West Nile Virus Epidemics in North America Are Driven by Shifts in Mosquito Feeding Behavior

Abstract

West Nile virus (WNV) has caused repeated large-scale human epidemics in North America since it was first detected in 1999 and is now the dominant vector-borne disease in this continent. Understanding the factors that determine the intensity of the spillover of this zoonotic pathogen from birds to humans (via mosquitoes) is a prerequisite for predicting and preventing human epidemics. We integrated mosquito feeding behavior with data on the population dynamics and WNV epidemiology of mosquitoes, birds, and humans. We show that Culex pipiens, the dominant enzootic (bird-to-bird) and bridge (bird-to-human) vector of WNV in urbanized areas in the northeast and north-central United States, shifted its feeding preferences from birds to humans by 7-fold during late summer and early fall, coinciding with the dispersal of its preferred host (American robins, Turdus migratorius) and the rise in human WNV infections. We also show that feeding shifts in Cx. tarsalis amplify human WNV epidemics in Colorado and California and occur during periods of robin dispersal and migration. Our results provide a direct explanation for the timing and intensity of human WNV epidemics. Shifts in feeding from competent avian hosts early in an epidemic to incompetent humans after mosquito infection prevalences are high result in synergistic effects that greatly amplify the number of human infections of this and other pathogens. Our results underscore the dramatic effects of vector behavior in driving the transmission of zoonotic pathogens to humans.

Background matching behaviour and pathogen acquisition: plant site preference does not predict the bacterial acquisition efficiency of vectors

“…Vector host choice (Blua and Perring 1992;McElhany et al 1995;Alvarez et al 2007) and within-host feedingsite preference (Tsai et al 2002;Marucci et al 2004) can influence patterns of vector-borne pathogen distribution and disease dynamics (McElhany et al 1995;Kilpatrick et al 2006;Sisterson 2008). Moreover, variations in feeding behaviour among species may also contribute to the existing differential transmission efficiency of vectors (Turell et al 2001;Daugherty and Almeida 2009) through governing the degree to which they are exposed to a pathogen.…”

“…Moreover, variations in feeding behaviour among species may also contribute to the existing differential transmission efficiency of vectors (Turell et al 2001;Daugherty and Almeida 2009) through governing the degree to which they are exposed to a pathogen. Differential exposure may result from the heterogeneous distribution of pathogens, either temporally or spatially, among and/or within host species (Dekker et al 1998;Saracco et al 2005;Shriram et al 2005;Kilpatrick et al 2006;Tatineni et al 2008). Furthermore, while feeding behaviour may affect vector exposure to pathogens, it also affects an individual's exposure to would-be predators present in the surrounding environment.…”

Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant

“…quinquefasciatus in Africa (16). Also, feeding shifts from birds to humans in Culex are well documented in the literature (17).…”

“…We also provide a list of potent semiochemicals that are detected with high sensitivity by other ORNs. Also, we discuss how nonanal could be involved in the unique shifts in Culex feeding between birds and humans (17).…”

Usutuvirus

“…Die überwie-gende Mehrzahl der afrikanischen Isolate stammte von verschiedenen Mückenspe-zies, unter anderem aus Culex neavi, Culex perfuscus, Mansonia africana, Mansonia aurites und Aedes (Aedimorphus) minutus ( [6], Übersichtsartikel [7]). Man geht davon aus, dass die Verbreitung von USUV im Zyklus zwischen ornithophilen Mücken und Vögeln -vergleichbar zur Epidemiologie von West-Nil-Virus (WNV) -erfolgt [8,9]. Im Jahr 1981 wurde erstmals USUV von einem Patienten mit Fieber und Hautausschlag in RCA isoliert [5].…”