Potential for urban warming to postpone overwintering dormancy of temperate mosquitoes.

Cities are generally hotter than surrounding rural areas due to the Urban Heat Island (UHI) effect. These increases in temperature advance plant and animal phenology, development, and reproduction in the spring. However, research determining how increased temperatures affect the seasonal physiology of animals in the fall has been limited. The Northern house mosquito, Culex pipiens, is abundant in cities and transmits several pathogens including West Nile virus. Females of this species enter a state of developmental arrest, or reproductive diapause, in response to short days and low temperatures during autumn. Diapausing females halt reproduction and blood-feeding, and instead accumulate fat and seek sheltered overwintering sites. We found that exposure to increased temperatures in the lab that mimic the UHI effect induced ovarian development and blood-feeding, and that females exposed to these temperatures were as fecund as non-diapausing mosquitoes. We also found that females exposed to higher temperatures had lower survival rates in winter-like conditions, despite having accumulated equivalent lipid reserves relative to their diapausing congeners. These data suggest that urban warming may inhibit diapause initiation in the autumn, thereby extending the active biting season of temperate mosquitoes.

Light pollution disrupts circadian clock gene expression in two mosquito vectors during their overwintering dormancy.

Artificial light at night (ALAN) is an increasingly important form of environmental disturbance as it alters Light:Dark cycles that regulate daily and seasonal changes in physiology and phenology. The Northern house mosquito (Culex pipiens) and the tiger mosquito (Aedes albopictus) enter an overwintering dormancy known as diapause that is cued by short days. These two species differ in diapause strategy: Cx. pipiens diapause as adult females while Ae. albopictus enter a maternally-programmed, egg diapause. Previous studies found that ALAN inhibits diapause in both species, but the mechanism is unknown. As the circadian clock is implicated in the regulation of diapause in many insects, we examined whether exposure to ALAN altered the daily expression of core circadian cloc genes (cycle, Clock, period, timeless, cryptochrome 1, cryptochrome 2, and Par domain protein 1) in these two species when reared under short-day, diapause-inducing conditions. We found that exposure to ALAN altered the abundance of several clock genes in adult females of both species, but that clock gene rhythmicity was maintained for most genes. ALAN also had little effect on clock gene abundance in mature oocytes that were dissected from female Ae. albopictus that were reared under short day conditions. Our findings indicate that ALAN may inhibit diapause initiation through the circadian clock in two medically-important mosquitoes.

Trade-offs between winter survival and reproduction in female insects.

In temperate environments most species of insects enter an arrested state of development, known as diapause, that enables them to survive the adverse environmental conditions associated with winter. Although diapause is restricted to a single life stage within species of insects, there are examples of insects that overwinter in the egg, larval, pupal and adult stages. Here we offer a targeted, non-systematic literature review examining how overwintering impacts subsequent reproduction in female insects. Several factors, including the lifestage at which insects overwinter, the type of energy investment strategy females use for breeding, elements of the winter environment, and contributions from male insects can influence trade-offs that female insects face between overwintering survival and post-diapause reproduction. Additionally, climate change and elements of the urban environment, including light pollution and higher temperatures in cities, can exacerbate or ameliorate trade-offs faced by reproducing female insects. Better understanding trade-offs between overwintering survival and reproduction in insects not only enhances our understanding of the underlying physiological mechanisms and ecological processes governing diapause and reproduction, but also provide opportunities to better manage insect pests and/or support beneficial insects.

Light Pollution Disrupts Seasonal Differences in the Daily Activity and Metabolic Profiles of the Northern House Mosquito, Culex pipiens.

The Northern House mosquito, Culex pipiens, is an important disease vector, and females are capable of surviving the winter in a state of overwintering diapause. This species' diapause response has been extensively studied, and recent evidence suggests that the circadian clock is involved in measuring seasonal changes in daylength to initiate the diapause response. However, differences in the circadian activity of diapausing and non-diapausing Cx. pipiens have not been thoroughly investigated. Additionally, recent findings indicate that artificial light at night (ALAN) can disrupt mosquito diapause, potentially prolonging the mosquito biting season. We compared the circadian locomotor activity of mosquitoes reared in diapause-averting, long-day conditions and diapause-inducing, short-day conditions with and without ALAN to elucidate the interplay between circadian activity, diapause, and light pollution. We also uncovered metabolic differences between mosquitoes reared under diapausing and non-diapausing photoperiods with and without ALAN by measuring the concentration of protein, fructose, glycogen, water-soluble carbohydrates, and lipids. We found that ALAN exposure altered several diapause-associated phenotypes including slightly, but not significantly, increasing activity levels in short day-reared mosquitoes; and preventing some short day-reared mosquitoes from accumulating lipids. ALAN also significantly reduced glycogen and water-soluble carbohydrate levels in long day-reared mosquitoes. Based on our findings, light pollution may decrease insect fitness by perturbing metabolism, and may also impact several phenotypes associated with insect diapause, potentially extending the mosquito biting season and preventing insects in urban environments from overwintering successfully.

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

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.

Artificial light at night alters the seasonal responses of biting mosquitoes.

Urban light pollution caused by artificial light at night (ALAN) profoundly affects the ecology, behavior, and physiology of plants and animals. Further, this widespread environmental pollutant has the potential to negatively impact human and animal health by changing the seasonal dynamics of disease-transmitting insects. In response to short days, females of the Northern house mosquito enter an overwintering dormancy, or diapause. While in diapause, female mosquitoes divert energy away from reproduction, cease blood-feeding, and no longer transmit disease. We demonstrate that exposure to dim ALAN (~4 lx) causes female mosquitoes to avert diapause and become reproductively active, as these females acquired less fat content, developed larger egg follicles, imbibed vertebrate blood, and produced viable eggs and larvae. Our findings suggest that mosquitoes in highly light-polluted areas such as cities may be actively reproducing and biting later in the season, thereby extending the period of disease risk for urban residents. Our results suggest that ALAN should be considered when modeling mosquito abundance, disease risk, and when deciding how long mosquito surveillance and control should persist in temperate regions.