Avian species diversity and transmission of West Nile virus in Atlanta, Georgia

Abstract

Background: The dilution effect is the reduction in vector-borne pathogen transmission associated with the presence of diverse potential host species, some of which are incompetent. It is popularized as the notion that increased biodiversity leads to decreased rates of disease. West Nile virus (WNV) is an endemic mosquito-borne virus in the United States that is maintained in a zoonotic cycle involving various avian host species. In Atlanta, Georgia, substantial WNV presence in the vector and host species has not translated into a high number of human cases.

Methods: To determine whether a dilution effect was contributing to this reduced transmission, we characterized the host species community composition and performed WNV surveillance of hosts and vectors in urban Atlanta between 2010 and 2011. We tested the relationship between host diversity and both host seroprevalence and vector infection rates using a negative binomial generalized linear mixed model.

Results: Regardless of how we measured host diversity or whether we considered host seroprevalence and vector infection rates as predictor variables or outcome variables, we did not detect a dilution effect. Rather, we detected an amplification effect, in which increased host diversity resulted in increased seroprevalence or infection rates; this is the first empirical evidence for this effect in a mosquito-borne system.

Conclusions: We suggest that this effect may be driven by an over-abundance of moderately- to poorly-competent host species, such as northern cardinals and members of the Mimid family, which cause optimal hosts to become rarer and present primarily in species-rich areas. Our results support the notion that dilution or amplification effects depend more on the identities of the species comprising the host community than on the absolute diversity of hosts.

Keywords: Amplification; Community composition; Dilution effect; Host competence; Northern cardinal; West Nile virus.

Fig. 1

Map of the eight study sites in urban Atlanta, GA, USA, 2010–2011. Grant and Piedmont Parks each included two sampling zones, outlined within the park borders: (1) a water feature and surrounding structures; (2) a wooded area and associated walking paths. Survey points within each site are also shown. Copyright: Licensed to Mary Ann Liebert, Inc., New Rochelle, NY and reprinted in part with permission. Citation: Levine et al (2013) Limited spillover to humans from West Nile Virus viremic birds in Atlanta, Georgia: Fig. 1, Vector-Borne and Zoonotic Diseases 2013, 13: 11, pp. 812–817

Fig. 2

Shannon-Wiener avian species diversity indices. Indices were calculated at each of the eight study sites representing 4 microhabitat types in urban Atlanta, GA, USA, May-October, 2010–2011. a Species diversity at-large, calculated considering all observed birds. b Species diversity experienced by the pathogen, calculated considering only species observed previously to have been utilized as a Culex blood-meal host

Fig. 3

Association between avian species diversity and seroprevalence rates. Included are hatch-year birds at each of the eight study sites representing 4 microhabitat types in urban Atlanta, GA, USA, July-October, 2010–2011. a Species diversity at-large: here diversity was calculated considering all observed birds and infection status was examined in all sampled birds. b Species diversity experienced by the pathogen: here, both diversity and infection status were calculated considering only species observed previously to have been utilized as a Culex blood-meal host

Fig. 4

Association between avian species diversity and Culex minimum infection rate (MIR). Included are MIRs from each of the eight study sites representing 4 microhabitat types in urban Atlanta, GA, USA, July-September, 2010–2011. a Species diversity at-large: here diversity was calculated considering all observed birds. b Species diversity experienced by the pathogen: here, diversity was calculated considering only species observed previously to have been utilized as a Culex blood-meal host