Characterizing seasonal changes in the reproductive activity of Culex mosquitoes throughout the fall, winter, and spring in Ohio

Abstract

Background: Culex mosquitoes are the primary vectors of West Nile virus (WNV) across the USA. Understanding when these vectors are active indicates times when WNV transmission can occur. This study determined the proportion of female Culex mosquitoes that were in diapause during the fall and winter and when they terminated diapause and began blood feeding in the spring.

Methods: Mosquitoes were collected from parks using various traps and/or aspirated from culverts in Franklin County, Ohio, from October to mid-May from 2019 to 2022. Culex mosquitoes were morphologically identified to species, and the ovaries of females were dissected to determine their diapause and parity statuses.

Results: By early October 2021, roughly 95% of Culex pipiens collected in culverts were in diapause and 98% of Cx. erraticus were in diapause. Furthermore, gravid and blood-fed Culex salinarius, Cx. pipiens, and Cx. restuans were collected in late November in 2019 and 2021 in standard mosquito traps. In the winter of 2021, the proportions of non-diapausing Culex decreased within culverts. The last non-diapausing Cx. erraticus was collected in late December 2021 while the final non-diapausing Cx. pipiens was collected in mid-January 2022, both in culverts. Roughly 50% of Cx. pipiens terminated diapause by mid-March 2022, further supported by our collections of gravid females in late March in all 3 years of mosquito collection. In fact, male mosquitoes of Cx. pipiens, Cx. restuans, and Cx. territans were collected by the 1st week of May in 2022, indicating that multiple species of Culex produced a second generation that reached adulthood by this time.

Conclusions: We collected blood-fed and gravid Culex females into late November in 2 of the 3 years of our collections, indicating that it might be possible for WNV transmission to occur in late fall in temperate climates like Ohio. The persistence of non-diapausing Cx. pipiens and Cx. erraticus throughout December has important implications for the winter survival of WNV vectors and our overall understanding of diapause. Finally, determining when Culex terminate diapause in the spring may allow us to optimize mosquito management programs and reduce the spread of WNV before it is transmitted to humans.

Keywords: Culex erraticus; Culex pipiens; Culex restuans; Culvert; Diapause; Overwintering; Seasonality; West Nile virus.

Fig. 1

Distribution and examples of collection sites. A All 2021–2022 collection sites designed using ArcGIS pro [66]. Mosquito traps were placed in lightly wooded parks which are referred to as park sites (n = 5). Mosquitoes were aspirated from culvert sites (n = 5). Additionally, mosquitoes were collected from locations that contained both a park and culvert site (n = 4). B Example of a lightly wooded park site. C Example of a culvert site

Fig. 2

Counts of Cx. pipiens (A), Cx. restuans (B), and Cx. erraticus (C) collected across time and relative abundance of Cx. pipiens (D), Cx. restuans (E), and Cx. erraticus (F) at various collection sites in Franklin County, Ohio, during the 2021 to 2022 collection season. For panels D–F the size of the point at each site is proportional to the number of mosquitoes collected at that site

Fig. 3

Counts of all Culex collected from traditional mosquito traps placed at park sites (blue) and counts of mosquitoes aspirated from culvert sites (red) during the 2021–2022 collection season. Mosquitoes were initially collected from park sites using gravid trap and BG Sentinel traps from October–February; starting in March, CDC light traps were also used weekly. Mosquitoes were collected from culverts using aspirators throughout the collection season

Fig. 4

The proportions of diapausing Cx. pipiens (A) and Cx. erraticus (B) collected from culverts in fall 2021 through spring 2022. The size of each point is proportional to the number of culverts where Culex were collected. Gray shading highlights dates between March 1, 2022, and April 21, 2022, when there was a rapid decrease in the proportion of mosquitoes in diapause. Although all nine culverts were sampled during each collection event, Cx. pipiens and/or Cx. erraticus were not necessarily collected from every culvert on every collection date