Bloodfeeding Patterns of the Culex Pipiens Complex in Sacramento and Yolo Counties California
Abstract
Mosquitoes in the Culex pipiens complex are competent vectors of West Nile virus (WNV; family Flaviviridae, genus Flavivirus) in the laboratory, and field-collected mosquitoes have tested positive for the virus in California and elsewhere. A better understanding of Cx. pipiens complex blood-feeding patterns will help define the threat that these mosquitoes pose to human health and their role in WNV amplification in northern California. We collected blood-engorged Cx. pipiens complex mosquitoes from resting sites near and away from human habitation in Sacramento and Yolo Counties. Cytochrome c oxidase 1 gene sequences were used to identify the vertebrate species from which blood meals were taken. Of 330 engorged mosquitoes collected at 28 sites from June through August 2007 and May through August 2008, >99% fed on an avian host. Three mosquitoes contained bovine blood and none had fed on a human. American Robins (Turdus migratorius) were bitten most often, and the proportion of American Robin blood meals increased significantly over the summer. Other important avian hosts included House Finches (Carpodacus mexicanus), Barn Swallows (Hirundo rustica), Western Meadowlarks (Sturnella neglecta), and Mourning Doves (Zenaida macroura). In rural areas, Barn Swallows, Brewer's Blackbirds (Euphagus cyanocephalus), and House Sparrows (Passer domesticus) were frequent hosts. In settings near human habitation, Mourning Doves and Western Meadowlarks were common hosts. Our data indicate that in north central California mosquitoes in the Cx. pipiens complex may be more important as epiornitic than epidemic vectors of WNV.
The Culex pipiens complex (Diptera: Culicidae) is found throughout the United States and in temperate and tropical climates of most continents. The Cx. pipiens complex in California is believed to consist of populations representing Cx. pipiens pipiens L. (Diptera: Culicidae) in the north and Cx. pipiens quinquefasciatus Say (Diptera: Culicidae) in the south, as well as hybrids in much of the Central Valley (Iltis 1966, Tabachnick and Powell 1983, Cornel et al. 2003, McAbee et al. 2008).
Populations of the Cx. pipiens complex are competent laboratory vectors of West Nile virus (WNV; family Flaviviridae, genus Flavivirus) (Goddard et al. 2002, Vaidyanathan and Scott 2007, Reisen et al. 2008), and field-caught Cx. pipiens complex from the Sacramento area have tested positive for WNV (Sacramento-Yolo Mosquito and Vector Control District 2004). WNV is of increasing public health concern in California, and a better understanding of their feeding patterns will more clearly define the threat that this group of mosquitoes poses to human health and its relative role in WNV transmission. This information will have practical implications for designing increasingly effective vector control strategies that target species and their habitats at times when adults are most active and thus most susceptible to intervention.
Throughout much of the world, Cx. p. pipiens readily feeds on humans (Edman and Downe 1964, Farid et al. 1991,Vinogradova 2000, Hamer et al. 2009). In the northeastern United States, Cx. p. pipiens is thought to be one of the principal human vectors of St. Louis encephalitis (family Flaviviridae, genus Flavivirus) (Monath 1980) and WNV (Turell et al. 2005). Cx. p. quinquefasciatus is considered a generalist feeder and will readily take blood from both bird and mammal hosts (Reisen et al. 1990, Molaei et al. 2007), thus greatly increasing its potential to act as an epidemic vector of WNV to humans (Vinogradova 2000).
Currently in Sacramento and Yolo Counties, California, it is not known to what extent the Cx. pipiens complex feeds on humans compared with birds and other mammals, although a common assumption is that most of their blood meals come from birds (Reeves 1990). A compilation of blood meal analyses using serological methods by Tempelis, Reeves, and Washino in Sacramento Valley indicated that ≈75% of Cx. pipiens complex blood meals originated from avian hosts, and mammalian hosts accounted for the remainder (Reeves 1990). These results, unfortunately, were based on only 28 mosquitoes and were not distinguished by location or time of collection, and passerine hosts were identified only to order.
More recently, assays based on host genome sequences have been developed and used to identify the vertebrate species from which mosquitoes obtained their blood meals (Apperson et al. 2004; Kilpatrick et al. 2006a, b; Cooper et al. 2007; Savage et al. 2007; Hamer et al. 2009). The principal advantage of this approach is its capability of identifying a wide range of hosts to species (Cooper et al. 2007). Recently developed methods use the cytochrome c oxidase 1 (CO1) gene, which codes for a protein in the mitochondrial electron transport chain (Hebert et al. 2003). The CO1 gene is known to have considerable interspecies variation and relatively little intraspecies variation (Cooper et al. 2007).
In this study, we sought to determine the role that the Cx. pipiens complex plays in the transmission of WNV in Sacramento and Yolo Counties by studying its host associations. We hypothesized that the Cx. pipiens complex feeds on mammalian and avian hosts (Reeves 1990), including humans, and, therefore, functions as both an amplifying and epidemic vector in this region. Accordingly, the aim of our study was to identify the blood meal hosts of engorged Cx. pipiens complex mosquitoes that were collected from natural resting sites in a variety of habitats in the two-county region.
Materials and Methods
Study Area.
Our study took place in Sacramento and Yolo Counties, both of which are situated in California's Central Valley and comprise an area of 2,018 square miles. The human population of Sacramento County is ~1.2 million (2000 census figures), and ~200,000 live in Yolo County. Both counties contain a diverse array of habitats, including rangelands, riparian ecosystems, wetlands, farmlands, and suburban and urban centers.
Cx. pipiens Collection.
Engorged Cx. pipiens complex mosquitoes were captured using a hand-held vacuum aspirator primarily from artificial resting sites, including bridges, awnings of homes and businesses, walls, patios, and public restrooms. Mosquitoes also were collected using a hand-held vacuum aspirator from red resting boxes (Meyer 1985) previously set out by the Sacramento-Yolo Mosquito and Vector Control District. Collection locations were selected from potential resting sites based on previous reports of engorged female Cx. pipiens complex resting behavior (Irby and Apperson 1992). The majority of sampling took place in proximity to urban and suburban centers, rather than rural areas, based on the assumption that they would offer a greater availability of human hosts to address our research hypothesis.
Mosquitoes were collected during the morning hours (05:00–11:00). Preliminary field studies indicated that very few mosquitoes were present at these sites between 02:00 and 05:00 in the morning, and the largest number of mosquitoes was present between 06:00 and 10:00. Before and after that time period, very few mosquitoes were found at our collection sites. The collection container for each area was labeled by date and location, stored on wet ice in the field, and transported to the field laboratory where engorged females were identified to Cx. pipiens complex based on morphological characters (Meyer and Durso 1998). Male mosquitoes, nonengorged females, and engorged females not in this complex or species other than the Cx. pipiens complex were discarded. Engorged Cx. pipiens complex females were then placed in marked individual 1.5-μl tubes and stored at −80°C.
Site Classification.
To account for differences in host availability, sites were divided into rural and nonrural categories. Rural sites had no human inhabitants within 500 m, whereas sites classified as nonrural had some form of human habitation within 500 m, including homeless encampments underneath bridges.
Mosquito Blood Meal DNA Extraction.
Mosquitoes were placed on wax paper, and the abdomen was removed using a razor blade. Razor blades were discarded, and a new one was used for each dissection. Abdomens were then placed in 0.5-ml polymerase chain reaction (PCR) tubes containing 20 μl of phosphate-buffered saline. The heads and thoraces of engorged Cx. pipiens complex mosquitoes were returned to their original tubes and stored at −80°C as voucher specimens. Abdomens were ground with a 100-μl pipet tip, which was used to push the abdomen against the side of the tube and force out the blood, after which 200 μl of phosphate-buffered saline was added to each tube. DNA was extracted using a Qiagen DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA) and then stored at −20°C in 200 μl of elution buffer AE (Qiagen) (T.T., personal communication).
Blood Meal CO1 Amplification.
Vertebrate host mitochondrial CO1 genes in blood meals were amplified via PCR. Universal vertebrate primers, as previously described by Cooper et al. (2007), were used for PCR of the 648-bp CO1 gene. Forward primers VF1, VF1d, and VF1i and reverse primers VR1, VR1d, and VR1i were combined at 1:1:2 ratios to create a VF and VR primer mix. Then 0.5 μl of 20 μM forward and reverse primer mixes were added to PuReTaq Ready-To-Go PCR beads (GE Healthcare, Buckinghamshire, United Kingdom) along with 1.0 μl of template DNA and 23 μl of denucleated water. Amplifications were done on a GeneAmp PCR System 9700 (Applied Biosystems, Singapore) with thermocycling conditions of one initial denaturing cycle at 95°C for 5 min, then 30 denaturing cycles at 95°C for 30 s, 45°C annealing cycle for 15 s, and 72°C extension cycle for 30 s, followed by one final extension cycle at 72°C for 7 min with a final hold at 4°C.
CO1 Sequencing.
Before sequencing, PCR products were purified using ExoSAP-IT for PCR Product Clean-Up (United States Biomedical, Cleveland, OH). Purified PCR products were submitted to the College of Agricultural Sciences Genomics Facility at the University of California (Davis, CA) for sequencing. CO1 sequences were matched to host species using the Barcode of Life Data System (www.barcodinglife.com) (Ratnasingham and Hebert 2007). All matches were at least 95% homologous to a specific host species.
Before sequencing field-collected mosquitoes, blood pellets from 13 known avian species (provided by W. K. Reisen, University of California, Davis) underwent PCR and were submitted for sequencing. Ten mixed blood meals containing two of these known species' DNA that underwent PCR were also submitted for sequencing.
Statistical Analysis.
Results were analyzed to determine seasonal changes in host associations and differences in targeted hosts among habitat types. A fit model test on the JMP 8.0 software was used (SAS Institute, Cary, NC). A χ2 test (P ≤ 0.05) was used to detect statistically significant differences between the proportions of American Robin (Turdus migratorius) feeds over time.
Results
Field Collections.
A total of 433 engorged Cx. pipiens complex was collected at 28 sites from June through August 2007 and May through August 2008 (Table 1); 240 mosquitoes were collected during 2007 and 193 during 2008. Numbers varied markedly from month to month (June 2007, n = 111; July 2007, n = 97; August 2007, n = 32; May 2008, n = 5; June 2008, n = 37; July 2008, n = 126; and August 2008, n = 28). Nonrural sites accounted for 23 of the 28 sites and 288 of the total mosquitoes collected. The remaining 145 mosquitoes were collected from five rural sites.
Table 1.
Locations where engorged Cx. pipiens complex were collected
Table 1.
Locations where engorged Cx. pipiens complex were collected
Blood Meal Identifications.
Amplifying and sequencing bird blood of known origin for 13 species resulted in CO1 sequences that correctly identified all 13 species: Western Scrub-Jay (Aphelocoma californica), American Crow (Corvus brachyrhyncho), Yellow-billed Magpie (Pica nuttalli), Song Sparrow (Melospiza melodia), House Sparrow (Passer domesticus), House Finch (Carpodacus mexicanus), European Starling (Sturnus vulgaris), Cliff Swallow (Petrochelidon pyrrhonota), Red-winged Blackbird (Agelaius phoeniceus), Mourning Dove (Zenaida macroura), Rock Pigeon (Columba livia), Chicken (Gallus Gallus), and Snowy Egret (Egretta thula). Attempts to identify intentionally mixed blood meals taken from two known species failed; only one host could be identified. It is possible, therefore, that some blood meals in the current study were from two host species, and in those cases we detected only one species.
DNA was extracted from 409 of the 433 mosquitoes; 24 of the mosquitoes had too small a quantity of blood (less than ≈20% of the abdomen) and did not warrant extraction. Of the 409 blood meals, 330 (80.6%) were matched to a single host species. Blood in the remaining 79 engorged Cx. pipiens complex mosquitoes was either identified as Cx. pipiens complex DNA or could not be sequenced. Each blood meal not identified to species in the first attempt underwent a second PCR and was submitted for sequencing no fewer than two times. Mosquitoes were not tested for WNV.
Identified Hosts.
Blood meals were identified from 24 avian and one mammal species (Table 2). In total, 99.1% of all blood meals came from avian hosts. The American Robin was the most common host and accounted for 17.3% of all blood meals. American Robin-derived blood meals were detected at 21 of the 28 sites from which samples were obtained. Other prevalent hosts that accounted for between 11.8 and 15.5% were House Finches, Barn Swallows (Hirundo rustica), Western Meadowlarks (Sturnella neglecta), and Mourning Doves (Table 3). The House Sparrow and Brewer's Blackbird (Euphagus cyanocephalus) accounted for 7.6 and 5.5% of bloodmeals, respectively. There were no mosquitoes with detectable bloodmeals taken from humans. Three bloodmeals came from a mammalian host, the domestic cow (Bos taurus).
Table 2.
Vertebrate host from which Cx. pipiens complex collected in Sacramento and Yolo Counties imbibed blood (2007–2008)
Table 2.
Vertebrate host from which Cx. pipiens complex collected in Sacramento and Yolo Counties imbibed blood (2007–2008)
Seasonal Shifts in Host Association.
The proportion of American Robin-derived blood meals significantly increased as the summer progressed (P = 0.03), with the peak in August (Table 3). The role of Brewer's Blackbirds as a host was significantly higher in June 2007 than in any other time period (P = 0.008). It accounted for 16.7% of bloodmeals during that month. Only during two other occasions was Brewer's Blackbird feeding detected during the 2-yr study. Barn Swallows appeared to be an ephemeral host. It represented a major portion of Cx. pipiens complex blood meals for short periods in June 2007 and late June and early July 2008. House Finches were the only host that accounted for >10% of bloodmeals in every month across all collections, with the exception of May 2008, during which only three mosquito blood meals were identified (Table 3).
Identified Hosts by Location.
In rural areas, significantly more bloodmeals were taken from Barn Swallows (P = 0.0004), Brewer's Blackbirds (P = 0.0001), and House Sparrows (P = 0.007) than in nonrural areas. House Sparrow- and Barn Swallow-derived blood meals were significantly correlated with one another (P = 0.0001). Mourning Doves (P = 0.0036) and Western Meadowlarks (P = 0.0163) represented significantly higher proportions of targeted hosts in nonrural areas (Table 4).
Table 4.
Number and percentage of hosts from which Cx. pipiens complex collected in rural and nonrural areas of Sacramento and Yolo Counties took blood (2007–2008)
Table 4.
Number and percentage of hosts from which Cx. pipiens complex collected in rural and nonrural areas of Sacramento and Yolo Counties took blood (2007–2008)
Discussion
WNV epidemics depend on both amplifying and bridge vectors, and the Cx. pipiens complex has been shown to function as both in many areas (Vinagradova et al. 2000; Kilpatrick et al. 2006a,b; Savage et al. 2007; Hamer et al. 2009). Results from our study do not support this scenario in Sacramento and Yolo Counties. Based on the analysis of blood meals in field-caught engorged Cx. pipiens complex at the locations and during the times sampled, this species complex appears to function primarily as a WNV-amplifying, enzootic vector. Not a single incident of human feeding was detected among 330 mosquitoes. Overall, mammals accounted for <1% of blood meal hosts. Although it is possible that humans are occasionally bitten between May and August or after August when we were unable to collect members of the complex, results of the current study do not support the hypothesis that the Cx. pipiens complex functions as a bridge vector in Sacramento and Yolo Counties.
The American Robin was bitten most often by the Cx. pipiens complex mosquitoes assayed in our study. American Robin-derived bloodmeals were found in 21 of the 28 sites from which Cx. pipiens complex mosquitoes were collected. Available data indicate that this species is a competent amplification host for WNV; this was, however, based on only two birds (Komar et al. 2003). It is, therefore, possible that this species plays an important role in local, California WNV amplification. The propensity of the Cx. pipiens complex to target American Robins is consistent with other studies that established that species as a preferred host of the Cx. pipiens complex in other areas of the United States (Kilpatrick et al. 2006a, b; Savage et al. 2007; Hamer et al. 2009; Kent et al. 2009). Although other investigators have reported a steep decline in the number of blood meals derived from American Robins during late summer (Kilpatrick et al. 2006a, b; Hamer et al. 2009; Kent et al. 2009), our results indicate the opposite was taking place in north central California (Table 3). During 2007 and 2008, a higher percentage of American Robin blood meals was taken during late than early summer. It is possible that postnesting robin populations aggregate near the mosquito collection sites, such as suburban lawns and in parks, and could consist of residents as well as arriving overwintering immigrants from montane populations.
Another important passeriformes host for the Cx. pipiens complex was the House Finch. This species was a relatively consistent host across time, accounting for >10% of blood meals in every month of the year. It was the second most common overall host after the American Robin. Numerous studies have established this species as having an important role in the amplification of WNV throughout the United States (Komar et al. 2003, Hamer et al. 2009), and it has frequently been found antibody positive for WNV in California (Wilson et al. 2006, Reisen et al. 2009). As a result of this species' known competence as a WNV amplification host and its role as principal host throughout the summer months, it is likely that it plays an important role as a vertebrate amplification host of WNV in Sacramento and Yolo counties.
Similarly, the House Sparrow is an extremely competent WNV amplification host (Komar et al. 2003) and is frequently found WNV antibody positive in California (Wilson et al. 2006, Komar et al. 2001, 2003). Cx. pipiens complex blood feeding on this species was found in close association with feeding on Barn Swallows. This is an expected outcome because House Sparrows use abandoned Barn Swallow nests to construct their nests and rear their young (Weisheidt and Creighton 1988).
Cx. pipiens complex frequently took blood meals from other passeriformes hosts that have not been subjected to experimental laboratory infections with WNV, including Western Meadowlarks and Barn Swallows. The Western Meadowlark was the source of 16.9% of feedings in nonrural areas and 4.1% in rural areas. It should be noted, however, that all of the sites where Western Meadowlark blood meals were detected were associated with large and open expanses of grass interspersed with trees. The competence of Western Meadowlarks as amplifying hosts of WNV has not been experimentally evaluated in the laboratory. The frequency at which Western Meadowlarks were bitten by the Cx. pipiens complex warrants further study of this species' role in amplification and transmission of WNV.
Barn Swallows were an important rural host during the early summer (32.5% of all rural blood meals). Large numbers of engorged Cx. pipiens complex were found in close proximity to nesting Barn Swallows and their young, especially at the Twin Cities Bridge and Bruceville Road bridge sites. After the swallow nests were abandoned, very few engorged Cx. pipiens complex were collected from those sites and no other Barn Swallow blood meals were identified. To date, no experiments have been conducted to test the efficacy of this species as amplification hosts of WNV, although dead Barn Swallows have tested positive for WNV in California (CDC 2009).
Of the nonpasseriformes hosts from which the Cx. pipiens complex fed, the Mourning Dove was the only host that accounted for >10% of bloodmeals. This was an important host in many nonrural sites. Although this species is not an especially competent amplification host of WNV (Reisen et al. 2005), its role as a common blood meal host of the Cx. pipiens complex in nonrural areas could potentially make it an important host in amplifying virus transmission if large numbers of viremic birds are bitten.
Surprisingly, corvids accounted for only 2.4% of all Cx. pipiens complex blood meals in our study. This is especially interesting considering that the majority of dead birds that tested positive for WNV in the study area are corvids (SYMVCD 2008). Although corvids have been shown to be especially susceptible to WNV and act as extremely competent amplifying hosts (Komar et al. 2003), they may be acquiring their infections from other mosquito species or a portion of corvid infections may come from bird-to-bird transmission (Dawson et al. 2007) rather than from the bite of a mosquito. At the locations and times we sampled, they were not major hosts of detectable Cx. pipiens complex blood meals, although their abundance at those sites was not recorded.
Although foraging indexes and host availability surveys have proven useful in field studies of mosquito blood-feeding patterns (Kent et al. 2009), we did not include a foraging index in this study. The impetus of the current study was to collect the maximum number of mosquitoes from as many different locations and habitats as possible. Consequently, the focus was on collecting engorged mosquitoes from multiple sites over a 3- to 4-mo period, which made it logistically impractical with the resources available to simultaneously carry out host availability surveys.
Our study sought to provide a better understanding of the feeding patterns of Cx. pipiens complex in California's Sacramento and Yolo Counties to better understand the role that this species complex plays in the spread of WNV. Avian hosts bitten by mosquitoes in this complex varied significantly by month and location. The American Robin was fed upon most often, and the Cx. pipiens complex's propensity to feed on this species increased as the summer progressed. Other important hosts were Western Meadowlarks, Barn Swallows, House Finches, and Mourning Doves. No human feeding was detected. Accordingly, our study indicates that mosquitoes in the Cx. pipiens complex found in Sacramento and Yolo Counties are involved mainly in the enzootic cycle of WNV. It is possible, however, that members of the complex bite humans after August when we were unable to collect Cx. pipiens complex mosquitoes, in which case they could contribute to epidemic WNV transmission.
Acknowledgments
William Reisen and Anton Cornel are owed a debt of gratitude for advice and encouragement throughout the project and for editing an earlier version of this manuscript. Stan Wright and Marcia Reed of the Sacramento-Yolo Mosquito and Vector Control District guided the collections phase of this project and helped shape its overall direction. The Sacramento-Yolo Mosquito and Vector Control District funded the study and provided the equipment necessary to carry it out.
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