West Nile Virus Epidemics in North America Are Driven by Shifts in Mosquito Feeding Behavior
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Taken together, these data suggest that mosquito feeding shifts appear to be a continent-wide phenomenon that amplifies the transmission of WNV from birds to humans and other mammals. Feeding shifts have two synergistic effects on the intensity of WNV transmission to humans.
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First, we have shown that the increase over time in the probability of Cx. Second, feeding primarily on WNV-competent avian hosts during the amplification period of the epidemiological cycle maximizes the intensity of the epidemic in mosquitoes. If mosquitoes fed on humans in early summer with the same probability as that seen in late summer approximately 0. In contrast, holding the probability of mosquitoes feeding on humans at its lowest level, 0. This is because mosquito WNV prevalences are already beginning to decline possibly as a result of increased acquired immunity in juvenile birds when mammals begin to make up an important fraction of the blood meals.
Thus, the shift in feeding from competent hosts early in the season to humans later leads first to greater amplification of the virus as transmission intensifies between birds and mosquitoes and subsequently to an even greater number of human WNV infections. First, although it is possible that the feeding shift we observed in Cx. In any case, increasing hybridization would offer an explanation only in areas where Cx. In addition, a temporally invariant increase in feeding on humans by hybrid Cx. Third, the introduced strain of WNV appears to be more virulent compared to an Old World strain in American crows Corvus brachyrhynchos [ 13 ], but not in more important amplification hosts such as house sparrows Passer domesticus [ 34 , 35 ].
Finally, high vector competence of Cx. In sum, although many factors influence WNV transmission to humans, our results suggest that feeding shifts occur across North America and offer a direct explanation for the greater number of human WNV infections compared to the Old World. More broadly, our findings show that shifts in mosquito feeding behavior are a geographically widespread phenomenon that intensifies epidemics of several avian zoonotic viruses including WNV, Western equine encephalitis virus, and St.
Louis encephalitis virus [ 16 ] , and may affect other zoonotic vector-borne pathogens. Studies aimed at determining the factors that influence pathogen transmission to humans are critical to reducing the impact of these and other devastating diseases. We collected field data at six sites in Maryland and Washington, D. The sites included three urban areas, the National Mall in Washington, D. Each site was approximately 1 km in diameter, with a relatively homogeneous percent forest cover and land use in the site and surrounding area. The sites span a distance of greater than 40 miles and are separated by 3 to 25 miles.
We estimated the abundance of host-seeking Culex mosquitoes at each site using eight CDC light traps, baited with dry ice CO 2. We ran these traps for two nights every 2 wk from May to September at each site and averaged abundance across the sites. To determine the species composition of Culex mosquitoes at our sites, which are difficult to identify morphologically [ 37 ], we used PCR on the internal spacer gene [ 38 ] to identify all engorged Culex mosquitoes to species and an additional subset of 40 Culex mosquitoes at each site.
We collected engorged mosquitoes from each site using CDC light and gravid traps and by collecting mosquitoes resting on vegetation with a large backpack-mounted aspirator.
Blood meals were identified as avian, mammalian, or other following extraction of DNA from the engorged mosquitoes and PCR amplification of the cytochrome b gene as described and verified [ 39 ]. Only engorged mosquitoes identified as Cx. We modeled the risk of the transmission of WNV to humans by Cx. We calculated the variance of predicted risk using a Taylor series expansion approximation:. We compared predicted WNV risk to the number of human cases in Maryland [ 42 , 43 ].
We corrected the date of reporting by obtaining the date of the onset of illness for each case unpublished data, A. We estimated the abundance of birds using four- to six-point transects, six minutes in duration, performed at each site monthly from May through September and analyzed the data using Program Distance [ 44 ], which accounts for species' differences in detectability. We estimated the decline of American robin abundance Figure 1 B over time using a regression of the relative abundance of robins at each site on the Julian date.
The changes in robin and total bird abundance were similar across the six sites. To examine the temporal overlap between feeding shifts and human WNV epidemics in other parts of North America, we obtained data on temporal variation in feeding on birds and mammals for Cx. We compared these patterns with data on the date of onset of illness and number of human cases of WNV in Colorado [ 45 ] and California [ 27 ] in Finally, we compared these to periods of postbreeding dispersal and migration for robins in California [ 23 , 46 ] and in four different habitats in Arizona [ 47 — 49 ].
We thank the field crew especially H. Brightman and R. Brashares and J. McEntee for help obtaining ancient obscure literature; and A. Bergmann for assistance with the Maryland human WNV data. We also thank the Wadsworth Center Molecular Genetics Core for nucleotide sequencing and production of primers.
Abstract West Nile virus WNV has caused repeated large-scale human epidemics in North America since it was first detected in and is now the dominant vector-borne disease in this continent. Introduction Approximately three quarters of human emerging infectious diseases are caused by zoonotic pathogens [ 1 ]. Download: PPT.
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Figure 1. Figure 2. Discussion Our data from the mid-Atlantic demonstrate a late-summer shift in the feeding behavior of Cx. Acknowledgments We thank the field crew especially H.
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West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior
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Female mosquitoes have a long appendage on their head called a proboscis that allows them to bite other animals and suck their blood. Generally, WNV is transferred between mosquitoes and birds. However, scientists noticed that between late summer and early fall the transfer of WNV from mosquitoes to humans became more common than between mosquitoes and birds. The American robin is the primary food source of the mosquito during early summer.
West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior.
Image by Dakota Lynch. They thought that perhaps this change was due to mosquitoes shifting their feeding behavior from birds to mammals, which included humans. If mosquitoes fed mainly on birds in the summer and then switched to humans in the fall, it could explain the increase in transmission of WNV to humans during that time of the year. Mosquitoes are attracted to light. They would fly into the traps to get closer to the light source at which point they would be unable to escape. From each trap, the scientists collected only the mosquitoes that had abdomens full of blood.
This meant that the mosquitoes had recently eaten, and thus could be tested. The blood in their abdomens was tested and identified as coming from a bird, a mammal, or another animal "other".