1921
Volume 80, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Recent field studies have suggested that the dynamics of West Nile virus (WNV) transmission are influenced strongly by a few key super spreader bird species that function both as primary blood hosts of the vector mosquitoes (in particular ) and as reservoir-competent virus hosts. It has been hypothesized that human cases result from a shift in mosquito feeding from these key bird species to humans after abundance of the key birds species decreases. To test this paradigm, we performed a mosquito blood meal analysis integrating host-feeding patterns of , the principal vector of WNV in the eastern United States north of the latitude 36°N and other mosquito species with robust measures of host availability, to determine host selection in a WNV-endemic area of suburban Chicago, Illinois, during 2005–2007. Results showed that fed predominantly (83%) on birds with a high diversity of species used as hosts (25 species). American robins () were marginally overused and several species were underused on the basis of relative abundance measures, including the common grackle (), house sparrow (), and European starling (). also fed substantially on mammals (19%; 7 species with humans representing 16%). West Nile virus transmission intensified in July of both years at times when American robins were heavily fed upon, and then decreased when robin abundance decreased, after which other birds species were selected as hosts. There was no shift in feeding from birds to mammals coincident with emergence of human cases. Rather, bird feeding predominated when the onset of the human cases occurred. Measures of host abundance and competence and feeding preference were combined to estimate the amplification fractions of the different bird species. Predictions were that approximately 66% of WNV-infectious became infected from feeding on just a few species of birds, including American robins (35%), blue jays (17%, ), and house finches (15%, ).

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References

  1. Kilpatrick AM, LaDeau SL, Marra PP, 2007. Ecology of West Nile virus transmission and its impact on birds in the western hemisphere. Auk 124 : 1121–1136.
  2. Kramer LD, Styer LM, Ebel GD, 2008. A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53 : 61–81.
  3. Yaremych SA, Warner RE, Mankin PC, Brawn JD, Raim A, Novak R, 2004. West Nile virus and high death rate in American crows. Emerg Infect Dis 10 : 709–711.
  4. LaDeau SL, Kilpatrick AM, Marra PP, 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447 : 710–714.
  5. Koenig WD, Marcus L, Scott TW, Dickinson JL, 2007. West Nile virus and California breeding bird declines. EcoHealth 4 : 18–24.
  6. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD, 2006. Host heterogeneity dominates West Nile virus transmission. Proc R Soc Lond B Biol Sci 273 : 2327–2333.
  7. Savage HM, Aggarwal D, Apperson CS, Katholi CR, Gordon E, Hassan HK, Anderson M, Charnetzky D, McMillen L, Unnasch EA, Unnasch TR, 2007. Host choice and West Nile virus infection rates in blood-fed mosquitoes, including members of the Culex pipiens complex, from Memphis and Shelby County, Tennessee, 2002–2003. Vector Borne Zoonotic Dis 7 : 365–386.
  8. Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4 : 606–610.
  9. Edman JD, Taylor DJ, 1968. Culex nigripalpus: seasonal shift in bird-mammal feeding ratio in a mosquito vector of human encephalitis. Science 161 : 67–68.
  10. Tempelis CH, Reeves WC, Bellamy RE, Lofy MF, 1965. A 3-year study of feeding habits of Culex tarsalis in Kern county California. Am J Trop Med Hyg 14 : 170–177.
  11. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M, 2003. Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9 : 311–322.
  12. Reisen WK, Fang Y, Martinez VM, 2005. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol 42 : 367–375.
  13. Wonham MJ, de-Camino-Beck T, Lewis MA, 2004. An epidemiological model for West Nile virus: invasion analysis and control applications. Proc R Soc Lond B Biol Sci 271 : 501–507.
  14. Freier JE, 1989. Estimation of vectoral capacity: vector abundance in relation to man. Bull Soc Vector Ecol 14 : 41–46.
  15. Kay BH, Boreham PFL, Edman JD, 1979. Application of the feeding index concept to studies of mosquito host-feeding patterns. Mosq News 39 : 68–72.
  16. Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR, 2004. Host feeding patterns of established and potential mosquito vectors of West Nile virus in the eastern United States. Vector Borne Zoonotic Dis 4 : 71–82.
  17. Stout WE, Cassini AG, Meece JK, Papp JM, Rosenfield RN, Reed KD, 2005. Serologic evidence of West Nile virus infection in three wild raptor populations. Avian Dis 49 : 371–375.
  18. Hull J, Hull A, Reisen W, Fang Y, Ernest H, 2006. Variation of West Nile virus antibody prevalence in migrating and wintering hawks in central California. Condor 108 : 435–439.
  19. Beveroth TA, Ward MP, Lampman RL, Ringia AM, Novak RJ, 2006. Changes in seroprevalence of West Nile virus across Illinois in free-ranging birds from 2001 through 2004. Am J Trop Med Hyg 74 : 174–179.
  20. Ringia AM, Blitvich BJ, Koo HY, Van de Wyngaerde M, Brawn JD, Novak RJ, 2004. Antibody prevalence of West Nile virus in birds, Illinois, 2002. Emerg Infect Dis 10 : 1120–1124.
  21. Komar O, Robbins MB, Klenk K, Blitvich BJ, Marlenee NL, Burkhalter KL, Gubler DJ, Gonzalvez G, Pena CJ, Peterson AT, Komar N, 2003. West Nile virus transmission in resident birds, Dominican Republic. Emerg Infect Dis 9 : 1299–1302.
  22. Gibbs SEJ, Hoffman DM, Stark LM, Marlenee NL, Blitvich BJ, Beaty BJ, Stallknecht DE, 2005. Persistence of antibodies to West Nile virus in naturally infected rock pigeons (Columba livia). Clin Diagn Lab Immunol 12 : 665–667.
  23. Gibbs SEJ, Allison AB, Yabsley MJ, Mead DG, Wilcox BR, Stallknecht DE, 2006. West Nile virus antibodies in avian species of Georgia, USA: 2000–2004. Vector Borne Zoonotic Dis 6 : 57–72.
  24. McLean RG, 2006. West Nile virus in North American birds. Ornithol Mono 60 : 44–64.
  25. Hess AD, Hayes RO, Tempelis CH, 1968. Use of forage ratio technique in mosquito host preference studies. Mosq News 28 : 386.
  26. Boreham PFL, Garrettj C, 1973. Prevalence of mixed blood meals and double feeding in a malaria vector (Anopheles sacharovi favre). Bull World Health Organ 48 : 605–614.
  27. Lardeux F, Loayza P, Bouchite B, Chavez T, 2007. Host choice and human blood index of Anopheles pseudopunctipennis in a village of the Andean valleys of Bolivia. Malar J 6 : 8.
  28. Darbro JM, Harrington LC, 2006. Bird-baited traps for surveillance of West Nile mosquito vectors: effect of bird species, trap height, and mosquito escape rates. J Med Entomol 43 : 83–92.
  29. Edman JD, Day JF, Walker ED, 1984. Field confirmation of laboratory observations on the differential antimosquito behavior of herons. Condor 86 : 91–92.
  30. Scott TW, Lorenz LH, Edman JD, 1990. Effects of house sparrow age and arbovirus infection on attraction of mosquitos. J Med Entomol 27 : 856–863.
  31. Sota T, Hayamizu E, Mogi M, 1991. Distribution of biting Culex tritaeniorhynchus (Diptera, Culicidae) among pigs: effects of host size and behavior. J Med Entomol 28 : 428–433.
  32. Zweighaft RM, Rasmussen C, Brolnitsky O, Lashof JC, 1979. St. Louis encephalitis: Chicago experience. Am J Trop Med Hyg 28 : 114–118.
  33. Huhn GD, Austin C, Langkop C, Kelly K, Lucht R, Lampman R, Novak R, Haramis L, Boker R, Smith S, Chudoba M, Gerber S, Conover C, Dworkin MS, 2005. The emergence of West Nile virus during a large outbreak in Illinois in 2002. Am J Trop Med Hyg 72 : 768–776.
  34. Ruiz MO, Walker ED, Foster ES, Haramis LD, Kitron UD, 2007. Association of West Nile virus illness and urban landscapes in Chicago and Detroit. Int J Health Geogr 6 : 10–18.
  35. Hamer GL, Walker ED, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Schotthoefer AM, Brown WM, Wheeler E, Kitron UD, 2008. Rapid amplification of West Nile virus: the role of hatch-year birds. Vector Borne Zoonotic Dis 8 : 57–67.
  36. Andreadis TG, Thomas MC, Shepard JJ, 2005. Identification Guide to the Mosquitoes of Connecticut. New Haven, CT: The Connecticut Agricultural Experiment Station.
  37. Biggerstaff BJ, 2006. PooledInfRate, Version 3.0: A Microsoft Excel Add-In to Compute Prevalence Estimates from Pooled Samples. Fort Collins, CO: Centers for Disease Control and Prevention.
  38. Crabtree MB, Savage HM, Miller BR, 1995. Development of a species-diagnostic polymerase chain-reaction assay for the identification of Culex vectors of St. Louis encephalitis-virus based on interspecies sequence variation in ribosomal DNA spacers. Am J Trop Med Hyg 53 : 105–109.
  39. Detinova TS, 1962. Age-grouping methods in diptera of medical importance. Monogr Ser World Health Organ 47 : 13–191.
  40. Molaei G, Andreadis TA, Armstrong PM, Anderson JF, Vossbrinck CR, 2006. Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis 12 : 468–474.
  41. Perez-Tris J, Bensch S, 2005. Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131 : 15–23.
  42. Cupp EW, Zhang DH, Yue X, Cupp MS, Guyer C, Sprenger TR, Unnasch TR, 2004. Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. Am J Trop Med Hyg 71 : 272–276.
  43. Loss SR, Hamer GL, Walker ED, Ruiz MO, Goldberg TL, Kitron UD, Brawn JD, 2009. Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia (in press).
  44. Thomas L, Laake JL, Strindberg S, Marques FFC, Buckland ST, Borchers DL, Anderson DR, Burnham KP, Hedley SL, Pollard JH, Bishop JRB, Marques TA, 2006. Distance 5.0. Release 5. Research Unit for Wildlife Population Assessment. St. Andrews, UK: University of St. Andrews.
  45. Manly BF, McDonald LL, Thomas DL, McDonald TL, Erickson WP, 2002. Resource Selection by Animals: Statistical Design and Analysis for Field Studies. Dordrecht, The Netherlands: Kluwer Academic Publishers.
  46. Team RDC, 2005. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
  47. Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED, 2008. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. J Med Entomol 45 : 125–128.
  48. Kilpatrick AM, Kramer LD, Campbell S, Alleyne EO, Dobson AP, Daszak P, 2005. West Nile virus risk assessment and the bridge vector paradigm. Emerg Infect Dis 11 : 425–429.
  49. Gruwell JA, Fogarty CL, Bennett SG, Challet GL, Vanderpool KS, Jozan M, Webb JP, 2000. Role of peridomestic birds in the transmission of St. Louis encephalitis virus in southern California. J Wildl Dis 36 : 13–34.
  50. Komar N, Panella NA, Burns JE, Dusza SW, Mascarenhas TM, Talbot TO, 2001. Serologic evidence for West Nile virus infection in birds in the New York City vicinity during an outbreak in 1999. Emerg Infect Dis 7 : 621–625.
  51. Komar N, Panella NA, Boyce E, 2001. Exposure of domestic mammals to West Nile virus during an outbreak of human encephalitis, New York City, 1999. Emerg Infect Dis 7 : 736–738.
  52. Ostfeld RS, Keesing F, 2000. Biodiversity and disease risk: the case of Lyme disease. Cons Bio 14 : 722–728.
  53. Apperson CS, Harrison BA, Unnasch TR, Hassan HK, Irby WS, Savage HM, Aspen SE, Watson DW, Rueda LM, Engber BR, Nasci RS, 2002. Host-feeding habits of Culex and other mosquitoes (Diptera: Culicidae) in the Borough of Queens in New York City, with characters and techniques for identification of Culex mosquitoes. J Med Entomol 39 : 777–785.
  54. Patrican LA, Hackett LE, Briggs JE, McGowan JW, Unnasch TR, Lee JH, 2007. Host-feeding patterns of Culex mosquitoes in relation to trap habitat. Emerg Infect Dis 13 : 1921–1923.
  55. Byrne K, Nichols RA, 1999. Culex pipiens in London underground tunnels: differentiation between surface and subterranean populations. Heredity 82 : 7–15.
  56. Fonseca DM, Keyghobadi N, Malcolm CA, Mehmet C, Schaffner F, Mogi M, Fleischer RC, Wilkerson RC, 2004. Emerging vectors in the Culex pipiens complex. Science 303 : 1535–1538.
  57. Kent RJ, Harrington LC, Norris DE, 2007. Genetic differences between Culex pipiens f. molestus and Culex pipiens pipiens (Diptera: Culicidae) in New York. J Med Entomol 44 : 50–59.
  58. Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, Fonseca DM, 2007. Genetic influences on mosquito feeding behavior and the emergence of zoonotic pathogens. Am J Trop Med Hyg 77 : 667–671.
  59. Fyodorova MV, Savage HM, Lopatina JV, Bulgakova TA, Ivanitsky AV, Platonova OV, Platonov AE, 2006. Evaluation of potential West Nile virus vectors in Volgograd region, Russia, 2003 (Diptera: Culicidae): species composition, bloodmeal host utilization, and virus infection rates of mosquitoes. J Med Entomol 43 : 552–563.
  60. Reuben R, Thenmozhi V, Samuel PP, Gajanana A, Mani TR, 1992. Mosquito blood feeding patterns as a factor in the epidemiology of Japanese encephalitis in southern India. Am J Trop Med Hyg 46 : 654–663.
  61. Anderson RA, Edman JD, Scott TW, 1990. Rubidium and cesium as host blood-markers to study multiple blood feeding by mosquitos (Diptera, Culicidae). J Med Entomol 27 : 999–1001.
  62. Hodgson JC, Spielman A, Komar N, Krahforst CF, Wallace GT, Pollack RJ, 2001. Interrupted blood-feeding by Culiseta melanura (Diptera: Culicidae) on European starlings. J Med Entomol 38 : 59–66.
  63. Edman JD, 1971. Host-feeding patterns of Florida mosquitos. 1. Aedes, Anopheles, Coquillettidia, Mansonia and Psorophora. J Med Entomol 8 : 687–695.
  64. Molaei G, Andreadis TG, 2006. Identification of avian- and mammalian-derived bloodmeals in Aedes vexans and Culiseta melanura (Diptera: Culicidae) and its implication for West Nile virus transmission in Connecticut, USA. J Med Entomol 43 : 1088–1093.
  65. Dobson A, 2004. Population dynamics of pathogens with multiple host species. American Naturalist 164 : S64–S78.
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  • Received : 10 Jun 2008
  • Accepted : 06 Oct 2008

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