Overwintering Biology of <I>Culex</I> (Diptera: Culicidae) Mosquitoes in the Sacramento Valley of California

Abstract

At temperate latitudes, Culex (Diptera: Culicidae) mosquitoes typically overwinter as adult females in reproductive arrest and also may serve as reservoir hosts for arboviruses when cold temperatures arrest viral replication. To evaluate their role in the persistence of West Nile virus (WNV) in the Sacramento Valley of California, the induction and termination of diapause were investigated for members of the Culex pipiens (L.) complex, Culex tarsalis Coquillett, and Culex stigmatosoma Dyar under field, seminatural, and experimental conditions. All Culex spp. remained vagile throughout winter, enabling the collection of 3,174 females and 1,706 males from diverse habitats during the winters of 2010–2012. Overwintering strategies included both quiescence and diapause. In addition, Cx. pipiens form molestus Forskäl females remained reproductively active in both underground and aboveground habitats. Some blood-fed, gravid, and parous Cx. tarsalis and Cx. pipiens complex females were collected throughout the winter period. Under both field and experimental conditions, Cx. tarsalis and Cx. stigmatosoma females exposed to autumnal conditions arrested primary follicular maturation at previtellogenic stage I, with primary to secondary follicular ratios <1.5 (indicative of a hormonally induced diapause). In contrast, most Cx. pipiens complex females did not enter reproductive diapause and ovarian follicles matured to ≥stage I–II (host-seeking arrest) or were found in various stages of degeneration. Diapause was initiated in the majority of Cx. tarsalis and Cx. stigmatosoma females by mid-late October and was terminated after the winter solstice, but host-seeking seemed limited by temperature. An accrual of 97.52 ± 30.7 and 162.85 ± 79.3 degree-days after the winter solstice was estimated to be necessary for diapause termination in Cx. tarsalis under field and seminatural conditions, respectively. An increase in the proportion of blood-fed Culex females in resting collections occurred concurrently with diapause termination in field populations based on ovarian morphometrics. WNV RNA was detected in one pool of 18 males and in a single blood-fed female Cx. tarsalis collected during winter. Therefore, both vertically and horizontally infected Culex females may persist through winter and possibly transmit WNV after diapause termination in late winter or early spring in the Sacramento Valley of California.

West Nile Virus Activity in a Winter Roost of American Crows (Corvus brachyrhynchos): Is Bird-To-Bird Transmission Important in Persistence and Amplification?

“…Winter infections were unlikely to have arisen by recent bites from infected mosquitoes, because Culex mosquito activity was very low in winter and all mosquitoes collected during winter months tested negative for WNV. Similar mosquito results were reported recently for other sites within the Davis and Sacramento areas (Nelms et al 2013b). In contrast, consistent opportunities existed for fecal-oral transfer at the overwintering roost.…”

“…In temperate climates, winter temperatures are generally low, which, in conjunction with declining photoperiod, typically leads to Culex diapause or quiescence (Nelms et al 2013b). We captured some Culex host-seeking during the winter, and therefore it is possible that mosquitoes may have contributed to WNV transmission to crows at the winter roost.…”

“…In support, WNV was recovered from a single blood-fed Cx. tarsalis collected during January (Nelms et al 2013b). Active mosquitoes should theoretically be able to find bloodmeals among the mass of crows that congregate at nocturnal winter roosts, and, if infected, mosquito--crow transmission could occur.…”

Phenotypic Variation among Culex pipiens Complex (Diptera: Culicidae) Populations from the Sacramento Valley, California: Horizontal and Vertical Transmission of West Nile Virus, Diapause Potential, Autogeny, and Host Selection

“…43 Autogenous populations of Cx. pipiens recently were detected in catch basins and manholes in the Sacramento Valley of California, 44 Marin County, 45 and Santa Clara County, 42 supporting the unpublished studies of Iltis (Iltis WG, unpublished dissertation) who reported widespread autogeny among pipiens populations throughout much of central California.…”

Rift Valley fever virus: strategies for maintenance, survival and vertical transmission in mosquitoes

“…Thus, for these mosquitoes to become infected with WNV they require infection by VT, not oral infection, prior to overwintering. VT of WNV by Culex mosquitoes and subsequent detection in overwintering populations has been recorded [111,128]. Therefore, when considering RVFV in temperate regions outside Africa, it may be necessary to consider a similar overwintering model.…”