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Ecological correlates of risk and incidence of West Nile virus in the United States

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Abstract

West Nile virus, which was recently introduced to North America, is a mosquito-borne pathogen that infects a wide range of vertebrate hosts, including humans. Several species of birds appear to be the primary reservoir hosts, whereas other bird species, as well as other vertebrate species, can be infected but are less competent reservoirs. One hypothesis regarding the transmission dynamics of West Nile virus suggests that high bird diversity reduces West Nile virus transmission because mosquito blood-meals are distributed across a wide range of bird species, many of which have low reservoir competence. One mechanism by which this hypothesis can operate is that high-diversity bird communities might have lower community-competence, defined as the sum of the product of each species’ abundance and its reservoir competence index value. Additional hypotheses posit that West Nile virus transmission will be reduced when either: (1) abundance of mosquito vectors is low; or (2) human population density is low. We assessed these hypotheses at two spatial scales: a regional scale near Saint Louis, MO, and a national scale (continental USA). We found that prevalence of West Nile virus infection in mosquito vectors and in humans increased with decreasing bird diversity and with increasing reservoir competence of the bird community. Our results suggest that conservation of avian diversity might help ameliorate the current West Nile virus epidemic in the USA

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References

  • Akaike H (1992) Information theory and an extension of the maximum likelihood principle. In: Kotz S, Johnson N (eds) Breakthroughs in statistics. Springer, Berlin, pp 610–624

    Google Scholar 

  • Anderson R, May R (1979) Population biology of infectious diseases: part II. Nature 280:455–461

    Article  PubMed  Google Scholar 

  • Apperson C, Harrison B, Unnasch T, Hassan H, Irby W, Savage H, Aspen S, Watson D, Rueda L, Engber B, Nasci R (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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Balvanera P, Daily G, Ehrlich P, Ricketts T, Bailey S, Kark S, Kremen C, Pereira H (2001) Conserving biodiversity and ecosystem services. Science 291:2047

    Article  PubMed  CAS  Google Scholar 

  • Barr A (1957) The distribution of Culex p. pipiens and Culex p. quinquefasciatus in North America. Am J Trop Med Hyg 6:153–165

    PubMed  CAS  Google Scholar 

  • Bernard K, Maffei J, Jones S, Kauffman E, Ebel G, Dupuis A, Ngo K, Nicholas D, Young D, Shi P, Kulasekera V, Edison M, White D, Stone W, Kramer L (2001) West Nile virus infection in birds and mosquitoes, New York State, 2000. Emerg Infect Dis 7:679–685

    Article  PubMed  CAS  Google Scholar 

  • Bibby C, Burgess N, Hill D, Mustoe S (2000) Bird census techniques. Academic Press, London

    Google Scholar 

  • Biggerstaff B (2003) PooledInfRate: a Microsoft Excel Add-In to computer prevalence estimates from pooled samples. CDC, Fort Collins

    Google Scholar 

  • Blair R (1996) Land use and avian species diversity along an urban gradient. Ecol Appl 6:506–519

    Article  Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer, New York

    Google Scholar 

  • Collinge SK, Ray C (2006) Community epidemiology. In: Collinge SK, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, New York, pp 1–5

  • CDC: Center for Disease Control and Prevention (2007) CDC—West Nile virus—surveillance and control case count of West Nile Disease. http://www.cdc.gov/ncidod/dvbid/westnile/

  • Crooks K, Suarez A, Bolger D (2004) Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol Conserv 115:451–462

    Article  Google Scholar 

  • Daszak P, Cunningham A, Hyatt A (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116

    Article  PubMed  CAS  Google Scholar 

  • Dobson A, Cattadori I, Holt RD, Ostfeld RS, Keesing F, Krichbaum K, Rohr JR, Perkins SE, Hudson PJ (2006) Sacred cows and sympathetic squirrels: the importance of biological diversity to human health. PLoS Med 3(6):e231

    Article  PubMed  Google Scholar 

  • Donald P, Green R, Heath M (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc Lond Ser B 268:25–29

    Article  Google Scholar 

  • Ebel G, Rochlin I, Longacker J, Kramer L (2005) Culex restuans (Diptera: Culicidae) relative abundance and vector competence for West Nile virus. J Med Entomol 42:838–843

    Article  PubMed  Google Scholar 

  • Ezenwa V, Godsey M, King R, Guptill S (2006) Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proc R Soc B 273:109–117

    Article  PubMed  Google Scholar 

  • Ezenwa VO, Milheim LE, Coffey MF, Godsey MS, King RJ, Guptill SC (2007) Land cover variation and West Nile virus prevalence: patterns, processes, and implications for disease control. Vector Borne Zoonotic Dis 7(2):173–180. doi:10.1089/vbz.2006.0584

    Article  PubMed  Google Scholar 

  • Fonseca D, Keyghobadi N, Malcom C, Mehmet C, Schaffner F, Mogi M, Fleischer R, Wilkerson R (2004) Emerging vectors in the Culex pipiens complex. Science 303:1535–1538

    Article  PubMed  CAS  Google Scholar 

  • Fortin M, Gurevitch J (2001) Mantel tests: spatial structure in field experiments. In: Scheiner S, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 308–326

    Google Scholar 

  • Goddard L, Roth A, Reisen W, Scott T (2002) Vector competence of California mosquitoes for West Nile virus. Emerg Infect Dis 8:1385–1391

    PubMed  Google Scholar 

  • Gubler D, Petersen L, Roehrig J, Campbell G, Komar N, Nasci R, Zielinski-Gutierrez E, Marfin A, Lanciotti R, Bunning M, O’Leary D, Fernandez M, Dieterich L, Tuttle B, Deavours R (2003) Epidemic/epizootic West Nile virus in the United States: guidelines for surveillance, prevention and control, 3rd edn. CDC, Fort Collins

    Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Keesing F, Holt R, Ostfeld R (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498

    Article  PubMed  CAS  Google Scholar 

  • Kenney BC (1982) Beware of spurious self-correlations! Water Resour Res 18:1041–1048

    Google Scholar 

  • Kilpatrick A, Kramer L, Campbell S, Alleyne E, Dobson A, Daszak P (2005) West Nile virus risk assessment and the bridge vector paradigm. Emerg Infect Dis 11:425–429

    PubMed  Google Scholar 

  • Kilpatrick A, Daszak P, Jones M, Marra P, Kramer L (2006a) Host heterogeneity dominates West Nile virus transmission. Proc R Soc B 273:2327–2333

    Article  PubMed  Google Scholar 

  • Kilpatrick A, Kramer L, Jones M, Marra P, Daszak P (2006b) West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4:606–610

    Article  CAS  Google Scholar 

  • Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112:145–164

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Komar N, Panella N, Langevin S, Brault A, Amador M, Edwards E, Owen J (2005) Avian hosts for West Nile virus in St. Tammany Parish, Louisiana, 2002. Am J Trop Med Hyg 73:1031–1037

    PubMed  Google Scholar 

  • LaDeau S, Kilpatrick A, Marra P (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–713

    Article  PubMed  CAS  Google Scholar 

  • Lanciotti R, Roehrig J, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe K, Crabtree M, Scherret J, Hall R, MacKenzie J, Cropp C, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage H, Stone W, McNamara T, Gubler D (1999) Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286:2333–2337

    Article  PubMed  CAS  Google Scholar 

  • LoGiudice K, Ostfeld R, Schmidt K, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA 100:567–571

    Article  PubMed  CAS  Google Scholar 

  • Magurran A (1988) Ecological diversity and its measurement, 1st edn. Princeton University Press, Princeton

    Google Scholar 

  • Manly B (1991) Randomization and Monte Carlo methods in biology. Chapman & Hall, London

    Google Scholar 

  • Marra P, Griffing S, Caffrey C, Kilpatrick A, McLean R, Brand C, Saito E, Dupuis A, Kramer L, Novak R (2004) West Nile virus and wildlife. Bioscience 54:393–402

    Article  Google Scholar 

  • McLean R, Ubico S, Docherty D, Hansen W, Sileo L, McNamara T (2001) West Nile virus transmission and ecology in birds. Ann N Y Acad Sci 951:54–57

    PubMed  CAS  Google Scholar 

  • Miller J, Wiens J, Hobbs N, Theobald D (2003) Effects of human settlement on bird communities in lowland riparian areas of Colorado (USA). Ecol Appl 13:1041–1059

    Article  Google Scholar 

  • Naugle D, Aldridge C, Walker B, Cornish T, Moynahan B, Holloran M, Brown K, Johnson G, Schmidtmann E, Mayer R, Kato C, Matchett M, Christiansen T, Cook W, Creekmore T, Falise R, Rinkes E, Boyce M (2004) West Nile virus: pending crisis for greater sage-grouse. Ecol Lett 7:704–713

    Article  Google Scholar 

  • Ostfeld R, Keesing F (2000) The role of biodiversity in the ecology of vector-borne zoonotic disease. Can J Zool 78:2061–2078

    Article  Google Scholar 

  • Ostfeld R, Keesing F, LoGiudice K (2006) Community ecology meets epidemiology: the case of Lyme disease. In: Collinge S, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, New York, pp 28–40

  • Pain D, Pienkowski M (1997) Farming and birds in Europe: the common agricultural policy and its implications for bird conservation. Academic Press, San Diego

    Google Scholar 

  • Patz J, Daszak P, Tabor G, Aguirre A, Pearl M, Epstein J, Wolfe N, Kilpatrick A, Foufopoulos J, Molneux D, Bradley D (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112:1092–1098

    PubMed  Google Scholar 

  • Pratt H, Moore C (1993) Mosquitoes of public health importance and their control. US Department of Health and Human Services

  • Reisen W, Fang Y, Martinez V (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

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg M (2001) PASSAGE: pattern analysis, spatial statistics, and geographic exegesis. Department of Biology, Arizona State University, Tempe

    Google Scholar 

  • Schmidt K, Ostfeld R (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82:609–619

    Article  Google Scholar 

  • Sheets HD, Mitchell CE (2001) Uncorrelated change produces the apparent dependence of evolutionary rate of interval. Paleobiology 27:429–445

    Article  Google Scholar 

  • Smith P (2003) Winter bird use of urban and rural habitats in Ontario. Can Field Nat 117:173–183

    Google Scholar 

  • Smouse P, Long J, Sokal R (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Su T, Webb J, Meyer R, Mulla M (2003) Spatial and temporal distribution of mosquitoes in underground storm drain systems in Orange County, California. J Vector Ecol 28:79–89

    PubMed  Google Scholar 

  • Tiawsirisup S, Platt K, Evans R, Rowley W (2005) A comparison of West Nile virus transmission by Ochlerotatus trivittatus (COQ.), Culex pipiens (L.), and Aedes albopictus (Skuse). Vector Borne Zoonotic Dis 5:40–47

    Article  PubMed  Google Scholar 

  • Turell M, Dohm D, Sardelis M, O’Guinn M, Andreadis T, Blow J (2005) An update on the potential for North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol 42:57–62

    Article  PubMed  Google Scholar 

  • Vinogradova E (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft, Sofia

    Google Scholar 

  • Yaremych S, Warner R, Mankin P, Brawn J, Raim A, Novak R (2004) West Nile virus and high death rate in American Crows. Emerg Infect Dis 10:709–711

    PubMed  Google Scholar 

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Acknowledgments

We thank D. Allan, L. Blaustein, J. Bradford, S. Crawford, C. Frazier, P. Green, F. Keesing, T. Knight, B. McCauley, P. Morin, C. Osenberg, K. Schmidt, J. Scott, G. Storch, D. Tulloch, K. Yates, the Chase lab group, the Rutgers Center for Remote Sensing & Spatial Analysis laboratory and two anonymous reviewers for discussions, comments, and logistical support. The cooperation of numerous private land owners and public land managers made this project feasible, as did logistical support from Washington University and the Tyson Research Center. Financial support was provided by Washington University (to J.M.C.), and the Webster Groves Nature Study Society and Saint Louis Audubon Society (to B.F.A.). The authors declare that the studies described herein comply with the laws of the USA.

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Correspondence to Brian F. Allan.

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Communicated by Craig Osenberg.

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Allan, B.F., Langerhans, R.B., Ryberg, W.A. et al. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158, 699–708 (2009). https://doi.org/10.1007/s00442-008-1169-9

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  • DOI: https://doi.org/10.1007/s00442-008-1169-9

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