Host choice and West Nile virus infection rates in blood-fed mosquitoes, including members of the Culex pipiens complex, from Memphis and Shelby County, Tennessee, 2002-2003

Abstract

The source of bloodmeals in 2,082 blood-fed mosquitoes collected from February 2002 through December 2003 in Memphis and surrounding areas of Shelby County, Tennessee were determined. Members of the genus Culex and Anopheles quadrimaculatus predominated in the collections. Members of the Cx. pipiens complex and Cx. restuans were found to feed predominately upon avian hosts, though mammalian hosts made up a substantial proportion of the bloodmeals in these species. No significant difference was seen in the host class of bloodmeals in mosquitoes identified as Cx. pipiens pipiens, Cx. p. quinquefasciatus, or hybrids between these two taxa. Anopheles quadrimaculatus and Cx. erraticus fed primarily upon mammalian hosts. Three avian species (the American Robin, the Common Grackle, and the Northern Cardinal) made up the majority of avian-derived bloodmeals, with the American Robin representing the most frequently fed upon avian host. An analysis of these host feeding data using a modification of a transmission model for Eastern Equine encephalitis virus suggested that the American Robin and Common Grackle represented the most important reservoir hosts for West Nile virus. A temporal analysis of the feeding patterns of the dominant Culex species did not support a shift in feeding behavior away from robins to mammals late in the summer. However, a significant degree of temporal variation was noted in the proportion of robin-derived bloodmeals when the data were analyzed by semi-monthly periods throughout the summers of 2002 and 2003. This pattern was consistent with the hypothesis that the mosquitoes were preferentially feeding upon nesting birds.

FIG. 1

Location of the 70 mosquito resting sites in Shelby County, Tennessee, that yielded mosquito specimens with blood-meal hosts identifiable to host class.

FIG. 2

Number of blood-fed mosquitoes collected, for species and members of the Culex pipiens complex represented by more than 50 specimens, by monthly intervals from Shelby County, Tennessee, 2002–2003. (A) Species other than members of the Cx. pipiens complex. (B) Taxa in the Cx. pipiens complex.

FIG. 3

Schematic of model used to compare reservoir capacities of different avian species. Large boxes highlight the avian and mosquito modules that make up the model. Variables that affect the interaction of the three modules are listed in small boxes interrupting the arrows that connect the modules. The arrows connecting the modules indicate the direction of the interactions among the modules. Within each module, the white boxes indicate stocks of the avian reservoir and vector mosquito species in different states (e.g., uninfected or infectious). Gray boxes indicate conveyors, in which animals moving from one stock to another must rest for a defined period of time before moving to the next stock. The bold Xs indicate death of animals in a given stock, resulting in removal from subsequent iterations of the model. Arrows indicate the direction that animals may move from stock to stock. Arrows interrupted by a circle indicate that movement from one stock to another stock is governed by a single variable. This variable is indicated by the curved arrow pointed to the circle in question. Arrows interrupted by hexagons symbolize that movement between the stocks indicated is controlled by multiple variables, most of which affect the interactions between the modules. Variables affecting the transitions in each hexagon are as follows. Hexagon A: Number of uninfected birds of species 1 (susceptible and immune), number of uninfected birds of species 2 (susceptible and immune), and relative feeding upon species 1 and species 2, calculated from the relative feeding indices of the two species. Hexagon B: Number of infectious birds of species 1, number of infectious birds of species 2 and relative feeding upon species 1 and species 2. Hexagon C: Total number of birds of species 1, total number of birds of species 2, and relative feeding upon species 1 and species 2. Hexagon D: Number of infectious mosquitoes, number of susceptible birds, and relative feeding preference on species 1 and species 2.

FIG. 4

Temporal distribution of bloodmeals taken by Cx. pipiens complex and Cx. restuans mosquitoes for host groups (robin, other avian, mammal, and amphibian/reptilian combined) at semi-monthly intervals, Shelby County, Tennessee, 2002–2003. Time intervals during which no collections were made are indicated by “NC.”

FIG. 5

Non-parametric analysis of the numbers of robin and non-robin avian bloodmeals by semi-monthly period. (A) Predicted and observed numbers of robin blood meals. (B) Predicted and observed numbers of avian blood-meals derived from species other than robin. (C) Predicted numbers of blood-meals from robins and other avian species. In A and B, asterisks (*) indicate time periods where the observed numbers of meals differed significantly from those predicted by the models (p < 0.05; χ² test).

FIG. 6

Percent of American Robin derived bloodmeals taken during semi-monthly periods during the 2002 transmission season, May 1, 2002 to September 15, 2002, at four collection sites. Only sites where greater than 10 robin-derived bloodmeals and at least 25 total bloodmeals were identified, and where blood-fed mosquitoes were found during at least six of the 11 possible semi-monthly periods are included.