Hugh D. Lothrop

West Nile Virus in California

The spread of WNV in California is tracked.

Overwintering of West Nile Virus in Southern California

Abstract West Nile virus (family Flaviviridae, genus Flavivirus, WNV) invaded southern California during 2003, successfully overwintered, amplified to epidemic levels, and then dispersed to every county in the state. Although surveillance programs successfully tracked and measured these events, mechanisms that allowed the efficient overwintering and subsequent amplification of WNV have not been elucidated. Our current research provided evidence for three mechanisms whereby WNV may have persisted in southern California during the winters of 2003–2004 and 2004–2005: 1) continued enzootic transmission, 2) vertical transmission by Culex mosquitoes, and 3) chronic infection in birds. WNV was detected in 140 dead birds comprising 32 species, including 60 dead American crows, thereby verifying transmission during the November–March winter period. Dead American crows provide evidence of recent transmission because this species always succumbs rapidly after infection. However, WNV RNA was not detected concurrently in 43,043 reproductively active female mosquitoes comprising 11 species and tested in 1,258 pools or antibody in sera from 190 sentinel chickens maintained in 19 flocks. Although efficient vertical transmission by WNV was demonstrated experimentally for Culex tarsalis Coquillett infected per os, 369 females collected diapausing in Kern County and tested in 32 pools were negative for WNV. Vertical transmission was detected in Culex pipiens quinquefasciatus Say adults reared from field-collected immatures collected from Kern County and Los Angeles during the summer transmission period. Chronic infection was detected by finding WNV RNA in 34 of 82 birds that were inoculated with WNV experimentally, held for >6 wk after infection, and then necropsied. Frequent detection of WNV RNA in kidney tissue in experimentally infected birds >6 wk postinfection may explain, in part, the repeated detection of WNV RNA in dead birds recovered during winter, especially in species such as mourning doves that typically do not die after experimental infection. In summary, our study provides limited evidence to support multiple modes of WNV persistence in southern California. Continued transmission and vertical transmission by Culex p. quinquefasciatus Say seem likely candidates for further study.

Role of Corvids in Epidemiology of West Nile Virus in Southern California

Abstract The invasion of different southern California landscapes by West Nile virus (WNV) and its subsequent amplification to epidemic levels during 2004 enabled us to study the impact of differing corvid populations in three biomes: the hot Colorado desert with few corvids (Coachella Valley), the southern San Joaquin Valley (Kern County) with large western scrub-jay but small American crow populations, and the cool maritime coast (Los Angeles) with a large clustered American crow population. Similar surveillance programs in all three areas monitored infection rates in mosquitoes, seroconversion rates in sentinel chickens, seroprevalence in wild birds, numbers of dead birds reported by the public, and the occurrence of human cases. Infection rates in Culex tarsalis Coquillett and sentinel chicken seroconversion rates were statistically similar among all three areas, indicating that highly competent mosquito hosts were capable of maintaining enzootic WNV transmission among less competent and widely distributed avian hosts, most likely house sparrows and house finches. In contrast, infection rates in Culex pipiens quinquefasciatus Say were statistically higher in Kern and Los Angeles counties with elevated corvid populations than in Coachella Valley with few corvids. Spatial analyses of dead corvids showed significant clusters near known American crow roosts in Los Angeles that were congruent with clusters of human cases. In this area, the incidence of human and Cx. p. quinquefasciatus infection was significantly greater within corvid clusters than without, indicating their importance in virus amplification and as a risk factor for human infection. In contrast the uniform dispersion by territorial western scrub-jays resulted in a high, but evenly distributed, incidence of human disease in Kern County.

Patterns of Avian Seroprevalence to Western Equine Encephalomyelitis and Saint Louis Encephalitis Viruses in California, USA

Abstract Temporal and spatial changes in the enzootic activity of western equine encephalomyelitis (WEE) and St. Louis encephalitis (SLE) viruses were monitored at representative wetland study sites in the Coachella, San Joaquin, and Sacramento valleys of California from 1996 to 1998 using three methods: (1) virus isolation from pools of 50 host-seekingCulex tarsalisCoquillett females, (2) seroconversions in flocks of 10 sentinel chickens, and (3) seroprevalence in wild birds collected by mist nets and grain baited traps. Overall, 74 WEE and one SLE isolates were obtained from 222,455Cx. tarsalisfemales tested in 4,988 pools. In addition, 133 and 40 seroconversions were detected in 28 chicken flocks, and 143 and 27 of 20,192 sera tested from 149 species of wild birds were positive for antibodies to WEE and SLE, respectively. WEE was active in all three valleys, whereas SLE only was detected in Coachella Valley. Seroconversions in sentinel chickens provided the most sensitive indication of enzootic activity and were correlated with seroprevalence rates in wild birds. Avian seroprevalence rates did not provide an early warning of pending enzootic activity in chickens, because positive sera from after hatching year birds collected during spring most probably were the result of infections acquired during the previous season. Few seroconversions were detected among banded recaptured birds collected during spring and early summer. Age and resident status, but not sex, were significant risk factors for wild bird infection, with the highest seroprevalence rates among after hatching year individuals of permanent resident species. Migrants (with the exception of mourning doves) and winter resident species rarely were positive. House finches, house sparrows, Gambel’s quail, California quail, common ground doves, and mourning doves were most frequently positive for antibodies. The initial detection of enzootic activity each summer coincided closely with the appearance of hatching year birds of these species in our study areas, perhaps indicating their role in virus amplification. Bird species most frequently positive roosted or nested in elevated upland vegetation, sites whereCx. tarsalishost-seeking females hunt most frequently. These serosurveys provided important background information for planned host competence and chronic infection studies.

Landscape Affects the Host-Seeking Patterns of Culex tarsalis (Diptera: Culicidae) in the Coachella Valley of California

Abstract Effective arbovirus transmission requires that the principal vertebrate hosts and vectors have frequent contact. Vegetation and other landscape features used by roosting or nesting birds at night dictate their exposure to nocturnally active host-seeking Culex tarsalis Coquillett and therefore to western equine encephalomyelitis and St. Louis encephalitis viruses. Precipitin tests on 645 Cx. tarsalis that were collected resting and host-seeking near the Salton Sea in Coachella Valley, CA, indicated that passeriform birds (64%) and rabbits (25%) were the most frequent bloodmeal hosts and that the percentage of females feeding on birds varied temporally as an inverse function of mosquito abundance. Blood meals were not taken from communally roosting water birds. The spatial distribution of host-seeking females then was investigated by deploying dry ice baited traps within seven sites representative of habitats found along the Salton Sea. Mosquito catch was greatest at traps within elevated vegetation such as Tamarisk, mesquite, cattails, and orchards and lowest at traps positioned at snags over water, sand bars, open fields, and within housing in a small rural community. These data indicate that host-seeking Cx. tarsalis females congregated at specific landscape features that were not necessarily associated with large concentrations of potential bloodmeal hosts.

Effects of warm winter temperature on the abundance and gonotrophic activity of Culex (Diptera: Culicidae) in California.

ABSTRACT Culex tarsalis Coquillett, Cx. quinquefasciatus Say, and Cx. pipiens L. were collected during the warm winter of 2009 using dry ice-baited and gravid traps and walk-in red boxes positioned in desert, urban, and agricultural habitats in Riverside, Los Angeles, Kern, and Yolo Counties. Temperatures exceeded the preceding 50 yr averages in all locations for most of January, whereas rainfall was absent or below average. Abundance of Culex species in traps during January ranged from 83 to 671% of the prior 5 yr average in all locations. Few females collected resting were in diapause during January based on follicular measurements. Evidence for early season gonotrophic activity included the detection of freshly bloodied, gravid, and parous females in resting collections, gravid oviposition site-seeking females in gravid female traps, and nulliparous and parous host-seeking females at dry ice-baited traps. Female Culex seemed to employ multiple overwintering strategies in California, including larval and adult quiescence, adult female diapause, and an intermediate situation with adult females collected with enlarged follicles, but without evident vitellogenesis. West Nile, St. Louis, or western equine encephalitis viruses were not detected in 198 pools of adults or 56 pools of adults reared from field-collected immatures collected during January and February 2009. Our preliminary data may provide insight into how climate change may extend the mosquito season in California.

Spatial Variation in Host Feeding Patterns of Culex tarsalis and the Culex pipiens Complex (Diptera: Culicidae) in California

ABSTRACT West Nile virus (family Flaviviridae, genus Flavivirus, WNV) is now endemic in California across a variety of ecological regions that support a wide diversity of potential avian and mammalian host species. Because different avian hosts have varying competence for WNV, determining the blood-feeding patterns of Culex (Diptera: Culicidae) vectors is a key component in understanding the maintenance and amplification of the virus as well as tangential transmission to humans and horses. We investigated the blood-feeding patterns of Culex tarsalis Coquillett and members of the Culex pipiens L. complex from southern to northern California. Nearly 100 different host species were identified from 1,487 bloodmeals, by using the mitochondrial gene cytochrome c oxidase I (COI). Cx. tarsalis fed on a higher diversity of hosts and more frequently on nonhuman mammals than did the Cx. pipiens complex. Several WNV-competent host species, including house finch and house sparrow, were common bloodmeal sources for both vector species across several biomes and could account for WNV maintenance and amplification in these areas. Highly competent American crow, western scrub-jay and yellow-billed magpie also were fed upon often when available and are likely important as amplifying hosts for WNV in some areas. Neither species fed frequently on humans (Cx. pipiens complex [0.4%], Cx. tarsalis [0.2%]), but with high abundance, both species could serve as both enzootic and bridge vectors for WNV.

Persistence and Amplification of St. Louis Encephalitis Virus in the Coachella Valley of California, 2000-2001

Abstract The introduction of a St. Louis encephalitis virus (SLE) genotype new to southeastern California during 2000 was followed by focal enzootic amplification in the Coachella Valley that was detected by seroconversions of 29 sentinel chickens in five of nine flocks of 10 chickens each, isolations of virus from 30 of 538 pools of 50 Culex tarsalis Coquillett females, and collection of 30 positive sera from 2,205 wild birds. This SLE strain over wintered successfully and then amplified during the summer of 2001, with 47 sentinel seroconversions in eight of nine flocks, 70 virus isolations from 719 pools of Cx. tarsalis and Cx. p. quinquefasciatus Say, and 40 positive sera from 847 wild birds. Human illness was not detected by passive case surveillance, despite issuance of a health alert during 2001. Virus amplification during both years was associated with above average temperatures conducive for extrinsic incubation and below average precipitation during spring associated with below average vector abundance. Seroconversions by sentinel chickens provided the timely detection of virus activity, with initial conversions detected before positive mosquito pools or wild bird infections. Vertical infection was not detected among Cx. tarsalis adults reared from immatures collected during the fall-winter of 2000, even though SLE over wintered successfully in this area. Early seroconversions by a sentinel chicken during February 2001 and a recaptured Gambel’s quail in April 2001provided evidence for transmission during winter and spring when ambient temperatures averaged below 17°C, the threshold for SLE replication.

Factors Influencing the Outcome of Mark-Release-Recapture Studies with Culex tarsalis (Diptera: Culicidae)

Abstract Three potentially important aspects of mark-release-recapture experimentation were addressed: 1) source of mosquitoes for release, 2) time of release, and 3) weather during recapture. Culex tarsalis Coquillett mosquitoes collected as adult host-seeking females from dry ice-baited traps (CO2 traps) operated within the study area (local) were recaptured more frequently than females collected from traps operated outside the study area (foreign) or reared from field-collected immatures (reared). These results supported published studies on Anopheles and Ochlerotatus that indicated mosquitoes may “memorize” flight paths within their environment. Releasing gravid females provided a potentially useful replacement for reared females, because these gravids oviposited at wetlands and then dispersed to upland traps. Releasing local, foreign, or reared mosquitoes just after sunrise or just before sunset did not alter recapture success or the distance dispersed. Elevated wind speeds inhibited dispersal from protected microhabitats with citrus orchards and resulted in most recaptures being found at the leeward portion of the orchard.

Intensive Early Season Adulticide Applications Decrease Arbovirus Transmission Throughout the Coachella Valley, Riverside County, California

In the Coachella Valley of California the seasonal onset of St. Louis encephalitis virus (SLEV), western equine encephalomyelitis virus (WEEV), and West Nile virus (WNV) has been detected consistently at the shoreline of the Salton Sea near the community of North Shore. The timing and intensity of initial amplification in the Culex tarsalis Coquillett/wild bird cycle at this focus seemed closely linked to the subsequent dispersal of virus to the rest of the Coachella Valley and perhaps southern California. In 2004, an attempt was made to interrupt the amplification and dispersal of WNV using ground ultra-low volume (ULV) applications of Pyrenone 25-5. Although these localized treatments were started 1 month after the initial detection in April, surveillance indicated no dispersal from this focus at this time. However, these treatments appeared to have little effect, and WNV eventually was detected throughout the valley, with seven human cases reported in the urbanized upper valley near Palm Springs. In 2005, the initial detection of WNV at North Shore at the end of May was followed rapidly by dispersal throughout the valley precluding efforts at containment. Evaluation of ground and aerial applications at North Shore during May and June 2005, respectively, indicated variable kill of sentinel mosquitoes (overall mortality: ground, 43%; air, 34%) and limited control of the target Cx. tarsalis population. In 2006, aerial ULV applications with the same chemical were begun immediately following the first detection of virus in mid-April, resulting in an apparent reduction of Cx. tarsalis abundance and delay of WNV activity in the rural lower valley and a marked decline in transmission by Culex quinquefasciatus Say populations in the densely populated upper northwestern valley with no human cases reported.