Skip to main content

Advertisement

Log in

Avian host community structure and prevalence of West Nile virus in Chicago, Illinois

  • Community Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Vertebrate host diversity has been postulated to mediate prevalence of zoonotic, vector-borne diseases, such that as diversity increases, transmission dampens. This “dilution effect” is thought to be caused by distribution of infective bites to incompetent reservoir hosts. We quantified avian species richness, avian seroprevalence for antibodies to West Nile virus (WNV), and infection of WNV in Culex mosquitoes, in the Chicago metropolitan area, Illinois, USA, a region of historically high WNV activity. Results indicated high overall avian seroprevalence and variation in seroprevalence across host species; however, there was no negative correlation between avian richness and Culex infection rate or between richness and infection status in individual birds. Bird species with high seroprevalence, especially northern cardinals and mourning doves, may be important sentinels for WNV in Chicago, since they were common and widespread among all study sites. Overall, our results suggest no net effect of increasing species richness to West Nile virus transmission in Chicago. Other intrinsic and extrinsic factors, such as variation in mosquito host preference, reservoir host competence, temperature, and precipitation, may be more important than host diversity for driving interannual variation in WNV transmission. These results from a fine-scale study call into question the generality of a dilution effect for WNV at coarser spatial scales.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andreadis TG, Thomas MC, Shepard JJ (2005) Identification guide to the mosquitoes of Connecticut. The Connecticut Agricultural Experiment Station, New Haven

    Google Scholar 

  • Bell JA, Mickelson NJ, Vaughan JA (2005) West Nile virus in host-seeking mosquitoes within a residential neighborhood in Grand Forks, North Dakota. Vector Borne Zoonotic Dis 5:373–382. doi:10.1089/vbz.2005.5.373

    Article  PubMed  Google Scholar 

  • Bernard KA, Maffei JG, Jones SA, Kauffman EB, Ebel GD, DuPuis APII, Ngo KA, Nicholas DC, Young DM, Shi P-Y, Kulasekera VL, Edison M, White DJ, Stone WB, New York State West Nile Virus Surveillance Team , Kramer LD (2001) WNV infection in birds and mosquitoes, New York State, 2000. Emerg Infect Dis 7:679–685

    PubMed  CAS  Google Scholar 

  • Bernasconi NL, Traggiai E, Lanzavecchia A (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199–2202

    Article  PubMed  CAS  Google Scholar 

  • Bertolotti L, Kitron UD, Walker ED, Ruiz MO, Brawn JD, Loss SR, Hamer GL, Goldberg TL (2008) Fine scale genetic variation and evolution of West Nile virus in a transmission “hot spot” in suburban Chicago, USA. Virology 374:381–389

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Biggerstaff BJ (2006) PooledInfRate, version 3.0: a microsoft excel add-in to compute prevalence estimates from pooled samples

  • Blitvich BJ, Marlenee NL, Hall RA, Calisher CH, Bowen RA, Roehrig JT, Komar N, Langevin SA, Beaty BJ (2003) Epitope-blocking enzyme-linked immunosorbent assays for the detection of serum antibodies to West Nile virus in multiple avian species. J Clin Microbiol 41:1041–1047. doi:10.1128/JCM.41.3.1041-1047.2003

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Aldstadt J, Getis A (2008) Point pattern analysis version 1.0. San Diego State University

  • Davies KF, Margules CR, Lawrence JF (2000) Which traits of species predict population declines in experimental forest fragments? Ecology 81:1450–1461

    Google Scholar 

  • Dobson AP (2004) Population dynamics of pathogens with multiple host species. Am Nat 164:S64–S78. doi:10.1086/424681

    Article  PubMed  Google Scholar 

  • Epstein PR, Defillipo C (2001) West Nile virus and drought. Global Change Hum Health 2:2–4

    Article  Google Scholar 

  • Ezenwa VO, Godsey MS, King RJ, Gupthill SC (2006) Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proc R Soc B 273:109–117. doi:10.1098/rspb.2005.3284

    Article  PubMed  Google Scholar 

  • 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. doi:10.1089/vbz.2006.6.57

    Article  PubMed  Google Scholar 

  • Gilbert L, Norman R, Laurenson K, Reid HW, Hudson PJ (2001) Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large scale wild populations. J Anim Ecol 70:1053–1061

    Article  Google Scholar 

  • Godsey MS, Blackmore MS, Panella NA, Burkhalter K, Gottfried K, Halsey LA, Rutledge R, Langevin SA, Gates R, Lamonte KM, Lambert A, Lanciotti RS, Blackmore CGM, Loyless T, Stark L, Oliver T, Conti L, Komar N (2005) West Nile virus epizootiology in the southeastern United States, 2001. Vector Borne Zoonotic Dis 9:483–484

    Google Scholar 

  • Gylfe A, Bergstrom S, Lundstrom J (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1089/vbz.2007.0123

    Article  PubMed  Google Scholar 

  • 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 (in press)

  • Hayes CG (1989) West Nile fever. In: Monath TP (ed) The Arboviruses: epidemiology and ecology. CRC Press Inc, Boca Raton, pp 59–88

    Google Scholar 

  • Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM (2003) Parasite establishment in host communities. Ecol Lett 6:837–842. doi:10.1046/j.1461-0248.2003.00501.x

    Article  Google Scholar 

  • Illinois Department of Agriculture (2008) Illinois Gap Analysis Program, Land Cover Classification. (online) URL: http://www.agr.state.il.us/gis/pass/gapdata. Accessed 7-15-2008

  • Illinois Department of Public Health. West Nile virus. [online] URL: http://www.idph.state.il.us/envhealth/wnv.htm. Accessed 7-15-2008

  • Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498. doi:10.1111/j.1461-0248.2006.00885.x

    Article  PubMed  CAS  Google Scholar 

  • Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD (2006) Host heterogeneity dominates West Nile virus transmission. Proc R Soc B 273:2327–2333. doi:10.1098/rspb.2006.3575

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kleen VL, Cordle L, Montgomery RA (2004) The Illinois Breeding Bird Atlas. Illinois Natural History Survey, Champaign

    Google Scholar 

  • Komar N, Panella NA, Burns JE, Dusza SW, Mascarenhas TM, Talbot TO (2001a) 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

    PubMed  CAS  Google Scholar 

  • Komar N, Burns J, Dean C, Panella NA, Dusza S, Cherry B (2001b) Serologic evidence for West Nile virus infection in birds in Staten Island, New York, after an outbreak in 2000. Vector Borne Zoonotic Dis 1:191–196

    Article  PubMed  CAS  Google Scholar 

  • Komar N (2001) West Nile virus: epidemiology and ecology in North America. Adv Virus Res 61:185–234

    Google Scholar 

  • Komar N, Langevin S, Hinten DB, Nemeth N, Edwards E, Hettler DL, Davis B, Bowen R, Munning M (2003) Experimental infection of the New York 1999 strain of West Nile virus in North American birds. Emerg Infect Dis 9:311–322

    PubMed  Google Scholar 

  • Komar N, Panella NA, Langevin SA, Brault AC, Amador M, Edwards E, Owen JC (2005) Avian hosts for West Nile virus in St. Tammany Parrish, Louisiana, 2002. Am J Trop Med Hyg 73:1031–1100

    PubMed  Google Scholar 

  • LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–713. doi:10.1038/nature05829

    Article  PubMed  CAS  Google Scholar 

  • Lampman RL, Novak RJ (1996) Oviposition preferences of Culex pipiens and Culex restuans for infusion-baited traps. J Am Mosq Control Assoc 12:23–32

    PubMed  CAS  Google Scholar 

  • Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe KE, Crabtree MB, Scherret JH, Hall RA, MacKenzie JS, Cropp CB, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage HM, Stone W, McNamara T, Gubler DJ (1999) Origin of the West Nile virus responsible for an outbreak of Encephalitis in the northeastern United States. Science 286:2333–2337. doi:10.1126/science.286.5448.2333

    Article  PubMed  CAS  Google Scholar 

  • Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol 38:4066–4071

    PubMed  CAS  Google Scholar 

  • McLean RG, Ubico SR, Docherty DE, Hansen WR, Sileo L, McNamara TS (2001) West Nile virus transmission and ecology in birds. Ann NY Acad Sci 951:54–57

    Article  PubMed  CAS  Google Scholar 

  • McLean RG (2006) West Nile virus in North American birds. Ornithol Monogr 60:44–64. doi:10.1642/0078-6594(2006)60[44:WNVINA]2.0.CO;2

    Article  Google Scholar 

  • Meyer RP, Hardy JL, Reisen WK (1990) Diel changes in adult mosquito microhabitat temperatures and their relationship to the extrinsic incubation of arboviruses in mosquitoes in Kern County, California. J Med Entomol 27:607–614

    PubMed  CAS  Google Scholar 

  • Molaei G, Andreadis TG, 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

    PubMed  Google Scholar 

  • Naugle DE, Aldridge CL, Walker BL, Cornish TE, Moynahan BJ, Holloran MJ, Brown K, Johnson GD, Schmidtmann ET, Mayer RT, Kato CY, Matchett MR, Christiansen TJ, Cook WE, Creekmore T, Falise RD, Rinkes ET, Boyse MS (2004) West Nile virus: pending crisis for greater sage-grouse. Ecol Lett 7:704–713. doi:10.1111/j.1461-0248.2004.00631.x

    Article  Google Scholar 

  • Norman R, Bowers RJ, Begon M, Hudson PJ (1999) Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite-mediated competition. J Theor Biol 200:111–118. doi:10.1006/jtbi.1999.0982

    Article  PubMed  CAS  Google Scholar 

  • Ostfeld RS, Keesing F (2000a) The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 78:2061–2078. doi:10.1139/cjz-78-12-2061

    Article  Google Scholar 

  • Ostfeld RS, Keesing F (2000b) Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 14:722–728. doi:10.1046/j.1523-1739.2000.99014.x

    Article  Google Scholar 

  • Peixoto ID, Abramson G (2006) The effect of biodiversity on the hantavirus epidemic. Ecology 87:873–879

    Article  PubMed  Google Scholar 

  • Petersen LR, Roehrig JT (2001) West Nile virus: a reemerging global pathogen. Emerg Infect Dis 7:611–614

    PubMed  CAS  Google Scholar 

  • Platonov AE, Shipulin GA, Shipulina OY, Tyutyunnik EN, Frolochkina TI, Lanciotti RS, Yazyshina S, Platonov OV, Obukhov IL, Zhukov AN, Vengerov YY, Pokrovskii VI (2001) Outbreak of West Nile virus infection, Volgograd Region, Russia, 1999. Emerg Infect Dis 7:128–132

    Article  PubMed  CAS  Google Scholar 

  • Reisen WK, Fang Y, Martinez VM (2006) Effects of temperature on transmission of West Nile virus by Culex tarsalis (Diptera: Culicidae). J Med Entomol 43:309–317

    Article  PubMed  Google Scholar 

  • Reynolds RT, Scott JM, Nussbaum RA (1980) A variable circular-plot method for estimating bird numbers. Condor 82:309–313. doi:10.2307/1367399

    Article  Google Scholar 

  • Ringia AM, Blitvich BJ, Koo H-Y, 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

    PubMed  Google Scholar 

  • Rocke T, Converse K, Meteyer C, McLean B (2005) The impact of disease in the American White Pelican in North America. In: Anderson DW, King DT, Coulson J (eds) Waterbirds, special publication 1: the biology and conservation of the American White Pelican 28:87–94

  • Ruiz MO, Tedesco C, McTighe TJ, Austin C, Kitron U (2004) Environmental, social determinants of human risk during a West Nile virus outbreak in the greater Chicago area, 2002. Int J Health Geogr 3:11

    Article  Google Scholar 

  • Schmidt KA, Ostfeld RS (2000) Biodiversity and the dilution effect in disease ecology. Ecology 82:609–619

    Article  Google Scholar 

  • Shaman J, Day JF, Stieglitz M (2005) Drought-induced amplification and epidemic transmission of West Nile Virus in southern Florida. J Med Entomol 42:134–141. doi:10.1603/0022-2585(2005)042[0134:DAAETO]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Simberloff D (1972) Properties of the rarefaction diversity measurement. Am Nat 106:414–418

    Article  Google Scholar 

  • Staszewski V, McCoy KD, Tveraa T, Boulinier T (2007) Interannual dynamics of antibody levels in naturally-infected long-lived colonial birds. Ecology 88:3183–3191

    Article  PubMed  Google Scholar 

  • Swaddle JP, Calos SE (2008) Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLOS One 3:e2488

    Article  PubMed  CAS  Google Scholar 

  • Tempelis CJ (1975) Host feeding patterns of mosquitoes with a review of advances in analysis of blood meals by serology. J Med Entomol 11:635–653

    PubMed  CAS  Google Scholar 

  • Thomas L, Laake JL, Strindberg S, Marques FFC, Buckland ST, Borchers DL, Anderson DR, Burnham KP, Hedley SL, Pollard JH, Bishop JRB, Marques TA (2005) Distance 5.0, Release 5. Research Unit for Wildlife Population Assessment, University of St. Andrews, UK. http://www.ruwpa.stand.ac.uk/distance/

  • Turrell MJ, Dohm DJ, Sardelis MR, O’Guinn ML, Andreadis TG, Blow JA (2005) An update on the potential of NA mosquitoes (Diptera: Culicidae) to transmit WNV. J Med Entomol 42:57–62

    Article  Google Scholar 

  • U.S. Census Bureau. American Factfinder: 2000 census of population and housing, summary file 3. (online) URL: http://factfinder.census.gov. Accessed 7-15-2008

  • U.S. Geological Survey: North American Breeding Bird Survey. 1998 BBS Instructions. (online) URL: http://www.pwrc.usgs.gov/bbs/participate/instructions.html. Accessed 7-15-2007

  • Woolhouse MEJ, Dye C, Etard J-F, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JLK, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA 94:338–342. doi:10.1073/pnas.94.1.338

    Article  PubMed  CAS  Google Scholar 

  • Zinkernagel RM, Hengartner H (2006) Protective “immunity” by pre-existent neutralizing antibody titers and preactivated T cells but not by so-called “immunological memory”. Immunol Rev 211:310–319

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Village of Oak Lawn, Illinois, especially the Department of Public Works, who generously provided laboratory space during the study, as well as the municipalities who cooperated with us during field research (Alsip, City of Chicago, Evergreen Park, Harvey, Indian Head Park, Orland Park, Palos Hills). T. Thompson, G. Amore, S. Dallman, D. Gohde, M. Goshorn, J. McClain, M. Neville, B. Pultorak, and E. Secker, provided field assistance, and B. Bullard, B. Morgan, A. Thelen, M. Bender, L. Abernathy, and J. McClain assisted with processing samples in the laboratory. L. Stark and the Florida Department of Health provided positive control chicken serum, L. Mosher and the Michigan Department of Community Health provided the positive control NY99 strain of WNV, and the CDC Division of Vector Borne Infectious Diseases supplied the 4G2 and 6B6C-1 antibodies. This work was supported by the NSF/NIH program in the Ecology of Infectious Diseases (grant 04-29124). All fieldwork was carried out under appropriate collecting permits with approvals from the University of Illinois Animal Use Protocol no. 03034 and Institutional Animal Care and Use Committee at Michigan State University, Animal Use Form no. 12/03-152-00.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Scott R. Loss.

Additional information

Communicated by Heli Siitari.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Loss, S.R., Hamer, G.L., Walker, E.D. et al. Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia 159, 415–424 (2009). https://doi.org/10.1007/s00442-008-1224-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1224-6

Keywords

Navigation