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Culex interrogator (Diptera: Culicidae), a mosquito species new to Florida

2016; Wiley; Volume: 41; Issue: 2 Linguagem: Inglês

10.1111/jvec.12230

1948-7134

Dongyoung Shin, George F. O’Meara, Ayse Civana, Donald A. Shroyer, Evaristo Miqueli,

Vector-borne infectious diseases

In recent years, two mosquito species, Culex declarator Dyar and Knab and Culex coronator Dyar and Knab, have been detected for the first time in Florida. Single specimens of Cx declarator were collected in 1998 and 2002 in Indian River County and many more Cx. declarator adults were encountered in county surveillance activities during 2003 (Darsie and Shroyer 2004). However, since 2003 this mosquito has been collected infrequently and has been reported from only one additional Florida county, Monroe. Culex coronator is thought to have spread eastward from Texas (Gray et al. 2008) and was initially found in the western panhandle section of Florida in 2005 (Smith et al. 2006). Unlike Cx. declarator, Cx coronator is now found in nearly all Florida counties and is especially common in the southern part of the state (Connelly et al. 2016). Here we report on the finding of yet another Culex spp., Culex interrogator (Dyar and Knab), which is new to Florida. Historically, the northern geographic distribution limit of all three of these Culex (Culex) mosquitoes was southern Texas and other states bordering Mexico (Carpenter and LaCasse 1955, Darsie and Ward 1981). Culex interrogator was initially discovered in Florida in Broward County (Lat. 26°01′10.0″N, Long. 80°07′16.1″W) in August, 2013 when several larvae of this species were collected from a storm water drain that was 53 cm in diameter and contained a considerable amount of grass cuttings. Co-occurring with Cx. interrogator were three other mosquito species: Culex nigripalpus (Theobald), Culex quinquefasciatus (Say), and Culex salinarius (Coquillett). A second Broward County site with Cx. interrogator was found in October, 2014, when immatures of this species were collected from a roadside swale. This site was approximately 26 km west of the first site. In July and August, 2014 at two field study sites in Indian River County, more than 3,000 Culex egg rafts were collected from two types of ovitraps (busboy trays, 56 cm × 44 cm, 8 cm depth) that had been deployed to assess oviposition site preferences of Culex spp. Egg rafts were returned to Florida Medical Entomology Laboratory (FMEL) and held in insectary conditions at 28° C and 80% humidity. After eggs hatched, larvae were identified to species based on larval morphological features. Nine of these egg rafts, all from a single study site, produced Cx. interrogator. Other mosquito species collected with Cx. interrogator in the ovitraps included Cx. nigripalpus, Cx. quinquefasciatus, Cx. coronator, and Cx. salinarius. The ovitraps with Cx. interrogator egg rafts were located in a subdivision with numerous undeveloped lots bordering on agricultural lands. During the summer and autumn of 2014, Cx. interrogator adults were collected at seven other locations in Indian River County, including six of the eight sentinel chicken sites operated by the Indian River Mosquito Control District (IRMCD) where mosquitoes were captured in chicken coop exit traps. In the southern part of the county, near the edge of a pasture, several Cx. interrogator were captured in a dry-ice baited CDC miniature light trap and a passive box trap (Ritchie et al. 2013). Many more were taken in early morning collections of resting adults made with a battery powered aspirator (Table 1). More recently, Cx interrogator has been detected in two other Florida counties. In August, 2015 adults of this mosquito were collected in a CO2-baited light trap near Okeechobee City, Okeechobee County. In January, 2016, immature Cx. interrogator were found in a sample taken from a roadside swale with grass cuttings in Citrus County (Figure 1). Culex interrogator larvae are readily distinguished from those of other Culex (Culex) species found in Florida based on the morphological features of the siphon, which is relatively short (siphonal index 3.0 – 3.5) with a pecten extending 0.75 the length of the siphon and having distal spines much larger than basal spines (Carpenter and LaCasse 1955, Darsie and Ward 2005). The adults of Cx interrogator (especially rubbed specimens) are more difficult to identify, since morphologically they are rather similar to Cx. quinquefasciatus and Culex restuans (Theobald). Compared to these two species, Cx. interrogator is a much smaller mosquito, with wing length 2.5 – 2.8 mm (Carpenter and LaCasse 1955). Rubbed specimens can also potentially be confused with smaller-than-average Cx. nigripalpus females. In Darsie and Ward (2005), Cx. restuans and Cx. interrogator appear in the same terminal couplet with three features listed for distinguishing the two species: (1) medium vs small size (4.0 vs 2.8 mm wing length), (2) a pair of pale spots on the scutum of Cx. restuans, which is absent in Cx. interrogator, and (3) wing cell R2, 4.5× or more length of vein R2+3 (Cx. restuans) vs wing cell 3.0 – 4.0 length of vein R2+3 (Cx. interrogator). The size of an adult mosquito varies considerably in many species depending upon conditions experienced in the larval stage. Therefore, mosquito size should be used in conjunction with other features for species identification. Unfortunately, the absence of pale spots on the scutum is an unreliable diagnostic feature since some specimens of Cx. restuans lack these markings. The wing cell/vein length feature in our experience seems to be a reliable characteristic for distinguishing Cx. interrogator from Cx. restuans. However, this feature requires careful examination of each specimen and does not facilitate expedient identification of these species, nor does it appear to allow for separation from Cx. quinquefasciatus (Darsie and Ward 2005). Mosquito surveillance activities in Florida and elsewhere rely primarily on monitoring adult populations and often use identification keys that are limited to a specific geographical area, for example, a state (Darsie and Morris 2003). Thus, the arrival of a new mosquito may go undetected for a period of time, especially if it is morphologically similar to common native or resident species. During the late spring and summer when mosquito monitoring activities are regularly performed, Cx. restuans adults are rarely collected in any type of trap, particularly in south and central Florida. However, this time period is also when Cx. quinquefasciatus are found in abundance in many trap types and is when a Cx. interrogator might be misidentified as an aberrant Cx. quinquefasciatus. The cuticle of field-collected Cx. interrogator females seen to date appear to be somewhat paler than typical Cx. quinquefasciatus, a feature that may prove to be helpful in identification. Culex interrogator joins an expanding list of mosquito species that have recently invaded Florida, and one trait some of these species have in common is that they utilize artificial containers as production sites. To date, only two of these container-inhabiting mosquito species, Aedes albopictus (Skuse) and Cx. coronator, have become widely distributed in Florida where they pose a threat to human health (Alto et al. 2014, Connelly et al. 2016, O'Meara et al. 1995). During our study, larvae of Cx. interrogator were found in two types of containers: a storm water drain and black plastic vats (bus boy trays) containing 3.8L of hay infusion. Thus, it is likely that they would lay egg rafts in water-holding automotive and truck tires that may be moved from one location to another. Potentially, some tires might carry various amounts of water containing aquatic stages of this species or egg raft. Throughout its range, Cx. interrogator occurs in a wide variety of aquatic habitats from natural and artificial containers, including storm sewers (Manrique-Saide et al. 2012) to ground pools and shallow water-holding depressions (Baak-Baak et al. 2014, Calderόn-Arguedas et al. 2009). In recent years, four mosquito species, Aedes bahamensis (Berlin), Aedes pertinax (Grabham), Aedes condolescens (Dyar and Knab), and Anopheles grabhamii (Theobald), have invaded Florida (Darsie 2003, Darsie et al 2002, Pafume et al. 1988, Shroyer et al. 2015). These mosquito species likely entered Florida from the south, as they have well-established populations nearby in the Bahamas and/or Cuba. Cx. interrogator is not known to occur either in the Bahamas, in Cuba, or elsewhere in the Caribbean region. A single report of this species in Puerto Rico was called "undoubtedly erroneous" by Belkin et al. 1970. Thus, an introduction of Cx. interrogator into Florida from the Bahamas or the Caribbean would seem to be unlikely. Warmer climatic conditions, particularly mild winter temperatures prevalent since the 1990s, may be facilitating the spread of tropical and subtropical species such Cx. declarator, Cx. coronator, and Cx. interrogator from south Texas to central and south Florida. These climatic conditions would allow cold-limited Culex (Culex) mosquitoes to survive at higher latitudes, thereby enhancing opportunities to move eastward along the Gulf Coast states and then down the Florida peninsula. This pattern has clearly been documented for Cx. coronator (Gray et al. 2008). Only two counties in Texas were listed as being occupied by Cx. interrogator in Darsie and Ward (1981), and a single county was added in the second edition (2005). An online publication on the Mosquitoes of Texas (http://agrilifecdn.tamu.edu/aes/files/2010/06/Culex-interogator1.pdf -accessed May 2, 2016) currently shows the occurrence of Cx. interrogator in five counties, including one in north Texas (Figure 1). Major east-west interstate highways connect the two northern-most counties in Texas with documented populations of Cx. interrogator to major highways that allow direct travel to the Florida peninsula. The spread of Cx. interrogator from Texas to Florida was likely facilitated by the movement of mosquito-infested containers, such as tires, along these major highways. At the present time, it is difficult to predict the extent to which Cx. interrogator may become established in Florida and expand its range throughout the state, as the success of this species will depend not only on climatic factors but also on the outcomes of interactions with other mosquito species that occur in water-holding containers and other types of aquatic habitats. Unfortunately little, if any, information is available on these biotic factors. We thank Roxanne Connelly, Billy Kellner, Chris Nelson, Mitchell Smeykal, and Carol Thomas for technical assistance and Nathan Burkett-Cadena and Chelsea Smartt for their comments on an earlier draft of this manuscript. The Applied Mosquito Research Program of Florida Department of Agriculture and Consumer Services, project # 00123786 provided funding for this study.