Volume 95, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



In the eastern United States, human cases of West Nile virus (WNV) result from spillover from urban epizootic transmission between passerine birds and mosquitoes. In Atlanta, GA, substantial WNV presence in hosts and vectors has not resulted in the human disease burden observed in cities with similar infection pressure. Our study goal was to investigate extrinsic ecological conditions that potentially contribute to these reduced transmission rates. We conducted WNV surveillance among hosts and vectors in urban Atlanta and recorded an overall avian seroprevalence of nearly 30%, which was significantly higher among northern cardinals, blue jays, and members of the mimid family, and notably low among American robins. Examination of temporal feeding patterns showed a marked feeding shift from American robins in the early season to northern cardinals in the late season. We therefore rule out American robins as superspreaders in the Atlanta area and suggest instead that northern cardinals and mimids act as WNV “supersuppressor” species, which slow WNV transmission by drawing many infectious bites during the critical virus amplification period, yet failing to amplify transmission due to low host competencies. Of particular interest, urban forest patches provide spillover protection by increasing the WNV amplification fraction on supersuppressor species.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Kramer LD, Styer LM, Ebel GD, , 2008. A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53: 6181.[Crossref] [Google Scholar]
  2. CDC, 2015. West Nile Virus Infection. Available at: http://www.cdc.gov/westnile/index.html. Accessed May 28, 2016. [Google Scholar]
  3. Petersen LR, Brault AC, Nasci RS, , 2013. West Nile virus: review of the literature. JAMA 310: 308315.[Crossref] [Google Scholar]
  4. CDC, 2002. Provisional surveillance summary of the West Nile virus epidemic: United States, January–November 2002. Morb Mortal Wkly Rep 51: 11291133. [Google Scholar]
  5. Fenton A, Pedersen AB, , 2005. Community epidemiology framework for classifying disease threats. Emerg Infect Dis 11: 18151821.[Crossref] [Google Scholar]
  6. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, Hudson PJ, Grenfell BT, , 2009. Epidemic dynamics at the human-animal interface. Science 326: 13621367.[Crossref] [Google Scholar]
  7. Vazquez Prokopec GM, Eng JV, Kelly R, Mead DG, Kolhe P, Howgate J, Kitron UD, Burkot T, , 2010. The risk of West Nile virus infection is associated with combined sewer overflow streams in urban Atlanta, Georgia, USA. Environ Health Perspect 118: 13821388.[Crossref] [Google Scholar]
  8. Allison AB, Mead DG, Gibbs SEJ, Hoffman DM, Stallknecht DE, , 2004. West Nile virus viremia in wild rock pigeons. Emerg Infect Dis 10: 22522255.[Crossref] [Google Scholar]
  9. 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: 5772.[Crossref] [Google Scholar]
  10. Bradley CA, Gibbs SEJ, Altizer S, , 2008. Urban land use predicts West Nile virus exposure in songbirds. Ecol Appl 18: 10831092.[Crossref] [Google Scholar]
  11. 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: 5767.[Crossref] [Google Scholar]
  12. USGS, 1966. North American Breeding Bird Survey. Available at: https://www.pwrc.usgs.gov/bbs/. Accessed December 19, 2013. [Google Scholar]
  13. Kilpatrick A, Daszak P, Jones M, Marra P, Kramer L, , 2006. Host heterogeneity dominates West Nile virus transmission. Proc R Soc Lond B Biol Sci 273: 23272333.[Crossref] [Google Scholar]
  14. Diuk-Wasser MA, Molaei G, Simpson JE, Folsom-O'Keefe CM, Armstrong PM, Andreadis TG, , 2010. Avian communal roosts as amplification foci for West Nile virus in urban areas in northeastern United States. Am J Trop Med Hyg 82: 337343.[Crossref] [Google Scholar]
  15. Godsey MS, King RJ, Burkhalter K, Delorey M, Colton L, Charnetzky D, Sutherland G, Ezenwa VO, Wilson LA, Coffey M, Milheim LE, Taylor VG, Palmisano C, Wesson DM, Guptill SC, , 2013. Ecology of potential West Nile virus vectors in southeastern Louisiana: enzootic transmission in the relative absence of Culex quinquefasciatus . Am J Trop Med Hyg 88: 986996.[Crossref] [Google Scholar]
  16. Nowak DJ, Rowntree RA, McPherson EG, Sisinni SM, Kerkmann ER, Stevens JC, , 1996. Measuring and analyzing urban tree cover. Landsc Urban Plan 36: 4957.[Crossref] [Google Scholar]
  17. Sibley DA, , 2000. The Sibley Guide to Birds. New York, NY: Alfred A. Knopf. [Google Scholar]
  18. Pyle P, , 1997. Identification Guide to North American Birds. Bolinas, CA: Slate Creek Press. [Google Scholar]
  19. USGS, 1920. Bird Banding Laboratory. Available at: https://www.pwrc.usgs.gov/bbl/. Accessed December 19, 2013. [Google Scholar]
  20. 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 159: 415424.[Crossref] [Google Scholar]
  21. Young JS, Climburg A, Smucker K, Hutto RL, , 2007. Point Count Protocol, Northern Region Landbird Monitoring Program. Avian Science Center, Division of Biological Sciences, University of Montana. [Google Scholar]
  22. Newhouse VF, Chamberlain RW, Johnson JG, Sudia WD, , 1966. Use of dry ice to increase mosquito catches of the CDC miniature light trap. Mosq News 26: 3035. [Google Scholar]
  23. Reiter P, , 1983. A portable, battery-powered trap for collecting gravid Culex mosquitoes. Mosq News 43: 496498. [Google Scholar]
  24. Detinova TS, , 1962. Age-Grouping Methods in Diptera of Medical Importance. Geneva, Switzerland: World Health Organization. [Google Scholar]
  25. Levine RS, Mead DG, Kitron UD, , 2013. Limited spillover to humans from West Nile virus viremic birds in Atlanta, Georgia. Vector Borne Zoonotic Dis 13: 812817.[Crossref] [Google Scholar]
  26. Roellig DM, Gomez-Puerta LA, Mead DG, Pinto J, Ancca-Juarez J, Calderon M, Bern C, Gilman RH, Cama VA, The Chagas Disease Workgroup in Arequipa, , 2013. Hemi-nested PCR and RFLP methodologies for identifying blood meals of the Chagas disease vector, Triatoma infestans . PLoS One 8: e74713.[Crossref] [Google Scholar]
  27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, , 1990. Basic local alignment search tool. J Mol Biol 215: 403410.[Crossref] [Google Scholar]
  28. Chaves LF, , 2010. An entomologist guide to demystify pseudoreplication: data analysis of field studies with design constraints. J Med Entomol 47: 291298.[Crossref] [Google Scholar]
  29. Hurlbert SH, , 1984. Pseudoreplication and the design of ecological experiments. Ecol Monogr 54: 187211.[Crossref] [Google Scholar]
  30. Skaug H, Fournier D, Nielsen A, Magnusson A, Bolker B, , 2013. Generalized linear mixed models using AD model builder. R Package Version 0.7.2. Available at: http://glmmadmb.r-forge.r-project.org. [Google Scholar]
  31. Elston DA, Moss R, Bouliner T, Arrowsmith C, Lambin X, , 2001. Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122: 563569.[Crossref] [Google Scholar]
  32. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Brunning M, , 2003. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9: 311322.[Crossref] [Google Scholar]
  33. Nemeth NM, Oesterle PT, Bowen RA, , 2009. Humoral immunity to West Nile virus is long-lasting and protective in the house sparrow (Passer domesticus). Am J Trop Med Hyg 80: 864869. [Google Scholar]
  34. Fiske I, Chandler R, , 2011. Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Softw 4: 123. [Google Scholar]
  35. Dail D, Madsen L, , 2011. Models for estimating abundance from repeated counts of an open metapopulation. Biometrics 67: 577587.[Crossref] [Google Scholar]
  36. 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. [Google Scholar]
  37. Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED, , 2009. Host selection by Culex pipiens mosquitoes and West Nile virus amplification. Am J Trop Med Hyg 80: 268278. [Google Scholar]
  38. Calenge C, , 2006. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Modell 197: 516519.[Crossref] [Google Scholar]
  39. Hamer GL, Chaves LF, Anderson TK, Kitron UD, Brawn JDO, Ruiz M, Loss SR, Walker ED, Goldberg TL, , 2011. Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile Virus transmission. PLoS One 6: e23767.[Crossref] [Google Scholar]
  40. US Census Bureau, 2010. Data Tools Easy Stats. Available at: http://www.census.gov/en.html. [Google Scholar]
  41. Kilpatrick AM, LaDeau SL, Marra PP, , 2007. Ecology of West Nile virus transmission and its impact on birds in the western hemisphere. Auk 124: 11211136.[Crossref] [Google Scholar]
  42. Wheeler SS, Vineyard MP, Barker CM, Reisen WK, , 2012. Importance of recrudescent avian infection in West Nile virus overwintering: incomplete antibody neutralization of virus allows infrequent vector infection. J Med Entomol 49: 895902.[Crossref] [Google Scholar]
  43. Kilpatrick A, Kramer L, Jones M, Marra P, Daszak P, , 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4: e82.[Crossref] [Google Scholar]
  44. LaDeau SL, Marra PP, Kilpatrick AM, Calder CA, , 2008. West Nile virus revisited: consequences for North American ecology. Bioscience 58: 937946.[Crossref] [Google Scholar]
  45. Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, Diuk-Wasser MA, , 2012. Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. Proc Biol Sci 279: 925933.[Crossref] [Google Scholar]

Data & Media loading...

Supplementary PDF

  • Received : 11 Nov 2015
  • Accepted : 09 Jun 2016
  • Published online : 02 Nov 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error