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A taxonomic checklist of the mosquitoes of Harris County, Texas

2016; Wiley; Volume: 41; Issue: 1 Linguagem: Inglês

10.1111/jvec.12212

1948-7134

Martin Reyna Nava, Mustapha Debboun,

Dengue and Mosquito Control Research

Carpenter and LaCasse (1955) reviewed 143 mosquito species and Darsie and Ward (1981) listed 167 species in North America. Darsie and Ward (2005) included 174 species in North America. However, Aedes pertinax Grabham is a newly discovered species for North America (Shroyer et al. 2015), thus increasing the total to 175 and of those, 85 are listed in Texas. A list of mosquitoes of Texas by McGregor and Eads (1943) contained 54 species; 75 by the Division of Medical Entomology Bureau of Laboratories Texas State Health Department (TSHD) (Randolph and O'Neill 1944), and 79 by the Entomology Division, State Department of Health Laboratories in Austin, TX (1965). Additionally, other researchers have published their findings regarding mosquito densities and distribution in Texas (Breland 1956, Hill et al. 1958, Eads et al. 1960, Easton et al. 1968, Nielsen et al. 1968, Sublette and Sublette, 1970, Moore et al. 1990). The number of mosquito species recorded in Texas increased, including nine new species reported by O'Neill et al. (1944) and the discoveries of other mosquito species reported over the course of time, viz. Deinocerites spanius Dyar and Knab (Fisk 1941), Psorophora mexicana (Bellardi) (Joyce 1945), Anopheles albimanus Wiedemann (Eads 1946), Aedes dupreei (Coquillett), Culex peccator Dyar and Knab, and De. epitedeus Knab (Rueger and Druce 1950), Cx. erythrothorax Dyar (Menzies et al. 1955), Ae. grossbecki Dyar and Knab (Keith 1979), Ae. albopictus (Skuse) (Sprenger and Wuithiranyagool 1986) and Cx. arizonensis Bohart (Reeves and Darsie 2003). Currently, the Texas Department of State Health Services (DSHS) lists 79 species including the subgenus Cx. (Melanoconion) Theobald and Ps. varipes (Coquillett) (Fournier et al. 1989); whereas, the Texas A&M AgriLife Extension Agricultural and Environmental Safety Department (Texas A&M 2013) lists a total of 85 including the two aforementioned species. The same number was reported by the Texas Mosquito Control Association (TMCA 2001) based on Fournier's original list of species and by Darsie and Ward (2005). However, the TMCA list contains species from Texas not reported in Fournier's list. This type of discrepancy occurs among all lists, as one would expect considering the extent and the year in which each study was conducted combined with the changes in mosquito taxonomy through time. Thus, there appear to be differences among all Texas checklists based on the number of species reported. Although mosquito species were collected and data compiled for 51 years in Harris County, there has not been a checklist published for the mosquitoes of Harris County and the City of Houston. The goal of this report is to provide for the first time a checklist of the mosquitoes found in Harris County and the City of Houston as reported in the literature and from our collection records. Harris County is in southeastern Texas. It is irregular in shape measuring about 90.6 km north to south, 129.5 km east to west, and covers 4,603.65 km2 (Figure 1) with a population of over 4.4 million, making it the most populous county in Texas and the third most populous county in the United States (U.S. Census Bureau, 2014a). Northern and eastern portions are largely forested, southern and western portions are predominantly prairie grassland, and coastal areas are prairie and sand. The City of Houston, seat of Harris County, TX, is located on the upper Gulf coastal plain, the most populous city in Texas, and the fourth most populous city in the United States. Surface water in the Houston region consists of lakes, rivers, and an extensive system of bayous and manmade canals that are part of the rainwater runoff management system. Abundant rainfall is a result of the proximity to the Gulf, except for rare extended dry periods, (USDA 1976). Yearly average temperature is approximately 21°C with an average high of 26.5°C, an average low of 15.5°C, and 1,264.1 mm total precipitation (NOAA 2015). Harris County Mosquito Control District (HCMCD), a Division under Harris County Public Health and Environmental Services (HCPHES), was established in 1964 following a St. Louis encephalitis (SLE) epidemic in Houston, TX (Luby et al. 1967, Bartnett et al. 1967, Chamberlain, 1980, Bell et al. 1981, Tsai et al. 1988). The HCMCD used an in-house list of 51 species representing ten genera reported to occur in Harris County, TX, in 1983. Since then, and until 2001, the list increased to 55 species under the same ten genera (HCPHES-MCD, unpublished data). Since its establishment, mosquito surveillance included a variety of collection methods: New Jersey Light Traps (NJLT), Centers for Disease Control and Prevention (CDC) battery operated traps, bait traps, resting stations, larval collections, mechanical aspirators, and landing rate counts. Collected specimens included Ps. columbiae (Dyar and Knab), Cx. salinarius Coquillett, Culiseta inornata (Williston), An. crucians Wiedemann, Ae. sollicitans (Walker), and Cx. quinquefasciatus Say. Thirty-four species were collected out of 50 species reported in Harris County (Bartnett et al. 1967). Since the introduction of West Nile virus (WNV) in Texas in 2002, trapping methodologies changed to the use of modified gravid (GV) traps, CDC light traps (John W. Hock, Gainesville, FL) placed in residential properties, and CDC traps in the storm sewer (SS) system of Harris County and the City of Houston. This accomplished the trapping of the main vector for SLE and WNV, the Southern house mosquito, Cx. quinquefasciatus (Chamberlain et al. 1966, Sudia et al. 1967). Harris County is divided into 268 mosquito control operational areas (MCOA), where half are monitored by GV traps and the other half with CDC light traps (SS). In addition, the implementation of BioGents (BG) Sentinel collecting traps (BioGent, Regensburg, Germany) to target the main vectors of dengue (DEN) and chikungunya (CHIK) viruses (Ae. aegypti (Linnaeus) and Ae. albopictus) have been used since 2012. Storm sewer collections began in July, 1979 with a few areas inside Interstate 610 (Loop 610), a freeway that forms a 61 km-long loop around the downtown sector of City of Houston, TX, and gradually increased until all 268 MCOA were included in 1990. Harris County's activities also contributed to the faunal list. A study conducted in late summer of 1964 yielded 17 species in Houston, TX (Sudia et al. 1967). Five of those species were present in collections made while testing the mesh size in the NJLT to observe the effects on mosquito collections (Bartnett and Stephenson, 1968). Likewise, an arbovirus study from 1968 to 1970 yielded 37 species including An. barberi Coquillett, Ae. atlanticus Dyar and Knab, Ae. tormentor Dyar and Knab, Ae. dupreei, Ae. sticticus (Meigen), Ae. zoosophus Dyar and Knab, and Ps. varipes with the use of battery-operated aspirators, CDC light traps baited with CO2 (dry ice) in resting sites, storm drains, and human bait collections in Houston, TX (Kokernot et al. 1974). However, Ps. varipes should be referred to as Ps. mathesoni, as it was concluded that Ps. ferraroi Duret was a synonym of Ps. varipes, thus the species previously called Ps. varipes in the eastern U.S. was new and named Ps. mathesoni (Belkin and Heinemann 1975). Aedes grossbecki was first recorded in Crosby, TX in 1966 and in Spring, TX, in 1979 in Harris County, TX (Keith 1979). Moreover, collections made in a woodland area within the City of Houston revealed the presence of Ae. atlanticus, Ae. tormentor, Ae. infirmatus Dyar and Knab, Ae. vexans (Meigen), and Ps. ferox (von Humboldt) (Roberts and Scanlon 1979). In addition, Hunt and Hacker (1984) collected mosquitoes in five genera and 13 species using CDC light traps baited with dry ice in the storm drain system inside the Interstate 610 Loop in Houston, TX, where 99% of the specimens collected were Cx. quinquefasciatus, in contrast to the results of Sudia et al. (1967) and Kokernot et al. (1974). Similarly, some species such as Ae. aegypti, Ae. triseriatus (Say), Toxorhynchites rutilis septentrionalis Dyar and Knab, Or. signifera (Coquillett), and Cx. territans Walker, among others, were collected during the discovery of Ae. albopictus in Harris County, TX in 1985 (Sprenger and Wuithiranyagool 1986). Aedes epactius Dyar and Knab, and Ae. hendersoni Cockerell were collected in Harris County during routine collections in 1986 (Wuithiranyagool, personal communication). Aedes hendersoni had been restored to full specific rank, illustrating the differences between this species and those of Ae. triseriatus, thus being resurrected from synonymy (Breland 1960, Darsie 1973). Harris County Mosquito Control District did not have a reference collection, therefore one was established in 1986 after the discovery of Ae. albopictus. Forty-two species are currently deposited within the collection out of the current 56 mosquito species, representing ten genera (Knight and Stone 1977, Knight 1978), reported to occur in Harris County based on our collections and records (Table 1). I) Genus AEDES Meigen •Subgenus Aedimorphus Theobald 1) vexans (Meigen) •Subgenus Georgecraigius Reinert, Harbach & Kitching 2) epactius Dyar & Knab •Subgenus Ochlerotatus Lynch Arribalzaga 3) atlanticus Dyar & Knab 4) canadensis (Theobald) 5) dupreei (Coquillett) 6) fulvus pallens Ross 7) grossbecki Dyar & Knab 8) infirmatus Dyar & Knab 9) mitchellae (Dyar) 10) nigromaculis (Ludlow) 11) sollicitans (Walker) 12) sticticus (Meigen) 13) taeniorhynchus (Wiedemann) 14) tormentor Dyar & Knab 15) trivittatus (Coquillett) •Subgenus Protomacleaya Theobald 16) hendersoni Cockerell 17) triseriatus (Say) 18) zoosophus Dyar & Knab •Subgenus Stegomyia Theobald 19) aegypti (Linnaeus) 20) albopictus (Skuse) II) Genus ANOPHELES Meigen •Subgenus Anopheles Meigen 21) atropos Dyar & Knab 22) barberi Coquillett 23) bradleyi King 24) crucians Wiedemann 25) pseudopunctipennis Theobald 26) punctipennis (Say) 27) quadrimaculatus Say III) Genus COQUILLETTIDIA Dyar •Subgenus Coquillettidia Dyar 28) perturbans (Walker) IV) Genus CULEX Linnaeus •Subgenus Culex Linnaeus 29) coronator Dyar & Knab 30) nigripalpus Theobald 31) quinquefasciatus Say 32) restuans Theobald 33) salinarius Coquillett 34) tarsalis Coquillett 35) thriambus Dyar •Subgenus Melanoconion Theobald 36) abominator Dyar & Knab 37) erraticus (Dyar & Knab) •Subgenus Neoculex Dyar 38) territans Walker V) Genus CULISETA Felt •Subgenus Culiseta Felt 39) inornata (Williston) VI) Genus MANSONIA Blanchard •Subgenus Mansonia Blanchard 40) titillans (Walker) VII) Genus ORTHOPODOMYIA Theobald 41) alba Baker 42) signifera (Coquillett) VIII) Genus PSOROPHORA Robineau-Desvoidy •Subgenus Grabhamia Theobald 43) columbiae (Dyar & Knab) 44) discolor (Coquillett) 45) signipennis (Coquillett) •Subgenus Janthinosoma Lynch Arribalzaga 46) cyanescens (Coquillett) 47) ferox (von Humboldt) 48) horrida (Dyar & Knab) 49) longipalpus Randolph & O'Neill 50) mathesoni Belkin & Heinemann •Subgenus Psorophora Robineau-Desvoidy 51) ciliata (Fabricius) 52) howardii Coquillett IX) Genus TOXORHYNCHITES Theobald •Subgenus Lynchiella Lahille 53) rutilus septentrionalis (Dyar & Knab) X) Genus URANOTAENIA Lynch Arribalzaga •Subgenus Pseudoficalbia Theobald 54) anhydor syntheta Dyar & Shannon •Subgenus Uranotaenia Lynch Arribalzaga 55) lowii Theobald 56) sapphirina (Osten Sacken) The following species were not collected in recent years but were reported to occur in earlier studies in Harris County, including Ae. dupreei, Ae. zoosophus, An. barberi Coquillett, (Kokernot et al. 1974), and Ps. varipes (O'Neill et al. 1944). Similarly, Ae. hendersoni, An. bradleyi King, Cx. abominator Dyar and Knab, Cx. thriambus Dyar, Ps. mathesoni, and Uranotaenia anhydor syntheta Dyar and Shannon, described by Belkin and McDonald (1956), have not been collected recently. However, most of these species were collected nearby in the northern and southern bordering counties of Montgomery and Galveston (Fournier et al. 1989), McLennan County (Duhrkopf 1994), and in San Antonio, TX (McPhatter et al. 2012). Possible factors for this outcome are related to: 1) discontinuing the use of some of the old trapping methodologies while adopting new developments in trapping designs, targeting species derived from different types of habitats, age structure, and physiology, thus not collecting all species as in previous years; 2) record keeping performed manually during the first ten years of operations making retrieval, sorting, and analysis of data difficult due to illegible records and archiving methods; and 3) the number of times data transitioned from one relational database to another, limiting the information available to confirm occurrence of these species in Harris County. Harris County Public Health and Environmental Services Mosquito Control Division will continue to monitor the entire county with previously mentioned collecting devices, and expand its reference collection to include all recorded mosquito species in Harris County and the City of Houston. Moreover, it shall re-incorporate the use of old trapping methodologies as well as the implementation of new collecting strategies to increase the likelihood of collecting rare and new record specimens for Harris County, particularly those medically important species such as Aedes japonicus japonicus (Theobald), as its distribution continues to move south (Bevins 2007, Harris et al. 2015) after its introduction into the U.S. (Peyton et al. 1999). It will also continue testing all new and re-emerging vector-borne pathogens that threaten the community in the future. The authors thank all past and present Harris County Mosquito Control Division surveillance personnel for all their entomological efforts. We thank Mr. Vence Salvato for his assistance with the creation of the map. We also thank Dr. Dan Strickman for reviewing this manuscript.