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
Similar content being viewed by others
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
Anderson R, May R (1979) Population biology of infectious diseases: part II. Nature 280:455–461
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
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
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
Barr A (1957) The distribution of Culex p. pipiens and Culex p. quinquefasciatus in North America. Am J Trop Med Hyg 6:153–165
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
Bibby C, Burgess N, Hill D, Mustoe S (2000) Bird census techniques. Academic Press, London
Biggerstaff B (2003) PooledInfRate: a Microsoft Excel Add-In to computer prevalence estimates from pooled samples. CDC, Fort Collins
Blair R (1996) Land use and avian species diversity along an urban gradient. Ecol Appl 6:506–519
Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer, New York
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
Daszak P, Cunningham A, Hyatt A (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116
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
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
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
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
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
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
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
Goddard L, Roth A, Reisen W, Scott T (2002) Vector competence of California mosquitoes for West Nile virus. Emerg Infect Dis 8:1385–1391
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
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
Keesing F, Holt R, Ostfeld R (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498
Kenney BC (1982) Beware of spurious self-correlations! Water Resour Res 18:1041–1048
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
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
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
Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112:145–164
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
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
LaDeau S, Kilpatrick A, Marra P (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–713
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
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
Magurran A (1988) Ecological diversity and its measurement, 1st edn. Princeton University Press, Princeton
Manly B (1991) Randomization and Monte Carlo methods in biology. Chapman & Hall, London
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
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
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
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
Ostfeld R, Keesing F (2000) The role of biodiversity in the ecology of vector-borne zoonotic disease. Can J Zool 78:2061–2078
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
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
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
Rosenberg M (2001) PASSAGE: pattern analysis, spatial statistics, and geographic exegesis. Department of Biology, Arizona State University, Tempe
Schmidt K, Ostfeld R (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82:609–619
Sheets HD, Mitchell CE (2001) Uncorrelated change produces the apparent dependence of evolutionary rate of interval. Paleobiology 27:429–445
Smith P (2003) Winter bird use of urban and rural habitats in Ontario. Can Field Nat 117:173–183
Smouse P, Long J, Sokal R (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632
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
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
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
Vinogradova E (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft, Sofia
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Craig Osenberg.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-008-1169-9