintering site / May be a snap-shot of longer-term normal disease dynamics
Mycoplasma gallisepticum21-25 / Probably occurs globally in gallinaceous birds; an epidemic of mycoplasmal conjunctivitis in house finches (Carpodacusmexicanus)due to pathogen pollution from poultry began in 1994 in the mid-Atlantic states of the USA and spread to the entire eastern population (also Canada) within a few years; correlated with population declines; prior to this, reports in wild passerines were rare; novel strain facilitated by clustering at bird feeders / Ongoing
2002
2004 / Montana, USA
Portland, USA / Individual cases of severe morbidity in house finches
Individual cases of severe morbidity in house finches / First report of M. gallisepticum infection in the western USA population of house finches (their native range)
Local spatial spread in western population / Wild bird dispersal
Wild bird dispersal / Continuing spread hypothesised to be facilitated by clustering at bird feeders.
Environmental stress may play a role in increasing the pathogenic effects on the host.
MACROPARASITES
Protozoa
Trichomonas26-32 / Globally distributed except Antarctica, with multiple epizootics on record; some strains particularly common (e.g. Trichomonasgallinae in pigeons, raptors and owls); infection in passerines sporadic; infection in finches known from captivity; retrospective analysis indicates a greenfinch mortality incident in Great Britain in 1993 hypothesised to be caused by trichomoniasis / 2002
2005-9
2007-9
2008-11
2009-12 / Kentucky, USA
Great Britain
Canadian maritime provinces
Finland
Germany; Czech Republic / Mortality of >200 house finches and house sparrows
Small die-offs and individual mortality of mainly greenfinch (Chloris chloris)but also chaffinch (Fringellacoelebs)and a few dunnock(Prunellamodularis); cases peaked in 2006-7 then greatly reduced in 2008-9; correlated with 50% greenfinch population decline
Individual cases of morbidity and mortality in multiple species, mainly purple finch (Carpodacuspurpureus) and American goldfinch (Carduelistristis)
Individuals cases of mortality of multiple species (mainly greenfinch) peaking in 2009; correlated with approx. 50% greenfinch population decline
Individual cases of mortality of multiple species (mainly greenfinches and chaffinches); linked to epidemic finch mortality / First confirmed report of a passerine die-off caused by trichomoniasis
First confirmed report of passerine die-offs caused by trichomoniasis in Europe
Increased surveillance detecting cases
Local spatial spread from Great Britain
Potential spatial spread from Great Britain or Finland / Hypothesised that congregation (e.g. at food sources) increases disease transmission
Hypothesised spread of a strain from columbiforms to passeriforms; no consistent pattern with climate identified
No consistent pattern with climate identified
Spread via strain introduction from Great Britain by wild bird dispersal/migration
Potentially wild bird dispersal / All outbreaks reported may be snap-shots of longer-term normal disease dynamics
Classic epizootic dynamics suggest not emergence, but re-emergence of a highly sporadic disease
Canadian cases may be due toincreased surveillance in response to UK outbreak
Classic epizootic dynamics suggest not emergence, but re-emergence of a highly sporadic disease
May be epizootic dynamics or increased surveillance

References

  1. Becker WB 1966. Isolation and classification of tern virus:Influenza virus A/Tern/South Africa/1961. Journal of Hygiene 64: 309-320.
  2. World Health Organization 2011. H5N1 avian influenza: Timeline of major events.
  3. Liu J et al. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309: 1206.
  4. Zylerberg M et al. 2012. Increasing avian pox prevalence varies by species, and with immune function, in Galapagos finches. Biological Conservation 153: 72-79.
  5. Smits JE et al. 2005. An Epizootic of Avian Pox in Endemic Short-toed Larks (Calandrellarufescens) and Berthelot’s Pipits (Anthusberthelotti) in the Canary Islands, Spain. Veterinary Pathology 42: 59-65.
  6. Carrete M et al. 2009. Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecological Applications 19: 840-853.
  7. Lawson B et al. 2012. Emergence of a novel avian pox disease in British tit species. PLoS ONE 7: e40176.
  8. Nikolay B et al. 2011. Usutu virus in Africa. Vector Borne and Zoonotic Diseases 11: 1417-1423.
  9. Weissenbock et al. 2002. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerging Infectious Diseases 8: 652-656.
  10. Buckley A et al. 2003. Serological evidence of West Nile virus, Usutu virus and Sindbis virus infection of birds in the UK. Journal of General Virology 84: 2807-2817.
  11. Bakonyi T et al. 2004. Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001. Comparison with the South African strain SAAR-1776 and other flaviviruses. Virology 328: 301-310.
  12. Vázquez A et al. 2011. USUTU VIRUS – POTENTIAL RISK OF HUMAN DISEASE IN EUROPE. Eurosurveillance 16(31): pii=19935.
  13. Lanciotti et al. 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 2333-2337.
  14. Ciccozzi M et al. 2013. Epidemiological history and phylogeography of West Nile virus lineage 2. Infection, Genetics and Evolution 17: 46-50.
  15. LaDeau SL, Kilpatrick AM, Marra PP 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710-713.
  16. Kilpatrick AM 2011.Globalization, Land Use, and theInvasion of West Nile Virus.Science334: 323-327.
  17. Pradier S 2012. West Nile virus epidemiology and factors triggering change in its distribution in Europe. Rev. sci. tech. Off. Int. Epiz. 31: 829-844.
  18. Calistri P et al. 2010. West Nile Virus Transmission in 2008 in North-Eastern Italy. Zoonoses and Public Health 57: 211-219.
  19. Bakonyi et al. 2013. Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009. Veterinary Microbiology 165: 61-70.
  20. Kwon YK, Kang MI 2003. Outbreak of Fowl cholera in Baikal teals in Korea. Avian Diseases 47: 1491-1495
  21. Dhondt AA et al. 2006. Dynamics of mycoplasma conjunctivitis in the native and introduced range of the host. EcoHealth 3: 95-102.
  22. Hosseini, P. R., A. A. Dhondt, and A. P. Dobson. 2006. Spatial spread of an emerging infectious disease: conjunctivitis in house finches. Ecology 87:3037-3046.
  23. Hochachka, W. M., A. A. Dhondt, A. Dobson, D. M. Hawley, D. H. Ley, and I. J. Lovette. 2013. Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen. Proceedings of the Royal Society B: Biological Sciences 280:20131068.
  24. Duckworth RA et al. 2003. First case of mycoplasmosis in the native range of the House Finch (Carpodacusmexicanus). Auk 120: 528-530.
  25. Ley DH, Sheaffer DS, Dhondt AA 2006. Further western spread of Mycoplasma gallisepticum infection of house finches. Journal of Wildlife Diseases 42: 429-431.
  26. Lawson B et al. 2012. The emergence and spread of finch trichomonosis in the BritishIsles. Philosophical Transactions of the Royal Society B 367: 2852–2863.
  27. Lawson B et al. 2011. Evidence of spread of the emerging infectious disease, finch trichomonosis, by migrating birds. EcoHealth 8: 143-153.
  28. Lehikoinen A et al. 2013. Impacts of trichomonosis epidemics on Greenfinch Chloris chloris and Chaffinch Fringillacoelebs populations in Finland. Ibis 155: 357-366.
  29. Peters M et al. 2009. Epidemic mortality in greenfinches at feeder stations caused by Trichomonasgallinae – a recent problem in Northern Germany. Kleintierpraxis 54: 433–438.
  30. Forzan M et al. 2010. Trichomoniasis in finches from the Canadian Maritime provinces – An emerging disease. Canadian Veterinary Journal 51: 391-396.
  31. Robinson RA et al. 2010. Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 5: e12215.
  32. NWHC. 1983-2006. Epizootic files. United States Geological Survey, National Wildlife Health Center, Madison, WI.