ABSTRACT

In 1920, Culex coronator was reported from San Benito, Texas, and later in Arizona, New Mexico, and Oklahoma. In 2005, this species was reported to be spreading across the southeastern USA. Now reported in 14 states, it has been found as far north as northern Oklahoma; Memphis, TN; and Suffolk, VA. The public health significance of Cx. coronator is not firmly established, even though it has been implicated as a potential vector of several arboviral diseases. This study aims to document additional Cx. coronator county-level records, to provide information about its continued expansion across the southern USA, and to provide a short research update into its vector potential. Data acquired through multistate collaborations and author collections resulted in 146 new county records from Alabama, Arkansas, Florida, Georgia, Louisiana, Mississippi, North Carolina, Oklahoma, South Carolina, and Texas. No new county records were presented for Arizona, New Mexico, Tennessee, or Virginia, which had previously reported this species. With these new data, this species has been documented in 386 counties in 14 states of the continental USA.

INTRODUCTION

The first collection of Culex coronator Dyar and Knab in the USA was made on August 21, 1920, by Harrison G. Dyar (1921) in San Benito, Cameron County, TX. Subsequently, it was reported from Arizona, Louisiana, New Mexico, and Oklahoma (Beyer 1923, King et al. 1942, Murphy 1953, Richards et al. 1956, Hill et al. 1958, Carpenter 1970, Wolff et al. 1975, Hayes et al. 1976, Jones et al. 1977), but it did not receive attention until 2005, when it was reported again in Louisiana (Debboun et al. 2005) and for the first time in Mississippi (Varnado et al. 2005). Over the next 12 years, it was reported in Alabama, Florida, Georgia, North Carolina, again in Oklahoma, South Carolina, Tennessee, and Virginia (Smith et al. 2006, McNelly et al. 2007, Kelly et al. 2008, Moulis et al. 2008, Noden et al. 2015, Harrison et al. 2016, Akaratovic and Kiser 2017, Trimm et al. 2017). In 2019, the Texas distribution records were updated (Sames et al. 2019), and additional records were published for Oklahoma (Bradt et al. 2019). No other new published county records were found for this species.

This study aims to document additional Cx. coronator county-level records, to provide information about its continued expansion across the southern USA, and to provide a short research update into its vector potential.

MATERIALS AND METHODS

Many of the collections were from routine surveillance programs conducted from May through October or in response to a nonroutine public health concern such as posthurricane or Zika vector surveillance. Other collections were made by authors in counties where routine surveillance was not conducted.

Adult collections were made with Biogents-Sentinel (BGS), gravid, or Centers for Disease Control and Prevention (CDC) light traps. Larval collections were made using cups, dippers, basters, or siphons. Collections, identifications, and reporting procedures were in accordance with individual state guidance. Independent collectors used Darsie and Ward (2005) and Carpenter and LaCasse (1955) for identifications.

RESULTS

This study reports 146 new county records for Cx. coronator (Table 1) from Alabama (1), Arkansas (1), Florida (2), Georgia (71), Louisiana (3), Mississippi (2), North Carolina (2), Oklahoma (4), South Carolina (25), and Texas (35). No new records were reported from Arizona, New Mexico, Tennessee, or Virginia. Overall, Cx. coronator has been reported in 386 US counties across 14 states (Fig. 1).

Table 1.

New county-level records for Culex coronator in the USA.

New county-level records for Culex coronator in the USA.
New county-level records for Culex coronator in the USA.
Fig. 1.

Distribution of Culex coronator in the southern USA.

Fig. 1.

Distribution of Culex coronator in the southern USA.

Culex coronator has been collected January through December in at least the southern counties of Florida, Georgia, Louisiana, Mississippi, and Texas. The remaining states vary in seasonality in part due to a low number of collection events and due to potential unfavorable weather conditions during winter months. Studies following statistical protocols are needed to accurately measure and portray the development and seasonality of this species.

In the following paragraphs, details pertaining to the new county records for Cx. coronator are presented by state. All new records are listed in Table 1. The number and percentage of counties with reported collections of Cx. coronator and earliest and latest annual collections by state are reported in Table 2.

Table 2.

Number and percent of counties with reported collections of Cx. coronator and earliest and latest annual collections by state.

Number and percent of counties with reported collections of Cx. coronator and earliest and latest annual collections by state.
Number and percent of counties with reported collections of Cx. coronator and earliest and latest annual collections by state.

Alabama

Previously, Cx. coronator was reported from Mobile County (McNelly et al. 2007) and Macon County (Gray et al. 2008). On September 12, 2019, Cx. coronator adults were collected in Baldwin County (Dan Killingsworth, personal communication). No other Alabama records were available for this report.

Arizona

Historically, Murphy (1953) reported 2 collections of Cx. coronator (as Cx. coronata) in Pima County. Richards et al. (1956) collected 1 larval Cx. coronator in Cochise County (St. David, October 22, 1953) and republished the 2 Pima County collections (Arivaca, June 17, 1934, 1 reared female, Coll. LP Wehrle, Det. A. Stone, and Santa Catalina Mountains, March 27, 1930, 1 reared female, Coll. LP Wehrle, Det. A. Stone), which are housed in the University of Arizona Insect Collection (UAIC). An additional 6 reared specimens (2 males, 4 females) from Pima County (Sabino Canyon, Santa Catalina Mountains, November 1, 1963, Coll. and Det. John Burger) are also in the UAIC.

Since its construction in 1996, some 178 Cx. coronator females were collected from the 60-acre Sweetwater Wetland, Tucson, AZ (Pima County), which is maintained by Tucson Water. Six CO2 trap collections were run weekly from March through November, with most Cx. coronator being collected from September to November and some collected in March, April, May, and June. The earliest season collection date was March 15, 2017; the latest was November 28, 2012.

Additionally, 2 Cx. coronator larvae were collected in a dog's water bowl in Tucson in October 2000 as part of a student project and identified by Frank Ramberg.

Arkansas

On September 5, 2020, early instar Cx. coronator larvae were collected in a large ground pool from rains associated with Hurricane Laura in Texarkana, Miller County, AR, for the first report of this species in Arkansas. These larvae were reared to 4th instar (7 identified as larvae) or the adult stage (2 males, 3 females) for identification. In the same pool, Psorophora columbiae Dyar and Knab and Aedes vexans Meigen were collected in the pupal stage along with all instars of Cx. nigripalpus Theobald. The probability that Cx. coronator has been in Arkansas for many years is likely given that this species has been collected in states that border Arkansas, including Bowie County, TX (Hill et al. 1958), Shelby County, TN (Trimm et al. 2017), and Sequoyah and McCurtain counties, OK (Noden et al. 2015 and Bradt et al. 2019, respectively).

Florida

Connelly et al. (2016) presented collection data for 64 of the 67 counties in Florida. New records of Cx. coronator larvae collected in tires in Gulf and Franklin counties are reported. In Gulf County, the larvae were associated with Ae. albopictus (Skuse) and in Franklin County, they were associated with Cx. quinquefasciatus Say (Table 1). Monroe County is the only county without a confirmed presence of Cx. coronator. Staff members at the Florida Keys Mosquito Control District in Monroe County have not collected Cx. coronator in the Florida Keys and they do not survey the mainland area of Monroe County, which is primarily the Everglades National Park (Larry Hribar, personal communication).

Georgia

Prior to this study, Cx. coronator was reported from Baker, Chatham, Dougherty, Lowndes, and Muscogee counties (Kelly et al. 2008, Moulis et al. 2008, Buckner et al. 2011). Data from the Georgia Department of Public Health, health districts, county mosquito control districts, and other collaborators resulted in the detection of Cx. coronator in an additional 71 counties (Table 1). Gravid or CDC light traps were used to acquire these data, which resulted in the collection of 5,313 females during 892 adult collection events. No larval collections were reported.

Louisiana

Culex coronator were reported in Orleans Parish (Beyer 1923) and Vernon Parish (Hill et al. 1958), but these reports were negated by King et al. (1942) and Carpenter (1970), respectively. Later, Debboun et al. (2005) reported Cx. coronator in Vernon Parish, and Mackay et al. (2008) reported it in East Baton Rouge Parish. In addition to Vernon and East Baton Rouge parishes, this study reports 3 new parish records.

Culex coronator adults were collected in St. Tammany Parish in 181 trapping events using gravid and CDC light traps from 2013 to 2019 according to digital records. During these 7 years, 325 specimens (mean = 1.8 per trap; range = 1–8) were collected. Hard copy records prior to 2013 were not accessed (St. Tammany Parish Mosquito Abatement District, personal communication).

In Tangipahoa Parish, Cx. coronator and Ae. albopictus larvae were collected from a jon boat in a private yard on September 12, 2020.

During October 6–11, 2020, Cx. coronator larvae were collected at 4 of 6 locations in Shreveport, Caddo Parish, and identified by WJ Sames. The larvae were collected in a ground pool and in 3 separate tire piles. They were associated with Ae. albopictus, Ae. vexans, Anopheles quadrimaculatus Say, Cx. nigripalpus, Cx. restuans Theobald, Cx. quinquefasciatus, Orthopodomyia signifera (Coquillett), and Ps. columbiae. This was the first time Or. signifera was collected in association with Cx. coronator.

Mississippi

Previously, Cx. coronator had been reported in 28 counties (Varnado et al. 2005, Goddard et al. 2006, Varnado et al. 2012, Skiff and Yee 2014, Varnado and Goddard 2015, Yee et al. 2015, Goddard et al. 2017). Data from the Mississippi Department of Health's mosquito-borne disease surveillance program resulted in the detection of Cx. coronator in Jones and Neshoba counties.

New Mexico

Culex coronator were reported in Dona Ana County (Wolff et al. 1975) and Quay County (Jones et al. 1977). No new records or collections of Cx. coronator in New Mexico are reported here.

North Carolina

In North Carolina, Harrison et al. (2016) reported Cx. coronator in Brunswick and New Hanover counties and Brown et al. (2017) reported it in Columbus County. This study reports 2 new county records: Craven and Mecklenburg counties. The separation of the southeastern cluster of Brunswick, New Hanover, and Columbus counties from the eastern Craven County and more central Mecklenburg County suggest this species may be more widespread throughout the eastern half of the state.

Oklahoma

Prior to this study, Cx. coronator were reported from 12 counties (Hayes et al. 1976, Paras et al. 2014, Noden et al. 2015, Bradt et al. 2018, 2019). In July–August 2020, Cx. coronator were collected at 14 CDC light trap sites, which resulted in 4 new county records: Blaine, Caddo, Kingfisher, and Murray counties.

South Carolina

Moulis et al. (2008) collected Cx. coronator in Jasper County for the first record of this species in South Carolina. County surveillance samples submitted to the South Carolina Department of Health and Environmental Control (SCDHEC) resulted in 25 additional county records: Aiken, Anderson, Beaufort, Berkeley, Charleston, Clarendon, Colleton, Darlington, Dorchester, Florence, Georgetown, Greenville, Greenwood, Horry, Lancaster, Lexington, Marion, Newberry, Oconee, Orangeburg, Richland, Spartanburg, Sumter, Union, and York. The adult samples were collected using BGS, gravid, and CDC light traps.

Tennessee

Trimm et al. (2017) reported Cx. coronator in Shelby County, TN. While no new county records of Cx. coronator in Tennessee were reported, Andrew Insch (personal communication) reported that Cx. coronator were not found in 2018–2019, but collected again in October 2020 when Cx. coronator larvae were found at 2 locations. Of 49 collection events (2017, 2020), 48 were larval collections associated with ground pools (natural and concrete ditches, and around culverts). The larval collections were identified as larvae, and the Cx. coronator larvae were associated with larvae of Ae. albopictus, Cx. erraticus (Dyar and Knab), Cx. pipiens/quinquefasciatus, Cx. restuans, Cx. salinarius Coquillett, Cx. territans Walker, Ps. columbiae, and Ps. ferox (von Humboldt).

Texas

Sames et al. (2019) reported 127 historical and new Cx. coronator records in Texas. Since then, data for 35 new county records were acquired, of which 30 were larval collections, 2 were light trap collections by the Brazos County Health Department, and 3 were light trap collections by Clarke Mosquito Control, St. Charles, IL, under contract to the Texas Department of State Health Services after Hurricane Harvey in 2017 (Whitney Qualls, personal communication). In 2019–2020, Cx. coronator larval collections (n = 157; 30 were records plus 127 other collections) were from ground pools (97, which included roadside ditches, flooded depressions in fields, areas around leaking pipes or overflowing water troughs), water troughs (concrete [11], metal [8], plastic [5]), tires (17), plastic tubs (12), steel barrels (4), abandoned swimming pools (2), and a steel wheelbarrow (1). These author collections were in the eastern half of Texas and not limited to the counties with new records of this species.

Except for Ae. trivittatus (Coquillett), the 22 species reported by Sames et al. (2019) were collected in association with Cx. coronator larvae. Additionally, 8 new larval associates were collected. These were Ae. bimaculatus (Coquillett), Ae. taeniorhynchus (Wiedemann), Cx. erraticus, Cx. pilosus (Dyar and Knab), Ps. cyanescens (Coquillett), Ps. longipalpus Randolph and O'Neill, Ps. signipennis (Coquillett), and Uranotaenia anhydor syntheta Dyar and Shannon.

Virginia

Akaratovic and Kiser (2017) reported Cx. coronator in the independent City of Suffolk for the first record of this species in Virginia. In addition to this collection, Karen Akaratovic (personal communication) reported a second BG-Sentinel trap collection of 1 female Cx. coronator in Suffolk on November 16, 2020. These data suggest Cx. coronator, if not established, is still making seasonal incursions into the state.

DISCUSSION

The collection of Cx. coronator in 146 additional counties (total = 386) in the continental USA is documented in this paper. These collections suggest that this species is well established across the southern states (Alabama, Florida, Georgia, Louisiana, Mississippi, South Carolina, Texas). States to the north of these (Arkansas, North Carolina, Oklahoma, Tennessee, Virginia) may be in a unique situation to study the northern limits of this species, and states along the western edge (Arizona, New Mexico, Oklahoma, Texas) of the Cx. coronator geographic range can study its northern and western expansion into arid ecosystems.

As the range of Cx. coronator has expanded at a surprisingly rapid rate in the USA, including in major metropolitan areas, more studies are needed to clarify the vector competency of Cx. coronator and its potential to act as a bridge vector for arboviruses. Although historically Cx. coronator has not been linked to outbreaks of human disease, arboviruses of medical relevance have been identified in field collected Cx. coronator adults. Examples include isolation of St. Louis virus (SLV) from a field specimen in Trinidad (Aitken et al. 1964), West Nile virus (WNV) from specimens in Louisiana (Mackay et al. 2008, Unlu et al. 2010), and Zika virus detected in salivary glands of Cx. coronator collected near Guadalajara, Mexico (Elizondo-Quiroga et al. 2018). In the latter study, Zika was found in female and male specimens, leading the authors to suggest that vertical transmission is possible. Laboratory experiments have demonstrated susceptibility of Cx. coronator to viral infection of both SLV and WNV. In the former case, transmission of SLV to chickens occurred 8–10 days after a suspension of the virus was fed to females (Hammon and Reeves 1943a, 1943b). In the latter, WNV dissemination rates were noted to be comparable to those of other Culex vectors, while transmission rates were lower under the conditions examined (Alto et al. 2014). A recent study (Miranda et al. 2019) reported the presence of Culex Flavivirus (CxFV) in Cx. coronator pools from Colombia. Although insect-specific flaviviruses do not cause disease in humans, their presence can potentially block infection by other flaviviruses of public health importance (Burivong et al. 2004, Kent et al. 2010).

Culex coronator females have been characterized as preferring mammalian hosts (Mackay et al. 2010). Notably, a recent report (Mann et al. 2020) identified chickens and white-winged doves in Cx. coronator bloodmeals from Harris County, TX, indicating that this species may feed opportunistically, perhaps varying with seasonal host availability. Added to this, Cx. coronator may also be a vector of avian malaria (Noden et al. 2021). Like Ae. aegypti (L). and Ae. albopictus, Cx. coronator appears to be adaptable to artificial container breeding (Yee 2012, Yee and Skiff 2014, Skiff and Yee 2015), implying that the prospects for its control in urban areas could be quite challenging.

Looking for this and other mosquito species in previously unreported areas and habitats is encouraged in order to improve mosquito distributional information and help provide a baseline from which species movement can be observed and monitored. Studies designed to determine factors related to its development and other bionomical factors are needed to understand and predict the geographic range of Cx. coronator. States should continue to report the distribution of Cx. coronator to help determine the spread and limits of this species.

ACKNOWLEDGMENTS

The authors thank the many participants in county, university, and other surveillance programs that indirectly impacted this study as they worked diligently to protect the people in their communities. The authors also thank the following for their support of this study: Karen Akaratovic, Suffolk Mosquito Control, Whitney Qualls (former TX DSHS Entomologist), Nicolas DeLisi and staff (St. Tammany Parish, LA), David and Margaret Desha, David Gaines (Virginia Department of Health), Wesley E. Hall, University of Arizona Insect Collection, Andrew Insch, James Washington, and Adrianna Sharkey (Shelby County Vector Control, Shelby, TN), Herff Jones (AMCA South Central Regional Director), Margaret Snyder, Tucson Water, and the Vector Control staff of the Brazos County Health Department. The authors also thank the property owners or managers who granted permission to collect mosquito larvae on their property. The authors thank mapchart.net for allowing access and use of their online mapping capabilities in the creation of Fig. 1.

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Author notes

1

PO Box 547, Leakey, TX 78873.

2

Baylor University, Department of Biology BSB A 159R, 101 Bagby Avenue, Waco, TX 76706.

3

Vector-Borne & Zoonotic Diseases Team, Environmental Health Section, 13-414, Georgia Department of Public Health, 2 Peachtree Street, NW, Atlanta, GA 30303.

4

Environmental Health Services, Department of Health and Environmental Control, 2600 Bull Street, Columbia, SC 29201.

5

Mississippi State Department of Health, 570 E Woodrow Wilson Avenue, Jackson, MS 39216.

6

13955 Beechwood Circle, Lindale, TX 75771-7703.

7

Medical and Veterinary Entomology, Department of Entomology & Plant Pathology, Oklahoma State University, 127 Noble Research Center, Stillwater, OK 74078.

8

Department of Entomology, University of Arizona, Tucson, AZ 85721.

9

Arbovirus Surveillance Team Leader, Beach Mosquito Control District, 509 Griffin Boulevard, Panama City, FL 32413.

10

Environmental Security Pest and Lawn, 3182 Gateway Lane, Cantonment, FL 32533.

11

Communicable Disease Branch, Division of Public Health, North Carolina Department of Health and Human Services, 225 N McDowell Street, Raleigh, NC 27699-1902.