Supersuppression: Reservoir Competency and Timing of Mosquito Host Shifts Combine to Reduce Spillover of West Nile Virus

Abstract

In the eastern United States, human cases of West Nile virus (WNV) result from spillover from urban epizootic transmission between passerine birds and Culex 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 Culex 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.

Figure 1.

Map of study sites in urban Atlanta, GA, 2010–2012. Grant and Piedmont Parks each included two sampling zones, for a total of nine study sites: 1) a water feature and surrounding built structures and 2) a wooded area and associated walking paths. Reprinted with permission from Vector-Borne and Zoonotic Diseases 13 (11), pp. 812–817, published by Mary Ann Liebert, Inc., New Rochelle, NY.

Figure 2.

Temporal trends of West Nile virus (WNV) infection among birds and mosquitoes sampled in urban Atlanta, GA, 2010–2012. For birds, infection was measured by seroprevalence in hatch-year individuals (incidence), who necessarily became infected in the sampling year. Error bars show the standard error of this binomial variable. For mosquitoes, infection was measured by maximum likelihood estimates of WNV minimum infection rates in Culex mosquitoes. Error bars show the 95% confidence intervals of these estimates.

Figure 3.

Predicted probability of seropositivity among seven key avian species across microhabitat types as generated by a binomial generalized linear mixed effects model among birds captured in urban Atlanta, GA, 2010–2012. Error bars indicate standard error of each estimate.

Figure 4.

(A) Relative avian abundance, (B) proportion of Culex blood meals, (C) and amplification fraction (force of infection) among microhabitat types in urban Atlanta, GA, 2010–2011.

Figure 5.

Predicted probability of finding West Nile virus (WNV)–positive mosquitoes over time across microhabitat types as generated by a negative binomial generalized linear mixed effects model for mosquitoes captured in urban Atlanta, GA, 2010–2012. Error bars indicate standard error of each estimate.

Figure 6.

Temporal trends of blood-meal hosts among Culex mosquitoes sampled in urban Atlanta, GA, 2010–2011. Error bars show the standard errors of these binomial variables.