Do contrasting patterns of migration movements and disease outbreaks between congeneric waterfowl species reflect differing immunity?
Long-distance migrations influence the dynamics of hostpathogen interactions and understanding the role of migratory waterfowl in the spread of the highly pathogenic avian influenza viruses (HPAIV) is important. While wild geese have been associated with outbreak events, disease ecology of closely related species has not been studied to the same extent. The swan goose (Anser cygnoides) and the bar-headed goose (Anser indicus) are congeneric species with distinctly different HPAIV infection records; the former with few and the latter with numerous records. We compared movements of these species, as well as the more distantly related whooper swan (Cygnus cygnus) through their annual migratory cycle to better understand exposure to HPAIV events and how this compares within and between congeneric and noncongeneric species. In spite of their record of fewer infections, swan geese were more likely to come in contact with disease outbreaks than bar-headed geese. We propose two possible explanations: i) frequent prolonged contact with domestic ducks increases innate immunity in swan geese, and/or ii) the stress of high-elevation migration reduces immunity of bar-headed geese. Continued efforts to improve our understanding of species-level pathogen response is critical to assessing disease transmission risk.
Altizer S, Bartel R, Han BA, 2011. Animal migration and infectious disease risk. Science 331:296-302. DOI: https://doi.org/10.1126/science.1194694
Batbayar N, Takekawa JY, Newman SH, Prosser DJ, Natsagdorj T, Xiao X, 2013. Migration strategies of Swan Geese Anser cygnoides from northeast Mongolia. Wildfowl 61:90-109.
Batbayar N, 2013. Breeding and migration ecology of bar-headed goose Anser indicus and swan goose Anser cygnoides in Asia. University of Oklahoma.
Battley PF, Piersma T, 2005. Body composition and flight ranges of bar-tailed godwits (Limosa lapponica baueri) from New Zealand. The Auk 122:922-37. DOI: https://doi.org/10.1093/auk/122.3.922
Bishop CM, Spivey RJ, Hawkes LA, Batbayar N, Chua B, Frappell PB, Milsom WK, Natsagdorj T, Newman SH, Scott GR, 2015. The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations. Science 347:250-54. DOI: https://doi.org/10.1126/science.1258732
Brown JD, Stallknecht DE, Swayne DE, 2008. Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg Infect Dis 14:136-42. DOI: https://doi.org/10.3201/eid1401.070740
Cappelle J, Zhao D, Gilbert M, Nelson MI, Newman SH, Takekawa JY, Gaidet N, Prosser DJ, Liu Y, Li P, 2014. Risks of avian influenza transmission in areas of intensive free-ranging duck production with wild waterfowl. EcoHealth 11:109-19. DOI: https://doi.org/10.1007/s10393-014-0914-2
Chen H, Smith GJD, Zhang SY, Qin K, Wang J, Li KS, Webster R, Peiris J, Guan Y, 2005. Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191-2. DOI: https://doi.org/10.1038/nature03974
Darwin C, 1859. On the origin of species by means of natural selection. Murray, London, UK, 502.
Dunn OJ, 1961. Multiple comparison among means. J Am Stat Assoc 56:52-64. DOI: https://doi.org/10.1080/01621459.1961.10482090
Fearnley L, 2015. Wild goose chase: The displacement of influenza research in the fields of Poyang Lake, China. Cult Anthropol 30:12-35. DOI: https://doi.org/10.14506/ca30.1.03
Frank J, Massey JR, 1951. The Kolmogorov-Smirnov test for goodness of fit. J Am Stat Assoc 46:68-78. DOI: https://doi.org/10.1080/01621459.1951.10500769
Fritzsche MA, Hoye BJ, 2016. Are migratory animals superspreaders of infection? Integr Comp Biol 56:260-7. DOI: https://doi.org/10.1093/icb/icw054
Gilbert M, Jambal L, Karesh WB, Fine A, Shiilegdamba E, Dulam P, Sodnomdarjaa R, Ganzorig K, Batchuluun D, Tseveenmyadag N, 2012. Highly pathogenic avian influenza virus among wild birds in Mongolia. PLoS One 7:e44097. DOI: https://doi.org/10.1371/journal.pone.0044097
Gilbert M, Xiao X, Chaitaweesub P, Kalpravidh W, Premashthira S, Boles S, Slingenbergh J, 2007. Avian influenza, domestic ducks and rice agriculture in Thailand. Agr Ecosyst Environ 119:409-15. DOI: https://doi.org/10.1016/j.agee.2006.09.001
Hall RJ, Altizer S, Bartel RA, 2014. Greater migratory propensity in hosts lowers pathogen transmission and impacts. J Anim Ecol 83:1068-77. DOI: https://doi.org/10.1111/1365-2656.12204
Hawley DM, Altizer SM, 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25:48-60. DOI: https://doi.org/10.1111/j.1365-2435.2010.01753.x
Hawkes LA, Balachandran S, Batbayar N, Butler PJ, Frappell PB, Milsom WK, Tseveenmyadag N, Newman SH, Scott GR, Sathiyaselvam P, 2011. The trans-Himalayan flights of bar-headed geese (Anser indicus). Proc Natl Acad Sci 108:9516-9. DOI: https://doi.org/10.1073/pnas.1017295108
Hénaux V, Samuel MD, 2011. Avian influenza shedding patterns in waterfowl: implications for surveillance, environmental transmission, and disease spread. J Wild Dis 47:566-78. DOI: https://doi.org/10.7589/0090-3558-47.3.566
Hill NJ, Takekawa JY, Ackerman JT, Hobson KA, Herring G, Cardona CJ, Runstadler JA, Boyce WM, 2012. Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos). Mol Ecol 21:5986-99. DOI: https://doi.org/10.1111/j.1365-294X.2012.05735.x
Johnson WP, Schmidt PM, Taylor DP, 2014. Foraging flight distances of wintering ducks and geese: a review. Avian Conserv Ecol 9:2. DOI: https://doi.org/10.5751/ACE-00683-090202
Kou Z, Li Y, Yin Z, Guo S, Wang M, Gao X, Li P, Tang L, Jiang P, Luo Z, 2009. The survey of H5N1 flu virus in wild birds in 14 provinces of China from 2004 to 2007. PLoS One 4:e6926. DOI: https://doi.org/10.1371/journal.pone.0006926
Kranstauber B, Kays R, Lapoint SD, Wikelski M, Safi K, 2012. A dynamic Brownian bridge movement model to estimate utilization distributions for heterogeneous animal movement. J Anim Ecol 81:738-46. DOI: https://doi.org/10.1111/j.1365-2656.2012.01955.x
Leung TL, Koprivnikar J, 2016. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 85:1471-80. DOI: https://doi.org/10.1111/1365-2656.12581
Lisovski S, van Dijk JGB, Klinkenberg D, Nolet BA, Fouchier RAM, Klaassen M, 2018. The roles of migratory and resident birds in local avian influenza infection dynamics. J Appl Ecol 55:2963-75. DOI: https://doi.org/10.1111/1365-2664.13154
Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XLW, Zhang Xl, Zhao D, Wang G, Feng Y, 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309:1206. DOI: https://doi.org/10.1126/science.1115273
Møller AP, Erritzøe J, 1998. Host immune defence and migration in birds. Evol Ecol 12: 945-953. DOI: https://doi.org/10.1023/A:1006516222343
Newman SH, Iverson SA, Takekawa JY, Cappelle M, Prosser DJ, Batbayar N, Natsagdorj T, Douglas DC, 2009. Migration of whooper swans and outbreaks of highly pathogenic avian influenza H5N1 virus in eastern Asia. PLoS One 4:e5729. DOI: https://doi.org/10.1371/journal.pone.0005729
Newman SH, Hill NJ, Spragens KA, Janies D, Voronkin IO, Prosser DJ, Yan B, Lei F, Batbayar N, Natsagdorj T, 2012. Eco-virological approach for assessing the role of wild birds in the spread of avian influenza H5N1 along the Central Asian Flyway. PLoS One 7:e30636. DOI: https://doi.org/10.1371/journal.pone.0030636
Nemeth N, Brown JD, Stallknecht D, Howerth E, Newman S, Swayne D, 2013. Experimental infection of bar-headed geese (Anser indicus) and ruddy shelducks (Tadorna ferruginea) with a clade 2.3.2 H5N1 highly pathogenic avian influenza virus. Vet Pathol 50:961-70. DOI: https://doi.org/10.1177/0300985813490758
Niu Y, 2016. Traditional agriculture technique in China. Shantou University Press, Shantou, China.
Owen JC, Moore FR, 2006. Seasonal differences in immunological condition of three species of thrushes. Condor 108:389-98. DOI: https://doi.org/10.1093/condor/108.2.389
Owen JC, Moore FR, 2008. Swainson’s thrushes in migratory disposition exhibit reduced immune function. J Ethol 26:383-8. DOI: https://doi.org/10.1007/s10164-008-0092-1
Pantin-Jackwood MJ, Costa-Hurtado M, Bertran K, DeJesus E, Smith D, Swayne DE, 2017. Infectivity, transmission and pathogenicity of H5 highly pathogenic avian influenza clade 126.96.36.199 (H5N8 and H5N2) United States index viruses in Pekin ducks and Chinese geese. Vet Res 48:33. DOI: https://doi.org/10.1186/s13567-017-0435-4
Palm EC, Newman SH, Prosser DJ, Xiao X, Ze L, Batbayar N, Balachandran S, Takekawa JY, 2015. Mapping migratory flyways in Asia using dynamic Brownian bridge movement models. Mov Ecol 3:3. DOI: https://doi.org/10.1186/s40462-015-0029-6
Prosser DJ, Hungerford LL, Erwin RM, Ottinger MA, Takekawa JY, Ellis EC, 2013. Mapping avian influenza transmission risk at the interface of domestic poultry and wild birds. Front Public Heal 1:28. DOI: https://doi.org/10.3389/fpubh.2013.00028
Prosser DJ, Palm EC, Takekawa JY, Zhao D, Xiao X, Li P, Liu Y, Newman SH, 2016. Movement analysis of free-grazing domestic ducks in Poyang Lake, China: a disease connection. Int J Geogr Inf Sci 30:869-80. DOI: https://doi.org/10.1080/13658816.2015.1065496
QGIS Development Team, 2015. QGIS geographic information system. Open Source Geospatial Foundation Project.
R Development Core Team, 2016. R: A language and environment for statistical computing. R Found Stat Comput Vienna Austria.
Risely A, Klaassen M, Hoye BJ, 2018. Migratory animals feel the cost of getting sick: A meta‐analysis across species. J Anim Ecol 87:301-14. DOI: https://doi.org/10.1111/1365-2656.12766
Shimada T, Yamaguchi NM, Hijikata N, Hiraoka E, Hupp JW, Flint PL, Tokita K, Fujita G, Uchida K, Sato F, Kurechi M, Pearce JM, Ramey AM, Higuchi H, 2014. Satellite tracking of migrating whooper swans Cygnus cygnus wintering in Japan. Ornithol Sci 13:67-75. DOI: https://doi.org/10.2326/osj.13.67
Si Y, Skidmore AK, Wang T, De Boer WF, Debba P, Toxopeus AG, Li L, Prins HHT, 2009. Spatio-temporal dynamics of global H5N1 outbreaks match bird migration patterns. Geospat Health 4:65-78. DOI: https://doi.org/10.4081/gh.2009.211
Si Y, Xu Y, Xu F, Li X, Zhang W, Wielstra B, Wei J, Liu G, Luo H, Takekawa J, 2018. Spring migration patterns, habitat use, and stopover site protection status for two declining waterfowl species wintering in China as revealed by satellite tracking. Ecol Evol 8:6280-9. DOI: https://doi.org/10.1002/ece3.4174
Stallknecht D, Kearney M, Shane S, Zwank P, 1990. Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian Dis 34:412-8. DOI: https://doi.org/10.2307/1591429
Takekawa JY, Newman SH, Xiao X, Prosser DJ, Spragens KA, Palm EC, Yan B, Li T, Lei F, Zhao D, 2010a. Migration of waterfowl in the East Asian flyway and spatial relationship to HPAI H5N1 outbreaks. Avian Dis Dig 5:101-2. DOI: https://doi.org/10.1637/9187-891409-DIGEST.1
Takekawa JY, Palm EC, Prosser DJ, Hawkes LA, Batbayar N, Balachandran S, Luo Z, Xiao X, Newman SH, 2017. Goose migration across the Himalayas: Migratory routes and movement patterns of bar-headed geese. Cambridge University Press, Cambridge, UK, pp. 15-29. DOI: https://doi.org/10.1017/9781316335420.004
Takekawa JY, Prosser DJ, Newman SH, Muzaffar S Bin, Hill NJ, Yan B, Xiao X, Lei F, Li T, Schwarzbach SE, 2010b. Victims and vectors: highly pathogenic avian influenza H5N1 and the ecology of wild birds. Avian Biol Res 3:51-73. DOI: https://doi.org/10.3184/175815510X12737339356701
Tian H, Zhou S, Dong L, Van Boeckel TP, Cui Y, Newman SH, Takekawa JY, Prosser DJ, Xiao X, Wu Y, 2015. Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci 112:172-7. DOI: https://doi.org/10.1073/pnas.1405216112
van Dijk JG, Matson KD, 2016. Ecological immunology through the lens of exercise immunology: new perspective on the links between physical activity and immune function and disease susceptibility in wild animals. Integr Comp Biol 56:290-303. DOI: https://doi.org/10.1093/icb/icw045
van Dijk JG, Verhagen JH, Wille M, Waldenström J, 2018. Host and virus ecology as determinants of influenza A virus transmission in wild birds. Curr Opin Virol 28:26-36. DOI: https://doi.org/10.1016/j.coviro.2017.10.006
Verhagen JH, Herfst S, Fouchier RA, 2015. How a virus travels the world. Science 347:616-7. DOI: https://doi.org/10.1126/science.aaa6724
Verhagen JH, van Dijk JGB, Vuong O, Bestebroer T, Lexmond P, Klaassen M, Fouchier RA, 2014. Migratory birds reinforce local circulation of avian influenza viruses. PLoS One 9:e112366. DOI: https://doi.org/10.1371/journal.pone.0112366
Wallace R, 2016. Big farms make big flu: dispatches on influenza, agribusiness, and the nature of science. NYU Press, NY, USA.
Wang Y, Jiang Z, Jin Z, Tan H, Xu B, 2013. Risk factors for infectious diseases in backyard poultry farms in the Poyang Lake area, China. PLoS One 8:e67366. DOI: https://doi.org/10.1371/journal.pone.0067366
Welte VR, Terán MV, 2004. Emergency prevention system (EMPRES) for transboundary animal and plant pests and diseases. The EMPRES-Livestock: An FAO initiative. Ann N Y Acad Sci 1026:19-31. DOI: https://doi.org/10.1196/annals.1307.003
Xu F, Si Y, 2019 The frost wave hypothesis: How the environment drives autumn departure of migratory waterfowl. Ecol Indic 101:1018-25. DOI: https://doi.org/10.1016/j.ecolind.2019.02.024
Xu Y, Gong P, Wielstra B, Si Y, 2016. Southward autumn migration of waterfowl facilitates cross-continental transmission of the highly pathogenic avian influenza H5N1 virus. Sci Rep 6:30262. DOI: https://doi.org/10.1038/srep30262
Xu Y, Si Y, Takekawa J, Liu Q, Prins HHT, Yin S, Prosser D, Gong P, de Boer WF, 2020. A network approach to prioritize conservation efforts for migratory birds. Conserv Biol 34:416-26. DOI: https://doi.org/10.1111/cobi.13383
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